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Ann Thorac Surg 2000;69:989-992
© 2000 The Society of Thoracic Surgeons

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ORIGINAL ARTICLES: GENERAL THORACIC

Pharyngeal dysphagia in postesophagectomy patients: correlation with deglutitive biomechanics

^a Dysphagia Institute, Division of Gastroenterology and Hepatology, Milwaukee, Wisconsin, USA
^b Division of Cardiothoracic Surgery, Medical College of Wisconsin, Zablocki Veterans Affairs Medical Center, Milwaukee, Wisconsin, USA

Address reprint requests to Dr Shaker, Division of Gastroenterology and Hepatology, Froedtert Memorial Lutheran Hospital, 9200 W Wisconsin Ave, Milwaukee, WI 53226

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. Because of the transient nature of pharyngeal phase dysphagia, posttranshiatal esophagectomy patients provide a model for studying the correlation of dysphagic symptoms and aspiration with deglutitive biomechanics.

Methods. We studied 8 transhiatal esophagectomy patients (age range, 51 to 78 years) and 8 normal age-matched controls in upright position using lateral and anteroposterior (AP) projection videofluoroscopy during three 5 mL barium swallows.

Results. The maximum upper esophageal sphincter (UES) AP diameter and maximum anterior excursion of the hyoid bone in patients with transhiatal esophagectomy who experienced aspiration (6.2 ± 0.6 and 9.0 ± 2.0 mm, respectively) were significantly smaller than those of age-matched normal controls (9.4 ± 0.7 and 17.0 ± 1.0 mm, respectively). Resolution of aspiration was associated with a significant increase in AP diameter of the UES as well as anterior and superior excursion of the hyoid bone (p < 0.05).

Conclusions. Dysphagic symptoms and aspiration in posttranshiatal esophagectomy patients are associated with significant abnormalities of deglutitive biomechanics. Improvement in deglutitive biomechanics is associated with resolution of dysphagic symptoms as well as postdeglutitive aspiration in these patients.

	Introduction

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After transhiatal esophagectomy a substantial number of patients (ranging between 47% and 67%) develop abnormalities of the pharyngeal phase of swallowing [1, 2]. These abnormalities include laryngeal penetration, tracheal aspiration, deglutitive cough, and feeling of incomplete pharyngeal clearance and resolve after a period of time ranging from 1 to 6 months after the operation [1, 2]. Because of the transient nature of pharyngeal phase dysphagia, these patients provide a model for studying the correlation of dysphagic symptoms and aspiration with deglutitive biomechanics. This study was undertaken to correlate the deglutitive biomechanical events in transhiatal esophagectomy patients who experienced pharyngeal phase dysphagia with the resolution of their dysphagic symptoms and aspiration.

	Material and methods

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We studied 8 consecutive transhiatal esophagectomy patients (age range, 51 to 78 years) and 8 normal age-matched controls in the upright position using videofluoroscopy in the lateral and anteroposterior (AP) projection. The esophagectomy was performed for esophageal malignancy and the margin of resection was clear of tumor in all patients. All patients had pharyngeal phase dysphagia. Each patient was studied during three 5 mL barium swallows. Control subjects were studied once, whereas patient subjects were studied two or three times, depending upon persistence of their dysphagic symptoms. Esophagectomy was performed because of adenocarcinoma of the distal esophagus in all patients. Transhiatal esophagectomy was performed as described by Orringer [3] for lesions in the distal third of the esophagus or gastroesophageal junction tumors. The transhiatal approach mobilized the stomach by division of the left gastric artery and vein and by division of the short gastric vessels. A gastric tube was fashioned by resection of the cardia and lesser curvature of the stomach. Transhiatal dissection was performed under direct vision distally and by blunt dissection proximally. Similarly, the upper thoracic esophagus was dissected under direct vision and bluntly through the left neck incision. After division of the esophagus, the stomach was passed up through the hiatus, through the posterior mediastinum and into the neck. The cervical exploration was performed through a low transverse incision curved along the sternocleidomastoid muscle. During the operation the sternocleidomastoid muscle and carotid sheath were retracted laterally. The middle thyroid vein was divided, and the sternohyoid and sternothyroid muscles were retracted medially. If adequate exposure was not gained, these muscles were partially divided. The tracheoesophageal groove was exposed by digital retraction of the trachea and larynx. The recurrent laryngeal nerve was avoided by maintaining dissection directly on the esophagus and gently separating the esophagus from the membranous trachea. An anastomosis was performed between the 2 to 4 cm residual cervical esophagus, measured intraoperatively, and the gastric tube using a single layer interrupted suture technique. The neck was drained with a small Jackson-Pratt drain, which was removed on the 2nd or 3rd postoperative day, when drainage was negligible. Patients were kept non per os until the videofluoroscopic swallow study verified absence of aspiration or defective anastomosis.

The first videofluoroscopic swallow study was performed on all 8 patients between the 7th and 10th postoperative days, and because dysphagic complaints continued the second study was done between the 17th and 29th postoperative days. The third study was performed on 4 patients between the 42nd and 105th postoperative days because of persistent symptoms or aspiration. The videofluoroscopic recordings were digitized and subsequently analyzed independently by three individuals. For calibration of videofluoroscopic measurements and to compensate for magnification error, before each study lead markers 1.0 cm apart were taped on the skin covering the left sternocleidomastoid muscle. Videofluoroscopic recordings of biomechanical swallow events were timed using a specially designed timer (Thalner Electronics, Ann Arbor, MI). Videofluoroscopic recordings were obtained at 90 KEV using a 9 inch image intensifier mode and appropriate collimation so that an image was obtained of the posterior mouth, pharynx, and pharyngoesophageal region. Fluoroscopic images were recorded on a super-VHS videocassette recorder and were timed using the output signal from the above timer. The output of the timer provided a video displayed time signal in hundredths of a second superimposed on the fluoroscopic images. The computer analysis system used for analyzing the videofluoroscopic data consisted of an IBM-compatible Compaq Presario Model 4704 computer (Compaq Computer Corp, Houston, TX) operating with a Pentium Processor. The computer system derives an analog-to-digital conversion board (TARGA) and program specifically designed for image capture and analysis. The image analysis and capture software (JAVA, Jandel Scientific, San Mateo, CA) allows capture of standard raster scan video images and morphologic analysis of digitized image data. The digitized images are stored as computer files for any subsequent recall or analysis.

Using these techniques we measured: (1) maximum AP diameter of the upper esophageal sphincter (UES) opening, taken from the narrowest area within the pharyngoesophageal junction when this area became maximally opened during bolus transit across the sphincter; (2) maximum superior and anterior excursions of the larynx; and (3) maximum superior and anterior excursions of the hyoid bone. Statistical analysis was done using two-way analysis of variance with repeated measures to account for both intrasubject variability and the change between videofluoroscopic study sessions. Data represent means ± standard errors unless otherwise stated.

These events also were noted: (1) penetration of liquid barium bolus into the laryngeal vestibule above the level of the true vocal cords; (2) aspiration of liquid barium bolus below the true vocal cords; (3) timing of the penetration and aspiration relative to the pharyngeal bolus transit; penetration or aspiration before, during, or after the pharyngeal phase of the swallow; (4) presence or absence of pyriform sinus residue after completion of the initial swallow; and (5) epiglottic inversion during the pharyngeal phase of swallowing classified as absent, partial, or complete. Absent epiglottic movement was defined as the epiglottis remaining in the upright position, ie, parallel to the posterior pharyngeal wall during the pharyngeal phase of swallow. Partial epiglottic inversion was defined as its movement to a position between a vertical and horizontal position. Complete epiglottic inversion was when the epiglottis achieved a horizontal position covering the glottis.

	Results

Top Abstract Introduction Material and methods Results Comment References

 
During the first videofluoroscopic swallow study, 5 of 8 patients exhibited aspiration. Whereas 2 patients exhibited only postdeglutitive aspiration, 1 exhibited pre- and postdeglutitive aspiration, 1 pre- and intradeglutitive aspiration, and 1 pre-, inter-, and postdeglutitive aspiration (Fig 1). The 2 patients with intradeglutitive aspiration had sustained left true vocal cord paralysis. All 5 patients who aspirated ceased aspirating by the third videofluoroscopic swallow study, 42 to 105 days postoperatively.

View larger version (29K): [in this window] [in a new window]   Fig 1. A summary of postoperative aspiration, pharyngeal residue, and epiglottal movement in 8 patients from study I to study III. The presence or absence of aspiration was associated with a variety of combination of presence and absence of pharyngeal residue and epiglottal movement. Although patients 1, 2, 3, 7, and 8 exhibit similar pharyngeal residue and epiglottal movement patterns, patients 7 and 8 did not aspirate whereas patients 1, 2, and 3 did. During study II, patients 2 and 3 continue their pattern of pharyngeal residue and epiglottal excursion. However, only patient 3 continued to aspirate.

Abnormalities of epiglottal movement were noted in 5 of 8 esophagectomy patients. None of these patients exhibited epiglottal movement. During the second study complete inversion of the epiglottis was achieved by 1 patient and partial movement was noted in another patient. Epiglottal movement during the swallow continued to be abnormal in the remaining 3 patients (Fig 1). During the initial studies, the maximum UES AP diameter and maximum anterior excursion of the hyoid bone in patients with transhiatal esophagectomy who experienced aspiration (6.2 ± 0.6 and 9.0 ± 2.0 mm, respectively) were significantly smaller than those of age-matched normal controls (9.4 ± 0.7 and 17.0 ± 1.0 mm, respectively) (p < 0.05) (Fig 2; Table 1).

View larger version (21K): [in this window] [in a new window]   Fig 2. Comparison of biomechanical deglutitive events among 5 transhiatal esophagectomy patients who demonstrated aspiration postoperatively and the same biomechanical events when these patients ceased aspirating and age-matched normal controls. Resolution of aspiration in these 5 posttranshiatal esophagectomy patients with deglutitive aspiration was associated with a significant increase in the anteroposterior diameter of the upper esophageal sphincter (UES-D) opening during 5 mL barium swallows. *p < 0.05, aspirators vs normal controls; p < 0.05, aspirators vs resolution of aspiration. (AH = anterior hyoid; AL = anterior laryngeal; Asp = aspiration; SH = superior hyoid; SL = superior laryngeal.)

Resolution of aspiration was associated with a significant increase in anterior and superior excursion of the hyoid bone (p < 0.05) (Fig 2). Although there was an increase in the magnitude of anterior and superior laryngeal movement in these patients after the cessation of aspiration, these differences did not reach statistical significance (p = 0.05).

The 3 transhiatal esophagectomy patients who did not exhibit aspiration had a UES AP diameter of 7.3 ± 1.1 mm during their initial study. This value did not change significantly compared with the 7.8 ± 0.6 mm measured during their second study (p = 0.1). In addition, these values were not significantly different from those of normal age-matched controls.

	Comment

Top Abstract Introduction Material and methods Results Comment References

 
Patients who undergo transhiatal esophagectomy often have transient subjective and objective findings of oropharyngeal dysphagia [1, 2]. In this study we correlated the resolution of these dysphagic findings with the deglutitive biomechanical events during the pharyngeal phase of swallowing.

Similar to previous studies [1, 2], a combination of abnormalities such as incomplete pharyngeal clearance resulting in pyriform sinus residue, incomplete or absent epiglottal descent, as well as deglutitive aspiration were identified in our patients. Biomechanical abnormalities associated with these findings included a significantly smaller UES opening and anterior excursion of the hyoid bone in patients who aspirated compared with when they ceased aspiration as well as compared with age-matched controls.

Normal opening of the UES is associated with relaxation of the cricopharyngeus muscle, forceful anterior and superior distraction of the UES by contraction of the suprahyoid UES opening muscles resulting in active opening of the UES, as well as pulsion forces imparted on the pharyngoesophageal segment by the oncoming swallowed bolus [4, 5, 11]. Abnormalities of one or more of these factors may result in abnormality of UES opening.

Significant differences in UES AP diameter and hyoid anterior excursion between the time that patients aspirated and the time that their aspiration was resolved suggest inadequate distraction of the UES. This may be due to either reduced function of the UES opening muscles, including but not limited to the geniohyoid, thyrohoid, and digastric muscles, or increased resistance and passive tone of the pharyngoesophageal junction due to surgical trauma and edema resulting in reduced compliance of this region during the first study.

As the diminished UES opening in our patients, observed during the first videofluoroscopic swallow study, improved significantly by the third study, the abnormalities in UES relaxation are less likely and the above-mentioned finding can be explained by either reduced distraction forces of UES opening muscles or reduced compliance of the UES secondary to the local effect of surgical manipulation such as trauma and edema.

Although in this study no therapeutic intervention was made, it is conceivable that the recovery may be expedited by utilizing rehabilitative techniques such as the Shaker exercise [6], which has been shown to improve the upper esophageal sphincter opening and pharyngeal clearance [7, 8].

Airway closure mechanisms required to prevent aspiration during the pharyngeal phase of swallowing include vocal cord closure, aryepiglottic approximation, and epiglottic descent [5, 9, 10]. Left true vocal cord paresis was verified in 2 of our patients who exhibited intradeglutitive aspiration. This resolved with return of adduction of the true vocal cords by the third videofluoroscopic swallow study.

In summary, dysphagic symptoms in posttranshiatal esophagectomy patients is associated with significant reduction in UES opening and hyoid bone excursion. Resolution of these symptoms as well as postdeglutitive aspiration in these patients are associated with a significant increase in AP opening diameter of the UES and hyoid bone excursion. The possibility of acceleration of this resolution process by swallow exercises and maneuvers merits investigation.

	Acknowledgments

 
This work was supported in part by NIH grant R01-DC00669. Dr Eytan Bardan is affiliated with the Chaim Sheba Medical Center, Tel Hashomer, Israel.

	References

Top Abstract Introduction Material and methods Results Comment References

 

1. Hambraeus G.M., Ekberg O., Fletcher R. Pharyngeal dysfunction after total and suboesophagectomy. Acta Radiol 1987;28:409-412.[Medline]
2. Heitmiller R.F., Jones B. Transient diminished airway protection after transhiatal esophagectomy. Am J Surg 1991;162:442-446.[Medline]
3. Orringer M.B. Palliative procedures for esophageal cancer. Surg Clin North Am 1983;63:941-950.[Medline]
4. Kahrilas P.J., Dodds W.J., Dent J., Logemann J.A., Shaker R. Upper esophageal sphincter function during deglutition. Gastroenterology 1988;95:52-62.[Medline]
5. Shaker R, Ren J, Kern M, Dodds WJ, Hogan WJ, Li Q. Mechanisms of airway protection and upper esophageal sphincter opening during belching. Am J Physiol 1992;262(Gastrointest Liver Physiol 25):G621–8.
6. Buchholz D.W., Neumann S. Comments on selected recent dysphagia literature. Dysphagia 1999;14:113-115.[Medline]
7. Shaker R, Kern M, Bardan E, et al. Augmentation of deglutitive upper esophageal sphincter opening in the elderly by exercise. Am J Physiol 1997;272(Gastrointest Liver Physiol 35):1518–22.
8. Easterling C., Kern M., Nitschke T., et al. Effect of a novel exercise on swallow function and biomechanics in tube fed cervical dysphagia patients. Dysphagia 1999;14:119.
9. Shaker R., Dodds W., Dantas R., Hogan W.J., Arndorfer R. Coordination of deglutitive glottic closure with oropharyngeal swallowing. Gastroenterology 1990;98:1478-1494.[Medline]
10. Logemann J., Kahrilas P., Cheng J., et al. Closure mechanisms of laryngeal vestibule during swallow. Am J Physiol 1992;92:338-344.
11. Jacob P., Kahrilas, Logemann J.A., Shah V., Ha T. Upper esophageal sphincter opening and modulation during swallowing. Gastroenterology 1989;87:1469-1478.

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