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Positron Emission Tomography in the Evaluation of Synchronous Lung Lesions in Patients With Untreated Head and Neck Cancer
Mark K. Wax, MD;
Larry L. Myers, MD;
Edward C. Gabalski, MD;
Syed Husain, MD;
Jayakumari M. Gona, MD;
Hani Nabi, MD
Arch Otolaryngol Head Neck Surg. 2002;128:703-707.
ABSTRACT
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Background Positron emission tomography (PET) with the glucose analogue fludeoxyglucose
F 18 uses the increased glucose uptake that is observed in neoplastic cells.
It can differentiate between benign and malignant pulmonary lesions in patients
with lung tumors. Applications of PET in extracranial head and neck neoplasms
have included evaluating patients with unknown primary lesions, detecting
primary and recurrent head and neck tumors, monitoring response to radiotherapy,
and evaluating the N0 neck in oral cavity carcinomas. Its role in determining
the presence of synchronous lung lesions has not been defined.
Patients and Methods A retrospective review of 115 patients who underwent PET between October
1994 and October 1996 was performed to evaluate extracranial head and neck
neoplasms. Fifty-nine (51%) previously untreated patients with squamous cell
carcinoma of the upper aerodigestive tract were analyzed.
Results Fifteen patients (25%) had PET scans that were positive for synchronous
lung lesions. Five patients had a disease process that did not warrant further
investigation; they did not have pathological confirmation of their lung lesions.
Of these, 3 died of disease within 2 months of the diagnosis of primary head
and neck squamous cell carcinoma, 1 was unavailable for follow-up, and 1 had
lung lesions that were considered metastatic and no pathological confirmation
of lung lesions was obtained. The remaining 10 patients with positive PET
scan findings were investigated further: 8 patients had biopsy-confirmed lung
lesions; 5 patients had positive findings on chest x-ray films; 8 had positive
findings on computed tomographic scans; and 3 had positive findings on bronchoscopy.
The results of 2 PET scans were false-positive. The PET scans were important
in altering treatment in 3 patients; of these, 3 had negative findings on
chest x-ray films, 2 had positive findings on computed tomographic scans,
and 1 had positive findings on bronchoscopy.
Conclusions The overall sensitivity, positive predictive value, and accuracy of
PET were 100%, 80%, and 80%, respectively. The overall accuracy of radiography
of the chest, computed tomography of the chest, and bronchoscopy was 70%,
90%, and 50%, respectively. The accuracy of PET over bronchoscopy was statistically
significant (P<.05). PET appears to be a promising
imaging modality for the detection of synchronous lung lesions in patients
with negative findings on chest x-ray films.
INTRODUCTION
BILROTH, IN 1889, described a patient with multiple primary lesions
in the upper aerodigestive tract (UADT).1 Since
then, many reports have described the association between squamous cell carcinoma
(SCCa) of the UADT and a second malignant neoplasm in the UADT. Tumors found
simultaneously or within 6 months from the diagnosis of a primary index tumor
are classified as synchronous. A malignancy found later than 6 months is considered
a metachronous tumor.1-9
The incidence of these synchronous lesions in patients with tumors of the
UADT is between 2% and 16%.10-13
Advances in surgery, radiation therapy, and chemotherapy have improved the
ability to control local disease, yet less fewer than 50% of patients are
alive 5 years after diagnosis.2 The frequent
development of a second primary tumor is one reason for the lack of improvement
in the overall survival.5 Half of the deaths
are the result of the initially diagnosed cancer, while the other half are
caused by a second primary cancer or other comorbid conditions.2
Detection of the second primary tumor is crucial for both prognosis
and management.1 Routine radiography of the
chest, panedoscopy, bronchial washings, and computed tomography of the chest
are investigations that attempt to identify synchronous primary tumors. Controversy
exists regarding the efficacy of these tests.
Positron emission tomography (PET), using fludeoxyglucose (FDG) F 18,
is a functional imaging modality that has been applied to the evaluation of
extracranial head and neck neoplasms. It has been used to evaluate patients
with an unknown primary lesion, to monitor the response to therapy, and to
detect recurrent head and neck tumors.14 Recent
experience has demonstrated the utility of PET in the evaluation and treatment
of patients with cervical metastatic disease. The role of PET in the evaluation
of synchronous lung lesions in patients with head and neck cancer has not
been well defined. The purpose of this study was to assess the clinical effectiveness
of PET in the evaluation of lung lesions in patients with SCCa of the UADT.
Secondarily, we wished to correlate the PET findings with those of pathological
examination of the lung lesion.
PATIENTS AND METHODS
Between October 1994 and October 1996, 115 consecutive patients with
a clinical diagnosis of a head and neck malignancy underwent PET scans at
the Veterans Affairs Western New York Health System (VAWNYHCS), Buffalo, NY,
as part of an ongoing study to assess the utility of PET with FDG F 18 in
the evaluation of head and neck neoplasms. This larger study was approved
by the institutional review board of VAWNYHCS. Fifty-six patients (49%) with
recurrent SCCa or head and neck tumors, such as salivary gland neoplasm, malignant
melanoma, thyroid neoplasm, nasopharyngeal carcinoma, metastatic adenocarcinoma,
neurogenic neoplasm, and lymphoma, were excluded. Fifty-nine patients (51%)
had biopsy-proved, previously untreated primary SCCa of the UADT.
All patients underwent PET scans, which were performed in the following
manner: After informed consent was obtained, the patients were positioned
in the machine (ECAT 951/31R; Siemens CTI, Knoxville, Tenn). A transmission
scan of the body encompassing the head, neck, and thorax was obtained in each
patient. Approximately 10 mCi (370 Mbq) of FDG F 18 was intravenously administered
to each patient. After a waiting period of approximately 30 minutes for FDG
F 18 incorporation into presumed lesions, total body imaging was obtained
in the same planes in which transmission data were acquired. Approximately
35 million coincident events were registered, and the images were reconstructed
using a Hann filter with a cutoff frequency of 0.3 cycle per pixel. The technical
quality of the resulting images was high. Coronal, axial, and sagittal sections
were reviewed (Figure 1 and Figure 2). The total average time for the
entire PET procedure was approximately 1 hour. No untoward cardiac or respiratory
events occurred during PET scanning.
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Figure 1. A, Positron emission tomographic
scan demonstrating the presence of primary upper aerodigestive tract lesion
as well as lung lesion (arrows). B, Corresponding computed tomographic scan
of the chest does not demonstrate the lung lesion.
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Figure 2. A, Positron emission tomographic
scan demonstrating the presence of primary upper aerodigestive tract lesion
as well as lung lesion (arrows). B, Corresponding computed tomographic scan
of the chest shows the lung lesion.
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All patients underwent radiography of the chest. Sixteen patients (30%)
underwent computed tomography (CT) of the chest. The decision to obtain a
CT scan of the chest was at the discretion of the attending otolaryngologist
at the VAWNYHCS. All patients underwent a complete head and neck examination
in the otolaryngology clinic at the VAWNYHCS. Panendoscopy was performed after
the chest radiographic, chest CT, and PET scans were obtained. After disease
staging, the patients were presented at a joint head and neck tumor conference.
The PET findings were correlated with those of chest radiograpy, chest CT,
bronchoscopy, and lung biopsy or bronchial washings.
For statistical analysis, the sensitivity, specificity, positive predictive
value, negative predictive value, and accuracy of the PET and CT scans were
calculated as follows: sensitivity, number of true-positive results/(number
of true-positive results + number of false-negative results); specificity,
true-negative results/(true-negative results + false-positive results); positive
predictive value, true-positive results/(true-positive results + false-positive
results); negative predictive value, true-negative results/(true-negative
results + false-negative results); and accuracy (validity), (true-positive
results + true-negative results)/total.
RESULTS
Of the 59 patients analyzed, 15 (25%) had PET scans that were positive
for synchronous lung lesions. All patients with synchronous lung lesions were
men (mean age, 65 years; age range, 44-78 years). Five patients did not have
further workup of their PET findings: 3 died of disease within 2 months of
diagnosis of primary head and neck SCCa, 1 was unavailable for follow-up,
and 1 had lung lesions that were considered metastasic and no pathological
confirmation of lung lesions was obtained.
Ten (19%) of 54 patients with previously untreated primary SCCa of the
UADT had positive results on PET scans (both UADT and lung lesions). Pathological
examination of the lung tissue was performed in 8 patients (Table 1). Eight of these lung lesions were malignant: 5 SCCa, 1
adenocarcinoma, 1 small cell carcinoma, and 1 non–small cell carcinoma.
Eight of the 10 patients with positive results on PET scans underwent chest
CT. Thirty-one patients (57%) underwent bronchoscopy (24 flexible, 7 rigid).
All 10 patients with positive results on PET scans underwent bronchoscopy
(all flexible).
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Table 1. Demographics, Examination Results, and Lung Pathological Findings*
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The site, nodal status, and stage of disease of the primary tumor in
relation to the incidence of positive results on PET scans are shown in Table 2. There was no statistical difference
in relation to site, tumor size, presence or absence of cervical metastasis,
or stage of disease and the incidence of lung lesions.
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Table 2. Comparison of the Site and Stages of Primary Tumor in Patients
With Synchronous Lung Lesions Detected by PET* and All Patients Who Had PET
Scans
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For PET scans, the overall sensitivity of PET in detecting lung lesions
(Table 3) was 100%, the positive
predictive value was 80%, and the accuracy (validity) was 80%. The specificity
and negative predictive values were 0, because only patients with positive
PET scans were selected for inclusion. For chest x-ray films, the sensitivity
was 62%, the specificity was 100%, the positive predictive value was 100%,
the negative predictive value was 40%, and the accuracy was 70%. For chest
CT scans, the sensitivity was 87%, the specificity was 100%, the positive
predictive value was 100%, the negative predictive value was 66%, and the
accuracy was 90%. For bronchoscopies, the sensitivity was 38%, the specificity
was 100%, the positive predictive value was 100%, the negative predictive
value was 100%, and the accuracy was 50%. The accuracy of PET over bronchoscopy
was statistically significant (P<.05). PET scans
demonstrating lung lesions were important in altering treatment in 3 of 10
patients. The results of chest x-ray scans were negative in all 3 patients;
those of chest CT scans were positive in 2 of the 3 patients; and those of
bronchoscopies were positive in only 1 of the 3 patients.
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Table 3. Comparison of Sensitivity, Specificity, Positive and Negative
Predictive Values, and Accuracy of PET, CXR, CCT, and Bronchoscopy*
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COMMENT
The pathogenesis of multiple primary cancers is not well understood,
but is thought to be related to the effects of carcinogens on an organ system.
In 1953, Slaughter et al15 applied the term field cancerization to the oral mucosa. This concept has
since been applied to other organ systems, including skin, bladder, colon,
breast, and lung.4 The phenomenon of neoplastic
multicentricity may explain the pathogenesis of multiple UADT tumors that
occur in some patients who abuse tobacco and alcohol. These substances may
induce multiple areas of premalignant epithelial changes that in turn may
give rise to multifocal primary neoplasms. An alternative theory is based
on the premise that an initial single transforming event is rare. After this
rare initial transformation, the progeny of the single neoplastic cell spread
through the mucosa and give rise to a geographically distinct but genetically
related tumors.16 Recent genetic investigation
has found that the local clinical phenomenon of field cancerization seems
to involve the expansion and migration of clonally related preneoplastic cells.17
PET with FDG F 18 uses abnormal tissue metabolism to detect neoplasms.
The radioactive glucose analogue FDG is metabolized in normal tissue and neoplastic
tissues in proportion to the rate of tissue glucose metabolism.18
It is phosphorylated to FDG-6 phosphate by the intracellular enzyme hexokinase.
Fludeoxyglucose 6 phosphate does not serve as a substrate for further metabolisms,
nor does it diffuse back across cell membranes to any significant degree.
Fludeoxyglucose is metabolically trapped in the intracellular space, more
so in tumors than in normal tissues,19 and
can be used to identify tumors based on accelerated glycolytic rates using
PET. Because of the higher glycolytic rate of many neoplasms compared with
normal tissue, PET-FDG imaging is now being applied to many organ systems
for tumor identification.19
Rege et al14 have shown PET to be a useful
diagnostic modality for evaluating patients with unknown primary tumors, monitoring
response to therapy, and detecting recurrent tumors of the head and neck.
They studied 60 patients with biopsy-proved cancers of the head and neck.
Among a group of 4 patients with an unknown primary tumor, PET localized the
tumor in 2 patients, whereas magnetic resonance imaging (MRI) was unable to
localize the tumor in any patient. Among a group of 30 patients with a known
primary tumor, PET detected the tumor in 29 patients, whereas MRI detected
the tumor in only 23. Among 10 patients with biopsy-proved recurrent disease
and 7 patients with no recurrence, the results of PET were positive in 9 of
the 10 patients with recurrence, while those of MRI were positive in 6 of
the 10 patients, and the results of PET were negative for recurrent disease
in 7 of the 7 biopsy-negative patients, while those of MRI were negative for
recurrent disease in 4 of the 7 patients.
Sazon et al20 used PET to evaluate 107
patients with abnormal findings on chest x-ray films. All 82 patients with
lung cancer had positive results on PET scans. Sazon and colleagues observed
false-positive results in 12 of 25 patients with nonmalignant diseases. Sixteen
patients with lung cancer and mediastinal metastasis had positive results
on PET scans in the mediastinum, and 3 of them had negative results on chest
CT scans. Sixteen patients with lung cancer and no mediastinal nodal involvement
had negative results on PET scans. Seven of these patients had positive results
on CT scans. Sazon and colleagues found an overall sensitivity of 100% and
a specificity of 52% in predicting the malignant nature of an abnormality
on a chest x-ray film. They also found an accuracy of 100% in predicting mediastinal
involvement.
Duhaylongsod et al21 studied 100 patients
with indeterminate focal pulmonary abnormalities. They found PET to have a
sensitivity, a specificity, and an accuracy of 97%, 82%, and 92%, respectively,
for detecting lung lesions. Dewan et al22 prospectively
studied 30 patients who presented with indeterminate solitary pulmonary nodules
smaller than 3 cm based on chest x-ray films and chest CT scans. Twenty-seven
of 30 pulmonary nodules were correctly characterized on PET scans. The diagnostic
sensitivity was 95%, specificity 80%, positive predictive value 90%, and negative
predictive value 89%.
Our data are consistent with these studies. The overall sensitivity
of PET in detecting lung lesions in our study was 100%, the positive predictive
value was 80%, and the accuracy (validity) was 80%. There was selection bias
inherent in our study in that only patients with positive results on PET scans
were included, which precluded us from detecting any false negative results.
Previous studies1, 13 have
reported the overall incidence of synchronous lesions in the entire UADT to
be between 2% and 16%. Our study examined the incidence of synchronous lung
lesions in patients with primary SCCa of the UADT. The incidence of synchronous,
pathologically proved lung lesions detected by PET in our study was 15% (8
of 54 patients). These figures are higher than those of other investigators
who reported on the incidence of second lung lesions. Leipzig et al13 found a 3.3% incidence of a second primary lung lesion;
Maisel and Vermeersch,3 a 3.8% incidence; McGuirt,23 a 3.7% incidence; and Atabek et al,11
a 5.4% incidence. The reason the incidence of synchronous lung lesions in
patients with head and neck cancer in our study differs from that in other
studies is unclear. This discrepancy may be because our institution is a tertiary
Veterans Affairs referral center and patients are often referred late in their
disease process.
Oncological management was changed based on the PET findings in 3 of
10 patients. Patient 3 had positive results on PET scan and negative results
on CT scan of the chest. The findings of radiography of the chest were also
negative. He underwent treatment for his head and neck primary tumor and a
second PET scan 6 months later. The results of the latter were again positive,
and a second CT scan of the chest was performed. A lesion was now apparent
on the CT scan. This correlated with the findings on the PET scan. Patient
3 underwent resection of an early-stage pulmonary tumor. Patient 4 had negative
findings on chest x-ray films and underwent CT of his chest on the basis of
the PET scan findings. A lesion that correlated with the PET scan was found
on the CT scan of the chest, and the patient underwent treatment of that lesion,
followed by treatment of the primary tumor in his head and neck. Patient 9
was found to have multiple metastatic nodules throughout the lungs and liver
on his PET scan. The surgical treatment of the primary tumor in his head and
neck was canceled, and he underwent palliative chemotherapy for metastatic
lung disease and a synchronous primary tumor.
There were 2 PET scans (patients 2 and 6) with positive results in our
study. The PET scan of patient 2 revealed a lesion in his right lung. After
treatment of the tumor in his head and neck, he underwent a CT scan of his
chest, the results of which were negative. A follow-up CT scan of his chest
did not reveal any lesion. Patient 2 is alive without evidence of disease
after 18 months of follow-up. The PET scan of patient 6 showed a left upper
lobe lesion. The results of a follow-up scan of the chest were negative. The
patient was followed up clinically and has had no evidence of disease after
10 months of follow-up. The treatment of patients with false-positive results
on lung PET scans is problematic. Follow-up evaluation detected a primary
tumor in the lung in 1 of our 3 patients with false-positive results, while
the other 2 patients remained free of disease. It is possible that their follow-up
was not long enough. Currently, patients with positive results on PET scans
and negative results on CT scans of the chest are followed up with serial
CT scans: the first is performed at 3 months; the rest are performed at 6-month
intervals. A larger number of patients will be required before we can evaluate
or comment on the utility of serial follow-up CT scans.
In 1979, Weaver et al24 recognized that
early diagnosis of lung cancer is difficult, with fewer than 30% of proved
lung cancers identified on bronchoscopy. Some authors4-7
have shown that the presence of synchronous primary tumors or metastasis in
the lung decreases patient survival. Others25-27
have shown that with the proper patient selection, pulmonary resection of
lung metastasis is a potentially curable measure. PET appears to show promise
in identifying synchronous lung lesions, which may have an impact on the choice
of treatment in this patient population.
Our study demonstrated that of the 8 patients with carcinoma of the
lung that correlated with the findings of pathological examination of tissue,
4 had normal findings on chest x-ray films. Three of these 4 patients had
CT scans of the chest that confirmed the PET scan findings. One patient's
lesion did not show up until a CT scan was obtained 6 months later. At our
institution, we routinely order CT scans of the chest in cases involving advanced-stage
neck disease. Three of the 4 patients who had positive findings on PET scan
and normal findings on chest x-ray films had N0 neck disease. Consequently,
a CT scan of the chest would not have been part of the routine in these patients.
The fourth patient had N1 neck disease, and in that type of case it is arguable
whether a CT scan of the chest should be part of the routine. We are currently
evaluating the role of routine CT scanning of the chest in patients with head
and neck cancer.
CONCLUSIONS
PET is a dynamic imaging modality that is increasingly being applied
to the investigation of extracranial head and neck neoplasms. We investigated
the ability of PET to determine the presence or absence of synchronous lung
lesions in patients with UADT SCCa.
Fifteen patients had PET scans that were positive for primary UADT and
synchronous lung lesions. In 5 of these patients, the PET findings added little
to their overall prognosis or treatment course. Of the remaining 10 patients,
3 had their treatment changed because of the findings on the PET scans.
PET appears to be a promising imaging modality for the investigation
and detection of second primary lesions in the lung.
AUTHOR INFORMATION
Accepted for publication November 19, 2001.
This study was presented at the Fifth International Conference on Head
and Neck Cancer, San Francisco, Calif, July 31, 2000.
Corresponding author and reprints: Mark K. Wax, MD, Department of
Otolaryngology–Head and Neck Surgery, Oregon Health Sciences University,
3181 SW Sam Jackson Park Rd, PV-01, Portland, OR 97201 (e-mail: waxm{at}ohsu.edu).
From the Department of Otolaryngology–Head and Neck Surgery,
Oregon Health Sciences University, Portland (Dr Wax); the Department of Otolaryngology,
University of Michigan, Ann Arbor (Dr Myers), Long Island Surgical Specialists,
Lake Success, NY (Dr Gabalski); the Department of Nuclear Medicine, State
University of New York at Buffalo (Drs Husain, Gona, and Nabi); and the Center
for Positron Emission Tomography, Veterans Affairs Medical Center at Buffalo
(Drs Husain, Gona, and Nabi).
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