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1 Department of Radiology, University of Vienna, Waehringer Guertel 18-20,
A-1090 Vienna, Austria.
2 Department of Psychoanalysis and Psychotherapy, Documentation and Statistics
Branch, University of Vienna, A-1090 Vienna, Austria.
3 Department of Thoracic and Cardiovascular Surgery, University of Vienna,
A-1090 Vienna, Austria.
4 Department of Otolaryngology, University of Vienna, A-1090 Vienna,
Austria.
Received July 2, 2002;
accepted after revision August 29, 2002.
Address correspondence to B. L. Partik.
Abstract
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MATERIALS AND METHODS. From 1994 to 2001, 22 patients (17 males and five females; age range, 4–89 years; mean age, 64 years) who had swallowing abnormalities after cardiovascular surgery were referred for a videofluoroscopic swallowing study. Each study was analyzed for functional abnormalities of the tongue, soft palate, epiglottis, hyoid and larynx, pharynx, upper esophageal sphincter, and esophagus. Also, the performance of transesophageal echocardiography, long-term intubation, or both was noted.
RESULTS. Swallowing abnormalities were present in 18 patients
(81.8%) (range, one to eight functional abnormalities; mean, 3.9 functional
abnormalities). The distribution of abnormalities across the functional units
statistically significantly deviated (
2 = 14.4; df =
6; p = 0.025) from uniform distribution, with abnormalities most
commonly involving the hyoid and larynx (13 patients [59.1%]) and the pharynx
(10 patients [45.5%]). Aspiration was found in 13 patients (59.1%)
(predeglutitive, n = 1; intradeglutitive, n = 4;
postdeglutitive, n = 3; and mixed, n = 5). In the 14
patients (63.6%) who underwent transesophageal echocardiography, long-term
intubation, or both, we frequently found incomplete tilting of the epiglottis,
pharyngeal weakness, and postdeglutitive aspiration.
CONCLUSION. Most patients with swallowing problems after cardiovascular surgery present with multiple abnormalities that most commonly affect the hyoid and larynx and the pharynx and result predominantly in intra- or postdeglutitive aspiration. The performance of transesophageal echocardiography and long-term intubation may influence the types of swallowing abnormalities.
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Patients' histories included remote ischemic stroke (n = 7), diabetes mellitus (n = 6), goiter (n = 2), postoperative neurologic deficit (n = 1), and tracheostomy (n = 1). The histories of seven patients (31.8%) were unremarkable regarding underlying diseases or conditions that are considered to cause swallowing abnormalities. The patients underwent surgery for replacement of the aortic (n = 7) or mitral valve (n = 3), aortocoronary bypass grafting (n = 4), heart transplantation (n = 2), patent ductus arteriosus (n = 2), aneurysms of the thoracic aorta (n = 2), atrial septal defect (n = 1), and transposition of the subclavian artery (n = 1). Fourteen (63.6%) of 22 patients underwent intraoperative transesophageal echocardiography (n = 4), long-term intubation (n = 4) defined as more than 8 days [8], or both (n = 6). Six patients underwent CT of the brain during the time between surgery and the swallowing study. In five patients, four of whom had a documented history of stroke, CT showed remote ischemic changes. In the sixth patient, findings of the head CT were normal.
Technique
All examinations were carried out by one of three board-certified
investigators experienced in performing swallowing studies using a fluoroscopy
unit with an undercouch tube (Pantoskop 5; Siemens, Erlangen, Germany)
connected to a video recorder (Betacam BVW 75 SP; Sony, Tokyo, Japan).
Videofluoroscopic studies were performed in lateral and anteroposterior
projections with the patient in the upright position. In patients with
suspected aspiration, swallowing studies were started with 3 mL of thin liquid
and non-ionic iodinated contrast material ([iopamidol] Gastromiro; Amersham
Health, Vienna, Austria). If the patient was able to swallow a bolus of 3 mL,
the bolus size was sequentially increased to 5, 10, and 15 mL
[9]. In patients with
aspiration, the examination was terminated
[10]. In patients without
evidence of aspiration, this sequential augmentation of the bolus size was
repeated with a high-density (250% g per volume) barium suspension
(Prontobario [barium sulfate], Gerot, Vienna, Austria). In patients with
dysphagia or globus sensation, the examination was started with a bolus of 15
mL of high-density barium suspension. If the patient had no difficulty in
swallowing a 15 mL bolus, the patient was asked to swallow a bolus of 30 mL
[9]. The videofluoroscopic
studies of all patients were retrospectively reviewed by two radiologists
experienced in performing and interpreting swallowing studies. The
videofluoroscopic tapes of all patients were reviewed in real time and slow
motion frame by frame. The radiographic interpretation was made by consensus
of the two radiologists.
Image Analysis of the Seven Functional Swallowing Units
Oral cavity.—We assessed the upload of the contrast bolus on
the tongue. Findings of weakness of the tongue and leaking were deemed
positive when retentions of contrast material on the hard palate or the back
of the tongue were seen after the contrast bolus had left the oral cavity and
when contrast material was seen in the pharynx before initiation of
swallowing, respectively
[7].
Soft palate.—Posterior sealing of the oral cavity and appropriateness of elevation on swallowing were assessed. Incomplete posterior sealing may result in premature leakage of contrast material into the pharynx, whereas inadequate elevation may result in nasal regurgitation [7].
Epiglottis.—Impaired epiglottic movement was defined as absent or incomplete tilting if the epiglottis did not completely invert [9].
Hyoid and larynx.—Reduced hyoid elevation was defined as limited superior or anterior movement of the hyoid during swallowing. Laryngeal elevation was considered reduced if it did not exceed that of the hyoid during swallowing [11]. Penetration of contrast medium into the upper, subepiglottic portion of the laryngeal vestibule was considered normal [12]. Penetration of contrast material into the lower, supraglottic portion of the larynx and aspiration into the subglottis and trachea were considered abnormal [12]. Aspiration was classified according to the time of its occurrence as pre-, intra-, or postdeglutitive (before, during, or after swallowing) [10].
Pharynx.—The triggering of the swallowing reflex was considered normal when swallowing was initiated immediately after arrival of contrast material at the level of the valleculae [7]. Pharyngeal weakness or paresis was diagnosed when there was diminished or absent obliteration of the pharynx by the peristaltic pharyngeal contraction [13].
Upper esophageal sphincter.—The opening of the upper esophageal sphincter was considered normal if no posterior indentation of the pharyngoesophageal segment occurred during bolus passage [14]. Upper esophageal sphincter dysfunction was divided into four types: delayed opening, incomplete opening, premature closure, and prolonged opening on swallowing [9]. Other causes of obstruction at the level of the upper esophageal sphincter (cervical osteophytes, strictures, webs) were noted.
Esophagus.—The esophageal bolus passage was assessed for a proximal bolus escape, which was deemed present when a portion of the contrast bolus remained in the upper part of the esophagus or showed retrograde movement [15]. Furthermore, we assessed the presence of support levels, which were defined as fluid–air interfaces in the esophagus, and of tertiary contractions, which were defined as nonperistaltic contractions that were often multiple and simultaneous and caused focal but transient narrowings of the esophageal lumen. Also, we noted the presence of hiatal hernia, diverticula, and reflux of contrast material from the stomach to the esophagus [15].
Statistical Analysis
For assessing whether the abnormal findings were uniformly distributed
across the seven functional units of swallowing, we used the exact version of
the one-sample chi-square goodness-of-fit test, as implemented in the StatXact
software (CYTEL Software, Cambridge, MA), which is tailored for small-sample
data analysis [16]. Value
combinations of the variables of transesophageal echocardiography (yes/no) and
long-term intubation (yes/no) were used to constitute four distinct
groups—that is, patients without transesophageal echocardiography and
without long-term intubation, with transesophageal echocardiography and
without long-term intubation, without transesophageal echocardiography and
with long-term intubation, and with both procedures. Surgical procedures were
aggregated into five categories: valve replacement procedures (n =
10), aortocoronary bypass grafts (n = 4), other cardiac operations in
adults (n = 3), other cardiac operations in children (n =
2), and operations on the great intrathoracic vessels (n = 3). Group
differences in number of abnormalities per patient across these grouping
variables were tested with one-way analyses of variance. A p value of
0.05 or less was considered significant.
To explore the co-occurrence pattern among abnormalities, along with the presence or absence of transesophageal echocardiography and long-term intubation, we performed nonmetric multidimensional scaling with these variables. We used the squared Euclidean distance as the dissimilarity measure for these dichotomous data. Multidimensional scaling attempts to find the structure in a set of distance measures between objects (in our study, presence versus absence of abnormalities, transesophageal echocardiography and long-term intubation), which is accomplished by assigning observations to specific locations in a conceptual space (Euclidean and low-dimensional) such that the distances between the spatially arranged points are the best possible fit of the distance scores among them. A badness-of-fit measure (termed "stress") was computed and used to determine the degree of optimality of the dimensional configuration of the input data [17].
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The distribution of abnormalities across the functional units statistically
significantly deviated from uniform distribution (2 = 14.4;
df = 6; p = 0.025), with abnormalities of the hyoid and
larynx (Fig. 1) and of the
pharynx (Fig. 2) being
overrepresented and of the soft palate and upper esophageal sphincter (Fig.
3A,
3B) being underrepresented.
Group means (± SD) of the number of abnormalities per patient for those
without transesophageal echocardiography and without long-term intubation
(n = 8), with transesophageal echocardiography and without long-term
intubation (n = 4), without transesophageal echocardiography and with
longterm intubation (n = 4), and with both transesophageal
echocardiography and long-term intubation (n = 6) were, in order, 3.9
(± 2.6), 2.3 (± 1.7), 1.5 (± 1.9), and 4.0 (±
1.7); these group differences were not statistically significant (p =
0.21). Group means (± SD) of the number of abnormalities per patient
for those with valve replacement procedures, aortocoronary bypass surgery,
other cardiac operations in adults, other cardiac operations in children, and
operations on the great intrathoracic vessels were, in order, 3.0 (±
2.2), 4.3 (± 3.3), 3.7 (± 1.5), 0.5 (± 0.7), and 3.7
(± 1.5); these group differences were not statistically significant
(p = 0.42).
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The multidimensional scaling solution—that is, a two-dimensional representation of the associations among swallowing abnormalities, the use of transesophageal echocardiography, and the long-term intubation—satisfactorily represents the higher dimensional associations between the variables investigated because the stress index (Kruskal's stress formula 1) for this solution was rather low (0.19) and R2 (the proportion of variance of the scaled data or disparities that is accounted for by their corresponding distances) was rather high (0.86). Incomplete tilting of the epiglottis (Fig. 4), postdeglutitive aspiration, and pharyngeal weakness were more frequent when either transesophageal echocardiography or long-term intubation or both procedures were performed. Impaired elevation of the hyoid and larynx and predeglutitive aspiration were more frequently seen when only long-term intubation was performed.
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Previous studies have indicated the clinical importance of swallowing abnormalities in patients who had undergone cardiac surgery [2, 3]. Hogue et al. [3] found in their group of 34 patients a reduced oral preparatory phase in 22%, impaired swallowing reflex in 67%, incomplete closure of the epiglottis in 48%, decreased pharyngeal peristalsis in 56%, and aspiration in 90% of patients. In comparison, the results of our study are similar regarding the frequency of abnormalities of the tongue, closure of the epiglottis, and pharyngeal peristalsis. However, the percentage of patients who had aspirated or had an impaired swallowing reflex was considerably lower in our study. Ferraris et al. [2] detected in 31 patients an impaired oral bolus transit in 7%, an impaired pharyngeal transit in 23%, and abnormalities in both oral and pharyngeal transit in 55% of patients. In 55% of their patients, aspiration occurred, which is similar to the percentage identified in our study. Identified differences in study results may relate to differences in entry criteria and examination technique. However, for previous studies, information regarding classification of abnormalities and the detailed examination technique are not available in the literature.
Hogue et al. [3] identified age, duration of intubation, and the use of transesophageal echocardiography as independent predictors of swallowing dysfunctions. Harrington et al. [18] also suggested that postoperative pharyngeal dysfunction may be caused by mechanical trauma from esophageal intubation with an echocardiography probe. In addition, congestive heart failure and non–coronary bypass grafting procedures have been found to be risk factors for development of oropharyngeal dysphagia, whereas patients with remote stroke or diabetes mellitus are at the same risk as patients without these diseases [2]. In general, swallowing abnormalities may result from a variety of neuromuscular and mechanical conditions and inflammatory, anatomic, traumatic, and cancer-related mechanisms [19]. Iatrogenic causes such as insertion of nasogastric feeding tubes, tracheal intubation and tracheostomy, general anesthesia, and treatments for head and neck cancer are also responsible for swallowing abnormalities [19]. Many of these risk factors were present in our patients and may have contributed to their symptoms. After cardiovascular surgery, patients may have a disturbed function of the recurrent laryngeal nerve, which may cause not only dysphonia, but also dysphagia and aspiration due to an incomplete laryngeal closure, pharyngeal weakness or laryngeal closure, and pharyngeal weakness.
In 18% of the patients in our study, videofluoroscopy showed no reason for the patients' symptoms. These findings are in concordance with the results of Ferraris et al. [2], who found that 13% of symptomatic patients have videofluoroscopic swallowing studies without abnormalities. However, in their study, assessment of the upper esophageal sphincter and the esophagus was not performed. Recently, a suprahyoid muscle strengthening exercise program has proven to be effective in restoring oral feeding in some patients with deglutitive failure due to abnormal upper esophageal sphincter opening [5]. Incomplete opening of the upper esophageal sphincter was also detected in two of our patients. Thus, assessment of the entire swallowing phase is recommended to allow the identification of all possible morphologic and functional abnormalities, although this assessment may be difficult in patients with limited mobility.
Videofluoroscopy enables assessment of complex swallowing abnormalities and may facilitate precise planning of an individually tailored functional swallowing therapy. In our experience, the radiologic division of swallowing into functional units serves as an effective method for clinical communication as well as for teaching purposes. Moreover, this division may also have an electrophysiologic correlation. McKeown et al. [20] recently introduced a noninvasive method of monitoring muscle activation during swallowing based on computing of the independent components of the simultaneous superficial electromyographic recordings to detect the underlying functional muscle activations during swallowing. The authors showed that the independent components, each consisting of a unique temporal wave-form and a spatial resolution, provided a means to segregate the complex sequence of muscle activation into rigorously defined separate functional units [20].
Our study was limited by the relatively small sample size. Although cardiologists and cardiothoracic surgeons at our institution estimate the number of patients with swallowing abnormalities after cardiovascular surgery to be much higher, the number of symptomatic patients who were referred for a videofluoroscopic swallowing study was low. We believe that many symptomatic patients are transferred to rehabilitation facilities after being discharged from the intensive care or intermediate care unit and are subsequently treated elsewhere. Moreover, aspiration that occurs after surgery may go unnoticed (so-called silent aspiration) [18]. Another limitation was the relatively old age of our patients, which may render differentiation between altered swallowing functions because of aging and surgically related functional abnormalities difficult [15, 21, 22]. To define preexistent swallowing abnormalities in this patient group, preoperative evaluation by videofluoroscopy would have been necessary. Although no patient reported a prior history of swallowing abnormalities, we cannot exclude the possibility that some had clinically insignificant episodes of aspiration or other swallowing abnormalities before surgery. In addition, because the time between surgery and videofluoroscopy was relatively long for some patients, a direct causal relationship between the development of swallowing abnormalities and medical procedures is uncertain. To overcome the limitations of this retrospective pilot study, our institution is conducting a large prospective study to evaluate the pre- and postoperative swallowing function in candidates for cardiac surgery, which will allow more reliable exclusion of patients with preexisting swallowing abnormalities, as well as more clearly show the causal relationship between swallowing abnormalities and prior medical procedures.
In conclusion, most of the patients with swallowing problems after cardiovascular surgery present with multiple abnormalities, most commonly affecting the hyoid and larynx and the pharynx and resulting predominantly in intra- or postdeglutitive aspiration. The performance of transesophageal echocardiography and long-term intubation may influence the types of swallowing abnormalities.
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