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Prevention of phrenic nerve injury during interventional electrophysiologic procedures Marcin Kowalski, MD, FHRS,* Kenneth A. Ellenbogen, MD, FHRS,† Jayanthi N. Koneru, MBBS† From the *Department of Medicine, Division of Cardiac Electrophysiology, Staten Island University Hospital, Staten Island, New York, and †Department of Medicine, Division of Cardiology, VCU School of Medicine, Medical College of Virginia Hospitals, Richmond, Virginia.

Introduction The advent of innovative, potent ablative technologies and the adoption of endo–epicardial approaches to treat various arrhythmias have engendered a need for developing strategies to prevent collateral damage to critical structures such as the phrenic nerve (PN) and the esophagus during percutaneous electrophysiologic interventions. Here we detail phrenic nerve injury (PNI) prevention strategies during atrial fibrillation (AF), atrial tachycardia (AT), and ventricular tachycardia (VT) ablation. PNI is more common on the right side because of the anatomic course of the nerve and the greater preponderance of AF and AT ablations. PNI also is more common with cryoballoon ablation (nearly 10% in large multicenter trials) than it is with radiofrequency ablation (RFA); thus, the crux of this discussion is centered on strategies to prevent right PNI during cryoballoon ablation for AF. However, the expanded scope of this article includes strategies to prevent both right and left PN injury with interventional electrophysiologic procedures.

Anatomy The PN originates from the third, fourth, and fifth cervical nerves and provides the only motor output to the diaphragm and sensory input from the central tendon, mediastinal pleura, and pericardium (Figure 1). The right PN descends almost vertically along the right brachiocephalic vein and continues along the right anterolateral surface of the superior vena cava (SVC). It is separated only by the pericardium at the KEYWORDS Phrenic nerve; Phrenic nerve injury; Atrial fibrillation; Cryoballoon ablation; Diaphragmatic compound motor action potential ABBREVIATIONS AF ¼ atrial fibrillation; AT ¼ atrial tachycardia; CMAP ¼ compound motor action potential; ICE ¼ intracardiac echocardiography; LV ¼ left ventricle; PN ¼ phrenic nerve; PNI ¼ phrenic nerve injury; PV ¼ pulmonary vein; RFA ¼ radiofrequency ablation; RIPV ¼ right inferior pulmonary vein; RSPV ¼ right superior pulmonary vein; SVC ¼ superior vena cava; VT ¼ ventricular tachycardia (Heart Rhythm 2014;11:1839–1844) Address reprint requests and correspondence: Dr. Marcin Kowalski, Cardiac Electrophysiology Laboratory, Division of Cardiac Electrophysiology, Staten Island University Hospital, Staten Island, NY 10305. E-mail address: [email protected].

1547-5271/$-see front matter B 2014 Heart Rhythm Society. All rights reserved.

anterolateral junction between the SVC and the right atrium.1 The close proximity of the nerve to the SVC in this location facilitates capture of the nerve while pacing from the lateral wall of the SVC. Once the right PN descends the anterolateral wall of the SVC, it veers posteriorly, as it approaches the superior cavo–atrial junction and the inferior course of the nerve is in close proximity to the pulmonary veins (PVs) before reaching the diaphragm. Histologic examinations demonstrate that the right PN is located closer to the right superior pulmonary vein (RSPV) (2.1 ⫾ 0.4 mm) than the right inferior pulmonary vein (RIPV) (3.2 ⫾ 0.9 mm).2 This close proximity of the right PN to the RSPV and SVC renders it vulnerable to injury during ablation of the RSPV, and atrial tachycardias arising in the vicinity of the crista terminalis and the SVC. The left PN travels behind the left brachiocephalic vein and continues over the aortic arch, pulmonary trunk, over the left atrial appendage, and to the left ventricle (LV). The relationship of the nerve to the left heart structures depends on whether it descends along a path related to the anterior surface of the LV or passes leftward along a course related to the obtuse margin of the LV. The nerve passing along the obtuse margin is closer to the lateral vein or left obtuse marginal vein and left marginal artery.2 Thus, epicardial ablation of inferolateral and inferoposterior VTs could have the potential to cause PNI.

Strategies to prevent PNI during ablations Currently, no reliable method predicts PNI before the procedure, and injury to the nerve can occur despite the most compulsive monitoring. Traditionally, operators have used PN pacing during ablation and terminated ablation immediately on diminution of ipsilateral diaphragmatic contractility. However, such an approach may result in “closing the door after the horse has left the barn” scenarios. We propose defining different stages of PN damage, with early PN injury defined as any detection of PN damage before a detectable decrease in diaphragmatic excursion, PN injury as any decrease in diaphragmatic excursion resolved before the end of the procedure, PN palsy as diaphragmatic paralysis confirmed by exhalation and inhalation X-ray with http://dx.doi.org/10.1016/j.hrthm.2014.06.019

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Figure 1 Specimen showing the courses of the phrenic nerves and the close anatomic relationship to other structures. Asc Aorta ¼ ascending aorta; RB ¼ right bronchus; RI ¼ right inferior pulmonary vein; RPA ¼ right pulmonary artery; RS ¼ right superior pulmonary vein; SCV ¼ superior caval vein. (Reproduced with permission from Ho SY, Cabrera JA, Sanchez-Quintana D. Left atrial anatomy revisited. Circ Arrhythm Electrophysiol 2012;5:220–228.)

elevated diaphragm lasting less then 3 months, and PN paralysis as any PN palsy lasting 43 months. Here we describe methods of monitoring PN function and interventions to displace the PN in those situations where ablation must be performed in the vicinity of the PN.

provides important information regarding the anatomic course of the PN. Such an approach is valuable not only for atrial ablation but also for epicardial VT ablation. The 3dimensional display of PN position relative to potential ablation targets is valuable for preventing PNI (Figure 2).5 Although alternative methods have been described (radiographic tissue density of the right PN, computed tomographic

Pacing the PN With this method, right PN function is monitored by advancing a pacing catheter into the SVC and capturing the PN at twice the capture threshold. A high current strength can potentially overcome early nerve injury and conceal incipient damage to the nerve.3 It is imperative that this pacing catheter be placed above the level of ablation. The optimal site for PN capture is the anterolateral portion of the SVC, near the atrial–SVC junction because, at that location, the PN is separated from the SVC wall only by pericardium. Although the operator can use any catheter to capture the PN, we found a deflectable decapolar catheter to be most useful. The catheter can be prolapsed into the SVC with a retroflexed tip for better stability (see Online Supplemental Figure 1). Catheter stability and reliable capture of the PN are essential because sudden loss of capture because of catheter movement may mimic PNI and cause unnecessary cessation of ablation. The PN should be paced at cycle lengths ranging from 1500 to 1000 ms. A slower pacing rate can delay the detection of PN palsy, and a rapid pacing rate can prematurely fatigue the diaphragm.4 It is imperative that paralytics not be administered during ablation. If they were administered during the induction of general anesthesia, sufficient time should be allowed for the paralytic effect to reverse before ablation. If the paralytic effect lingers, neostigmine may be used as a reversal agent. Pace-mapping of the PN and tagging the course of the PN using electroanatomic mapping can be performed and

Figure 2 Electroanatomic map in the right anterior oblique view with phrenic nerve (PN) pacing sites (blue dots represent phrenic nerve capture; red dots represent sites of radiofrequency ablation in a wide antral circumferential ablation pattern) showing area of PN capture in the lateral wall of the superior vena cava (SVC) and near the right superior pulmonary vein (RSPV) and right inferior pulmonary vein (RIPV) os. RA ¼ tight atrium.

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scan enhanced with contrast of the right pericardiophrenic artery6), we have not found them to be reliable.

Fluoroscopy and palpation During ablation, multiple additional modalities may be used to monitor PN function while pacing the nerve from the SVC (Table 1). Continuous or intermittent fluoroscopy of the right hemidiaphragm during PN pacing can accurately diagnose a diminished diaphragmatic excursion; however, it is the least optimal method because it exposes the patient and operator to additional radiation. Palpation of the strength of diaphragmatic excursion during PN pacing, below the costal margin, is the most common method of monitoring PN function. We do not recommend using this method as the sole technique for monitoring PNI.

Intracardiac echocardiography and fetal heart monitor Intracardiac echocardiography (ICE) can be used to continuously visualize the motion of the liver within its capsule and indirectly image the contraction of the diaphragm during PN pacing.7 The transducer is positioned at the level of the diaphragm and pointed at the liver (see Online Supplemental Figure 2). The decrease in hepatic movement from the diaphragmatic excursion can be easily observed and correlated with impending PNI. An external fetal heart Doppler monitor placed at the costal margin also can be used to monitor PN function. As the strength of the diaphragmatic contraction decreases during PN pacing, an easily

1841 recognizable change in the pitch of the diaphragmatic contraction can be perceived. The fetal heart monitor can provide an auditory cue of impending PNI to the physician and staff (see Online Supplemental Figure 3 and audio).

Diaphragmatic compound motor action potential Diaphragmatic electromyography is being increasingly used to provide diagnostic information about PN function in patients with neuromuscular disorders that affect respiration. Recording of diaphragmatic compound motor action potential (CMAP) during PN pacing can predict and prevent PN damage during cryoballoon ablation of the right-sided PVs. We have evaluated the utility of CMAP to recognize early PNI, and other investigators have obtained similar results.8–11 CMAPs can be successfully recoded on a modified lead I by placing a standard surface right arm ECG electrode 5 cm above the xiphoid and a left arm ECG electrode 16 cm along the right costal margin (Figure 3). The CMAP amplitude is measured from peak to peak with each PN capture. The largest amplitude signal at baseline is compared to the real-time CMAP amplitude during ablation. Studies have shown that a decrease in CMAP amplitude by 35% from baseline predicted and prevented PNI (Figure 4).10 CMAP amplitude can be continuously monitored during cryoballoon ablation by placing horizontal calipers on the screen of a recording system at the level of 35% below the baseline CMAP amplitude. The average time interval from CMAP amplitude decrease of 35% to palpable PNI was 59 seconds (range 30–110 seconds) in

Table 1

Pros and cons of various phrenic nerve monitoring strategies

Method

Description

Advantages

Disadvantages

Fluoroscopy

Direct visualization of diaphragmatic motion

Palpation

Palpation of diaphragmatic excursion

Sensitive method for monitoring diaphragmatic motion Reliable and practical method for monitoring diaphragmatic motion

Electromyography

Recording of diaphragmatic CMAP by 2 standard surface electrodes positioned across the diaphragm or by advancing a quadripolar catheter in the right hepatic vein during PN pacing Decrescendo pitch on fetal heart monitor (placed across patient’s chest that can detect diaphragmatic contractions) Direct visualization of diaphragmatic excursion

Additional radiation exposure to patient and operator Does not predict PNI Requires additional staff member Palpable strength of diaphragmatic excursion may vary with respiration CMAP signals might be susceptible to respiratory variations Baseline amplitude must be adequate Affected by paralytic agents

Auditory cardiotocography

Intracardiac echocardiography (ICE)

Earliest detection of PNI Simple, reliable, and easily applicable Only technique that predicts PNI Auditory cue to the operator May portend PNI before palsy

Extra equipment needed Difficult to record in obese patients

Minimal radiation exposure to patient and operator

Requires additional venous access and intracardiac ultrasound

CMAP ¼ compound motor action potential; PN ¼ phrenic nerve; PNI ¼ phrenic nerve injury. Modified with permission from Kowalski M. Prevention of phrenic nerve palsy during cryoballoon ablation for atrial fibrillation. In: Chan N-Y, editor. The Practice of Catheter Cryoablation for Cardiac Arrhythmias. Hoboken, NJ: Wiley Blackwell; 2014:67–81.

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Heart Rhythm, Vol 11, No 10, October 2014 with this approach might be less than the modified lead I method. A right-sided subdiaphragmatic hepatic vein large enough to accommodate a quadripolar catheter is a prerequisite for this method. Hence, the operator may initially attempt to record CMAP amplitude using modified lead I. If the amplitude is o0.2 mV or shows significant respiratory variation, a catheter can be advanced into the hepatic vein to record CMAP amplitude. The recorded CMAP amplitude by either method also can be easily displayed directly on the electrophysiology workstation and followed during ablation. Use of a combination of these methods can significantly improve the safety profile of cryoballoon ablations for AF and prevent the majority of persistent PNI during cryoballoon ablation. In our combined experience, such a strategy has resulted in no persistent PNI in 470 cases. This is in marked contradistinction to reported rates of 10% to 12% incidence of PNI with the second-generation cryoballoon. Existing methods for prevention of PNI and their respective pros and cons are detailed in Table 1.

Figure 3 Configuration of surface electrodes for recording diaphragmatic compound motor action potential on modified lead I in an obese patient. The right arm (RA black oval) surface electrode is placed 5 cm above the xiphoid, the left arm (LA black oval) surface electrode is placed 16 cm from the xiphoid along the costal margin, and corresponding compound motor action potential (CMAP) recordings on modified lead show low-amplitude signal during phrenic nerve (PN) capture (top recording). In some instances, the leads must be modified because of the patient’s body habitus by moving the leads to the right and more separated (white ovals) to obtain the optimal CMAP amplitude (lower recording).

published studies, although we have recently seen a case where transient PNI occurred in o15 seconds.10 Franceschi et al9 described a different method of recording phrenic CMAP amplitude during cryoballoon ablation by advancing a quadripolar catheter in the right hepatic vein during PN pacing (Figure 5). In their study, ablation was discontinued if the observed CMAP amplitude decreased by Z30% from baseline. There were no reported cases of PNI, including the patients in whom ablation was discontinued early because of a decrease in CMAP amplitude. A synthesis of published data suggests that ceasing cryoballoon ablation immediately on reduction of CMAP amplitude of 30% to 35% can successfully prevent long-standing and persistent PNI during right-sided PV cryoablation. Monitoring PN function using a modified lead I is simple and easily applicable. It is noninvasive and does not require any additional equipment. However, the surface electrodes may be subject to CMAP amplitude variations with respiratory movements and body habitus. Obtain CMAP recordings may be difficult in obese patients. Adjusting the electrode to a more superior location may help obtain a better signal in these patients as the viscera push the diaphragm superiorly when the patient is supine. Monitoring CMAP amplitude by advancing a quadripolar catheter in the hepatic vein is an excellent alternative method, especially in patients in whom the recorded CMAP amplitude is o0.2 mV. The respirophasic variations

Recommendations specific to cryoballoon ablation for AF Early detection of PNI and immediate termination of ablation is essential in the prevention of PN palsy. If cryoballoon ablation is being performed, it is important to continuously monitor the PN function by pacing the PN above the cryoballoon during ablation of both right-sided PVs (Table 2). Ablation of the RIPV may be attempted prior to

Figure 4 Recordings of the diaphragmatic compound motor action potential (CMAP) during pacing from the multipolar catheter at a cycle length of 1000 ms located in the superior vena cava. CMAP amplitude was measured at baseline (panel 1) and continuously monitored during right superior pulmonary vein ablation by placing horizontal calipers on the screen of a recording system at the level of 35% below the baseline CMAP amplitude (panel 2). Note attenuation of CMAP amplitude by 435% from baseline amplitude at 180 seconds of cryoballoon application (panel 3). At the time of phrenic nerve palsy (210 seconds), CMAP amplitude was a fraction of baseline CMAP amplitude (panel 4). The amplitude of CMAP, despite some recovery 2 minutes after discontinuation of cryoenergy, did not return to baseline value (panel 5).

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Figure 5 Diaphragmatic compound motor action potential (CMAP). Left: Surface ECG lead V1 and a diaphragmatic CMAP tracing obtained by a quadripolar catheter in the right hepatic vein. Right: Catheter position for phrenic CMAP recording. Anteroposterior fluoroscopic view centered on the diaphragm. The quadripolar catheter is positioned in a hepatic vein to record phrenic CMAP. A hexapolar catheter is placed in the superior vena cava to pace the right phrenic nerve. (Reproduced with permission from Franceschi F, Koutbi L, Mancini J, Attarian S, Prevot S, Deharo JC. Novel electromyographic monitoring technique for prevention of right phrenic nerve palsy during cryoballoon ablation. Circ Arrhythm Electrophysiol 2013;6:1109–1114.)

RSPV because the chance of PNI during ablation of the RIPV is lower in comparison to RSPV due to the closer proximity of the RSPV to the PN than the RIPV. Once PNI occurs during ablation of the RSPV, the inability to monitor PN function may prevent the ablation of the RIPV. Immediate balloon deflation at the first sign of PN dysfunction would prevent persistent PNI.12 Because the decrease in CMAP amplitude is the earliest sign of detectable injury to the nerve and is simple and easily measurable, it should be used as the primary technique for monitoring in conjunction with 1 or 2 other methods. These methods include either palpation of the diaphragmatic excursion or movement of liver visualized on ICE or a fetal heart monitor. Once PNI occurs and the ablation is immediately terminated, PN function should be continuously monitored by pacing above the lesion. If PN function returns within a few minutes, a second attempt at ablation can be made with the balloon located more antrally. Alternatively, the wire/catheter used to engage the vein can be manipulated to subselect a different branch of the vein so that the balloon–vein angle is modified. If PN function does not return in a reasonable time, then the ablation may be completed using radiofrequency with a wide antral circumferential ablation. Similar methods can be used to prevent PNI during RFA. Additionally, the ablation catheter can be paced at high outputs (10 mA at 2 ms) at putative ablation sites to discern phrenic capture. Capture of PN with high output indicates higher risk of PNI at that particular site, and RFA should be performed more proximally (antrally).

Percutaneous displacement of the PN via epicardial approach Buch et al13 described a novel technique for preventing left PNI during catheter ablation for left VT. It entails inflation of

a pericardial balloon to displace the heart from the PN during ablation (see Online Supplemental Figure 4). Although any peripheral vascular angioplasty balloon can be used, the size of the balloon should be sufficient (eg, 25-mm  40-mm balloon) to displace the left heart structures away from the PN. This technique has also been applied to protect the right PN when ablating near the SVC. Alternative methods of preventing PNI involve injection of air or saline or a combination (“controlled hydropneumopericardium”) through a Table 2 Recommendations to prevent phrenic nerve injury during cryoballoon ablation for atrial fibrillation Avoid long-acting paralytics during ablation. Consider performing inhalation and exhalation chest X-ray in patients with previous history of coronary artery bypass graft to evaluate for injury to left PN. Inflate the balloon outside the PV and maintain the balloon as antrally as possible to prevent anatomic distortion of the PV orifice. Monitor the rate of temperature descent. A steep descent (colder than –401 at 30 seconds) may indicate distal location of the balloon. Rigorously monitor PN function by pacing the phrenic nerve from the superior vena cava above the cryoballoon. Stimulation of the PN should be carried out at twice the pacing threshold, and PN function should be monitored for both the right superior and right inferior PVs. Simultaneously employ diaphragmatic compound motor action potential amplitude and one or two additional techniques to monitor phrenic nerve function. Terminate ablation immediately if PNI is suspected. Immediate deflation of the balloon can be initiated by pressing the emergency deflation button twice on the console. PN ¼ phrenic nerve; PNI ¼ phrenic nerve injury; PV ¼ pulmonary vein. Modified with permission from Kowalski M. Prevention of phrenic nerve palsy during cryoballoon ablation for atrial fibrillation. In: Chan N-Y, editor. The Practice of Catheter Cryoablation for Cardiac Arrhythmias. Hoboken, NJ: Wiley Blackwell; 2014:67–81.

1844 hemostatic sheath in the pericardium to create a space between the PN and the ablation catheter.14,15 The major concern about injection of air is that it is a poor conductor of electricity, and once a layer of air surrounds the heart, defibrillating the patient may be difficult. Injection of saline may result in tamponade physiology, and the operators must be vigilant for hemodynamic compromise. Tamponade physiology could easily be reversed by saline aspiration through the pericardial sheath. An additional technical feature is that introduction of a large balloon involves a second pericardial access and careful positioning of the balloon in such a way as to not hinder catheter mapping. With any of these approaches, one should still make ensure that the ablation catheter no longer captures the PN before radiofrequency energy delivery.

Conclusion The risks of PNI during ablation make it imperative that reliable strategies be used for monitoring PN function. CMAP recordings, when performed properly, can herald PNI before development of frank PN palsy when ablating in the right-sided PVs. Occasionally, the PN may need to be displaced from the area of interest to achieve optimal ablation outcomes.

Appendix A Supplementary data Supplementary data associated with this article can be found in the online version at http://dx.doi.org/10.1016/j.hrthm. 2014.06.019.

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Heart Rhythm, Vol 11, No 10, October 2014 2. Sanchez-Quintana D, Cabrera JA, Climent V, Farre J, Weiglein A, Ho SY. How close are the phrenic nerves to cardiac structures? Implications for cardiac interventionalists. J Cardiovasc Electrophysiol 2005;16:309–313. 3. Gooch CL, Weimer LH. The electrodiagnosis of neuropathy: basic principles and common pitfalls. Neurol Clin 2007;25:1–28. 4. Glenn WW, Phelps ML. Diaphragm pacing by electrical stimulation of the phrenic nerve. Neurosurgery 1985;17:974–984. 5. Schmidt B, Chun KR, Ouyang F, Metzner A, Antz M, Kuck KH. Threedimensional reconstruction of the anatomic course of the right phrenic nerve in humans by pace mapping. Heart Rhythm 2008;5:1120–1126. 6. Horton R, Di Biase L, Reddy V, Neuzil P, Mohanty P, Sanchez J, Nguyen T, Mohanty S, Gallinghouse GJ, Bailey SM, Zagrodzky JD, Burkhardt JD, Natale A. Locating the right phrenic nerve by imaging the right pericardiophrenic artery with computerized tomographic angiography: implications for balloon-based procedures. Heart Rhythm 2010;7:937–941. 7. Lakhani M, Saiful F, Bekheit S, Kowalski M. Use of intracardiac echocardiography for early detection of phrenic nerve injury during cryoballoon pulmonary vein isolation. J Cardiovasc Electrophysiol 2012;23:874–876. 8. Franceschi F, Dubuc M, Guerra PG, Delisle S, Romeo P, Landry E, Koutbi L, Rivard L, Macle L, Thibault B, Talajic M, Roy D, Khairy P. Diaphragmatic electromyography during cryoballoon ablation: a novel concept in the prevention of phrenic nerve palsy. Heart Rhythm 2011;8:885–891. 9. Franceschi F, Koutbi L, Mancini J, Attarian S, Prevot S, Deharo JC. Novel electromyographic monitoring technique for prevention of right phrenic nerve palsy during cryoballoon ablation. Circ Arrhythm Electrophysiol 2013;6: 1109–1114. 10. Lakhani M, Saiful F, Parikh V, Goyal N, Bekheit S, Kowalski M. Recordings of diaphragmatic electromyograms during cryoballoon ablation for atrial fibrillation accurately predict phrenic nerve injury. Heart Rhythm 2014;11:369–374. 11. Parikh V, Torbey E, Agarwal V, Bekheit S, Koneru J, Ellenbogen K, Kowalski M. Compound diaphragmatic action potentials can prevent phrenic nerve injury during cryoballoon ablation of atrial fibrillation. Heart Rhythm 2014;11:S374. 12. Ghosh J, Sepahpour A, Chan KH, Singarayar S, McGuire MA. Immediate balloon deflation for prevention of persistent phrenic nerve palsy during pulmonary vein isolation by balloon cryoablation. Heart Rhythm 2013;10: 646–652. 13. Buch E, Vaseghi M, Cesario DA, Shivkumar K. A novel method for preventing phrenic nerve injury during catheter ablation. Heart Rhythm 2007;4:95–98. 14. Di Biase L, Burkhardt JD, Pelargonio G, Dello Russo A, Casella M, Santarelli P, Horton R, Sanchez J, Gallinghouse JG, Al-Ahmad A, Wang P, Cummings JE, Schweikert RA, Natale A. Prevention of phrenic nerve injury during epicardial ablation: comparison of methods for separating the phrenic nerve from the epicardial surface. Heart Rhythm 2009;6:957–961. 15. Matsuo S, Jais P, Knecht S, Lim KT, Hocini M, Derval N, Wright M, Sacher F, Haissaguerre M. Images in cardiovascular medicine: novel technique to prevent left phrenic nerve injury during epicardial catheter ablation. Circulation 2008; 117:e471.

Prevention of phrenic nerve injury during interventional electrophysiologic procedures.

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