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1 Research Article Prolonged Preoperative Weakness Affects Recovery of Motor Function After Anterior Cervical Diskectomy and Fusion Tyler Kreitz, MD Ronald Huang, MD David Beck, MD Andrew G. Park, MD Alan Hilibrand, MD From the Department of Orthopaedic Surgery, Thomas Jefferson University Hospitals, Philadelphia, PA (Dr. Kreitz, Dr. Huang, Dr. Beck, and Dr. Park), and the Rothman Institute, Thomas Jefferson University Hospitals, Philadelphia (Dr. Hilibrand). Correspondence to Dr. Kreitz: tyler.m. Dr. Hilibrand or an immediate family member has received royalties from Aesculap/B.Braun, Amedica, and Zimmer Biomet; has stock or stock options held in Amedica, Benvenue Medical, Life Spine, NexGen Medical Systems, Paradigm Spine, Spinal Ventures, and Vertiflex; and serves as a board member, owner, officer, or committee member of the American Academy of Orthopaedic Surgeons, the Cervical Spine Research Society, and the North American Spine Society. None of the following authors or any immediate family member has received anything of value from or has stock or stock options held in a commercial company or institution related directly or indirectly to the subject of this article: Dr. Kreitz, Dr. Huang, Dr. Beck, and Dr. Park. J Am Acad Orthop Surg 2018;26: DOI: /JAAOS-D Copyright 2017 by the American Academy of Orthopaedic Surgeons. Abstract Introduction: Some patients who undergo anterior cervical diskectomy and fusion for radiculopathy or myelopathy demonstrate preoperative weakness. The purpose of this study was to determine which factors predict motor recovery in patients undergoing anterior cervical diskectomy and fusion. Methods: A retrospective review of our institutional database identified patients undergoing anterior cervical diskectomy and fusion between 2010 and 2013 with 2 years of clinical follow-up. Patients with substantial weakness, defined as preoperative grade #3 (on a scale from 0 to 5) in one or more upper extremity muscle groups, were identified. Regression analysis was used to determine risk factors associated with persistent postoperative weakness. Results: Of the 1,001 patients who were included, 54 (5.4%) demonstrated substantial weakness. By 2 years postoperatively, 47 of 54 patients (87%) demonstrated motor recovery. The duration of preoperative weakness was an independent predictor of recovery (median, 4 months of preoperative weakness among patients with recovery versus 10 months in patients with persistent weakness; P = 0.012). Discussion: Duration of preoperative motor weakness is an independent predictor of motor recovery after anterior cervical diskectomy and fusion in patients with substantial motor weakness. Conclusion: Patients being considered for anterior cervical diskectomy and fusion who have substantial preoperative motor deficits may benefit from earlier surgical intervention. After unsuccessful nonsurgical management, anterior cervical diskectomy and fusion (ACDF) may be considered for surgical management of radicular and myelopathic symptoms associated with disk herniation and spondylotic anterior compression of the cervical spine. 1-5 In appropriately selected patients, ACDF demonstrates reliable improvement in radicular symptoms, 6,7 myelopathy, 8,9 and function. 7 Often, patients with cervical radiculopathy and myelopathy have concomitant motor and sensory dysfunction. Recovery of sensory and motor symptoms has been demonstrated in up to 90% of patients who underwent ACDF for radiculopathy However, previous studies have been limited by the lack of a strict definition of motor and sensory dysfunction January 15, 2018, Vol 26, No 2 67

2 Prolonged Preoperative Weakness After Anterior Cervical Diskectomy and Fusion and the heterogeneity of symptoms evaluated. Although ACDF has been shown to effectively relieve radicular symptoms and neurologic dysfunction, the factors that influence recovery of motor function after ACDF have not been clearly identified. A prospective analysis by Peolsson and Peolsson 3 demonstrated that lower preoperative disability, pain intensity, and male sex were predictors of short- and long-term improvement of health-related quality of life indexes after ACDF. The duration of motor dysfunction, the severity of symptoms, and early surgical intervention 17 have been suggested as predictors of motor recovery in patients undergoing lumbar spine surgery for stenosis with concomitant motor deficits. To our knowledge, no studies have investigated factors that may predict motor recovery after ACDF for radiculopathy or myelopathy in patients with associated motor dysfunction. Furthermore, the natural history of weakness in patients with degenerative cervical spine disease is unclear. The purpose of our study was to determine the incidence of substantial weakness in patients undergoing ACDF for cervical radiculopathy or myelopathy at our institution and identify factors that significantly affect the postoperative recovery of motor function in this population. We hypothesized that patients with greater duration of preoperative weakness may demonstrate prolonged postoperative recovery of motor function after ACDF. Methods Institutional Review Board approval was obtained for this retrospective study. We identified 1,299 patients who underwent one-, two-, three-, or four-level ACDF by all orthopaedic spine surgeons at our institution between January 1, 2010, and December 31, Only patients with available preoperative and postoperative clinical examination data were included. Patients who underwent surgery for the management of trauma, tumor, infection, or congenital malformation; revision index-level or adjacent-level procedures; concomitant corpectomy; or arthroplasty were excluded. Demographic information and preoperative physical examination findings, including symptoms of myelopathy, sensory changes, and motor strength measured by manual muscle testing (MMT), 19 were obtained for all included patients. Motor strength grading by MMT was documented for arm abduction, elbow flexion, elbow extension, wrist extension, wrist flexion, finger abduction, and finger flexion. Surgical reports and follow-up data, including postoperative MMT strength, were obtained for each patient at 2 weeks, 6 weeks, 3 months, 6 months, 1 year, and 2 years postoperatively when available from our institution s electronic medical record system. Subgroup Analysis A total of 1,001 patients met inclusion criteria and were available for analysis. Patients with substantial weakness, defined as preoperative strength of grade #3 (on a scale from 0 to 5) in at least one upper extremity muscle group by MMT, were identified. Time from the onset of motor symptoms to surgery was determined from preoperative office notes. All patients who were included had undergone preoperative cervical spine MRI. Some patients also underwent electromyography confirming cervical pathology as the cause of their symptoms. Postoperative recovery of motor function in patients with weakness was defined as improvement of one grade of strength in at least two muscle groups or improvement of two grades of strength in one muscle group by MMT. The orthopaedic spine surgeon who performed the surgery also performed the preoperative and postoperative MMT in all patients. Patients with persistent postoperative weakness underwent extensive physical therapy. Patients with persistent postoperative deltoid weakness were evaluated by a shoulder specialist for additional pathology. Statistical Analysis Statistical analyses were performed with SPSS version 22 (IBM). Backward stepwise logistic regression analysis was used to identify risk factors associated with a lack a recovery of motor function in patients with substantial preoperative weakness, as defined previously. Additionally, chi-square and Student t-tests were used to compare the demographic information, including age, sex, body mass index (BMI), comorbidities, and functional scores, of patients who had recovery of motor function with that of patients who did not. Results Of 1,001 patients included in this study, 471 underwent two-level ACDF, 284 underwent one-level ACDF, 230 underwent three-level ACDF, 16 underwent four-level ACDF. In this study, patients who underwent ACDF had a mean age of 51.7 years (range, 18 to 86 years) and a mean BMI of 29.2 kg/m 2 (range, 13.5 to 55.0 kg/m 2 ); 516 (51.5%) were men. A total of 447 patients (44.7%) had concomitant preoperative sensory deficit, and 316 patients (31.6%) had symptoms of myelopathy during preoperative examination (Table 1). The 68 Journal of the American Academy of Orthopaedic Surgeons

3 Tyler Kreitz, MD, et al Table 1 Demographic Information, Presence of Preoperative Sensory Deficits, and Presence of Symptoms of Myelopathy for All Patients in the Study (N = 1,001) Variable Patient Data a Age (years) 51.7 (18 86) Body mass index (kg/m 2 ) 29.2 ( ) Sex Male 516 (51.5%) Female 485 (48.6%) Sensory deficits 447 (44.7%) Myelopathy 316 (31.6%) a Data are given as mean (range) or number (percentage). incidence of substantial preoperative weakness was 5.4%. In patients with substantial preoperative weakness (n = 54), the mean age was 54.2 years (range, 30 to 82 years) and the mean BMI was 28.4 kg/m 2 (range, 19.7 to 37.9 kg/m 2 ). Of these 54 patients, 30 (55.6%) had sensory symptoms along with pain and 21 (38.9%) had signs of cervical myelopathy (Table 2). By 2 years postoperatively, 47 of 54 patients (87.0%) with weakness had recovery of their motor function; 7 (13.0%) had persistent weakness. We found no difference in the mean age (6 SD) of patients with persistent weakness and that of patients with recovery of motor function ( years versus years, respectively; P = 0.196). Average BMI was similar in patients with motor recovery ( kg/m 2 ) and patients with persistent weakness ( kg/m 2 ; P = 0.869). Sex distribution also was not statistically different between groups (P = 0.412). The median duration of preoperative weakness was 10 months (interquartile range [IQR], 8.0 to 17.5 months) in patients with persistent postoperative weakness and 4 months (IQR, 2.3 to 9.0 months) in patients with motor recovery (P = 0.002; Table 2). The presence of preoperative sensory deficits in cervical distributions (P = 0.928) and the presence of cervical myelopathy (P = 0.288) did not predict persistent weakness at 2 years postoperatively (Table 2). Multivariate logistic regression analysis demonstrated that shorter duration of preoperative weakness was an independent predictor of motor function recovery after ACDF (P = 0.008). Of the seven patients who did not demonstrate motor recovery, most had persistent weakness in the fifth and sixth cervical nerve root distributions; five of these had evidence of myelomalacia on preoperative MRI (Figure 1). Six patients demonstrated fusion based on postoperative lateral flexion and extension radiographs. One patient required an additional procedure during the follow-up period for adjacent segment disease (Table 3). All patients with persistent weakness in deltoid testing underwent postoperative evaluation by a shoulder specialist, who did not think that their weakness was related to shoulder pathology in the postoperative period. Discussion Studies have shown that ACDF provides reliable improvement in radicular and myelopathic symptoms associated with disk herniation and spondylotic anterior compression of the cervical spine. 6-8,11 A substantial proportion of patients undergoing ACDF for radiculopathy and myelopathy have some degree of preoperative concomitant motor or sensory dysfunction. 9-11,20 Previous studies have demonstrated reliable relief of radicular and myelopathic symptoms in up to 90% of patients within 1 year postoperatively. 9-11,20 However, persistent motor weakness can be a devastating problem for patients. The natural history of motor weakness and predictors of motor recovery after ACDF in patients with cervical spondylosis is unclear. In the current study, 5.4% of patients undergoing ACDF had substantial preoperative weakness. This percentage is much lower than that reported in previous studies. A retrospective analysis by Lehmann et al 11 reported a 55% incidence of motor deficit among patients undergoing single-level ACDF for the management of radicular symptoms, although the authors defined motor weakness as anything less than full strength (grade 5 on a scale from 0 to 5) in any major upper extremity muscle group. In a retrospective analysis of 122 patients undergoing ACDF for radiculopathy, Bohlman et al 10 demonstrated a 45% incidence of preoperative motor weakness, again defined as any degree of weakness on physical examination. Our study used a higher threshold in the definition of motor weakness to identify patients with substantial limitation, to limit heterogeneity among our analyzed cohort, and to reduce the subjectivity inherent in MMT. 21,22 We found a 44.7% incidence of sensory deficit, lower than the 63% to 66% incidence reported previously in patients undergoing ACDF for radiculopathy. 10,11 Our study included all January 15, 2018, Vol 26, No 2 69

4 Prolonged Preoperative Weakness After Anterior Cervical Diskectomy and Fusion Table 2 Demographic Information, Preoperative Sensory Deficits, Myelopathy, and Duration of Preoperative Weakness Among Patients With Substantial Preoperative Motor Weakness Variable patients undergoing ACDF for radicular and myelopathic symptoms, which likely contributed to the lower overall incidence of sensory deficit compared with that reported in previous studies examining only patients with radicular symptoms. We found motor recovery at 2 years postoperatively in 87% of patients undergoing ACDF with substantial preoperative weakness. This finding is similar to that of previous studies, which demonstrated motor recovery rates.90% within 1 year of surgery among patients with one or more grades of motor weakness. 9,10,11 In the first report of a large series of patients undergoing ACDF for the management of radiculopathy, Bohlman et al 10 demonstrated motor recovery in 96% of patients with preoperative motor deficit at an average final follow-up of 6 years. No patients in the study had a new or worsening deficit described. Patients With Motor Recovery (n = 47) Patient Data a Patients With Persistent Weakness (n = 7) P Value b Age (yr) Body mass index (kg/m 2 ) Sex Male 31 (66%) 6 (85.7%) Female 16 (34%) 1 (14.3%) Sensory deficits Yes 26 (55.3%) 4 (57.1%) No 21 (44.7%) 3 (42.9%) Myelopathy Yes 17 (36.2%) 4 (57.1%) No 30 (63.8%) 3 (42.9%) Duration of preoperative weakness (mo) 4 ( ) 10 ( ) a Data are given as mean 6 SD, number (percentage), or median (interquartile range). b Statistically significant at P, 0.05 More recently, a retrospective review of 118 patients undergoing single-level ACDF for radiculopathy by Lehmann et al 11 demonstrated recovery of motor symptoms by 1 year postoperatively in 95% of patients with any degree of preoperative motor weakness. The authors of the study reported new postoperative motor deficits in 14% of patients, occurring most often at a level adjacent to that of the index procedure. Similarly, Chiles et al 20 reported on the neurologic outcomes of 76 patients undergoing ACDF for myelopathy. They demonstrated motor recovery in up to 91% of patients at a mean follow-up of 8.9 months. In two large prospective trials comparing cervical disk arthroplasty to ACDF, recovery of neurologic symptoms was demonstrated among 88% and 84% of patients at 2 years postoperatively. 23,24 Both of these trials examined only neurologic symptoms and did not differentiate between motor and sensory deficits. In our study, most patients (89.3%) who demonstrated motor recovery did so within 6 weeks of surgery. Adhering to strict criteria for the definition of substantial preoperative motor weakness and recovery, we demonstrated rates of motor recovery similar to those found in previous studies. 7,9-11,23,24 This finding may reassure patients with substantial preoperative motor weakness as defined in this study. These patients appear to demonstrate an incidence of motor recovery after ACDF similar to that of patients with any degree of preoperative motor deficit. Several prospective and retrospective studies have demonstrated a relationship between the duration and severity of preoperative motor deficit and motor recovery after lumbar microdiskectomy and decompression in patients with preoperative deficit. 12,14-17 A prospective evaluation by Postacchini et al 14 and a retrospective analysis by Aono et al 12 demonstrated a correlation between the duration of preoperative motor deficit and recovery of motor function in patients undergoing microdiskectomy for the management of lumbar disk herniation and in patients undergoing decompression for the management of degenerative lumbar disease, respectively. Postacchini et al 14 showed that among 24 patients undergoing microdiskectomy for lumbar disk herniation with severe preoperative weakness, defined as grade 3 (of 5) strength, those with complete postoperative motor recovery had a shorter mean preoperative duration of motor deficit (35 days) compared with that of those with partial recovery (69 days). This finding is consistent with ours, suggesting that those with shorter duration of preoperative weakness are more likely to have motor 70 Journal of the American Academy of Orthopaedic Surgeons

5 Tyler Kreitz, MD, et al Figure 1 Spine radiographs of a 59-year-old man who presented with 8 months of worsening right-side radicular symptoms in the distribution of the 5th and 6th cervical nerves, deltoid and biceps weakness, and symptoms of myelopathy. A, Preoperative lateral radiograph shows a decrease in the disk space height at the C4-5 level with anterior osteophytes and mild listhesis (grade I) at the C5-6 level. B, Midsagittal T2-weighted MRI demonstrates myelomalacia at C4-5 with moderate to severe stenosis and cord compression at the C5-6 level. C, Postoperative lateral radiograph demonstrates expected findings after anterior cervical diskectomy and fusion between the C4-C5 and C5- vertebrae. recovery than those with persistent preoperative weakness are. In our study, those with recovery had a median duration of preoperative weakness of 4 months; those with persistent weakness had a median duration of preoperative weakness of 10 months. Aono et al 12 retrospectively evaluated recovery from motor deficit among 46 patients undergoing lumbar decompression who had preoperative foot drop. Multivariate analysis demonstrated that the duration (P = 0.004) and degree (P = 0.049) of preoperative motor deficit were independent predictors of motor recovery. Lønne et al 16 performed a prospective analysis evaluating motor recovery among 91 patients undergoing lumbar microdiskectomy for radicular symptoms with concomitant motor deficit. Within this cohort, the degree of preoperative motor deficit was the only independent predictor of motor recovery. Duration of preoperative motor deficit was not associated with recovery of symptoms; however, the duration of preoperative deficit in this cohort was short (mean, 30 days). However, several studies have demonstrated no correlation between duration of preoperative motor deficit and motor recovery after lumbar surgery. 15,17,18,25,26 These differences may be explained by varied onset of motor deficit before surgery, heterogeneity of definitions of motor deficit, subjective examination findings, and limitations of patient recall. Furthermore, some studies have demonstrated delayed motor recovery in patients undergoing lumbar surgery with extruded or sequestrated disk herniation. 14,18,25 To the best of our knowledge, our study is the first that evaluates predictors of motor recovery in patients undergoing ACDF for radicular and myelopathic symptoms. Our study has several limitations. First, the study is limited by its retrospective design. Data were retrospectively collected by reviewing notes of physical examinations performed by physicians during perioperative clinic visits. Heterogeneity likely exists among each surgeon s physical examination findings, interpretation, surgical indications, and determination of postoperative fusion. We think that our strict definition of preoperative motor deficit(atleasttwogradesofmotor deficit) reduces the subjectivity associated with MMT. Second, the duration of preoperative symptoms January 15, 2018, Vol 26, No 2 71

6 Prolonged Preoperative Weakness After Anterior Cervical Diskectomy and Fusion Table 3 Demographic Information, Procedure Level, Preoperative Symptoms, Duration of Symptoms, Preoperative Myelomalacia, Fusion, and Secondary Cervical Surgery Among Patients With Preoperative Weakness Who Did Not Demonstrate Postoperative Recovery a Patient Age (yr) Sex Body Mass Index (kg/ m 2 ) Procedure Level Sensory Deficits b Myelopathy b Duration of Symptoms (mo) Myelomalacia b, c Fusion b, d Repeat Surgery b Weak Nerve Root 60 M 26.5 C C5 and 75 M 27.5 C C5 47 M 26.9 C4-C and C7 54 M 29.5 C C5 and 65 M 28.2 C M 31.3 C C5 and 56 F 30.6 C4-C C5 and a Recovery in the postoperative period was determined according to the criteria listed in the Methods section. b A plus sign (1) indicates presence of the column variable. A minus sign (2) indicates absence of the variable. c Myelomalacia was determined by preoperative MRI evaluation. d Fusion was determined on postoperative flexion and extension lateral radiographs evaluated by the surgeon who performed the procedure. documented by the physician is based on objective reports by the patients and is limited by recall bias. Additionally, it was not routine protocol for patients with persistent weakness to obtain postoperative advanced imaging to evaluate for persistent nerve compression unless the patient exhibited a new neurologic deficit. Nonetheless, this study demonstrates a clear difference in duration of preoperative symptoms in patients who had recovery of motor function and those with persistent weakness among a large cohort of patients undergoing ACDF. In our study, the patients with recovery of motor deficit had a substantially shorter duration of preoperative deficit (median, 4 months), compared with that of patients without recovery of function (median, 10 months). This study suggests that patients being considered for ACDF who have substantial preoperative motor deficits may benefit from earlier surgical intervention. Conclusion In this large retrospective study of patients undergoing ACDF who had substantial preoperative motor weakness, we observed a motor recovery rate of 87% at 2 years postoperatively. We found an association between prolonged preoperative motor deficit and absence of motor recovery. Patients demonstrating recovery of motor symptoms at 2 years postoperatively had a median duration of preoperative motor deficit of 4 months, compared with 10 months among patients with persistent weakness at 2 years postoperatively, thus supporting our hypothesized association between duration of weakness and motor recovery. These results suggest that earlier surgical intervention may be beneficial in this patient population when initial nonsurgical treatment does not restore motor function. Additional prospective studies with large cohorts of patients are necessary to accurately identify additional factors that may play a role in recovery of motor function after ACDF in patients with substantial upper extremity weakness. References Evidence-based Medicine: Levels of evidence are described in the table of contents. In this article, references 5, 6, and 17 are level I studies. References 3, 4, 7, 8, 16, and are level II studies. References 2, 9-15, 18, 20, and 26 are level III studies. References 1, 19, 21, and 22 are level IV studies. References printed in bold type are those published within the past 5 years. 1. Bono CM, Ghiselli G, Gilbert TJ, et al; North American Spine Society: An evidence-based clinical guideline for the diagnosis and treatment of cervical radiculopathy from degenerative disorders. Spine J 2011;11(1): Journal of the American Academy of Orthopaedic Surgeons

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