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Ann Thorac Surg 1998;65:930-934
© 1998 The Society of Thoracic Surgeons

Pathogenesis of Systemic Air Embolism During Bronchoscopic Nd:YAG Laser Operations

George Tellides, MDa, Baran S. Ugurlu, MDa, Richard W. Kim, MDa, Graeme L. Hammond, MDa

a Section of Cardiothoracic Surgery, Department of Surgery, Yale University School of Medicine, New Haven, Connecticut, USA

Accepted for publication November 20, 1997.

Address reprint requests to Dr Tellides, Section of Cardiothoracic Surgery, Department of Surgery, Yale University School of Medicine, 333 Cedar St, 121 FMB, New Haven, CT 06510
e-mail: (george.tellides {at}yale.edu)


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Background. The occurrence of systemic air embolism during bronchoscopic neodymium:yttrium-aluminum garnet laser operations has been suspected. Here we describe its mechanism.

Methods. Two patients with embolic cardiac and neurologic complications after bronchoscopic neodymium:yttrium-aluminum garnet laser tumor ablation are described. A subsequent third patient was monitored for intracardiac and aortic air by transesophageal echocardiography. A review of the literature and safety recommendations are discussed.

Results. The appearance of systemic air emboli was related to the use of the laser fiber air coolant at high flow and resolved by decreasing the air flow. The presence of intracardiac and aortic air was associated with hypotension and inferior ischemic electrocardiographic changes.

Conclusions. Systemic air embolism during bronchoscopic laser operations is a potentially catastrophic complication and is related to the use of gas-cooled laser fibers and contact probes. We recommend using the noncontact mode whenever possible and maintaining the coaxial coolant air flow at the minimum level or using a fluid coolant if contact is necessary.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
The excellent palliative results and relative safety of bronchoscopic neodymium:yttrium-aluminum garnet (Nd:YAG) laser ablation of obstructive malignant tumors of the tracheobronchial tree have been well described in large series of patients [13]. Hypoxemia, hemorrhage, airway perforation, pneumothorax, cardiovascular morbidity, and anesthetic complications are reported as the major complications [15]. More than 100 bronchoscopic Nd:YAG laser operations have been performed at our institution since 1989 with minimal morbidity [6]. Recently, 2 patients suffered severe intraoperative arrythmias and hypotension during laser therapy for endobronchial tumors. Despite rapid resuscitation, seizures and major strokes developed in both patients. The cardiac and neurologic complications were characteristic of systemic air embolism for numerous reasons. The patients had no history of cardiovascular or cerebrovascular disease. The arrhythmias and hypotension were temporally associated with laser therapy and not with anesthesia induction or preliminary bronchoscopy. There was no significant hypoxia or hemorrhage before the cardiac events. The cardiovascular collapse was rapidly resuscitated in the operating room, and the duration of hypotension was unlikely to have resulted in anoxic brain injury. Finally, the manifestations of early seizures and focal neurologic deficits were typical of the clinical presentation of cerebral air embolism [7]. To investigate the pathogenesis of the complications, we monitored the possible presence of systemic air emboli in the left cardiac chambers and aorta by transesophageal echocardiography in a third patient undergoing endobronchial tumor laser ablation.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Endobronchial laser operations were performed under general anesthesia with endotracheal intubation using an SLT Contact Laser System (CL MD/DUAL Nd:YAG Laser, 600-µm gas cooled FEF small flexible fiber, SMTR 1.5 contact probe; Surgical Laser Technologies, Oaks, PA) inserted through the suction channel of a flexible fiberoptic bronchoscope (Olympus BF-1T2Od, New Hyde Park, NY). Power settings ranged from 25 to 35 watts in 0.5-second intermittent pulses, and a continuous air flow of 0.8 to 1.5 L/min through the coaxial fiber channel cooled the laser fiber tip and contact probe. Blood pressure, electrocardiogram, pulse oximetry, and end-tidal carbon dioxide were continuously monitored. Transesophageal echocardiography was performed with a two-dimensional probe (Imaging System 77020; Hewlett-Packard Corp, Andover, MA) and real-time video recording.


    Results
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 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
The first patient was a 68-year-old woman with progressive shortness of breath and no significant past medical history. She presented with acute dyspnea and hypoxemia. A chest radiograph showed atelectasis of the left lower lobe and partial aeration of the left upper lobe. Bronchoscopy revealed an endobronchial lesion almost completely obstructing the left main bronchus, and biopsies documented a histology of squamous cell carcinoma. She underwent bronchoscopic Nd:YAG laser ablation therapy using a contact probe at a power setting of 25 watts in single 0.5-second pulses. The air coolant flow was not recorded. After a total energy delivery of 125 joules within a 5-minute period, bradycardia abruptly developed and then deteriorated into pulseless ventricular tachycardia. Chest compressions, cardioversion, and pharmacologic resuscitation were successful, and the procedure was aborted. Postoperatively, she had stable hemodynamics with no ischemic electrocardiographic changes, but remained comatose with frequent right-sided seizure activity for 2 weeks. Serial brain computed tomographic scans showed no organic lesions, and a transthoracic echocardiogram revealed no abnormalities. Her neurologic status gradually improved, although a left hemiplegia persisted. Palliative irradiation was administered to the mediastinum and left hilum. She was transferred to a skilled nursing facility after 10 weeks.

The second patient was a 45-year-old woman who presented with a productive cough, shortness of breath, and fevers that persisted despite antibiotic therapy. Her history was significant for a left upper extremity malignant melanoma resected 3 years previously with metastasis to the axillary lymph nodes. Chest radiographs and a chest computed tomographic scan revealed right middle lobe atelectasis and mediastinal lymphadenopathy. Flexible bronchoscopy revealed a large endobronchial lesion in the bronchus intermedius, and bronchial washings confirmed metastatic malignant melanoma. Palliative Nd:YAG laser tumor ablation was attempted using a contact probe and a power setting of 25 watts in 0.5-second intermittent pulses. The coolant air stream was set at 1 L/min. A total energy of 324 joules had been delivered over 4 minutes, when bradycardia abruptly developed with a brief episode of asystole. She was treated with atropine and epinephrine. Laser therapy was resumed. After a further delivery of 37 joules she became hypotensive, requiring phenylephrine and epinephrine, and the procedure was aborted. Postoperatively, she was comatose with right-sided seizures. A right frontal infarct was demonstrated by a computed tomographic scan and magnetic resonance imaging of the brain. Electrocardiograms, serum cardiac enzyme measurements, transthoracic echocardiogram, and carotid duplex studies showed no abnormalities. After 3 weeks her neurologic status gradually improved, although a left hemiplegia persisted. Palliative irradiation was administered to the right hilum and mediastinum. She was transferred to a skilled nursing facility after 8 weeks.

The third patient was a 60-year-old man with a history of a pyriform sinus squamous cell carcinoma diagnosed 3 years previously. He underwent external beam radiation therapy, left radical neck dissection, and brachytherapy seed placement. Eighteen months later, metastatic disease to the right lung, mediastinum, and pelvis was documented, and he received chemotherapy and mediastinal irradiation. Despite the palliative therapy, his recurrent disease continued to progress, and an increase in the size of the right upper lobe mass and hilar adenopathy was shown by serial chest computed tomographic scans. Pleuritic chest pain and shortness of breath developed. Chest radiographs and a chest computed tomographic scan revealed right upper lobe atelectasis and tumor invading the right upper lobe bronchus. An exercise tolerance test with thallium revealed no electrocardiographic or perfusion abnormalities. Fulguration of the endobronchial tumor was planned, using intraoperative transesophageal echocardiography to detect any systemic air emboli. Bronchoscopy revealed a right upper lobe tumor invading and almost completely obstructing the right main bronchus. Neodymium:yttrium-aluminum garnet laser therapy was performed using a contact probe and a power setting of 35 watts in 0.5-second intermittent pulses. The coolant air stream was initially set at a flow rate of 1.5 L/min. Care was taken not to bury the contact probe into the tissue. After 7 minutes of laser therapy, air bubbles were visualized in the left atrium, left ventricle, and ascending aorta (Fig 1A). Electrocardiographic monitoring showed associated ST segment depressions in lead II of 1.68 mV, compared with a baseline of 0.12 to 0.48 mV. There were no changes noted in lead V6. The blood pressure dropped temporarily to 90/60 mm Hg from 140/70 mm Hg, and the oxygen saturation decreased to a low of 93%. The air coolant flow was immediately decreased to 0.8 L/min, with abrupt cessation of air accumulation (Fig 1B), resolution of lead II ST depression to 0.44 mV, and subsequent improvement of the blood pressure to 130/70 mm Hg and the oxygen saturation to 98%. Laser therapy was continued, and after a total of 400 pulses with an energy delivery of 6,103 joules, the patency of the right main and upper lobe bronchi was restored. Postoperatively, there were no apparent cardiovascular or neurologic sequelae. The right upper lobe was reinflated on chest radiograph, and the patient was discharged home after 5 days.



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Fig 1. Transesophageal two-dimensional echocardiographic images depicting the left atrium (LA), left ventricular outflow tract (LV), and proximal aorta (Ao). (A) Prominent intracardiac air bubbles with the laser gas cooling system set at 1.5 L/min. (B) Resolution of the systemic air emboli with the laser fiber coaxial air flow decreased to 0.8 L/min.

 

    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Systemic air emboli were suspected as the cause of intraoperative arrythmias, cardiac arrest, postoperative seizures, and strokes in 2 patients undergoing endobronchial Nd:YAG laser tumor ablation. This suspicion prompted us to monitor the next scheduled patient with a transesophageal echocardiogram. The presence of air bubbles in the left atrium, left ventricle, and aorta was documented during use of the Nd:YAG laser, with concurrent signs of inferior myocardial ischemia. Reduction of the laser fiber coolant air flow resulted in resolution of the intracardiac air, hypotension, and ischemic electrocardiographic changes, confirming the pathogenesis of the systemic air emboli. The inferior but not anterolateral ischemic changes were consistent with the fact that in the supine position the anterior, least dependent position of the right coronary artery ostium is susceptible to air emboli, in contrast to the posterior, dependent position of the left main artery ostium. These 3 patients add to the growing literature of air emboli complications after Nd:YAG laser operations.

Air embolism associated with Nd:YAG laser operations has been reported after procedures for endometrial ablation [811], hepatic metastasis ablation [12], laparoscopic cholecystectomy [13], congenital choanal stenosis [14], and endobronchial tumor ablation [1518]. The diagnosis of air emboli was clinically suspected in the majority of cases, although definitive evidence of air emboli in some patients was by aspiration of intravascular air [810], documentation of retinal artery bubbles on fundoscopy [15], and demonstration of intravascular air by radiographs [9, 14] or computed tomographic scan [17]. One case report demonstrated increases in end-tidal CO2 that were temporally related to Nd:YAG laser activation using a CO2-cooled laser fiber and documented a moderately increased arterial carbon dioxide tension that may have been due to absorption or embolization of the coolant gas [19].

Introduction of air into systemic veins may result in cardiovascular collapse due to right heart and pulmonary emboli. Air entry into the pulmonary veins may result in myocardial ischemia and strokes due to systemic emboli to the coronary and cerebral circulations. Left ventricular and aortic air has been documented after endometrial ablation operations even in the absence of a patent foramen ovale on postmortem examination [9]. The complication of air emboli after an Nd:YAG laser operation may be catastrophic, with 9 fatalities reported from the 21 cases in the literature (2 reports were duplicated from a total of 11 deaths in the literature). Seven deaths occurred after venous embolization [810, 12, 14], and 2 deaths after systemic embolization [15, 17]. A further 2 patients sustained permanent strokes [10, 17], and the remaining 10 patients made full recoveries after sustaining cardiac and neurologic complications [11, 13, 1618]. The treatment of choice for air emboli is hyperbaric oxygen therapy. Three patients with strokes after systemic air emboli during endobronchial Nd:YAG laser operations were treated early with hyperbaric oxygen and had complete resolution of their neurologic deficits [1618], although 1 patient treated with hyperbaric oxygen after laser endometrial ablation and venous air emboli had residual neurologic deficits [10]. The common denominator in the 3 patients described in this report and 19 of 21 patients in the literature who suffered air emboli during Nd:YAG laser operations was the use of a gas-cooled laser fiber tip. In the remaining 2 patients, the type of laser fiber and coolant mechanism were not mentioned [15, 16]. In the majority of cases artificial sapphire contact probes were attached to the fiber tips, and none of the reports specify that a noncontact mode was used. Air, carbon dioxide, and nitrogen were used as coolants at flows ranging from 0.5 to 5 L/min.

Light energy emitted by the laser source is transmitted to the target tissue through flexible quartz fibers. The radiant energy absorbed by the tissue is converted to thermal energy with various tissue effects. At temperatures between 60 and 100°C the tissue is denatured and coagulated, and at temperatures greater than 100°C the tissue is vaporized with cutting or ablation results. The thermal tissue effect depends on factors such as the laser wavelength and the power or duration of the laser energy. Neodymium:yttrium-aluminum garnet lasers result in effective coagulation and are preferred in airway operations because of their hemostatic effect and efficient application with flexible quartz fibers. Increasing the power setting of the Nd:YAG laser can result in tissue vaporization rather than coagulation, and both effects can be used for ablation of endobronchial tumors [1, 3]. Alternatively, artificial sapphire probes attached to the laser fiber tips can alter power densities and thermal gradients, and thus decrease the dependence of tissue effect on the particular laser wavelength used [8, 10]. Specific probes of various shapes, sizes, and finishes can achieve predictable tissue effects of coagulation or vaporization with the Nd:YAG laser. The laser fiber tips and probes can be used in contact or noncontact modes with the tissue. Direct contact results in a greater efficiency of energy utilization and more precise control. Cooling of the laser fiber and contact probe is required to prevent thermal damage. Gas or fluid coolant is delivered to the fiber tip through a coaxial channel provided by a polyethylene sheath around the laser fiber. Gas such as compressed air, carbon dioxide, or nitrogen is preferred over fluid because of improved visibility. The delivery of gas is variable, but inadequate flows lead to frequent charring and fracturing of the contact probe from the fiber tip. The pressure of air exiting the distal coaxial sheath can be excessive and has been measured at greater than 500 mm Hg when the flow rate was set at 0.4 L/min [17].

Our observations indicate that a high flow of coolant gas during use of the contact probe leads to vascular air emboli. This is consistent with the hypothesis that air emboli during endobronchial laser operations result either from direct air flow from the coaxial cooling sheath into open pulmonary venous tributaries or from occlusion of the proximal recanalized bronchus by the bronchoscope with distal high pressures forcing gas into vascular channels [17]. Transesophageal echocardiographic monitoring did not document systemic air emboli at lower coolant air flow rates or when the laser was not engaged. These findings do not support an alternative hypothesis that positive-pressure ventilation under conditions of pulmonary instrumentation with limited vision, superatmospheric pressure of intrathoracic gas, and pathologic consolidation processes encircling the pulmonary veins are responsible for systemic air emboli during laser bronchoscopy [15]. However, these mechanisms may be operative under certain circumstances, and fatal systemic air embolism has been reported after transbronchial lung biopsies where gas cooling is not used [20, 21]. Because the major risk factor for air embolism during laser operations appears to be inherent to the use of gas-cooled laser fibers, the risk of air embolism is not limited to the Nd:YAG laser but could occur with lasers of other wavelengths. A further mechanism for air dissection and embolism during laser operations is related to the use of gas for insufflation or ventilation, and reports of this complication range from subcutaneous emphysema and hypercapnia in a patient undergoing knee CO2 laser arthroscopy [22] to cardiac arrest in patients undergoing urethral Nd:YAG laser operations [23].

Systemic air emboli have not been reported as a cause of mortality or morbidity in many of the major series of bronchoscopic Nd:YAG laser operations, although all reports describe cardiovascular complications, including arrhythmias and cardiac arrest, attributed to cardiac disease [15]. One reason may be that the clinical diagnosis of air emboli is difficult to differentiate from other causes of cardiac and neurologic dysfunction. Nevertheless, the largest series of 2,710 bronchoscopic Nd:YAG laser procedures by Cavaliere and colleagues [3] reported very few complications that could be attributed to systemic air embolism, with no strokes and 17 episodes (0.6%) of heart failure and myocardial infarction resulting in 7 deaths (0.3%). Another possible reason is that minor systemic air embolism may result in subclinical or subtle cardiac and neurologic sequelae that are not diagnosed. Our third patient had no obvious complications despite documented systemic air emboli. Finally, differences in experience and technique such as the use of noncontact modes and rigid bronchoscopy may account for differences in embolic complications. Retrospective studies that have systematically investigated the frequency of Nd:YAG laser-associated cardiovascular and cerebrovascular events during treatment for endobronchial cancer have found a much higher incidence of complications. Lang and colleagues [17] reported that 8 of 62 patients undergoing 111 bronchoscopic Nd:YAG laser operations had serious cardiac and cerebral complications. Bradycardia developed in 5 patients, 4 of whom progressed to intraoperative cardiac arrest and were resuscitated, and 1 patient sustained a postoperative myocardial infarction and died. Four patients had both strokes and electrocardiographic changes, which resolved in 3; 1 had persistent neurologic deficits. The procedural incidence of cardiovascular and cerebrovascular complications was 8.1% and 3.6%, respectively. Hanowell and associates [24] studied the frequency of cardiovascular complications associated with general anesthesia in 73 patients undergoing 87 Nd:YAG laser endobronchial tumor resections. The procedural incidence of cardiovascular complications was 27.6%, consisting of arrythmias, hypotension, hypertension, myocardial ischemia, and infarction. A more accurate assessment of the incidence and clinical relevance of systemic air emboli during bronchoscopic Nd:YAG laser operations would require a prospective study with transesophageal echocardiographic monitoring and detailed perioperative studies of cardiac and neurologic function.

The details of laser cooling systems and coolant flow rates can be of critical importance and are not discussed in many reports of Nd:YAG laser operations [15]. It is essential that thoracic surgeons be familiar with the risks of gas-cooled fibers and contact probes, as the indications for the Nd:YAG laser are increasing to include ablation of benign bronchial lesions [25] and thoracoscopic resection of pulmonary lesions [26]. In addition to the warning issued by the Food and Drug Administration regarding the danger of air embolism during the intrauterine use of gas-cooled laser fibers [27], we caution that this hazard can occur in any part of the body. Fatal embolic complications have been reported after laparoscopic, otolaryngologic, and bronchoscopic procedures as well as gynecologic operations. The use of contact probes with high-flow gas cooling systems in enclosed areas of the body should be abandoned in all surgical specialities. We believe that the major mechanism of systemic air embolism during bronchoscopic Nd:YAG laser operations is as follows: capillary integrity is disrupted by laser energy, the laser fiber is partially buried in the tumor, coolant air enters the tumor from the distal coaxial sheath, and the air is forced through disrupted capillaries into the pulmonary venous circulation, and subsequently to the left heart. We conclude that systemic air emboli are not primarily related to tissue vaporization or the total amount of heat energy delivered. The complication of air emboli can be avoided by using endobronchial lasers in the noncontact mode. Our experience has led us to change our technique, and we use the noncontact mode whenever possible, maintaining the laser fiber coolant air flow at the minimum level. If direct contact between the probe and tissue is necessary, then a fluid coolant should be considered. Surgeons who continue to use gas-cooled contact probes should take particular care to avoid burying the probe into the tissue, to avoid obstructing the proximal recanalized bronchus with the bronchoscope, and to maintain the coolant air flow at the lowest possible level.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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