16
Imaging of the hypopharynx and cervical esophagus Ilona M. Schmalfuss, MD Division of Neuroradiology, Department of Radiology, University of Florida College of Medicine, 1600 Southwest Archer Road, Post Office Box 100374, Gainesville, FL 32610-0374, USA Cross-sectional CT is a well-established method used to evaluate the hypopharynx and the cervical esophagus. Most institutions prefer CT: it is widely available and better tolerated by patients because it requires less imaging time [1]. In the hypopharyngeal and cervical esophagus region, as many as 16% of MR imaging studies have been reported to be nondiagnostic secondary to claustrophobia or motion artifacts [2]. MR imaging is particularly prone to be inadequate in patients with recurrent tumor or following radiation therapy [3]; however, MR imag- ing is superior in evaluating the esophageal verge and cervical esophagus because of better soft tissue delineation and less obscuration of this area by beam-hardening artifacts caused by the shoulders (as seen on CT). Until recently, MR imaging’s multiplanar capabilities have been a major advantage [1]. The introduction of the multislice helical CT scanner now almost outweighs this advantage. Imaging protocol Considerable differences in MR imaging proto- cols exist based on personal preferences and ven- dor-related variations in hardware and software. Nevertheless, the following parameters should be followed to obtain high-resolution images of the hypopharynx and cervical esophagus and to max- imize the image quality: 1. Use of dedicated neck coil 2. Perform noncontrasted and contrasted T1- weighted images and fast-spin-echo T2- weighted images in axial plane parallel to the true vocal cords extending from the naso- pharynx to the thoracic inlet 3. Acquire all sets as contiguous 3-mm images 4. Use field-of-view less than or equal to 16 cm 5. Use image matrix of at least 256 256 Other sequences may be used to better evaluate certain structures, such as the intramural fat planes (see subsection on cross-sectional anatomy). Normal anatomy Descriptive anatomy The hypopharynx extends from the level of the hyoid bone to the esophageal verge and the cervical esophagus from the hypopharynx to the thoracic inlet. There is no anatomic barrier between the two structures. The hypopharynx is subdivided arbitrarily into three regions: pyriform sinus (one on each side), postcricoid area, and posterior hypopharyngeal wall. The pyriform sinus arises at the level of the aryepiglottic fold and extends inferiorly as an inverted pyramid to the inferior margin of the cricoid cartilage. The pyramid tip is called the pyriform sinus apex . The pyriform sinus is formed by the anterior, 1052-5149/04/$ – see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.nic.2004.07.003 This article was originally published in Magnetic Resonance Imaging Clinics of North America 10:3, 2002. E-mail address: [email protected] Neuroimag Clin N Am 14 (2004) 647 – 662

Imaging of the hypopharynx and cervical esophagus

  • Upload
    ilona-m

  • View
    221

  • Download
    0

Embed Size (px)

Citation preview

Page 1: Imaging of the hypopharynx and cervical esophagus

Neuroimag Clin N

Imaging of the hypopharynx and cervical esophagus

Ilona M. Schmalfuss, MD

Division of Neuroradiology, Department of Radiology, University of Florida College of Medicine, 1600 Southwest Archer Road,

Post Office Box 100374, Gainesville, FL 32610-0374, USA

Cross-sectional CT is a well-established method

used to evaluate the hypopharynx and the cervical

esophagus. Most institutions prefer CT: it is widely

available and better tolerated by patients because it

requires less imaging time [1]. In the hypopharyngeal

and cervical esophagus region, as many as 16% of

MR imaging studies have been reported to be

nondiagnostic secondary to claustrophobia or motion

artifacts [2]. MR imaging is particularly prone to be

inadequate in patients with recurrent tumor or

following radiation therapy [3]; however, MR imag-

ing is superior in evaluating the esophageal verge and

cervical esophagus because of better soft tissue

delineation and less obscuration of this area by

beam-hardening artifacts caused by the shoulders

(as seen on CT). Until recently, MR imaging’s

multiplanar capabilities have been a major advantage

[1]. The introduction of the multislice helical CT

scanner now almost outweighs this advantage.

Imaging protocol

Considerable differences in MR imaging proto-

cols exist based on personal preferences and ven-

dor-related variations in hardware and software.

Nevertheless, the following parameters should be

followed to obtain high-resolution images of the

1052-5149/04/$ – see front matter D 2004 Elsevier Inc. All rights

doi:10.1016/j.nic.2004.07.003

This article was originally published in Magnetic

Resonance Imaging Clinics of North America 10:3, 2002.

E-mail address: [email protected]

hypopharynx and cervical esophagus and to max-

imize the image quality:

1. Use of dedicated neck coil

2. Perform noncontrasted and contrasted T1-

weighted images and fast-spin-echo T2-

weighted images in axial plane parallel to

the true vocal cords extending from the naso-

pharynx to the thoracic inlet

3. Acquire all sets as contiguous 3-mm images

4. Use field-of-view less than or equal to 16 cm

5. Use image matrix of at least 256 � 256

Other sequences may be used to better evaluate

certain structures, such as the intramural fat planes

(see subsection on cross-sectional anatomy).

Normal anatomy

Descriptive anatomy

The hypopharynx extends from the level of the

hyoid bone to the esophageal verge and the cervical

esophagus from the hypopharynx to the thoracic

inlet. There is no anatomic barrier between the

two structures.

The hypopharynx is subdivided arbitrarily into

three regions: pyriform sinus (one on each side),

postcricoid area, and posterior hypopharyngeal wall.

The pyriform sinus arises at the level of the

aryepiglottic fold and extends inferiorly as an

inverted pyramid to the inferior margin of the cricoid

cartilage. The pyramid tip is called the pyriform sinus

apex. The pyriform sinus is formed by the anterior,

Am 14 (2004) 647 – 662

reserved.

Page 2: Imaging of the hypopharynx and cervical esophagus

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662648

medial, and lateral walls. Laterally, the superior

aspect of the pyriform sinus is bordered by the

thyrohyoid membrane containing the superior la-

ryngeal neurovascular bundle—a possible pathway

of tumor spread from the pharynx. The sensory axons

of the superior laryngeal nerve connect with the

Arnold nerve within the jugular foramen and are

responsible for the referred otalgia seen with tumors

of the pyriform sinus. The postcricoid area forms the

anterior wall of the hypopharynx. It extends from

the posterior surface of the arytenoid cartilage to the

esophageal verge. Anteriorly, it opens directly into

the larynx. The posterior hypopharyngeal wall

represents the posterior boundary of the hypophar-

ynx. It extends from the level of the top of the

aryepiglottic fold to the esophageal verge and has free

communication to the oropharynx and the esophagus.

It is separated from the vertebral and paravertebral

structures by the retropharyngeal space, which allows

the pharynx to move freely during swallowing.

The wall of the hypopharynx is composed of four

layers: a mucosal lining of stratified squamous

epithelium over loose stroma, a fibrous layer formed

by the pharyngeal aponeurosis, the muscular layer,

and the fascial layer derived from the buccopha-

ryngeal fascia. The loose stroma can be identified on

cross-sectional images as a thin fat plane (see

following subsection). Anteriorly, the muscular layer

consists of the posterior cricoarytenoid muscles and

posteriorly of the middle or inferior constrictor

muscles. The inferior constrictor muscle melts into

the cricopharyngeus muscle inferiorly, which forms

the upper esophageal sphincter at the esophageal

verge. The cervical esophagus abuts the posterior

trachea with a small amount of fatty tissue between

the two. It is lined by non-keratinizing squamous

epithelium over loose areolar tissue surrounded by a

muscular layer of inner circular and outer longitudi-

nal fibers. The muscular layer is covered by a fascial

sheath, which is continuous with the buccopharyn-

geal fascia. The tracheoesophageal (TE) groove abuts

the cervical esophagus on each side and contains the

recurrent laryngeal nerves and the TE groove lymph

nodes. Occasionally, the parathyroid and/or the

thyroid gland extend into the TE groove.

Cross-sectional anatomy

On cross-sectional images, all three components

of the hypopharynx contribute to the structures seen

posterior to the cricoid cartilage (postcricoid portion

of the hypopharynx): the postcricoid area anteriorly

located immediately posterior to the cricoid cartilage,

inferior aspect of the pyriform sinus laterally includ-

ing the pyriform sinus apex, and the posterior

hypopharyngeal wall posteriorly. Since the hypophar-

ynx collapses during MR imaging, the mucosa of the

postcricoid area and posterior hypopharyngeal wall

are in direct contact and are seen as one structure.

Because of their complex anatomy, the postcricoid

portion of the hypopharynx and the esophageal verge

are usually the most challenging images to evaluate.

The knowledge of normative data is essential in

detecting abnormalities [4].

The anteroposterior (AP) dimensions of the

postcricoid portion of the hypopharynx are relatively

constant from the upper to lower margin of the

cricoid cartilage, and an AP diameter of more than

10 mm should be considered abnormal [4]. The

postcricoid area is usually slightly thinner than the

posterior pharyngeal wall (average, 2.5 and 3.5 mm,

respectively) [4]. The transverse dimension of the

postcricoid portion of the hypopharynx tapers from

the upper to the lower margin of the cricoid cartilage.

Observation of lack of normal tapering, particularly

in combination with some other morphologic fea-

tures, such as obscuration of intramural or surround-

ing fat planes, is probably a better indicator of an

underlying abnormality than an overall change in size

[4]. The esophageal diameter varies with the amount

of intraluminal air and is not as useful for evaluation

as the thickness of the esophageal wall itself. An

esophageal wall thickness of less than 5 mm should

be considered normal [4]. The esophageal wall

should also be homogeneously isointense to the sur-

rounding musculature on T2-weighted images

(Fig. 1), demonstrating no signs of enhancement on

the contrasted T1-weighted images [4,5].

The surrounding fat planes lateral to the postcri-

coid portion of the hypopharynx and cervical

esophagus are most consistently seen with the left

side being visualized in most patients followed by the

right lateral fat plane (66% of patients; see Fig. 1) [4].

The posterior fat plane is less frequently seen, with

the best visibility around the esophageal verge (53%

of patients) and in contrast to adjacent levels (20%

of patients) [4]. No differences in visibility of the

surrounding fat planes can be detected with the

various sequences [4]. The fat planes of the TE

groove accommodate the TE groove lymph nodes.

Homogenous-appearing TE groove lymph nodes of

less than 1 cm should be considered normal by

imaging criteria [4,6].

The common wall of the trachea and the esopha-

gus is clearly seen (66% of patients) at the esophageal

verge, with a gradual decrease in frequency more

distally. The contrasted T1-weighted images are

superior to the other sequences in delineation of

Page 3: Imaging of the hypopharynx and cervical esophagus

Fig. 1. Axial T2-weighted image (repetition time 6000 ms, echo time 91 ms) through the cervical esophagus demonstrates

homogeneous signal intensity of the esophageal wall. The hyperintense curvilinear structure within the center of the esopha-

gus represents the mucosa (.). The fat planes lateral to the cervical esophagus are well demarcated (arrows). The posterior

fat plane is not seen, a common finding at the level of the upper cervical esophagus. p, prevertebral musculature; T, trachea;

v, vertebral body.

Fig. 2. Axial noncontrasted T1- (repetition time [TR] 700 ms, echo time [TE] 15 ms) and gradient echo– (TR 733 ms, TE 18 ms,

flip angle 20�) weighted images through the upper cervical esophagus are shown in (A) and (B), respectively. The gradient

echo–weighted image (B) emphasizes the intact fat plane (arrows) within the common wall of the trachea and esophagus,

which is not as clearly seen on the T1-weighted image (A).

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662 649

Page 4: Imaging of the hypopharynx and cervical esophagus

Fig. 3. Noncontrasted T1- (repetition time [TR] 650 ms, echo time [TE] 17 ms) and gradient echo– (TR 550 ms, TE 11 ms, flip

angle 30�) weighted images performed in axial plane at the same level through the hypopharynx demonstrate markedly decreased

visibility of the intramural fat planes (arrowheads) on the T1-weighted image (A) when compared with the gradient echo image

(B). Asymmetry of the intramural fat planes as visualized in (B) can be seen in approximately one third of patients. As in this

case, the left-sided intramural fat planes are typically more obvious. Notice the better delineation of the surrounding fat planes

(arrows) on the gradient echo image with a clear plane toward the prevertebral muscles. c, cricoid cartilage; p, prevertebral

muscles; t, thyroid cartilage; v, vertebral body.

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662650

the common wall of the trachea and the esophagus

(Fig. 2) [4].

The intramural fat planes in the postcricoid

portion of the hypopharynx are especially import

because obliteration of these fat planes might be the

only sign of infiltration by cancer. The visibility of

intramural fat planes decreases in frequency from the

upper to the lower cricoid cartilage (69–30%,

respectively) [4]. The intramural fat planes at the

mid- and lower cricoid levels are identified more

frequently on gradient- echo T2-weighted images

than on T1- or T2-weighted images (Fig. 3) [4]. In

addition, asymmetry of the intramural fat planes is

seen on MR imaging (30% of patients), and typically,

the left-sided fat planes are more obvious [4].

Pathology

Less than 5% of tumors of the hypopharynx and

cervical esophagus are of nonsquamous cell origin

[2]. These include benign tumors, such as lipomas,

retention cysts of minor salivary glands, leiomyomas,

papillomas, adenomas, or angiomatous tumors, and

nonsquamous cell malignancies, such as various

sarcomas, lymphoma, or malignant minor salivary

gland tumors [2,7,8]. Because these lesions are rare,

this article focuses on squamous cell carcinoma of the

hypopharynx and cervical esophagus alone. Pyriform

sinus cancer is the most common subtype of squa-

mous cell carcinoma of this region. Usually, the

definitive diagnosis of hypopharyngeal and esopha-

geal masses requires biopsy, and the radiologist must

recognize high-vascular masses to prevent extensive

bleeding when a biopsy is performed.

Hypopharyngeal and cervical esophageal cancer

are usually indolent and in advanced stage at pre-

sentation. Up to 75% of patients have nodal metas-

tasis and 20% to 40% patients have distant metastasis

at presentation [9]. Even patients with N0 neck have a

30% chance of having occult metastasis on elective

dissections [10].

The most often encountered symptoms are neck

masses secondary to metastatic lymph nodes, dys-

phagia, odynophagia, globus sensation, otalgia,

weight loss, voice changes (bhot potatoQ voice), andfood impaction. The main risk factors are smoking,

alcohol abuse, and previous radiation therapy. Post-

cricoid area tumors are also associated with Plum-

mer-Vinson syndrome, rarely seen in the United

States or continental Europe but commonly encoun-

tered in the United Kingdom [11]. In contrast to

most hypopharyngeal and cervical esophageal

cancers, tumors associated with Plummer-Vinson

syndrome typically occur in women and are hy-

pothesized to come from food stasis caused by

hypopharyngeal or esophageal webs, one of the

main findings besides iron deficiency anemia seen

with this syndrome.

Growth pattern

Overall, hypopharyngeal and cervical esophageal

cancers are predisposed to spread in sub-mucosal

fashion [12]. The submucosal spread is often unde-

tectable on clinical and/or endoscopic examination.

Page 5: Imaging of the hypopharynx and cervical esophagus

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662 651

Otherwise, the various subtypes of the hypopharyng-

eal malignancies have a different spread pattern.

Postcricoid area tumors tend to invade the

posterior aspect of the larynx, causing vocal cord

paralysis and hoarseness. The cricoarytenoid joint

itself is rarely involved. In addition, these tumors

have a high tendency to involve the pyriform sinuses

Fig. 4. Axial noncontrasted (A, C) and contrasted T1- (B, D) weig

72-year-old patient with squamous cell carcinoma of the posterior

gus. (A, B) The noncontrasted T1-weighted image at the level of

(AP) diameter of the postcricoid region (between arrows) measuri

tumor is otherwise difficult to delineate but is clearly seen on the co

(C, D) The noncontrasted (C) and contrasted (D) T1-weighted imag

the cervical diameter in AP and lateral dimensions with 22 mm an

wall of the esophagus cannot be clearly identified as separate struc

fat plane within the common wall of the trachea and esophagus is n

tumor (arrows). E, esophagus; t, trachea.

(100%), trachea (71%), and/or esophagus (71%) [13].

Tracheal or esophageal invasion is missed by endo-

scopic evaluation in approximately 50% of these

patients [13].

Posterior hypopharyngeal wall cancers tend to

spread in a craniocaudal direction and can extend into

the nasopharynx and/or esophagus (Fig. 4) [14]. The

hted images (repetition time 800 ms, echo time 12 ms) of a

pharyngeal wall extending into the upper cervical esopha-

the hypopharynx (A) demonstrates abnormal anteroposterior

ng 13 mm. The normal AP dimension is up to 10 mm. The

ntrasted T1-weighted image at the same level (arrows in B).

es through the upper esophagus show marked enlargement of

d 26 mm, respectively. The muscosal layer and the muscular

tures as expected on contrasted T1-weighted image (D). The

ot seen on either image, consistent with gross invasion by the

Page 6: Imaging of the hypopharynx and cervical esophagus

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662652

craniocaudal extension of these tumors may occur in

superficial fashion only and remain undetectable on

cross-sectional examination. Rarely, these tumors

cause infiltration of the prevertebral fascia or

musculature at presentation. Even when there is

effacement of the prevertebral fat planes on cross-

sectional imaging, including MR imaging, the diag-

nosis of prevertebral fascia or muscle invasion cannot

be made. Surgical exploration is necessary for

Fig. 5. Axial T2-weighted images (repetition time 6000 ms, echo tim

cancer on the left side. Large nodal metastasis (N) is seen in the

(open arrow). (A) There are signs of invasion of the inferior constr

side seen as thinning of the muscle thickness when compared wi

focal area of disruption of the inferior constrictor muscle (arrows)

the neck at this level. (B) The tumor (T ) is extending between

(arrows) to grossly invade the true vocal cord on the left side in sub

suspected clinically because of the more medial position of the le

internal jugular vein.

definitive diagnosis because of the high false-positive

rate on imaging.

The growth pattern of pyriform sinus cancers

depends on their origin and extent. Tumors arising

from or involving the lateral wall tend to invade

the posterior aspect of the thyroid cartilage and ex-

tend into the soft tissues of the lateral compartment

of the neck (Fig. 5A). Direct infiltration of the

intrinsic laryngeal muscles is rarely seen, in con-

e 99 ms) of a 73-year-old patient with a large pyriform sinus

left neck with significant compression of the jugular vein

ictor muscle (small arrowheads) by the tumor (T) on the left

th the right side (large arrowheads). In addition, there is a

consistent with early invasion of the lateral compartment of

the thyroid cartilage and the cricoarytenoid joint anteriorly

mucosal fashion. The submucosal extension of the tumor was

ft true vocal cord when compared with the right. i, normal

Page 7: Imaging of the hypopharynx and cervical esophagus

Table 1

Spread pattern of pyriform sinus carcinomas

Lateral wall tumor (%) Medial wall tumor (%)

Tumor involving lateral

and medial wall (%)

Thyroid cartilage 83.3 12.5 60

Cricoid cartilage 0 12.5 20

Arytenoid cartilage 0 12.5 10

Cricoarytenoid joint 0 18.8 5

Paraglottic space 66.7 50 70

Pre-epiglottic space 0 50 35

Tumor outside of thyroid ala 66.7 0 50

Contralateral tumor extension 0 87.5 40

Submucosal spread >8 mm 16.7 56.3 25

Perineural invasiona 0 43.8 55

Thyroid gland 33.3 0 25

a Was always associated with involvement of the laryngeal muscles and never seen as an isolated finding.

Data from Zbaren P, Egger C. Growth pattern of piriform sinus carcinomas. Laryngoscope 1997;107:511–8.

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662 653

trast to tumors arising from or involving the medial

wall of the pyriform sinus. The latter show early

laryngeal infiltration with cord fixation (60%;

Fig. 5B) [2,11,14]. Table 1 shows characteristics

in spread pattern of pyriform sinus cancers and

their frequency.

Cervical esophageal tumors tend to involve ana-

tomically adjacent structures, such as the trachea,

Fig. 6. Axial noncontrasted T1-weighted image (repetition time

squamous cell carcinoma of the cervical esophagus (E) illustrates co

fat plane on the left side (arrows). The left lateral fat plane is the

indicate gross extension of the tumor through the esophageal seros

(open arrows).

recurrent laryngeal nerve, and adjacent vasculature

(Fig. 6). In addition, they tend to spread in a sub-

mucosal fashion to the hypopharynx (Fig. 7).

The craniocaudal extension of the hypopharyngeal

tumor into the cervical esophagus and vice versa is

crucial for the extent of surgical resection (limited

versus extensive resection; see later discussion).

Because this type of tumor can spread in a superficial

850 ms, echo time 15 ms) of a 56-year-old patient with

mplete obliteration of the anterior portion of the surrounding

most consistently seen surrounding fat plane. These findings

a. Notice the normal appearance of the right lateral fat plane

Page 8: Imaging of the hypopharynx and cervical esophagus

Fig. 7. Axial noncontrasted T1-weighted images (repetition time 800 ms, echo time 15 ms) through the upper esophagus (A) and

the hypopharynx (B) of a 69-year-old patient with entirely submucosally located squamous cell carcinoma of the esophagus. The

diagnosis was made by percutaneous biopsy under CT guidance. The anteroposterior (between arrows) and lateral diameters

(between arrowheads in A) of the esophagus are markedly increased with 30 and 33 mm, respectively. The tumor extended in

submucosal fashion into the postcricoid region on the right side reflected as mild posterior bulging of the right postcricoid region

(arrows in B) and lack of intramural fat planes on the right when compared with the left (arrowheads in B).

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662654

or submucosal pattern, a combination of clinical

examination and crosssectional study should be used

in the treatment planning process.

Nodal chain involvement

The three portions of the hypopharynx and

cervical esophagus have slightly different lymphatic

drainage pathways: the postcricoid area tumors tend

to metastasize to group III, IV, and VI lymph nodes

(paratracheal/TE groove); the pyriform sinus tumors

drain primarily into group II, III, and V lymph nodes;

and posterior hypopharyngeal wall cancers have the

tendency primarily to involve the retropharyngeal

lymph nodes and secondarily the internal jugular

chain lymph nodes. In contrast, the other types of

hypopharyngeal cancer involve the retropharyngeal

lymph nodes (15%), but only if the neck is also

positive [9]. The cervical esophageal cancer drains

into group VI and mediastinal lymph nodes. The

group VI lymph nodes are involved usually (71%) at

the time of diagnosis [15].

Page 9: Imaging of the hypopharynx and cervical esophagus

Table 2

Staging of primary tumors of the hypopharynx

Stage Characteristics

Primary tumor

Tis Carcinoma in situ

T1 Tumor limited to one subsite of hypopharynx and 2 cm or less in greatest dimension

T2 Tumor invades more than one subsite of hypopharynx or an adjacent site, or measures more

than 2 cm but not more than 4 cm in greatest dimension without fixation of hemilarynx

T3 Tumor more than 4 cm in greatest dimension or with fixation of the hemilarynx

T4 Tumor invades thyroid/cricoid cartilage, hyoid bone, thyroid gland, esophagus, or central

compartment soft tissuesa

Central compartment soft tissues includes prelaryngeal strap muscles and subcutaneous fata

Regional lymph nodes

NX Regional lymph nodes cannot be assessed

N0 No regional lymph node metastasis

N1 Metastasis in a single ipsilateral lymph node, of 3 cm or less in greatest dimension

N2

N2a Metastasis in a single ipsilateral lymph node more than 3 cm but not more than 6 cm in

greatest dimension

N2b Metastasis in multiple ipsilateral lymph nodes, none more than 6 cm in greatest dimension

N2c Metastasis in bilateral or contralateral lymph nodes, none more than 6 cm in greatest dimension

N3 Metastasis in a lymph node more than 6 cm in greatest dimension

a Adapted from American Joint Committee on Cancer. AJCC cancer staging handbook. 6th edition. Philadelphia: Lippincott,

Williams, & Wilkins; 2002.

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662 655

Tumor, node, metastases classification

Classification of primary tumors of the hypophar-

ynx and cervical esophagus according to the Amer-

ican Joint Committee on Cancer [16] is listed in

Tables 2 and 3, respectively. The recommended

staging of cervical esophageal lesions is identical to

that of the intrathoracic esophagus.

able 3

taging of primary tumors of the cervical esophagus

tage Characteristics

rimary tumor

Tis Carcinoma in situ

T1 Tumor invades the lamina propria

or submucosa

T2 Tumor invades muscularis propria

T3 Tumor invades adventitia

T4 Tumor invades adjacent structures

egional lymph nodes

NX Regional lymph nodes cannot be assessed

N0 No regional lymph node metastasis

N1 Regional lymph node metastasis

dapted from American Joint Committee on Cancer. AJCC

ancer staging handbook. 6th edition. Philadelphia: Lippin-

ott, Williams, & Wilkins; 2002.

Secondary involvement by other tumors

Direct invasion of the hypopharynx and cervical

esophagus by surrounding tumors is uncommon but

may be seen with advanced head and neck tumors,

thyroid tumors, and bronchogenic carcinomas [17].

Focal areas of increased signal intensity on the

T2-weighted images suggest presence of invasion

[17] (Fig. 8). Focal enhancement following contrast

administration might also be a sign of infiltration;

however, it is not as specific as the T2 changes [17]

(see Fig. 8). Circumferential mass at the level of the

cervical esophagus is the most sensitive and specific

sign of invasion (accuracy, 100%) [17]. An intact fat

plane, absence of wall thickening, and normal

T2 wall signal intensity indicate no invasion with a

very high degree of confidence (see Fig. 1) [17].

Impact of cross-sectional imaging

Multiple published studies document the impact

of cross-sectional imaging on staging of hypophar-

yngeal and/or esophageal cancer [1,2,13,14,18,19].

Most of these studies focus on CT, but the limited

data on MR imaging suggest that a similar or

T

S

S

P

R

A

c

c

Page 10: Imaging of the hypopharynx and cervical esophagus

Fig. 8. A 77-year-old man with large medullary thyroid cancer (T) on the right side. At the level of the lower hypopharynx, there

are signs of early infiltration of the inferior pharyngeal constrictor muscle on the left side (arrowheads, B). This is clearly

identified on the contrasted T1-(repetition time [TR] 600 ms, echo time [TE] 15 ms) and T2- (TR 5000 ms, TE 99 ms) weighted

images (B and C, respectively), but difficult to appreciate on the noncontrasted T1-weighted image (A). On the noncontrasted

T1-weighted image (A), the absence of the intramural fat planes on the left side when compared with the right (arrows) should

raise the suspicion for tumor invasion. (D) Axial T2-weighted image at the level of the upper cervical esophagus demonstrates

the significant impression of the esophagus from left lateral by the tumor and the gross invasion of the posterior esophageal wall

(arrows) and the left lateral tracheal wall (open arrows).

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662656

even higher percentage in upstaging of tumors is

expected with MR imaging alone [1,2]. Overall,

the clinical tumor stage was increased with cross-

sectional imaging in up to 90% of patients [1,13,14,

18,19]. In up to 67% of patients, the T stage

was changed based on soft tissue involvement

(�88% of patients) or bone/cartilage invasion

(�23% of patients) [13,14,18]. The N stage was

changed in up to 33% of patients [14,18]. According

to Wenig et al [1], the accuracy in tumor staging

improved in 40% of patients with MR imaging alone.

The tumor staging accuracy when compared with

pathologic findings has been reported to be 58% for

clinical examination, 80% for CT, and 85% for MR

imaging [2]. These facts clearly demonstrate the

essential role of cross-sectional imaging in staging

of hypopharyngeal and esophageal cancer. None of

the other cancers of the head and neck region

Page 11: Imaging of the hypopharynx and cervical esophagus

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662 657

shows such a significant impact of cross-sectional

imaging on staging.

Radiologist’s role during pretreatment

As with other cancers of the head and neck region,

the radiologist must report the origin and full extent

of the primary tumor and the nodal status throughout

the neck. The specific issues pertinent to hypophar-

yngeal and esophageal cancer in the following

subsections should be emphasized.

Submucosal spread

Submucosal tumor spread remains undetectable

in a significant number of patients on clinical and

endoscopic examination [12]. The tumor often grows

over a significant distance in submucosal fashion,

precluding planned limited surgical intervention

(see later discussion) in a significant number of

patients. Occasionally, the entire tumor is submucosal

in location and cannot be assessed to endoscopic

biopsy. Under these circumstances, the radiologist

may offer percutaneous biopsy performed with cross-

sectional guidance.

Cartilage involvement

Most radiologists prefer CT for evaluating carti-

lage involvement. This is partially because of the

assumption that cartilage involvement (cartilage

sclerosis and cartilage erosion or lysis) is more easily

detected on CT studies than MR imaging. MR

imaging findings indicating cartilage invasion might

be more difficult to be interpreted by the inexper-

ienced radiologist.

The assessment of MR imaging should include

detection of altered signal intensity of the hyaline

cartilage and bone marrow within it [2]. The invaded

hyaline cartilage typically demonstrates increased T2

and decreased T1 signal intensity [2]. The involved

bone marrow demonstrates decreased attenuation on

T1-weighted images in relation to the uninvolved

fatty replaced bone marrow typically seen in older

patients [2]. Both involved hyaline cartilage and bone

marrow enhance markedly after contrast administra-

tion. With these imaging criteria, a very high

sensitivity (89% to 100%) for detection of cartilage

involvement can be found [1,2]. The problem,

however, is that similar changes can be caused by

reactive inflammation, edema, or fibrosis [2]; there-

fore, MR imaging has an overall specificity of

only 74% to 88%, and an even lower positive pre-

dictive value of 68% to 71% [1,3,20,21]. In addition,

the specificity depends on the cartilage type, as

also demonstrated for CT [2]. The thyroid cartilage

with its variable ossification has the lowest specificity

for cartilage involvement (56%) [2]. Therefore,

thyroid cartilage involvement by tumor should only

be made with caution when based on MR imaging

findings alone. The specificity for cartilage invasion

detection is the highest for arytenoid cartilage (95%)

and intermediate for cricoid cartilage (87%) [2].

Nevertheless, MRimaging is valuable as a good pre-

dictor of the absence of cartilage invasion with

negative predictive values of more than 92% [2,3,

20,21].

Why is it so important to detect involved cartilage

even though it does not play a role in tumor staging

itself? It is well known that nonremoval of an

involved cartilage carries a risk (50–60%) of leaving

tumor behind; therefore, this information is pertinent

for therapy planning, particularly if the patient is

suitable for limited laryngectomy.

Tumor volume

In recent years, emphasis has been placed on

stratifying patients in high- or low-risk groups re-

garding certain treatment modalities and their out-

come. The most important criteria have been volume

of the tumor and cartilage involvement (see previ-

ous discussion).

Pameijer et al [22] found two important prognos-

tic factors for T1 and T2 pyriform sinus cancers

treated with radiation therapy alone: tumor volume

and amount of disease at the pyriform sinus apex

[22]. Although this study was conducted based on CT

imaging findings, the same or similar results are

expected for MR imaging. The authors defined

pyriform sinus apex disease as bminimal apical

diseaseQ if the tumor was less than 10 mm in diameter

at the level of the base of the arytenoid cartilage and

upper 3 mm of the cricoid cartilage or as bbulkyapical diseaseQ if the diameter was greater than or

equal to 10 mm. Their results characterized three

different patient groups with the following criteria

and local control rates if treated with radiation

therapy alone:

Low-risk group: Patients with tumor volume

<6.5 mL and no or minimal apical disease

showed a local control rate of 94% [22].

Moderate-risk group: Patients with tumor volume

of <6.5 mL and bulky apical disease or tumor

volume �6.5 mL and no or minimal apical

Page 12: Imaging of the hypopharynx and cervical esophagus

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662658

disease demonstrated local control rates of

50% [22].

High-risk group: None of the patients survived

with tumor volume of �6.5 mL and bulky

apical disease [22].

Therefore, reporting of tumor volume and apical

disease should be done for all T1 and T2 stage

pyriform sinus cancers.

Detection of second primary tumors

The rate of second primary tumors in patients with

hypopharyngeal or cervical esophagus cancer is

higher than for the remainder of head and neck

cancers, with a reported frequency of up to 15% [9].

In 25% of patients, the second primary tumor (syn-

chronous lesion) is found at the time of the diagnosis

of the hypopharyngeal or esophageal cancer and in

75% of patients at other times (metachronous lesion)

[9]. Therefore, every cross-sectional study, including

posttreatment examinations, should be evaluated for

a second primary tumor.

Radiologist’s role during treatment

Currently, the radiologist does not play a signifi-

cant role during the treatment phase itself unless the

patient requires a percutaneous feeding tube place-

ment or complications occur, such as development of

fistula, vascular rupture requiring embolization, or

abscess formation. Advances in current therapy

options and development of new treatment regimes,

however, may require the radiologist to take an

active role in the therapy delivery, such as intra-

arterial administration of chemotherapy and intra-

arterial or percutaneous administration of gene

therapy agents.

The published results for intravenous administra-

tion of induction, neoadjuvant, or adjuvant chemo-

therapy have been rather disappointing because all of

these studies demonstrated no significant differences

in survival or local control [23–25]. The addition of

chemotherapy to other treatment options, however,

significantly reduced the incidence of distant meta-

stasis [23–25]. Cisplatin-based chemotherapy agents

showed the most effect upon head and neck cancers,

which might be due to higher sensitivity of esoph-

ageal cell lines to cisplatin as suggested by Kovacs

et al [26]. Potentially this might also apply to the cell

line of the hypopharyngeal region. Published results

of intra-arterial administration of a supradose of

cisplatin into the tumor supplying vessels combined

with concurrent radiation therapy (bRADPLAT pro-

tocolQ) suggest a significantly increased rate of local

control in advanced head and neck tumors (80%) and

an improved 5-year disease-specific and overall

survival rate (54% and 39%, respectively) [27].

Preliminary results of the RADPLAT protocol

applied to pyriform sinus cancers specifically showed

a complete local response rate of 92% and of 76% at

the nodal site and the 5-year disease-specific and

overall survival rates (of 50% and 23%, respectively)

[28]. These survival rates are similar or slightly

higher than reported by other treatment modalities;

however, the main advantage of this treatment regime

is the very high organ preservation rate (88%) with

adequate voice preservation (88%) and acceptable

swallowing abilities at 6-month and 12-month fol-

low-up (50% and 67%, respectively) [28]. Samant

et al [28] noted an altered pattern of failure with

shift from local recurrences to distant metastasis. No

data regarding other sites of the hypopharynx or

cervical esophagus are available.

Radiologist’s role during posttreatment

Currently, most tumors of the hypopharynx and

cervical esophagus present at advanced stage and,

therefore, only a relatively small percentage of

patients can undergo organ preservation therapy, such

as seen with the larynx, sparing surgical resection or

radiation therapy alone. Most patients undergo total

laryngectomy with resection of the entire larynx,

pyriform sinuses, surrounding strap muscles, and

various options for reconstruction of the pharynx (eg,

primary closure with hypopharyngeal mucosa and

inferior constrictor muscles, jejunal interposition, or

gastric pull-up) [29]. Often, these patients also

receive pre- or postsurgery radiation therapy, possibly

combined with chemotherapy. Despite the extensive

treatment protocols, the 5-year survival rates are

dismal (range, 20–34%), with local recurrence rates

of 32% to 46% at 2 years for advanced hypophar-

yngeal and cervical esophageal cancers [10,29,30].

The addition of pre-surgery radiation therapy also

has a high incidence of postsurgical complications

(47%) [30].

Postradiation therapy

Postradiotherapy changes sometimes are difficult

to be distinguished from recurrent tumor on clinical

examination. Therefore, the referring physicians rely

on imaging evaluation. Up to 40% of recurrent

tumors are detected with cross-sectional imaging

Page 13: Imaging of the hypopharynx and cervical esophagus

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662 659

prior to visibility on clinical examination [30]. To

allow easier and faster detection of recurrent or

persistent tumor, a follow-up CT and/or MR imaging

study is recommended at 3 to 4 months following

completion of radiation therapy. Hermans et al [31]

characterized three groups of patients based on the

3-to 4-month follow-up CT scans of patients treated

for laryngeal or hypopharyngeal carcinoma:

1. None of the patients showed local failure if

complete resolution of the tumor and symmet-

ric-appearing soft tissue planes were seen on

the baseline CT examination at 3 to 4 months

following completion of radiation therapy. This

patient group requires continued clinical fol-

low-up and cross-sectional imaging only if

suspicion for recurrent tumor is raised on the

clinical examination [31].

2. Patients with tumor volume reduction of <50%

or a persistent mass of �1 cm in diameter

demonstrated a high likelihood of local failure,

with failure rates of 100% and 30%, respec-

tively. These patients should undergo immedi-

ate further investigation with biopsy for lesions

with less than 50% response in tumor volume.

In patients with a persistent mass of �1 cm in

diameter, follow-up imaging at 3 to 4 months,

fluorine-18 fluorodeoxyglucose (FDG) positron

emission tomography scan and/or biopsy are

appropriate alternatives [31,32].

3. If the baseline CT shows a residual mass of <1

cm in diameter or asymmetry, of the soft tissue

planes, cross-sectional follow-up at 3-to

4-month intervals for 2 years should be

performed if there is no clinical suspicion for

recurrent tumor [31]. Two consecutive stable

studies after the baseline study are consistent

with control at the primary site.

Although all results were conducted on CT

imaging alone, MR imaging studies are expected to

yield the same data [31].

In the same study, Hermans et al [31] also

evaluated cartilage alterations and likelihood of

recurrence. They found that a persistent mass �1 cm

in diameter in association with cartilage changes

should be considered as local failure. Minimal soft

tissue asymmetry and cartilage changes should be

closely monitored because these changes could be

caused by recurrent tumor or chondronecrosis [30].

It is uncertain if the results regarding cartilage

alteration can be transferred, and to what degree, to

MR imaging studies. Fluorine-18 FDG positron

emission tomography may also gain a dominant

role in posttreatment evaluation of patients with

hypopharyngeal and/or cervical esophageal cancer

treated with the newer, more aggressive type of

therapy options as more results are published in this

regard [33].

Postsurgery

Recurrent tumors typically occur at the margins of

the resection or within the deep tissues of the neck in

surgical patients. Therefore, it is pertinent that the

radiologist is familiar with the normal appearance of

the reconstructed pharynx and possible complica-

tions. The most commonly encountered complica-

tions are fistula formation (26%), wound infection

(22%), and stricture (9%) [10,34].

Currently, the methods of hypopharyngeal recon-

struction most often employ the jejunal free flap, with

microvascular anastomosis, or the gastric pull-up.

Pectoralis major myocutaneous and radial forearm

flaps may be used for subtotal hypopharyngeal

defects in which a posterior stripe of mucosa remains

intact. Their use is precluded if extension of the

tumor into the cervical esophagus is present. The use

of the radial forearm flap over jejunal interposition

has the advantage of improved swallowing function

[35]. The pectoralis flap is associated with higher

incidence of fistulas and strictures, which may be

because of difficulty in formation of the required

tubal shape secondary to lack of pliability. A free

jejunal graft with microvascular anatostomosis is the

reconstructive method of choice for lesions of the

hypopharynx that require total pharyngectomy for

reconstruction of extensive defects and for limited

invasion of the cervical esophagus. The jejunal graft

has a low incidence of strictures and fistula formation

and tolerates postoperative radiation therapy better

than any other method of reconstruction [36]. Occa-

sionally, dysphagia and stasis symptoms may be seen

because of a kink in the conduit if a too-long jejunal

interposition was chosen [36]. Gastric pull-up is the

reconstruction method of choice in patients with

cervical esophagus involvement of a longer segment.

It shows a low rate of fistula formation, but dumping

and reflux are frequent patient complaints.

On cross-sectional images, the appearance of the

mucosa is not very helpful in evaluating recurrent

tumor because single or multiple irregular-appearing

folds are typically seen in jejunal inter-position and

with gastric pull-up. The evaluation of cross-sectional

imaging studies should instead focus on regular

thickness and smooth external margins of the neo-

pharyngeal wall (Fig. 9) [2].

Page 14: Imaging of the hypopharynx and cervical esophagus

Fig. 9. Sagittal noncontrasted T1- (repetition time [TR] 700 ms, echo time [TE] 15 ms) weighted image of a 72-year-old man

demonstrates the craniocaudal extent of the squamous cell cancer of the posterior pharyngeal wall (arrows in A). (A, B) The

bulk of the tumor is superior to the cricoid cartilage (c), but it is extending into the postcricoid region. The axial noncontrasted

T1-weighted image (TR 500 ms, TE 15 ms) confirms the left-sided tumor (T) in the postcricoid region identified as absence

of the intramural fat plane on the left when compared with the right (arrowheads in B). This patient underwent total

laryngectomy and pharyngectomy with jejunal interposition. (C) Axial contrasted T1- (TR 500 ms, TE 17 ms) weighted

image through the neopharynx performed 2 years after the surgery shows a polypoid lesion (white arrows) along the right

lateral wall of the jejunal interposition. Because the external wall of the neopharynx (black arrows) is well defined, this

should be considered a mucosal fold rather than mistaken for recurrent tumor.

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662660

Page 15: Imaging of the hypopharynx and cervical esophagus

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662 661

References

[1] Wenig BL, Ziffra KL, Mafee MF, et al. MR imaging of

squamous cell carcinoma of the larynx and hypophar-

ynx. Otolaryngol Clin North Am 1995;28:609–19.

[2] Becker M. Larynx and hypopharynx. Radiol Clin

North Am 1998;36:891–920.

[3] Castelijns JA, Gerritsen GJ, Kaiser MC, et al. Invasion

of laryngeal cartilage by cancer: comparison of CT and

MR imaging. Radiology 1987;166:199–206.

[4] Schmalfuss IM, Mancuso AA, Tart R. Postcricoid

region and cervical esophagus:normal appearance at

CT and MRimaging. Radiology 2000;214:237–46.

[5] Quint L, Glazer G, Orringer M. Esophageal imaging

by MR CT: study of normal anatomy and neoplasms.

Radiology 1985;156:727–31.

[6] Glazer GM, Gross BH, Quint LE, et al. Normal

mediastinal lymph nodes: number and size according

to American Thoracic Society mapping. AJR Am J

Roentgenol 1985;144:261–5.

[7] Hovelmann B, Pau HW. Diagnostische schwierigkeiten

bei gutartigen hypopharynxgeschwulsten. Laryngo-

Rhino-Otol 1991;70:239–42.

[8] Jungehulsing M, Fischbach R, Pototschnig C, et al.

Rare benign tumors: laryngeal and hypopharyngeal

lipomata. Ann Otol Rhinol Laryngol 2000;109:301–5.

[9] Million RR. Pharyngeal walls, pyriform sinus, post-

cricoid pharynx. In: Million RR, editor. Management

of head and neck cancer. Philadelphia7 JB Lippincott,

1994. p. 502–32.

[10] Kraus DH, Zelefsky MJ, Brock HA, et al. Combined

surgery and radiation therapy for squamous cell

carcinoma of the hypopharynx. Otolaryngol Head

Neck Surg 1997;116:637–41.

[11] Zbaren P, Egger C. Growth pattern of piriform sinus

carcinomas. Laryngoscope 1997;107:511–8.

[12] Saleh E, Mancuso AA, Stringer S. Relative roles of

computed tomography and endoscopy for determining

the inferior extent of pyriform sinus carcinoma:

correlative histopathologic study. Head Neck 1993;

15:44–52.

[13] Aspestrand F, Kolbenstvendt A, Boysen M. Carcinoma

of the hypopharynx: CT staging. J Comput Assist

Tomogr 1990;14:72–6.

[14] Nowak B, Di Martino E, Janicke S, et al. Diagnostic

evaluation of malignant head and neck cancer by F-18-

FDG PET compared to CT/MRI. in GermanNuklear-

medizin 1999;38:312–8.

[15] Weber RS, Marvel J, Smith P, et al. Paratracheal lymph

node dissection for carcinoam of the larynx, hypo-

pharynx and cervical esophagus. Otolaryngol Head

Neck Surg 1993;108:11–7.

[16] American Joint Committee on Cancer. AJCC cancer

staging handbook. 6th edition. Philadelphia7 Lippin-

cott, Williams, & Wilkins; 2002.

[17] Roychowdhury S, Laevner LA, Yousem DM, et al.

MR imaging for predicting neoplastic invasion of the

cervical esophagus. AJNR Am J Neuroradiol 2000;

21:1681–7.

[18] Prehn RB, Pasic TR, Harari PM, et al. Influence of

computed tomography on pretherapeutic tumor staging

in head and neck cancer patients. Otolaryngol Head

Neck Surg 1998;119:628–33.

[19] Thabet HM, Sessions DG, Gado MH, et al. Compar-

ison of clinical evaluation and computed tomographic

diagnostic accuracy for tumors of the larynx and

hypopharynx. Laryngoscope 1996;106:589–94.

[20] Becker M, Zbaren P, Laeng H, et al. Neoplastic

invasion of the laryngeal cartilage: comparison of

MR imaging and CT with histopathologic correlation.

Radiology 1995;194:661–9.

[21] Zbaren P, Begger M, Laeng H. Pretherapeutic staging

of laryngeal cancer: clinical findings, computed

tomography and magnetic resonance imaging versus

histopahtology. Cancer 1996;77:1263–73.

[22] Pameijer FA, Mancuso AA, Mendenhall WM, et al.

Evaluation of pretreatment computed tomography as a

predictor of local control in T1/T2 pyriform sinus

carcinoma treated with definitive radiotherapy. Head

Neck 1998;20:159–68.

[23] Adjuvant chemotherapy for advanced head and neck

squamous carcinomas. Final report of the Head and

Neck Contracts Program. Cancer 1987;60:301–11.

[24] Laramore GE, Scott CB, Al-Sarraf M, et al. Adjuvant

chemotherapy for resectable squamous cell carcinomas

of the head and neck: report on intergroup study 0034.

Int J Radiat Oncol Biol Phys 1992;23:705–13.

[25] Paccagnella A, Orlando A, Marchiori C, et al. Phase III

trail of initial chemotherapy in stage III or IV head and

neck cancers: a study by the Gruppo di Studio Sui

Tumori Della Testa e Del Collo. J Natl Cancer Inst

1994;86:265–72.

[26] Kovacs AF, Cinatl Jr J. In vitro cytotoxic close-relation

of cisplatin and sodium thiosulphate in human tongue

and oesophageal squamous carcinoma cell lines.

J Craniomaxillofac Surg 2002;30:54–8.

[27] Robbins KT, Kumar P, Wong FS, et al. Targeted

chemoradiation for advanced head and neck cancer:

analysis of 213 patients. Head Neck 2000;22:687–93.

[28] Samant S, Kumar P, Wan J, et al. Concomitant

radiation therapy and targeted cisplatin chemotherapy

for the treatment of advanced pyriform sinus carci-

noma: disease control and preservation of organ

function. Head Neck 1999;21:595–601.

[29] Kraus DH, Pfister DG, Harrison LB, et al. Larynx

preservation with combined chemotherapy and radia-

tion therapy in advanced hypopharynx cancer. Otolar-

yngol Head Neck Surg 1994;148:31–7.

[30] Pawlik AB, Stockli SJ, Schmid S. Salvage surgery

in laryngeal and hypopharyngeal carcinoma. in

GermanSchweiz Med Wochenschr Suppl 2000;116:

27S–30S.

[31] Hermans R, Pameijer FA, Mancuso AA, et al. Laryn-

geal or hypopharyngeal squamous cell carcinoma:

can follow-up CT after definitive radiation therapy

be used to detect local failure earlier than clinical

examination alone? Radiology 2000;214:683–7.

[32] Mukherji SK, Mancuso AA, Kotzur IM, et al. Radio-

Page 16: Imaging of the hypopharynx and cervical esophagus

I.M. Schmalfuss / Neuroimag Clin N Am 14 (2004) 647–662662

logic appearance of the irradiated larynx. Part 2. Pri-

mary site response. Radiology 1994;193:149–54.

[33] Kitagawa Y, Nishizawa S, Sano K, et al. Prospective

comparison of 18-FDG PET with conventional imag-

ing modalities (MRI, CT, and 67 Ga scintigraphy) in

assessment of combined intraarterial chemotherapy

and radiotherapy for head and neck carcinoma. J Nucl

Med 2003;44:198–206.

[34] Wei WI, Lam KH, Choi S, et al. Late problems after

pharyngolaryngoesophagectomy and pharyngogastric

anastomosis for cancer of the larynx and hypopharynx.

Am J Surg 1984;148:509–13.

[35] Anthony JP, Singer MF, Mathes SJ, et al. Pharyngoe-

sophgeal reconstruction using the tube free radial

forearm flap. Clin Plast Surg 1994;21:137–47.

[36] Reece GP, Schusterman MA, Miller MJ, et al. Morbid-

ity and functional outcome of free jejunal transfer

reconstruction for circumferential defects of the phar-

ynx and cervical esophagus. Plast Reconstr Surg 1995;

96:1307–16.