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Biceps Tenodesis cannot be used as primary treatment option in baseball pitchers with intact rotator cuff muscles

Open AccessPublished:November 15, 2022DOI:https://doi.org/10.1016/j.clinbiomech.2022.105819

      Highlights

      • Analysis of shoulder stability with biceps tenodesis.
      • No increase in rotator cuff muscle force with biceps tenodesis.
      • Biceps tenodesis not as primary treatment in baseball pitchers.

      Abstract

      Background
      Surgeons remain hesitant to perform biceps tenodesis in athletes with type II superior labrum anterior-to-posterior tears due to the lack of reported clinical outcomes for individual overhead throwing sports and associated concerns that this may predispose the joint to instability. This study aimed to assess the effect of biceps tenodesis on shoulder stability for major overhead throwing sports to aid sport-specific surgical decision-making for athletes with type II superior labrum anterior-to-posterior tears.

      Methods

      This is a combined modelling and experimental study. Motion data and external forces were measured from 13 participants performing five overhead throwing motions. These data served as input into a musculoskeletal shoulder model that quantifies shoulder stability and muscle loading.

      Findings

      The loading of the long head of the biceps brachii decreases significantly following biceps tenodesis in three overhead throwing motions (p = 0.02). The loss in joint stability following biceps tenodesis is compensated by a non-significant increase in rotator cuff muscle force which maintains shoulder stability across all overhead throwing motions, except baseball pitching (p = 0.01). The presence of a full-thickness supraspinatus tear post biceps tenodesis further decreases shoulder stability in four of the five overhead throwing motions (p = 0.01).

      Interpretation

      The study findings demonstrate that an increase in rotator cuff muscle force maintains joint stability for all overhead throwing motions post biceps tenodesis, except baseball pitching. As the presence of a full-thickness tear of the supraspinatus significantly reduces joint stability, biceps tenodesis may be used as a primary treatment in overhead throwing athletes with intact rotator cuff muscles, except baseball pitchers.

      Level of evidence

      Controlled Laboratory Study; Level of Evidence 3.

      Keywords

      1. Introduction

      The superior glenoid labrum, including the insertion of the long head of the biceps brachii, is a common site of injury in overhead activities (
      • Michener L.A.
      • Abrams J.S.
      • Bliven K.C.H.
      • Falsone S.
      • Laudner K.G.
      • McFarland E.G.
      • Tibone J.E.
      • Thigpen C.A.
      • Uhl T.L.
      National Athletic Trainers’ association position statement: evaluation, management, and outcomes of and return-to- play criteria for overhead athletes with superior labral anterior-posterior injuries.
      ), with superior labrum anterior-to-posterior (SLAP) tears being present in as many as 26% of shoulder arthroscopies (
      • Waterman B.R.
      • Arroyo W.
      • Heida K.
      • Burks R.
      • Pallis M.
      SLAP repairs with combined procedures have lower failure rate than isolated repairs in a military population: surgical outcomes with minimum 2-year follow-up.
      ). Type II SLAP lesions, which are characterized by superior labral fraying with a detached biceps anchor (
      • Snyder S.J.
      • Karzel R.P.
      • Del Pizzo W.
      • Ferkel R.D.
      • Friedman M.J.
      SLAP lesions of the shoulder.
      ), account for the majority of these SLAP tears (
      • Brockmeyer M.
      • Tompkins M.
      • Kohn D.M.
      • Lorbach O.
      SLAP lesions: a treatment algorithm.
      ). Although the exact cause of type II SLAP tears is unknown, these lesions are frequently related to large traction of the superior glenoid labrum-biceps complex during traumatic events or repeated overhead activity (
      • Welton K.L.
      • Bartley J.H.
      • Major N.M.
      • McCarty E.C.
      MRI to arthroscopy correlations in SLAP lesions and long head biceps pathology.
      ;
      • Wilk K.E.
      • Macrina L.C.
      Nonoperative and postoperative rehabilitation for glenohumeral instability.
      ). Prior clinical research studies demonstrated that some of the radiologically diagnosed SLAP lesions are asymptomatic (
      • Lansdown D.A.
      • Bendich I.
      • Motamedi D.
      • Feeley B.T.
      Imaging-based prevalence of superior labral anterior-posterior tears significantly increases in the aging shoulder.
      ;
      • Schwartzberg R.
      • Reuss B.L.
      • Burkhart B.G.
      • Butterfield M.
      • Wu J.Y.
      • McLean K.W.
      High prevalence of superior labral tears diagnosed by MRI in middle-aged patients with asymptomatic shoulders.
      ). Surgical treatment options include SLAP repair as well as biceps tenodesis, biceps tenotomy and arthroscopic debridement (
      • Paoli A.R.
      • Gold H.T.
      • Mahure S.A.
      • Mai D.H.
      • Agten C.A.
      • Rokito A.S.
      • Virk M.S.
      Treatment for symptomatic SLAP tears in middle-aged patients comparing repair, biceps Tenodesis, and nonoperative approaches: a cost-effectiveness analysis.
      ). The treatment of type II SLAP lesions with arthroscopic debridement has yielded poor clinical outcomes in young patients (
      • Parnes N.
      • Dunn J.C.
      • Czajkowski H.
      • DeFranco M.J.
      • Green C.K.
      • Scanaliato J.P.
      Biceps Tenodesis as an attractive alternative to superior labral anterior-posterior (SLAP) repair for type II SLAP lesions in active-duty military patients younger than 35 years.
      ;
      • Patterson B.M.
      • Creighton R.A.
      • Spang J.T.
      • Roberson J.R.
      • Kamath G.V.
      Surgical trends in the treatment of superior labrum anterior and posterior lesions of the shoulder: analysis of data from the American Board of Orthopaedic Surgery Certification Examination Database.
      ), thus arthroscopic SLAP repair is widely considered as standard of care (
      • Cvetanovich G.L.
      • Gowd A.K.
      • Frantz T.L.
      • Erickson B.J.
      • Romeo A.A.
      Superior labral anterior posterior repair and biceps Tenodesis surgery: trends of the American Board of Orthopaedic Surgery Database.
      ;
      • Shin M.H.
      • Baek S.
      • Kim T.M.
      • Kim H.
      • Oh K.-S.
      • Chung S.W.
      Biceps Tenodesis versus superior labral anterior and posterior (SLAP) lesion repair for the treatment of SLAP lesion in overhead athletes: a systematic review and Meta-analysis.
      ). Published studies for arthroscopically repaired type II SLAP lesions have reported good clinical outcomes in 75% to 97% of cases (
      • Aida H.F.
      • Shi B.Y.
      • Huish E.G.J.
      • McFarland E.G.
      • Srikumaran U.
      Are implant choice and surgical approach associated with biceps Tenodesis construct strength? A systematic review and Meta-regression.
      ;
      • Pougès C.
      • Hardy A.
      • Vervoort T.
      • Amouyel T.
      • Duriez P.
      • Lalanne C.
      • Szymanski C.
      • Deken V.
      • Chantelot C.
      • Upex P.
      • Maynou C.
      Arthroscopic Bankart repair versus immobilization for first episode of anterior shoulder dislocation before the age of 25: a randomized controlled trial.
      ). However, less consistent functional outcomes have been reported in overhead throwing athletes, with only 22% to 75% of athletes returning to preinjury level of sport participation(
      • Fedoriw W.W.
      • Ramkumar P.
      • McCulloch P.C.
      • Lintner D.M.
      Return to play after treatment of superior labral tears in professional baseball players.
      ;
      • Lorentz N.A.
      • Hurley E.T.
      • Colasanti C.A.
      • Markus D.H.
      • Alaia M.J.
      • Campbell K.A.
      • Strauss E.J.
      • Jazrawi L.M.
      Return to play after biceps Tenodesis for isolated SLAP tears in overhead athletes.
      ;
      • Smith R.
      • Lombardo D.J.
      • Petersen-Fitts G.R.
      • Frank C.
      • Tenbrunsel T.
      • Curtis G.
      • Whaley J.
      • Sabesan V.J.
      Return to play and prior performance in Major League Baseball pitchers after repair of superior labral anterior-posterior tears.
      ). In contrast, treating type II SLAP tears in overhead throwing athletes with arthroscopic biceps tenodesis using an interference screw fixation has yielded improved clinical outcomes, with return rates to preinjury level of sport participation exceeding 80% in prior studies (
      • Chalmers P.N.
      • Trombley R.
      • Cip J.
      • Monson B.
      • Forsythe B.
      • Nicholson G.P.
      • Bush-Joseph C.A.
      • Cole B.J.
      • Wimmer M.A.
      • Romeo A.A.
      • Verma N.N.
      Postoperative restoration of upper extremity motion and neuromuscular control during the overhand pitch: evaluation of tenodesis and repair for superior labral anterior-posterior tears.
      ;
      • Ek E.T.H.
      • Shi L.L.
      • Tompson J.D.
      • Freehill M.T.
      • Warner J.J.P.
      Surgical treatment of isolated type II superior labrum anterior-posterior (SLAP) lesions: repair versus biceps tenodesis.
      ).
      These superior outcomes of arthroscopic biceps tenodesis in terms of pain and function, when compared to arthroscopic SLAP repair, have been associated with the absence of traction in the superior glenoid labrum-biceps complex following the surgical transfer of the long head of the biceps brachii from its anatomical position at the superior glenoid to the bicipital groove of the humerus (
      • Boileau P.
      • Parratte S.
      • Chuinard C.
      • Roussanne Y.
      • Shia D.
      • Bicknell R.
      Arthroscopic treatment of isolated type II SLAP lesions: biceps tenodesis as an alternative to reinsertion.
      ;
      • Strauss E.J.
      • Salata M.J.
      • Sershon R.A.
      • Garbis N.
      • Provencher M.T.
      • Wang V.M.
      • McGill K.C.
      • Bush-Joseph C.A.
      • Nicholson G.P.
      • Cole B.J.
      • Romeo A.A.
      • Verma N.N.
      Role of the superior labrum after biceps tenodesis in glenohumeral stability.
      ). However, there is clinical concern that this may lead to a reduction in joint stability, with previous biomechanical studies indicating that the long head of the biceps brachii may restrict anterior and superior humeral head translation (
      • Su W.-R.
      • Budoff J.E.
      • Luo Z.-P.
      The effect of posterosuperior rotator cuff tears and biceps loading on glenohumeral translation.
      ;
      • Youm T.
      • ElAttrache N.S.
      • Tibone J.E.
      • McGarry M.H.
      • Lee T.Q.
      The effect of the long head of the biceps on glenohumeral kinematics.
      ) and work in conjunction with the rotator cuff muscles to center the humeral head on the glenoid fossa through concavity compression. Although the precise contribution of the long head of the biceps brachii to glenohumeral stability is not fully established, even a small biomechanical role of the long head of the biceps brachii to joint stability is likely to be important for high-speed athletic motions such as overhead throwing (
      • Chalmers P.N.
      • Trombley R.
      • Cip J.
      • Monson B.
      • Forsythe B.
      • Nicholson G.P.
      • Bush-Joseph C.A.
      • Cole B.J.
      • Wimmer M.A.
      • Romeo A.A.
      • Verma N.N.
      Postoperative restoration of upper extremity motion and neuromuscular control during the overhand pitch: evaluation of tenodesis and repair for superior labral anterior-posterior tears.
      ). Therefore, surgeons remain hesitant to perform biceps tenodesis on overhead throwing athletes (
      • Hurley E.T.
      • Fat D.L.
      • Duigenan C.M.
      • Miller J.C.
      • Mullett H.
      • Moran C.J.
      Biceps tenodesis versus labral repair for superior labrum anterior-to-posterior tears: a systematic review and meta-analysis.
      ;
      • Patterson B.M.
      • Creighton R.A.
      • Spang J.T.
      • Roberson J.R.
      • Kamath G.V.
      Surgical trends in the treatment of superior labrum anterior and posterior lesions of the shoulder: analysis of data from the American Board of Orthopaedic Surgery Certification Examination Database.
      ) due to concerns that the surgical transfer of the long head of the biceps brachii tendon away from its anatomical position may predispose the joint to instability, particularly in overhead throwing athletes with concominant rotator cuff pathology (
      • Merolla G.
      • Paladini P.
      • Porcellini G.
      Assessment of return to play in professional overhead athletes subjected to arthroscopic repair of rotator cuff tears and associated labral injuries using the Italian version of the Kerlan-Jobe Orthopedic Clinic Shoulder and Elbow score.
      ).
      Despite several studies being reported in the literature (
      • Chalmers P.N.
      • Trombley R.
      • Cip J.
      • Monson B.
      • Forsythe B.
      • Nicholson G.P.
      • Bush-Joseph C.A.
      • Cole B.J.
      • Wimmer M.A.
      • Romeo A.A.
      • Verma N.N.
      Postoperative restoration of upper extremity motion and neuromuscular control during the overhand pitch: evaluation of tenodesis and repair for superior labral anterior-posterior tears.
      ;
      • Denard P.J.
      • Ladermann A.
      • Parsley B.K.
      • Burkhart S.S.
      Arthroscopic biceps tenodesis compared with repair of isolated type II SLAP lesions in patients older than 35 years.
      ;
      • Ek E.T.H.
      • Shi L.L.
      • Tompson J.D.
      • Freehill M.T.
      • Warner J.J.P.
      Surgical treatment of isolated type II superior labrum anterior-posterior (SLAP) lesions: repair versus biceps tenodesis.
      ), there is no current knowledge of the effect of biceps tenodesis on shoulder stability for specific overhead throwing sports. Existing clinical studies only focus on clinical outcomes such as pain and joint functionality, which are presented for a mixture of overhead throwing sports (
      • Denard P.J.
      • Ladermann A.
      • Parsley B.K.
      • Burkhart S.S.
      Arthroscopic biceps tenodesis compared with repair of isolated type II SLAP lesions in patients older than 35 years.
      ;
      • Ek E.T.H.
      • Shi L.L.
      • Tompson J.D.
      • Freehill M.T.
      • Warner J.J.P.
      Surgical treatment of isolated type II superior labrum anterior-posterior (SLAP) lesions: repair versus biceps tenodesis.
      ;
      • Frantz T.L.
      • Shacklett A.G.
      • Martin A.S.
      • Barlow J.D.
      • Jones G.L.
      • Neviaser A.S.
      • Cvetanovich G.L.
      Biceps Tenodesis for superior labrum anterior-posterior tear in the overhead athlete: a systematic review.
      ), despite known differences in shoulder loading for different overhead throwing motions (
      • Ramappa A.J.
      • Chen P.-H.
      • Hawkins R.J.
      • Noonan T.
      • Hackett T.
      • Sabick M.B.
      • Decker M.J.
      • Keeley D.
      • Torry M.R.
      Anterior shoulder forces in professional and little league pitchers.
      ;
      • Usman J.
      • McIntosh A.S.
      • Frechede B.
      An investigation of shoulder forces in active shoulder tackles in rugby union football.
      ). Therefore, the aim of this study is to assess the effect of biceps tenodesis on shoulder stability for major overhead throwing sports in order to aid sport-specific surgical decision-making for athletes with type II SLAP tears. We hypothesize that biceps tenodesis does not reduce shoulder stability in overhead throwing sports.

      2. Methods

      2.1 Subjects

      Thirteen healthy right-handed volunteers (10 males, 3 females; height 1.69 ± 0.10 m, body mass 68.5 ± 18.2 kg; age 26.4 ± 4.7 years) with no history of shoulder pathology participated in this study. All volunteers reported regular participation in contact sports and/or team sports, and also performed strength and conditioning exercises on a weekly basis, as a minimum. Informed consent was obtained from each subject and ethical approval was granted by our Institutional Research Ethics Committee.

      2.2 Overhead throwing sports

      The volunteers were instructed to perform throwing motions from five overhead throwing sports with three sets per activity (Fig. 1). These sports were selected based on prior works (
      • Brockmeier S.F.
      • Voos J.E.
      • Williams 3rd, R.J.
      • Altchek D.W.
      • Cordasco F.A.
      • Allen A.A.
      Outcomes after arthroscopic repair of type-II SLAP lesions.
      ;
      • Coleman S.H.
      • Cohen D.B.
      • Drakos M.C.
      • Allen A.A.
      • Williams R.J.
      • O’brien S.J.
      • Altchek D.W.
      • Warren R.F.
      Arthroscopic repair of type II superior labral anterior posterior lesions with and without acromioplasty: a clinical analysis of 50 patients.
      ). All volunteers were given instructions on how to accurately perform each of the overhead throwing activity and were given 3 to 5 min to familiarize with each throwing task. (See Fig. 2.)
      Fig. 1
      Fig. 1Overhead throwing motions included in this study.
      Fig. 2
      Fig. 2Illustration of surgical techniques: (1) SLAP repair shown (left), and (2) biceps tenodesis (right).

      2.3 Protocol

      Kinematic data collection was performed using a 10-camera optical motion tracking system (Vicon Motion Tracking System, Oxford, UK) at 240 Hz.
      A scapula tracker (ST) was used to measure scapula kinematics (
      • Prinold J.A.I.
      • Shaheen A.F.
      • Bull A.M.J.
      Skin-fixed scapula trackers: a comparison of two dynamic methods across a range of calibration positions.
      ). The ST consists of a base attached to the mid-portion of the scapula spine and an adjustable foot positioned on the meeting-point between acromion process and scapular spine (
      • Shaheen A.F.
      • Alexander C.M.
      • Bull A.M.J.
      Effects of attachment position and shoulder orientation during calibration on the accuracy of the acromial tracker.
      ). The ST technical coordinate frame was calibrated with the anatomical coordinate frame of the scapula using the International Society of Biomechanics (ISB) recommended landmarks and measured directly using a scapula locator (
      • Shaheen A.F.
      • Alexander C.M.
      • Bull A.M.J.
      Effects of attachment position and shoulder orientation during calibration on the accuracy of the acromial tracker.
      ). Calibration was performed in three static positions: (1) shoulder at 90° humero-thoracic abduction and elbow at 90° flexion with arm positioned at approximately 30° to the coronal plane, (2) shoulder at approximately 150° humero-thoracic abduction and (3) shoulder at <10° of humero-thoracic abduction.
      Twenty-one retro-reflective markers were used to track the thorax, scapula, clavicle, humerus, radius and ulna (
      • Wu G.
      • van der Helm F.C.T.
      • Veeger H.E.J.D.
      • Makhsous M.
      • Van Roy P.
      • Anglin C.
      • Nagels J.
      • Karduna A.R.
      • McQuade K.
      • Wang X.
      • Werner F.W.
      • Buchholz B.
      ISB recommendation on definitions of joint coordinate systems of various joints for the reporting of human joint motion--Part II: shoulder, elbow, wrist and hand.
      ). The elbow epicondyles were defined as a rigid offset from the humeral technical frame with the arm at 90° of humerothoracic flexion, 45° from the coronal plane, 90° elbow flexion and a vertical forearm. Least-square fitting was used to calculate the glenohumeral head rotational centre during a functional task using the locator to track the scapula (
      • Gamage S.S.H.U.
      • Lasenby J.
      New least squares solutions for estimating the average Centre of rotation and the axis of rotation.
      ).
      A low-pass fourth-order Butterworth filter (cut-off 4.7 Hz) was used to remove noise from the kinematic data after spectral analysis of the signal (
      • Prinold J.A.I.
      • Bull A.M.J.
      Scapula kinematics of pull-up techniques: avoiding impingement risk with training changes.
      ).

      2.4 Modelling and analysis

      The motion and external forces for each athletic activity served as inputs into the UK National Shoulder Model (UK NSM; as described in Charlton and Johnson(
      • Charlton I.W.
      • Johnson G.R.
      A model for the prediction of the forces at the glenohumeral joint.
      )), a 3D musculoskeletal modelling software written in Matlab (The Mathworks Inc., Cambridge, UK) that models forces at the right shoulder. The version of the UK NSM used in this study additionally incorporates the effect of anthropometric scaling of ten subject-specific shoulder anatomies (
      • Klemt C.
      • Toderita D.
      • Nolte D.
      • Di Federico E.
      • Reilly P.
      • Bull A.M.J.
      The critical size of a defect in the glenoid causing anterior instability of the shoulder after a Bankart repair, under physiological joint loading.
      ,
      • Klemt Christian
      • Nolte D.
      • Ding Z.
      • Rane L.
      • Quest R.A.
      • Finnegan M.E.
      • Walker M.
      • Reilly P.
      • Bull A.M.J.
      Anthropometric scaling of anatomical datasets for subject-specific musculoskeletal modelling of the shoulder.
      ), glenohumeral concavity compression (
      • Klemt C.
      • Nolte D.
      • Grigoriadis G.
      • Di Federico E.
      • Reilly P.
      • Bull A.M.J.
      The contribution of the glenoid labrum to glenohumeral stability under physiological joint loading using finite element analysis.
      ) and subject-specific scapula tracking (
      • Prinold J.A.I.
      • Shaheen A.F.
      • Bull A.M.J.
      Skin-fixed scapula trackers: a comparison of two dynamic methods across a range of calibration positions.
      ). The shoulder model is an inverse dynamics musculoskeletal model of the upper limb that includes 87 muscle elements and three glenohumeral ligaments crossing five functional joints (sternoclavicular, acromioclavicular, scapulothoracic, glenohumeral and elbow). Model validation was previously performed by comparison to instrumented implant measurements (
      • Bergmann G.
      • Graichen F.
      • Bender A.
      • Ka M.
      In Vivo Glenohumeral Contact Forces — Measurements in the First Patient 7 Months Postoperatively.
      ) and electromyography for functional activities with large ranges of motion (
      • Klemt C.
      • Prinold J.A.
      • Morgans S.
      • Smith S.H.L.
      • Nolte D.
      • Reilly P.
      • Bull A.M.J.
      Analysis of shoulder compressive and shear forces during functional activities of daily life.
      ;
      • Pandis P.
      • Prinold J.A.I.
      • Bull A.M.J.
      Shoulder muscle forces during driving: sudden steering can load the rotator cuff beyond its repair limit.
      ). Intersegmental moments are calculated using the measured kinematics and an optimisation algorithm that minimises the sum of muscle stresses squared is used to solve the natural muscle load-sharing redundancy. Subject-specific measurements, including segment lengths and body weight and height, are used for scaling of body segment parameters (
      • De Leva P.
      Adjustments to zatsiorsky-seluyanov’s segment inertia parameters.
      ). Muscle parameters were scaled linearly from an anatomical atlas of subject-specific shoulder models based on the length of body segments, with the anatomically closest dataset for each study participant being identified based on the ratio of body height to shoulder width and gender (Christian
      • Klemt C.
      • Toderita D.
      • Nolte D.
      • Di Federico E.
      • Reilly P.
      • Bull A.M.J.
      The critical size of a defect in the glenoid causing anterior instability of the shoulder after a Bankart repair, under physiological joint loading.
      ,
      • Klemt Christian
      • Nolte D.
      • Ding Z.
      • Rane L.
      • Quest R.A.
      • Finnegan M.E.
      • Walker M.
      • Reilly P.
      • Bull A.M.J.
      Anthropometric scaling of anatomical datasets for subject-specific musculoskeletal modelling of the shoulder.
      ). We used a partially closed chain method to optimise scapula and clavicle kinematics (
      • Prinold J.A.I.
      • Bull A.M.J.
      Scaling and kinematics optimisation of the scapula and thorax in upper limb musculoskeletal models.
      ). The model outputs include glenohumeral contact forces as well as muscle forces including the long head of the biceps brachii and the rotator cuff muscles (C
      • Klemt C.
      • Toderita D.
      • Nolte D.
      • Di Federico E.
      • Reilly P.
      • Bull A.M.J.
      The critical size of a defect in the glenoid causing anterior instability of the shoulder after a Bankart repair, under physiological joint loading.
      ,
      • Klemt Christian
      • Nolte D.
      • Ding Z.
      • Rane L.
      • Quest R.A.
      • Finnegan M.E.
      • Walker M.
      • Reilly P.
      • Bull A.M.J.
      Anthropometric scaling of anatomical datasets for subject-specific musculoskeletal modelling of the shoulder.
      ). The resultant glenohumeral joint contact force vector is constrained to be within the glenoid rim, enforcing rotator cuff muscle co-contraction to provide joint stability.
      The athletic activities for each study participant were simulated with four different anatomical variants of the UK NSM in order to investigate the effect of biceps tenodesis on shoulder stability. These variants were: (1) intact anatomy (
      • Charlton I.W.
      • Johnson G.R.
      A model for the prediction of the forces at the glenohumeral joint.
      ) with the long head of the biceps tendon being attached to its anatomical origin, (2) post biceps tenodesis without cuff tear with the attachment point of the long head of the biceps tendon transferred from its anatomical origin to the top of the bicipital groove (
      • Boileau P.
      • Parratte S.
      • Chuinard C.
      • Roussanne Y.
      • Shia D.
      • Bicknell R.
      Arthroscopic treatment of isolated type II SLAP lesions: biceps tenodesis as an alternative to reinsertion.
      ), (3) post biceps tenodesis with full-thickness supraspinatus tear (most commonly torn rotator cuff muscle) with the attachment point of the long head of the biceps tendon transferred from its anatomical origin to the top of the bicipital groove, with combined presence of a full-thickness tear of the supraspinatus (detachment of the entire supraspinatus off the greater tuberosity) that was modelled by setting the muscle volume to zero, and (4) an isolated full-thickness supraspinatus tear (detachment of the entire supraspinatus off the greater tuberosity) that was modelled by setting the muscle volume to zero in order to exclude significant losses in shoulder stability solely due to the presence of a full-thickness supraspinatus tear.
      For each variant of the shoulder model, the peak forces in the long head of the biceps brachii and the rotator cuff muscles were analysed in Newtons, for each athletic activity in order to evaluate changes in shoulder muscle loading through biceps tenodesis for each overhead throwing sport. Similarly, the stability of the shoulder was assessed for all model instances and athletic activities using the superior and anterior glenoid stability ratio. This is defined by peak translational shear force in Newtons divided by the joint stabilising compression force in Newtons (
      • Fukuda K.
      • Chen C.M.
      • Cofield R.H.
      • Chao E.Y.
      Biomechanical analysis of stability and fixation strength of total shoulder prostheses.
      ). This serves to assess the effect of biceps tenodesis on joint stability for each overhead throwing sport. The stability ratios were obtained in two main anatomical directions of the glenoid as superior and anterior stability ratio respectively, with increasing stability ratios indicating a loss in joint stability. As the stability ratio is quotient of two forces, it has no units.
      Data normality was assessed using the Shapiro-Wilk's test. Statistical differences in shoulder stability and shoulder muscle loading between the intact shoulder model and the other three model instances were assessed using a Kruskal-Wallis test. A p-value of 0.05 was used for all tests. All statistical analysis was performed in SPSS (version 23, IBM Corp., Armonk, NY) (
      • Zubair M.
      • Haider Z.
      • Khan S.A.
      • Nasir J.
      Atmospheric influences on satellite communications.
      ).

      3. Results

      The muscle force of the long head of the biceps brachii decreases post biceps tenodesis across all five overhead motions (Fig. 3), with significant reductions in long head of biceps brachii loading for a baseball pitch (327 N vs 194 N; p < 0.01), quarterback throw (198 N vs 141 N; p = 0.01) and volleyball serve (174 N vs 128 N; p = 0.02).
      Fig. 3
      Fig. 3Median (±IQR) of the peak muscle forces of the long head of the biceps brachii (BIC.L), supraspinatus (SS), infraspinatus (IS), subscapularis (SBS) and teres minor (T.min), for the intact anatomy (model 1; white bars), post biceps tenodesis (model 2; light gray bars), post biceps tenodesis with combined presence of a full-thickness supraspinatus tear (model 3; black bars), and full-thickness supraspinatus tear (model 4; dark gray bars), for the five overhead throwing motions.
      The rotator cuff muscle forces significantly increase (p < 0.02) post biceps tenodesis with associated full-thickness supraspinatus tear across all overhead motions (Fig. 3), with none of these increases in rotator cuff muscle force being induced solely by the presence of a full-thickness supraspinatus tear (p = 0.23).
      The stability of the shoulder decreases (reflected by an increase in stability ratio) post biceps tenodesis for baseball pitching only in the anterior direction (0.47 vs 0.69; p = 0.01; Fig. 4). The stability of the shoulder further decreases post biceps tenodesis with combined presence of a full-thickness tear of the supraspinatus, with significant losses in anterior shoulder stability for a baseball pitch (0.47 vs 0.76; p < 0.01), quarterback throw (0.41 vs 0.65; p < 0.01) and volleyball serve (0.36 vs 0.62; p = 0.01), as well as significant losses in superior joint stability for a baseball pitch (0.44 vs 0.73; p < 0.01), quarterback throw (0.37 vs 0.68; p < 0.01), volleyball serve (0.37 vs 0.54; p = 0.02) and rugby lineout throw (0.38 vs 0.48; p = 0.03). None of these significant losses in joint stability was induced by solely the presence of a full-thickness tear of the supraspinatus (p = 0.27).
      Fig. 4
      Fig. 4Median stability ratios (±IQR) in the superior and anterior anatomical direction of the glenoid, for the intact anatomy (model 1; white bars), post biceps tenodesis (model 2; light gray bars), post biceps tenodesis with combined presence of a full-thickness supraspinatus tear (model 3; black bars), and full-thickness supraspinatus tear (model 4; dark gray bars), for the five overhead throwing motions.

      4. Discussion

      This study has investigated the effect of biceps tenodesis on shoulder stability for major overhead throwing motions in order to aid sport-specific surgical decision-making for athletes with type II SLAP tears. The study findings demonstrate a decreased loading of the long head of the biceps following biceps tenodesis, with statistically significant losses in muscle loading for three of the five overhead throwing motions (baseball pitch, quarterback throw, volleyball serve). It is likely that a reduction of loading through an abnormal biceps origin would bring an improvement in symptoms in agreement with the literature that has shown superior clinical outcomes for biceps tenodesis, when compared to arthroscopic SLAP repair (
      • Chalmers P.N.
      • Trombley R.
      • Cip J.
      • Monson B.
      • Forsythe B.
      • Nicholson G.P.
      • Bush-Joseph C.A.
      • Cole B.J.
      • Wimmer M.A.
      • Romeo A.A.
      • Verma N.N.
      Postoperative restoration of upper extremity motion and neuromuscular control during the overhand pitch: evaluation of tenodesis and repair for superior labral anterior-posterior tears.
      ;
      • Ek E.T.H.
      • Shi L.L.
      • Tompson J.D.
      • Freehill M.T.
      • Warner J.J.P.
      Surgical treatment of isolated type II superior labrum anterior-posterior (SLAP) lesions: repair versus biceps tenodesis.
      ).
      In agreement with findings from cadaveric studies, our results suggest that the long head of the biceps significantly contributes to shoulder stability during overhead throwing activities (
      • Chan C.M.
      • Behrend C.
      • Shields E.
      • Maloney M.D.
      • Voloshin I.
      Effects of varying locations for biceps tendon tenotomy and superior labral integrity on shoulder stability in a cadaveric concavity-compression model.
      ;
      • Itoi E.
      • Newman S.R.
      • Kuechle D.K.
      • Morrey B.F.
      • An K.N.
      Dynamic anterior stabilisers of the shoulder with the arm in abduction.
      ;
      • Su W.-R.
      • Budoff J.E.
      • Luo Z.-P.
      The effect of posterosuperior rotator cuff tears and biceps loading on glenohumeral translation.
      ). This observation indicates that the long head of the biceps brachii assists the rotator cuff muscles to stabilise the shoulder through concavity compression (
      • Lazarus M.D.
      • Sidles J.A.
      • Harryman D.T.
      • Matsen F.A.
      Effect of a chondral-labral defect on glenoid concavity and glenohumeral stability. A cadaveric model.
      ;
      • Lippitt S.
      • Matsen F.
      Mechanisms of glenohumeral joint stability.
      ). The influence of biceps on shoulder stability has important clinical implications and has to be considered when choosing biceps tenodesis as a treatment method for overhead throwing athletes with type II SLAP tears. In addition to the biceps, the superior labrum contributes to shoulder stability, with prior computer simulations reporting a contribution of around 10% to shoulder stability (
      • Klemt C.
      • Nolte D.
      • Grigoriadis G.
      • Di Federico E.
      • Reilly P.
      • Bull A.M.J.
      The contribution of the glenoid labrum to glenohumeral stability under physiological joint loading using finite element analysis.
      ). Therefore, leaving a stump of the biceps anchor attached to the labrum and then performing a labral repair will provide stability to the shoulder and resist against superior migration of the humeral head.
      The observed loss in joint stability following the surgical transfer of the long head of the biceps brachii tendon away from its anatomical position is compensated by a non-significant increase in rotator cuff muscle force, with these muscles maintaining shoulder stability post biceps tenodesis across all overhead throwing motions, except baseball pitching. Therefore, we can partially accept our hypothesis that biceps tenodesis does not reduce shoulder stability in overhead throwing sports, expect for the baseball pitching motion. The increased long-term injury risk that has been associated with rotator cuff muscle overloading and increased shoulder joint shear forces (
      • Orchard J.W.
      • Blanch P.
      • Paoloni J.
      • Kountouris A.
      • Sims K.
      • Orchard J.J.
      • Brukner P.
      Cricket fast bowling workload patterns as risk factors for tendon, muscle, bone and joint injuries.
      ;
      • Wang V.M.
      • Romeo A.A.
      Are anterior supraspinatus tendon tears more prone to propagation? Commentary on an article by Daisuke Araki, MD, PhD, et al., “Effect of tear location on propagation of isolated supraspinatus tendon tears during increasing levels of cyclic loading”.
      ) is widely accepted. However, it is not clear if the non-significant increases in rotator cuff forces seen in this study post biceps tenodesis would cause higher rates of rotator cuff pathology in a high risk population.
      The integrity of the rotator cuff is an important factor when considering a biceps tenodesis; the stability of the shoulder post biceps tenodesis is further reduced in the presence of a full-thickness tear of the supraspinatus, with significant losses in shoulder stability for four of the five overhead throwing motions as well as significant increases in rotator cuff muscle loading across all overhead throwing motions. Therefore, the treatment of type II SLAP tears in overhead throwing athletes with full-thickness supraspinatus tear, which represents the most commonly torn rotator cuff muscle in these athletes, is not recommended as it predisposes the joint to instability. This study finding corresponds well with clinical observations, demonstrating low rates of return to preinjury level of sport participation in overhead throwing athletes with concominant rotator cuff pathology (
      • Beyzadeoglu T.
      • Circi E.
      Superior labrum anterior posterior lesions and associated injuries: return to play in elite athletes.
      ;
      • Merolla G.
      • Paladini P.
      • Porcellini G.
      Assessment of return to play in professional overhead athletes subjected to arthroscopic repair of rotator cuff tears and associated labral injuries using the Italian version of the Kerlan-Jobe Orthopedic Clinic Shoulder and Elbow score.
      ).
      The study findings regarding baseball pitching are in agreement with clinical observations, which report that major league baseball pitchers have by far the lowest rate of return to preinjury level of sport participation across all overhead throwing sports (
      • Chalmers P.N.
      • Erickson B.J.
      • Verma N.N.
      • D’Angelo J.
      • Romeo A.A.
      Incidence and return to play after biceps Tenodesis in professional baseball players.
      ). In fact, the treatment of professional baseball pitchers with arthroscopic SLAP repair has yielded higher rates of return to preinjury level of sport participation with 63%, when compared to 17% of those baseball pitchers that were treated with arthroscopic biceps tenodesis (
      • Sayde W.M.
      • Cohen S.B.
      • Ciccotti M.G.
      • Dodson C.C.
      Return to play after type ii superior labral anterior-posterior lesion repairs in athletes: a systematic review.
      ). This may be explained through a loss in power and control of the pitch due to the loss in shoulder stability (
      • Hurley E.T.
      • Fat D.L.
      • Duigenan C.M.
      • Miller J.C.
      • Mullett H.
      • Moran C.J.
      Biceps tenodesis versus labral repair for superior labrum anterior-to-posterior tears: a systematic review and meta-analysis.
      ). In addition, the decreased superior shoulder stability, although non-significant, represents the largest loss in superior stability across all overhead throwing motions, highlighting the demand that is placed on the shoulder during baseball pitching. As tears of the supraspinatus as well as shoulder impingement are a common clinical problem in baseball pitchers (
      • McHugh M.P.
      • Tyler T.F.
      • Mullaney M.J.
      • Mirabella M.R.
      • Nicholas S.J.
      The effect of a high pitch volume on musculoskeletal adaptations in high school baseball pitchers.
      ;
      • Milgrom C.
      • Schaffler M.
      • Gilbert S.
      • van Holsbeeck M.
      Rotator-cuff changes in asymptomatic adults. The effect of age, hand dominance and gender.
      ;
      • Ouellette H.
      • Labis J.
      • Bredella M.
      • Palmer W.E.
      • Sheah K.
      • Torriani M.
      Spectrum of shoulder injuries in the baseball pitcher.
      ), the treatment of type II SLAP lesions in baseball pitchers with biceps tenodesis is not recommended as an increased superior shear force could potentially worsen the clinical situation. A recent systematic review by Frantz et al. also highlighted that careful consideration should be given to performing biceps tenodesis in baseball pitchers due to poor postoperative functional outcomes(
      • Frantz T.L.
      • Shacklett A.G.
      • Martin A.S.
      • Barlow J.D.
      • Jones G.L.
      • Neviaser A.S.
      • Cvetanovich G.L.
      Biceps Tenodesis for superior labrum anterior-posterior tear in the overhead athlete: a systematic review.
      ).
      A well-validated musculoskeletal shoulder model (
      • Charlton I.W.
      • Johnson G.R.
      A model for the prediction of the forces at the glenohumeral joint.
      ) was utilized in this study to investigate the effect of biceps tenodesis on joint stability for major overhead throwing motions. The novelty in this modelling approach is the use of anthropometric-scaling of subject-specific shoulder anatomies (Christian
      • Klemt C.
      • Toderita D.
      • Nolte D.
      • Di Federico E.
      • Reilly P.
      • Bull A.M.J.
      The critical size of a defect in the glenoid causing anterior instability of the shoulder after a Bankart repair, under physiological joint loading.
      ,
      • Klemt Christian
      • Nolte D.
      • Ding Z.
      • Rane L.
      • Quest R.A.
      • Finnegan M.E.
      • Walker M.
      • Reilly P.
      • Bull A.M.J.
      Anthropometric scaling of anatomical datasets for subject-specific musculoskeletal modelling of the shoulder.
      ), which has been demonstrated to accurately predict shoulder muscle and joint loading. Therefore, this is the first study to model changes in shoulder joint loading and rotator cuff muscle forces following biceps tenodesis, with existing clinical studies only reporting short-term functional outcomes (
      • Chalmers P.N.
      • Trombley R.
      • Cip J.
      • Monson B.
      • Forsythe B.
      • Nicholson G.P.
      • Bush-Joseph C.A.
      • Cole B.J.
      • Wimmer M.A.
      • Romeo A.A.
      • Verma N.N.
      Postoperative restoration of upper extremity motion and neuromuscular control during the overhand pitch: evaluation of tenodesis and repair for superior labral anterior-posterior tears.
      ;
      • Ek E.T.H.
      • Shi L.L.
      • Tompson J.D.
      • Freehill M.T.
      • Warner J.J.P.
      Surgical treatment of isolated type II superior labrum anterior-posterior (SLAP) lesions: repair versus biceps tenodesis.
      ;
      • Frantz T.L.
      • Shacklett A.G.
      • Martin A.S.
      • Barlow J.D.
      • Jones G.L.
      • Neviaser A.S.
      • Cvetanovich G.L.
      Biceps Tenodesis for superior labrum anterior-posterior tear in the overhead athlete: a systematic review.
      ).
      The use of a combined experimental and modelling approach allows the assessment of shoulder stability for individual overhead throwing motions. This is of particular importance as significant differences in shoulder loading have been demonstrated for different overhead throwing motions (
      • Ramappa A.J.
      • Chen P.-H.
      • Hawkins R.J.
      • Noonan T.
      • Hackett T.
      • Sabick M.B.
      • Decker M.J.
      • Keeley D.
      • Torry M.R.
      Anterior shoulder forces in professional and little league pitchers.
      ;
      • Usman J.
      • McIntosh A.S.
      • Frechede B.
      An investigation of shoulder forces in active shoulder tackles in rugby union football.
      ), with larger shoulder shear forces being associated with an increased likelihood of joint instability (
      • Klemt C.
      • Prinold J.A.
      • Morgans S.
      • Smith S.H.L.
      • Nolte D.
      • Reilly P.
      • Bull A.M.J.
      Analysis of shoulder compressive and shear forces during functional activities of daily life.
      ). As existing clinical studies report functional outcomes for only a mixture of overhead throwing sports (
      • Chalmers P.N.
      • Trombley R.
      • Cip J.
      • Monson B.
      • Forsythe B.
      • Nicholson G.P.
      • Bush-Joseph C.A.
      • Cole B.J.
      • Wimmer M.A.
      • Romeo A.A.
      • Verma N.N.
      Postoperative restoration of upper extremity motion and neuromuscular control during the overhand pitch: evaluation of tenodesis and repair for superior labral anterior-posterior tears.
      ;
      • Frantz T.L.
      • Shacklett A.G.
      • Martin A.S.
      • Barlow J.D.
      • Jones G.L.
      • Neviaser A.S.
      • Cvetanovich G.L.
      Biceps Tenodesis for superior labrum anterior-posterior tear in the overhead athlete: a systematic review.
      ;
      • Smith C.D.
      • Dugas J.R.
      • Emblom B.A.
      • Cain E.L.
      Biceps Tenodesis in Pitchers.
      ), this study represents the first approach to investigate the effect of biceps tenodesis on shoulder stability for individual overhead throwing motions in order to aid sport-specific surgical decision-making for athletes with type II SLAP tear.
      This study has several limitations. Firstly, the kinematic data were collected from healthy individuals who regularly participated in contact and/or team sports. None of the study participants were professional athletes, which may affect the generalizability of the study findings. Additionally, we were limited by a small number of study participants. Secondly, we utilized only one throwing activity for each of the five overhead throwing sports, lacking generalization to all throwing motions for each sport. Thirdly, the musculoskeletal shoulder model did not define an upper bound for each muscle to quantify the maximum muscle force that each muscle can contribute to shoulder movement. This approach has been widely used in the literature (
      • Delp S.L.
      • Anderson F.C.
      • Arnold A.S.
      • Loan P.
      • Habib A.
      • John C.T.
      • Guendelman E.
      • Thelen D.G.
      OpenSim: open-source software to create and analyze dynamic simulations of movement.
      ;
      • Garner B.A.
      • Pandy M.G.
      Musculoskeletal model of the upper limb based on the visible human male dataset.
      ) to account for the inherent difficulty in measuring muscle stresses (
      • van der Helm F.C.
      • Pronk G.M.
      Loading of shoulder girdle muscles in consequence of a glenohumeral arthrodesis.
      ). Also, this study did not represent muscle activation dynamics or pre-tension forces in the modelling. Despite the lack of those data in the literature and thus in the computational shoulder model, the model predictions have previously been validated against electromyographic measurements for athletic motions (
      • Prinold J.A.I.
      • Bull A.M.J.
      Scapula kinematics of pull-up techniques: avoiding impingement risk with training changes.
      ) in addition to functional daily activities (
      • Pandis P.
      • Prinold J.A.I.
      • Bull A.M.J.
      Shoulder muscle forces during driving: sudden steering can load the rotator cuff beyond its repair limit.
      ).

      5. Conclusions

      The study findings demonstrate that an increase in rotator cuff muscle force maintains joint stability for all overhead throwing motions post biceps tenodesis, except baseball pitching. As the presence of a full-thickness tear of the supraspinatus significantly reduces joint stability in four of the five overhead throwing motions, biceps tenodesis may be used as a primary treatment in overhead throwing athletes with intact rotator cuff muscles, except baseball pitchers, as shoulder stability is not compromised following biceps tenodesis.

      Funding

      No funding was received for this study.

      Declaration of Competing Interest

      All authors declare no conflict of interest.

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