Marcin Barczyński 1, Aleksander Konturek 1, Małgorzata Stopa 1, Alicja Hubalewska-Dydejczyk 2, Piotr Richter 1, Wojciech Nowak 1

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1 POLSKI PRZEGLĄD CHIRURGICZNY 2011, 83, 4, /v Clinical value of intraoperative neuromonitoring of the recurrent laryngeal nerves in improving outcomes of surgery for well-differentiated thyroid cancer* Marcin Barczyński 1, Aleksander Konturek 1, Małgorzata Stopa 1, Alicja Hubalewska-Dydejczyk 2, Piotr Richter 1, Wojciech Nowak 1 3 rd Chair and Department of General Surgery, Collegium Medicum Jagiellonian University in Cracow 1 Kierownik: prof. dr hab. W. Nowak Chair and Department of Endocrinology, Collegium Medicum Jagiellonian University in Cracow 2 Kierownik: dr hab. A. Hubalewska-Dydejczyk, prof. UJ The recurrent laryngeal nerve (RLN) is particularly prone to injury during thyroidectomy in case of extralaryngeal bifurcation being present in approximately one-third of patients near the inferior thyroid artery or ligament of Berry. Meticulous surgical dissection in this area may be additionally facilitated by the use of intraoperative neuromonitoring (IONM) to assure safe and complete removal of thyroid tissue. The aim of the study was to verify the hypothesis that meticulous surgical technique of tissue dissection in the area of the posterior surface of the thyroid capsule and adjacent RLN may be additionally facilitated by intraoperative neuromonitoring (IONM), and may contribute to increasing the safety and radicalness of total thyroidectomy in patients with well-differentiated thyroid cancer. Material and methods. The outcomes of total thyroidectomy with level VI lymph node clearance for well-differentiated thyroid cancer (WDTC; pt1-3,n0-1,mx) were retrospectively compared between 151 patients undergoing surgery with IONM (01/ /2009) and 151 patients undergoing surgery without IONM ( ). RLN morbidity (calculated for nerves at risk) was assessed by videolaryngoscopy or indirect laryngoscopy (mandatory before and after surgery and at 12-month follow-up). The anatomical course of the extralaryngeal segment of RLNs were analyzed in detail in each operation. Thyroid iodine uptake ( 131 I) was measured during endogenous TSH stimulation test a week before radioiodine therapy. Results. Among patients operated with vs. without IONM, the early RLN injury rate was 3% vs. 6.7% (p=0.02), including 2% vs. 5% (p=0.04) of temporary nerve lesions, and 1% vs. 1.7% of permanent nerve events (p=0.31), respectively. Extralaryngeal RLN bifurcation was identified in 42 (27.8%) vs. 25 (16.6%) of patients operated with vs. without IONM, respectively (p=0.001). Mean I-131 uptake following total thyroidectomy with vs. without IONM was 0.67 ± 0.39% vs ± 0.69% (p<0.001). 131 I uptake lower than 1% was found in 106 (70.2%) vs. 38 (25.2%) patients operated with vs. without IONM, respectively (p<0.001). Conclusions. Most patients with WDTC who undergo total thyroidectomy have a small amount of residual thyroid tissue. The use of IONM may improve the outcomes of surgery among these patients by both increasing the completeness of total thyroidectomy and significantly reducing the prevalence of temporary RLN injury. The possible mechanism of this improvement is the aid in dissection at the level of the Berry s ligament offered by IONM which enhances the surgeon s ability to identify a branched RLN, and allows for reduction of traction injury and neuropraxia of the anterior branch of bifid nerves. Key words: thyroid cancer, recurrent laryngeal nerve, intraoperative neuromonitoring * This paper has been presented during the 4 th Conference on Thyroid Cancer, Zakopane May, 2010

2 Clinical value of intraoperative neuromonitoring in surgery of thyroid cancer 197 Total extracapsular thyroidectomy is recommended in Poland in all patients with welldifferentiated thyroid cancer diagnosed preoperatively (1, 2). Removal of the entire thyroid tissue decreases the risk of local recurrent disease and in patients after surgical treatment followed by adjuvant 131 I therapy it facilitates detection of metastatic lesions based on thyroglobulin monitoring or total body 131 I scintiscan (1, 3). Additionally, after total thyroidectomy, one may expect improved effects of 131 I therapy, such as a successful ablation of residual thyroid cells and destruction of possible microfoci of thyroid cancer. In the hands of an experienced surgeon, total extracapsular thyroidectomy is associated with an acceptable risk of permanent complications, such as injury to the recurrent laryngeal nerve (RLN) or hypoparathyroidism; however, in rare instances only can the thyroid tissue be completely excised and as a rule supplementary 131 I ablation is necessary (1, 2, 3). In 1938, Lahey of Boston observed that identification and preserving the anatomical integrity of RLN in the course of thyroidectomy decreased the percentage of RLN injuries, what was later confirmed by numerous publications (4-8). Today, such a management strategy is a commonly accepted standard of a safe surgical technique in thyroid cancer. In the past few years, however, closer attention was focused on the phenomenon of anatomical diversity of the extralaryngeal RLN segment and its possible bifurcation, what is observed in almost 30% of patients (9-13). Sancho et al. demonstrated that the risk of damaging a bifurcated RLN was two times higher as compared to a single-trunk nerve (9). Barczyński et al. drew attention to the possibility of increasing the accuracy of macroscopic identification of RLN bifurcation in the area of the Berry s ligament by RLN neuromonitoring (IONM) and to an achievable significant decrease in the percentage of transient RLN damage by employing IONM as compared to procedures performed with RLN identification, but without IONM (10). Recent papers by Serpell et al. confirm the validity of this statement, pointing to the topographical anatomy of the distal, 2 cm-long RLN segment at the level of the Berry s ligament, where the nerve is sheeted with two ligament lamellae, which in case of total thyroidectomy may expose the nerve to the risk of undue traction at the site and neuropraxia manifested as a transient RLN injury (11, 12, 13). The purpose of the present study was to verify the hypothesis that meticulous surgical technique of tissue dissection in the area of the posterior surface of the thyroid capsule and adjacent RLN may be additionally facilitated by intraoperative neuromonitoring (IONM), and may contribute to increasing the safety and radicalness of total thyroidectomy in patients with well-differentiated thyroid cancer. MATERIAL AND METHODS In this study prospectively collected data in the Department s register of thyroid surgery were analyzed. The authors compared the results of total extracapsular thyroidectomies with level VI lymph node clearance for welldifferentiated thyroid cancer (WDTC; pt1-3-,n0-1,mx) in two groups of patients: 151 patients operated on with IONM (between January 2005 and June 2009) and 151 patients operated on without IONM (between January 2003 and December 2004). Protocol of this study was approved by the Bioethics Committee of the Jagiellonian University. Both groups of patients were subjected to total extracapsular thyroidectomies with intraoperative RLN identification and intent to preserve the parathyroids in situ. During each procedure, the anatomical diversity of the extralaryngeal RLN segments was analyzed, attention was focused on their possible bifurcation and their topography was precisely described. In the group of patients operated on with IONM, the authors employed either a Neurosign 100 unit (Inomed, Teningen, Germany) with laryngeal needle electrodes (112 procedures), or a NIM2.0 unit (Medtronic, Jacksonville, USA) with surface electrodes integrated with intubation tube (39 procedures). The nerves were stimulated using a monopolar electrode and the interrupted stimulation technique at 1mA, 100ms impulse duration and 4 Hz frequency. The assessment included the effect of indirect stimulation via the vagus nerve prior to (V1) and after completion of lobectomy (V2), and of direct stimulation using RLN mapping prior to its visualization (R1), in the course of tissue dissection and following completion of lobectomy (R2). In case of bifurcated nerves, the assess-

3 198 M. Barczyński et al. ment included post-stimulation response of each nerve branch based on acoustic evaluation of the signal and using the technique of posterior larynx palpation ( laryngeal twitch ). The employed neuromonitoring technique is in agreement with the recommendations formulated recently by the International Intraoperative Monitoring Study Group that are presented in fig. 1 (14). RLN complications were assessed by videolaryngoscopy or indirect laryngoscopy (mandatory prior to L1, and after surgery L2, and at 12-month follow-up; chi2 test). Iodine uptake was determined following administration of 6 MBq 131I during endogenous TSH stimulation (the patient was off L-thyroxine in preparation for 131I treatment and one week prior to administration of a therapeutic dose had a scintiscan with uptake assessment performed). The percentage of 131I uptake was expressed as the percentage of the administered dose (t-test). The patients were subsequently treated with radioisotopes in keeping with standards obligatory in Poland; a detailed discussion of the protocol is well beyond the scope of the present paper (15). RESULTS Demographic data, thyroid cancer stage according to TNM 2002, details of procedures performed and TSH concentration values during endogenous stimulation prior to assessment of 131I uptake after surgery are presented in tab. 1, while tab. 2 illustrates the compari- Fig. 1. Recommended methodology of intraoperative recurrent laryngeal nerve monitoring (according to the International Intraoperative Neuromonitoring Study Group) (14)

4 Clinical value of intraoperative neuromonitoring in surgery of thyroid cancer 199 Table 1. Demographic data, thyroid cancer stage according to TNM 2002, type of procedure, TSH prior to postoperative 131 I uptake assessment Patients with WDTC operated on without IONM (years ) n=151 Patients with WDTC operated on with IONM (years ) n=151 Age, mean ± SD, years 44,9 ± 15,7 43,9 ± 18,1 0,82 Gender (F : M) 135 : : 14 0,70 BMI, mean ± SD 24,3 ± 3,1 24,5 ± 3 0,91 Histopathological diagnosis, n (%): Papillary carcinoma Follicular carcinoma TN stage according to TNM 2002, n (%) pt1a pt1b pt2 pt3 ptm N0 N1 130 (86,1) 21 (13,9) 134 (88,7) 17 (11,3) p 0,48 0, ,42 0,81 0,60 0,24 0,31 0,52 0,52 Total thyroidectomy, n (%) 151 (100) 151 (100) 1 Lymphadenectomy n (%): VI wg ATA, unilateral VI wg ATA, bilateral II, III, IV wg ATA unilateral II, III, IV wg ATA bilateral ,24 0,15 0,56 1 TSH during endogenous stimulation, mu/l 32,4 ± 3,7 31,4 ± 4,2 0,82 test χ 2 ; test-t; test χ 2 ; test-t; WDTC well-differentiated thyroid cancer RLN damage,%: Transient Permanent Total RLN bifurcated in the extralaryngeal segment, n (%) Table 2. Comparison of results in the two groups of surgical patients Patients with WDTC operated on without IONM (lata ) n=151 Patients with WDTC operated on with IONM (lata ) n= ,7 6, ,02 0,31 0,04 25 (16,6) 42 (27,8) <0,01 Mean 131 I uptake in the post-surgical bed, (%) / 1,59 ± 0,69 0,67 ± 0,39 <0, I uptake in the post-surgical bed < 1%, n (%) 38 (25,2) 106 (70,2%) <0,001 test χ 2 ; test-t; test χ 2 ; test-t; WDTC well-differentiated thyroid cancer p son of results obtained in the two groups of patients. In the group of patients operated on with vs. without RLN neuromonitoring, early RLN injury was noted in 3% vs. 6.7% individuals (p=0.02); of these patients, 2% vs. 5% (p =0.04) manifested transient damage, while 1% vs. 1.7% (p=0.31) permanent damage. RLN bifurcation in the extralaryngeal segment was seen respectively in 42 (27.8%) vs. 25 (16.6%) patients with vs. without IONM (p <0.01). The mean 131 I uptake following total thyroidectomy with vs. without IONM was 0.67 ± 0.39% vs ± 0.69% (p <0.001). 131 I uptake below 1% was noted in 106 (70.2%) vs. 38 (25.2%) of patients operated on with vs. without IONM, respectively (p<0.001). DISCUSSION Intraoperative electrophysiological neuromonitoring of recurrent laryngeal nerves in the course of thyroid and parathyroid surgery has been gaining acceptance worldwide as an

5 200 M. Barczyński et al. additional tool that supplements the standard of visual RLNs identification and allows for their intraoperative functional assessment (10, 12, 13, 16-25). Potential advantages of employing IONM in surgical treatment of thyroid cancer, i.e. the subject of the present report, are shown in brief in tab. 3 (10, 12, 16, 18, 20). Within the past few years, closer attention has been focused on the phenomenon of anatomical diversity of the extralaryngeal RLN segment and the possibility of the nerve bifurcation, what is observed in almost 30% of patients (9-13). Sancho et al. demonstrated that the risk of damaging a bifurcated recurrent laryngeal nerve was almost twice as high as in the case of a single-trunk nerve (15.8% vs. 8.1%; p<0.01) (9). Barczyński et al. emphasized the possibility of increasing the accuracy of macroscopic identification of RLN branches close to the Berry s ligament by almost 10% through employing IONM, and the achievable significant decrease of the percentage of transient RLN damage when using IONM as compared to procedures with RLN identification, but without IONM (2% vs. 4.9%; p=0.01) (10). Recent reports by Serpell et al. confirm the validity of this statement, drawing attention to the topographic anatomy of the distal 2 cmlong RLN segment situated at the level of the Berry s ligament, where the nerve is sheeted by two ligament lamellae, which in case of total thyroidectomies may expose the nerve to the risk of undue traction at the site and neuropraxia manifested as transient RLN damage (11, 12, 13). The above observations are of a great importance for a surgeon performing thyroid cancer surgery, when total extracapsular thyroidectomies are recommended. Radical excision of the thyroid tissue in the area of the Zuckerandl s tubercle and Berry s ligament, where RLN extends prior to entering the larynx, may be technically difficult and a surgeon, striving for preserving the integrity of RLN, may decide to leave some residuals thyroid tissue at the site, thus restricting the scope of resection to the so-called near-total thyroidectomy (an almost complete resection of the thyroid, with less than 1 g of thyroid tissue left in situ bilaterally), a management strategy that is in accordance with the most recent Table 3. Potential advantages of intraoperative RLN neuromonitoring in thyroid cancer surgery I. CLINICAL ADVANTAGES 1. Facilitated RLN identification and dissection: a) trln mapping electrophysiological assessment precedes visual assessment, b) electrophysiological confirmation of the accuracy of visual assessment, c) facilitation of assessment of RLN anatomical diversity (bifurcation of RLNs in the extralaryngeal segment approximately 30%, including the non-recurrent laryngeal nerve approximately 0.5%), d) facilitation of RLN identification in a scarred surgical field (reoperation), e) increasing radicalness of surgical thyroid tissue ablation in thyroid cancer. 2. Intraoperative prognosticating of RLN function: a) minimizing the risk of bilateral RLN damage, b) individualized surgical strategy (two-stage thyroidectomy possible in case of neuromonitoring signal loss following resection of the tumor-containing thyroid lobe, especially in patients with well-differentiated thyroid cancer regarded low-risk ). 3. Location of the site of RLN injury and assessment of damage mechanism: a) maintaining anatomical RLN integrity with loss of neuromonitoring signal indicates a prognosis of a transient injury, what facilitates a conversation between the surgeon and the patient after the procedure on further prognosis and recovery of motor function of the vocal fold, b) assistance in RLN reconstruction surgery. II. EDUCATIONAL TOOL IN TEACHING RESIDENTS 1. Understanding normal anatomy of RLNs and their anatomical diversity. 2. Facilitation of RLN identification in a scarred surgical field (reoperation). 3. Assistance in orientation in the surgical field in cases of high-stage thyroid cancer. III. ASSISTANCE IN RESEARCH 1. Correlation of RLN anatomical diversity and neurophysiologic versatility. 2. Assessment of prognostic value of neuromonitoring. IV. MEDICO-LEGAL ISSUES 1. Intraoperative assessment of treatment quality. 2. Documenting electromyographic records of RLN function. 3. Effect on developing management standards in thyroid surgery.

6 Clinical value of intraoperative neuromonitoring in surgery of thyroid cancer 201 revised recommendations of the American Thyroid Association (ATA) (1), as well as with Polish recommendations formulated in A procedure may be regarded a near-total thyroidectomy if ultrasonography shows that bilaterally, the volume of residual thyroid tissue does not exceed 1 ml. Evaluation of iodine uptake and postoperative thyroid scintiscan, when performed during TSH stimulation, are helpful in assessing the scope of the procedure but cannot provide an absolute criterion of its radicalness. In a surgical patient after total thyroidectomy, post-rhtsh iodine uptake is generally lower than 1%. Under TSH stimulation obtained through interrupting thyroxine administration, one should expect an iodine uptake value below 5%, while the value below 2% is a reliable proof of a total excision of the thyroid. Nevertheless, a higher iodine uptake combined with a small volume of residual thyroid tissue seen in ultrasound does not per se constitute an indication for reoperation (15). In the presented study, the use of IONM allowed for decreasing the risk of RLN injury by 3.7% (p =0.04), including a 3% drop in the risk of transient (p =0.02) and a 0.7% drop in the risk of permanent damage (p =0.31). What is most important, the improvement of these outcomes was accompanied by a significant increase of radicalness of thyroid tissue resection in the group operated on with IONM as assessed by postoperative 131 I uptake (by the mean value of 0.92%), and the percentage of patient with iodine uptake below 1% increased when IONM was employed by as much as 45%. In cases when such a low iodine uptake value is achieved in the post-thyroidectomy bed, individualized consideration of recommendations for 131 I ablation seems warranted. This is particularly true in patients with well-differentiated thyroid cancer described as lowrisk in keeping with the commonly accepted criteria (e.g. AGES, AMES or MACIS), in whom we may refrain from 131 I ablation providing postoperative ultrasonography failed to visualize residual thyroid tissue. Explaining the mechanism of this phenomenon is associated with facilitated identification of RLN bifurcation in the extralaryngeal segment using the technique of intraoperative RLN mapping (electrophysiological location of the nerve bifurcation precedes visual identification). Thus, a tangible effect of the use of IONM was an increase in the percentage of patients with intraoperatively detected bifurcation of RLN in its distal segment within the area of 2 cm prior to the nerve entering into the larynx (at the level of the Zuckerandl s tubercle and Berry s ligament) by as much as 11.2% as compared to the group without IONM (p <0.01). IONM allows for minimizing the risk of damaging a visually undetected anterior branch of RLN, which as a rule travels between the trachea and the Zuckerandl s tubercle or Berry s ligament. A surgeons who does not take advantage of IONM may mistakenly interpret the visualized posterior branch of RLN, which generally has a lateral course, frontally with respect to the Zuckerandl s tubercle, as the entire nerve trunk, what favors damaging the undetected anterior RLN branch, leading to paralysis or paresis of the ipsilateral vocal fold (10, 12, 15, 17, 21). Finally, we should give some thought to the perspectives of popularizing IONM in thyroid surgery in Poland as compared to other countries. In the United States, approximately 40%, and in Germany, almost 90% of thyroid surgery procedures are estimated to be monitored in this manner. The technique is more commonly employed in thyroid surgery referral centers and by surgeons below 40 years of age (23, 24, 25). To date, in Poland, IONM is used but in a few thyroid surgery centers and, according to the data collected by the Polish Club of Endocrine Surgeons, only 1-2% of thyroid procedures are monitored in this manner nationally (10, 19, 26). The situation may soon improve thanks to the Polish Intraoperative Neuromonitoring Study Group appointed in 2010 by the Polish Club of Endocrine Surgeons; details of the project can be found on the website www. neuromonitoring.com.pl. Additionally, it should be also borne in mind that the active since 2007 International Intraoperative Neuromonitoring Study Group finalized development of recommendations addressing neuromonitoring standards, what should facilitate the application of the technique in interested centers (14). The recommended methodology of IONM as described by the International Intraoperative Neuromonitoring Study Group is presented in brief in fig. 1. Summing up, it should be emphasized that the majority of patients subjected to total thyroidectomies due to thyroid cancer still have a

7 202 M. Barczyński et al. small volume of residual thyroid tissue in the post-surgical bed in the neck. The use of IONM may improve the outcome in these patients through increasing radicalness of total thyroidectomies, at the same time significantly decreasing the risk of transient damage to RLNs. A possible explanation of the mechanism underlying the phenomenon lies in facilitation of tissue dissection at the level of the Berry s ligament that may be achieved with use of IONM. Neuromonitoring increases the accuracy of macroscopic identification of anatomical variants of bifurcated RLNs and allows for decreasing undue traction injuries, thus preventing neuropraxia of the anterior branch of the bifurcated recurrent laryngeal nerve. REFERENCES 1. Cooper DS, Doherty GM, Haugen BR et al.: Revised American Thyroid Association Management Guidelines for Patients with Thyroid Nodules and Differentiated Thyroid Cancer. Thyroid 2009; 19: Barczyński M, Konturek A, Hubalewska-Dydejczyk A et al.: Five-year follow-up of a randomized clinical trial of total thyroidectomy versus Dunhill operation versus bilateral subtotal thyroidectomy for multinodular nontoxic goiter. World J Surg 2010; 34: Salvatori M, Raffaelli M, Castaldi P et al.: Evaluation of the surgical completeness after total thyroidectomy for differentiated thyroid carcinoma. Eur J Surg Oncol 2007; 33: Lahey FH: Routine dissection and demonstration of recurrent laryngeal nerves in subtotal thyroidectomy. Surg Gynecol Obstet 1938; 66: Riddel VH: Injury to recurrent laryngeal nerves during thyroidctomy a comparison between the results of identification and non-identification in 1022 nerves exposed to risk. Lancet 1956; 29: Hermann M, Alk G, Roka R et al.: Laryngeal recurrent nerve injury in surgery for benign thyroid disease: effect of the nerve dissection and impact of individual surgeon in more than 27,000 nerves at risk. Ann Surg 2002; 235: Steurer M, Passler C, Denk DM et al.: Advantages of recurrent laryngeal nerve identification in thyroidectomy and parathyroidectomy and the importance of preoperative and postoperative laryngoscopic examination in more than 1000 nerves at risk. Laryngoscope 2002; 112: Randolph GW: The importance of pre- and postoperative laryngeal examination for thyroid surgery. Thyroid 2010; 20: Sancho JJ, Pascual-Damieta M, Pereira JA et al.: Risk factors for transient vocal cord palsy after thyroidectomy. Br J Surg 2008; 95: Barczyński M, Konturek A, Cichoń S: Randomized clinical trial of visualization versus neuromonitoring of recurrent laryngeal nerves during thyroidectomy. Br J Surg 2009; 96: Serpell JW: New operative surgical concept of two fascial layers enveloping the recurrent laryngeal nerve. Ann Surg Oncol 2010; 17: Serpell JW, Yeung MJ, Grodski S: The motor fibers of the recurrent laryngeal nerve are located in the anterior extralaryngeal branch. Ann Surg 2009; 249: Barczyński M, Nowak W, Sancho JJ et al.: The motor fibers of the recurrent laryngeal nerves are located in the anterior extralaryngeal branch. Ann Surg 2010; 251: Randolph GW, Dralle H with the International Intraoperative Monitoring Study Group. Electrophysiologic recurrent laryngeal nerve monitoring during thyroid and parathyroid surgery International standards guideline statement. Laryngoscope 2011; 121(S1): S1-S Jarząb B, Sporny S, Lange D i wsp.: Diagnostyka i leczenie raka tarczycy rekomendacje polskie. Endokrnol Pol 2010; 61: Dralle H, Sekulla C, Lorenz K et al with the German IONM Study Group. Intraoperative monitoring of the recurrent laryngeal nerve in thyroid surgery. World J Surg. 2008; 32: Chiang FY, Lu IC, Kuo WR: The mechanism of recurrent laryngeal nerve injury during thyroid surgery the application of intraoperative neuromonitoring. Surgery 2008; 143: Snyder SK, Hendricks JC: Intraoperative neurophysiology testing of the recurrent laryngeal nerve: Plaudits and pitfalls. Surgery 2005; 138: Barczyński M, Konturek A, Cichoń S: Value of intraoperative neuromonitoring in surgery for thyroid cancer in identification and prognosis of function of the recurrent laryngeal nerves. Endokrynol Pol 2006; 57: Chan WF, Lang BHH, Lo CY: The role of intraoperative neuromonitoring of recurrent laryngeal nerve during thyroidectomy: A comparative study on 1000 nerves at risk. Surgery 206; 140: Snyder SK, Lairmore TC, Hendricks JC et al.: Elucidating mechanisms of recurrent laryngeal nerve injury during thyroidectomy and parathyroidectomy. J Am Coll Surg 2008; 206: Kruse E, Olthoff A, Schiel R: Functional anatomy of the recurrent and superior laryngeal nerve. Langenbecks Arch Surg 2006; 391: Angelos P: Recurrent laryngeal nerve monitoring: state of the art, ethical and legal issues. Surg Clin North Am 2009; 89: Horne SK, Gal TJ, Brennan JA: Prevalence and patterns of intraoperative nerve monitoring for

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