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doi: 10.1097/BRS.0000000000000102
Cervical Spine

Impact of Diabetes on the Outcomes of Cervical Laminoplasty: A Prospective Cohort Study of More Than 500 Patients With Cervical Spondylotic Myelopathy

Machino, Masaaki MD; Yukawa, Yasutsugu MD, PhD; Ito, Keigo MD, PhD; Inoue, Taro MD; Kobayakawa, Akinori MD; Matsumoto, Taro MD; Ouchida, Jun MD; Tomita, Keisuke MD; Kato, Fumihiko MD, PhD

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Author Information

From the Department of Orthopedic Surgery, Chubu Rosai Hospital, Japan Labor Health and Welfare Organization.

Address correspondence and reprint requests to Masaaki Machino, MD, Department of Orthopedic Surgery, Chubu Rosai Hospital, Japan Labor Health and Welfare Organization, 1-10-6 Komei, Minato-ku, Nagoya, Aichi 455-8530, Japan; E-mail: masaaki_machino_5445_2@yahoo.co.jp

Acknowledgment date: July 25, 2013. First revision date: September 27, 2013. Acceptance date: October 19, 2013.

The manuscript submitted does not contain information about medical device(s)/drug(s).

This research was supported by research funds to promote the hospital functions of Japan Labor Health and Welfare Organization.

No relevant financial activities outside the submitted work.

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Abstract

Study Design. A prospective cohort study.

Objective. This study aimed to compare the outcome of cervical laminoplasty between diabetic patients and nondiabetic patients with cervical spondylotic myelopathy.

Summary of Background Data. A few retrospective studies have investigated the outcomes of cervical myelopathy in diabetic patients; therefore, our large-scale cohort study was designed to assess these outcomes in cervical spondylotic myelopathy.

Methods. In total, 505 consecutive patients with cervical spondylotic myelopathy (311 males, 194 females; mean age, 66.6 yr; range, 41–91 yr) who underwent double-door laminoplasty were prospectively enrolled. They were followed up for more than 12 months after surgery (mean follow-up period, 25.6 ± 12.6 mo). The patients were divided on the basis of diabetic criteria for glucose intolerance into 2 groups: the diabetic group (n = 105) and nondiabetic group (n = 400). We evaluated differences in pre- and postoperative Japanese Orthopaedic Association (JOA) scores, recovery rate, achieved JOA scores (postoperative JOA score − preoperative JOA score), and complications between both groups.

Results. The mean JOA scores in the diabetic and nondiabetic groups were 10.1 and 10.8 points before surgery and 13.1 and 13.9 points after surgery, respectively. The diabetic group showed significantly low pre- and postoperative JOA scores and low recovery rate of JOA scores compared with the nondiabetic group (47.3% vs. 53.6%, P < 0.05). However, mean achieved JOA scores in the diabetic and nondiabetic groups were 3.0 and 3.1 points respectively, with no significant difference between both groups (P = 0.343). The groups showed no significant difference in the postoperative complication rate.

Conclusion. Pre- and postoperative JOA scores and recovery rates were lower in the diabetic group than the nondiabetic group. However, the achieved JOA scores were not significantly different between both groups. Diabetic and nondiabetic patients experienced similar benefits from laminoplasty.

Level of Evidence: 3

Cervical spondylotic myelopathy (CSM) is one of the most prevalent and increasingly observed neurological disorders in the geriatric population.1,2 Decompression surgical procedures are the established treatment for CSM. Cervical laminoplasty is a decompression procedure for CSM, and many authors have described its excellent surgical results.3–8 The reported prognostic factors include age, symptom duration, preoperative neurological condition, smoking, and signal changes in the spinal cord on magnetic resonance imaging.5,9–14

Diabetes mellitus is one of the most frequent comorbidities; the number of diabetic individuals in the population is also increasing. Therefore, surgical treatment of clinical conditions in these patients is becoming a greater concern. Diabetes is a chronic systemic disease that can affect the peripheral nervous system and microvascular system. Previous authors have reported that diabetic neuropathy and/or angiopathy influences the outcomes of lumbar spine surgery.15–17

To the best of our knowledge, there have been 3 reports on the outcomes of surgery for CSM in diabetic patients.9,18,19 Diabetic patients with cervical myelopathy show a poorer sensory function recovery in the lower extremities and a poorer recovery rate (RR).18 However, the outcome of laminoplasty has not been fully evaluated in diabetic patients with CSM because those retrospective studies included both ossification of the posterior longitudinal ligament (OPLL) and CSM and the sample size was small. The results of cervical laminoplasty in patients with CSM have been reported to be superior to those in patients with OPLL,20 and it is likely that previous studies contained some bias. Therefore, we designed a large-scale cohort study examining the outcome of surgery for CSM with regard to a single exclusive operative procedure. This study aimed to compare the outcome of cervical laminoplasty in diabetic patients and nondiabetic patients with CSM and to analyze the impact of diabetes on these outcomes.

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MATERIALS AND METHODS

Study Population

Between January 2007 and March 2011, 701 consecutive patients underwent modified double-door laminoplasty for CSM. Exclusion criteria included the following: (1) presence of OPLL; (2) history of rheumatoid arthritis, cerebral palsy, or tumors; (3) spinal injuries; (4) destructive spondylarthritis caused by hemodialysis; (5) previous cervical surgery; (6) spinal fusion with instrumentation; (7) thoracic spondylotic myelopathy; and (8) lumbar spinal canal stenosis. Of the 701 patients, 528 with CSM were eligible for participation in the study. Of the 528 patients, 505 consecutive patients with CSM who were followed up for more than 12 months after surgery were prospectively enrolled in this study (follow-up rate, 95.6%). The final sample comprised 311 males and 194 females; their mean age was 66.6 years (range, 41–91 yr).

The patients were divided into 2 groups: diabetic and nondiabetic groups. The diabetic group included patients with fasting blood glucose levels of 126 mg/dL or more on preoperative screening or those who were previously diagnosed with diabetes. We consulted diabetes specialists at our hospital for these patients, and all patients had well-controlled blood glucose levels during the perioperative period. We evaluated the differences in age, sex, symptom duration, body height, body weight, body mass index, cervical alignment, and range of motion (ROM), increased signal intensity on magnetic resonance T2-weighted imaging (MRT2WI), prevalence of hypertension and hyperlipidemia, use of anticoagulant or antiplatelet agents, smoking history, and postoperative follow-up period between both groups.

All patients presented with symptoms of myelopathy. Magnetic resonance imaging and myelography findings were consistent with myelopathy secondary to multisegmental cervical spondylotic stenosis. Each patient had myelopathy confirmed by a physical examination, and cord compression was present only between C2–C3 and C7–T1 disc levels. The institutional review board in our institution approved this study, and written informed consent was obtained from each patient before study participation or surgery.

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Surgical Technique for Modified Double-Door Laminoplasty

We performed double-door laminoplasty according to Kurokawa method with some modifications.8,21–23 The muscles attached to the C2 spinous process were preserved without detachment. Surgical exposure was limited as much as possible. The spinous processes between C3 and C7 were resected at their bases, and the laminae were cut at the center using a high-speed drill. Bilateral gutters were created as hinges at the border between the laminae and the facets in a fashion that was slightly more medial than the original procedure, thus minimizing invasion of the facets. After the halves of the laminae were elevated in a manner similar to a French door, the bone graft struts (length, 16–18 mm) created from the C6 or C7 spinous process were tied to bridge the bilateral edges of the laminae.

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Postoperative Considerations

After surgery, all patients, with exceptions, were allowed to sit up and walk on the first postoperative day while wearing a Philadelphia collar. The collars were fitted to all patients, but they were able to take them off at their discretion. Cervical ROM exercises were performed as early as possible during the rehabilitation program. We explained the ideal alignment to all patients after surgery.

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Clinical Outcomes

Operation time and blood loss were assessed. The severity of myelopathy before and after surgery was evaluated according to a scoring system proposed by the Japanese Orthopaedic Association (JOA) score for cervical myelopathy.14,24 The assessment of postoperative JOA score was performed 1 year after surgery and at the final follow-up. The JOA score quantifies neurological impairment by evaluating motor function in the upper and lower extremities (4 points each), sensory function in the upper and lower extremities as well as in the trunk sensibility (2 points each, total 6 points), and urinary bladder function (3 points). Therefore, a perfect JOA score for cervical myelopathy is 17 points (Table 1). The RR of the JOA score was calculated using the following formula originally suggested by Hirabayashi et al25 [RR = (postoperative JOA score − preoperative JOA score)/(17 − preoperative JOA score) × 100%] (Table 1). In addition, the achieved JOA score (postoperative JOA score − preoperative JOA score) was also evaluated.14

Table 1
Table 1
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Complications such as dural tear, postoperative epidural hematoma, and C5 palsy as well as local wound problems such as infection and delayed wound healing were investigated. C5 palsy was defined as paresis of the deltoid (manual muscle test score of 1 or 2) with or without the involvement of the biceps but no loss of strength in other muscles.23 Major complications such as death, myocardial infarction, heart failure, pulmonary thrombosis, pneumonia, cerebral infarction, and organ failure were assessed.

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Radiographical Outcomes

The lordotic angle between C2 and C7 was measured before surgery and at the final follow-up in the neutral and maximal flexion-extension lateral radiographical view by the Cobb method, with negative and positive lordotic angles indicating cervical kyphosis and lordosis, respectively.22,26–28 The alignment change was also assessed: [alignment change (°) = (preoperative C2–C7 lordotic angle) − (postoperative C2–C7 lordotic angle)].

ROM of the cervical spine was assessed by measuring the difference in alignment at flexion and extension.29 Angles created by a line parallel to the inferior aspect of the C2 vertebral body and a line parallel to that of the C7 vertebral body were measured on flexion and extension lateral radiographs, and a total ROM value was obtained by summation of these angles. ROM preservation was assessed by the formula [ROM preservation (%) = (postoperative ROM)/(preoperative ROM) × 100]. The occurrence of increased signal intensity on MRT2WI was also evaluated.13

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Statistical Analysis

A standard StatView software package (SAS Institute, Cary, NC) was used for statistical analysis. All values are expressed as means ± standard deviation. A nonparametric analysis (Mann-Whitney U test) or the χ2 test was used to analyze differences between groups. A P value of less than 0.05 was considered statistically significant.

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RESULTS

Laminoplasty was performed at the following disc levels: C3–C7 in 432 patients, C3–C6 in 37 patients (along with C7 dome-shaped fenestration), C4–C7 in 21 patients, C3–C6 in 11 patients, and C3–T1 in 4 patients. The average operation time for laminoplasty was 76.6 minutes (range, 38–160 min) and the average blood loss was 51.2 mL (range, 1–500 mL). The average postoperative follow-up period was 26.5 months (range, 12–66 mo). The mean disease duration was 15.4 months (range, 1–200 mo). The mean preoperative JOA score was 10.6 ± 2.6 points; the mean postoperative JOA score was 13.6 ± 2.5 points 1 year after surgery and 13.8 ± 2.5 points at the final follow-up. The mean RR of the JOA score was 51.8% ± 32.0%.

There were 105 patients in the diabetic group and 400 patients in the nondiabetic group (Figure 1). There was no statistically significant difference in patient demographic data between both groups (Table 2). There was no significant difference in age, sex, symptom duration, body mass index, preoperative cervical alignment and ROM, or occurrence of increased signal intensity between both groups. Although the diabetic group showed a significantly higher prevalence of hypertension and hyperlipidemia and greater use of anticoagulants and/or antiplatelet agents than the nondiabetic group, there was no significant difference in smoking history (Table 3). There was no statistically significant difference in the follow-up period, operation time, blood loss, postoperative cervical alignment and ROM, and alignment change and ROM preservation between the 2 groups (Table 4).

Figure 1
Figure 1
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Table 2
Table 2
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Table 3
Table 3
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Table 4
Table 4
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Mean JOA scores in the diabetic and nondiabetic groups were 10.1 ± 2.7 and 10.8 ± 2.5 points before surgery, 13.0 ± 2.8 and 13.8 ± 2.4 points 1 year after surgery, 13.1 ± 2.9 and 13.9 ± 2.4 points at the final postoperative follow-up, respectively. The pre- and postoperative JOA scores at the final follow-up of the diabetic group were significantly lower than those of the diabetic group (Figure 2). The diabetic group showed significantly lower RRs of JOA scores than the diabetic group (47.3% ± 30.7% vs. 53.6% ± 29.4%, P = 0.047, Figure 3). However, mean achieved JOA scores in the diabetic and nondiabetic groups were 3.0 ± 2.3 and 3.1 ± 2.0 points respectively, with no significant difference between the 2 groups (P = 0.343, Figure 4).

Figure 2
Figure 2
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Figure 3
Figure 3
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Figure 4
Figure 4
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Neither group had any major complications such as death, myocardial infarction, or pulmonary thrombosis. No intraoperative neural deterioration was observed. However, the diabetic group had other complications such as superficial wound complications (delayed wound healing) in 2, postoperative epidural hematoma in 1, C5 palsy in 1, heart failure in 1, and pneumonia in 1 patient. The nondiabetic group had other complications such as intraoperative dural tears requiring repair in 6; C5 palsy in 6, postoperative epidural hematoma in 2, postoperative deep infection below the deep fascia and muscles in 1, cerebral infarction in 2, and heart failure in 1 patient. There was no significant difference in surgical site infection. In this study, no patient with a C5 palsy needed additional surgery. All patients were treated conservatively with rest, rehabilitation of muscle strength, and ROM exercises in bed, and further physiotherapy after their pain subsided. Seven patients had spontaneous recovery from C5 palsy at final follow-up, and satisfactory recovery was achieved with conservative treatment. There was also no significant difference in the postoperative complication rate in the diabetic and nondiabetic groups (6/105 [5.71%] vs. 18/400 [4.50%), P = 0.603].

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DISCUSSION

Given that CSM is one of the most common spinal disorders, the prevalence of surgery for CSM has been increasing and is currently approximately 2- to 7-fold higher than that during the past decade.30,31 Diabetes, which is 1 of the most frequent coexisting comorbidities, may affect surgical outcomes in spinal disorders. The number of diabetic patients is increasing worldwide. The global prevalence of diabetes among adults aged 20 to 79 years was estimated to be 285 million people in 2010 and is projected to increase to 439 million by 2030.32 To our knowledge, there have only been 3 previous reports describing the influence of diabetes on surgical outcomes in patients with cervical myelopathy.9,18,19 The management of CSM with diabetes has been a matter of debate; thus, it remains unclear whether and how diabetes affects the surgical outcomes of cervical laminoplasty for CSM. This study aimed to compare the outcome of laminoplasty between diabetic and nondiabetic patients with CSM. This study evaluated the largest number of patients; it is the first well-matched control study diabetic patients with CSM, which is the strength of our study. Pre- and postoperative JOA scores and RRs were low in diabetic patients compared with nondiabetic patients. However, the achieved JOA score was not significantly different between the diabetic and nondiabetic patients. Diabetic and nondiabetic patients experienced similar benefits from laminoplasty for CSM, which was probably because of strict blood glucose level control enforced by diabetes specialists during the perioperative period. If blood glucose levels are appropriately controlled before and after surgery, diabetic patients might obtain reasonable recovery after cervical laminoplasty.

Although there have been 3 reports of the influence of diabetes on surgical outcomes for cervical myelopathy, the controversy is mostly related to the impact of surgical outcomes on the cervical spine.9,18,19 Kawaguchi et al18 reported that diabetic patients were more likely to have a poor recovery of sensory function in the lower extremities.18 Kim et al9 also reported that RR in diabetic patients was expected to be inferior to that in nondiabetic patients. They speculated that the poor recovery of neurological function resulted from diabetic polyneuropathy. These previous studies had several limitations. First, they retrospectively reviewed only patients who underwent surgery. Therefore, a further prospective study should be conducted to identify the relationship between the severity of diabetes and surgical outcomes more clearly. Second, those retrospective studies included both patients with OPLL and patients with CSM, which may have resulted in bias to a certain extent. Third, the sample of diabetic patients was small, which could have affected the results and led to no difference in surgical outcome between diabetic and nondiabetic patients (Table 5).

Table 5
Table 5
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Many previous investigators have used the JOA scoring system and its RR as the parameter for evaluating treatment, but certain limitations exist despite its popularity. The most crucial scientific limitation of this scoring system is that the actual surgical outcome in patients with the same RR may differ according to the preoperative JOA scores. If patients have low preoperative JOA scores, their actual surgical outcomes may be poorer than those of patients with high preoperative JOA scores. For example, Figure 5 shows RRs in cases with an achieved JOA score of 3. Even in instances with the same achieved JOA score, RR changed because of the preoperative JOA score (Figure 5). Results of this study indicate that the resumption of normal daily activities after surgery is strongly influenced by the severity of the pre-existing disease.

Figure 5
Figure 5
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Therefore, the decision of surgical intervention, particularly in diabetic patients, requires special consideration that is based on balancing the risks and benefits associated with surgery. In previous assessments of surgical outcome in the diabetic patients with CSM, Kawaguchi et al18 reported that although the preoperative JOA score was lower in diabetic patients, they found no significant difference in RR of the JOA score between 2 groups. Dokai et al19 reported that diabetic patients obtained benefits similar to those in nondiabetic patients. They described that cervical laminoplasty improves the quality of life and activities of daily living even in diabetic patients with CSM.18,19

On the contrary, our study found significant differences between the diabetic and nondiabetic groups with respect to pre- and postoperative JOA scores and RR of the JOA score. However, this study showed that even diabetic patients achieved a significant JOA score after surgery. On the basis of the achieved score, no significant difference was observed in the surgical outcome between both groups. Improvement in neurological function is an essential surgical outcome for diabetic patients. In this study, patients who achieved a significant JOA score showed improvement in neurological function. Therefore, we suggest that not only RR but also the achieved JOA score is important for evaluating the surgical outcome in CSM.

When surgery is performed in diabetic patients, more attention is required to avoid postoperative complications because diabetes is reportedly to be one of the risk factors for surgical site infections.15–18 Diabetic patients have microvascular angiopathy and lower immunity.19 Kawaguchi et al18 reported that diabetic patients with cervical myelopathy were more likely to develop wound complications. However, there was no significant difference in surgical site infection in our series, probably because strict blood glucose level control was enforced by diabetes specialists during the perioperative period. In our study, the prevalence of hypertension and hyperlipidemia, and use of anticoagulant and/or antiplatelet agents may have affected the microvascular system in the patients, probably influencing the outcomes of cervical laminoplasty.

One of the possible limitations of our study was the relatively brief follow-up period. Moreover, patient-based objective outcomes such as quality of life determined using the Short-Form Health Survey 36 and subjective satisfaction as well as axial back pain using the visual analogue scale were not assessed. There was no electrophysiological study performed to evaluate the existence of diabetic polyneuropathy. Therefore, preoperative and postoperative neurological status may be ascribed to polyneuropathy and CSM in diabetic patients. Therefore, further electrophysiological studies are required. However, this study evaluated the largest number of patients who underwent the same single procedure. The patients were prospectively followed up with high a follow-up rate.

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CONCLUSION

Pre- and postoperative JOA scores and RRs were lower in the diabetic patients than the nondiabetic patients. However, achieved JOA scores were not significantly different between both groups. Diabetic and nondiabetic patients experienced similar benefits from laminoplasty.

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Key Points

* Outcomes of laminoplasty in diabetic and nondiabetic patients with CSM were compared.

* This study evaluated the largest number of patients; this is the first well-matched control study for diabetic patients with CSM, which is the strength of our study.

* Pre- and postoperative JOA scores and their RRs were low in diabetic patients compared with nondiabetic patients.

* The achieved JOA score was not significantly different between the diabetic and nondiabetic patients.

* Diabetic and nondiabetic patients experienced similar benefits from laminoplasty for CSM, which was probably because of strict blood glucose level control enforced by diabetes specialists during the perioperative period.

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Acknowledgement

Presented at the Cervical Spine Research Society (Asia Pacific Section), 4th Annual Meeting, Seoul, Korea, April 2013.

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diabetes; cervical spondylotic myelopathy; surgical outcomes; cervical laminoplasty; prospective study

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