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1157

Expert

Radiologic Marc

S. Levine1

Dysphagia lowing

Investigation and Stephen

is defined

difficulty

passage

the mouth to the stomach.

of Dysphagia

E. Rubesin

as the subjective

during

awareness

of swal-

of a solid or liquid bolus

This symptom

from

may be caused

by

abnormalities of the oral cavity, pharynx, esophagus, or cardia ofthe stomach. A barium study is often requested to elucidate the underlying abnormality. In the best circumstances, this examination should include videofluoroscopic evaluation of the oral cavity, pharynx, and cervical esophagus; upright double-contrast views of the pharynx and esophagus; recumbent double-contrast views of the gastric cardia and fundus;

prone single-contrast

and mucosal

relief views of the esoph-

On the basis of our experience,

practical phagia.

approach

for

the

radiologic

we have devised investigation

a

of dys-

Many patients with dysphagia subjectively can localize a sensation of blockage or discomfort to the throat or chest. Patients with pharyngeal dysphagia typically complain of a “lump in the throat” or of food “sticking in the throat” during swallowing. Pharyngeal dysphagia may be caused by a functional abnormality such as cricopharyngeal dysmotility or by a morphologic abnormality such as a Zenker diverticulum or

Received Both

December authors:

Other pharyngeal during swallowing

pharynx,

a dynamic

symptoms include due to laryngeal pen-

should

examination

be performed

in all

patients with pharyngeal symptoms [1 2]. Other patients with dysphagia have a sensation of blockage at the level of the suprastemal notch or thoracic inlet. This ,

symptom

raises the possibility

of a cervical

esophageal

web

or of extrinsic compression of the cervical or upper esophagus by an enlarged thyroid, mediastinal

or other

mass

lesion.

The videofluoro-

scopic examination of the pharynx therefore should include views of the cervical or upper thoracic esophagus in these patients. Other patients have substemal dysphagia with a sensation of blockage or discomfort anywhere from the thoracic inlet to the xiphoid process. As in the pharynx, this symptom may be caused by a functional abnormality in the esophagus such as achalasia or by a structural abnormality such as a ring, stricture, or tumor. Carcinoma of the gastric cardia or fundus may produce similar symptoms. Therefore, a careful radiologic examination of the esophagus and cardia should be performed as the initial study in all patients with substernal dysphagia. Unfortunately, the ability of the radiologist to perform a tailored examination is complicated by the fact that the patient’s subjective assessment of the site of dysphagia does not always correlate with the site of the pathologic finding. Not infrequently, abnormalities of the mid or distal esophagus or even the gastric cardia may cause referred dysphagia to

11, 1989; accepted after revision February 1, 1990.

Department

of Radiology,

Hospital of the University

of Pennsylvania,

3400

M. S. Levine. AJR 154:1157-1163,

a nasal-quality voice or nasal regurgitation due insufficiency. An abnormal oral phase of swalbe manifested by food dribbling from the mouth, chewing, or difficulty in initiating the swallow. abnormality is suspected in the oral cavity or

lymphadenopathy,

Clinical Perspective

pharyngeal tumor. coughing or choking

etration and to soft-palate lowing may difficulty in Whether an

or tumor thoracic

agus; and evaluation of esophageal motility. In practice, however, the examination usually is tailored to individual patients on the basis of the clinical history. Our radiologic techniques for evaluating these patients at the Hospital of the University of Pennsylvania have evolved considerably during the past

decade.

Advice

June

1990 0361 -803X/90/1

546-11570

American Roentgen Ray Society

Spruce

St.,Philadelphia, PA 19104. Address reprint requests

to

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1158

LEVINE

AND

the pharynx or upper thorax. As a result, the esophagus and cardia also must be examined radiographically in patients with pharyngeal symptoms, particularly if the pharyngeal study fails to explain the patient’s dysphagia. At the same time, pharyngeal abnormalities almost never cause referred dysphagia

below

the

pharyngeal

study

is localized

to the

level

of

the

is unnecessary region

of the

thoracic

inlet,

in patients mid

or lower

so

whose

AJR:154, June 1990

coating during the barium study [4]. The patient is instructed to fast overnight before having the examination. The patient also should avoid smoking or chewing gum, as these activities may stimulate salivary and/or gastric secretions and impair mucosal coating [4].

a careful dysphagia

sternum.

Thus,

a combined radiologic examination of the pharynx, esophagus, and gastric cardia should be performed primarily in patients who have pharyngeal or upper esophageal symptoms [3]. Other patients may have odynophagia (pain on swallowing) without a sensation of blockage. Odynophagia is the classic symptom in patients with opportunistic (i.e., fungal or viral) esophagitis. However, this symptom also may be caused by mucosal ulceration associated with other types of esophagitis or esophageal tumors. Still other patients may have chest pain unrelated to swallowing. The presence of episodic substernal burning or pain exacerbated by lying down or bending over is highly characteristic of gastroesophageal reflux disease. Chest pain or dysphagia also may be a symptom of diffuse esophageal spasm or other esophageal motor disorders. Thus, the radiologic examination should include both functional and morphologic evaluation of the esophagus in patients with substernal symptoms. In summary, a rational approach for examining the patient with dysphagia requires a clear understanding of the nature and location of the underlying symptoms.

Examination

RUBESIN

Technique

Preparation The pharynx, esophagus, and stomach should be as free of fluid and secretions as possible to permit optimal mucosal

Routine

Examination

of the Pharynx

The pharyngeal study requires both a dynamic examination (either cineradiography or videofluoroscopy) to evaluate motility and a series of double-contrast spot films to evaluate morphology.

Cine

or video

recordings

of swallowing

permit

a

frame-by-frame or slow-motion analysis of the parameters of deglutition, including tongue movement, soft-palate elevation, epigloftic tilt, laryngeal closure, cricopharyngeal opening, and pharyngeal peristalsis. At the same time, double-contrast spot films of the pharynx are important for detecting pharyngeal tumors or other morphologic abnormalities [5-7]. The radiologist’s challenge is to integrate the dynamic and static images in a way that minimizes examination time without compromis-

ing diagnostic value. The following is a step-by-step approach for examining the pharynx: Step 1.-Standing in a right lateral position (all radiographic projections are indicated with respect to the table top), the patient takes a mouthful (i.e., 8-10 ml) of high-density barium (E-Z-HD, E-Z-EM Co., Westbury, NY) and swallows the barium as a video recording is obtained on a full-field lateral view of the oral cavity and pharynx to show both the oral and pharyngeal phases of swallowing. After the fluoroscopic image is columnated and centered on the pharynx, a second swallow is videotaped in the lateral projection. Step 2.-One set of two-on-one vertically split spot films of the pharynx is obtained in a lateral projection, centering the image so that it includes the region extending inferiorly

Fly. 1.-Spot films of normal pharynx. A, Lateral view during phonation shows normal contours of soft palate (S), base of tongue (T), epiglottis (E), posterior pharyngeal wall (arrows), and palatine tonsil en face (P). B, Frontal view shows normal contours of tonslllar fossee (TF), valleculae (V), lateral walls of hypopharynx (H), and base of tongue en face (1).

RADIOLOGIC

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AJR:154, June 1990

INVESTIGATION

from the soft palate to the cricopharyngeus. One film is exposed during suspended respiration and the other during phonation. For the latter view, the patient is instructed to say “Eeeee . . . to expand the pharynx and permit optimal visualization of pharyngeal structures (Fig. 1 A) [8]. These spot films should be obtained rapidly, and the patient should be instructed to avoid swallowing saliva between exposures to prevent deterioration of mucosal coating. Lateral views are best for showing abnormalities of the base of the tongue, posterior pharyngeal wall, anterior hypopharyngeal wall, epigIottis, and cricopharyngeus (Fig. 2) [8]. Step 3.-The patient is placed in a frontal position with the head tilted until the mandible is superimposed over the occiput, so that the pharynx is not obscured by these bony structures. Two separate swallows are videotaped to evaluate the pharynx in this projection. If esophageal compression by an enlarged thyroid or other cervical esophageal abnormalities are suspected, one or two additional swallows should be videotaped in a frontal projection with the image centered more distally at the level of the clavicles. Step 4.-A second set of two-on-one vertically split spot films of the pharynx is obtained in a frontal projection (Fig. 1 B). One film is taken during suspended respiration and the other during a modified Valsalva maneuver (i.e., the patient puffs out the cheeks against closed lips to optimally distend the pharynx) [9]. The frontal views are best for showing abnormalities of the vaileculae, tonsillar fossae, and lateral walls of the hypopharynx (Fig. 3). “

Examination

of the Pharynx

Although scout films are not obtained routinely, frontal and lateral plain films of the neck may be helpful in cases of suspected foreign body, abscess, or fistula formation. In other

Fig. 2.-Spot films show pharyngeal carcinoma best on lateral view. A, Frontal view shows retention of barium in vaiIeculae (V) and hypopharynx (H) with aspirated barium In larynx. Note nodular mucosa (arrows) below level of valieculae. B, Lateral view during phonation shows large, lobulated mass (arrows) on posterior pharyngeal wall that is poorly seen on frontal view. (Reprinted with permission from Rubesin and Glick [4].)

DYSPHAGIA

1159

patients who have an equivocal abnormality on the initial video recordings or spot films, additional swallows may be obtained to better delineate the area in question. Oblique views of the pharynx sometimes may be helpful in these patients. Flexion or extension of the neck under fluoroscopic guidance also may permit better visualization of anatomic structures such as the uvula, epiglottic tip, and hypopharynx [4].

In patients who have neuromuscular disorders resulting in laryngeal penetration (i.e., aspiration just before or during swallowing), the pharyngeal study may be performed with the assistance of a swallowing therapist from rehabilitation medicine or speech pathology. These patients may be asked to ingest barium of different viscosity or barium-impregnated substances (i.e., marshmallows or bread) so that swallowing can be evaluated better. They also may be asked to modify the position of the head or their breathing technique during swallowing to prevent or decrease laryngeal penetration or other types of swallowing dysfunction. If the soft palate moves abnormally or nasopharyngeal regurgitation occurs during the routine pharyngeal study, intranasal barium may be given for a more detailed examination of this region [10]. Approximately 1-2 ml of high-density barium are instilled into the nares via a small syringe as the patient tilts the head up and swallows. This technique also permits better delineation of tumors or other abnormalities involving the superior surface of the soft palate (Fig. 4).

Routine Tailored

OF

Examination

of the Esophagus

and Cardia

As in the pharynx, the radiologic examination of the esophagus and cardia is performed to assess both morphologic and functional abnormalities. Double-contrast radiographs of upright patients are best for providing morphologic informa-

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1160

LEVINE

AND

RUBESIN

AJR:154, June 1990

Fig. 3.-Spot films show aryepiglottic fold cyst best on frontal view. A, Frontal view during modified Valsalva maneuver shows smooth, ovoid, 2-cm mass (arrows) in right hypopharynx. (Reprinted with permission from Rubesin and Glick [4].) B, Mass is difficult to identify on lateral view during phonation.

Fig. 4.-Spot films show value of intranasal barium for delineating tumor involving soft palate. A, Frontal view of pharynx shows 6cm mass (arrows) in region of right tonslilar fossa. B, Lateral view during phonation shows centrally ulcerated mass (arrows) in palatine fossa. T = base of tongue; e = epiglottis; h = hyoid bone.

C, Lateral view after intranasal instillatlon of 2 ml of high-density barium shows enlarged, lobulated soft palate (S). Note irregular contour of posterior pharyngeal wall and widening of retropharyngeal space (double arrow). Biopsies revealed non-Hodgkin lymphoma.

tion

about

the

esophagus.

the cardia

are also

abnormalities

in this

Double-contrast

important region

for detecting that

may

cause

radiographs

tumors dysphagia.

of

or other At the

same time, single-contrast radiographs of prone patients with the esophagus and gastroesophageal junction fully distended are best for detecting webs, rings, or strictures that can be missed on double-contrast views of an inadequately distended esophagus and gastroesophageal junction. Finally, single swallows of barium in the prone position are important for evaluating esophageal motility without the effects of gravity. Thus, a combination of techniques is required for optimal radiologic evaluation of the esophagus and cardia [11]. The following is a step-by-step approach for examining the esophagus and cardia:

Step 1.-The patient swallows a packet of effervescent granules (Baros, Lafayette Pharmacal, Lafayette, IN) and then 10 ml of water. Step 2.-The patient rapidly gulps a cup (120 ml) of highdensity barium (E-Z-HD) as one three-on-one or two two-onone upright spot films of the esophagus are obtained in a left posterior oblique projection (Fig. 5A). Two exposures should be centered on the upper or mid esophagus and two on the distal esophagus. Although most patients swallow enough air to produce a double-contrast effect in the esophagus, subsequent peristalsis causes the esophagus to collapse almost immediately after passage of the barium bolus into the stomach. The fluoroscopist therefore must time the exposures to capture the esophagus during a relatively brief period of

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AJR:154,

June

1990

RADIOLOGIC

Fig. 5.-Spot films of normal esophagus and cardia. A, Upright left posterior oblique view of esophagus. B, Right lateral view of gastric cardia and fundus. Note radiating toward gastroesophageal junction.

INVESTIGATION

stellate

folds

optimal distension and coating. With some experience, it is possible to obtain satisfactory double-contrast views of the esophagus in 75-85% of patients [1 2, 13]. Step 3.-The table is brought to the horizontal position, and the patient turns to a right lateral position for a doublecontrast view of the gastric cardia and fundus (Fig. 5B). The normal cardia usually appears en face as a stellate collection of folds radiating to a central button or dimple at the gastroesophageal junction (the esophageal “rosette”) [14]. Step 4.-The patient drinks a low-density barium suspension (Solopake, E-Z-EM Co.) while in a prone right anterior oblique position. The patient takes two to five separate swallows of barium so that esophageal motility can be evaluated at fluoroscopy. During the initial swallow, the pharynx also should be observed fluoroscopically. If esophageal motility appears abnormal, a video recording of additional swallows should be obtained to document the abnormality. Then, one three-on-one or two two-on-one spot films of the esophagus are obtained while the patient continuously drinks low-density barium for optimal distension of the distal esophagus and gastroesophageal junction. This technique permits detection of lower esophageal rings and strictures that are not visible on double-contrast radiographs (Fig. 6) [15, 16]. Step 5.-The patient is turned onto the left side and then onto the back, so that barium pools in the gastric fundus. The gastroesophageal junction then is monitored fluoroscopically as the patient turns slowly to the right in order to show spontaneous gastroesophageal reflux. The patient also can

OF

1161

DYSPHAGIA

Fig. 6.-Radiographs of lower esophageal ring. A, Double-contrast radiograph of distal esophagus in upright patient shows no definite ring. B, Single-contrast radiograph of prone patient shows unequivocal Schatzki ring (arrow) above sliding hiatal hernia. (Reprinted with permission from Laufer [11].)

perform a straight-leg-raising to increase intraabdominal

Tailored

Examination

When

mucosal

maneuver or Valsalva maneuver pressure and elicit reflux.

of the Esophagus

and Cardia

is suspected fluoroscopically on the of the study, the patient may be turned 90#{176} to the right and asked to swallow additional highdensity barium in a right posterior oblique position in order to show protruded or depressed lesions both en face and in profile. Double-contrast radiographs in various projections are particularly helpful for showing plaques or ulcers associated double-contrast

with

reflux

disease

portion

disease,

opportunistic

infection,

and

other

types

of esophagitis (Fig. 7) [1 7-20]. If the initial double-contrast radiographs are inadequate, mucosal relief views of the collapsed or partially collapsed esophagus may provide additional information by showing abnormalities of the longitudinal folds that are due to vances, tumor, or esophagitis (Fig. 8). In other patients who have equivocal abnormalities on the routine double-contrast study, a tube esophagogram may be obtained for a more detailed examination [21]. The tube esophagogram is obtained by passing a small red rubber catheter through the patient’s mouth into the proximal thoracic esophagus. The patient then swallows high-density barium as air is gently insufflated through the catheter. The tube esophagogram is particularly helpful when the initial double-contrast examination is inconclusive because of in-

LEVINE

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1162

AND

RUBESIN

AJR:154,

June 1990

Fig. 7.-Infectious esophagitis diagnosed on basis of double-contrast esophagograms. A, Candlda esophagitis with multiple discrete plaquelike lesions. B, Herpes esophagitis with numerous punctate ulcers. (Reprinted with permission from Levine et al. [19].)

Fig. 8.-Mucosal relief esophagograms. A, Normal appearance of collapsed esophagus. Longitudinalfolds are thin,delicatestructuresseveral millimetersin diameter. B, Marked thickening of longitudinal folds due to Candida esophagitis. (Reprinted with permission from Levine et al. [18].)

adequate distension or pooling of barium in the distal esophagus that obscures mucosal detail in this region (Fig. 9). Double-contrast views of the gastric cardia are important for detecting malignant tumors or other abnormalities involving the cardia. Some patients with carcinoma of the cardia have an obvious mass lesion in the fundus; others have

function (i.e., aspiration or nasopharyngeal regurgitation) cccurs, particularly in stroke patients, a detailed study of the esophagus is unwarranted. Instead, one or two additional swallows with the patient in a recumbent or semiupright position are probably adequate to rule out gross esophageal disease. However, patients with pharyngeal carcinomas have a significantly increased risk of synchronous esophageal carcinomas [24, 25]. Therefore, a double-contrast examination of the esophagus should be performed when there is evidence of tumor in the pharynx. Finally, a normal pharyngeal study should always be followed by a careful examination of the esophagus and cardia to rule out more distal abnormalities causing referred dysphagia to the pharynx. A complete radiologic examination of the pharynx, esophagus, and cardia can be performed in reasonably cooperative patients in less than 10 mm (including 2-4 mm of fluoroscopy). Conversely, patients with substernal dysphagia or odynophagia, reflux symptoms, or nonspecific chest pain should first undergo a detailed radiologic examination of the esophagus and cardia. A double-contrast esophagogram (done as a biphasic study, as described) can be obtained in most patients, although some debilitated or elderly individuals are able to tolerate only a limited single-contrast examination. When doubleand single-contrast techniques are used to evaluate morphology and function, it generally is possible to show esophagitis, tumors, webs, rings, or strictures in the

distortion or obliteration of the normal landmarks with irregular areas of ulceration in this region 22, 23]. Occasionally, it may be unclear whether

at the cardia

(Fig. 10) [14, a suspected

mass at the cardia is a true lesion or normal invagination of the cardia into the fundus. In such cases, the patient should swallow additional barium in a recumbent right lateral position with the cardia visualized en face. The normal defect associated with the cardia should disappear as the lower esophageal sphincter relaxes and barium enters the stomach, whereas a true mass lesion at the cardia should be recognized as a persistent finding as barium streams past this region.

Recommended

Approach

Patients with pharyngeal dysphagia or other symptoms localized to the pharynx, neck, or suprasternal notch should undergo a careful radiologic examination of the pharynx with videofluoroscopic recordings and double-contrast spot films. If the patient aspirates a substantial amount of barium, the examination should be terminated. If marked swallowing dys-

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AJR:154,

RADIOLOGIC

June 1990

INVESTIGATION

OF

DYSPHAGIA

1163

[26]. However, pharyngeal abnormalities virtually never cause referred dysphagia below the level of the thoracic inlet, so a limited pharyngeal study may be performed in patients with substernal symptoms.

REFERENCES 1 . Curtis DJ, Hudson T. Laryngotracheal aspiration: neuromuscular factors. Radiology 1983;1 49:517-522 2. Jones

B, Kramer

SS,

Donner

MW.

Dynamic

analysis

imaging

of specific

of the

pharynx.

1985;10:213-224 3. Jones B, Ravich WJ, Donner MW, Kramer 55, Hendrix TR. Pharyngoesophageal interrelationships: observations and working concepts. Gastrointest Radio! 1985;10:225-233 4. Rubesin SE, Glick SN. The tailored double-contrast pharyngogram. CRC Crit Rev Diagn Imaging 1988:28:133-179 5. Ekberg 0, Nylander G. Double contrast examination of the pharynx. Gastrointest

Radiol

Gastrointest

Radio!

6. Balfe DM, Heiken pharynx.

1985;1 0:263-271

JP. Contrast

Curr Prob!

evaluation

of structural

Radio! 1986;1 5:73-160 7. Rubesin SE, Jessurun J, Robertson D, Jones B, Bosma Unes of the pharynx. RadioGraphics 1987:7:217-237

lesions of the

Diagn

JF, Donner MW.

8. Rubesin SE, Jones B, Donner MW. Contrast pharyngography: the importenon of phonation. AiR 1987;148:269-272 9. Jing BS. The pharynx and larynx: roentgenographic technique. Semin Roentgeno!

1974;9:259-265

10. Rubesin SE, RabiSchOng P. Bilaniuk LT, Laufer I, Levine MS. Contrast examination of the soft palate with cross sectional correlation. RadioGraphics

Fig. 9.-Value of tube esophagogram. A, Initial double-contrast esophagogram

11 . Laufer shows distal esophageal

nar-

rowing with fine marginal serrations, suggesting benign peptic stricture with associated reflux esophagitis. However, distal esophagus is not distended optimally, and pooling of barium in this region obscures mucosal detail B, Tube esophagogram permits better distension of distal esophagus, revealing infiltrating lesion with shelflike upper borders due to esophageal carcinoma (arrow shows tip of tube). (Reprinted with permission from Levine et al. [21].)

1988;8:641-665

I. Technique

the esophagus.

and normal anatomy. in: Levine MS, ed. Radio!ogy

Philadelphia:

Saunders,

of

1989:1-14

12. Balfe DM, Koehier RE, Weyman PJ, Baron AL, Remus WA. Routine aircontrast esophagography during upper gastrointestinal examinations. Radio!ogy 1981;139:739-741 13. Maglinte DDT, Schuitheis TE, Krol KL, Caudill LD, Chemish SM, McCune WM. Survey of the esophagus during the upper gastrointestinal examination in 500 patients. Radio!ogy 1983;147:65-70 14. Herlinger H, Grossman A, Laufer I, Kressel HY, Ochs RH. The gastric cardia in double-contrast study: its dynamic image. AJR 1980:135:21-29 15. Chen YM, Ott DJ, Gelfand DW, Munitz HA. Multiphasic examination of the esophagogastric region for strictures, rings, and hiatal hernia: evaluation of the individual techniques. Gastrointest Radio! 1985:10:311-316 16. Ott DJ, Chen YM, Wu WC, Gelfand DW, Munitz HA. Radiographic and endoscopic sensitivity in detecting lower esophageal mucosal ring. AiR 1986;147:261

-265

17. Laufer I. Radiology of esophagitis. Radio! C!in North Am 1982:20:687-699 18. Levine MS, Macones AJ, Laufer I. Candida esophagitis: accuracy of radiographic diagnosis. Radiology 1985;154:581-587 19. Levine MS, Loevner LA, Saul SH, Rubesin SE, Herlinger H, Laufer I. Herpes esophagitis: sensitivity of double-contrast esophagography. AiR 1988:151:57-62

20. Bova

JG, Dutton NE, Goldstein

esophagitis:

21 .

22. Fig. 10.-Double-contrast with obliteration of normal areas of ulceration (arrows)

radiograph shows carcinoma of gastric cardia anatomic landmarks at cardia and irregular due to tumor in this region.

23. 24. 25.

esophagus or esophageal motor abnormalities responsible for the patient’s symptoms. Some esophageal disorders such as achalasia and gastroesophageal reflux disease may be associated with pharyngeal or cricopharyngeal dysfunction

diagnosis

by double

HM, Hoberman contrast

U. Medication-induced

esophagography.

AIR

1987;

148:731 -732 Levine MS, Kressel HY, Laufer I, Herlinger H, Goren A. The tube esophagram: a technique for obtaining a detailed double-contrast examination of the esophagus. AiR 1984;142:293-298 Freeny PC, Marks WM. Adenocarcinoma of the gastroesophageal junction: barium and CT examination. AiR 1982;138: 1077-1084 Levine MS, Laufer I, Thompson JJ. Carcinoma of the gastric cardia in young people. AiR 1983:140:69-72 Goldstein HM, Zomoza J. Association of squamous cell carcinoma of the head and neck with cancer of the esophagus. AiR 1978:131 :791 -794 Thompson WM, Oddson TA, Kelvin F, Daffner R, Postelthwait RW. Synchronous and metachronous squamous cell carcinomas of the head, neck, and esophagus. Gastroint eat Radio! 1978:3:123-127 BJ, Donner MW, Rubesin SE, Ravich JJ, Hendrix TA. Pharyngeal findings in 21 patients with achalasia of the esophagus. Dysphagia 1988;2:87-92

26. Jones

Radiologic investigation of dysphagia.

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