Multicenter, prospective study.
To investigate the effects of diabetes mellitus (DM) on surgical outcomes in patients with cervical myelopathy.
To date, few studies have investigated the influence of postoperative blood glucose or glycated hemoglobin (HbA1c) levels on surgical outcomes.
The participants were patients who underwent surgery for the treatment of cervical spondylotic myelopathy and ossification of the posterior longitudinal ligament. The 61 cases were evaluated preoperatively and 1 year postoperatively using the Japanese Orthopaedic Association (JOA) scores and the JOA Cervical Myelopathy Evaluation Questionnaire (JOACMEQ). The study variables included fasting blood glucose and HbA1c levels measured preoperatively and at 1 week, 4 weeks, and 1 year postoperatively; the F-wave conduction velocity, latency, rate of occurrence, and M-wave latency in the ulnar and tibial nerves were measured preoperatively and at 1 year postoperatively. The patients were divided into a group without diabetes (N group, 42 patients) and a group with diabetes (DM group, 19 patients). We then assessed the associations between the surgical outcomes and each of the study variables.
JOA scores significantly improved in both groups; however, no significant between-group differences were found. There was no significant improvement in the JOACMEQ scores, which assessed cervical function, upper and lower limb function, and bladder function in both groups. We then subdivided the DM group into those with a good control of HbA1c after 1 year (DMG group, 12 patients) and those with HbA1c deterioration after 1 year (DMB group, seven patients), prior to comparing the surgical outcomes. The JOACMEQ scores for upper and lower limb function significantly improved in the DMG group (
Poor glycemic control might prevent postoperative functional recovery of the spinal cord.
Cervical spondylotic myelopathy (CSM) is generally observed in adults aged >50 years [
Dokai et al. [
DM is a frequent comorbidity that affects many organs and causes numbness and weakness in the extremities due to peripheral nerve damage. The effects of DM on the peripheral nervous system and microvasculature are of concern.
Surgeons must consider issues surrounding DM control during the perioperative period. Previous reports have indicated that preoperative glycated hemoglobin (HbA1c) and blood sugar levels affect surgical outcomes in patients with CSM. However, few studies have examined the influence of postoperative blood glucose or HbA1c levels on surgical outcomes. Our study investigated the effects of DM on surgical outcomes in patients with CSM by assessing DM control postoperatively.
We performed a prospective multicenter study at Tottori University Hospital, comprising eight hospitals in and around the Tottori Prefecture in Japan from 2012 to 2015.
Informed consent was obtained from all participants. Inclusion criteria were patients who underwent surgical treatments for CSM and ossification of the posterior longitudinal ligament. We used magnetic resonance imaging (MRI) to determine the compression level and regarded the compression level with cord intensity change at T2WI. If cord intensity changes were never determined, we considered the level of most severe stenosis within the cervical spine as the origin of the myelopathy.
All the patients underwent laminoplasty or anterior decompression and fusion at the discretion of the spinal surgeon at each institution. Exclusion criteria were (1) past history of cervical spine surgery; (2) congenital deformity of the cervical spine; (3) infection; (4) trauma; (5) tumor; (6) rheumatoid arthritis; (7) cervical palsy; (8) pacemaker treatment; and (9) paralysis without cervical disorder. The patients were divided into two groups: a group without diabetes (N group) and a group with diabetes (DM group). DM was diagnosed if any or all the following criteria were met, as defined by the Japan Diabetes Society: (1) fasting blood sugar >126 mg/dL, (2) causal blood sugar over 200 mg/dL; (3) blood sugar over 200 mg/dL under 2 hours 75 g, and oral glucose-tolerance test; and (4) HbA1c over 6.5%.
The patients diagnosed with diabetic mellitus were treated with intensive blood sugar control by a doctor of internal medicine during the perioperative period. This study was approved by the local ethics committee of the Faculty of Medicine, Tottori University (IRB approval no., 1824).
The Japanese Orthopaedic Association (JOA) [
Patient characteristics recorded included sex, age, height, weight, body mass index, and disease duration.
We evaluated fasting blood glucose (FBG) and HbA1c levels via routine blood testing preoperatively and 1 week, 4 weeks, and 1 year postoperatively.
M- and F-waves were recorded from the ulnar and tibial nerves. Surface recording electrodes were placed bilaterally on the abductor digiti minimi and abductor hallucis muscles. Stimulations were delivered from the proximal elbow to the ulnar nerve and from the popliteus to the tibial nerve. The peripheral conduction time (PCT) was calculated using Kimura’s method [
These assessments were performed preoperatively and 1 year postoperatively.
All the data are expressed as mean±standard deviation. The statistical analyses were performed using StatMate ver. 5.0 for Windows and Mac (ATMS Co., Tokyo, Japan). Differences between groups were determined using Pearson’s chi-square test, Fisher’s exact test, and the Mann–Whitney
Between-group differences in FBG and HbA1c levels were compared using paired
A total of 148 participants were registered. A total of 140 patients were included during the 3-year study period. Seventy-nine of these patients were excluded: 66 for missing values at the 1-year follow-up, two patients died, two patients suffered from lumbar spinal stenosis, two patients had spinal injuries, one patient had cerebrovascular disease, one patient was diagnosed with bile duct cancer, one patient was diagnosed with a vitamin B12 deficiency postoperatively, and four patients failed to present for the 1-year follow-up appointment, resulting in 61 evaluable patients. The patients were then divided into two groups: a group without diabetes (N group, 42 patients) and a group with diabetes (DM group, 19 patients). The characteristics of the N and DM groups are presented in
We also divided the DM group into two subgroups according to HbA1c levels over the preoperative period and the levels at the 1-year follow-up, in order to investigate the effects of HbA1c levels on surgical outcomes. The DMG group (n=12) consisted of individuals with good DM control at the 1-year follow-up. The DMB group (n=7) consisted of patients with DM control deteriorations at the 1-year follow-up (
FBG and HbA1c level changes are shown in
JOA scores significantly improved in both groups postoperatively (N group,
To determine whether reduced HbA1c levels correlated with surgical outcomes, we analyzed the relationship between HbA1c levels and RR in all cases. There was no correlation throughout the study period (
The surgical outcomes with JOACMEQ are shown in
The ratio of males to females was higher in the DMG group than in the DMB group. There were no significant physical differences between the groups. Bowel and bladder disturbances were observed more frequently in the DMG group than in the DMB group (
JOA scores were significantly improved in both groups postoperatively (DMG group,
The DMG group exhibited less improvement in UE and LE surgical outcomes (
Preoperative PCT results are shown in
We evaluated surgical outcomes associated with CSM. Surgical outcomes based on JOA scores were not significantly different between the N and DM groups. Furthermore, there were no significant differences relative to DM control. In fact, with respect to the RR with JOA, there were no significant differences between the N and DM groups and between the DMG and DMB groups with respect to the presence of DM. Poor glycemic control affected CSM surgical outcomes as indicated by the JOACMEQ evaluation. We conclude that poor DM control impaired surgical outcomes in patients with CSM. Previous studies have reported that preoperative HbA1c levels affected recovery after CSM surgery [
DM affects outcomes of all types of spinal surgeries, yet most studies do not include postoperative DM control. The between-group differences in surgical outcomes in our study and in previous studies might be explained by conditional differences in patients with DM.
Diabetic neuropathy is one of the main factors in the diagnosis of patients with myelopathy. Nakanishi et al. [
Patients with poor DM control often experience poorer recovery postoperatively than patients with good DM control. However, our results showed that peripheral disorders associated with DM did not directly affect surgical outcomes.
We could not identify the mechanism(s) by which DM was associated with CSM; however, we consider two theories relevant. The first of these involves DM-linked microangiopathy. Microangiopathy interferes with nutrient diffusion through the vertebral endplate, potentially leading to disk degeneration [
Our second theory involves DM myelopathy. Following a post-mortem study, Reske-Nielsen and Lundbaek [
Selvarajah et al. [
The 6.5-year Diabetes Control and Complication Trial in the United States divided patients with DM into two groups. The first group included patients receiving ‘typical’ DM therapy. The average HbA1c level in this group during the study was approximately 9.0%. The other group of patients received strictly controlled DM therapy. The average HbA1c level in this group during the study was approximately 7.0%. The prevalence of DM neuropathy was 13% among the patients receiving typical DM therapy and 5.0% among those receiving a stricter DM therapy at the end of this trial. DM control, therefore, appears to be important for preventing complications associated with DM, including neuropathy and angiopathy [
This study has several limitations. First, many patients were excluded because of a lack of data, particularly regarding HbA1c levels or PCT values at the 1-year follow-up. Second, we investigated only FBG and HbA1c levels during the perioperative period and at 1 year postoperatively. We did not record glycemic control between these time points. Despite these limitations, we believe that strict control of DM is necessary for achieving good longterm outcomes.
Postoperative improvement in CSM varies in association with control of DM symptoms during the preoperative and postoperative periods. We believe that poor glycemic control might prevent postoperative functional recovery of CSM.
No potential conflict of interest relevant to this article was reported.
Study flowchart. N group: a group without diabetes; DM group: a group with diabetes; DMG group: those with a good control of HbA1c after 1 year; DMB group: those with HbA1c deterioration after 1 year. DM, diabetes mellitus; HbA1c, glycated hemoglobin.
Patient characteristics and demographics
Characteristic | N group | DM group | |
---|---|---|---|
Age (yr) | 69.6±13.3 | 69.3±10.7 | 0.78 |
Gender (male:female) | 25:11 | 12:17 | 0.79 |
Height (cm) | 158.5±9.6 | 160.7±10.2 | 0.43 |
Weight (kg) | 57.6±12.2 | 60.1±11.7 | 0.28 |
Body mass index (kg/m2) | 22.8±3.4 | 23.2±3.7 | 0.72 |
CSM:OPLL | 29:13 | 14:5 | 0.71 |
Peripheral conduction time (ms) | |||
Ulna (right) | 15.3±2.3 | 17.4±6.2 | 0.05 |
Ulna (left) | 15.5±2.7 | 17.3±5.2 | 0.08 |
Tibia (right) | 25.6±2.9 | 27.1±3.0 | 0.09 |
Tibia (left) | 25.6±3.1 | 26.8±3.0 | 0.14 |
JOA score (total) | 10.9±2.8 | 10.8±7.5 | 0.80 |
JOACMEQ | |||
Cervical | 70.5±30.7 | 62.6±30.2 | 0.37 |
Upper extremity | 66.7±23.7 | 72.4±18.2 | 0.47 |
Lower extremity | 52.3±31.7 | 52.3±26.4 | 0.91 |
Bowe & bladder | 68.9±19.2 | 71.7±16.1 | 0.98 |
Quality of life | 45.3±16.0 | 38.6±18.9 | 0.15 |
Values are presented as mean±standard deviation or number. No variables significantly differed between the groups (a group without diabetes [N group] and a group with diabetes [DM group]).
DM, diabetes mellitus; CSM, cervical spondylotic myelopathy; OPLL, ossification of the posterior longitudinal ligament; JOA, Japanese Orthopaedic Association; JOACMEQ, JOA Cervical Myelopathy Evaluation Questionnaire.
By Mann-Whitney
By chi-square test.
Changes in FBG and HbA1c levels
Variable | Preoperative | Postoperative period |
||
---|---|---|---|---|
1 wk ( |
4 wk ( |
1 yr ( |
||
N group (n=42) | ||||
FBG (mg/dL) | 101.0±18.4 | 93.4±15.6 (0.00) | 97.2±20.2 (0.29) | 103.5±23.8 (0.60) |
HbA1c (%) | 5.6±0.4 | 5.6±0.4 (0.68) | 5.5±0.4 (0.07) | 5.6±0.3 (0.19) |
DM group (n=19) | ||||
FBG (mg/dL) | 155.1±48.9 | 115.4±21.9 (0.00) | 114.8±29.2 (0.00) | 149.9±50.9 (0.75) |
HbA1c (%) | 6.9±0.9 | 6.8±0.4 (0.19) | 6.5±0.4 (0.04) | 6.8±0.9 (0.06) |
Values are presented as mean±standard deviation, unless otherwise stated. N group: a group without diabetes; DM group: a group with diabetes.
FBS, fasting blood glucose; HbA1c, glycated hemoglobin; DM, diabetes mellitus.
Compared with perioperative value.
Surgical outcomes as assessed on the basis of the JOA scores between the N and DM groups
Variable | JOA (total score) |
Recovery ratio (%) | |
---|---|---|---|
Preoperative | After 1 yr (p -value) | ||
N group | 10.9±2.8 | 13.5±4.8 (0.01) | 40.1±39.0 |
DM group | 10.8±7.5 | 12.9±5.0 (0.01) | 26.3±34.4 |
0.80 | 0.35 | 0.41 |
Values are presented as mean±standard deviation, unless otherwise stated. N group: a group without diabetes; DM group: a group with diabetes;
JOA, Japanese Orthopaedic Association; DM, diabetes mellitus.
Correlations between hemoglobin A1c and recovery ratio levels
Variable | Correlation coefficient | |
---|---|---|
Preoperative | -0.15 | 0.26 |
At 1 wk | -0.13 | 0.30 |
At 4 wk | -0.02 | 0.85 |
At 1 yr | -0.02 | 0.99 |
Pearson’s correlation coefficient.
Surgical outcomes as assessed on the basis of the JOACMEQ scores between the N and DM groups
Group | JOACMEQ |
||||
---|---|---|---|---|---|
Cervical function | Upper extremity function | Lower extremity function | Bowel & bladder | Quality of life | |
N group | |||||
No. of patients | 37 | 38 | 36 | 37 | 42 |
Score | |||||
Preoperative | 67.5±30.8 | 64.6±23.3 | 44.6±27.3 | 66.2±18.2 | 45.3±16.0 |
At 1 yr | 71.8±24.4 | 79.3±17.7 | 56.6±20.8 | 70.7±22.4 | 51.5±17.9 |
EV | 4.3±28.8 | 14.7±22.2 | 12.1±23.7 | 4.5±20.3 | 6.2±18.1 |
|
0.36 | <0.01 | <0.01 | 0.18 | 0.31 |
DM group | |||||
No. of patients | 12 | 18 | 19 | 16 | 19 |
Score | |||||
Preoperative | 55.4±27.9 | 70.9±17.4 | 52.3±16.4 | 67.5±13.9 | 38.6±18.9 |
At 1 yr | 50.0±26.0 | 82.7±18.1 | 68.3±26.0 | 72.1±17.0 | 48.9±18.1 |
EV | 6.3±37.4 | 12.0±24.3 | 15.9±29.6 | 4.6±19.0 | 10.3±16.6 |
0.55 | 0.05 | 0.03 | 0.35 | 0.14 |
Values are presented as number or mean±standard deviation, unless otherwise stated. N group: a group without diabetes; DM group: a group with diabetes.
JOACMEQ, JOA Cervical Myelopathy Evaluation Questionnaire; DM, diabetes mellitus; EV, effective value.
Characteristics and demographics of the DMG and DMB groups
Characteristic | DMG group | DMB group | |
---|---|---|---|
Age (yr) | 66.4±10.3 | 74.1±10.1 | 0.11 |
Gender (male:female) | 10:1 | 2:5 | <0.01 |
Height (cm) | 160.1±9.1 | 160.4±12.4 | 0.87 |
Body mass index (kg/m2) | 23.3±3.3 | 23.2±4.2 | 0.93 |
Weight (kg) | 60.5±12.4 | 59.4±11.2 | 0.70 |
CSM:OPLL | 8:4 | 6:1 | 0.50 |
Peripheral conduction time (ms) | |||
Ulna (right) | 15.3±2.3 | 17.4±6.2 | 0.61 |
Ulna (left) | 15.5±2.7 | 17.3±5.2 | 0.32 |
Tibia (right) | 25.6±2.9 | 27.1±3.0 | 0.55 |
Tibia (left) | 25.6±3.1 | 26.8±3.0 | 0.55 |
JOA | 11.1±3.1 | 10.4±1.1 | 0.55 |
JOACMEQ | |||
Cervical | 64.6±32.2 | 59.3±28.3 | 0.70 |
Upper extremity | 73.5±18.6 | 70.6±18.9 | 0.63 |
Lower extremity | 54.8±27.8 | 48.1±28.4 | 0.55 |
Bowel & bladder | 77.8±15.5 | 61.4±12.2 | 0.02 |
Quality of life | 42.2±19.7 | 32.4±17.1 | 0.18 |
Values are presented as mean±standard deviation or number, unless otherwise stated. DMG group: those with a good control of HbA1c after 1 year; DMB group: those with HbA1c deterioration after 1 year.
DM, diabetes mellitus; CSM, cervical spondylotic myelopathy; OPLL, ossification of the posterior longitudinal ligament; JOA, Japanese Orthopaedic Association; JOACMEQ, JOA Cervical Myelopathy Evaluation Questionnaire; HbA1c, glycated hemoglobin.
By Mann-Whitney
By Fisher's exact test.
Surgical outcomes between the DMG and DMB groups as assessed on the basis of the JOACMEQ scores
Variable | JOA (total score) |
Recovery ratio (%) | |
---|---|---|---|
Preoperative | At 1 yr ( |
||
DMG group | 11.1±3.1 | 13.6±2.1 (0.03) | 30.1±48.0 |
DMB group | 10.4±2.5 | 11.7±2.0 (0.02) | 19.8±15.9 |
0.55 | 0.06 | 0.44 |
Values are presented as mean±standard deviation or number, unless otherwise stated. DMG group: those with a good control of HbA1c after 1 year; DMB group: those with HbA1c deterioration after 1 year.
DM, diabetes mellitus; JOACMEQ, JOA Cervical Myelopathy Evaluation Questionnaire; JOA, Japanese Orthopaedic Association; HbA1c, glycated hemoglobin.
Surgical outcomes between the DMG and DMB groups as assessed on the basis of the JOA scores
Variable | JOACMEQ |
||||
---|---|---|---|---|---|
Cervical function | Upper extremity function | Lower extremity function | Bowel & bladder | Quality of life | |
DMG group | |||||
No. of patients | 9 | 11 | 12 | 9 | 12 |
Score | |||||
Preoperative | 52.8±28.3 | 71.1±17.4 | 54.8±27.8 | 72.2±14.0 | 42.2±19.7 |
At 1 yr | 67.2±31.6 | 90.3±14.3 | 80.6±13.5 | 78.7±17.3 | 56.0±16.6 |
EV | 14.4±42.1 | 19.6±23.7 | 26.2±31.0 | 6.4±15.7 | 13.8±16.3 |
|
0.34 | 0.02 | 0.01 | 0.28 | 0.02 |
DMB group | |||||
No. of patients | 6 | 7 | 7 | 7 | 7 |
Score | |||||
Preoperative | 52.5±24.0 | 70.6±18.9 | 48.1±25.3 | 61.4±112.2 | 32.4±17.1 |
At 1 yr | 46.7±24.2 | 71.3±18.2 | 47.1±29.4 | 63.6±18.8 | 36.7±14.2 |
EV | -5.8±18.8 | 3.4±22.3 | 1.4±18.2 | 2.1±21.1 | 4.3±14.1 |
|
0.51 | 0.93 | 0.89 | 0.81 | 0.48 |
Values are presented as number or mean±standard deviation, unless otherwise stated. DMG group: those with a good control of HbA1c after 1 year; DMB group: those with HbA1c deterioration after 1 year.
DM, diabetes mellitus; JOA, Japanese Orthopaedic Association; JOACMEQ, JOA Cervical Myelopathy Evaluation Questionnaire; EV, effective value; HbA1c, glycated hemoglobin.
Changes in PCT between the DMG and DMB groups
Variable | PCT (ms) |
|||
---|---|---|---|---|
Ulna (right) | Ulna (left) | Tibia (right) | Tibia (left) | |
DMG group | ||||
Preoperative | 18.3±7.8 | 18.2±6.4 | 26.7±3.1 | 25.6±3.1 |
At 1 yr | 16.0±3.0 | 16.7±3.2 | 24.9±3.7 | 26.5±2.7 |
|
0.14 | 0.18 | 0.12 | 0.18 |
DMB group | ||||
Preoperative | 15.9±0.8 | 15.6±1.5 | 27.7±2.8 | 27.4±3.6 |
At 1 yr | 16.0±1.1 | 15.8±1.5 | 27.5±3.1 | 27.5±3.2 |
|
0.78 | 0.47 | 0.61 | 0.86 |
Values are presented as mean±standard deviation or number, unless otherwise stated. DMG group: those with a good control of HbA1c after 1 year; DMB group: those with HbA1c deterioration after 1 year.
PCT, peripheral conduction time; DM, diabetes mellitus; HbA1c, glycated hemoglobin.