Perioperative Retinal Artery Occlusion: Incidence and Risk Factors in Spinal Fusion Surgery From the US National Inpatient Sample 1998-2013

Retinal artery occlusion (RAO) is a rare but devastating complication of spinal fusion surgery. We aimed to determine its incidence and associated risk factors. Hospitalizations involving spinal fusion surgery were identified by searching the National Inpatient Sample, a database of hospital discharges, from 1998 to 2013. RAO cases were identified using ICD-9-CM codes. Using the STROBE guidelines, postulated risk factors were chosen based on literature review and identified using ICD-9-CM codes. Multivariate logistic models with RAO as outcome, and risk factors, race, age, admission, and surgery type evaluated associations. Of an estimated 4,784,275 spine fusions in the United States from 1998 to 2013, there were 363 (CI: 291-460) instances of RAO (0.76/10,000 spine fusions, CI: 0.61-0.96). Incidence ranged from 0.35/10,000 (CI: 0.11-1.73) in 2001-2002 to 1.29 (CI: 0.85-2.08) in 2012-2013, with no significant trend over time (P = 0.39). Most strongly associated with RAO were stroke, unidentified type (odds ratio, OR: 14.33, CI: 4.54-45.28, P < 0.001), diabetic retinopathy (DR) (OR: 7.00, CI: 1.18-41.66, P = 0.032), carotid stenosis (OR: 4.94, CI: 1.22-19.94, P = 0.025), aging (OR for age 71-80 years vs 41-50 years referent: 4.07, CI: 1.69-10.84, P = 0.002), and hyperlipidemia (OR: 2.96, CI: 1.85-4.73, P < 0.001). There was an association between RAO and transforaminal lumbar interbody fusion (OR: 2.95, CI: 1.29-6.75, P = 0.010). RAO was more likely to occur with spinal surgery performed urgently or emergently compared with being done electively (OR: 0.40, CI: 0.23-0.68, P < 0.001).; Patient-specific associations with RAO in spinal fusion include aging, carotid stenosis, DR, hyperlipidemia, stroke, and specific types of surgery. DR may serve as an observable biomarker of heightened risk of RAO in patients undergoing spine fusion.

Original Contribution Perioperative Retinal Artery Occlusion: Incidence and Risk Factors in Spinal Fusion Surgery From the US National Inpatient Sample 1998-2013 Tyler Calway, BS, Daniel S. Rubin, MD, Heather E. Moss, MD, PhD, Charlotte E. Joslin, OD, PhD, Ankit I. Mehta, MD, Steven Roth, MD Background: Retinal artery occlusion (RAO) is a rare but devastating complication of spinal fusion surgery. We aimed to determine its incidence and associated risk factors. Methods: Hospitalizations involving spinal fusion surgery were identified by searching the National Inpatient Sample, a database of hospital discharges, from 1998 to 2013. RAO cases were identified using ICD-9-CM codes. Using the STROBE guidelines, postulated risk factors were chosen based on literature review and identified using ICD-9-CM codes. Multivariate logistic models with RAO as outcome, Rosalind Franklin University Medical School (TC), North Chicago, Illinois; Department of Anesthesia and Critical Care (DSR), the University of Chicago Medicine, Chicago, Illinois; Departments of Ophthalmology and Visual Science (HEM, SR), Neurology and Rehabilitation (HEM), Neurosurgery (AIM), and Anesthesiology (SR), College of Medicine, University of Illinois at Chicago, Chicago, Illinois; Dr. Moss is now with Department of Ophthalmology, Stanford University, Palo Alto, California; Department of Ophthalmology and Visual Science (CEJ), College of Medicine, and School of Epidemiology and Public Health, University of Illinois at Chicago, Chicago, Illinois; and Department of Anesthesia and Critical Care (SR), University of Chicago, Chicago, Illinois. Supported by National Institutes of Health (Bethesda, MD) grants RO1 EY10343 to S. Roth, UL1 RR024999 to the University of Chicago Institute for Translational Medicine, K23 EY024345 to H. E. Moss, UL1 TR000050 to the University of Illinois at Chicago Center for Clinical and Translational Sciences, Core Grant P30 EY001792 to the Department of Ophthalmology of the University of Illinois, a Summer Medical Student Research Grant from The Foundation for Anesthesia Education and Research (Schaumburg, IL) to T. Calway, and an Unrestricted Grant from Research to Prevent Blindness (New York, NY) to the University of Illinois Department of Ophthalmology & Visual Sciences. The funding organizations had no role in the design or conduct of this research. S. Roth has served as an expert witness in cases of perioperative eye injuries on behalf of patients, physicians, and hospitals. The remaining authors report no conflicts of interest. Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the full text and PDF versions of this article on the journal's Web site (www. jneuro-ophthalmology.com). Address correspondence to Steven Roth, MD, Department of Anesthesiology, University of Illinois Medical Center, 1740 West Taylor Street, MC 515, Chicago, IL 60612; E-mail: [e-mail] 36 and risk factors, race, age, admission, and surgery type evaluated associations. Results: Of an estimated 4,784,275 spine fusions in the United States from 1998 to 2013, there were 363 (CI: 291- 460) instances of RAO (0.76/10,000 spine fusions, CI: 0.61-0.96). Incidence ranged from 0.35/10,000 (CI: 0.11-1.73) in 2001-2002 to 1.29 (CI: 0.85-2.08) in 2012-2013, with no significant trend over time (P = 0.39). Most strongly associated with RAO were stroke, unidentified type (odds ratio, OR: 14.33, CI: 4.54-45.28, P , 0.001), diabetic retinopathy (DR) (OR: 7.00, CI: 1.18- 41.66, P = 0.032), carotid stenosis (OR: 4.94, CI: 1.22- 19.94, P = 0.025), aging (OR for age 71-80 years vs 41-50 years referent: 4.07, CI: 1.69-10.84, P = 0.002), and hyperlipidemia (OR: 2.96, CI: 1.85-4.73, P , 0.001). There was an association between RAO and transforaminal lumbar interbody fusion (OR: 2.95, CI: 1.29-6.75, P = 0.010). RAO was more likely to occur with spinal surgery performed urgently or emergently compared with being done electively (OR: 0.40, CI: 0.23-0.68, P , 0.001). Conclusions: Patient-specific associations with RAO in spinal fusion include aging, carotid stenosis, DR, hyperlipidemia, stroke, and specific types of surgery. DR may serve as an observable biomarker of heightened risk of RAO in patients undergoing spine fusion. Journal of Neuro-Ophthalmology 2018;38:36-41 doi: 10.1097/WNO.0000000000000544 © 2017 by North American Neuro-Ophthalmology Society P erioperative visual loss (POVL) is a rare but devastating complication that occurs most commonly after spinal fusion or cardiac surgery (1). The 3 primary causes of POVL are ischemic optic neuropathy (ION), cortical blindness, and retinal artery occlusion (RAO) (2). Although perioperative ION is classically associated with spinal fusion surgery and perioperative RAO with cardiac surgery presumably related to embolism, a minority of those with POVL have RAO with spinal fusion surgery. Better understanding of these less common events remains significant since US spi- Calway et al: J Neuro-Ophthalmol 2018; 38: 36-41 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution nal fusion volume in the United States is the highest in the world (3). The impact of RAO on a patient's life is considerable, with disability from what is often irreversible visual loss (4). Proposed mechanisms for RAO in spine fusion surgery are embolic and compressive. Both have been described almost exclusively in case reports. Nonperioperative RAO is associated with stroke, coronary artery disease, atrial fibrillation, and carotid stenosis and is most commonly embolic (5). Possible embolization has been reported with a patent foramen ovale in an adolescent who underwent spinal fusion for scoliosis (6). Associations also have been described between RAO or stroke and hypercoagulable states (7), relevant to patients undergoing spine surgery for cancer metastasis (8,9). RAO associated with cardiac surgery also is thought to be embolic and is associated with valvular heart surgery, giant cell arteritis, carotid stenosis, hypercoagulable state, ophthalmic diabetic complications, and male sex. By contrast, acute coronary syndrome, atrial fibrillation, congestive heart failure, diabetes without ophthalmic complications, and smoking were associated with an odds ratio (OR) of less than 1 (2). A unique postulated cause of RAO in spine surgery is eye compression related to prone positioning, evident when signs and symptoms such as eye pain, ophthalmoplegia, and bruising are present (10). In a study of visual loss in spine surgery from the American Society of Anesthesiologists Postoperative Visual Loss Registry, of 10 patients with RAO only 3 had no reported signs of eye compression (11). Compression of the eye has been reported from apparently poorly or improperly fitted headrests (12). Another potential source of compressive injury associated with RAO is pressure from a retractor on the carotid artery during cervical spine fusion, leading to decreased flow through the carotid artery (13,14). Because most of the data pertaining to RAO and spinal fusion surgery is primarily based on relatively small numbers of patients, we undertook a more rigorous study of the etiology and risk factors of RAO in spinal fusion surgery (15-18). We hypothesized that perioperative RAO with spinal fusion surgery is associated with risk factors for spontaneous RAO, with spine operations for cancer, and in instances where the head is more likely to move and the eyes could be compressed during surgery (cervical spine operations). To test our hypotheses, we examined hospital discharges in the National Inpatient Sample (NIS) for posterior spinal fusion surgery evaluating the incidence for associations with RAO. METHODS NIS, maintained by the Healthcare Cost and Utilization Project (HCUP) of the Agency for Healthcare Research and Quality (AHRQ), is an approximately 20% stratified sample of US inpatient discharges. Demographics, diagnoCalway et al: J Neuro-Ophthalmol 2018; 38: 36-41 ses (principal and secondary), procedures (principal and secondary), charges (dollars), length of stay (days), discharge status, outcomes, and medical diagnoses are included. Diagnoses and procedures are coded using the International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM). Because there are no specific patient identifiers, the Institutional Review Boards of the University of Chicago and the University of Illinois deemed this study "exempt." Data Classification Discharges with posterior cervical, thoracic, lumbar, or sacral spine fusion surgery in the NIS from 1998 to 2013 have formed the basis of other reports (19,20). Operations with anterior approach to the spine were excluded, and the number of vertebrae fused was included as a proxy for intraoperative time or procedure complexity (See Supplemental Digital Content 1, Table 1, http://links.lww.com/WNO/A240). ICD-9CM codes were compared against Current Procedural Technology spinal fusion codes using EncoderPro.com (Optum, Salt Lake City, UT). Patients discharged with a primary or secondary diagnostic ICD-9-CM code for RAO (362.30-362.34) and a relevant spine procedure were considered to have developed RAO during the hospitalization. Missing Data and Sources of Bias To account for missing data for race and admission type in the multivariate analysis, we performed multiple (10) imputations by chained equations (21) with race, sex, admission type, and age in the imputation model. The most important potential source of data bias is the possibility of misclassification from erroneous or absent coding of procedures and diagnoses. Patient Characteristics Patient characteristics included age (years divided into 10year periods, categorical variable), sex, length of hospital stay (days), yearly inflation-adjusted total hospital charges (both as continuous variables), type of admission (elective vs nonelective), discharge status (routine, short-term hospital, home health care, died, other), and race. Surgical factors included the medical diagnosis prompting surgery, divided into degenerative disc disease, scoliosis, or cancer of the spine. The number of levels operated on was determined from ICD-9-CM codes. Hospital conditions included anemia, transfusion, and postoperative bleeding. Potential risk factors for RAO were identified before analysis based on previous case series, large database reviews, and case reports as recommended in the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement (22). Medical diagnoses (See Supplemental Digital Content 2, Table 2, http://links.lww.com/WNO/A241) were atrial 37 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution fibrillation, coronary artery disease (23), carotid artery stenosis (23,24), stroke, diabetes mellitus (Type 1 and 2) without complications (25), diabetes with complications (ophthalmic, renal, or neurological) (26), hypertension (24), hypertension with cardiac complications (27), obesity (24), peripheral vascular disease, smoking (28), congestive heart failure, atrial fibrillation (23), giant cell arteritis (29), thrombocytopenia, and hypercoagulable state (including primary and secondary hypercoagulable states, homocystinuria, and presence of antiphospholipid antibodies) (30-32). Stroke was classified as embolic, thrombotic, transient ischemia, unspecified, or iatrogenic (33). Analysis We used the AHRQ "trend weights" (hcupnet.ahrq.gov) to ensure accurate weighting (34), as previously described (20) with the "Survey" function in Stata (Stata Corp, College Station, TX). To calculate the incidence of RAO in spine fusion surgery, the 16 years of data were divided into 2-year periods (1998-1999, 2000-2001, 2002-2003, 2004-2005, 2006-2007, 2008-2009, 2010-2011, and 2012-2013). This enabled the numerator (cases per time period) to reach the threshold for reporting (.10), while the denominator was the number of procedures per time period. (AHRQ does not allow reporting of any result ,10). Patient characteristics, surgical factors, and RAO as a primary or secondary diagnosis from 1998 to 2013 were tabulated using national estimates. Multivariate logistic regressions were conducted with RAO as the dependent variable and postulated risk factors (patient characteristics excluding length of stay, total charges, discharge status; surgical factors; medical diagnoses) as independent variables as described previously (20). Because RAO is a rare outcome, the study design maximized analysis power by comparing affected to unaffected patients. There was no attempt to exclude any unaffected (control) cases (20). Results are reported as ORs with 95% confidence intervals (CI). P , 0.05 was considered significant for associations. Stata v14.0MP (College Station, TX) was used for statistical analyses. A post hoc power analysis for logistic regression was performed using G-power 3.1 (http://gpower.hhu.de/). Because RAO is rare, analysis was adjusted using Hseih formula (35). RESULTS There were estimated 4,828,126 spine fusions in the United States from 1998 to 2013, with 363 (CI: 291-460) instances of RAO, an overall incidence of 0.76/10,000 spine fusions (CI: 0.61-0.96). Incidence (Fig. 1) ranged from 0.35/10,000 (CI: 0.11-1.73) in 2001-2002 to 1.29 (CI: 0.85-2.08) in 2012-2013, with no significant trend for change over time (P = 0.39). A post hoc logistic regression power analysis was performed with total sample size 4.8 million, adjusted for rare outcome. For detecting associations with a low prevalence (e.g., 1%), the database was adequately powered (a = 0.05, power = 80%) to detect an OR as low as 1.6. With more prevalent parameters (e.g., 40%), an OR as low as 1.2 could be robustly detected (a = 0.05, power = 80%). FIG. 1. Incidence of retinal artery occlusion (RAO) among patients undergoing spinal fusion in the national inpatient sample. 38 Calway et al: J Neuro-Ophthalmol 2018; 38: 36-41 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution Supplemental Digital Content 1 (see Table 1, http:// links.lww.com/WNO/A240) shows the patients' characteristics, surgical factors, and medical diagnoses. Age was missing in ,0.1% and #2.8% (nonaffected and RAO, respectively), race in 18.9% and 20.3%, and discharge status was missing or "other" in 39.4% and 13.6% of discharges. Those who sustained RAO had higher total hospital costs ($136,648, CI: $110,130-$163,166) than the unaffected ($78,726, CI: 76,456-80,997). Nonelective admission occurred in 28.3% and in 12.9% in RAO and unaffected cases, respectively. Discharge was "routine" in 41.1% of RAO cases and in 75.6% non-RAO. The clinical conditions most strongly associated with RAO in a multivariate model (See Supplemental Digital Content 2, Table 2, http://links.lww.com/WNO/A241) were stroke other than embolic or thrombotic, that is, "unspecified" (OR: 14.33, CI: 4.54-45.28, P , 0.001), diabetes with ophthalmic complications (OR: 7.00, CI: 1.18-41.66, P = 0.032), carotid stenosis (OR: 4.94, CI: 1.22-19.94, P = 0.025), and hyperlipidemia (OR: 2.96, CI: 1.85-4.73, P , 0.001). Age .71 years was associated with RAO (OR: 4.07, CI: 1.69-10.84, P = 0.002), sex had no impact, and neither did the number of levels operated on, nor cancer of the spine. The level of the spine procedure (cervical, thoracic, lumbar, and sacral) was not associated with RAO, but there was an association with transforaminal lumbar interbody fusion (TLIF, OR: 2.95, CI: 1.29-6.75, P = 0.010). Having surgery electively was inversely associated with RAO (OR: 0.40, CI: 0.23-0.68, P , 0.001), that is, patients undergoing electively scheduled surgery had a significantly lower OR of developing RAO compared with those scheduled urgently or emergently. DISCUSSION We identified an overall RAO incidence of 0.76/10,000 for posterior spinal fusion surgeries, with no significant change during the 16-year study period. RAO was associated with age .71 years, diabetic retinopathy (DR), carotid stenosis, "unspecified" stroke, and hyperlipidemia. Associated surgical factors were nonelective surgery and TLIF. Some factors identified in this study were similar to those associated with spontaneous RAO, and with RAO in cardiac surgery. Carotid stenosis overlapped with associations found with spontaneous RAO, and with RAO in cardiac surgery. As in spontaneous RAO, we found an association with stroke and RAO in spinal fusion. We did not identify any associations between RAO in spinal fusion and other factors reported in association with spontaneous RAO and/or RAO in cardiac surgery including sex, giant cell arteritis, hypercoagulable state, atrial fibrillation, and coronary artery disease. Carotid stenosis has been reported in association with spontaneous and cardiac surgery-related RAO (24), and this study adds spinal fusion-associated RAO to the list. A Calway et al: J Neuro-Ophthalmol 2018; 38: 36-41 potential mechanism is that carotid stenosis predisposes to RAO because of an increased risk of hypoperfusion of the ophthalmic artery. Systemic hemodynamic factors may contribute to RAO among patients with carotid stenosis by exacerbating locally impaired perfusion (25). Carotid stenosis could predispose to an embolic event causing RAO by plaque dislodging from the carotid artery. It is not known if head positioning during surgery contributes. This common association suggests some shared pathophysiology between spontaneous, cardiac surgery-associated, and spinal surgeryassociated RAO. We demonstrated the association between RAO in spinal fusion surgery and one systemic vascular risk factor, hyperlipidemia. While DM has been cited as a risk factor for spontaneous RAO (25), we did not find uncomplicated DM, or DM with complications, other than DR, to be associated with RAO in spinal fusion surgery. Other vascular risk factors including hypertension and smoking also lacked significant associations. Therefore, RAO in spinal fusion surgery does not seem related to systemic vascular disease. The association between DR and RAO in spinal fusion surgery is new and builds on our report of association between DR and RAO in cardiac surgery (2). DR is characterized by loss of retinal capillary pericytes, increased retinal vascular permeability, neovascularization secondary to chronic hypoxia, and eventually degeneration of retinal neurons (36). The increased risk of RAO in patients with DR may be due to susceptibility of the retinal vasculature (37,38) to systemic alterations during complex spine surgery, including blood loss, hypotension, and systemic inflammation (39). However, this remains conjectural and further studies are required. Caution should be exercised in interpreting our results because there were #10 RAO subjects with DR, and the degree of DR was not assessable. Because the NIS does not include surgical time, we used the number of levels operated on as a proxy for surgical time. We found that there was no relationship to development of RAO, suggesting that the amount of time to perform the procedure was not a factor, unlike our previous findings for perioperative ION in spine fusion (11). Also, contrary to our theory, surgical site, that is, cervical, thoracic, lumbar, or sacral, was not related to RAO. However, the TLIF procedure was associated with RAO. This procedure necessitates a more difficult surgical approach (40), but we cannot conclude from the study why it was associated with RAO. The elderly patient undergoing spine fusion was more susceptible to RAO. These patients tend to undergo more complex spine surgery because of more advanced disease (41), but no further conclusions about the association with RAO can be made from our data. This result agrees with our previous study on ION in spinal fusion, which found that aging, male sex, transfusion, and obesity significantly increased the risk of ION. However, 39 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution aging was the only risk factor that was the same among the studies. There are limitations to our study. It is likely that many, if not all, patients who developed RAO underwent a detailed neurological and ophthalmologic examination leading to increased documentation of ophthalmic diagnoses such as DR. Furthermore, the presence of visual loss, particularly if unilateral, might prompt testing for carotid artery stenosis. Thus, the associations of diabetic eye complications and carotid stenosis with RAO in our study may partly reflect heightened suspicion by the clinician of carotid stenosis. We cannot determine whether stroke diagnoses were used to represent RAO as a stroke to the eye or concurrent intracranial stroke. We also could not determine the treatment status of any given diagnosis. For example, those patients with atrial fibrillation may have received appropriate treatment, which may have lowered their likelihood of developing RAO. The NIS, an administrative database of discharge records, is susceptible to undocumented diagnoses, overor under-diagnosis, and coding errors. The severity of visual loss and unilateral or bilateral involvement cannot be determined. Longitudinal follow-up for progression or improvement after discharge was not possible. Similarly, we could not determine with certainty if a diagnosis was pre-existent or developed during the hospitalization. The incidence of RAO in the general population is far less than our results, approximately 1/100,000 (42), suggesting that our findings reflect a diagnosis that was made perioperatively. Our study is limited to identification of factors associated with RAO during hospitalization for surgery and cannot conclusively address causation or independent risk factors, although the present results suggest new areas for research into the mechanisms of perioperative RAO. We also are unable to assess the impact of important recent trends in spine surgery, including minimally invasive spine surgery (43) which was without a specific ICD-9-CM procedure code until 2014. In conclusion, DR, stroke, and carotid stenosis are associated with RAO in patients undergoing spine fusion surgery. Other associations include age greater than 71 years, hyperlipidemia, and the TLIF procedure. Additional studies in the perioperative environment could afford a unique window into the natural history of RAO and give greater insight into potential mechanisms and treatment options. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: S. Roth, T. Calway, D. S. Rubin, C. E. Joslin, A. I. Mehta, and H. E. Moss; b. Acquisition of data: S. Roth, T. Calway, and D. S. Rubin; c. Analysis and interpretation of data: S. Roth, T. Calway, D. S. Rubin, C. E. Joslin, A. I. Mehta, and H. E. Moss. Category 2: a. Drafting the manuscript: S. Roth, T. Calway, D. S. Rubin, C. E. Joslin, A. I. Mehta, and H. E. Moss; b. Revising it for intellectual content: S. Roth, T. Calway, D. S. Rubin, C. E. Joslin, A. I. Mehta, and H. E. Moss. Category 3: a. 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