Overall, the most common loading type was torsion LT2, followed by LT4, LT1 and LT3. For each of the four mechanically simple loading type categories (LT1-4), both cadaveric and synthetic humeri had been tested. Each category also included studies testing two- and three-part fracture models as well as static and cyclic loading. Overall, synthetic humeri were assessed in ten studies [41, 47, 55, 59, 62, 66, 70,71,72,73] while others tested human cadaveric humeri. Only two studies involved four-part fractures [72, 73], both of which belonged to humerus-tendon category.
Loading type 1: Axial compression and tension
Loading conditions
The LT1 involved the mechanically simple loading of the humerus along its shaft axis. In most studies, this was axial compression, but Instrum et al. [25] imposed tension to simulate the longitudinal distraction of humerus caused by the upper limb weight. Chudik et al. [36] did perform axial compression but only on unplated humeri during the preloading stage of their study, while the main focus was LT4. Thus, their study was not included in this category.
For Dietz et al. [52], static LT1 and cyclic LT2 were applied simultaneously, and vice versa, while for Schumer et al. [51], only static LT1 and cyclic LT2 loads were simultaneously applied. The most common set-up was to fix the humeral shaft and load the humeral head, which was often potted in a polymer holder. In static tests, displacement-control loading at a rate of 5 mm/min have been most frequently employed [24, 26, 27, 30, 49, 66, 67, 70] while displacement rate of 0.1 mm/s [68, 69] and 20 mm/min [25] and load rates of 1 N/s [28] and 20 N/s [51] have also been used. In terms of the loading order, seven [24, 25, 27, 28, 51, 68, 69] of the eleven studies involving both static and cyclic axial loading, performed a static loading-to-failure step at the end to characterise constructs’ load to failure behaviour.
Failure was most often defined as the complete (or irreversible) closure of fracture gap [24, 30, 50,51,52, 68, 69] and as the clear deviation in linearity of the load–displacement curve [26, 27, 50, 52]. Based on the load–displacement curve plots, failure was also defined as a point of a major drop in the load [24, 51] and this was elaborated by Zettl et al. [28] to be a greater than 30% drop in the pressure. Another criterion described failure as humeral displacement greater than 20 [29] or 30 mm [28] on the load–displacement curve.
Measurements and data analysis
For quantitative analysis, most studies recorded the universal testing machine’s actuator loads and displacements. In five studies [49, 64, 65, 68, 69], relative movements of the proximal and distal fracture fragments were recorded during tests using optical and ultrasound-based three-dimensional (3D) motion analysis systems. This was often achieved with the use of reflective markers attached on either side of the fracture gap to describe movements in terms of translations and rotations in the x-, y- and z-axes.
Linear elastic stiffness of the construct, i.e. the gradient of the linear elastic region of the load–displacement curve was most commonly calculated to compare mechanical performance. At the start of their tests, Dietz et al. [52] loaded humeri under elastic conditions to calculate their initial stiffness. After introducing the fracture and fixating the implant, they tested the same humeri to find their second stiffness. They then reported the difference between these two stiffness values as the “loss of stiffness” which was represented as a percentage. Load to failure was also found from load–displacement data, often in studies with initial submaximal cyclic loading and final static loading to failure tests. Moreover, displacement at failure [28], maximum load [30] and yield load [25] was also reported in the literature. The latter was defined graphically as the peak of the load–displacement curves and in case of Instrum et al. [25], it was the tensile yield load. For cyclic loading, number of cycles to failure [26, 51], plastic deformation after a certain number of cycles [27, 28, 50] and maximum [39] and final [51] plastic deformation have been calculated. Hsiao et al. [24] determined peak-to-peak (inter- cyclic) displacement and cumulated deformation at specific cycles.
Loading type 2: Torsion
Loading conditions
LT2, torsional moment on the humerus along the shaft axis, was the most prevalent type of loading in literature. The most popular setup was the direct application of torsion using a material testing machine on a holder (e.g. polymer pot) which held the humerus, with the distal fragment fixed. Three studies [54, 55, 60] imposed torsion on the distal fragment instead of the humeral head. Indirect loading has also been achieved via the use of cables connected to a holding construct [8, 62] and by projecting devices connected parallel [9, 53], and perpendicular [56], to the shaft axis. Internal and external rotations have been performed both in separation and union, from which different parameters and criteria were determined to define the behaviour of bone-plate constructs.
In general, for both static and cyclic loading, the studies could be separated according to the ascending order of their angular displacement rates: 1°/s [10, 59, 61, 66], 5°/min [67], 0.1°/s [68, 69], 0.5°/s [9, 31, 32, 53, 57] and 20°/s [60] or the displacement rates: 1 mm/min [8], 5 mm/min [62] and 12 mm/min [70]. Similarly, large varieties were found among the values and ranges of torques, angles and the time duration of the tests. In case of Foruria et al. [32], rotational moments created by the subscapularis and infraspinatus muscles during shoulder elevation were simulated, based on a previous biomechanical study [74].
Although the studies involving torsion tests to failure were common, for most studies, separate failure criterion was not proposed for the torsion tests. From those that did, Unger et al. [58] set it to be a torsion greater than 4° during one load cycle while for Roderer et al. [57], it was axial displacement greater than 30°.
Measurements and data analysis
In terms of measurements, most studies measured angular displacement from actuator as well as the actuator load but interfragmentary motion was also recorded by nine studies [32, 49, 56,57,58, 61, 64, 68, 69] using 3D motion analysis systems. In addition to torsional stiffness, loss of stiffness [8, 52] after a set number of load cycles has also been calculated. Huff et al. [59] computed the peak torque of the first and the last cycles in the internal and external rotation. Other parameters to be reported were torque-at-failure, angular displacement-at-failure, maximum torque, angular displacement at maximum torsion and energy at failure (area under the torque-displacement plot) [32].
Loading type 3: Bending
Loading conditions
Loading type 3 (LT3) was the bending of the humerus, commonly by loads along either of the two axes perpendicular to its shaft axis (Fig. 2), resulting in either an extension/flexion or varus/valgus moment. In terms of the protocol, Chow et al. [34] and Weeks et al. [35], Lill et al. [64] and Duda et al. [65], and Ruch et al. [53] and Kitson et al. [9] were very similar. Eight studies [8, 33,34,35, 54, 55, 59, 60] subjected humeral shafts to perpendicular loads (Fig. 4A), in a cantilever fashion, with the humeral head fixed. To achieve the required head fixation, either an embedding material such as a resin [33,34,35, 59, 60], a low-melting point metallic alloy [55] or hard gypsum [8] was used, or, in case of Edwards et al., the head was held by a custom-made bone holder consisting of a tube and spiked screws [54]. All of these studies conducted varus bending by orthogonally loading the shaft along the frontal plane. Huff et al. [59] applied valgus, extension and flexion bending in addition to varus.
Several rationales were presented for the loading conditions used in these eight studies. In case of Mathison et al., the load was transmitted 70 mm distal to the third most proximal row of plate’s screw holes with the aim of replicating rotator cuff’s moment during abduction [33]. Most of the other seven studies aimed to load the humeral shaft such as to achieve a bending moment of 0–7.5 Nm at the fracture site [8, 34, 35, 54, 55, 60]. Chow et al. [34] and Weeks et al. [35] performed this on the basis of a biomechanical study by Poppen and Walker [75]. They aimed to replicate the supraspinatus forces on bone-plate constructs during the early stages of healing under shoulder immobilisation support. Mechanically, this loading is comparable to humeral immobilisation followed by a varus force acting directly at the supraspinatus insertion site.
In other eight studies, humeral head was loaded and the shaft fixed [9, 10, 53, 56,57,58, 63,64,65]. Roderer et al., Lever et al. and Kralinger et al. achieved this by fixing the humeral shaft and directly loading the humeral head in the desired direction (Fig. 4b) via a biaxial material testing machine or a 3D spinal loading simulator [56, 57, 63]. Lever et al. loaded the humeral head in the posterior direction for flexion and in a medial direction for abduction [63]. Four studies involved attachment of a circular plate (Fig. 4c) and/or a long metal rod projected horizontally (Fig. 4d) to the humeral head [10, 56, 64, 65]. The load was applied to the plate or the rod, at an offset distance away from the shaft axis, using a vertical machine actuator. This offset point was set along different directions to produce extension, flexion, valgus and varus bending to the constructs. Contrarily, Kitson et al. and Ruch et al. fixed a metal rod that projected vertically (Fig. 4e), along the shaft axis, and loaded it perpendicularly at a set height above the tip of the humeral head [9, 53]. Four of these eight studies performed all of the four key humeral bending movements: extension, flexion, varus, and valgus [9, 10, 53, 57].
Roderer et al. tried to replicate the peak resultant moment during several activities of daily livings such as combing, setting down a 2 kg weight on a board at head height and holding a 10 kg weight, developing on the findings of a previous biomechanical study by Bergmann et al. [76]. Kralinger et al. applied varus bending to reproduce the pull of the supraspinatus and medial shearing (lateral displacement of the head) to simulate the pull of the pectoralis major [56]. Lill et al. and Duda et al. only performed varus bending as the former aimed to reproduce the in vivo displacement of the fracture which occurs mainly due to the tension of the supraspinatus tendon [64, 65]. The study by Unger et al. was unique in the LT3 category in the sense that it neither involved the application of cantilever loads on the shaft nor was the humeral head loaded [58]. Instead, humerus was loaded on the shaft to produce varus bending, with the humeral head set in a custom holder which was connected to a ball-socket joint.
Unger et al. defined failure to be the increase of angular tilting of over 0.5° in varus within 100 load cycles at the lower load magnitudes. Moreover, failure criteria based on the varus collapse and passage of 25,000 cycles during the cyclic tests were implemented by Chow et al. and Weeks et al.
Measurements and data analysis
3D motion analysis systems were used to monitor the relative movements of the fracture fragments [56,57,58, 64, 65]. Mathison et al. [33] used digital image correlation to not only find the relative movement of fracture surfaces but also the local strain across the surface of the specimen. To achieve this, speckling pattern was applied to the specimen surface before starting the tests, which acted as the reference point. During the course of loading, photographs of the specimen were taken which allowed the computation of the relative displacement of the speckles due to the load translations.
Force–displacement data was generally used to measure elastic stiffness and failure load of the bone-plate construct for the corresponding type of bending. For cyclic tests, load per cycle [64, 65] and the mean displacement per cycle [34, 35] and its inverse (number of cycles required to achieve one millimetre of displacement) [34, 35] have been determined. Other parameters calculated for the comparison of constructs’ performance include the displacement and number of cycles at a set interval and to failure as well as the difference in the peak load of the first and last load cycle [59].
Loading type 4: Combined bending and axial loading
Loading conditions
Twenty-three studies conducted LT4 all of which loaded the humeral head except Kwon et al. [61] who loaded the shaft instead. Koval et al. fixed the humeral shaft at 20° of abduction to simulate the primarily shear loading (approximately twice the amount of shear than compression) of the bone-plate construct. This set up acted as the basis for nine biomechanical studies [37, 41, 42, 46, 47, 62, 63, 66, 70]. As well as 20° abduction, Lever et al. [63] mounted the shaft at 20° of forward flexion in a similar manner to Koval et al.
Poppen and Walker computed the force vectors at the glenohumeral joint during isometric scapular plane abduction [75]. Inspired by this study, Hymes et al. and Sanders et al. applied vertical loads to the humeral head 30° posteromedial to the anteroposterior in the plane of rotator cuff pull. This represented the glenohumeral joint force in 0° of abduction that occurs at the surgical neck due to rotator cuff [10, 40]. Similarly, Burke et al. imposed a vertical load of 532.6 N on the head [41]. This was to simulate the maximum reaction forces in the shoulder of a 72 kg average man at 90º of isometric scapular plane abduction, adapted from the Poppen and Walker study [75]. Kwon et al. loaded the humeral shaft with the head fixed and the scapulothoracic motion absent such that the rotation of the specimen from 30° to 80° approximately recreated the glenohumeral rotation that occurs through 30° to 120° shoulder abduction [61]. The 20-50% body weight joint compressive load applied during this cyclic abduction simulated in vivo joint compressive forces described by Poppen and Walker [75].
Six studies based their loading conditions on one of the two studies by Bergmann et al. [76, 77] to introduce glenohumeral contact forces measured in vivo during activities of daily living [39, 43,44,45, 68, 78]. Out of these, four studies [39, 43,44,45] fixed humeri in lateral angulation to perform varus movement, where Roderer et al. [45] and Schliemann et al. [43, 48] tilted the shaft at an angle of 25° while Gradl et al. [39] oriented them at 20°. The remaining two studies were by Katthagen et al. [68, 69] where loads were transmitted vertically to the humeral head with the shaft inclined at 20° in adduction, developed from the studies by Bergmann et al. [76] and Westerhoff et al. [79]. As an attempt to evenly load the specimens, Roderer et al. [45] and Gradl et al. [39] used a polymethyl methacrylate load-cup shaped as negative of the humeral head to represent the glenoid. The former also prevented relative rotation between the cup and the humeral head by applying sandpaper strips on parts of the cup that was in contact with the head.
Erhardt et al. loaded the humeral head while the humeral shaft was set at 30° flexion and 30° abduction to simulate the physiological load vector of a shoulder with an intact rotator cuff during 30°–90° abduction [38]. This load vector is perpendicular to the glenoid plane and generates a glenohumeral contact force of 240 N at 30° of abduction and increases up to 582 N at 90° abduction, as defined by Konrad et al. [80].
Ponce et al. [37] set separate criteria for the comminuted and non-comminuted specimen. For the former, it was the closure of the medial cortical defect while for the latter, it failure load was the maximum load recorded. Specimen angular displacement of 15° in an unloaded condition was considered by Gradl et al. [39] to be failure. Similarly, Roderer et al. [44] and Schliemann et al. [43, 48] defined failure as an increase of varus angular tilting greater than 0.5° within 100 load cycles at lower magnitude (constant 15 N), determined from the data from the 3D motion analysis system. In another study, Roderer et al. [45] employed a criterion of humeral head migration greater than 2 mm, based on fluoroscopic assessment.
Measurements and data analysis
Six studies [41, 43, 44, 48, 61, 68, 69] utilised 3D motion analysis systems for the measurement of humeral and interfragmentary motion. Roderer et al. [44] and Schliemann et al. [43, 48] also recorded the relative motion between the humerus and the plate. Other direct measurements taken were the number, amplitude and distribution of microcracks formed on humeri during testing, which was made possible via the use of acoustic emission testing by Hymes et al. [40]. Fluoroscopic assessment which is often conducted for qualitative analysis was used by Roderer et al. [45] to track the migration of humeral head after a certain number of load cycles from the recording of the relative position of radiopaque reference points with respect to the implant. Bulut et al. [47] measured displacements between fracture ends with a camera and extensometers to allow calculation of the gauge length elongation.
Parameters such as stiffness, ultimate load, as well as load and energy to failure, based on the load–displacement data acquired, have been of principal interest in most studies. In studies performing cyclic tests, the number of cycles at failure and the displacement at a given cycle number have been recorded. Inspired by the work of Poppen and Walker [75], Chudik et al. recorded displacement at 0.3 and 0.6 kN specifically to represent the forces on the humeral articular surface through the humeral geometrical centre during 30° and 90° arm abduction respectively.
Using the acoustic emission testing, Hymes et al. [40] located and recorded the number of the microcracks that were either theoretically locatable (type I) or not (type II). By combining the location information of these microcracks and the X-ray data, damage propagation was visualised in real time. From this, they plotted the number of each crack type against the number of cycles.
Complex loading using humerus-tendon setup
Loading conditions
Unlike the previous four types of loading, these studies involved tests that were both complex and physiologically more accurate. These eleven studies could be further divided according to the type of tendons used in them: cadaveric [81,82,83,84,85,86] or synthetic [71,72,73, 78, 87].
From the six studies testing cadaveric tendons, two studies by Voigt et al. involved the use of a RASS (robot-assisted shoulder simulator) along with hydraulic systems to control the pull of supraspinatus, subscapularis and infraspinatus and teres minor via brass wires sutured to the respective muscles [82, 83]. Both studies replicated the rotator cuff tension during glenohumeral elevation while one also recreated the axial loading at 0° and 60° of glenohumeral abduction as well as the external rotation at 0° abduction with the load magnitudes taken from previous in vitro biomechanical studies [88, 89]. Rose et al. [90] mimicked 10°–60° cyclic abduction by loading the supraspinatus, subscapularis and infraspinatus muscles for 5000 cycles or to failure, with 2.75 kg of mass affixed to distal humerus in order to approximate the mass of the upper extremity. The same three muscles were loaded by Walsh et al. [81] to represent glenohumeral abduction of 30°. Two studies [85, 86] testing cadaveric tendons were based on the biomechanical study by Osterhoff et al. [71]. Sinatra et al. [85] used custom-made shoulder testing setup connected to a material testing machine to recreate 50–100° single plane shoulder abduction. This was achieved with the application of cyclic tensile forces to supraspinatus, infraspinatus, subscapularis, and teres minor tendons while lifting 5 lbs to simulate arm weight. Similarly, Arvesen et al. used custom-made shoulder testing setup to perform 35–65° active glenohumeral abduction. To achieve this, cyclic tensile loads were applied to supraspinatus, subscapularis, and teres minor tendons.
The remaining five studies used different materials as synthetic tendons and all performed glenohumeral abduction. Both Brunner et al. [78] and Kathrein et al. [87] used shoulder joint test bench to perform abduction along the scapula plane and 15°–45° adduction. Pneumatic muscles mimicking the supraspinatus and deltoid for abduction and pectoralis major and teres major for adduction were attached to the insertions of the respective muscles using webbing straps. In case of Brunner et al., the applied muscle forces were comparable to those calculated in a finite element study by Terrier et al. [91]. Da Graca et al. simulated infraspinatus tendons for supraspinatus and subscapularis tendons as well as axillary recess, using leather straps. Straps were glued to the insertion points of the corresponding tendons at one end while on the other end they were drilled into an aluminium scapula that had holes for the supraspinatus, infraspinatus and subscapular fossae. Using this custom-made setup, abduction and internal rotation to failure were carried out.
In a similar fashion, Osterhoff et al. [71] used polyester webbings to represent the pull of muscles and attached them to the corresponding insertions using a cyanoacrylate adhesive for tendon-bone fixation. Pull of supraspinatus and deltoid tendon was replicated for the abduction of 45° to 60° while lifting a 3.75 kg weight at the distal humerus. Also, to simulate the action of infraspinatus/teres minor and subscapularis, constant loads of 25 N each were applied. Similar to da Graca et al., the loading by Osterhoff et al. was cyclic, albeit lasting only 400 cycles as opposed to until failure. Clavert et al. used a custom-made testing setup connected to a mechanical testing machine and used polyethene rope glued to superior and lateral greater tuberosity aspects to simulate 0° glenohumeral abduction and neutral rotation, relative to the scapula plane or 90° of abduction in the scapular plane.
In general, fracture criteria were not explicitly stated in these studies, presumably due to the fact that the loading range of motion was already well-defined in terms of maximum and minimum magnitudes, deeming it unnecessary to set additional criterion. da Graca et al. who defined failure as the sudden drop in the load applied by the universal testing machine, was among the exceptions.
Measurements and data analysis
Force–displacement data was often used to calculate the load and displacements at failure or at a specific number of cycles. Kathrein et al. [87], similar to Brunner et al. [78], reported the maximum resulting forces on the glenoid and of the individual muscles. Voigt et al. [83] recorded the deltoid forces necessary to elevate the arm in set positions, and determined the efficiency of supraspinatus as well as the ratio of deltoid force to arm elevation angle (N/°) in different phases of elevation.
With the aid of 3D motion analysis system, Kathrein et al. [87] recorded the relative motion of the humeral head and the plate and the change at the minimum value of abduction (varus impaction) for each load cycle. Brunner et al. [78] used a 3D motion analysis system, fracture gap motion along the shaft axis and the maximum varus tilt of the humeral head was recorded for each load cycle.
Osterhoff et al. utilised inductive sensor system to record fracture gap distance during the tests. Based on this data, they determined the intercyclic motion at a set number of cycles as well as the fragment migration and the change in the fracture gap distance. Arvesen et al. [86] used video recorder to record fracture gap distance and calculated intercyclic change in fracture gap. Brunner et al. [78] performed X-ray scans before testing and after every 500 cycles to determine the changes in the length of each telescoping pin of the Humerus Block implant, as well as the distance between the pins’ tips and the humeral head cortex.