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Risk Factors for Outcomes After Microvascular Decompression for Trigeminal Neuralgia
Journal Pre-proof Risk factors for outcomes following microvascular decompression for trigeminal neuralgia Jia Shi, Yitao Qian, Wei Han, Bo Dong, Yumin Mao, Jiachao Cao, Wei Guan, Qiang Zhou PII:
S1878-8750(20)30100-5
DOI:
https://doi.org/10.1016/j.wneu.2020.01.082
Reference:
WNEU 14112
To appear in:
World Neurosurgery
Received Date: 21 November 2019 Revised Date:
10 January 2020
Accepted Date: 11 January 2020
Please cite this article as: Shi J, Qian Y, Han W, Dong B, Mao Y, Cao J, Guan W, Zhou Q, Risk factors for outcomes following microvascular decompression for trigeminal neuralgia, World Neurosurgery (2020), doi: https://doi.org/10.1016/j.wneu.2020.01.082. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Elsevier Inc. All rights reserved.
Title Page
Risk factors for outcomes following microvascular decompression for trigeminal neuralgia
Jia Shi1*, Yitao Qian1*, Wei Han1, Bo Dong1, Yumin Mao1, Jiachao Cao1, Wei Guan1, Qiang Zhou1
1. Department of Neurosurgery, The Third Affiliated Hospital of Soochow University, Changzhou, China.
*. These authors contributed equally to this work.
Correspondence to: Qiang Zhou. E-mail: [email protected]. Address: No.185, Juqian Street, Changzhou, Jiangsu, 213003, China.
Risk factors for outcomes following microvascular decompression for trigeminal neuralgia
Abstract Background: Microvascular decompression (MVD) is the most effective long-term surgical treatment for trigeminal neuralgia (TN) patients. The risk factors for poor pain control following MVD surgery are not fully understood. Methods: A total of one hundred eighty-four patients were enrolled from patients with typical TN who underwent MVD at our institution between 1/3/2008 and 1/3/2016. The data were collected using electronic operative records and case notes and were retrospectively analyzed. Patients were followed up at the outpatient department or by telephone at a minimum of three months and at a maximum of forty-eight months. Results: 184 patients were enrolled in the study; 72.3% of patients achieved freedom from pain after MVD, 27.7% experienced poor pain control, with follow-up at a minimum of 3 months and at a maximum of 48 months. Risk factors for poor pain control after MVD according to binary logistic regression and ROC analysis included younger age (OR: 0.90; 95% CI: 0.82-0.99; P = 0.028; AUC=0.774); poor preoperative pain control (BNI score > IV) (OR: 52.03; 95% CI: 6.44-420.16, P < 0.001; AUC=0.858); intraoperatively detected multivessel compression (OR: 2.49; 95% CI: 3.10-46.59, P < 0.001; AUC=0.871). Furthermore, combined compression of the superior cerebellar artery (SCA) and the petrosal vein (PV) was an independent risk factor predicting a poor outcome following MVD (OR: 5.69; 95% CI: 33.78-2579.03, P < 0.001; AUC=0.812). Conclusions: Younger patients with TN had worse long-term pain outcomes following MVD. Additional factors associated with postoperative recurrence included poor preoperative pain control (BNI score > IV) and multivessel compression. Furthermore, SCA combined with PV was confirmed to be associated with a worse outcome.
Key words: trigeminal neuralgia, microvascular decompression, risk factors
Introduction Trigeminal neuralgia (TN) is a debilitating facial pain syndrome characterized by episodic pain in the branches of the trigeminal nerve1. The pain episodes are generally described as debilitating, severe, and sharp, although the typical episode may last only seconds to minutes1, 2. According to the Burchiel classification system, when lancinating facial pain predominates, it is described as “Burchiel type 1” or typical facial pain. Conversely, atypical TN is described as a “Burchiel type II”, which is a described as a constant burning pain accompanying the lancinating pain3. The first-line therapy for TN patients is pharmacological treatment with medications including carbamazepine or other antiepileptic drugs such as pregabalin, gabapentin, or oxcarbazepine4-6. Surgical therapy can provide long-lasting pain relief to TN patients whose treatment is limited by medication side effects or a small therapeutic window4. Microvascular depression (MVD) is currently acknowledged as the best surgical treatment for typical TN with vascular compression, especially with arterial compression7-9. With regard to MVD surgery, long-term pain outcomes are generally favorable, but there are still significant differences in outcome rates throughout the literature, attributed to variabilities in patient epidemiology, clinical data, and anatomical vascular compressions or differences pertaining to the study center itself. For example, several studies demonstrated that pain-free rates as high as 90% or more could be achieved following MVD surgery10-12, while other studies only identified rates of 50-70%13, 14. Moreover, although a few systematic reviews have evaluated risk factors for the recurrence of MVD, none have quantitatively analyzed these risk factors or predictors15-18. Therefore, studies regarding recurrence rates and predictors for freedom from pain after MVD remain uncertain. In this study, the goal was to determine the recurrence rates and risk factors for a poor pain outcome following MVD surgery. Our results may provide a significant addition to the current literature examining the predictors for MVD efficacy, thus
helping patients and clinicians make appropriate choices prior to intervention.
Materials and methods Setting and participants The study was a cross-sectional, case-control, single-center and retrospective study. The patients surveyed in this study were recruited from a group of patients who underwent MVD for TN in the Third Affiliated Hospital of Soochow University between March 2008 and March 2016. The study was approved by the Ethics Committee of the Third Affiliated Hospital of Soochow University. Patients with TN meeting the following criteria were enrolled: (1) at least 18 years of age at the time of surgery and (2) had typical (type I) TN with evidence of neurovascular compression (arterial and/or venous) on preoperative imaging. Patients who had undergone prior ablative or MVD procedures were excluded from the research study. A total of two hundred thirty-six patients were screened for eligibility. Twenty-two were excluded because they did not have evidence of neurovascular compression on preoperative imaging, while ten had atypical TN. Twenty were excluded because they had no follow-up information available. Finally, one hundred eighty-four patients were enrolled in the study (Figure 1). Each patient involved in this study signed an informed consent form after inclusion of the retrospective study. Data collection Prior to receiving MVD treatment, every patient in this group had a preoperative magnetic resonance imaging (MRI) scan of the brain according to the protocol developed at the Walton Center19, and all MRIs were reported by a neuroradiologist and reviewed by the operating neurosurgeon. Intraoperative findings at the time of exploration were noted and recorded in operative records at the time of surgery. Postoperative outcomes were assessed based on the Barrow Neurological Institute (BNI) pain intensity scale by an independent neurologist who was blinded to the patients’ preoperative pain scores. Recurrence was defined as an increase in pain requiring the introduction of new medication after successful pain relief following the
initial MVD. The interval of recurrence was defined as more than one month after operation. If The pain was not relieved within one month, it would be regarded as invalid20. The BNI score for all patients in this cohort was III-V prior to MVD; after MVD, BNI scores of I-II indicated a lack of recurrence, and scores of III-V indicated recurrence. According to a previous study, we categorized outcomes into good pain control (BNI scores I-II) (nonrecurrence group) and poor pain control (BNI scores III-V) (recurrence group)21. For further analysis of the connection between preoperative and postoperative BNI scores, the preoperative BNI score was subdivided into moderate pain control (BNI score III-IV) and poor pain control (BNI score V). The patients after microvascular decompression would be routinely reexamined with MRI, including the patients with recurrence. Patients were followed up at the outpatient department or by telephone at a minimum of three months and at a maximum of forty-eight months. The data were collected using electronic operative records and case notes and were retrospectively analyzed. Statistical analysis The statistical analysis was performed using SPSS 24.0. Subjects with missing information were excluded from the relevant portion of the analysis. Continuous data are presented as the mean ± SD and were compared using Student’s t tests. The categorical data are presented as percentage frequencies (%) and were compared using the chi-squared test. Binary logistic regression analyses were used to determine the factors associated with postoperative recurrence. The results are presented as ORs and 95% confidence intervals (CIs). We used a P value < 0.05 to indicate statistical significance. Results Clinical characteristics of patients with TN There were 184 patients with TN included in our study; 133 had good pain control (BNI score I-II, nonrecurrence group), and 51 had poor pain control (BNI score III-V, recurrence group). Table 1 and Table 2 show the clinical characteristics of the study patients. The mean age of patients in the recurrence group was younger than that of those in the nonrecurrence group (P < 0.001, Table 2). The BNI scores for patients
prior to MVD were III-V, with the following distribution: III (5.98%), IV (55.98%) and V (38.04%). As the preoperative BNI scores were subdivided into moderate pain control (BNI scores III-IV) and poor pain control (BNI score V), the number of patients with BNI score V in the recurrence group was greater than that in the nonrecurrence group (P < 0.001, Table 2). The number of intraoperatively identified compressive vessels was also analyzed as follows: single vessel (60.33%), double vessel (35.87%, including artery and vein) and triple vessel (3.80%). The number of patients with multivessel compression in the recurrence group was larger than that in the nonrecurrence group (P < 0.001, Table 2). No significant differences were found between the two groups with regard to the other parameters. Table 3 shows the risk factors associated with recurrence according to binary logistic regression analysis. Younger age (OR: 0.90; 95% CI: 0.82-0.99; P = 0.028), poor pain control prior to MVD (BNI score V, OR: 52.03; 95% CI: 6.44-420.16, P < 0.001) and intraoperatively identified multivessel compression (OR: 2.49; 95% CI: 3.10-46.59, P < 0.001) were significantly associated with recurrence in TN patients after MVD surgery. Furthermore, the ROC curve showed that younger age (95% CI: 0.68-0.86, AUC=0.774), intraoperatively determined multivessel compression (95% CI: 0.79-0.95, AUC=0.871) and preoperative BNI pain score (V) (95% CI: 0.79-0.93, ROC=0.858) could be specific predictors of recurrence following MVD surgery; the combination of all three resulted in a higher diagnostic value with regard to recurrence (95% CI: 0.94-0.99, AUC=0.968) (Figure 2). Association
of
intraoperatively
identified
vascular
compression
and
postoperative recurrence The most common intraoperative findings were the presence of vascular compression (including both artery and vein) in conflict with the trigeminal nerve. Table 4 shows the compressive vessels during the MVD process. The most common offending vessel was the superior cerebellar artery (SCA, 53.80%), followed by the combination of the SCA and the petrosal vein (PV, 24.46%) and the combination of the SCA and the anterior inferior artery (AICA, 5.98%). Patients with a compressed combination of an artery and a vein were more likely to experience recurrence (Table
5): SCA+PV (P < 0.001), AICA+PV (P = 0.005), basilar artery (BA) +PV (P = 0.005) and SCA+AICA+PV (P = 0.033). Further risk factors identified via binary logistic regression analysis showed that only SCA+PV (OR: 5.69; 95% CI: 33.78-2579.03, P < 0.001) was an independent risk factor for recurrence following MVD surgery. The ROC curve analysis also identified SCA+PA compression (95% CI: 0.81-0.91, AUC=0.812) as a specific predictor of recurrence after MVD surgery (Figure 2). Discussion MVD for patients suffering from TN is the most effective method of managing patients’ symptoms and is currently the only procedure that can arguably provide a cure22. However, previous studies demonstrated that the rate of recurrence of TN in patients after successful MVD is as high as 14% at 1 year and may rise as high as 20-40% at 10 years23. Therefore, it is of great importance to predict risk factors for the recurrence of TN in patients after MVD surgery. In this study, our results suggested that older patients have better pain outcomes following MVD than younger patients. Additional factors, including preoperative BNI pain score and intraoperatively detected multivessel compression, were confirmed to have positive associations with poor pain outcomes. The relationship between age and MVD efficacy in our studies is consistent with the findings in previous studies. A study examining the outcomes in patients 60 years and older with TN following MVD found that this older age group had relatively better pain outcomes21. A systematic review reported that while younger and older patients have similar initial success rates following MVD, older patients have lower rates of recurrence24. There are several possible reasons for this. First, TN has a close relationship with arteriosclerosis. The development of arteriosclerosis gradually leads to vascular tortuosity, deformation and even displacement, which may be the major cause of arterial neurovascular compression10. This association may explain the relationship between age and TN incidence, given the increasing prevalence of atherosclerosis with increasing age25. Second, atherosclerosis is positively correlated with age, which may contribute to the increased incidence of arterial neurovascular compression observed in older TN patients, while nerve compression caused by veins
is more common in younger patients26. From the perspective of anatomy, the variability of the venous system is greater, and the relationship between blood vessels and nerves is rather more complex, leading to the potential for operative difficulty, insufficient decompression, and a higher rate of overall recurrence27. Third, the improved outcomes in older patients may be partially explained by operative considerations. Compared to younger patients, cerebellar atrophy is more evident in older patients, facilitating cerebellopontine angle exposure26. Increased exposure may improve the ability to fully inspect and decompress nerves, free the responsible blood vessels, and achieve better decompressive efficacy and shorter operative durations28. Current studies on the relationship between preoperative pain symptoms and prognosis have mainly focused on the Burchiel type I and Burchiel type II classification. A systematic review and meta-analysis including 3897 patients from 46 studies demonstrated that Burchiel type II patients were more prone to recurrence following MVD surgery, and the recurrence rate was nearly twice that in type I patients29. However, few studies have focused on the relationship between the preoperative BNI pain score and MVD efficacy. In our results, binary logistic regression and ROC analysis confirmed that poor pain control prior to MVD (preoperative BNI pain score V) was an independent and specific risk factor for recurrence after MVD surgery, which may be attributed to the fact that the pain levels in TN patients are often associated with the number or extent of vascular and nerve compression, especially when involving venous vessels, which are associated with difficulty in obtaining adequate decompression and high recurrence rate30. According to the ignition hypothesis2, TN results from specific abnormalities of trigeminal afferent neurons in the trigeminal root or ganglion, and even the compression of a tiny blood vessel is enough to cause clinical symptoms2. Actually, the mechanisms underlying the correlation between a poor preoperative BNI score and recurrence after MVD are still uncertain, and large-scale and multicenter clinical studies are warranted for further analysis in the future. Previous studies clearly showed that vascular loop-related TNs are mainly caused by branches emanating from the distal basilar artery (SCA and AICA are the most
commonly responsible vessels)29. Our study also showed that nearly 53.80% of the cases had the usual SCA offenders, and 24.46% involved the accompanying veins. Binary logistic regression and ROC analysis confirmed that compared to single vessel compression, intraoperatively detected multivessel compression was an independent and specific predictor of postoperative recurrence. Further analysis of the compressive vessels showed that TN patients with the combination of an artery and PV had poor pain control after surgery, which was consistent with the findings in previous reports30. A possible explanation may be that compared to arteries, veins are firmly adhered to nerves and the brainstem, and they are less mobile, leading to difficulty in adequate decompression. In addition, the thickened arachnoid membrane around veins and thin and fragile venous wall are the anatomical factors that can easily lead to massive hemorrhage, operative difficulty and a higher recurrence rate31. Some scholars believe that intraoperative disconnection of the PV can better expose the root entry zone (REZ) of TN, helping the operators adequately decompress the TN without severe postoperative complications32. However, other researchers hold different opinions. Zhao et al believed that the veins should be preserved as much as possible during the operation33. Damage to large veins (diameter over 2 mm) may lead to serious complications, such as cerebral hemorrhage, infarction, edema, and even death. In our opinion, venous drainage should be maintained as smoothly as possible instead of directly disconnecting veins34. To determine the optimal management of veins during MVD, a larger number of cases, including various types of veins that block the approach to or compress the TN, should be further studied. In our study, we elaborated on the effects of different types of vascular compression on postoperative recurrence, which may provide an important addition to the limited existing literature examining the relationship between vessel compression and outcomes following MVD. Conclusions In this study, younger patients had worse long-term pain outcomes following MVD than older patients. Additional factors associated with postoperative recurrence included poor preoperative pain control (BNI score > IV) and intraoperatively detected
multivessel compression. Furthermore, with regard to multivessel compression, SCA combined with PV was confirmed to be associated with a worse outcome. Our study may provide a perioperative suggestion for TN patients undergoing MVD surgery, which will help physicians appropriately counsel patients prior to the intervention and help clinicians make the appropriate choice tailored to each individual. Funding No Competing interests On behalf of all authors, the corresponding author states that there is no conflict of interest. Ethical approval and consent to participate This study was approved by the Regional Ethics Committee of the Third Affiliated Hospital of Soochow University and all patients signed informed consents. Authors’ contributions Qiang Zhou and Wei Guan were major contributors in writing and in a review of the manuscript. Jia Shi collected patient data and was involved in writing and in a review of the manuscript. YiTao Qian and Wei Han were in charge of data analysis. Yumin Mao, Bo Dong and Jiachao Cao were involved in patient management and review of the manuscript. All authors read and approved the final manuscript. Consent for publication Informed consent was obtained from the patient and is attached to the patient records in the hospital files. Acknowledgements No applicable. References 1.
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Figure legends Figure 1: Participant flow diagram. Figure 2: The ROC curve for age (A), preoperative pain control (B) and intraoperatively detected multivessel compression (B) for outcomes following MVD surgery. MVD: microvascular decompression. The ROC curve of SCA combined with PV for outcomes following MVD surgery (C). SCA: superior cerebral artery; PV: petrosal vein.
Table 1. Clinical characteristics of study patients with TN. Parameters Sex (% male)
116 (63.04%)
Age (mean ± SD) Hypertension (%)
59.86 ± 10.81
Diabetes (%)
10 (5.43%)
Side (% left)
80 (43.48%)
79 (42.93%)
Pain location Single division
83 (45.11%)
Double division
86 (46.74%)
Triple division
15 (8.15%)
Preoperative disease duration (mean ± SD years)
4.42 ± 4.40
Preoperative BNI pain score III
11 (5.98%)
IV
103 (55.98%)
V
70 (38.04%)
Intraoperative vascular compression
58 (31.52%)
Single vascular
111 (60.33%)
Double vascular
66 (35.87%)
Triple vascular
7 (3.80%)
Table 2. Clinical characteristics of study patients with or without post-operative recurrence. Parameters
Good pain
Poor pain
95% CI
P
control
control
Sex (% male)
83 (62.40%)
33 (64.71%)
0.81-1.17
0.772
Age (mean ± SD) Hypertension (%)
67.50 ± 6.36
52 ± 16.26
-11.66-(-6.24)
< 0.001
61 (45.86%)
18 (54.55%)
0.74-1.06
0.195
Diabetes (%)
6 (4.51%)
4 (7.84%)
0.73-2.03
0.372
Side (% left)
57 (30.98%)
23 (45.10%)
0.81-1.17
0.784
Pain location (single division)
64 (48.12%)
19 (37.25%)
0.95-1.35
0.185
Preoperative disease duration
4.50 ± 4.80
4.24 ± 3.17
-1.70-1.17
0.720
22 (16.54%)
48 (94.12%)
2.19-4.39
< 0.001
8 (6.02%)
43 (84.31%)
2.24-5.61
< 0.001
(mean ± SD years) Preoperative BNI pain score (> IV) Intraoperative vascular compression (% multivessel)
Table 3. Multiple regression analyses of clinical characteristics of patients with or without postoperative recurrence. Parameters
B
OR (95% CI)
P
Age
-0.105
0.90 (0.82-0.99)
0.028
Preoperative BNI pain score (> IV)
3.26
26.14 (4.44-153.80)
< 0.001
Intraoperative vascular compression
2.69
14.66 (4.14-51.85)
< 0.001
(% multivessel)
Table 4. Compressive vessels during the process of MVD. Compressive vessels
Number (%)
SCA
99 (53.80%)
AICA
3 (1.63%)
BA
3 (1.63%)
PV
3 (1.63%)
SCA+ PV
45 (24.46%)
AICA+ PV
3 (1.63%)
BA+ PV
3 (1.63%)
SCA+ AICA
11 (5.98%)
SCA+BA
7 (3.80%)
SCA+AICA+PV
4 (2.17%)
SCA+BA+PV
3 (1.63%)
SCA: superior cerebral artery; AICA: anterior inferior cerebellar artery; BA: basilar artery; PV: petrosal vein.
Table 5. Association of intra-operative vessel compression and post-operative recurrence. Parameters
Good pain
Bad pain
control
Control
95% CI
P
SCA
75 (56.39%)
24 (47.06%)
0.93-1.35
0.215
AICA
3 (3.26%)
0 (0.00%)
1.27-1.53
0.279
BA
3 (2.26%)
0 (0.00%)
1.27-1.53
0.279
PV
3 (2.26%)
0 (0.00%)
1.27-1.53
0.279
SCA+ PV
7 (5.26%)
38 (74.51%)
0.09-0.34
< 0.001
AICA+ PV
0 (0.00%)
3 (5.88%)
0.00-1.02
0.005
BA+ PV
0 (0.00%)
3 (5.88%)
0.00-1.02
0.005
SCA+ AICA
10 (7.52%)
1 (1.96%)
1.04-1.58
0.155
SCA+BA
3 (2.26%)
1 (1.96%)
0.59-1.84
0.902
SCA+AICA+PV
1 (1.12%)
3 (5.88%)
0.06-1.87
0.033
SCA+BA+PV
1 (1.12%)
2 (3.92%)
0.09-2.27
0.129
SCA: superior cerebral artery; AICA: anterior inferior cerebellar artery; BA: basilar artery; PV: petrosal vein.
Table 6. Multiple regression analyses of intra-operative vessel compression of patients with or without post-operative recurrence. Parameters
B
OR (95% CI)
P
SCA+ PV
5.69
295.17 (33.78-2579.03)
< 0.001
AICA+ PV
25.547
0.998
BA+ PV
25.547
0.998
SCA +AICA +PV
25.547
0.998
SCA: superior cerebral artery; AICA: anterior inferior cerebellar artery; BA: basilar artery; PV: petrosal vein.
Table1: BNI pain score BNI pain score
Description
I
No pain
II
Occasional pain, not taking any medications
III
Some pain, adequately control with medications
IV
Some pain, not adequately controlled with medications
V
Sever pain or no relief
Microvascular decompression (MVD) trigeminal neuralgia (TN) superior cerebellar artery (SCA) petrosal vein (PV) magnetic resonance imaging (MRI) Barrow Neurological Institute (BNI) anterior inferior artery (AICA)
S1878-8750(20)30100-5
DOI:
https://doi.org/10.1016/j.wneu.2020.01.082
Reference:
WNEU 14112
To appear in:
World Neurosurgery
Received Date: 21 November 2019 Revised Date:
10 January 2020
Accepted Date: 11 January 2020
Please cite this article as: Shi J, Qian Y, Han W, Dong B, Mao Y, Cao J, Guan W, Zhou Q, Risk factors for outcomes following microvascular decompression for trigeminal neuralgia, World Neurosurgery (2020), doi: https://doi.org/10.1016/j.wneu.2020.01.082. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Elsevier Inc. All rights reserved.
Title Page
Risk factors for outcomes following microvascular decompression for trigeminal neuralgia
Jia Shi1*, Yitao Qian1*, Wei Han1, Bo Dong1, Yumin Mao1, Jiachao Cao1, Wei Guan1, Qiang Zhou1
1. Department of Neurosurgery, The Third Affiliated Hospital of Soochow University, Changzhou, China.
*. These authors contributed equally to this work.
Correspondence to: Qiang Zhou. E-mail: [email protected]. Address: No.185, Juqian Street, Changzhou, Jiangsu, 213003, China.
Risk factors for outcomes following microvascular decompression for trigeminal neuralgia
Abstract Background: Microvascular decompression (MVD) is the most effective long-term surgical treatment for trigeminal neuralgia (TN) patients. The risk factors for poor pain control following MVD surgery are not fully understood. Methods: A total of one hundred eighty-four patients were enrolled from patients with typical TN who underwent MVD at our institution between 1/3/2008 and 1/3/2016. The data were collected using electronic operative records and case notes and were retrospectively analyzed. Patients were followed up at the outpatient department or by telephone at a minimum of three months and at a maximum of forty-eight months. Results: 184 patients were enrolled in the study; 72.3% of patients achieved freedom from pain after MVD, 27.7% experienced poor pain control, with follow-up at a minimum of 3 months and at a maximum of 48 months. Risk factors for poor pain control after MVD according to binary logistic regression and ROC analysis included younger age (OR: 0.90; 95% CI: 0.82-0.99; P = 0.028; AUC=0.774); poor preoperative pain control (BNI score > IV) (OR: 52.03; 95% CI: 6.44-420.16, P < 0.001; AUC=0.858); intraoperatively detected multivessel compression (OR: 2.49; 95% CI: 3.10-46.59, P < 0.001; AUC=0.871). Furthermore, combined compression of the superior cerebellar artery (SCA) and the petrosal vein (PV) was an independent risk factor predicting a poor outcome following MVD (OR: 5.69; 95% CI: 33.78-2579.03, P < 0.001; AUC=0.812). Conclusions: Younger patients with TN had worse long-term pain outcomes following MVD. Additional factors associated with postoperative recurrence included poor preoperative pain control (BNI score > IV) and multivessel compression. Furthermore, SCA combined with PV was confirmed to be associated with a worse outcome.
Key words: trigeminal neuralgia, microvascular decompression, risk factors
Introduction Trigeminal neuralgia (TN) is a debilitating facial pain syndrome characterized by episodic pain in the branches of the trigeminal nerve1. The pain episodes are generally described as debilitating, severe, and sharp, although the typical episode may last only seconds to minutes1, 2. According to the Burchiel classification system, when lancinating facial pain predominates, it is described as “Burchiel type 1” or typical facial pain. Conversely, atypical TN is described as a “Burchiel type II”, which is a described as a constant burning pain accompanying the lancinating pain3. The first-line therapy for TN patients is pharmacological treatment with medications including carbamazepine or other antiepileptic drugs such as pregabalin, gabapentin, or oxcarbazepine4-6. Surgical therapy can provide long-lasting pain relief to TN patients whose treatment is limited by medication side effects or a small therapeutic window4. Microvascular depression (MVD) is currently acknowledged as the best surgical treatment for typical TN with vascular compression, especially with arterial compression7-9. With regard to MVD surgery, long-term pain outcomes are generally favorable, but there are still significant differences in outcome rates throughout the literature, attributed to variabilities in patient epidemiology, clinical data, and anatomical vascular compressions or differences pertaining to the study center itself. For example, several studies demonstrated that pain-free rates as high as 90% or more could be achieved following MVD surgery10-12, while other studies only identified rates of 50-70%13, 14. Moreover, although a few systematic reviews have evaluated risk factors for the recurrence of MVD, none have quantitatively analyzed these risk factors or predictors15-18. Therefore, studies regarding recurrence rates and predictors for freedom from pain after MVD remain uncertain. In this study, the goal was to determine the recurrence rates and risk factors for a poor pain outcome following MVD surgery. Our results may provide a significant addition to the current literature examining the predictors for MVD efficacy, thus
helping patients and clinicians make appropriate choices prior to intervention.
Materials and methods Setting and participants The study was a cross-sectional, case-control, single-center and retrospective study. The patients surveyed in this study were recruited from a group of patients who underwent MVD for TN in the Third Affiliated Hospital of Soochow University between March 2008 and March 2016. The study was approved by the Ethics Committee of the Third Affiliated Hospital of Soochow University. Patients with TN meeting the following criteria were enrolled: (1) at least 18 years of age at the time of surgery and (2) had typical (type I) TN with evidence of neurovascular compression (arterial and/or venous) on preoperative imaging. Patients who had undergone prior ablative or MVD procedures were excluded from the research study. A total of two hundred thirty-six patients were screened for eligibility. Twenty-two were excluded because they did not have evidence of neurovascular compression on preoperative imaging, while ten had atypical TN. Twenty were excluded because they had no follow-up information available. Finally, one hundred eighty-four patients were enrolled in the study (Figure 1). Each patient involved in this study signed an informed consent form after inclusion of the retrospective study. Data collection Prior to receiving MVD treatment, every patient in this group had a preoperative magnetic resonance imaging (MRI) scan of the brain according to the protocol developed at the Walton Center19, and all MRIs were reported by a neuroradiologist and reviewed by the operating neurosurgeon. Intraoperative findings at the time of exploration were noted and recorded in operative records at the time of surgery. Postoperative outcomes were assessed based on the Barrow Neurological Institute (BNI) pain intensity scale by an independent neurologist who was blinded to the patients’ preoperative pain scores. Recurrence was defined as an increase in pain requiring the introduction of new medication after successful pain relief following the
initial MVD. The interval of recurrence was defined as more than one month after operation. If The pain was not relieved within one month, it would be regarded as invalid20. The BNI score for all patients in this cohort was III-V prior to MVD; after MVD, BNI scores of I-II indicated a lack of recurrence, and scores of III-V indicated recurrence. According to a previous study, we categorized outcomes into good pain control (BNI scores I-II) (nonrecurrence group) and poor pain control (BNI scores III-V) (recurrence group)21. For further analysis of the connection between preoperative and postoperative BNI scores, the preoperative BNI score was subdivided into moderate pain control (BNI score III-IV) and poor pain control (BNI score V). The patients after microvascular decompression would be routinely reexamined with MRI, including the patients with recurrence. Patients were followed up at the outpatient department or by telephone at a minimum of three months and at a maximum of forty-eight months. The data were collected using electronic operative records and case notes and were retrospectively analyzed. Statistical analysis The statistical analysis was performed using SPSS 24.0. Subjects with missing information were excluded from the relevant portion of the analysis. Continuous data are presented as the mean ± SD and were compared using Student’s t tests. The categorical data are presented as percentage frequencies (%) and were compared using the chi-squared test. Binary logistic regression analyses were used to determine the factors associated with postoperative recurrence. The results are presented as ORs and 95% confidence intervals (CIs). We used a P value < 0.05 to indicate statistical significance. Results Clinical characteristics of patients with TN There were 184 patients with TN included in our study; 133 had good pain control (BNI score I-II, nonrecurrence group), and 51 had poor pain control (BNI score III-V, recurrence group). Table 1 and Table 2 show the clinical characteristics of the study patients. The mean age of patients in the recurrence group was younger than that of those in the nonrecurrence group (P < 0.001, Table 2). The BNI scores for patients
prior to MVD were III-V, with the following distribution: III (5.98%), IV (55.98%) and V (38.04%). As the preoperative BNI scores were subdivided into moderate pain control (BNI scores III-IV) and poor pain control (BNI score V), the number of patients with BNI score V in the recurrence group was greater than that in the nonrecurrence group (P < 0.001, Table 2). The number of intraoperatively identified compressive vessels was also analyzed as follows: single vessel (60.33%), double vessel (35.87%, including artery and vein) and triple vessel (3.80%). The number of patients with multivessel compression in the recurrence group was larger than that in the nonrecurrence group (P < 0.001, Table 2). No significant differences were found between the two groups with regard to the other parameters. Table 3 shows the risk factors associated with recurrence according to binary logistic regression analysis. Younger age (OR: 0.90; 95% CI: 0.82-0.99; P = 0.028), poor pain control prior to MVD (BNI score V, OR: 52.03; 95% CI: 6.44-420.16, P < 0.001) and intraoperatively identified multivessel compression (OR: 2.49; 95% CI: 3.10-46.59, P < 0.001) were significantly associated with recurrence in TN patients after MVD surgery. Furthermore, the ROC curve showed that younger age (95% CI: 0.68-0.86, AUC=0.774), intraoperatively determined multivessel compression (95% CI: 0.79-0.95, AUC=0.871) and preoperative BNI pain score (V) (95% CI: 0.79-0.93, ROC=0.858) could be specific predictors of recurrence following MVD surgery; the combination of all three resulted in a higher diagnostic value with regard to recurrence (95% CI: 0.94-0.99, AUC=0.968) (Figure 2). Association
of
intraoperatively
identified
vascular
compression
and
postoperative recurrence The most common intraoperative findings were the presence of vascular compression (including both artery and vein) in conflict with the trigeminal nerve. Table 4 shows the compressive vessels during the MVD process. The most common offending vessel was the superior cerebellar artery (SCA, 53.80%), followed by the combination of the SCA and the petrosal vein (PV, 24.46%) and the combination of the SCA and the anterior inferior artery (AICA, 5.98%). Patients with a compressed combination of an artery and a vein were more likely to experience recurrence (Table
5): SCA+PV (P < 0.001), AICA+PV (P = 0.005), basilar artery (BA) +PV (P = 0.005) and SCA+AICA+PV (P = 0.033). Further risk factors identified via binary logistic regression analysis showed that only SCA+PV (OR: 5.69; 95% CI: 33.78-2579.03, P < 0.001) was an independent risk factor for recurrence following MVD surgery. The ROC curve analysis also identified SCA+PA compression (95% CI: 0.81-0.91, AUC=0.812) as a specific predictor of recurrence after MVD surgery (Figure 2). Discussion MVD for patients suffering from TN is the most effective method of managing patients’ symptoms and is currently the only procedure that can arguably provide a cure22. However, previous studies demonstrated that the rate of recurrence of TN in patients after successful MVD is as high as 14% at 1 year and may rise as high as 20-40% at 10 years23. Therefore, it is of great importance to predict risk factors for the recurrence of TN in patients after MVD surgery. In this study, our results suggested that older patients have better pain outcomes following MVD than younger patients. Additional factors, including preoperative BNI pain score and intraoperatively detected multivessel compression, were confirmed to have positive associations with poor pain outcomes. The relationship between age and MVD efficacy in our studies is consistent with the findings in previous studies. A study examining the outcomes in patients 60 years and older with TN following MVD found that this older age group had relatively better pain outcomes21. A systematic review reported that while younger and older patients have similar initial success rates following MVD, older patients have lower rates of recurrence24. There are several possible reasons for this. First, TN has a close relationship with arteriosclerosis. The development of arteriosclerosis gradually leads to vascular tortuosity, deformation and even displacement, which may be the major cause of arterial neurovascular compression10. This association may explain the relationship between age and TN incidence, given the increasing prevalence of atherosclerosis with increasing age25. Second, atherosclerosis is positively correlated with age, which may contribute to the increased incidence of arterial neurovascular compression observed in older TN patients, while nerve compression caused by veins
is more common in younger patients26. From the perspective of anatomy, the variability of the venous system is greater, and the relationship between blood vessels and nerves is rather more complex, leading to the potential for operative difficulty, insufficient decompression, and a higher rate of overall recurrence27. Third, the improved outcomes in older patients may be partially explained by operative considerations. Compared to younger patients, cerebellar atrophy is more evident in older patients, facilitating cerebellopontine angle exposure26. Increased exposure may improve the ability to fully inspect and decompress nerves, free the responsible blood vessels, and achieve better decompressive efficacy and shorter operative durations28. Current studies on the relationship between preoperative pain symptoms and prognosis have mainly focused on the Burchiel type I and Burchiel type II classification. A systematic review and meta-analysis including 3897 patients from 46 studies demonstrated that Burchiel type II patients were more prone to recurrence following MVD surgery, and the recurrence rate was nearly twice that in type I patients29. However, few studies have focused on the relationship between the preoperative BNI pain score and MVD efficacy. In our results, binary logistic regression and ROC analysis confirmed that poor pain control prior to MVD (preoperative BNI pain score V) was an independent and specific risk factor for recurrence after MVD surgery, which may be attributed to the fact that the pain levels in TN patients are often associated with the number or extent of vascular and nerve compression, especially when involving venous vessels, which are associated with difficulty in obtaining adequate decompression and high recurrence rate30. According to the ignition hypothesis2, TN results from specific abnormalities of trigeminal afferent neurons in the trigeminal root or ganglion, and even the compression of a tiny blood vessel is enough to cause clinical symptoms2. Actually, the mechanisms underlying the correlation between a poor preoperative BNI score and recurrence after MVD are still uncertain, and large-scale and multicenter clinical studies are warranted for further analysis in the future. Previous studies clearly showed that vascular loop-related TNs are mainly caused by branches emanating from the distal basilar artery (SCA and AICA are the most
commonly responsible vessels)29. Our study also showed that nearly 53.80% of the cases had the usual SCA offenders, and 24.46% involved the accompanying veins. Binary logistic regression and ROC analysis confirmed that compared to single vessel compression, intraoperatively detected multivessel compression was an independent and specific predictor of postoperative recurrence. Further analysis of the compressive vessels showed that TN patients with the combination of an artery and PV had poor pain control after surgery, which was consistent with the findings in previous reports30. A possible explanation may be that compared to arteries, veins are firmly adhered to nerves and the brainstem, and they are less mobile, leading to difficulty in adequate decompression. In addition, the thickened arachnoid membrane around veins and thin and fragile venous wall are the anatomical factors that can easily lead to massive hemorrhage, operative difficulty and a higher recurrence rate31. Some scholars believe that intraoperative disconnection of the PV can better expose the root entry zone (REZ) of TN, helping the operators adequately decompress the TN without severe postoperative complications32. However, other researchers hold different opinions. Zhao et al believed that the veins should be preserved as much as possible during the operation33. Damage to large veins (diameter over 2 mm) may lead to serious complications, such as cerebral hemorrhage, infarction, edema, and even death. In our opinion, venous drainage should be maintained as smoothly as possible instead of directly disconnecting veins34. To determine the optimal management of veins during MVD, a larger number of cases, including various types of veins that block the approach to or compress the TN, should be further studied. In our study, we elaborated on the effects of different types of vascular compression on postoperative recurrence, which may provide an important addition to the limited existing literature examining the relationship between vessel compression and outcomes following MVD. Conclusions In this study, younger patients had worse long-term pain outcomes following MVD than older patients. Additional factors associated with postoperative recurrence included poor preoperative pain control (BNI score > IV) and intraoperatively detected
multivessel compression. Furthermore, with regard to multivessel compression, SCA combined with PV was confirmed to be associated with a worse outcome. Our study may provide a perioperative suggestion for TN patients undergoing MVD surgery, which will help physicians appropriately counsel patients prior to the intervention and help clinicians make the appropriate choice tailored to each individual. Funding No Competing interests On behalf of all authors, the corresponding author states that there is no conflict of interest. Ethical approval and consent to participate This study was approved by the Regional Ethics Committee of the Third Affiliated Hospital of Soochow University and all patients signed informed consents. Authors’ contributions Qiang Zhou and Wei Guan were major contributors in writing and in a review of the manuscript. Jia Shi collected patient data and was involved in writing and in a review of the manuscript. YiTao Qian and Wei Han were in charge of data analysis. Yumin Mao, Bo Dong and Jiachao Cao were involved in patient management and review of the manuscript. All authors read and approved the final manuscript. Consent for publication Informed consent was obtained from the patient and is attached to the patient records in the hospital files. Acknowledgements No applicable. References 1.
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Figure legends Figure 1: Participant flow diagram. Figure 2: The ROC curve for age (A), preoperative pain control (B) and intraoperatively detected multivessel compression (B) for outcomes following MVD surgery. MVD: microvascular decompression. The ROC curve of SCA combined with PV for outcomes following MVD surgery (C). SCA: superior cerebral artery; PV: petrosal vein.
Table 1. Clinical characteristics of study patients with TN. Parameters Sex (% male)
116 (63.04%)
Age (mean ± SD) Hypertension (%)
59.86 ± 10.81
Diabetes (%)
10 (5.43%)
Side (% left)
80 (43.48%)
79 (42.93%)
Pain location Single division
83 (45.11%)
Double division
86 (46.74%)
Triple division
15 (8.15%)
Preoperative disease duration (mean ± SD years)
4.42 ± 4.40
Preoperative BNI pain score III
11 (5.98%)
IV
103 (55.98%)
V
70 (38.04%)
Intraoperative vascular compression
58 (31.52%)
Single vascular
111 (60.33%)
Double vascular
66 (35.87%)
Triple vascular
7 (3.80%)
Table 2. Clinical characteristics of study patients with or without post-operative recurrence. Parameters
Good pain
Poor pain
95% CI
P
control
control
Sex (% male)
83 (62.40%)
33 (64.71%)
0.81-1.17
0.772
Age (mean ± SD) Hypertension (%)
67.50 ± 6.36
52 ± 16.26
-11.66-(-6.24)
< 0.001
61 (45.86%)
18 (54.55%)
0.74-1.06
0.195
Diabetes (%)
6 (4.51%)
4 (7.84%)
0.73-2.03
0.372
Side (% left)
57 (30.98%)
23 (45.10%)
0.81-1.17
0.784
Pain location (single division)
64 (48.12%)
19 (37.25%)
0.95-1.35
0.185
Preoperative disease duration
4.50 ± 4.80
4.24 ± 3.17
-1.70-1.17
0.720
22 (16.54%)
48 (94.12%)
2.19-4.39
< 0.001
8 (6.02%)
43 (84.31%)
2.24-5.61
< 0.001
(mean ± SD years) Preoperative BNI pain score (> IV) Intraoperative vascular compression (% multivessel)
Table 3. Multiple regression analyses of clinical characteristics of patients with or without postoperative recurrence. Parameters
B
OR (95% CI)
P
Age
-0.105
0.90 (0.82-0.99)
0.028
Preoperative BNI pain score (> IV)
3.26
26.14 (4.44-153.80)
< 0.001
Intraoperative vascular compression
2.69
14.66 (4.14-51.85)
< 0.001
(% multivessel)
Table 4. Compressive vessels during the process of MVD. Compressive vessels
Number (%)
SCA
99 (53.80%)
AICA
3 (1.63%)
BA
3 (1.63%)
PV
3 (1.63%)
SCA+ PV
45 (24.46%)
AICA+ PV
3 (1.63%)
BA+ PV
3 (1.63%)
SCA+ AICA
11 (5.98%)
SCA+BA
7 (3.80%)
SCA+AICA+PV
4 (2.17%)
SCA+BA+PV
3 (1.63%)
SCA: superior cerebral artery; AICA: anterior inferior cerebellar artery; BA: basilar artery; PV: petrosal vein.
Table 5. Association of intra-operative vessel compression and post-operative recurrence. Parameters
Good pain
Bad pain
control
Control
95% CI
P
SCA
75 (56.39%)
24 (47.06%)
0.93-1.35
0.215
AICA
3 (3.26%)
0 (0.00%)
1.27-1.53
0.279
BA
3 (2.26%)
0 (0.00%)
1.27-1.53
0.279
PV
3 (2.26%)
0 (0.00%)
1.27-1.53
0.279
SCA+ PV
7 (5.26%)
38 (74.51%)
0.09-0.34
< 0.001
AICA+ PV
0 (0.00%)
3 (5.88%)
0.00-1.02
0.005
BA+ PV
0 (0.00%)
3 (5.88%)
0.00-1.02
0.005
SCA+ AICA
10 (7.52%)
1 (1.96%)
1.04-1.58
0.155
SCA+BA
3 (2.26%)
1 (1.96%)
0.59-1.84
0.902
SCA+AICA+PV
1 (1.12%)
3 (5.88%)
0.06-1.87
0.033
SCA+BA+PV
1 (1.12%)
2 (3.92%)
0.09-2.27
0.129
SCA: superior cerebral artery; AICA: anterior inferior cerebellar artery; BA: basilar artery; PV: petrosal vein.
Table 6. Multiple regression analyses of intra-operative vessel compression of patients with or without post-operative recurrence. Parameters
B
OR (95% CI)
P
SCA+ PV
5.69
295.17 (33.78-2579.03)
< 0.001
AICA+ PV
25.547
0.998
BA+ PV
25.547
0.998
SCA +AICA +PV
25.547
0.998
SCA: superior cerebral artery; AICA: anterior inferior cerebellar artery; BA: basilar artery; PV: petrosal vein.
Table1: BNI pain score BNI pain score
Description
I
No pain
II
Occasional pain, not taking any medications
III
Some pain, adequately control with medications
IV
Some pain, not adequately controlled with medications
V
Sever pain or no relief
Microvascular decompression (MVD) trigeminal neuralgia (TN) superior cerebellar artery (SCA) petrosal vein (PV) magnetic resonance imaging (MRI) Barrow Neurological Institute (BNI) anterior inferior artery (AICA)