Intermittent intraoperative nerve monitoring in thyroid reoperations: Preliminary results of a randomized, single-surgeon study

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1 ORIGINAL ARTICLE Intermittent intraoperative nerve monitoring in thyroid reoperations: Preliminary results of a randomized, single-surgeon study Hu Hei, MD, 1 Bin Zhou, MD, 1 Jianwu Qin, MD, 1 Yongping Song, MD, PhD 2 * 1 Department of Thyroid and Neck, The Affiliated Cancer Hospital of Zhengzhou University, Henan Cancer Hospital, Zhengzhou, China, 2 Department of Hematology, The Affiliated Cancer Hospital of Zhengzhou University, Henan Cancer Hospital, Zhengzhou, China. Accepted 25 November 2015 Published online 1 February 2016 in Wiley Online Library (wileyonlinelibrary.com). DOI /hed ABSTRACT: Background. The purpose of this study was to evaluate whether intermittent intraoperative nerve monitoring (IONM) could reduce the incidence of recurrent laryngeal nerve (RLN) paralysis in thyroid reoperations. Methods. Enrolled patients were randomly assigned into the nerve integrity monitor (NIM) group and the control group. Results. The incidence of temporary RLN paralysis and permanent RLN paralysis was 12.2% and 4.9% in the NIM group compared with 7.0% and 2.3% in the control group (p and p 5.966, respectively). The incidence of surgeon-related paralysis, tumor-related paralysis, and scar-related paralysis was 4.9%, 7.3%, and 4.9% in the NIM group compared with 4.7%, 2.3%, and 2.3% in the control group, respectively (p 5 1, p 5.575, and p 5.966, respectively). Conclusion. Intermittent IONM could not provide additional benefits to reduce the incidence of temporary RLN paralysis and permanent RLN paralysis in thyroid reoperations. It could not reduce the incidence of paralysis caused by unintentional injuries. VC 2016 Wiley Periodicals, Inc. Head Neck 38: E1993 E1997, 2016 KEY WORDS: thyroid reoperation, intraoperative nerve monitoring, recurrent laryngeal nerve, paralysis, thyroid cancer *Corresponding author: Y. Song, Department of Hematology, The Affiliated Cancer Hospital of Zhengzhou University, Henan Cancer Hospital, Zhengzhou , China. songyongping1961@126.com Contract grant sponsor: This study was funded by the Henan Health Agency (grant no ). Yongping Song and Jianwu Qin contributed equally to this work. INTRODUCTION Thyroid reoperation represents a great challenge to surgeons because of anatomic changes and existing scar tissues. Postoperative complications, which include recurrent laryngeal nerve (RLN) injury, hypoparathyroidism, and tracheotomy, are more common and serious after thyroid reoperation than after primary surgery. 1,2 Unilateral RLN injury causes the absence of movement of the ipsilateral vocal cord and leads to postoperative hoarseness. Whereas bilateral RLN damage may cause not only voice changes but also inspiratory dyspnea, and patients in such condition may need a tracheostomy. 3 The incidence of permanent RLN paralysis and transient RLN paralysis is 4.1% and 9.5% after thyroid reoperation, respectively. 4 Intermittent intraoperative nerve monitoring (IONM) is widely applied in thyroid and parathyroid surgeries during recent decades. As an adjunct method to locate and expose RLN, intermittent IONM has a high rate of nerve identification. 5 It is also assumed that this will help reduce the incidence of RLN injuries, especially in thyroid reoperations. However, the controversy still persists This study analyzed clinical data of a tertiary referral center to identify whether intermittent IONM could reduce the incidence of RLN paralysis during redo thyroid surgeries. MATERIALS AND METHODS This randomized controlled study was approved by the Ethics Committee of the Affiliated Cancer Hospital of Zhengzhou University and was performed according to the Declaration of Helsinki. Patients who underwent thyroid reoperations in the Department of Thyroid and Neck between January 2012 and August 2014 were enrolled in this study. All enrolled patients signed a written informed consent and then were randomly assigned into either the nerve integrity monitor (NIM) group or the control group. In the NIM group, RLNs were located and exposed with the assistance of intermittent IONM; whereas in the control group, RLNs were identified visually without IONM. All reoperations were carried out by 1 experienced thyroid surgeon who had more than 20 years experience with thyroidectomy. Fiber-optic laryngoscopy, as a gold standard to evaluate the functional integrity of RLNs, was mandatory for all patients before and after operations. 11,12 Enrolled patients were required to meet all the following inclusion criteria: (1) thyroid operations were carried out at least once before; (2) normal ipsilateral vocal cord function was detected by preoperative laryngoscopy; and (3) previous surgical field (either thyroid bed or central HEAD & NECK DOI /HED APRIL 2016 E1993

2 HEI ET AL. neck compartment), as well as ipsilateral RLN, would be exposed during reoperation. Patients who met one of the following conditions were excluded: (1) limited movement or paralysis of the ipsilateral vocal cord observed by preoperative laryngoscopy; and (2) previous surgical field and ipsilateral RLNs were not exposed during reoperation. The primary outcome measure was postoperative RLN function, which was evaluated by laryngoscopy. RLN function was divided into 3 groups: (1) normal function; (2) temporary RLN paralysis; and (3) permanent RLN paralysis. Temporary RLN paralysis was defined as recovery of RLN function within the first 6 months after thyroid reoperation, and permanent RLN paralysis was defined as no recovery of function during this period. 10,13 According to the causes of paralysis, RLN injuries were divided into 3 groups: (1) surgeon-related paralysis; (2) tumor-related paralysis; and (3) scar-related paralysis. Surgeon-related paralysis was defined as unintentional RLN injuries caused by surgical errors, such as ligation, clamping, burn, and so on. RLNs in this group should be neither surrounded by scar tissues nor invaded by tumors. Tumorrelated paralysis was defined as intentional injuries because of perineural invasion by tumors or metastatic lymph nodes, and RLNs were partially or completely transected on purpose. Scar-related paralysis was defined as RLN injuries because of tissue adhesion. The surgeon attempted to separate adhesions but failed to protect nerve function. Surgical technique Preoperative neck ultrasound was mandatory for all patients, as well as contrast-enhanced CT scans from the neck to the chest. These preoperative imaging evaluations could provide much useful information about the position and volume of thyroid remnant, the positional relationship between the remnant and tracheal wall, the status of lymph nodes in the central and lateral compartments, and the status of lung metastases. General anesthesia was administered to all patients. Low doses of short or intermediate-acting muscle relaxants were given only once for endotracheal intubation, and no other relaxants were given during operations. 5 All the reoperations were performed through the existing skin incision. In addition, one of the following surgical approaches was used to expose the thyroid bed or central neck compartment: lateral approach, central approach, or the strap muscle transected approach. The RLNs were then located and exposed by different methods. In the control group, RLNs were identified visually using different anatomic landmarks, such as Zuckerkandl tubercle, tracheoesophageal groove, and medial aspect of carotid artery. Then the RLNs were dissected upward to the larynx and downward to the thoracic inlet. In the NIM group, with the assistance of an intermittent IONM system, RLNs were located and then fully exposed by the method of nerve mapping. 5 Intermittent intraoperative nerve monitoring technique The RLNs of patients in the NIM group were monitored by the NIM Response 2.0 (Medtronic Xomed, Jacksonville, FL), which had a specific type of endotracheal tube with 4 surface electrodes. After the endotracheal tube was inserted into the trachea by an experienced anesthetist, a video laryngoscope was used to adjust its position to make sure that the surface electrodes fully contacted with the bilateral vocal cords. This study complied with the standard operating procedures of intermittent IONM. 5,14 All vagus nerves in the NIM group were dissected out of the carotid sheath for further stimulation. During dissection, V1, R1, R2, and V2 signals were obtained sequentially by stimulation of the vagus nerve or RLN at given times. The V1 signal was defined as an original electromyography signal obtained from the vagus nerve before identification of the RLN; the R1 signal was obtained from the RLN when it was first identified in the tracheoesophageal groove; the R2 signal was also obtained from the RLN after it was completely dissected and its full course in the neck was exposed; and the V2 signal was obtained from the vagus nerve after complete hemostasis of the surgical field. 14 In addition to these, stimulation of the vagus nerve or the RLN was also performed during challenging or concerning maneuvers. Data of peak amplitude and latency were collected and analyzed. Perioperative management As a gold standard for assessing the function of vocal cords, fiber-optic laryngoscopy was mandatory for all patients preoperatively and day 1 after reoperation. If RLN paralysis occurred, laryngoscopy was carried out routinely at 1, 3, and 6 months after operation and at the time that the patients felt that their voice obviously improved. Statistical analysis Data were analyzed by IBM SPSS statistics version 20. Student s t test was used for continuous variables, and data were presented as mean 6 SD. The chi-square test or Fisher s exact test was used for categorical variables. Any p value <.05 indicated statistical significance. RESULTS A total of 78 patients underwent thyroid reoperations during this period. Five patients were excluded because of RLN paralysis diagnosed by preoperative laryngoscopy; and 3 patients were excluded because the thyroid bed or central neck compartment was not involved during reoperations. Finally, 70 patients (mean age, years) were enrolled into this study, including 54 women and 16 men. Of these, 33 patients with 41 RLNs at risk were enrolled into the NIM group, and 37 patients with 43 RLNs at risk were enrolled into the control group. The characteristics of enrolled patients and data of previous procedures are summarized in Table 1. In this study, 62.9% (44/70) of redo dissections were carried out due to recurrence or persistence of papillary thyroid carcinoma (PTC), followed successively by nontoxic multinodular goiter (16 of 70), follicular thyroid carcinoma (5 of 70), and medullary thyroid carcinoma (5 of 70). In addition, 84.3% (59 of 70) of primary surgeries were partial lobectomy. In the group of patients who underwent operations just once, the incidence of RLN paralysis was 14.5% (9 of 62) compared with 28.6% (2 of 7) of patients who underwent operations twice (p 5.676; Table 1). E1994 HEAD & NECK DOI /HED APRIL 2016

3 INTERMITTENT INTRAOPERATIVE NERVE MONITORING IN THYROID REOPERATIONS TABLE 1. Characteristics Characteristics of patients and data of previous procedures. NIM group Control group p value Total no. of patients Sex.161 Female 23 (69.7) 31 (83.8) Male 10 (30.3) 6 (16.2) Mean age 6 SD, y * Preoperative diagnosis MNG 6 (18.2) 10 (27.0).379 PTC 23 (69.7) 21 (56.8).263 FTC 1 (3.0) 4 (10.8).426 MTC 3 (9.1) 2 (5.4).894 No. of previous operations 1 28 (84.8) 34 (91.9) (15.2) 2 (5.4) (0) 1 (2.7) 1 Previous procedure Partial lobectomy (unilateral) Partial lobectomy (bilateral) Subtotal lobectomy (unilateral) Subtotal lobectomy (bilateral) Subtotal lobectomy 1 partial lobectomy (contralateral) 16 (48.5) 24 (64.9) (18.2) 8 (21.6) (6.1) 2 (5.4) 1 1 (3.0) 1 (2.7) 1 3 (9.1) 2 (5.4).894 Lobectomy (unilateral) 2 (6.1) 0 (0).219 Total thyroidectomy 3 (9.1) 0 (0).199 Temporary RLN paralysis after previous operations, but recovered before this operation 1 (3.0) 3 (8.1).691 Mean time interval between this operation and previous operation, d * Abbreviations: NIM, nerve integrity monitor; MNG, nontoxic multinodular goiter; PTC, papillary thyroid carcinoma; FTC, follicular thyroid carcinoma; MTC, medullary thyroid carcinoma; RLN, recurrent laryngeal nerve. * Independent sample t test was used. Continuity corrected chi-square test was used. Fisher s exact test was used. Pearson chi-square test was used for all the others. Note: Data are presented as no. of patients or mean 6 SD. The information of reoperations is presented in Table 2, and the incidences of RLN paralysis are presented in Table 3. The total RLN paralysis rate was 13.1% (11 of 84). The incidence of temporary RLN paralysis and permanent RLN paralysis was 9.5% (8 of 84) and 3.6% (3 of 84), respectively. After the 6-month follow-up, 71.4% (5 of 7) of paralytic RLNs in the NIM group and 75% (3 of 4) in the control group recovered function. One patient in the NIM group and no patient in the control group underwent tracheotomy. According to surgical approaches of reoperations, 54 RLNs were exposed via lateral approach, and 27 RLNs were exposed via central approach. After reoperation, 1 RLN in the central-approach group and 10 RLNs in the lateral-approach group were found to be injured. Details are shown in Table 4. DISCUSSION Intermittent IONM has been widely accepted as useful assistance during thyroid and parathyroid operations. 15 In addition, to improve the rate of RLN identification, 16 IONM can also accurately predict postoperative functions of RLNs. 17 This may help in selecting patients for a possible emergency tracheotomy if electromyography signals of bilateral RLNs were lost. A large prospective randomized study also verified that IONM could reduce incidence of temporary RLN paralysis in primary thyroid surgeries. However, no statistically significant decrease was observed in the incidence of permanent RLN paralysis. 18 IONM was also reported to be helpful in identifying the external branch of the superior laryngeal nerve, thus providing more functional protection of the vocal cords. 19,20 Thyroid reoperation is a great challenge to all surgeons because of serious postoperative complications, especially to the surgeons working in low-volume hospitals. Surgeons should pay considerable attention to the anatomic changes, existing scar tissues, and tissue edema during reoperations. All of these can put RLNs and parathyroid glands at high risk of being injured. The incidence of RLN paralysis is higher in redo thyroid surgeries than in primary surgeries (8.7% vs 4.1%, respectively). 12,21 Surgeon experience and routine visual exposure are 2 crucial factors in reducing the incidence of RLN paralysis. 3,10 TABLE 2. Variables Information of reoperations. NIM group Control group p value Total no. of patients Nerves at risk Extent of thyroidectomy* Ipsilateral RTL 6 (18.2) 11 (29.7).261 Ipsilateral RTL and 14 (42.4) 15 (40.5).873 contralateral lobe Bilateral RTL 8 (24.2) 10 (27.0).79 Contralateral lobe 3 (9.1) 0 (0).199 Undone 2 (6.1) 1 (2.7).919 Extent of CND* Ipsilateral 16 (48.5) 19 (51.3).811 Bilateral 8 (24.2) 5 (13.5).249 Undone 9 (27.3) 13 (35.1).479 Surgical approaches Central approach 9 (22.0) 18 (41.9).051 Lateral approach 32 (78.0) 22 (51.2).01 Strap muscle 0 (0) 3 (7.0).257 transected approach RLN situation Excellent 32 (78.0) 36 (83.7).508 Adhered but could be 6 (14.6) 5 (11.6).683 completely dissected Partially invaded by 1 (2.4) 0 (0).488 tumors or lymph nodes Completely invaded by 2 (4.9) 2 (4.7) 1 tumors or lymph nodes Position of RLN exposed Zuckerkandl Tubercle 8 (19.5) 14 (32.6).174 TEG 30 (73.2) 27 (62.8).309 Medial aspect of carotid artery 3 (7.3) 2 (4.7).956 Abbreviations: NIM, nerve integrity monitor; RTL, residual thyroid lobe; CND, central neck dissection; RLN, recurrent laryngeal nerve; TEG, tracheoesophageal groove. * Calculated for patients. Continuity corrected chi-square test was used. Fisher s exact test was used. Pearson chi-square test was used for all the others. Note: Data are presented as no. of RLNs. HEAD & NECK DOI /HED APRIL 2016 E1995

4 HEI ET AL. TABLE 3. Incidence of recurrent laryngeal nerve paralysis. Postoperative laryngoscopy NIM group Control group p value Nerves at risk Paralysis Total 7 (17.1) 4 (9.3).291* Temporary RLN paralysis 5 (12.2) 3 (7.0).658 Permanent RLN paralysis 2 (4.9) 1 (2.3).966 Causes of paralysis Surgeon-related 2 (4.9) 2 (4.7) 1 Tumor-related 3 (7.3) 1 (2.3).575 Scar-related 2 (4.9) 1 (2.3).966 No. of tracheotomy 1 (3.0) 0 (0).471 Mean recovery time of temporary RLN paralysis, d Abbreviations: NIM, nerve integrity monitor; RLN, recurrent laryngeal nerve. * Pearson chi-square test was used. Calculated for patients. Fisher s exact test was used. Independent sample t test was used. Continuity corrected chi-square test was used for all the others. Note: Data are presented as no. of RLNs or mean. Whether intermittent IONM can provide additional benefits in thyroid reoperations is still controversial. Alesina et al 7 performed a retrospective analysis, including 91 operations with IONM and 159 operations without IONM. Neither temporary RLN paralysis rates nor permanent RLN paralysis rates between these 2 groups had statistical significance. Barczynski et al 8 also carried out a retrospective study, including 306 patients (500 RLNs) with IONM and 548 patients (826 RLNs) without IONM. Two different neuromonitoring systems were used in the IONM group. The incidence of temporary RLN paralysis and permanent RLN paralysis was 2.6% and 1.4% in the IONM group, respectively, compared with 6.3% and 2.4% in the control group. There was statistical significance in the temporary RLN paralysis rates between the 2 groups (p 5.003), but no significance was observed in the permanent RLN paralysis rates (p 5.202). To eliminate interpersonal variability and minimize confounding factors, all redo thyroid surgeries in this study were performed by 1 skilled surgeon who had sufficient experience in thyroid reoperations. As is shown in Table 3, no obvious difference was observed in the temporary RLN paralysis rates (12.2% vs 7.0%; p 5.658) and the permanent RLN paralysis rates (4.9% vs 2.3%; p 5.966) between the 2 groups. Moreover, RLN function was sometimes difficult to TABLE 4. Incidence of recurrent laryngeal nerve paralysis in different surgical approaches. Lateral approach Central approach p value Nerves at risk Total paralysis 10 (18.5) 1 (3.7).136 Temporary RLN paralysis 3 (5.6) 0 (0).533 Permanent RLN paralysis 7 (12.9) 1 (3.7).357 Abbreviation: RLN, recurrent laryngeal nerve. Data are presented as no. of RLNs. Continuity corrected chi-square test was used for all. be saved during reoperations because of invasion by tumors or metastatic lymph nodes. 4 In fact, what we were eager to know was whether or not intermittent IONM could reduce the incidence of RLN paralysis caused by surgeon-related factors and scar-related factors, but not tumor-related factors in which the condition of RLN injuries were inevitable. Thus, this study first divided RLN paralysis into surgeonrelated paralysis, tumor-related paralysis, and scar-related paralysis. The incidence of RLN paralysis with IONM and without IONM was 4.9% and 4.7% in the surgeon-related group, 7.3% and 2.3% in the tumor-related group, and 4.9% and 2.3% in the scar-related group, respectively (Table 3). No statistically significant differences were observed based on different causes of injury. Many reasons can lead to thyroid reoperation, such as nonstandardized surgical procedures, recurrence of multinodular goiter, or persistence of thyroid cancer. In our data, 84.3% (59 of 70) of primary surgeries were partial lobectomy, and 62.9% (44 of 70) of redo dissections were due to recurrence or persistence of PTC. All of these indicated the importance of a standard procedure of lobectomy or total thyroidectomy during initial operations. The positional relationship between the RLN and adjacent structures was complicated in thyroid reoperations, and the RLNs in different status were managed distinctly. The positional relationship in this study was first described as follows: (1) excellent; (2) adhered but could be completely dissected; (3) partially invaded by tumors or lymph nodes; and (4) completely invaded by tumors or lymph nodes (Table 2). RLNs adhered by scar tissues usually could be well preserved. RLNs partially invaded required partial resection along the longitudinal axis and the nerve s continuity was retained. RLNs completely invaded by tumors were transected intentionally. No significant differences were shown according to RLN status between these 2 groups (Table 2). There are some reasons to explain the results. First, a skilled surgeon could minimize the possibility of RLN paralysis, and the additional benefits of intermittent IONM did not seem apparent. All the reoperations in our study were done by the same surgeon. The thyroid bed was explored via different surgical approaches to avoid scar tissues, and the RLNs were located by different surgical landmarks and traced with delicate, blunt dissection. Although the proportion of the lateral approach was different between the NIM group and the control group, it did not significantly affect the incidence of RLN paralysis under a skilled surgeon s hands (Table 2). 22 Second, intermittent nerve stimulation was adopted in this study. Although intermittent IONM could predict the intraoperative and postoperative functional integrity of RLN, it could not provide continuous functional protection during the nonstimulation periods. Just like the temporary RLN paralysis that occurred in our study, it was too late to avoid RLN injuries because the damages had happened during these periods. Third, RLN injuries were inevitable in certain circumstances, such as RLNs adhered by scar tissues or invaded by tumors. Although signal amplitudes could be detected frequently, and an obvious drop of amplitudes could warn the surgeon to operate more gently or temporarily cease dissection, the additional benefits of intermittent IONM still seemed trivial. In this study, 1 E1996 HEAD & NECK DOI /HED APRIL 2016

5 INTERMITTENT INTRAOPERATIVE NERVE MONITORING IN THYROID REOPERATIONS patient in the NIM group underwent tracheotomy because of severe inspiratory dyspnea. This patient had undergone total thyroidectomy in a previous operation, which resulted in permanent paralysis of the right RLN. Combined bilateral central and lateral neck dissections were carried out during reoperation, and left RLN was found adhered severely with scar tissues. Although gentle dissection was performed and intermittent IONM was used, the amplitudes of V signals and R signals still decreased dramatically (V1 signal 1278 lv; V2 signal 235 lv; R1 signal 1493 lv; and R2 signal 304 lv). Our study had some limitations. First, this was a small sample study. To draw more persuasive conclusions, at least 434 RLNs in each group are needed to evaluate RLN injury reduction from 10% to 5% with a power of 80% and p However, thyroid reoperations are relatively rare, and it is of great difficulty to collect enough samples in 1 hospital. Second, this was a single-surgeon study, which would introduce bias of experience and limit the generalizability of these results. Intermittent IONM might be helpful to less experienced surgeons, as it could make their learning curve less steep. In conclusion, although intermittent IONM provided more intraoperative information about RLNs and helped predict postoperative RLN function, it still could not reduce the incidence of temporary and permanent RLN paralysis in a tertiary referral center, and it could not provide obvious benefits to skilled thyroid surgeons. 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