ORIGINAL ARTICLE

Masticatory Muscles Dysfunction after CT-guided Percutaneous Trigeminal Radiofrequency Thermocoagulation for Trigeminal Neuralgia: A Detailed Analysis Shuyue Zheng, MM*; Baishan Wu, MD*; Ying Zhao, MD†; Xiaoyu Wang, MM†; Xuanying Li, MD‡; Liqiang Yang, MM*; Mingwei He, MD*; Jianning Yue, MM*; Jiaxiang Ni, MD* *Department of Pain Management, Xuanwu Hospital, Capital Medical University, Beijing; † Department of Stomatology, Xuanwu Hospital, Capital Medical University, Beijing; ‡ The University of Hong Kong – Shenzhen Hospital, Shenzhen, China

& Abstract Objective: The aim of this study was to investigate the severity and the natural course of masticatory muscles weakness that developed after CT-guided percutaneous trigeminal radiofrequency thermocoagulation (PT-RFT) for the treatment of idiopathic trigeminal neuralgia (ITN). Methods: Twenty-seven patients with ITN were treated by CT-guided percutaneous trigeminal radiofrequency thermocoagulation. Each patients’ occlusal function and surface electromyographic (sEMG) activity of the ipsilateral anterior temporalis (TA) and masseter muscles (MM) at mandibular postural position (MPP), and during a fast maximum voluntary clenching (MVC) from MPP to intercuspal position (ICP), were simultaneously recorded by the T-Scan III system and Bio-pak sEMG III system before (baseline), 3 days, 3 months, and 12 months after procedure. The incidence, degree, and

Address correspondence and reprint requests to: Jiaxiang Ni, MD, No. 45 Changchun Street, Xicheng District, Beijing 100053, China. E-mail: [email protected]. Shuyue Zheng & Baishan Wu contributed equally to this work. Submitted: January 21, 2014; Revised July 13, 2014; Revision accepted: July 21, 2014 DOI. 10.1111/papr.12247

© 2014 World Institute of Pain, 1530-7085/14/$15.00 Pain Practice, Volume 15, Issue 8, 2015 712–719

prognosis of masticatory muscles dysfunction related to trigeminal nerve motor-branch injury were analyzed. Results: Three days and 3 months after procedure, both the occlusal symmetry and the sEMG activity of ipsilateral TA and MM became significantly decreased compared to the baseline (P < 0.05). However, they demonstrated a gradual improvement toward preoperative values in follow-up, returning to complete in 23 patients at 12 months after procedure. None reported permanent masticatory paralysis. Pain relief was most significant on the third day after procedure. At the final clinical visit, a pain-free status was observed in 25 patients (92.6%). Meanwhile, the intensity of facial dysesthesia was mildest, whereas there were statistic differences compared with baseline. Conclusion: CT-guided PT-RFT for ITN remains an effective and safe surgical procedure, but there is a high rate of temporary masticatory dysfunction during a short time after procedure, appearing to be reversible in a period of 12 months. & Key Words: percutaneous trigeminal radiofrequency thermocoagulation, idiopathic trigeminal neuralgia, masticatory dysfunction, CT-guidance

INTRODUCTION Idiopathic trigeminal neuralgia (ITN) is a common neuropathic pain disorder characterized by recurrent

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episodes of intense, lancinating pain localized to areas of the face innervated by the trigeminal nerve1,2. For lack of certainty regarding the etiology and pathophysiology, the treatment is challenging despite the numerous available options3. Surgical management need to be considered when patients are resistant or intolerant to medications4. Percutaneous trigeminal radiofrequency thermocoagulation (PT-RFT) is one of the most commonly used surgical procedures because of short hospitalization, avoidance of endotracheal anesthesia, and successful short-term and long-term results with low morbidity and mortality rates5, 6. Although clinical studies have shown that PT-RFT is a safe and effective alternative7, there are still some complications reported, such as masseter weakness with an incidence from 2.1% to 12.2%7–12. It is suspected that masticatory weakness is correlated with motor-branch injury during the procedure, even though final location of the electrode tip is proved by patients’ response to sensory and motor testing before thermocoagulation13. However, no quantitative evaluations of this complication have been reported in prior studies, expect for patients’ complaints. Therefore, this study was conducted to investigate the severity of the trigeminal nerve motor-branch injury with a follow-up of the natural course of the corresponding masticatory muscles weakness after CT-guided PT-RFT by serial quantitative masticatory function examinations using T-scan and Bio-pak system.

METHODS Subjects Institutional research ethics committee approval was obtained for the study. Twenty-seven patients with the diagnosis of ITN were recruited with informed consent. ITN was diagnosed according to the International Classification of Headache Disorder-II criteria2. Other inclusion criteria were as follows: (1) Mandibular nerve distribution was affected, (2) no satisfactory pain relief with medical treatment, (3) in accordance with radiofrequency operative indications. Exclusion criteria were as follows: (1) past invasive treatment, (2) serious cardiopulmonary dysfunction, (3) coagulation dysfunction, (4) severe tooth wear14; and/or oral–maxillofacial disease, (5) the habit of long-time hemimastication.

Examination Procedure T-Scan III (Tekscan Inc., South Boston, MA, U.S.A.) is a computerized occlusal analysis system which has a digital sensor. The sensor foils used have a layer thickness of 100 lm, which embeds a grid of conductive lines. Voltage drops in the conductive lines result from any force exerted on the foil. These voltage changes are measured and digitalized by the T-Scan software to record a sensor-loading graph numerically and visually displaying a 2-dimensional representation of occlusion15 (Figure 1). It can be recorded simultaneously with surface electromyographic (sEMG) activity. Bio-pak III (Bio-Research Associates Inc., Milwaukee, WI, U.S.A.) is a sEMG recording system interfaced with a computer, performing with surface electrodes. According to Ferrario’s description, the electrodes were placed on the skin overlying the anterior temporalis (TA) vertically along the anterior muscular margin, and parallel to muscular fibers for the masseter muscles (MM)16. A plate ground electrode was secured to the back of neck, over the 7th cervical vertebral segment17. All examinations were performed by the same dentist. Each subject was asked to sit upright on a chair with the head unsupported, the trunk perpendicular to the floor, both feet on the floor, hands resting on the lap, and looking forward18. Jaw posture tasks were performed 3 times by each subject to record occlusion and sEMG values during different conditions of intermaxillary relationship19. These included the following: (1) mandibular postural position (MPP), with no occlusal contact, (2) a 3-second period of maximum voluntary clenching (MVC) from MPP to intercuspal position (ICP) with 3 seconds relaxation between each clench. For each recording, the following parameters were calculated automatically by the combined system: (1) spatial distribution as a percentage of occlusal force in maximum occlusal contacts, this parameter could describe the distribution to the right and left sides in relation to the middle20, (2) the sEMG values of the ipsilateral TA and MM at MPP, (3) the peak values of sEMG during a fast MVC from MPP to ICP; and (4) the sEMG symmetry of bilateral TA and MM (Figure 2). Operative Technique and Postprocedure Follow-up All procedures were performed by a pain surgeon with expertise in PT-RFT under CT-guidance. Patients were placed in a supine position with their head overhanging

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Figure 1. Sensor-loading graph of TScanIII. The T-scan software automatically chose a 2 dimensional image with maximum occlusal contacts. The digital image illustrated occlusal force distribution with insertion of the percentage of force distribution in each contact area and represented the left/right symmetry of occlusion.

Figure 2. Bio-pak surface electromyographic (sEMG). EMG activity can be recorded simultaneously with T-scan results. Bio-pak software recorded sEMG values during a 3 seconds period of MVC from MPP to ICP for 3 times with 3 seconds between each clench, and automatically calculated the averaged sEMG values of TA and MM. sEMG, surface electromyographic; MPP, mandibular postural position; ICP, intercuspal position; MVC, maximum voluntary clenching; TA, anterior temporalis; MM, masseter muscles.

the table. Electrocardiography, blood pressure, and oxygen saturation monitoring were initiated. Thirty minutes before procedure, patients received an intravenous injection of atropine (0.01 mg/kg) and 0.05 mg of fentanyl. CT scanning determined the percutaneous insertion route, and the insertion point was marked correspondingly. Following sterilization and local anesthesia with 0.5% lidocaine, a 22-G (15 cm, with a 5-mm active tip, Cosman TIC-C5 electrode; Cosman Medical, Burlington, MA, U.S.A.) insulated needle was advanced slowly across the designed angle and route to the foramen ovale. When the depth of the needle was equal

to that measured in the predetermined route, a repeat CT scan was performed to certify the proper location of the needle tip. After verification, sensory (50 Hz) and motor (2 Hz) test stimulation was applied to adjust the needle position until paresthesia was elicited in the affected area21. Patients were administered intravenous anesthesia with propofol (1.5 to 2.0 mg/kg), which could be supplemented (0.05 mg/kg) according to the depth of anesthesia. All patients were thermally coagulated with radiofrequency at 75°C for 120 second in 3 cycles. The patients were discharged 48 hours after the procedure (per our institutional policy).

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Evaluated Measures All subjects were assessed for intensity of facial pain, facial dysesthesia, and masticatory muscles function at baseline (T0), 3 days (T1), 3 months (T2), and 12 months (T3) after procedure. Pain intensity was rated using visual analog scale (VAS, 0 = no pain and 10 = worst pain). Pain relief was graded excellent if the patient was completely pain-free with no medications, good if the patient was distinct pain-free with no medication, fair if the patient had mild pain and needed carbamazepine (≤ 200 mg/day), and poor if the patient still had intolerable pain and needed carbamazepine (> 200 mg/day). A successful treatment was defined as excellent or good pain relief, while recurrence was defined as fair or poor pain relief. Intensity of facial hypoesthesia was also rated by VAS score (0 = hypoesthesia and 10 = worst hypoesthesia). The occlusal symmetry was assessed by the distributing percentage of occlusal force on left or right (0 = symmetrical force distribution and 6 = complete asymmetrical force distribution). Statistical Analysis The repeated-measures analysis of variance (ANOVA) test was used for comparison, followed by Bonferroni test for pairwise multiple comparisons. Level of significant was set at 5%. All analysis was completed using SPSS version 19.0 (SPSS Inc., Chicago, IL, USA).

RESULTS Between March and November 2012, 27 PT-RFT were performed for 27 patients with ITN. The patient characteristics were shown in Table 1. All patients completed the follow-up evaluations. All procedures were performed successfully under CT-guidance. The immediate success rates at 3 days after procedure were 100%, and a pain-free status was still observed in 25 patients (92.6%) at 12 months. The Table 1. Characteristics of Patients (Mean  SD) Parameter

Patients (n = 27)

Age (years) Gender (female:male) Duration (years) Lateralization (L:R) Division of the trigeminal nerve, n (%) V3 V2 + V3 V1 + V2 + V3

56.30  12.85 19:8 4.87  3.85 11:16 9 (33.3) 13 (48.2) 5 (18.5)

efficacy in pain relief was most significant at the 3-day follow-up visit compared with baseline (P < 0.05); however, the mean VAS score did not differ between 3 follow-up visits after procedure (Table 2). No major complications (keratitis, anesthesia dolorosa, and hearing impairment) were observed, expect that facial dysesthesia was experienced in all patients, sustaining a period after procedure. The intensity of dysesthesia was mildest (2.26  0.90) at 12 months, decreasing to a tolerable level, significantly different from 3 days and 3 months values after procedure (Table 2). At the 3-day post-RFT examination, the occlusal symmetry and the sEMG values of ipsilateral TA and MM at MPP were diminished, differed from baseline values (P < 0.05). However, they demonstrated a gradual improvement toward the normal values, returning 12 months after procedure (Table 3, Figure 3). The peak values of sEMG during a fast MVC from MPP to ICP were significantly changed during the follow-up examinations (Table 3, Figure 4). Before procedure, normal values were observed in all patients. Three days after procedure, a parallel decrease was shown in all patients. Eleven of 27 patients experienced difficulty in chewing on the ipsilateral side on questioning. Three months postprocedure, the values moderately increased in more than 50% patients. Moreover, there was a continue increase toward baseline values in the followup evaluations. Twelve months after procedure, there was no significant difference compared with baseline (P < 0.05), and the peak values resolved completely in 23 patients. During a fast MVC from MPP to ICP, the baseline of sEMG symmetry rate was 94.7%, decreased to 13.8% and 54.9%, respectively among 3 days and 3 months in follow-up. However, it also returned to normal 12 months after procedure.

DISCUSSION Our findings suggested that all of the 27 patients who underwent PT-RFT for ITN experienced immediate Table 2. Visual Analog Scales Before and After Treatment (Mean  SD)

Pain VAS Hypoesthesia VAS

T0 (Baseline)

T1

T2

T3

7.96  1.14 0

0.08  0.28* 8.26  0.76*

0.04  0.20* 5.93  0.83*†

0.04  0.20* 2.26  0.90*†

*P < 0.05, when compared to the baseline. P < 0.05, when compared to the T1. †

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Table 3. Occlusal Symmetry and EMG of Masticatory Muscles (Mean  SD) T0 (Baseline) Occlusal symmetry EMG at MPP (lV) TA MM EMG at ICP clenching (lV) TA MM EMG symmetry rate (%) TA-TA MM-MM

T1

T2

T3 †

1.29  0.16†

1.24  0.18

5.50  0.34*

4.58  0.37*

2.31  1.37 1.45  0.90

0.59  0.33* 0.44  0.39*

1.21  0.64*† 0.75  0.50*

2.28  1.35† 1.42  0.86†

92.33  34.21 137.86  30.19

14.05  2.58* 8.15  3.35*

52.89  17.24*† 54.79  12.26*†

91.61  34.02† 137.15  30.28†

94.74  2.36 94.07  2.22

13.78  3.09* 4.93  2.57*

54.89  2.22*† 43.59  3.03*†

93.96  1.83† 93.59  2.27#

*P < 0.05, when compared to the baseline. † P < 0.05, when compared to the T1. EMG, electromyographic; MPP, mandibular postural position; ICP, intercuspal position; TA, anterior temporalis; MM, masseter muscles.

successful treatment (Table 2). In the long-term followup of 27 patients, 25 patients (92.6%) showed excellent or good pain relief with only 2 patients suffering a recurrence of pain. Three days and 3 months after procedure, the occlusal symmetry, the sEMG activity of TA, and MM became significantly decreased compared with the baseline (P < 0.05). However, they demonstrated a gradual improvement toward preoperative values in follow-up, returning 12 months postoperatively (Table 3, Figures 3 and 4). All 27 patients experienced variable facial dysesthesia that mostly subsided within 12 months after procedure. Meanwhile, the VAS score of facial dysesthesia was increased in the postoperative follow-up visits compared with baseline. Three days after procedure, it increased to 8 (Table 2). However, it showed a gradual downtrend, as the score decreased to 2 during last follow-up visit, and all patients with dysesthesia were regarded as a mild disturbance. T-Scan III system was a computer-based assessment of occlusal conditions in centric relation. It automatically chose the still image with maximum occlusal contacts and recorded the percentage force distribution in each contact area to illustrate the spatial distribution of occlusal force18. In this study, it was possible to make good estimates about the occlusal symmetry by calculating the left/right distributing percentage of occlusal force. Stomatology studies22 demonstrated that both sides achieved the maximum occlusal contact at the same time as a necessary component of ideal occlusion. Trigeminal motor-branch injury could decrease the velocity of nerve conduction, resulting in slower contraction of the innervated masticatory muscles23. Thus, the ipsilateral maximum occlusal contact was later than the contralateral, causing the occlusal asymmetry. Our results showed 3 days and 3 months postoperatively,

the occlusal symmetry increased to 5.50 and 4.58 respectively, compared with 1.24 preoperatively, indicating that it was reduced after procedure. This could be associated with slowed conduction velocity of trigeminal nerve motor-branch. However, after 12 months, it returned to 1.29, and there was no significant differences compared with baseline, prompting PT-RFT for ITN could impair trigeminal motor nerve, whereas the injury should be temporary and reversible. Bio-pak system was a commercially available device with 8-channel electromyograph, from which electrical activity could be obtained to access the masticatory muscles function18. The sEMG values at MPP described the electrical activity of jaw-closing muscles during the process of contraction to resist the gravity of mandibular. The peak values of sEMG during a fast MVC from MPP to ICP were defined as the greatest energy electrical signals released during each masticatory muscles contraction, it could reflect the strength of muscle contraction, as a form of muscle work. Recent evidence24,25 suggested that no significant difference was found with EMG values at MPP or ICP clenching among masticatory muscles. Therefore, the values of TA and MM could be perceived as a representation of masticatory function. Compared to baseline values, MPP values decreased significantly 3 days and 3 months after procedure, which would contribute to masticatory muscles’ disability to maintain normal mandibular posture, explaining that mandibular deviation symptoms could be obtained in ITN patients after PT-RFT. As to ICP clenching, which had a similar trend, the electric activity of TA and MM decreased significantly on the operative side, leading to the ipsilateral dysfunction of contraction. Moreover, lots of clinical studies reported patients complained of chewing weakness after PT-RFT26,27. Consistent with the previously reported, our results showed that during a

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Figure 3. Surface electromyographic (sEMG) at mandibular postural position (MPP) and T-Scan occlusion. The repeated-measures analysis of variance (ANOVA) for T-scan results and sEMG values at MPP (n = 27).

Figure 4. Surface electromyographic (sEMG) during a fast maximum voluntary clenching (MVC) from mandibular postural position (MPP) to ICP. The repeated-measures analysis of variance (ANOVA) for sEMG values during a fast MVC from MPP to ICP (n = 27).

fast MVC from MPP to ICP, the baseline of sEMG symmetry rate was 94.7%, but it reduced to 13.8% and 54.9%, respectively, among 3 days and 3 months in follow-up. It declared that a disorder of coordination between bilateral masticatory muscles during maximal

voluntary contraction. Above all, it was speculated that an injury of trigeminal motor fibers occurred during PT-RFT. However, all the sEMG activity values returned to normal 12 months postprocedure. It seemed that the injury was temporary and reversible.

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Experimental studies indicated nociceptive pain was conducted by the small Ad and C fibers and that, as Letcher demonstrated in cats, the effect of radiofrequency current and heat was first on small Ad and C fibers before the larger myelinated Aa and Ab fibers were affected28. However, there was animal histological confirmation29 that the larger myelinated fibers were not preserved without damage when a complete loss of pain was produced. Furthermore, the pathology studies30 also came to the similar conclusion. In this study, we found that patients’ masticatory muscle function was reduced after procedure, accompanied by the injury of trigeminal motor branches. Nevertheless, 23 patients recovered to their baseline values 12 months postprocedure. Although, some limitations of the study required consideration. In particular, the cohort size was not a large number (27 subjects), we hypothesized that trigeminal motor fibers could be injured in patients subjected to PT-RFT, but the corresponding masticatory muscles dysfunction were transient and insignificant, which could be successfully reversible with the repair of the limited damaged nerve in a short period after procedure, leaving no major morbidity. Gusmao31 reported the occurrence of masticatory paralysis was less than 2.2%, which were in accordance with our study. In conclusion, CT-guided PT-RFT for ITN remains an effective and safe surgical operation. However, there is a high rate of temporary masticatory dysfunction in a short time after the procedure, appearing to be reversible in a period of 12 months.

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Masticatory Muscles Dysfunction after CT-guided Percutaneous Trigeminal Radiofrequency Thermocoagulation for Trigeminal Neuralgia: A Detailed Analysis.

The aim of this study was to investigate the severity and the natural course of masticatory muscles weakness that developed after CT-guided percutaneo...
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