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Ann Thorac Surg 2006;82:1982-1988
© 2006 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Increased Risk of Aspiration and Pulmonary Complications After Lung Resection in Head and Neck Cancer Patients

Department of Thoracic and Cardiovascular Surgery, University of Texas, M. D. Anderson Cancer Center, Houston, Texas

Accepted for publication June 2, 2006.

^_* Address correspondence to Dr Mehran, MD, Department of Thoracic and Cardiovascular Surgery, 1515 Holcombe Blvd, Box 445, Houston TX 77030 (Email: rjmehran{at}mdanderson.org).

Presented at the Forty-second Annual Meeting of The Society of Thoracic Surgeons, Chicago, IL, Jan 10–Feb 1, 2006.

	Abstract

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BACKGROUND: Patients with head and neck cancers (HNCs) may have impaired deglutition and airway protection. The risk of pulmonary complications after lung resection has not been evaluated in HNC patients. We therefore reviewed the risk of aspiration-related pulmonary complications in HNC patients after pulmonary resection.

METHODS: Retrospective review of a prospectively collected database from a single institution identified 1633 patients who underwent pulmonary resection for suspected primary lung cancer from 1997 to 2004. Of these, 76 patients had a history of HNC. The remaining 1557 patients were defined as controls. Categoric variables were analyzed with the ² test. Univariate and multivariate logistic regression analyses determined the variables related to aspiration pneumonia after pulmonary resection.

RESULTS: Aspiration pneumonia occurred in 7 HNC patients (9.2%) versus 10 patients (0.6%) in the control group (p < 0.001). In the entire population with pulmonary resection, HNC history (p < 0.001; odds ratio (OR), 17.5; 95% confidence interval (CI), 6.0 to 50.6), and postoperative recurrent laryngeal nerve paralysis (p < 0.001; OR, 27.8; 95% CI, 5.2 to 148) were independent risk factors for aspiration pneumonia after pulmonary resection. Length of stay was longer in patients with aspiration pneumonia, with a median of 30 days (range, 10 to 258) versus 6 days (range, 0 to 374; p = 0.021). In the HNC patients, prior recurrent laryngeal nerve paralysis was predictive of aspiration pneumonia (p = 0.034; OR, 8.8; 95% CI, 1.1 to 65.4).

CONCLUSIONS: Patients with HNC have an increased risk of aspiration pneumonia after pulmonary resection. Evaluation of swallowing function to identify aspiration is indicated in HNC patients before pulmonary resection to avoid the morbidity and prolonged hospitalization associated with aspiration pneumonia.

	Introduction

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Patients with head and neck cancers (HNCs) frequently present to thoracic surgeons for resection of subsequent primary lung cancer as a result of the field cancerization effects of tobacco smoking in the aerodigestive tract [1–3]. Patients with HNCs may have disorders of deglutition, decreased airway protection, or impaired cough mechanisms caused by direct tumor effect or as a consequence of cancer therapy. Oropharyngeal dysphagia can be present in up to 68% of HNC patients, and aspiration can be silent in 36% to 62%, making the clinical diagnosis difficult [4, 5].

To date, no study has evaluated if patients with NHCs who undergo pulmonary resection have an increased incidence of aspiration-related pulmonary complications. We hypothesized that HNC patients who undergo pulmonary resections are at increased risk of aspiration related complications when compared to our general pulmonary resection population.

	Material and Methods

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The M. D. Anderson Institutional Review Board has approved retrospective studies with the use of a database from the Department of Thoracic and Cardiovascular Surgery, and individual consent for this study was waived. From January 1, 1997, to December 31, 2004, 1633 patients underwent pulmonary resection for a clinical diagnosis of primary lung cancer at the University of Texas, M. D. Anderson Cancer Center, and their data were prospectively collected and entered in a comprehensive database. Physicians, physician assistants, and nurse extenders involved in direct patient care collected data at the point of contact, which was defined as at the time of preoperative evaluation, at the time of operation, at the time of discharge, and on each postoperative follow-up visit. The database included a complete preoperative evaluation and a record of postoperative events, including pulmonary complications.

Of the 1633 patients who underwent pulmonary resection for suspected primary lung cancer, 76 (4.6%) had a history of HNC, and these patients formed the study population. Four HNC patients who had not received treatment of the primary tumor were excluded. In addition, patients who were noted to have had only skin or superficial lesions were excluded.

We compared the rate of complications in the HNC patients with the other 1557 patients without history of HNC that underwent lung resection for primary lung cancer at our institution during the same time period. We retrospectively reviewed the charts of all patients with HNC to obtain specific data about the history and treatment of their disease. Data collected in the database were then analyzed for postoperative general and pulmonary complications that could be aspiration-related, with the main end-point of aspiration pneumonia within 30 days of surgery or during hospitalization. Similar data analysis was performed on the patients without head-and-neck malignancies for direct comparison of postoperative complications.

Pneumonia was defined as at least three of the following: leukocytosis greater than 10,000/mm³ or white blood cell count of less than 3,000/mm³, temperature greater than 38.5°C or less than 35°C, purulent sputum, persistent infiltrate on chest roentgenogram, or pathogenic microorganisms from endotracheal aspirate [6, 7]. The diagnosis of aspiration was made from any of the following: speech pathologist evaluation with a bedside clinical evaluation, fiberoptic endoscopic evaluation of swallowing, barium video esophagogram demonstration of tracheobronchial penetration or aspiration, witnessed aspiration event, or bronchoscopic evidence of airway food particles or enteric contents. Aspiration pneumonia is defined as clinical evidence of pneumonia in a patient with contemporaneous documentation of aspiration [8, 9].

Statistical analysis was performed using SPSS 13.0 software (SPSS Inc, Chicago, IL). Categoric variables were analyzed using cross-tabulation with a Fisher exact test or ² test. Univariate analysis was performed to evaluate the risk factors for aspiration pneumonia, and variables with a p value of <0.25 were then entered into a multivariate logistic regression model. HNC patient characteristics were also studied using univariate and multivariate analyses to investigate risk factors for aspiration pneumonia specific for that population. An of 0.05 was established as the level of significance. Because postoperative complications are more likely to have an impact on early survival, Kaplan-Meier probability of survival curve was limited to the first postoperative year.

	Results

Top Abstract Introduction Material and Methods Results Comment Discussion Acknowledgments References

 
A total of 1633 patients underwent pulmonary resections for suspected primary lung cancer. Of these, 76 patients had a history of head-and-neck malignancies. The control group consisted of the 1557 patients without HNC history. The preoperative characteristics and comorbidities of HNC patients were similar to those of the control group, with no statistically significant differences except gender distribution (Table 1). More men were in the HNC group: 52 patients (68%) versus 812 (52.2%) (p = 0.006).

We investigated risk factors for aspiration pneumonia for the entire pulmonary resection population. Univariate analysis identified that the only significant factors for aspiration pneumonia were a history of HNC (p < 0.001), new recurrent laryngeal nerve paralysis (p = 0.011), and history of tobacco use (p = 0.019) (Table 3). Multivariate logistic regression analysis revealed that a history of HNC (p < 0.001; odds ratio (OR), 17.5; 95% confidence interval (CI), 6.0% to 50.6%) and postoperative recurrent laryngeal nerve paralysis (p < 0.001; OR, 227.8; 95% CI, 5.2 to 148) were independent risk factors for aspiration pneumonia (Table 4).

We investigated characteristics of the 76 patients with HNC for potential associations with aspiration pneumonia (Table 5). Factors that were associated with risk of aspiration pneumonia in univariate analysis with a p value < 0.25 included preoperative aspiration (p = 0.064), preoperative evidence of vocal cord paralysis (p = 0.064), surgery of mandible (p = 0.092), surgery of the hypopharynx (p = 0.092), and tongue resections (p = 0.182). In multivariate analysis using the Wald backward elimination method, the presence of preoperatively documented recurrent laryngeal nerve paralysis was the only statistically significant risk factor for postoperative aspiration pneumonia in the HNC group (p = 0.034; OR, 8.8; 95% CI, 1.1 to 65.4).

	Comment

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The cause of abnormal swallowing in HNC patients is multifactorial and may include decreased swallowing coordination, reduced laryngeal elevation and closure, reduced inversion of the epiglottis, reduced movement of the base of the tongue, and pooling of residue in the valleculae and piriform sinus [10–12]. In patients with head-and-neck malignancies treated with chemoradiation, barium videoesophagogram revealed a 62% incidence of aspiration within 1 month of treatment and a 60% incidence of aspiration 1 year after treatment [4]. Interestingly, a cough reflex did not develop in 50% of these patients, and therefore, they were classified as having silent aspiration.

Aspiration pneumonia can occur in up to 35% of patients with documented aspiration and has an associated in-hospital mortality as high as 33% [4, 5]. Aspiration and its associated clinical complications are feared in any postoperative setting. Aspiration can result in severe pneumonitis, pneumonia, acute lung injury, or adult respiratory distress syndrome. Despite a known propensity for oropharyngeal dysphagia and aspiration, the relative risk of aspiration pneumonia in HNC patients undergoing pulmonary resection has not been studied. In this study we found that a history of HNC resulted in a 17.5-fold risk of aspiration pneumonia. Interestingly, the only other independent risk factor for aspiration pneumonia was postoperative recurrent laryngeal nerve paralysis (OR, 27.8).

Aspiration pneumonia had serious consequences, with prolonged length of hospital stay and associated higher hospitalization charges. Unexpectedly, we observed a higher incidence of bronchopleural fistula in patients with aspiration pneumonia (11.8%) and in the HNC group (3.9%) compared with patients without those characteristics (0.8%). Given the small number of patients with bronchopleural fistula, it is unclear from this study and from the literature whether tracheobronchial aspiration contributes to the development of bronchial stump breakdown and fistulization, but further investigation of this association is warranted.

Despite no significant impact in hospital mortality or in long-term survival, patients with aspiration pneumonia had higher 90-day and 1-year mortality. The incidence of aspiration pneumonia in the control group was consistent with other published reports [13].

Our study has several limitations, one of which is the degree of accuracy of the diagnosis of aspiration pneumonia. The diagnosis of aspiration pneumonia was based on an indirect association of pneumonia in a patient with contemporaneous documentation of aspiration. This clinical diagnosis can be difficult and may be underreported. Because the evaluation for aspiration was entertained as a result of clinical suspicion, a limited number of patients underwent formal swallowing evaluations. It is unclear how many patients had oropharyngeal dysphagia and silent aspiration and who were not identified. In addition, the likelihood of obtaining a swallowing evaluation is probably lower in patients without HNC history compared with HNC patients. Patients with HNCs also had a statistically significant increased incidence of pneumonia than the control group. Some of these pneumonias may have been related to silent, undocumented aspiration.

HNC patients are a heterogeneous population, with differing tumor characteristics and variability in the extent of therapy for their primary malignancy. We endeavored to determine whether particular types of head and neck malignancy or treatment conferred increased risk of aspiration pneumonia, but no specific factor could be identified because patient numbers were small. The only significant preoperative factors associated with aspiration pneumonia in the HNC group was the presence of a paralyzed recurrent laryngeal nerve related to treatment of HNC, a complication that developed in 3 of the 5 patients. Similarly, after pulmonary resection, pneumonia developed in 3 of the 5 HNC patients with aspiration documented preoperatively by modified barium swallow. Preoperative identification of aspiration in one of these patients allowed the patient to be fed through a gastrostomy tube after pulmonary resection, and aspiration was therefore avoided in this patient.

The 10 patients with an end tracheostomy at the time of pulmonary resection did not have a significantly lower risk for pulmonary complications. We presume factors other than aspiration, such as poor airway clearance, contributed to pulmonary complications in these patients.

Because of an increased risk of aspiration pneumonia in the HNC patients, it is beneficial to use formal swallow evaluations to preoperatively identify patients with oropharyngeal dysphagia and aspiration. A dedicated speech therapist evaluation complemented by modified barium swallow or fiberoptic endoscopic evaluation of swallowing has good sensitivity and specificity for detection of aspiration [14, 15]. These evaluations before pulmonary resection should identify patients with aspiration and help establish swallowing strategies to decrease aspiration risk.

It is unclear whether these preoperative interventions will actually decrease pulmonary complications in this group of patients, and further studies are necessary to identify the best prevention strategies. Given that the degree and severity of oropharyngeal dysphagia varies between patients, preventive strategies should be individualized after evaluation by a speech therapist. For patients with occasional or mild aspiration, it may suffice to modify food consistency, with thickening of liquids and swallowing posture changes. Postoperative swallowing reevaluations will document safety of oral intake before a diet is resumed. More severe cases of silent free tracheobronchial penetration require temporary perioperative enteral feeding through nasoenteric or gastrostomy tubes and judicious use of postoperative sedative analgesia.

Alternatively, if these evaluations are not practical or possible, or if the evaluation suggests aspiration, this group of patients should not be fed during the immediate postoperative period (3 to 5 days). The xerostomia of radiotherapy should be addressed with rinsing or washing maneuvers only until the patient is cleared to swallow again. Great vigilance should always be used in patients who have had a pneumonectomy or who have a borderline pulmonary reserve.

In conclusion, patients with history of HNCs have an increased risk of aspiration and aspiration pneumonia after pulmonary resection. Evaluation of swallowing function to identify aspiration is indicated in HNC patients before pulmonary resection to avoid the morbidity and prolonged hospitalization associated with aspiration pneumonia. If this is not possible, HNC patients should not be fed orally after their pulmonary resection until they have recovered from the procedure.

	Discussion

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DR ROBERT J. KORST (New York, NY): We at Cornell agree with this and also believe that these head and neck patients are at a higher risk for pulmonary complications. I know that you focused on aspiration pneumonia, but I think the problem is even deeper than that. These patients, even if they have never been operated on, have received radiation therapy, and they have difficulty with clearing their secretions. Even if you kept your patients NPO for a period of time postoperatively, I think you would still find an increased incidence of pneumonia. Did you have any patients who had a laryngectomy and an end tracheostome in this study? These patients are not going to aspirate, but they are still going to have problems with a loss of the ability to really cough and clear their secretions. If you had any of those patients, how many did you have and did they get pneumonia?

DR HERRERA: Thank you, Dr Korst. That is an excellent question. Of course, the assumption or the diagnosis of aspiration pneumonia is one that is indirect, and the fact that there is proven aspiration may not necessarily mean that it was the cause of the pneumonia. You are right. We had 10 patients who had an end tracheostomy. Of course, none of these patients could aspirate, and only one suffered pneumonia postoperatively. As you mentioned, there may be other factors that could contribute to pneumonia in these patients. We also found a statistically significant increased incidence of pneumonia in the head and neck cancer group regardless of the presence of documented aspiration. However, it seems that aspiration is the main reason for the increased incidence of pneumonia in these patients.

DR JOHN R. ROBERTS (Nashville, TN): I think you have really addressed an important topic. I have a few questions. First, I have a lot of trouble differentiating between aspiration pneumonia and a standard pneumonia. I wonder if you could give us some insights into how you made that decision. Second, did you do anything with respect to GI tract management? Some folks have written about keeping patients NPO for a certain period of time, using nasogastric tubes, that sort of thing. Third, I don’t know if I missed it or not, but did you present perioperative mortality statistics? If not, I would like to hear those.

DR HERRERA: Thank you, Dr Roberts. Regarding the first question, one of the main limitations is how to define aspiration pneumonia. Across the literature, and this has been mostly described in patients with head-and-neck cancer, in the elderly, and in patients with cerebrovascular disease. The diagnosis is an indirect association between a risk factor for aspiration or documented aspiration and the contemporaneous development of pneumonia. One can be more specific in terms of the features of the pneumonia that could help identify more clearly that an aspiration is the cause, for example, infiltrates in the dependent portions of the lung, or a preceding episode of pneumonitis associated with an obvious witnessed aspiration event, but it is often challenging to be absolutely certain of the etiology of the pneumonia.

In terms of the GI tract management, there were 5 patients who had known aspiration preoperatively with head-and-neck cancer. Two of them developed aspiration pneumonia. One did not develop aspiration pneumonia but was kept NPO through the duration of the postoperative period, only being fed by a G-tube. Whether that is necessary or not, I think it depends on your suspicion and the risk for aspiration in these patients.

Regarding the third question, there was no significant difference in perioperative mortality, defined as 30-day or in-hospital mortality. Patients with aspiration pneumonia had a 3% mortality compared to 2% for those without the complication.

	Acknowledgments

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We thank Dr Shanda Blackmon and David Galloway for valuable assistance and suggestions during the preparation of this manuscript.

	References

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