Introduction

Osteoporosis has presented itself as a growing problem for aging populations, both in the United States and worldwide, with over 10 million Americans and over 200 million women worldwide diagnosed with this bone disorder [1, 2]. As the number of aging adults continues to grow, the prevalence of osteoporosis and its health care, economic and social burdens continue to increase significantly [3]. Appropriate awareness and treatment of osteoporosis is crucial not only to prevent fractures and associated morbidity, but also to optimize surgical outcomes and overall quality of life for our patients.

Osteoporosis is common among patients who present to orthopaedic surgeons with an indication for shoulder surgery. Approximately 80% of operative proximal humerus fractures occur in women aged 74 to 84 years old [4]. Among patients proceeding with shoulder arthroplasty, at least 14.3% of those undergoing anatomic total shoulder arthroplasty and 26.2% of those undergoing reverse shoulder arthroplasty have preoperative osteoporosis [5]. With over 250,000 surgical repairs performed in the United States each year, rotator cuff tears are another common shoulder condition in this aging demographic, and quality of bone in the greater tuberosity known to play a crucial role in the durability of these repairs [6,7,8,9].

Osteoporosis is a leading risk factor for development of shoulder pathology requiring surgical intervention, and is implicated in surgical complications for all common shoulder procedures. Osteoporosis is the cause of fragility fractures; patients with osteoporotic bone are 2.6-fold more likely to incur proximal humerus fractures than those with non-osteoporotic bone [4, 10] The compromised bone quality, characterized by fragmentation, thinning of the cortical layer, and cancellous bone, also complicates osteosynthesis when surgical management is undertaken [4]. In terms of shoulder arthroplasty, osteoporosis increases the odds of peri-prosthetic fractures by 2.24 times, and prosthetic joint infections by 1.68 times, compared to non-osteoporotic controls [11,12,13]. Additionally, osteoporosis is an independent risk factor for acromial stress and scapular spine fractures after reverse shoulder arthroplasty [11, 14, 15]. Rotator cuff repairs are also highly dependent on overall, and especially tuberosity, bone quality for repair integrity and anchor pullout strength, with numerous studies identifying poor bone quality as a risk factor for repair failure and worse outcomes [7,8,9, 16].

Optimizing surgical outcomes and patient care of these shoulder conditions should routinely include consideration of bone quality, and in some cases, formal evaluation and treatment of it. The goals of this review are to synthesize the currently available data and offer evidence-based recommendations surrounding bone mineral density, as they apply to the shoulder surgeon and their patients.

Preoperative Evaluation and Optimization

A multidisciplinary approach to management of osteoporosis is essential due to the extensive number of risk factors. Modifiable risk factors include, but are not limited to the following: inadequate nutrition, lack of physical activity, smoking, weight loss, and alcohol use [17, 18]. Current management for osteoporosis involves mitigating these risk factors through lifestyle modifications in addition to vitamin D and calcium supplementation [19]. All patients undergoing shoulder surgery should be counseled on lifestyle factors as modifiable risk factors. Extending to pharmacologic treatment pre-operatively depends on many factors. Unfortunately, many shoulder surgery candidates who would benefit from osteoporosis screening or treatment do not receive it. Despite up to two thirds of patients undergoing shoulder arthroplasty having an osteoporotic bone mineral density (BMD), only 12% have been found to have had a pre-operative BMD evaluation [20]. Screening and treatment for osteoporosis has also been found to be severely underutilized in patients undergoing rotator cuff repair [21].

The gold standard diagnostic tool for osteoporosis includes a dual-energy X-ray absorptiometry (DXA) which measures BMD at various anatomical locations, most commonly the femoral neck, and compares an individual’s density to standardized results from healthy individuals aged 25 to 35 years old. A t-score between -1 to -2.5 standard deviations (SD) below the mean indicates a BMD consistent with osteopenia and a t-score beyond -2.5 SD below the mean is diagnostic of osteoporosis [22].

Numerous studies have highlighted the utility of computed tomography (CT) scans as an avenue to both correlate with DEXA results and to independently estimate BMD [23,24,25]. This can typically be done by a Hounsfield Units (HU) measurement in the proximal humerus or glenoid neck. Given the high proportion of patients undergoing shoulder surgery who have a pre-operative CT scan for surgical planning, additionally measuring HU to estimate BMD from this scan would be a simple way to identify patients with osteoporosis (Fig. 1).

Fig. 1
figure 1

Example measurement of bone mineral density of the humeral head by CT method. A line is drawn on a sagittal cut from the superior humeral head to the surgical neck. This line is divided into quarters, with the dividing lines providing 3 axial slices. An ellipse is drawn on each identified axial cut to measure Houndsfield units (HU) excluding all cortical bone. The average of the 3 measurements is taken as the final value [24]

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In addition to CT scans, plain films have been shown to have utility in assessing BMD for the proximal humerus. Cortical measurements from AP radiographs of the shoulder have shown an association with local BMD as well as with DEXA values for the femur, both by using the cortical bone thickness average (Fig. 2) or the deltoid tuberosity index (Fig. 3) [26,27,28]. With every shoulder surgery patient undergoing at least plain films preoperatively, this similarly presents a low cost, time-efficient way to screen for osteoporosis.

Fig. 2
figure 2

Example measurement of cortical bone thickness average. Cortical thickness is measured at two levels, 20 mm apart, with the proximal level being the first point at which the medial and lateral cortices become parallel. In this case the average of (M1-M2) and (M3-M4) is 8.35 [100]

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Fig. 3
figure 3

Example measurement of the deltoid tuberosity index. Cortical thickness for this measurement is taken at one site, immediately proximal to the deltoid tuberosity, and divided yielding a ratio (a/b) [28]

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Despite the clear prevalence of osteoporosis and osteopenia in shoulder surgery patients and its detrimental effect on outcomes, there is minimal data on the advantages to pre-operative medical treatment in the form of bisphosphonates or anabolic agents. In one database study looking at patients with fragility fracture history undergoing shoulder arthroplasty, no difference was found between patients who took bisphosphonates pre-operatively and those who did not with regard to periprosthetic fracture and all-cause revision [12]. Moreover, one study has previously identified pre-operative bisphosphonate use as a risk factor for intraoperative fractures [29]. In terms of operatively treated proximal humerus fracture, Seo et al. identified no difference in union rates or clinical outcomes with early bisphosphonate initiation. [30] Lastly, one clinical study found that zoledronic acid improved rotator cuff healing with reduced retear rate [31] and decreased failure rates [32] in female patients with osteoporosis. However, a database study found no difference in revision rates of rotator cuff repairs amongst patients with osteoporosis who did or did not take bisphosphonates [33].

A more easily agreed upon pre-operative intervention would be vitamin D supplementation, due to the low risk and cost of its administration. Recommended dietary allowances are listed in Table 1 [34,35,36]. Vitamin D deficiency has been linked to post-operative complications in shoulder arthroplasty and rotator cuff repair.84 Similarly, it has been associated with a higher retear rate, revision rate, and early pain score after rotator cuff repair [37,38,39]. Due to this, vitamin D supplementation has been identified as a worthy adjunct in rotator cuff repair [40, 41].

Table 1 Recommended daily intake of calcium and vitamin D for adults. Recommendations include the total amount from all sources, both dietary and supplements. IU = International Units; mg = milligrams
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Surgical Considerations

Despite appropriate patient screening, indications and pre-operative optimization, there will continue to be an increasing number of patients undergoing shoulder surgery with poor bone quality. Many of these are non-elective cases where optimization is not possible. In these cases, there are specific techniques and considerations that can be considered to optimize outcomes and minimize complications in patients with poor bone quality.

Proximal Humerus Fracture Fixation

As with all osteoporotic fractures, proximal humerus fracture fixation is fraught with difficulties, including limited screw purchase, screw pullout, and failure of fixation. These complications happen despite the standard of care being contoured locking plates used as a fixed angle construct. Failure of fixation in these cases often presents as varus collapse, which can also be associated with screw cutout and penetration into the articular surface. This is a particularly morbid complication as it can lead to destruction of the glenoid articular surface [42]. Some of these complications can be solved by the use of locking screws, which is why a fixed angle construct is often considered the standard of care in osteoporotic bone. In addition, the surgeon should be aware of the locking mechanism of the screws they are using (threaded, variable angle, locking caps, differential material properties), to ensure that they are employed in the method intended and reduce the likelihood of malfunction or loss of fixation at the screw-plate interface.

Screw positioning is another factor that has been studied in proximal humerus fracture fixation. Specifically, distal calcar screw placement compared to neutral placement in osteoporotic bone leads to increased torsional stiffness in external rotation, increased axial stiffness and decreased humeral head displacement during fatigue testing [43]. Optimal placement of the calcar screw was defined by Padegimas et al. as being within 12 mm of the calcar or with a ratio of the calcar distance and humeral head diameter of 25% (example measurement shown in Fig. 4). If these thresholds were not met, they found patients were at a higher risk for fixation failure and subsequent reoperation [44].

Fig. 4
figure 4

Example of a fixed angle locking plate used for fixation of a proximal humerus fracture, with measurement of the calcar screw distance demonstrated [44]

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Although not routinely used, screw augmentation through cement or bone grafting has been shown to have favorable mechanics and outcomes. Polymethyl methacrylate (PMMA) cement has been shown to decrease the chance of fixation failure in low bone mineral density patients [45]. Similarly, there is support for calcium phosphate augmentation in osteopenic bone because it increases torsional and axial stiffness [46], improves compressive strength and structural support, [47] and decreases fracture displacement without screw penetration [48]. Cancellous autograft bone has also been used as an augment to plate fixation for multipart fractures and fractures with severe comminution and has been shown to minimize complications including avascular necrosis and nonunion [49, 50].

Suture augmentation is another technique with good literature support that is routinely used to augment fixation of the tuberosities and prevent tendon tearing or pullout in osteoporotic bone [4]. This can usually be accomplished by tying a suture configuration through holes in a plate, and can help avoid secondary tuberosity displacement [47]. It should be considered in cases with suboptimal reduction, multiple fracture fragments, comminution and when a plate only partially covers the greater tuberosity [47].

Additionally, a medial strut graft, most commonly performed with fibula allograft, can be used to augment internal fixation in osteoporotic bone as medial support to prevent varus collapse [51]. Studies have found that fibular strut grafts in osteoporotic bone result in lower intercyclic motion [52], lower fragment migration [52], less residual deformation [52], greater load to failure[53], increased stability [54], increased resistance to repetitive varus loading [55], and increased stiffness [54].

Another consideration is intramedullary nailing, which allows load sharing and reduces stress at the bone implant surface. This makes it an excellent option for treating osteoporotic proximal humerus fractures [56]. Although previous studies have shown some associated morbidity, including rotator cuff injury, shoulder pain, subacromial implant prominence, inadequate fixation and difficulty with reconstruction of nonunion; evolving contemporary techniques are reducing the incidence [57] of these complications [42]. More recent studies have shown no difference in complication rates between intramedullary nailing and locking plate fixation for proximal humerus fractures [57, 58]. The decision between intramedullary nailing versus plate fixation should be chosen based on the type of fracture, patient factors and surgeon experience, utilizing shared decision making between patient and surgeon [57, 58].

Shoulder Arthroplasty for Fracture

Three and 4-part proximal humerus fractures in osteoporotic bone are considered to be at high risk for fixation failure or avascular necrosis. This reality combined with a growing body of literature supporting satisfactory outcomes for reverse shoulder arthroplasty performed for proximal humerus fractures has led to an increase in its utilization for this indication [59, 60].

Considerations for reverse total shoulder arthroplasty (RTSA) for repair of fracture in an osteoporotic patient includes stem positioning, tuberosity fixation, and cement utilization. Stem positioning and distalization is important for fixation and stability, because a shortened limb leads to instability and an increased incidence of dislocation, although balancing this with risk factors for scapular spine fractures must be considered [61]. In cases where a cortical read is not possible to assess height, the distance between the upper border of the pectoralis major tendon insertion and the top of the implant can be used for reconstruction of the humeral length for improved reduction and stability [62, 63].

Literature has shown that the successful healing of the greater tuberosity leads to improved external rotation after RTSA for fracture [64,65,66]. Cerclage fixation may cause less tuberosity interfragmentary rotation when compared to suture fixation, but has not been studied specifically in osteoporotic bones [67]. Autograft bone grafting of the tuberosities has been show to improve tuberosity healing, with greater disability of the arm, shoulder and hand (DASH) scores and American shoulder and elbow surgeons (ASES) scores [68,69,70].

Comparisons between cemented and uncemented stems for RTSA for fractures in osteoporotic bone have shown no difference in functional outcomes [71, 72]. One study found that cemented stems had higher rates of stem loosening than press fit stems [72]. Another study found that the incidence of radiographic signs of bone resorption was higher in uncemented RTSA, but was without clinical significance as both cemented and uncemented showed good functional results and low complications rates [71]. If using a cemented implant, keeping cement out of the metaphyseal region is expected to help with tuberosity healing [4].

Hemiarthroplasty (HA) is another option for management of proximal humeral fracture in patients with poor bone quality [73] or as an alternative arthroplasty in patients with glenoid bone deficiency or posterior wear [74]. Surgeons should consider that osteopenia is a risk factor for failure in HA [75]. Furthermore, healing from hemiarthroplasty is unreliable with an approximated 50% rate of tuberosity malposition [76]. Factors that contribute to this are improper prosthetic version and height and tuberosity mal-reduction that may stress the rotator cuff and hinder tuberosity healing [60].

Elective Shoulder Arthroplasty

As previously described, low BMD has been shown to increase the incidence of both periprosthetic fractures [11, 12] and infection [12] after elective shoulder arthroplasty. Surgical considerations to mitigate fracture risk and improve implant fixation include careful retractor placement, cement utilization, and use of longer stems. [77],24 Stem selection is particularly important in osteoporotic bone, with some literature recommending increased stem diameter and length to ensure adequate fixation.23,24 Additionally, some studies have found that in osteoporotic bone, hand reaming should be used instead of power instruments to reduce the risk of removing too much cancellous bone and the chance of cortical perforation [78, 79]. Stemless implants for anatomic TSA were initially advised to be avoided in patients with osteoporosis; however, contemporary practice continues to evolve and expand the indications for stemless implants [80]. Furthermore, the generally accepted intraoperative thumb test to determine candidate suitability for a stemless implant has shown to be a poor indicator of low BMD.37

Rotator Cuff Repair

In order to reduce incidence of re-tear or repair failure, surgeons should consider the bone density of the humerus, specifically the greater tuberosity, when planning rotator cuff surgery. Higher trabecular and cortical bone density were found in the proximal part of the tuberosities [16, 81, 82] and the humeral head has higher density then the neck [83]. As a result, these areas have been suggested as preferred anchor locations to prevent anchor loosening or pullout. Because osteoporotic patients have lower bone quality in the greater tuberosity, surgeons should limit or completely avoid aggressive decortications of the tuberosity region to preserve cortical bone [8].

In general, the more fixation points, the less stress concentrated over the anchor bone and suture tendon interface. This supports the use of a greater number of anchors to share the stress. [8] In the past, metal anchors have been a mainstay of rotator cuff repair; however, metal anchors were tested against newer bioabsorbable anchors in the osteoporotic patient, and bioabsorable anchors outperformed metal in pullout strength [84]. Additionally, bone screw anchors have increased pullout strength compared to hook type anchor in osteoporotic bone [81].

In cases of osteoporotic bone, both cement augmentation [85, 86] and magnesium phosphate augmentation [85] have been found to increase anchor pullout strength compared to conventional techniques. Previously, considering Burkhart’s Deadman angle [87] reduced the angle between suture anchor and rotator cuff tendon, resulting in higher pullout strength [84]. More recently, however, insertion angles of anchors were revisited. Strauss found 90 degree anchors had significantly improved anchor pullout strength than 45 degree, which was support by Eji et al. [88, 89].

Utility of Osteoporosis Medications

The role for osteoporosis medications in fracture prevention is beyond the scope of this review, which will focus on specific indications for pharmacotherapy as they relate to shoulder surgery. Historically, the mainstay of medical treatment for osteoporosis has been bisphosphonates, which are considered to be anti-resorptive agents [90]. More recently, anabolic agents have become available with US Food and Drug Administration (FDA) approvals of abaloparatide (Tymlos) in 2022, romosozumab (Evenity) in 2019, and teriparatide (Forteo) in 2002. Animal studies have begun to show promising results for anabolic agents used to biologically augment tendon repairs, and increasing attention has been turned towards their utility in fracture healing.

As previously stated, pre-operative use of bisphosphonates have not been found to consistently enhance outcomes in shoulder arthroplasty, fracture fixation or rotator cuff repair, in the few clinical studies that have examined this. [12, 29,30,31,32,33]. One clinical study found that zoledronic acid improved rotator cuff healing with reduced retear rate [31] and decreased failure rates [32] in female patients with osteoporosis. However, a database study found no difference in revision rates of rotator cuff repairs amongst patients with osteoporosis who did or did not take bisphosphonates [33]. One case study has shown effectiveness of teriparatide used as an adjunct for successful non-operative treatment of post operative acromial stress fracture after RTSA, which may merit further investigation [91]. Anti-osteoporosis agents raloxifene, [92] risedronate, [93] zoledronic acid [94], teriparatide [95] and abaloparatide [96] have been studied in rotator cuff healing in rats and all showed promising results.

Finally, and perhaps most importantly in present day clinical practice, is the use of these medications to prevent secondary fractures. Within 5 years of a proximal humerus fracture, 20% of patients have been found to suffer a secondary fracture, with database data supporting less than 2% of patients with proximal humerus fractures receiving appropriate evaluation and treatment [97, 98]. Shoulder surgeons frequently treat patients with proximal humerus fragility fractures, and increasing resources make evaluation, treatment, or referral accessible in many (though not all) regions. Implementation of a fracture liaison service has been shown to increase osteoporosis screening in all cases of fragility fractures, as well as specifically patients who suffer proximal humerus fractures [99].

Conclusions

As our population of increasing age with high functional demands continues to grow, we will increasingly perform shoulder surgery on patients with poor bone quality. Incorporating routine use of lifestyle and nutrition optimization, as well as opportunistic bone density screening into clinical practice, are simple steps to reduce surgical complications from low BMD. Intraoperative techniques should be modified when necessary to limit the risk of complications as well and improve implant longevity and outcomes. Further research is needed to identify the utility of pre-operative osteoporosis medications for patients with low BMD undergoing shoulder surgery; as well as clinical studies examining biologic augmentation with anabolic medications. Osteoporosis screening and referral should also have a low-barrier pathway for all shoulder surgeons to perform or direct their patients towards.

Key References

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    • This article provides from context surrounding the concern for complications after rotator cuff repair in patients with osteoporosis.

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    • This article provides from context surrounding the concern for complications after shoulder arthroplasty in patients with osteoporosis.

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    • A review of epidemiology related to shoulder arthroplasty, which highlights the scope of this challenge.

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    • This study presents one of several opportunistic methods to easily predict proximal humerus bone density using existing imaging.

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    • An important technical consideration in proximal humerus fracture fixation is reviewed and quantified in this paper.

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    • A common technical branch point in shoulder surgery patients with osteoporosis is discussed and examined in this study.

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    • One of several studies that reports outcomes in human patients after rotator cuff repair, when taking bisphosphonates post-operatively.

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    • This paper reports on the most recent investigation into anabolic anti-osteoporosis medications as a biologic augment to rotator cuff healing, in an animal model.