Bone mineral density, mechanical properties, and trabecular orientation of cancellous bone within humeral heads affected by advanced shoulder arthropathy

Abstract The mechanical properties of cancellous bone in the humeral head are increasingly interesting due to the increased popularity of stemless prosthetic fixation in the cancellous bone of the metaphysis. Age or pathology‐related systemic osteoporosis, inactivity, or pathology of the shoulder joint may influence the primary bonding of implants that rely on good cancellous bone quality. We assessed the bone mineral density (BMD) and anisotropy using micro‐computed tomography (micro‐CT) (0.04 mm voxel size) and correlated the results with indentation load/displacement response. Resected parts of humeral heads (from patients undergoing total shoulder replacement, n = 18) were used as probes. The region of interest was defined as 2 mm medial from the resection plane, presuming that it mirrored the bone quality lateral to the resection plane. The indentation tests were performed with a large probe (diameter 10 mm) in a single destructive loading procedure. The BMD and trabecular orientation were determined by micro‐CT. Our results showed a correlation between the BMD and the slope of the load/displacement curve. Furthermore, the trabeculae were predominantly oriented orthogonal to the joint surface. In conclusion, the predominant factor determining the bone quality and mechanical resistance to pressure appears to be the BMD, while trabecular orientation could not be related to load/displacement response. Statement of clinical significance: Bone quality predominately determines the mechanical properties of cancellous bone. This might be crucial when prosthetic implants need to be anchored in metaphyseal bone. Therefore, clinical decision‐making processes should also include local BMD measurements.


| INTRODUCTION
Mechanical bone properties are important in orthopedic surgery and traumatology as many procedures rely on the mechanical connection between the bone and implanted devices. Historically, the main research focus about bone properties was concentrated on long tubular bones. By introducing new implants that rely on stability and bonding in cancellous bone, the mechanical properties of cancellous bone might influence biological response with consequences on overall treatment results.
Total shoulder prosthesis with stemless humeral components is a new development that relies on uncemented pressfit fixation in the cancellous bone of the humeral metaphysis, preserving the bone, and sparing the humeral canal. Furthermore, this avoids stem-related complications such as intraoperative humeral fractures, stem loosening, stress-shielding, and postoperative periprosthetic fractures 1 as well as difficult stem extraction in cases of revision.
Computed tomography (CT) can be used to assess cancellous bone quality by measuring the local cancellous bone mineral density (BMD), for example, with peripheral quantitative CT (PQCT). Low BMD influences the failure rate after proximal humeral fracture fixation with locking plates, and the suggested threshold was found to be less than 95 mg/cm 3 . 2 The cortical thickness ratio of the proximal humeral diaphysis in standard anteroposterior X-rays is another valuable radiographic parameter to predict intraoperative bone quality in cases of proximal humeral fractures. 3 Estimate of BMD is also used as an input parameter in the algorithm for treatment of proximal humeral fractures. 4 Systemic measurement of BMD to predict mechanical bone response is not a practicable option for shoulder surgery. In cases of prosthetic replacement for arthritis or rotator cuff arthropathy, the local bone quality might be different from systemic BMD values due to inactivity. The surgeon has one final option to assess bone qualityintraoperative haptic assessment by pressing the cancellous bone surface, for example, with the thumb. However, Tulner et al 5 showed that there was consensus among surgeons about haptic characteristics of cancellous bone in the humeral head at the resection plane.
Cancellous bone of the hip shows compression and distraction trajectories (trabecular pattern) but in the humeral head, there is no clearly visible anatomic response to loading forces. A theoretical model that accurately explains the mechanical properties of the proximal humerus could be useful to better understand the pathophysiology of trauma and mechanical complications after shoulder surgery. Finite element (FE) models have already been published and studied for other bones like the proximal tibia 6,7 and proximal humerus. [8][9][10] However, all models rely on PQCT imaging which has insufficient resolution to determine the trabecular bone structure.
Furthermore, mechanical properties are tested on anatomic specimens and not on bone samples taken from patients. In the proximal humerus, this could be an important factor because osteoarthritis or inactivity alone might change bone quality and/or structure (reduced BMD, the formation of bone cysts). Therefore, measurements and FE models calculated for normal bone (or bone of unknown status) might not be applicable to bone encountered in patients. Typically, the indentation measurements and FE models include subchondral cortical bone, but this part of the bone gets removed when implanting shoulder prostheses. Therefore, the probe does not usually reach the cancellous bone at the center of the humeral head.
The aim of our study was to determine how BMD affects mechanical properties of cancellous bone in the humeral head, especially in cases of known pathology potentially affecting the bone structure.
We hypothesized that reduced BMD results in less resistance to penetrating the bone structure and that the trabecular orientation is mainly perpendicular to the joint surface.

| Specimens
The study was performed on 19 resected humeral heads from patients who had undergone a shoulder replacement. Inclusion criteria were: the patient had been scheduled for shoulder prosthesis and had signed informed consent. There were no age limitations. One sample had to be discarded from further analysis since the bone structure was altered due to aseptic bone necrosis. Eleven patients had osteoarthritis related to cuff tear arthropathy, five were classified as idiopathic primary osteoarthritis, and two as posttraumatic arthritis. The bone specimens were fixed in formalin. After nondestructive micro-CT imaging, the specimens were destructively

| RESULTS
The results of BMD measurement and indentation measurements for all specimen are presented in Table 1

| DISCUSSION
Regional or local BMD, in general, is an important factor to be considered in orthopedic surgery while determining treatment strategy.
Also, in the course of operation the information about BMD may be useful when the mechanical stability of implanted devices is questioned. In our study, we investigated BMD in the proximal humerus in the light of applying and potentially developing stemless prosthetic Our results indicate that BMD is the predominant factor for mechanical stability in terms of resisting penetration. Although not anisotropic, the direction of trabeculae did not correlate to load/ displacement response. There are no comparable results in the literature because recent similarly designed studies 6,10 also involved subchondral bone (Table 2) tests using one large probe, which limits the testing to only one assay.
We could have tested more spots on the specimen surface, map the results. and calculate average values using a small probe. We accepted this disadvantage in favor of applying a construction similar to the base plate of a stemless prosthesis. The next limitation is also related to prosthetic design: we did not measure pull-out strength or resistance to horizontal torsional loading, which might be of interest for prosthetic anchors, cages, or screws. However, an FE model could provide these answers in the future, with detailed micro-CT based structural information and the results of indentation tests. At present, the stemless design is mainly available for anatomic shoulder arthroplasty but there is a trend to implement stemless design for reverse shoulder arthroplasty as well. Therefore, we included also patients with cuff tear arthropathy, but this introduced further limitations to our study: small sample size and heterogeneities of pathologies.
In conclusion, the predominant factor determining the bone quality and mechanical resistance to pressure appears to be the BMDs, while the trabecular orientation could not be related to load/ displacement response. Abbreviation: QCT, quantitative computed tomography.