positron emission tomography-computerized tomography in the management of head and neck cancer

Positron Emission Tomography-ComputerizedTomography in the Management of Headand Neck Cancer

Luke Bolek, Michael M. GrahamDepartment of Radiology, Division of Nuclear Medicine, University of Iowa, Iowa, USA

Correspondence to:Luke Bolek M.D.MD Anderson Cancer Center Orlando, 1400 South Orange Avenue, Orlando, Florida 32806Tel: 321-843-5159; Fax: 321-841-7745; E-mail: [email protected] or [email protected]

Key words: PET/CT, squamous cell carcinoma, oropharyngeal cancer, EB, head and neck.

Summary

PET/CT plays an important role in the evaluation and

follow up of patients with various head and neck neo-

plasms.

The role of PET/CT in the management of a wide

variety of head and neck cancers varies based on the TNM

tumour stage. Futhermore, because there is a large overlap

between tumour and physiologic FDG uptake, interpreta-

tion of malignancies in the head and neck on PET/CT can

be confusing/unclear.

Thus, it is essential to have knowledge of the patient’s

prior history, including relevant surgical procedures as well

as prior chemo and radiation treatment for proper

interpretation of head and neck malignancies.

This article examines how FDG PET/CT is utilized in

squamous cell carcinoma of the nasopharyax and larynx.

Introduction

It is estimated there will be 45 660 new cases and 11 210

deaths from head and neck cancer, including larynx, in the

United States in 2007 (1). The death rate is falling, from

30% in 2003 to 25% in 2007. This improvement is almost

certainly due to better therapy; it is also due to more

accurate staging and follow-up. Positron emission

tomography-computerized tomography (PET-CT) with18F-fluorodeoxyglucose (FDG) has become a critical tool in

the evaluation and follow-up of these patients with a wide

variety of head and neck cancers. It is used for diagnosis in

patients with an unknown primary, staging for most

squamous cell cancers of the head and neck, evaluation

following treatment for residual or recurrent disease and

for surveillance after complete response (2).

PET imaging of the head and neck is more challenging

than in most other sites in the body because of the

complex, tightly packed anatomy and because several

normal structures often take up FDG and can be mistaken

for malignancy. Interpretation of PET studies in this region

must be performed carefully. The addition of registered

and fused CT images in the modern PET-CT systems

has helped enormously in improving the accuracy of

interpretation.

The following paper discusses the use of FDG PET-CT

in squamous cell malignancies in four major anatomic

regions of the head and neck, i.e. nasopharyngeal,

oropharyngeal, hypopharyngeal and larynx. These sites

are the most common locations for occurrence of

malignancy in the head and neck and covers at least

80% of the head and neck cancers. This paper is not

intended to be encyclopaedic and does not cover other

sites, including nasolacrimal, salivary and thyroid, or

other tumour types such as lymphoma, sarcoma or

neuroendocrine tumours.

Nasopharyngeal cancer

Nasopharyngeal cancer (Fig. 1) arises from the epithelium

of the nasopharynx. It is rare in the United States but is

more common in some Asian countries such as China (3).

The Ebstein Barr virus is a likely aetiology for most of these

malignancies. Ebstein Barr virus infects benign epithelial

cells and can cause their transformation into nasopharyn-

geal cancer (4–6).

Masses arising in the nasopharynx are often visible

through a nasopharyngoscope, most commonly in the fossa

of Rosemuller. T1 tumours are confined to the nasophar-

ynx. T2a tumours extend to the soft tissue of the

oropharynx and/or nasal fossa without parapharyngeal

extension, whereas T2b tumours involve the soft tissue of

the oropharynx and/or nasal fossa with parapharyngeal

extension. When a nasopharyngeal tumour invades bony

structures and/or paranasal sinuses it is a T3 tumour.

Once the tumour extends intracranially, and/or involves

cranial nerves, infratemporal fossa, hypopharynx or orbit it

is classified as T4 (7).

2/2007 n IMAGING DECISIONS

Because nasopharyngeal tumours metastasize very read-

ily, the most common clinical presentation of nasopharyn-

geal cancer, observed in 80% of the patients is a palpable

neck mass. Often this tumour involves neck nodes bilat-

erally and spreads to the jugulodiagastric, and the upper

and lower anterior cervical lymph node chain.

PET/CT is useful in nasopharyngeal cancer because it is

able to assess questionable lymph nodes as well as help

define the extent of the disease. Detection of an unknown

primary site may be limited by physiological uptake in the

lymphoid tissue of the Waldeyer’s ring, however when

positive, PET/CT may allow more effective directed

biopsy, thereby permitting more focused treatment and

reduced morbidity. Combined PET/CT has facilitated

directed biopsies and allowed more accurate sampling of

tissue that is highly suspicious for tumour. In addition,

follow-up PET/CT that demonstrates diminishing FDG

uptake suggests a favourable response to treatment and

thus may obviate biopsy.

Several limitations have been reported in PET/CT

evaluating nasopharyngeal cancer. Increased FDG uptake

has been reported in the nasopharynx after surgical

injection of teflon caused by a teflon granuloma and

leading to misinterpretation of tumour recurrence (8).

A muscle frequently demonstrating asymmetric FDG

uptake (and therefore misinterpreted as metastatic disease)

is the inferior obliquus capitus muscle. Uptake within this

muscle may appear focal on coronal images but its linear

nature is evidenced when the uptake is viewed in an axial

plane (9) (Fig. 2).

There are several lymphatic structures in the naso-

pharynx including the adenoid tonsils. Physiological

FDG uptake can be seen in these lymphatic structures

due at least in part to accumulation of FDG within

the macrophages and lymphocytes. The interpretation

is straightforward physiological activity in most cases,

especially when there is symmetric uptake. However,

malignancy or hyperplasia may have a similar appear-

j Fig. 1. 18F-fluorodeoxyglucose positron emission tomography-computerized tomography images of a 75-year-old malewith a nasopharyngeal mass. There is a hypermetabolic mass in the right posterior nasopharynx extending inferiorly andlaterally which was biopsy proven to be invasive moderately-to-poorly differentiated keratinizing squamous cell carcinoma.

1 2 n P E T - C T I N T H E M A N A G E M E N T O F H E A D A N D N E C K C A N C E R

IMAGING DECISIONS n 2/2007

ance. Uptake in Waldeyer’s ring will often be asym-

metric even from benign conditions such as infection

or inflammation. Malignancy will usually, but not

always, manifest as asymmetric FDG uptake as well,

with or without significant anatomic abnormality

(Fig. 3).

Oropharygeal cancer

The oral cavity is a large area within the head and neck

that extends from the skin-vermillion junctions of the

anterior lips to the junction of the hard and soft palates

above and to the line of the circumvallate papillae in the

posterior tongue. Oropharyngeal cancer (Fig. 4) can orig-

inate in any of the following areas: the lip, anterior

two-thirds of the tongue, buccal mucosa, floor of mouth,

retromolar trigone, upper and lower gingival mucosa, as

well as the hard palate. A primary neoplasm’s main route

of spread is through the lymph node drainage into the first

station nodes which consist of buccinator, jugulodiagastric,

submandibular and submental lymph nodes (levels I and

II). Tumours close to the midline often metastasize

j Fig. 2. Positron emission tomography/computerized tomography images of focal 18F-fluorodeoxyglucose uptake in the leftobliquus capitus muscle. On coronal images the pattern of uptake appears focal, but on the axial and sagittal planes, a linearpattern is demonstrated consistent with the physiological muscle uptake.

P E T - C T I N T H E M A N A G E M E N T O F H E A D A N D N E C K C A N C E R n 1 3


bilaterally. In more advanced oropharyngeal cancer, meta-

static lesions can spread to the second station nodes

including the parotid, jugular as well as the upper and

lower posterior cervical nodes ( levels IV and V ).

Primary oropharyngeal neoplasms less than or equal to

2 cm are classified as T1 tumours. When the primary

tumour is greater than 2 cm but less than 4 cm, it is a T2

lesion. Once an oropharyngeal neoplasm enlarges above

4 cm, it is categorized as a T3 tumour. T4 tumours are

classified based on local invasiveness: T4a tumours invade

the larynx, deep/extrinsic tongue muscles, medial ptery-

goid, hard palate or mandible, while T4b tumours are

more extensive and invade the lateral pterygoid muscle,

pterygoid plates, lateral nasopharynx, skull base or encase

the carotid vessels (7).

Clinically, oropharyngeal cancer manifests as an

ulcerative surface lesion. The patient is usually asymp-

tomatic in the early stages but often experiences pain in

advanced stages. Common early symptoms include a

mass, bleeding, foul odour, ill-fitting dentures or loose

teeth. In more advanced stages patients complain of

otalgia, trismus or a neck mass. Fortunately, because the

j Fig. 3. Asymmetric palatine tonsil uptake in a patient with an unknown primary tumour. Focal 18F-fluorodeoxyglucose(FDG) uptake is seen in a right-level IIA lymph node corresponding to a biopsy proven poorly differentiated squamous cellcarcinoma. Although the asymmetric FDG palatine tonsil uptake (R>L) is within physiological limits (max. SUV 4.9 on right,4.4 on left), the right tonsil is suspicious for being the site of the primary malignancy. In this patient the right tonsil turned out tobe the primary tumour.



oropharynx is easily visualized, tumours are often found

at early stages incidentally by the patient, dentist or

physician.

PET/CT has become more useful in oropharyngeal

cancer then conventional imaging modalities. Research

studies have shown FDG PET to be superior to CT/MRI

for detecting palpably occult neck metastasis of oral

squamous cell cancer. In T1 to T3 tumours, a negative

FDG PET study reduces the probability of occult neck

metastasis to less than 15%. As a result, PET is indicated

for evaluation of these subpopulations of oropharyngeal

cancer (10). Another study has shown that using PET in

combination with lymphoscintigraphy and sentinal node

biopsy considerably reduced the number of extensive neck

dissections in occult oropharyngeal squamous cell cancer

as compared with CT without locoregional hazard (11).

The overlap between tumour and physiological FDG

uptake may confound interpretation of oropharyngeal

cancer on PET/CT. Asymmetry is not always a reliable

indicator of disease, especially in post-surgical patients.

Although combined PET/CT has undoubtedly facilitated

the differentiation of the physiological from the pathologic

processes, there are new artefacts unique to this modality.

For example, the parotid and submandibular glands

normally demonstrate mild-to-moderate symmetric phys-

iological FDG uptake, however in some cases they may

demonstrate little or no uptake. Asymmetric uptake can be

seen in patients who have undergone surgical removal of

one of the glands or in patients with primary or metastatic

lesions to the glands.

Benign and malignant parotid tumours cannot be

distinguished with PET/CT alone because of high false-

positive rates (Figs 5 and 6). FDG-avid tumours include

Warthin’s and pleomorphic adenoma. Also there are

several salivary gland malignancies that have little or no

FDG avidity; therefore, lack of FDG uptake within the

j Fig. 4. 18F-fluorodeoxyglucose positron emission tomography-computerized tomography images of a 60-year-old femalewho has a hypermetabolic mass located in the base of the tongue adjacent to the right side of the hyoid bone that extendsinferiorly to involve the epiglottis and right aryepiglottic fold. This mass was later proven to be squamous cell carcinoma.Furthermore there is a hypermetabolic left-level IIA lymph node that is consistent with the metastatic disease.



salivary gland mass does not exclude malignancy.

Although FDG PET is not accurate in diagnosing malig-

nancy in salivary glands, it is useful in staging once salivary

gland malignancy is diagnosed. In a series of 31 patients,

Otsuka et al. (12) found that PET imaging changed the

management in 35%, primarily by identifying unsuspected

metastases.

Malignancy can occasionally cause bilateral FDG

uptake in the parotid or submandibular glands or in

intraparotid lymph nodes, mimicking a physiological

process. Non-neoplastic cases of increased FDG uptake

include infection causes and granulomatous disorders such

as sarcoidosis. It is necessary to consider all available

clinical information including prior oncological and

surgical history.

Hypopharygeal cancer

The hypopharynx is the region between the oropharynx

(at the level of the hyoid bone) and the oesophageal inlet

j Fig. 5. Malignant L parotid mass: the hypermetabolic left parotid mass has eroded into the skin (arrow). The mass wasbiopsied, which confirmed moderately differentiated SCCA with papillary architectural features.



(at the lower end of the cricoid cartilage). This structure

does not include the larynx but does involve epiglottis and

vallecula. Subsites within the hypopharynx include the

piriform sinus and the lateral and posterior walls of the

post-cricoid pharynx. Almost all hypopharyngeal malig-

nancies (Fig. 7) arise from the epithelium of the mucosa

(i.e. squamous cell cancers) (13). Hypopharyngeal malig-

nant lesions enlarge and invade local structures and invade

the lymphatics to spread to the regional lymph nodes as

well as the vascular channels to metastasize to other

organs.

Hypopharyngeal malignancies that are limited to one

subsite and are less than or equal to 2 cm are classified as

T1 tumours. Tumours greater than 2 cm but less than

4 cm without fixation or involve more than one subsite are

staged as T2. Hypopharyngeal tumours may invade

superiorly into the base of the tongue or inferiorly into

the larynx. T3 tumours are larger than 4 cm or have

hemilarynx fixation. A tumour that invades thyroid/

cricoid cartilage, hyoid bone, thyroid gland, oesophagus

or central compartment soft tissue is classified as a T4a

tumour. T4b tumours invade the prevertebral fascia,

j Fig. 6. Left intraparotid focus: 18F-fluorodeoxyglucose positron emission tomography imaging cannot distinguish betweenbenign and malignant masses in salivary glands. This hypermetabolic left intraparotid nodule was later proven to be a benignWarthin’s tumour with no evidence of carcinoma.



encase the carotid artery or involve the mediastinal

structures (7).

Hypopharyngeal tumours metastasize readily. In

approximately 50% of the hypopharyngeal cancer

cases, a cervical lymph node metastasis is the pre-

senting symptom (14). Distant metastatic disease devel-

ops in approximately 25% of the patients. The lungs,

liver and bones are the primary structures affected

(Fig. 8a,b).

Although combined PET/CT has undoubtedly

facilitated the differentiation of the physiological from

the pathologic processes, there are new artefacts unique

to this modality that limit the interpretation in the

assessment of hypopharyngeal cancer. Muscles often

demonstrate more focal uptake patterns, and combined

PET/CT frequently depicts FDG uptake localized to

the myotendinous junction in the posterior larynx.

Therefore, areas of FDG uptake can be difficult to

distinguish form abnormal lymph nodes in hypopharyn-

geal cancer.

Several muscles in the hypopharynx demonstrate sym-

metric physiological FDG uptake; when asymmetric,

uptake in these locations may mimic focal areas of

malignancies. Intense asymmetric FDG uptake can also

be seen within the sternocledomastoid muscle and can be

mistaken for an enlarged lymph node. Often, inspection of

coronal or sagittal reconstruction images will facilitate

characterization of muscle uptake by revealing the linear

extent on one or more images.

Glottic cancer

Laryngeal malignancies (Fig. 9) tend to involve the true

vocal cords (TVC) as well as at the anterior commissure,

the point where the TVC come together and at the pos-

terior commissure where the TVC attach to the arytenoids.

j Fig. 7. 18F-fluorodeoxyglucose positron emission tomography-computerized tomography (PET-CT) images of a 59-year-old female who presented with dysphagia and hoarseness. PET/CT images demonstrate a hypermetabolic mass in the leftside of the epiglottis and left aryepiglottic fold that extends to the left side of the hyoid bone. A biopsy of this mass revealedmoderately differentiated invasive squamous cell carcinoma.



The most common type of glottic tumour is a squamous

cell cancer. It often arises in the anterior portion of the

glottis usually on the free margin of the VC. The cancer

can then spread horizontally along the cord towards the

anterior commissure.

Glottic cancers often present during a very earlier

stage of disease because small VC lesions can result in

significant hoarseness and change in voice. These

symptoms are frequently the initial presenting symp-

tom of glottic carcinoma. However, if the glottic

cancer is large it may cause haemoptysis and airway

compromise.

Although there is no clear definition of a ‘large’ or

‘small’ tumour the following classification scheme helps

to define early (T1 and T2) and more advanced (T3

and T4) cancers. T1 tumours involve only the VC

which has normal mobility. T1a tumours invade only

one VC whereas T1b tumours invade both VC. T2

tumours extend upwards into the supraglottis and/or

inferiorly to the subglottis and may impair VC mobility.

On the other hand T3 tumours are localized within the

larynx with VC fixation. The most extensive laryngeal

tumours are the T4 tumours which invade through

tissues beyond the larynx. A T4a tumour invades the

thyroid cartilage and/or tissues beyond the larynx. T4b

tumours are more extensive and invade the prevertebral

space, encase carotid arteries or invade mediastinal

structures (7).

FDG PET can be used to identify primary and

recurrent early (T1 and T2) laryngeal cancer. In a group

of patients with laryngeal cancer, PET depicted 92% (11

of 12) of the laryngeal lesions. One of the lesions was not

detected and had a standard uptake value (SUV) of

2.3, which did not meet the criteria for malignancy.

j Fig. 8. 18F-fluorodeoxyglucose positron emission tomography-computerized tomography images of a patient withsquamous cell carcinoma of the right pyriform sinus (stage IVA T1N2B) 3 months following completion of chemoradiationtherapy. Part a (columns 1 & 2): Now the patient is free of disease in the neck but has multiple right axillary nodes and a liverhypermetabolic focus virtually diagnostic for metastatic disease. Part b (columns 3 & 4): Lung windows show ahypermetabolic nodule in the left upper lobe with lower uptake in a subcarinal lymph node (best seen on soft tissue windows,column 3), also consistent with metastatic disease.



Conversely, nine patients from the same group under-

went CT imaging which did not detect seven of the nine

leisons. Six of the seven were T1 tumours (15). This

study suggests that primary or recurrent early-stage

laryngeal cancers are detected with a greater sensitivity

then CT alone. Also PET imaging may aid in biopsy

guidance when the initial tissue sample is negative.

PET also appears to be useful in assessing the larynx for

residual or recurrent disease after therapy in early-stage

tumours. One study found the sensitivity and specificity of

PET for detection of residual disease to be 90% and 85%,

respectively. For example, in a 67-year-old patient with

squamous cell carcinoma (SCCA) of the base of tongue

(BOT) who underwent chemoradiation treatment, post-

treatment PET/CT scan showed new FDG uptake in the

VC and sclerosis of the left thyroid cartilage. This was

interpreted and later confirmed by laryngoscopy as radi-

ation induced inflammation. A follow-up PET/CT scan

showed increased FDG uptake in the thyroid cartilage, a

finding that represents recurrent neoplasm in the proximity

to the VC (16).

The rational of PET imaging after treatment is that a

decrease in metabolic activity after treatment should

indicate a good response. Such findings are dependent

on the time between treatment and imaging. Imaging

performed 1 month after treatment may be unreliable in

terms of evaluating the tumour response (17). However,

imaging performed 3–4 months after treatment can

provide prognostic information.

Although useful for diagnosis and staging of laryngeal

cancer, there are limitations to PET/CT evaluation of

laryngeal cancer. Most muscles in the neck can display

both a symmetric and asymmetric FDG uptake both

physiologically and after muscular activity. As a result,

close inspection of images obtained in all three orthogonal

planes is essential to avoid misdiagnosis. Although the use

of soft collars and administration of benzodiazapines

minimize muscle uptake, these techniques are often

inconvenient for the patient and may not be completely

effective.

A very common problem is speaking during the uptake

phase of a PET scan. Talking during the FDG uptake

j Fig. 9. 18F-fluorodeoxyglucose (FDG) positron emission tomography-computerized tomography(PET-CT) images of a 91-year-old male who presented with hoarseness. The PET/CT scan demonstrates focal increased FDG uptake in the left truevocal cord which extends to the anterior commissure. The left true vocal cord was biopsied and found to be squamous cellcarcinoma. The focal FDG uptake just medial of the left mandibular ramus (on the coronal images) is consistent withphysiological FDG uptake in the lateral pterygoid muscle.



j Fig. 10. 18F-fluorodeoxyglucose positron emission tomography-computerized tomography images of an 82-year-old malewith squamous cell carcinoma of the floor of the mouth, studied 2 months following completion of radiation therapy. The mildhypermetabolic activity in the larynx is symmetrically localized to the arytenoid and posterior pharyngeal muscles. This isnormal physiological activity seen with speech.



j Fig. 11. 18F-fluorodeoxyglucose (FDG) positron emission tomography-computerized tomography images of a 50-year-oldmale with biopsy proven T3N2 invasive moderately differentiated squamous cell carcinoma of the right true vocal cord.Although there is focal FDG uptake in the left level III lymph nodes (coronal image) consistent with metastatic disease, theintense symmetrical FDG uptake just posterior to the cricoid cartilage represents normal physiological muscle activityassociated with speech and should not be mistaken for metastatic spread.



phase can result in increased uptake in the cricopharyng-

eus muscle and coughing can produce intense FDG activity

in the pharyngeal constrictor muscles and VC as well

(Fig. 10). Focal intense activity in these muscles can

interfere with interpretation of PET scans of patients with

laryngeal malignancy (Fig. 11).

Post-surgical changes can also lead to pitfalls in the

interpretation of PET scans. Thus, it is essential to have

knowledge of prior surgery and of any surgical complica-

tions for proper interpretation of PET in the larynx.

Several cases of asymmetric VC uptake following injury

to the recurrent laryngeal nerve have been reported.

Asymmetric FDG uptake within a single VC can mimic

malignancy on PET (Fig. 12).

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j Fig. 12. 18F-fluorodeoxyglucose positron emission tomography images of a patient with T2N0 carcinoma of the left truevocal cord at 3 months following completion of curative radiotherapy. The focal area of increased uptake in the rightperilaryngeal region is because of uptake in the normal right vocal cord. The left vocal cord is paralysed. This phenomenoncan also be seen with recurrent laryngeal nerve injury and can be mistaken for malignant involvement of the normallyfunctioning vocal cord.



positron emission tomography-computerized tomography in the management of head and neck cancer

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