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1
Department of Radiology and Ludwig Boltzmann-Institute for Radiologic Tumor
Research, University of Vienna, Waehringer Guertel 18-20, A-1090 Vienna,
Austria.
2
Department of Medical Computer Sciences, University of Vienna, A-1090 Vienna,
Austria.
3
Department of Otolaryngology, University of Vienna, A-1090 Vienna,
Austria.
Received April 14, 1999;
accepted after revision June 30, 1999.
Address correspondence to G. Strasser.
Abstract
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MATERIALS AND METHODS. On videofluoroscopy, anterior cervical osteophytes were found in 55 (32 men, 23 women; mean age, 69 years) of 3318 patients with dysphagia (1.7%). Coexisting diseases that affected swallowing function were found in 28 patients (stroke, n = 7; thyroidectomy, n = 7; tongue base or laryngeal cancer surgery, n = 5; other diseases, n = 9). Swallowing function was assessed with videofluoroscopy evaluating epiglottic tilting, laryngeal closure, impression of the hypopharynx, pharyngeal residue, and aspiration.
RESULTS. With advancing age, the probability of aspiration (odds ratio, 1.07; p < 0.05) and of enlarging osteophytes (odds ratio, 1.26; p < 0.01) increased; the probability was higher for osteophytes at more than one vertebrae (odds ratio, 8.00; p < 0.01) and for concurrent diseases (odds ratio, 8.02; p < 0.01). Aspiration was found in 75% of patients with osteophytes larger than 10 mm and in 34% with osteophytes smaller than or equal to 10 mm. In 88% of patients with small osteophytes who aspirated, other diseases affected swallowing function.
CONCLUSION. Aspiration is common in patients with dysphagia and cervical osteophytes larger than 10 mm. Aspiration is rare in patients with osteophytes smaller than or equal to 10 mm unless these patients suffer from other disorders that may affect swallowing.
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In this study, the videofluoroscopic tapes and radiographs of all patients were retrieved and reviewed by two experienced examiners. The medical records of 40 patients were available for review. Videofluoroscopy was performed in a standardized fashion, using a fluoroscopy unit (Pantoskop 3 and 5, Siemens, Erlangen, Germany; and Diagnos, Philips, Best, the Netherlands) connected to a video recorder (Sirecord, Siemens; Betacam SP BVW 75 P, Sony, Tokyo, Japan). All patients were studied in the upright, lateral, and anteroposterior positions. If a patient complained of dysphagia or globus symptoms, the examination was started with a bolus of 15-ml high-density barium suspension (Prontobario; Gerot, Vienna, Austria) in the lateral view. If the patient had no difficulty swallowing a 15-ml bolus, the patient was asked to swallow a 30-ml bolus of barium. Patients were then repositioned for examination of the pharynx in the anteroposterior view with another barium bolus. In patients with suspected aspiration, videofluoroscopy was performed with thin liquid nonionic iodinated contrast material ([iopamidol] Gastromiro; Gerot) at a bolus of 3 ml. With these patients, nonionic iodinated contrast material was used because it is safe for aspirating patients [10]. If a bolus of 3 ml was tolerated, the bolus size was increased to 5 ml, 10 ml, and 15 ml. Then a bolus of thick liquid barium was given. When the mucosal coating was visible, double-contrast pharyngography was performed. Patients were asked to take another swallow of high-density barium. Thereafter, another double-contrast radiograph was obtained after breath-holding.
Cervical spine abnormalities were evaluated on the pharyngography in the lateral view. The sagittal diameter of the osteophytic spurs was measured from the superior or inferior anterior edge of the vertebral body to the tip of the osteophyte; the number of vertebral segments affected and the presence of bony bridges were assessed. The degree of magnification of the cervical spurs on the lateral pharyngography was not corrected for the study. Previous preliminary results have shown that lateral radiographs of the cervical spine at our institution have a magnification factor of 1.2. Barium pharyngograms obtained at our fluoroscopy unit had a magnification factor of 1.25, less than 10% higher than that of the lateral radiographs.
On videofluoroscopy, the degree of extrinsic compression of the hypopharynx, pharyngoesophageal sphincter, and upper esophagus was graded as mild, moderate, or severe. Mild compression was defined as an impression of the posterior pharyngeal wall or pharyngoesophageal segment of not more than 30% in an anteroposterior diameter. Moderate compression was defined as a narrowing of the pharynx or pharyngoesophageal segment of more than 30% with stasis of contrast material in the hypopharynx. Severe compression occurred when epiglottic tilting was severely impaired, the pharynx was narrowed by more than 50% in anteroposterior diameter with at least moderate stasis of contrast material, and the pharyngoesophageal segment was displaced laterally by the osteophytes. Oral bolus control and the elevation of the soft palate were assessed. The completeness of laryngeal closure, the movements of the epiglottis, the pharyngeal contraction on swallowing, and the presence or absence of retained barium in the pharynx were assessed. The presence or absence of laryngeal penetration or aspiration was assessed. Penetration was defined as entrance of contrast material into the laryngeal vestibule, either into the subepiglottic space or deep in relation to the supraglottic region. Laryngeal penetration can be seen in healthy individuals [11], whereas laryngeal penetration into the deep supraglottic region is abnormal. The amount of aspirated material was semiquantitatively graded [12]. Aspiration was classified according to the time of its occurrence as being pre-, intra-, or postdeglutitive (before, during, or after swallowing, respectively).
A univariate logistic regression model was performed to evaluate the influence of numbers of affected segments on aspiration and pharyngeal retention. Odds ratios and 95% confidence intervals (CIs) were calculated to describe the unadjusted relative risk of aspiration and retention. Univariate and multiple logistic regression models were performed to evaluate the influence of age, size of osteophytes, and presence of concurrent diseases on aspiration and retention. Odds ratios and 95% CIs from regression models were calculated to describe the age- and concurrent diseaseadjusted relative risk of aspiration and retention for the increasing size of osteophytes. A chi-square test was used to compare the frequency of aspiration in all dysphagic patients of our series against the frequency of aspiration in patients with osteophytes of at least 5 mm in sagittal diameter.
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On videofluoroscopy, moderate to severe retention of barium in the pharynx after swallowing occurred in 26 patients (47%). Univariate regression analysis showed that retention was more likely in patients with spurs involving more than one vertebral segment (odds ratio, 11.25 [95% CI, 1.31-96.39]; p < 0.05). The multiple regression model revealed that retention was more likely with increased osteophyte size (odds ratio, 1.35 [95% CI, 1.13-1.61] per millimeter increase in size; p < 0.001) and in patients with concurrent diseases (odds ratio, 5.23 [95% CI, 1.19-23.10]; p < 0.05). Neither univariate nor multivariate analysis showed a statistically significant relationship between barium retention and patient age.
Aspiration or supraglottic laryngeal penetration was found in 32 patients (58%) with osteophytes of at least 5 mm. In comparison, aspiration or supraglottic laryngeal penetration was found in 1095 (33%) of 3263 dysphagic patients without osteophytes (p < 0.001). Aspiration of osteophytic patients was minimal in seven, moderate in 15, and severe in five patients. It was predeglutitive in three patients, intradeglutitive in three, and postdeglutitive in seven patients. Intra- and postdeglutitive aspiration was present in 12 patients; a combination of pre-, intra-, and postdeglutitive aspiration was evident in two patients. In only six of the patients who aspirated on videofluoroscopy, was aspiration the presenting symptom. Penetration of barium into the supraglottic portion of the larynx was detected in five patients.
Univariate regression analysis showed that aspiration was more likely in patients with osteophytes at more than one vertebra (odds ratio, 8.00 [95% CI, 1.51-42.45]; p < 0.01). A multiple logistic regression model revealed that aspiration was more likely with increasing age of the patient (odds ratio, 1.07 [95 CI, 1.01-1.14] per year of increase in age; p < 0.05) and with increased osteophyte size (odds ratio, 1.26 [95% CI, 1.07-1.48] per millimeter increase in size; p < 0.01). However, the strongest independent factor responsible for aspiration was the presence of concurrent diseases (odds ratio, 8.02 [95% CI, 1.68-38.12]; p < 0.01). Aspiration was more often found in patients with osteophytes larger than 10 mm in anteroposterior diameter than in patients with small osteophytes (24/32 [75%] versus 8/23 [35%]) (Fig. 1A, 1B, 1C, 1D).
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Of the eight patients with small osteophytes who aspirated, seven (88%) had other diseases or conditions (thyroidectomy, n = 3; stroke, n = 2; other, n = 2) that may have contributed to swallowing dysfunction (Fig. 2).
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Three patients underwent surgical removal of cervical osteophytes. In two of these three patients, symptoms did not disappear completely. One patient suffered from transient vocal cord and hypoglossal nerve paralysis postoperatively and recovered completely after several months. One patient showed severe scarring with retention of contrast material and minimal overflow aspiration. One woman who had suffered from dysphagia caused by osteophytes and a prior cerebrovascular accident did not improve at all after surgery; instead, her neurogenic dysphagia worsened.
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Saffouri and Ward [14] reviewed 116 patients with known cervical exostosis but found dysphagia in only seven of them (6%). Cummings [15] reviewed the records of 100 patients with dysphagia and found only one case caused by extraluminal compression by cervical osteophytes. In an analysis of 1200 patients with dysphagia, Le Roux [16] did not attribute a single case to osteophytic disease. In our series of more than 3000 patients suffering from dysphagia, globus, or noncardiac chest pain, only 1.7% had cervical osteophytes of at least 5 mm in anteroposterior diameter. In 58% of these patients radiographic evidence of aspiration was considerably greater than the proportion of aspirating patients without osteophytes (33%).
A variety of mechanisms that can lead to dysphagia in patients with osteophytes have been described. First, if large enough, osteophytes may mechanically compress the pharynx or esophagus and cause obstruction [3, 17, 18]. Second, small osteophytes may cause obstruction if they impinge on the pharyngoesophageal segment where it is attached to the cricoid cartilage (most often at the level of C5 and C6) [19, 20]. Another reason described by Crowther and Ardran [19] for dysphagia in patients with osteophytes is impaired tilting of the epiglottis over the laryngeal inlet by osteophytes located at C3 and C4. The fourth circumstance in which cervical spine disease may cause dysphagia is inflammatory reaction of the prevertebral fascia that results in fibrosis and adhesions [1, 18].
In our study, the occurrence of pharyngeal residue and aspiration was primarily the result of extrinsic compression of the pharynx and upper esophagus and impaired epiglottic tilting. The findings of Lambert et al. [3], that pharyngeal residue and aspiration are primarily the result of extrinsic compression of the pharynx with obstruction of bolus passage, were confirmed. Overflow aspiration after swallowing, found in 66% of aspirating patients, was the predominant mechanism. We could not assess the obstructive effect of a single osteophyte at the cricopharyngeal level as described by Lambert et al. because polysegmental disease was found in 82% of our patients. However, the extensive up-and-down movement of the pharyngoesophageal sphincter of approximately 1.5 cm during swallowing [21] renders unlikely a special effect on bolus passage of a single C5- and C6 osteophyte.
Another important factor is impairment of epiglottic tilting by the producing osteophytes at midcervical level. However, incomplete epiglottic tilting cannot explain aspiration in otherwise healthy people if closure of the larynx is intact [22]. Nevertheless, intradeglutitive aspiration was found in 17 aspirating patients in our study; this finding hints at the absence of sufficient laryngeal closure in a large proportion of patients.
As expected, retention and aspiration were more often seen with increased osteophyte size. However, even small osteophytes may cause clinically relevant pharyngeal residue and aspiration if they occur concomitantly with other clinical conditions. In our study group, diseases that can also affect laryngeal closure, such as cerebrovascular accident and partial laryngeal resection, were found to be significant. A recent study suggested the presence of combined mechanisms in the cause of dysphagia [23]. This study reported on a patient with dysphagia caused by stroke and complicated by preexisting cervical osteophytes. In our study, the hypothesis that a variety of other clinical conditions or diseases (e.g., stroke, laryngopharyngeal surgery, Parkinson's disease) can significantly affect swallowing in patients with osteophytes is corroborated. The presence of such conditions or diseases was identified as an independent risk factor by a multiple regression model. Coexisting condition increased the risk of aspiration eightfold in our patients.
Zerhouni et al. [24] reported that any severe disease may trigger the onset of dysphagia with long-standing cervical osteophytes. In our study, two patients showed a sudden onset of dysphagia after trauma and after myocardial infarction. Neither patient underwent resuscitation during the acute episode; thus, hypoxemic brain damage seems unlikely. Neither patient had any history of other neurologic or pharyngeal disease. Videofluoroscopy revealed severe compression of the pharyngeal segment by large osteophytes of 15 and 12 mm in diameter. The sudden onset of dysphagia may be explained by the fact that patients can compensate for their slowly progressive swallowing impairment for several years until a severe general illness results in muscle weakness or altered mental status.
Increasing age was shown to be associated with increased risk of aspiration although the association was found to be much weaker than that between increasing size of osteophytes and aspiration.
Treatment of cervical osteophyteinduced dysphagia should depend on the nature and severity of disease. Sedation, antiinflammatory drugs, and muscle relaxants with an appropriate soft diet have been used successfully [25, 26]. Surgical excision of a large anterior cervical osteophyte via an anterior extrapharyngeal approach was first described by Iglauer [27] in 1938. In a review of the literature, Sobol and Rigual [18] found 70-80 patients with osteophyte-induced dysphagia. Of these, 19 patients underwent surgery that successfully relieved the dysphagia in all but three patients. Vocal cord paralysis has been reported in 2-11% of patients as the most common complication, followed by fistula, hematoma, infection, and transient aspiration [28, 29]. One of our patients suffered from a hypoglossal nerve paralysis postoperatively, which, to our knowledge, has not been reported as a complication of osteophyte surgery. However, some studies have suggested that surgery should be reserved for patients with severe symptoms or for those patients for whom conservative treatment failed [18, 29]. This opinion is in agreement with our limited experience showing that surgery did not resolve aspiration and dysphagia in three patients.
One weakness of our study is that we could not perform long-term follow-up of the patients to identify all who developed aspiration pneumonia. The data of the present study were collected from 1989 to 1997 and not all patients were available for follow-up. Therefore, the incidence of aspiration pneumonia in patients who were found to have aspiration on videofluoroscopy is uncertain. However, in a recent study the presence of dysphagia or aspiration was found to be an important risk factor for aspiration pneumonia [30]. The incidence of both dysphagia [31, 32] and hypertrophic cervical spine disease [33] increases with advancing age. Thus, clinical judgment is critical in determining the degree to which the enlarged cervical osteophytes are responsible for an individual patient's symptoms.
In conclusion, the presence of anterior osteophytes larger than 10 mm that impinge on the pharynx may explain aspiration in dysphagic patients. Other clinical conditions and diseases such as stroke and partial laryngeal resection, which can affect swallowing, dramatically increase the risk of aspiration even in patients with smaller osteophytes of the cervical spine.
Acknowledgments
We thank Johanna Hanel and Monika Boyer, technologists at our Department of
Radiology.
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