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272
Tracheostomies
optimal voice restoration. A physician, Brook (2009), provides a discussion of his own experience as a patient with a total laryngectomy undergoing voice rehabilitation with a TEP. He reported the following experience:
The task of talking again was most challenging and frustrating. I was unable
to speak for over 2 months and later wished I had used an electrolarynx
during that period. . . . I . . . realized that this field was not only a science, but
also an art. . . . I soon realized that this process was going to be a long pro-
cess of trial and error, repeated TEP failures due to leaks, and learning how
to master the art of sealing the housing of the heat-moisture exchanging
filter. . . . Fortunately, things improved significantly with the passage of time
and the reduction of the neck edema.
Patients who are about to undergo a total laryngectomy have a number of choices, only one of which is a puncture procedure. The speech-language pa­thologist will provide advice to the patient and family as they proceed through the process.

Ventilator-Dependent Tracheostomized Patients

The newest airway, developed by Dr. Eric Blom, enables a ventilator-dependent patient with a larynx to maintain positive-pressure ventilation while still di­verting some airflow into the larynx and creating voice. This new device facili­tates airflow around the tube and into the patient’s larynx, vibrating the vocal folds. In all cases where the tube is used to facilitate speech as well as respira­tion, the patient’s respiratory airflow must be adequate to move through the prosthesis and vibrate whatever tissues produce voice. If airflow is low or the patient has poor respiratory strength, these prostheses will provide suboptimal results. Similarly, the patient’s articulatory ability must be adequate to shape the vibratory airflow into speech sounds and words.
Balancing Breathing, Speech, and Swallowing
There are many conditions that may affect the patient’s ability to produce speech or breathe with the respiratory tube in place, and the clinician who introduces these tubes or airflow devices must be able to identify the precipitating condi­tion (Hess, 2005a, 2005b). The patient’s airflow may be inadequate or the device may be clogged with mucous or other secretions.
The upper aerodigestive tract is important in respiration, swallowing, and speech and voice production. The trachea’s role in respiration is obvious, as it delivers air to the lungs. Its role in swallowing, while critical, is often not en­tirely recognized.
The upper aerodigestive tract delivers airflow stimulation to the larynx and other structures of the upper airway. This stimulation contributes to vocal fold closure. Patients who are mechanically ventilated for even a short period of time often lose their vocal fold closure when they attempt to vocalize. This problem often requires speech therapy to stimulate vocal fold movement. Airway closure during swallow is necessary to protect the airway from food or liquid. The pre­vention of aspiration is essential to reduce the risk of pneumonia due to food
Chapter 9 Special Considerations for the Patient With a Laryngectomy
entering the lungs. Again, patients may need intensive therapy to facilitate or improve airway closure during swallow. Maintaining upper airway function is critical to successful swallowing and speaking as well as respiration.
Swallowing Function With Ventilator-Dependent Patients
Swallowing and respiration are reciprocal processes. Swallowing normally oc­curs toward the beginning of exhalation; thus, it is usually helpful to present food to the patient at that time. Since a mechanical ventilator controls the re­spiratory cycle, the patient cannot fully coordinate exhalation time with swal­lowing. If the patient has slow oral or pharyngeal stages of swallowing that cannot be completed during the time allocated for exhalation by the ventilator, the swallow may be disrupted by the next inspiration. If the patient restarts inspiration early, any residual food may be directed into the airway. The inflated cuff of the tracheostomy tube in a ventilator-dependent patient interferes with laryngeal elevation and, thus, reduces closure of the entrance of the airway. In turn, food or liquid may enter the airway and be aspirated after the swallow.
The blue dye test may be used at the bedside for a tracheostomized pa­tient (Thompson-Henry & Braddock, 1995; Tippett & Siebens, 1996). This test screens for the presence of aspiration. The patient is given measured amounts of blue-dyed foods, and the tracheostomy is suctioned immediately after the swallow for the presence of the blue-dyed foods, which would indicate aspira­tion. The test does not reveal the anatomic or physiologic cause(s) of aspiration, however, which is critical information. If the result is clearly positive (i.e., blue­dyed material is coughed or suctioned from the tracheostomy), the clinician should recommend a modified barium swallow to determine the cause of the aspiration and define the type of therapy needed. If blue-tinged secretions are later suctioned from the tracheostomy tube, the conclusion should not neces­sarily be that the patient is aspirating. The normal flow of secretions is down­ward from the mouth and pharynx, and it is quite normal for blue dye to mix with secretions and gradually coat the trachea. Also, the patient may aspirate on certain food consistencies and not on others.
273

Quality of Life

Because of the life-changing nature of the procedure and its sequelae, there are numerous studies assessing quality of life in the patient who has undergone a la­ryngectomy. Van den Brink and investigators (2006) studied 90 patients in the first 3 months following discharge after surgery for head and neck cancer. They found three factors that strongly associated with poorer quality of life: laryngectomy, lower levels of education, and being single. They also found that the dimensions of loss of control and physical self-efficacy worsened during this time period.
Lennie, Christman, and Jadack (2001) studied the eating-related experi­ences and educational needs of people following total laryngectomy. Most par­ticipants were not satisfied with the information they received from health care professionals and were unprepared for the potential alterations in eating following total laryngectomy. Ninety percent of the participants experienced a change in one or more aspects of eating. The most prominent changes were decreased sense of smell, decreased taste, decreased enjoyment of eating, and
274
Tracheostomies
increased time required to eat meals. The investigators concluded that total la­ryngectomy produced significant changes in factors related to eating that could affect nutritional intake and quality of life.
Terrell and others (2004) studied a sample of 570 patients with upper aerodi­gestive cancers. The presence of a feeding tube had the most negative impact on quality of life, followed by medical comorbidities, the presence of a tracheostomy tube, chemotherapy, and neck dissection. They found that those patients who took the survey more than 1 year after their diagnosis had improved quality of life in the domains of physical health and more favorable scores for pain, social functioning, speech, and emotion. Furthermore, factors such as age, education level, sex, race, and marital status were significant predictors of quality of life. The authors postulated that the feeding tube and the process of tube feeding were constant reminders of the patients’ disease in spite of the completion of therapy and/or eradication of the cancer. They also suggested that patients were less likely to enjoy the social aspects of eating due to their dysphagia. Limita­tions on activities such as going out to dinner may explain the decrements in social functioning and emotion for patients with feeding tubes.
Hanna and colleagues (2004) studied the differences in quality of life for pa­tients who underwent total laryngectomy with radiation therapy compared to those who underwent chemo-radiation (chemotherapy and radiation therapy) for laryngeal preservation. They found no significant differences in demographics and overall quality of life scores; however, they found some differences in the subscales. Patients in the surgery and radiation therapy group experienced greater difficul­ties in social functioning, sensory disturbances (e.g., taste and smell), coughing, and greater use of pain medication compared to the chemo-radiation group. By comparison, chemo-radiation patients reported problems with dry mouth.
Eadie and Doyle (2005) compared quality of life in two male patient popu­lations in two different hospital systems; the patients studied underwent total laryngectomy and used tracheoesophageal speech as their primary method of communication. One group of patients had higher quality of life measures in the domains of communication, eating, pain, and emotion. The authors reasoned that the better scores were due to a higher level of education and membership in a support group.
Su, Xian, Chai, Jiang, and Luo (2004) compared quality of life scores in pa­tients who underwent a partial laryngectomy to those with a total laryngectomy and found significantly higher composite quality of life scores in the first group. They also found significant enhancements in physical function, laryngeal func­tion, psychological state, and the ability to live independently in the partial laryngectomy group.
Quality of life seems to be affected by both treatment courses and social fac­tors. In general, there is a trend toward improved quality of life and improved physical functioning with the following conditions: less invasive forms of laryn­gectomy, higher education, and the presence of a supportive environment.

Summary

There are three types of surgical laryngectomy procedures: the supraglottic la­ryngectomy, the hemilaryngectomy, and the total laryngectomy. The supraglottic
Chapter 9 Special Considerations for the Patient With a Laryngectomy
and hemilaryngectomy are procedures that retain parts of the larynx, and re­covery is relatively rapid. The severity of swallowing difficulties varies based on the extent of the surgical resection involved. In contrast, a total laryngectomy involves the removal of the entire laryngeal apparatus, and the stump of the trachea is pulled forward to form a stoma. Because there is no longer a connec­tion between the trachea and the digestive tract, there is no risk of aspiration, although these patients may experience problems with dysphagia.
The restoration of voice also depends on the type of surgery involved. Supra­glottic and hemilaryngectomy patients can benefit from exercises to strengthen the voice and swallowing. TEP can be used in patients with total laryngectomies to create esophageal speech by vibrating tissue in the pharyngoesophagus.
In summary, the successful use of laryngectomy and/or tracheostomy tubes and the management of respiratory function depend on a multidisciplinary ap­proach and careful assessment by all team members. Generally, this team includes the speech-language pathologist, the nurse, the respiratory therapist, the patient’s physician, and others involved in assessment and treatment of the patient.

Key Points

Patients who undergo supraglottic and hemilaryngectomy may require ■ speech therapy, but they reestablish functional swallowing and retain the ability to use their natural voice; however, the patient with a total laryn­gectomy must learn new methods of phonation.
■
Patients may have difficulty swallowing after laryngectomy, particularly with an inflated cuff on the tracheostomy tube.
■
TEP, used only with total laryngectomy patients, creates a passageway between the trachea and esophagus and uses airflow to vibrate the tissue of the pharyngoesophagus.
■
The quality of life following total laryngectomy can be characterized by changes in self-image perception as well as social factors and may en­compass affective disorders.
275
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July 4, 2009, from http://www.cancer.org/docroot/CRI/content/CRI_2_4_1X_What_are_the_
key_statistics_for_Laryngeal_and_Hypopharyngeal_cancer_23.asp?rnav=cri Brook, I. (2009). A physician’s experience as a cancer of the neck patient. Surgical Oncology,
doi:10.1016/j.suronc.2009.05.005. Cavalot, A. L., Ricci, E., Schindler, A., Roggero, N., Albera, R., Utari, C., et al. (2009). The impor-
tance of preoperative swallowing therapy in subtotal laryngectomies. Otolaryngology—
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valve on aspiration in patients with tracheostomy. Head and Neck, 17(4), 297–302. Diedrich, W. M., & Youngstrom, K. A. (1966). Alaryngeal speech. Springfield, IL: Thomas. Dobbins, M., Gunson, J., Bale, S., Neary, M., Ingrams, D., & Brown, M. (2005). Improving pa-
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Eadie, T. L., & Doyle, P. C. (2005). Quality of life in male tracheoesophageal (TE) speakers. Jour-
nal of Rehabilitation Research and Development, 42(1), 115–124.
Hanna, E., Sherman, A., Cash, D., Adams, D., Vural, E., Fan, C. Y., et al. (2004). Quality of life for
patients following total laryngectomy vs. chemoradiation for laryngeal preservation. Arch
Otolaryngology—Head and Neck Surgery, 130(7), 875–879. Hess, D. R. (2005a). Facilitating speech in the patient with a tracheostomy. Respiratory Care,
50(4), 519–525. Hess, D. R. (2005b). Tracheostomy tubes and related appliances. Respiratory Care, 50(4),
497–510. Iseli, T. A., Agar, N.J.M., Dunemann, C., & Lyons, B. M. (2007). Functional outcomes following
total laryngecopharyngectomy. ANZ Journal of Surgery, 77(11), 954–957. Leder, S. B., Tarro, J. M., & Burrell, M. I. (1996). Effect of occlusion of a tracheotomy tube on
aspiration. Dysphagia, 11(4), 254–258. Lennie, T. A., Christman, S. K., & Jadack, R. A. (2001). Educational needs and altered eating
habits following a total laryngectomy. Oncology Nursing Forum, 28(4), 667–674. Logemann, J. A. (1998). Evaluation and treatment of swallowing disorders (2nd ed.). Austin,
TX: Pro-Ed. Logemann, J. A., Gibbons, P., Rademaker, A. W., Pauloski, B. R., Kahrilas, P. J., Bacon, M., et al.
(1994). Mechanisms of recovery of swallow after supraglottic laryngectomy. Journal of
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tube: A pilot study of effects on aspiration and biomechanics of the swallow. Head and
Neck, 20(1), 52–57. Maclean, J., Cotton, S., & Perry, S. (2009). Dysphagia following a total laryngectomy: The ef-
fect on quality of life, functioning, and psychological well-being. Dysphagia, doi 10.1007/
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head and neck cancer patients with tracheostomy. Head and Neck, 16(1), 17–20. Muz, J., Mathog, R. H., Nelson, R., & Jones, L. A., Jr. (1989). Aspiration in patients with head and
neck cancer and tracheostomy. American Journal of Otolaryngology, 10(4), 282–286. Rademaker, A. W., Logemann, J. A., Pauloski, B. R., Bowman, J. B., Lazarus, C. L., Sisson, G. A., et
al. (1993). Recovery of postoperative swallowing in patients undergoing partial laryngec-
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deglutition—observation of subglottal pressure and afferent discharge. Otolaryngology—
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(2004). Clinical predictors of quality of life in patients with head and neck cancer. Arch
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to detect aspiration in the tracheostomized patient: Five case reports. Dysphagia, 10(3),
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test: A comment on Thompson-Henry and Braddock. Dysphagia, 11(1), 78–79. van den Brink, J. L., de Boer, M. F., Pruyn, J. F., Hop, W. C., Verwoerd, C. D., & Moorman, P. W.
(2006). Quality of life during the first 3 months following discharge after surgery for head
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Neck Surgery, 133, 526–532.
Complications and Emergency Procedures
Michiel J. Bové and Linda L. Morris
10
Complications related to tracheostomies can be classified into immediate, early, and late (Table 10.1). Immediate complications occur during or immediately after the tracheotomy procedure and include hemorrhage and pneumotho­rax. Early complications often happen within the first postoperative week and include pneumonia, stomal infection, pneumomediastinum, pneumopericar­dium, obstruction, subcutaneous emphysema, and inadvertent decannulation, which can result in the creation of a false passage or complete loss of the air­way. Later complications include the development of mucus plugs, pneumonia or stoma infection, tracheoinnominate hemorrhage, tracheoinnominate fistula, tracheoesophageal fistula, tracheocutaneous fistula, stomal stenosis, stomal granulation tissue, tracheomalacia, tracheal stenosis, mediastinitis, mediastinal fistula, and tracheocele (DeLeyn et al., 2007; Heffner, 2005; Henderson, Har­rington, Izenberg, Dyess, & Silver, 1995; Neema & Manikandan, 2005; Singh, Fung, & Cole, 2007; St. John & Malen, 2004; Watanakunakorn, 1989; Wright & Van Dahm, 2003; Yaremchuk, 2003). It should be noted that there may be an overlap in the time frame in which early, intermediate, and late complications present.
277
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Tracheostomies
Complications of Tracheostomy
10.1
Immediate Early Late
Hemorrhage ■ Pneumothorax ■ Intra-operative ■ fire Air embolism
■
The rate of complications has been shown to be significantly elevated in specific patient populations, such as in the pediatric, post–head trauma, obese, burn, or seriously debilitated groups (Goldenberg et al., 2000). Published rates of tracheotomy-related complications vary greatly (5%–65%) and depend on study design, length of follow-up, and definition of complications (Francois et al., 2003; Waldron, Padgham, & Hurley, 1990).
The first study to prospectively quantify complications from tracheostomy was by Dane and King (1975), who observed 40 patients after tracheostomies were placed. Their study did not involve intraoperative complications. Five per­cent of patients (2 patients) had significant bleeding from the wound. Another 2 patients had bleeding from stomal granulation tissue. One patient bled upon decannulation, and another patient bled endotracheally as a result of granula­tion tissue extending from the stoma to the tracheal lumen. These 2 patients later developed stomal stenosis. One patient developed tube obstruction, 2 developed bilateral tension pneumothorax during the first tube change, and 4 developed severe necrotizing pneumonia. The investigators followed up all patients with a bronchoscopic exam. Fifteen patients died while still receiving mechanical ventilation, all of whom had severe tracheitis. All 25 patients who were successfully decannulated survived. Of these survivors, 60% had “minimal deformity” of the trachea, 32% had moderate deformity, and 8% had symptom­atic tracheal stenosis.
Pneumonia ■ Stoma infection ■ Pneumomediastinum ■ Pneumopericardium ■ Obstruction ■ Subcutaneous emphysema ■ (crepitus) Inadvertent decannulation,
■
loss of airway False passage
■
Mucus plugs ■
Mucus plugs ■ Pneumonia ■ Stoma infection ■ Tracheitis ■ Tracheomalacia ■ Tracheoinnominate ■ hemorrhage Tracheoinnominate fistula
■
Tracheoesophageal fistula ■ Tracheocutaneous fistula ■ (persistent stoma) Stomal stenosis
■
Stomal granulation tissue ■ Tracheal stenosis ■ Mediastinitis ■ Mediastinal fistula ■ Tracheocele ■
Chapter 10 Complications and Emergency Procedures
Francois and others (2003) reported a 2-year prospective trial of the com­plications following tracheostomy performed in the ICU. Out of their group of 118 patients, 86 patients underwent conventional subthyroid tracheotomy, while 32 underwent surgical cricothyroidotomy. Overall, complications occurred in 36 patients (30%), with 4 patients developing two complications. The incidence of complications was similar between conventional tracheotomy and cricothy­roidotomy. There were 6 patients with serious complications (5%), and minor complications occurred in 30 patients (25%). The two most common complica­tions during the immediate period were pneumothorax and minor bleeding. One minor episode of bleeding occurred in a patient with a cricothyroidotomy. In the patients with standard tracheotomies, there was one case of pneumotho­rax, four episodes of minor bleeding, and one episode of difficult cannulation.
For the early postoperative period, the researchers found 25 early compli­cations, of which 5 were considered major and 20 were considered minor. Major complications included subglottic stenosis, accidental decannulation caus­ing acute respiratory failure, tracheal fistula, and chronic vocal cord dysfunc­tion. Minor complications included accidental decannulation, laryngeal edema, stomal granulations, and temporary vocal cord dysfunction. There were 8 minor complications in the late postoperative phase. These included tracheal granu­lations, persistent wound, and scar formation. No deaths were attributable to surgical tracheostomy in this study.
This study had an unusually high percentage of cricothyroidotomies (27%), and it was reported that this procedure was done mainly in older patients. Overall mortality rates tended to be higher in these patients, although their APACHE II scores were not significantly different from those undergoing the standard tracheotomy procedure. At the end of the 6-month follow-up period, 32 patients (35%) still had a tracheostomy in place, with a similar proportion in both groups.
A retrospective 10-year study in Israel reviewed 1,130 tracheostomies per­formed in one hospital from January 1987 through December 1996. None were percutaneous tracheostomies. Indications included prolonged mechanical ven­tilation, adjunct to head or neck or chest surgery in which prolonged mechani­cal ventilation was anticipated; extensive maxillofacial trauma; or upper airway obstruction. Only three tracheotomies were performed as emergencies; how­ever, none of these three developed any postoperative complications. In this study, major complications occurred in 49 cases (4.3%) and included subglottic or tracheal stenosis (21), hemorrhage (9), severe postoperative hemorrhage (7), massive hemorrhage due to tracheoinnominate fistula (2), tracheocutaneous fistula (also called persistent fistula or persistent stoma; 6), severe infection (5), decannulation or tube obstruction (4), subcutaneous emphysema or pneumo­mediastinum (3), and tracheoesophageal fistula (1; Goldenberg et al., 2000).
In this Israeli study, 8 deaths were directly related to the tracheostomy. Im­mediate or intraoperative complications included intraoperative hemorrhage, air embolism, apnea, damage due to adjacent structures, and intraoperative fire. Early postoperative complications included postoperative hemorrhage, tube dis lodgement or obstruction, subcutaneous emphysema, pneumothorax, pneu­momediastinum, and infection. Late postoperative complications included hem­orrhage due to granulation or tracheoinnominate artery fistula, tracheal stenosis, tracheocutaneous fistula, and tracheoesophageal fistula.
279
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Tracheostomies
Let us consider each of these complications and the corresponding meth­ods to prevent and/or treat them.

Intraoperative Complications

Intraoperative complications include hemorrhage (usually from the anterior jugular veins, the thyroid isthmus, or vascular variants such as the thyroid ima artery), the creation of a false passage, electrocautery-induced airway fire, and surgical injury to adjacent structures.
The inability to ventilate immediately after placement of the tracheostomy tube suggests the tube has entered a false passage, usually anterior to the tra­cheal wall or, rarely, posterior to the trachea into the esophagus. Passing a soft suction catheter into the newly placed tracheostomy tube helps recognize false passage cannulation. Also, all retractors and cricoid hooks should be kept in place until successful cannulation is confirmed to allow for an immediate reat­tempt at cannulation should difficulties arise.
Hemorrhage
Hemorrhage can occur as a result of laceration of major blood vessels in the neck during the procedure. Tracheotomies that are placed lower than usual— below the fourth tracheal ring—have a higher incidence of damage to the in­nominate artery. Minor bleeding is far more common and is estimated to occur in up to 40% of cases.
Intraoperative hemorrhage most commonly results from injury to the an­terior jugular veins early in the dissection, especially during emergent pro­cedures, or to the thyroid isthmus later in the dissection during attempts to mobilize it from the anterior tracheal wall or during attempts to divide and ligate it. High-riding innominate arteries present a significant risk of severe hemorrhage when the dissection is carried inferiorly.
Prevention.
precede instrumentation to rule out prominent pulses in this region. Bleeding can be minimized by carefully identifying and staying in the midline, cautiously dissecting layer by layer, and maintaining a well-lit operative field and retrac­tion of the soft tissues. Patient position and neck extension should be optimized. If local anesthesia is used, the procedure should not be started until the vaso­constrictive agent in the local anesthetic has taken effect. Structures such as the anterior jugular vein and the thyroid isthmus should be carefully identi­fied in order to avoid inadvertent trauma and bleeding. An aberrant innominate artery may traverse anterior to the trachea in the field of dissection, making it vulnerable to laceration and potentially life-threatening hemorrhage (Grant, Dempsey, Harrison, & Jones, 2006).
Management.
should be carefully inspected for any bleeding sources. Increases in blood pressure—either as a result of coughing caused by tube insertion or recovery of normal blood pressure after relative hypotension during anesthesia—can
Finger palpation in the substernal region should, therefore, always
After the insertion of the tracheostomy tube, the surgical wound
Chapter 10 Complications and Emergency Procedures
disguise apparent bleeding sources during the procedure itself. If necessary, the tracheostomy tube should be removed to allow for better inspection of the surgical field for the source of bleeding. Superficial sources of bleeding can be addressed by mobilizing the flange on the tracheostomy tube while leaving the cannula in the trachea. Merely packing the wound to obtain hemostasis car­ries the risk of causing subcutaneous emphysema in the postoperative period.
Pneumothorax
Pneumothorax is usually the result of a traumatic puncture of the pleura. It is more common in pediatric tracheotomy, where the pulmonary apices are relatively elevated and therefore more vulnerable within the lower neck. In adults, this complication usually involves the rupture of a pulmonary bleb in a patient struggling to breathe during an awake, emergency tracheotomy. Pneu­mothorax can also result from damage to the posterior tracheal wall during the tracheal incision or during insertion of the tracheotomy tube. More commonly, the tracheostomy tube can be inadvertently inserted between the anterior tra­cheal wall and the anterior mediastinum. The insertion of the tube into this false passage results in worsening respiratory status after tube insertion and can be confirmed by the inability to pass a flexible suction catheter into the tracheal lumen. While some suggest obtaining postoperative radiographs on all tracheotomy patients, published data suggests this is unnecessary in routine, uncomplicated, elective cases (Smith, Grillone, & Fuleihan, 1999). These au­thors suggest restricting chest radiographs to emergency procedures, difficult procedures, or patients exhibiting signs or symptoms of pneumothorax.
281
Prevention.
performing a tracheotomy and by restricting the dissection to the midline. The tracheostomy tube should be inserted under direct visualization and good illu­mination. The ability to suction tracheal contents via a flexible suction catheter should be immediately confirmed after placement of the tracheostomy tube. End-tidal CO Insufflation through the tracheostomy tube should be delayed until these con­firmatory measures can be performed to avoid insufflating the mediastinum. If there remains any doubt about the placement of the tube, retractors can be placed within the stoma to maintain its patency while the tracheostomy tube is removed and replaced under direct visualization.
Management.
serting a chest tube.
Pneumothorax is best prevented by establishing an airway before
should be confirmed by the anesthesiologist as soon as possible.
2
When pneumothorax is symptomatic, it should be treated by in-
Intraoperative Fire
Although flammable anesthetic agents are no longer used, fire in the operating room continues to be a concern, particularly with tracheotomy. Although rare, airway fires are potentially devastating occurrences. There are approximately 100 intraoperative fires annually in the United States; 10 to 20 are deemed seri­ous, and 2 directly result in death. Seventy percent of these fires are related to the use of electrocautery near a high concentration of oxygen (Daane & Toth,