Abstract
Background
Pseudoarthrosis is the most common indication for revision in spinal deformity surgery. Parkinson’s disease (PD) is associated with postural instability and sagittal and coronal plane deformities. Spinal fusion in PD has a high rate of complications. The risk factors for pseudoarthrosis in PD cases are yet to be elucidated. This study identifies operative and patient factors associated with pseudoarthrosis after thoracolumbar (TL) fusion in patients with PD.
Methods
In this retrospective case-control study, adult PD patients who underwent posterior TL fusion at an academic center between 2017 and 2022 were retrospectively identified. Comorbidities, functional status, PD metrics, bone and muscle quality, indications, and construct-related factors were extracted. Fusion status was assessed via continuous osseous bridging on 1-year postoperative computer-aided tomography (CT) scan. Univariate analysis compared preoperative and intraoperative variables based on fusion status.
Results
Fifty-nine patients were analyzed (27% pseudoarthrosis rate). Pseudoarthrosis was associated with screw loosening (53% vs. 16%, P=0.01) and mortality (90-day: 13% P=0.05; 1-year: 31% P=0.001). Tremor (87% vs. 54%, P=0.049), lower Hounsfield units (HU: 97 vs. 138, P=0.03), wheelchair use (25% vs. 5%, P=0.01), and trauma indications (38% vs. 5%, P=0.003) showed elevated risk of pseudoarthrosis. There were no differences in fusion rates based on PD duration, PD medications, psoas muscle area, non-traumatic indications (spondylolisthesis, deformity), interbody utilization, construct length, and bone morphogenic protein usage (P>0.05).
Conclusions
PD remains a major risk factor for poor outcomes after TL spinal fusion. Wheelchair use, lower HU, essential tremor, and trauma patients increased pseudoarthrosis rate. Pseudoarthrosis was associated with increased mortality.
Keywords: Thoracic fusion, Parkinson’s disease (PD), lumbar fusion, spinal fusion
Highlight box.
Key findings
• Risk for pseudoarthrosis in patients undergoing thoracolumbar (TL) arthrodesis with Parkinson’s disease (PD) is higher for (I) wheelchair bound patients; (II) those with visible essential tremor; (III) those who are indicated due to trauma; and (IV) those with lower Hounsfield units on computer-aided tomography scan.
What is known and what is new?
• PD patients indicated for TL fusion are at increased risk for medical (morbidity and mortality) and surgical (failure of fusion or hardware, or adjacent segment stenosis) complications.
• This study adds specific risk factors that are clinically relevant, easily obtainable and clinically actionable in this rare and complex population. Pseudoarthrosis is relatively common and is associated with hardware failure and mortality in these patients.
What is the implication, and what should change now?
• Practitioners should recognize the presence of poor bone health, visible tremors, mobility aids and the link between pseudoarthrosis and complications.
• Appropriate counseling, optimization and shared decision-making discussions should include acknowledgment of these risks.
Introduction
Pseudoarthrosis after thoracolumbar (TL) fusion is a well-known cause of morbidity among spine patients. Occurring in nearly 2% of all thoracic and lumbar arthrodesis, it represents one of the most common causes of reoperation after fusion operations and a significant cost to healthcare systems (1,2). Furthermore, the rate drastically increases in spinal deformity surgery (3). Typical risk factors include increased length of construct, smoking, patient bone quality, age and long-term steroid use (1,3). Parkinson’s disease (PD) is a progressive neuromuscular disease characterized by tremors or rigidity and a background of generalized slowing of movements (bradykinesia). The incidence of PD increases with age, including nearly 1% of the population over the age of 60 years (4). Ongoing advancements in disease mitigation allow patients to maintain activity and survive longer than in previous decades (4). Despite this, the relentless and progressive nature of the disease results in poor quality of life for most patients (5). A combination of neurologic deterioration, muscular composition changes, and poor bone quality can result in a prototypical stooped posture, dropped head, and flexed trunk, hips, and knees (6). When PD progresses to its extreme of deformity, it results in disabling spinal conditions, such as scoliosis, antecollis, camptocormia, and Pisa syndrome (7). Multiple studies have demonstrated an increased cost of care, revision surgery, construct failure, and in-hospital medical complications for PD patients receiving spine surgery (8-10). Despite the significant risks, PD patients do experience significant improvement with successful surgical treatment (11,12). Pseudoarthrosis after spinal fusion is a multifactorial complication consisting of patient factors, biological influences, and surgical techniques. While there is literature documentation of increased rates of pseudoarthrosis, no study, to our knowledge, has explored specific risk factors predisposing PD patients to pseudoarthrosis. While there is considerable reassessment of spine surgery in PD patients, there is scant new contribution to the literature, which this assessment aims to add. This study seeks to identify the patient-specific, and surgical risk factors that lead to pseudoarthrosis after TL spinal fusion in a population of PD patients. Secondarily, we aim to identify the morbidity and mortality of pseudoarthrosis patients. We present this article in accordance with the STROBE reporting checklist (available at https://jss.amegroups.com/article/view/10.21037/jss-25-73/rc).
Methods
Study design and population
This retrospective review of single center experience with spinal fusion patients with concomitant PD at the time of spinal surgery. After Institutional Review Board approval, all PD patients over age 18 years who underwent primary or revision posterior TL fusion for deformity, degenerative, and traumatic indications at an academic center between 2017 and 2022 were retrospectively identified. Infection, oncologic and anterior or lateral only surgery were excluded from the patient cases. Patients were required to have a PD diagnosis by a neurologist within one year of spinal surgery. The included patients were divided into the case (with pseudoarthrosis) and control (without pseudoarthrosis) groups. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by institutional ethics committee of The Mayo Clinic Office for Human Research Protection (FWA00005001) and individual consent for this retrospective analysis was waived.
Postoperative and radiographic complications by X-ray and computer-aided tomography (CT) scan were analyzed for pseudoarthrosis, with fusion status being defined as continuous osseous bridging on 1-year postoperative CT scan. These were divided between gutter or disc space fusion. Univariate analysis compared preoperative and intraoperative variables based on fusion status.
Patient demographic and medical data including age, race, sex, smoking status (never/former/current), body mass index (BMI), presence of deep brain stimulator (DBS) before surgery, use of gait aid, chronic falls, use of non-carbidopa/levodopa medications, dementia status, presence of tremor, and length of Parkinson’s diagnosis, were recorded via chart review. Preoperative bone and paraspinal muscle quality were assessed through bone mineral density (BMD), BMD t-score, Hounsfield units (HU) at L3, iliopsoas area, and anterior-posterior diameter at the level of the L3–4 interspace. Surgical factors include operative indication (deformity, instability, radiculopathy), interbody use, length of construct (>3 defined as long construct), and use of bone morphogenic protein (BMP). Postoperative complications included superficial or deep infections, delayed healing or wound dehiscence, postoperative hematoma, reoperation, respiratory or cardiac event, deep vein thrombosis/pulmonary embolism (DVT/PE), 90-day or 1-year mortality.
Statistical analysis
Descriptive statistics were used to compare patient demographics in terms of mean and standard deviation or number of occurrences and percent of total. Continuous and categorical variables were analyzed with t-tests and Chi-squared tests or the corresponding non-parametric tests, respectively. Multivariate linear and logistic regression models were developed to isolate the effect of preoperative patient and intraoperative surgical variables on pseudoarthrosis formation. All statistical analysis was performed with R Studio Version 4.0.2 (Boston, MA). A P value <0.05 was statistically significant.
Results
Population statistics
Fifty-nine patients met the inclusion criteria for this study. Pseudoarthrosis occurred in 27% of the overall patient population (16/59), with overall reoperations in 15% (9/59) and total major complications in 22% (13/59). The mean age of all patients was 73.2 years and the population was 28% male and predominantly white.
Patient and disease characteristics (Table 1)
Table 1. Patient and disease characteristics.
| Characteristics | Pseudoarthrosis (n=16) | Fusion (n=43) | P |
|---|---|---|---|
| Mean age (years) | 75.4 | 72.4 | 0.14 |
| Sex | 0.76 | ||
| Male | 4 (25.0) | 13 (30.2) | |
| Female | 12 (75.0) | 30 (69.8) | |
| Race (%White) | 16 (100.0) | 43 (100.0) | 0.46 |
| BMI (kg/m2), mean (SE) | 27.6 (5.25) | 28.5 (6.04) | 0.59 |
| DBS before spine surgery | 0.31 | ||
| No | 16 (100.0) | 38 (88.4) | |
| Yes | 0 (0.00) | 5 (11.6) | |
| Gait aid | 0.01* | ||
| None | 6 (37.5) | 6 (14.0) | |
| Cane | 1 (6.25) | 8 (18.6) | |
| Walker | 5 (31.2) | 27 (62.8) | |
| Wheelchair | 4 (25.0) | 2 (4.65) | |
| Chronic falls | 0.42 | ||
| No | 5 (33.3) | 16 (37.2) | |
| Yes | 9 (66.7) | 27 (62.8) | |
| Non-Sinemet med | 0.71 | ||
| No | 8 (66.7) | 29 (76.3) | |
| Yes | 4 (33.3) | 9 (23.7) | |
| Dementia | 0.94 | ||
| No | 6 (42.9) | 21 (48.8) | |
| Yes | 8 (57.1) | 22 (51.2) | |
| Resting tremor | 0.04* | ||
| No | 2 (13.3) | 20 (46.5) | |
| Yes | 13 (86.7) | 23 (53.5) | |
| Days between diagnosis and surgery, mean [range] | 263 [48.8–1,027] | 1,063 [182–2,130] | 0.12 |
Data are presented as number (%) unless otherwise indicated. *, P<0.05. BMI, body mass index; DBS, deep brain stimulator; SE, standard error.
Baseline characteristics of age, sex, and BMI were statistically similar between cases and controls. Groups were similar between presence of DBS (100% vs. 88%, P=0.31), chronic falls (66.7% vs. 62.8%, P=0.42), use of supplementary (non-carbidopa/levodopa) medications (33% vs. 24%, P=0.71), presence of dementia (57% vs. 51%, P=0.94), and length of time with diagnosis of PD (mean 263 vs. 1,063 days, P=0.12). Pseudoarthrosis cases were more likely to occur in patients who were wheelchair bound (25.0% vs. 4.7%, P=0.01) and had visible resting tremors (86.7% vs. 53.5%, P=0.04).
Radiographic characteristics (Table 2)
Table 2. Preoperative radiographic characteristics.
| Characteristics | Pseudo (n=16) | Fusion (n=43) | P |
|---|---|---|---|
| HU at L3 | 92.8 [79.4–114] | 127 [104–169] | 0.03* |
| HU at L5 | 108 [96.6–137] | 136 [101–165] | 0.32 |
| Iliopsoas area at L3/4 (mm2) | 1,402 [550.0] | 1,277 [337.0] | 0.49 |
| Iliopsoas A-P diameter (mm2) | 47.1 [9.90] | 43.5 [6.32] | 0.28 |
| HU, iliopsoas at L3/4 | 45.5 [43.5–51.8] | 49.5 [45.8–53.0] | 0.54 |
| Radiculopathy | 0.10 | ||
| No | 12 (75.0) | 20 (46.5) | |
| Yes | 4 (25.0) | 23 (53.5) | |
| Fracture | 0.003** | ||
| No | 10 (62.5) | 41 (95.3) | |
| Yes | 6 (37.5) | 2 (4.65) | |
| Adult deformity | >0.99 | ||
| No | 15 (93.8) | 39 (90.7) | |
| Yes | 1 (6.25) | 4 (9.30) | |
| Revision surgery | 0.49 | ||
| No | 7 (43.8) | 25 (58.1) | |
| Yes | 9 (56.2) | 18 (41.9) | |
| Instability/spondylolisthesis? | 0.34 | ||
| No | 13 (81.2) | 28 (65.1) | |
| Yes | 3 (18.8) | 15 (34.9) | |
| ASD | >0.99 | ||
| No | 15 (93.8) | 39 (90.7) | |
| Yes | 1 (6.25) | 4 (9.30) |
Data are presented as number (%) or mean [range], or mean [standard deviation]. *, P<0.05; **, P<0.01. A-P, Anterior and Posterior Approach Surgery; ASD, Adjacent Segment Disease; HU, Hounsfield units.
The cases of pseudoarthrosis had a statistically decreased mean HU (92.8 vs. 127.0, P=0.03) and occurred more often in patients indicated for surgery due to fractures (37.5% vs. 4.65%, P=0.003). Other preoperative radiographic characteristics including the iliopsoas area and HU did not reveal an association with pseudoarthrosis. Similarly, the pseudoarthrosis and fusion cases did not differ for the surgical indications of radiculopathy, deformity, or instability. Revision surgery was not statistically associated with pseudoarthrosis.
Surgical characteristics (Table 3)
Table 3. Surgery characteristics.
| Characteristics | Pseudo (n=16) | Fusion (n=43) | P |
|---|---|---|---|
| Short or long | >0.99 | ||
| Short (1 to 3 levels of fusion) | 11 (68.8) | 30 (69.8) | |
| Long (4 levels of fusion or more) | 5 (31.2) | 13 (30.2) | |
| Interbody | 0.39 | ||
| No | 9 (56.2) | 17 (39.5) | |
| Yes | 7 (43.8) | 26 (60.5) | |
| Number of fusion levels | 2.00 [2.00–5.00] | 2.00 [1.00–4.00] | 0.39 |
| Number of interbody levels | 0.00 [0.00–2.00] | 1.00 [0.00–2.00] | 0.45 |
| Number of decompression levels | 1.50 [0.75–2.00] | 2.00 [1.00–3.00] | 0.31 |
| BMP | 0.10 | ||
| No | 14 (87.5) | 26 (60.5) | |
| Yes | 2 (12.5) | 17 (39.5) | |
| Ending at TL junction | 0.61 | ||
| No | 14 (87.5) | 40 (93.0) | |
| Yes | 2 (12.5) | 3 (6.98) | |
| Approach: single or A/P | 0.048* | ||
| A/P | 0 (0.00) | 8 (18.6) | |
| Single | 16 (100.0) | 35 (81.4) |
Data are presented as number (%) or mean [range]. *, P<0.05. A/P, Anterior and posterior approach surgery; BMP, bone morphogenic protein; TL, thoracolumbar.
There was no statistical association between pseudoarthrosis and length of fusion construct, use of interbody device, or the use of BMP. The only surgical factor of statistical significance was the use of a single approach was a risk factor for the formation of pseudarthrosis P=0.048.
Outcomes and complications (Table 4)
Table 4. Complications/outcomes.
| Complication type | Pseudo (n=16) | Fusion (n=43) | P |
|---|---|---|---|
| New postop falls | 0.73 | ||
| No | 11 (68.8) | 25 (59.5) | |
| Yes | 5 (31.2) | 17 (40.5) | |
| Deep Infection | 0.48 | ||
| No | 15 (93.8) | 41 (97.6) | |
| Yes | 1 (6.25) | 1 (2.38) | |
| Wound dehiscence | >0.99 | ||
| No | 16 (100.0) | 41 (97.6) | |
| Yes | 0 (0.00) | 1 (2.38) | |
| New or progressive neuro deficit | 0.33 | ||
| No | 13 (81.2) | 39 (92.9) | |
| Yes | 3 (18.8) | 3 (7.14) | |
| Postop hematoma requiring drainage? | 0.28 | ||
| No | 15 (93.8) | 42 (100.0) | |
| Yes | 1 (6.25) | 0 (0.00) | |
| Reoperation | >0.99 | ||
| No | 14 (87.5) | 33 (82.5) | |
| Yes | 2 (12.5) | 7 (17.5) | |
| Reop for infection | >0.99 | ||
| No | 15 (93.8) | 41 (95.3) | |
| Yes | 1 (6.25) | 2 (4.65) | |
| Respiratory event | >0.99 | ||
| No | 16 (100.0) | 43 (100.0) | |
| Yes | 0 (0.0) | 0 (0.0) | |
| Cardiac event | 0.18 | ||
| No | 14 (87.5) | 42 (97.7) | |
| Yes | 2 (12.5) | 1 (2.33) | |
| DVT/PE | >0.99 | ||
| No | 16 (100.0) | 43 (100.0) | |
| Yes | 0 (0.0) | 0 (0.0) | |
| Mortality (1 year) | 0.001** | ||
| No | 11 (68.8) | 43 (100.0) | |
| Yes | 5 (31.2) | 0 (0.00) | |
| Screw failure/loosening | 0.01* | ||
| No | 7 (46.7) | 36 (83.7) | |
| Yes | 8 (53.3) | 7 (16.3) | |
| Unilateral or bilateral screw failure/loosening | 0.002** | ||
| No | 7 (46.7) | 36 (83.7) | |
| Unilateral | 0 (0.00) | 3 (6.98) | |
| Bilateral | 8 (53.3) | 4 (9.30) | |
Data are presented as number (%). *, P<0.05; **, P<0.01. DVT/PE, deep vein thrombosis/pulmonary embolism.
Patients in the case and control groups did not differ in clinical outcomes of new falls, infections, wound complications, progressive neurological deficits, surgically relevant hematoma, reoperations. Similarly, cardiac, respiratory, thromboembolic medical complications did not differ between groups. One-year mortality rate in the pseudoarthrosis group was 31.2% compared to 0% in the control group (P=0.001). Pedicle screw loosening occurred more frequently in the pseudoarthrosis cases (53.3% vs. 16.3%, P=0.01).
Discussion
This retrospective case control study compared PD patients who underwent TL fusion with a primary objective of identifying associated risk factors that lead to pseudoarthrosis. Secondarily, we identified additional complications that co-occurred with pseudoarthrosis at exceptional rates. This information has the potential to guide pre-surgical optimization, and post-surgical prognosis of PD patients who undergo TL fusion.
A practical guide to prognosis can be found in the preoperative patient clinical evaluation, as reflected in this study. The patients who were wheelchair bound or had visible tremor or more likely to go on to pseudoarthrosis than those who did not. Tremors indicate unintentional, relentless motion, and this unwanted motion may overcome the ability to form fusion. Furthermore, PD patients have changed paraspinal muscle composition (6), and this, combined with frailty (wheelchair use), may place additional stress on the construct. These two findings present an easily identifiable and repeatable evaluation that can guide prognostic discussions around surgical treatment. This may signify overall poor control of Parkinson’s symptoms. Traditional treatments that imply disease control like the use of a DBS and second line medication (non-carbidopa/levodopa med) did not confer improved fusion, however in person clinical assessment revealed a significant risk. There are many Parkinson’s specific rating scales that monitor more specific PD symptoms. Further exploration of these specific metrics could be a fruitful line of inquiry.
In the same vein, CT evaluation of bone quality (HU at L3) and a patient presentation for fracture, were both associated with higher incidence of pseudoarthrosis after surgery. HU and fracture are possible covariates signifying poor bone biology. These risk factors for failure of fusion should be acknowledged and mitigated as much as possible to ensure optimal patient outcomes. Practically speaking, all the patients who went on to fusion had a HU above 100, while all those who had pseudoarthrosis had HU of less than 115. Additional prognostic information is gleaned about biologic potential for fusion in the opportunistic finding of decreased HU at L3 (115 or below), or presentation for fracture. Further research on this subject may reveal a more concrete threshold link.
One surprising finding is that the use of additional fusion aids such as an interbody device, BMP, and avoidance of junctional end point did not appear to reduce the risk of pseudoarthrosis. While the use of an anterior and posterior approach did. Obviously, correlation does not equal causation, however the patient’s protoplasm and disease control may carry an outside risk of pseudoarthrosis compared to the surgical techniques we have for mitigation. The presence of an anterior and posterior approach was more associated with fusion. Anterior lumbar interbody fusion confers the best opportunity for disc preparation and fusion surface maximization of the available interbody techniques. This may be why the patients who received a combined approach fared better than those using a singular approach, even if the rate of interbody use did not differ between groups.
The reoperation percentage for this investigation was 15% and was decreased compared to existing retrospective analysis of PD patients of 36–86% (10,13-18). The 22% rate of significant perioperative complications, while less than some, falls within literature data of 11–77% (10,13-18). This does also concur with the latest metanalysis demonstrating an increased risk of complications and revisions for hardware and pseudoarthrosis vs. non-PD-patients who are revised more often for infection and adjacent segment degeneration (17,18) While there is not an overt difference in our patient population, the study’s case control nature lends itself to a less direct comparison to the other data in the literature. Suffice it to say, this study adds to the argument that PD itself conveys a significant risk of reoperation and major complications. What this study found that others have not is an exceptionally high rate of 1-year mortality among PD patients who encountered pseudoarthrosis after surgery. The linkages between these two entities are likely multifactorial, relating to patient frailty and disease progression; however, the ongoing development of pseudoarthrosis should prompt increased observation and multidisciplinary investigation.
Limitations
As with many PD and spinal surgery investigations, this investigation also suffers from small sample size, which increases the risk for type 2 errors. Furthermore, the study design, as a retrospective case control investigation, allows only for commentary on associations, while much needed prospective work could provide a more powerful argument. Additionally, there may exist a selection bias because our inclusion criteria necessitated evaluation of fusion. Not all patients have CT scans in the postsurgical timeframe, and thus there may be additional factors that are unrecognized in this investigation. This investigation was performed at a quaternary care facility with significant resources. This limits the generalizability of the findings.
Conclusions
This study contributes additional information to the growing body of literature surrounding PD and spinal surgery. It confirms that PD presents a clinical and surgical conundrum in the setting of proper indications for surgery. Very practically, when a patient presents with a clinically visible tremor or is debilitated enough to need the use of a wheelchair, these patients are at an increased risk of the formation of pseudarthrosis when fusion is attempted. Patients with low bone quality or who present with fractures are at an additional risk for failure of fusion. The clinician should take caution and maximize all efforts for fusion, while counseling patients accordingly. Parkinson’s disease is a challenging surgical situation. The high rate of medical complications and failure necessitates trepidation around surgical management. The findings of this study further reinforce the need for a greater understanding of PD progression and its association with bone health, fusion potential, and perioperative risks.
Supplementary
The article’s supplementary files as
Acknowledgments
We acknowledge the important efforts of Cassandra Willson, in the completion of this project.
Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by institutional ethics committee of The Mayo Clinic Office for Human Research Protection (FWA00005001) and individual consent for this retrospective analysis was waived.
Footnotes
Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jss.amegroups.com/article/view/10.21037/jss-25-73/rc
Funding: None.
Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jss.amegroups.com/article/view/10.21037/jss-25-73/coif). B.F. serves as a paid consultant for Medtronic, Amgen, Kuros Biosciences, and DePuy Synthes Products LLC; receives research support from Medtronic; holds stock options in Clear Choice Therapeutics and Neuroinnovations; and receives meeting support and serves as a paid presenter for AO Spine. A.S. serves as a paid consultant for Cerapedics, DePuy (A Johnson & Johnson Company), Kyocera, and Osteocentric; is a paid presenter/speaker for Cerapedics; receives research support from DePuy; and receives IP royalties from Jaypee Publishers. A.N. is a paid consultant of Allosource and receives research support from AO Spine North America, 3 Spine and Premia Spine. The other authors have no conflicts of interest to declare.
Data Sharing Statement
Available at https://jss.amegroups.com/article/view/10.21037/jss-25-73/dss
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