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Jornal de Pneumologia

Print version ISSN 0102-3586On-line version ISSN 1678-4642

J. Pneumologia vol.29 no.3 São Paulo May/June 2003

https://doi.org/10.1590/S0102-35862003000300009 

UPDATE

 

The use of positron emission tomography in the evaluation of pleuropulmonary cancer*

 

Marcelo Jorge Jacó RochaI (te sbpt); Mário Terra FilhoII

IGraduate student of Pneumology. Specialist accredited by the Sociedade Brasileira de Pneumologia e Tisiologia (Brazilian Society of Pneumology and Phthisiology).
IIAssociate Professor of Pneumology.

Correspondence

 

 


ABSTRACT

Focal lung abnormalities are frequent X-ray findings and can have an infectious, inflammatory or neoplastic etiology. In the evaluation of such radiological alterations, it is important to make a distinction between benign and malignant (lung cancer) diseases. Computed tomography characterizes 25% of the lung nodules as indeterminate, requiring thoracotomy with biopsy for diagnostic clarification. FDG-PET has a 94% sensitivity and a 86% specificity in the differentiation of benign and malignant parenchymal lesions, thus reducing by 15% the need for surgery to make a diagnosis. It is useful in the staging of non-small-cell lung carcinoma, having a 91% sensitivity and a 86% specificity in the evaluation of mediastinal lymph nodes. It also seems to be useful in the analysis of liver, adrenal and bone metastases. In this review, the several indications for PET in pulmonary neoplasias are discussed, in addition to details about the examination technique.

Key words: Pulmonary nodules. Staging. Non-small-cell lung cancer. Positron emission tomography.


 

 

Acronyms and abbreviations used in this work
PET – Positron emission tomography
NSCPC – Non-small-cell pulmonary carcinoma
SCC – Squamous cell carcinoma
FDG – 2-D-glucose labeled with 18fluor
SUV – Standardized uptake value
SUR – Standardized uptake rate
SPECT – Sole-photon emission computed tomography
SPN – Solitary pulmonary nodule
ATS – American Thoracic Society
CT – Computed tomography
NPV – Negative predictive value
PPV – Positive predictive value
NMR – Nuclear magnetic resonance

 

Introduction

Lung cancer is a frequently diagnosed disease and the neoplasm causing the highest mortality in the whole world, being therefore considered a public health problem worldwide. The main risk factor for its occurrence is smoking, along with environmental pollutants, asbestos, pulmonary fibrosis, etc. About 175,000 new cases are diagnosed yearly in the U.S., with a mortality of about 140,000 yearly.(1) In Brazil, the estimated figures are about 20,000 new cases/year and a mortality of 15,000 yearly, representing, among the malignant tumors, the main cause of death in men and the second most frequent in women.(2) Currently, the non-small-cell pulmonary carcinoma (NSCPC) accounts for 80% of the cases, 40% being adenocarcinomas, 30% squamous cell carcinomas (SCC), and 10% large-cell carcinomas.(1) Surgical resection is the most effective treatment to control the disease, with a five-year survival rate varying between 60% and 80% in the early stages (T1-T2/N0/M0).(3) In more advanced cases, mortality is higher, despite the technological advances and the development of new chemotherapic drugs.

It is important to establish the criteria regarding the operability and resectability of the lesion in the initial evaluation of these patients. To this effect, clinical (for ex., performance status) and laboratory data (computed tomography of the chest and skull, bone scintigraphy, etc.) are used to indicate the best way of treatment: either surgical or clinical (chemotherapy and radiotherapy).(3) In recent years, positron emission tomography (PET) emerged as a major tool in the evaluation of pulmonary nodules and neoplasms, helping in the diagnosis, staging, and post-treatment evaluation of lung tumors.

Positron emission tomography (PET) is a non-invasive test, based on the principle of using biological compounds labeled with elements of high atomic instability which are positron emitters (particles with the same mass as the electron, but with the opposite charge), such as carbon-11, nitrogen-13, oxygen-15, fluorine-18.

Positrons have a very short half-life; the one of oxygen, for example, is 2.07 minutes, which unfortunately limits its use very much. These particles, when combined with electrons, are annihilated, and their mass transformed into energy, resulting in the release of two 511Kev photons (emitted in the opposite direction – 180o), which will be used to locate the positron-electron interaction. The released radiation is detected, computer-processed, and then transformed into images.(4,5)

The adoption of PET as a medical resource was enriched in 1995 by the use of deoxy-2-D-glucose labeled with fluorine-18 (FDG), an element with a half-life of 110 minutes, which made its transport over longer distances possible.

Differently from the other imaging diagnostic methods, PET is the only one capable of performing metabolic images in vivo. The studies evolved rapidly with this technology, and its use in the diagnostic routine of humans started to be strongly considered, mainly in oncology, since alterations of the cell metabolism are frequent in patients with malignant neoplasms.

One of the characteristics of neoplastic cells rich in hexokinase is an increase in the glucose metabolism. FDG is an analog of this substance and behaves as a tracer of its metabolism. After entering the cells, FDG is phosphorylated by hexokinase into FDG-6-phosphate and, in tissues with a low concentration of glucose-6-phosphatase, like the brain, the myocardium, and most of the malignant cells, FDG-6-P does not undergo the next enzyme sequence, accumulating proportionally to the rate of the glucolytic process, emitting positrons and generating the basis for image formation.(5,6) FDG-PET is a test that allows to evaluate the metabolism of glucose in living subjects.(4)

The first tomograph capable of performing PET was built at the Washington University, in 1974.(6) In Brazil, such examinations started to be performed on a regular basis in 1997. Soon after, their first results were presented at congresses(7) and, in 2000, the first paper was published reporting on the use of this technique for the evaluation of pulmonary nodules and granulomatous diseases in 15 patients.(8)

 

Technique

The test is performed while the patient is fasting, with administration of 10 to 20mCi of FDG, and the reading is made after 30 to 60 minutes. The serum glucose levels must be lower than 150mg/dl, in order to prevent competitive inhibition of the FDG uptake by the neoplastic cell.(6) The images, obtained in axial, coronal and sagittal sections, are analyzed qualitatively (visual analysis) or quantitatively through the standardized uptake value or rate (SUV or SUR), calculated as follows:

These two ways of expressing the result are similar. This test is always interpreted in association with the computed tomography of the same region under study. SUV or SUR values over 2.5 can be considered suggestive of malignancy.

There are two types of equipment used to perform the test: dedicated PET, and the hybrid systems (coincidence chamber). The first one has a detector, usually made of bismuth, that captures only photons emitted by positrons annihilated by electrons. In the hybrid types of equipment, there is a double detection system capable of analyzing sole photons (SPECT) and positrons (PET), allowing the same equipment to be used for different tests in nuclear medicine.(9) In Brazil, the hybrid equipment is predominant so far. However, at the Heart Institute (Instituto do Coração - InCor) of the HC-FMUSP, the first dedicated chamber was already installed and has been operating since February 2003.

Pulmonary nodule evaluation

Focal pulmonary abnormalities, including solitary pulmonary nodule, are frequent accidental X-ray findings, and their etiology may be infectious, neoplastic, inflammatory, etc. Malignant lung tumors present themselves as solitary pulmonary nodule (SPN) in approximately 20% to 30% of cases(10), and their resection at this early stage grants a five-year survival rate of up to 80%.(11) Parallel with the need for early diagnosis and treatment of lung cancer, it is important to prevent unnecessary surgeries in cases of benign nodules.

In the evaluation of a SPN, it is important to establish the probability of the lesion being malignant, in order to set the best therapeutic strategy from there.(12) As a rule, the X-ray characteristics and the clinical risk factors are considered, usually attributing a score to each finding. If the probability of malignancy is high (> 0.9), the best conduct would be surgical biopsy with freezing, followed by lobectomy (if the cancer diagnosis is confirmed). In cases with low probability (< 0.12), serial X-rays/tomography would be the better options. However, even with the routine use of computed chest tomography, about 25% of the lung nodules are characterized as indeterminate (0.12-0.9),(13) making a thoracotomy with lung biopsy necessary for diagnostic clarification. It is estimated that about 60% of the resected nodules are benign, showing the need for new complementary exams to better select those patients who are candidates for surgical treatment.(14,15)

Positron emission tomography has a 94% sensitivity and an 86% specificity for nodules over 1cm in size;(15-17) in this subgroup, the use of FDG-PET has reduced the surgical indication by 15%(18) (Figures 1A and 1B; 2A and 2B). As compared to Bayesian analysis, FDG-PET was the best malignancy predictor in the evaluation of a pulmonary nodule (altered PET revealed likelihood ratios of 7.11; normal test: likelihood ratio of 0.06).(19) Compared to CT-guided thin-needle transthoracic biopsy, FDG-PET had a better sensitivity (100% x 81%), but with less specificity (78% x 100%).(20)

 

 

 

 

 

 

 

 

False-positive results may occur in cases of acute inflammation (rheumatoid nodules, post-radiation therapy, etc.), muscle hypermetabolism, granulomatous infections (tuberculosis, histoplasmosis, etc.).(21) Bombarda et al. conducted a study in Brazil, showing that patients with tuberculosis frequently present positive results, even after treatment(7) (Figure 3). In regions with a high incidence of histoplasmosis, FDG-PET showed a sensitivity of 93% and a specificity of only 40% in the solitary pulmonary nodule analysis.(22)

 

 

False-negative results are infrequent and limited to tumors with low cell metabolism, such as the alveolar bronchiole and the carcinoid tumor.(23) Another important factor is the nodule size. Some studies show a decrease in the test sensitivity for nodules smaller than 1cm ( 80 %).(16) Recently, a technique used in dedicated equipment was described, consisting of two uptake measurements at an interval of approximately one hour.(24) This procedure apparently increases the sensitivity and the specificity of the method for the evaluation of pulmonary nodules.

Hyperglicemia may also be, by competitive inhibition, a complicating factor in the interpretation of the test, for serum glucose uptake occurs, reducing the FDG uptake. It is recommended that the patients have a capillary glycemia lower than 150mg/dL.(25)

Thus, the use of FDG-PET in the evaluation of patients with a solitary pulmonary nodule of indeterminate characteristics seems to be well indicated, implying a decrease in the number of unnecessary thoracotomies and a good cost/effectiveness ratio.

 

Staging of non-small-cell pulmonary carcinoma (nscpc)

Surgical treatment is still the most effective way of controlling NSCPC. However, before defining the best way of treating it, it is necessary to establish the extension of the disease first. The staging used in NSCPC is the TNM system. The American Thoracic Society (ATS) recommends an initial clinical evaluation (anamnesis + physical examination) associated with some complementary exams: computed tomography (CT) of the chest (extended up to the beginning of the abdomen for a joint evaluation of the liver and the supra-renal glands), blood count, hepatic and canalicular enzymes. In cases with specific symptoms and/or in the presence of clinical and laboratory signs of advanced disease (for ex., major weight loss, chronic disease anemia, increased hepatic enzymes, etc.), the staging should be completed by head CT and bone scintigraphy.(26)

Status T

Computed tomography of the chest is the examination currently used to evaluate the size of the lesion, its location and extension onto neighboring structures. FDG-PET does not add much to this evaluation. Its main function would be to analyze the degree of FDG uptake by the lesion, thereby providing information regarding the prognosis of the tumor (see below). In addition to that, it can help to differentiate malignant (T4) from benign pleural effusions, and even to identify pleural implants not visualized by other imaging methods.(6)

Status N

Lymph node evaluation is very important and is part of the mediastinum staging. On computed tomography and nuclear magnetic resonance, ganglial affection by neoplasia is diagnosed by the increase in size of the lymph node, which is the reason why the accuracy of mediastinum staging is low (specificity: 65%-85%, and sensitivity 50%-82%).(27) About 17% of the lymph nodes less than 1.0cm in size reveal metastatic disease, and up to 33% of the ganglia over 3.0cm are merely reactional, without any malignancy.(28)

By FDG-PET, the affected ganglia are revealed by the higher uptake of the radioactive drug rather than by their increase in size, allowing earlier diagnoses (Figure 4A and 4B). Regarding mediastinum evaluation of patients with non-small-cell lung carcinoma, the several series of patients studied show a sensitivity around 91% (81%-100%) and a specificity of 86% (82%-91%).(29-32) False-negative results usually correspond to micrometastases. Due to its low specificity, it is recommended that positive cases should be confirmed by histological analysis. In patients without mediastinal FDG uptake and with a primary tumor with a SUV < 2.5, the NPV is 100%, making mediastinoscopy unnecessary as a pre-operative staging method.(33) This strategy could lead to a 12% decrease in performing this procedure.(33)

 

 

 

 

Status M

An extrathoracic metastatic disease is found at diagnosis in up to 30% of the patients with NSCPC.(34) The most frequently affected organs are the liver, the adrenal glands, bones, and the brain. Whole-body FDG-PET allows to make intra- and extrathoracic staging in a single test, with higher accuracy than computed tomography. Occult extrathoracic metastases are detected in up to 14% of the patients selected for surgical treatment, and the conduct is changed in up to 40% of the cases.(32,35)

Adrenal: An adrenal affection occurs in up to 20% of patients with lung cancer.(36) The tests currently used for their evaluation (CT and nuclear magnetic resonance) are not very accurate. Up to 60% of the lesions smaller than 3cm are benign, which makes it often necessary to use percutaneous biopsy to confirm the diagnosis.(36,37) FDG-PET has a 100% sensitivity and an 80% specificity in the detection of adrenal metastases.(38) Thus, in cases of adrenal nodules which are negative on FDG-PET, the suspicion of malignancy can be discarded; in positive cases, histological confirmation is recommended before contraindicating surgical treatment based on a suspicion of disseminated disease.

Liver: The first studies show that FDG-PET is more specific than CT in evaluating liver metastases.(39) However, further studies are needed to establish the real accuracy of this test in detecting liver metastases.

Central nervous system: The occurrence of a brain metastase is usually accompanied by clinical symptoms. However, asymptomatic affections may occur in 2.7% to 16% of cases.(40) FDG-PET can detect occult brain disease (18). Yet, due to the high brain metabolism (and high glucose uptake), the visualizing of focal FDG accumulations may be difficult.

Bones: A bone evaluation is indicated only in cases with symptoms or with increased serum alkaline phosphatase.(26) Bone scintigraphy is the most frequently used examination, but its specificity is low (40% false-negatives).(3,18) The specificity of FDG-PET is considerably higher than the one of bone scintigraphy with technetium, but the available data are still scarce, not allowing further conclusions.

FDG-PET has an 82% sensitivity and a 93% specificity in detecting extrathoracic metastases.(29) A recently published study showed that adding FDG-PET to the conventional preoperative evaluation tests reduced by 51% (p = 0.003) the number of surgeries considered unnecessary (for every five patients, one surgery was prevented).(41) More studies are needed to evaluate if positron emission tomography can be used as the sole test for preoperative staging of lung cancer.

 

Evaluation of the therapeutic response and prognosis

Some studies suggest that FDG-PET has a prognostic value. Tumors with higher uptake (SUV > 7 to 10) present a worse evolution, with a shorter survival time.(42) This scintigraphic technique can also be used to evaluate the response to chemotherapy and radiotherapy. The normalization of FDG uptake after treatment seems to be an indicator of good prognosis (the lower the uptake, the longer the survival). Akhurst et al. recently demonstrated that FDG-PET had a 90% sensitivity and a 67% specificity in detecting residual lung disease after induction by chemotherapy and/or radiotherapy (VPP = 98%, and VPN = 29%).(43) However, its accuracy was lower in the evaluation of residual mediastinum disease, with a sensitivity of 67% and a specificity of 61%. Some studies also show an advantage of FDG-PET in the planning of radiotherapy.(44) Its use in association with CT allowed to reduce the radiation field (179cm² x 166cm²), favoring mainly patients with ventilation alterations (for ex., atelectasis).(45)

 

Evaluation of tumor recurrence

The sensitivity of the conventional radiographic examinations (X-rays, CT and NMR of the chest) is not good enough to differentiate a tumor relapse from necrosis or residual fibrosis. FDG-PET can be used for this purpose, although there is little experience in the world on that matter. Its sensitivity varies from 97% to 100%, and its specificity from 62% to 100%.(11) Thus, its use allows to make earlier diagnosis of a tumor relapse, allowing early treatment.

 

Other tumors

Data of the literature on the use of FDG-PET in small-cell pulmonary carcinoma are scarce. Chin et al. evaluated 18 patients, comparing conventional staging with FDG-PET.(46) There was concordance in 83% of the cases (15 out of 18). In the other three patients, FDG-PET showed a metastatic disease that had not been visualized by the conventional staging methods. Other authors demonstrated that FDG-PET has a prognostic value for the same neoplasm.(47)

Bénard et al. made a FDG-PET evaluation of 17 patients with malignant mesothelioma and observed that, the higher the uptake, the poorer the prognosis of those patients.(48) The authors concluded that uptake intensity was related to survival in patients with this kind of neoplasia, and that this information was clinically relevant. British authors reported the case of a 60-year-old patient, who presented, on computed tomography of the chest, a great lobular pleural thickening that had remained undiagnosed even after percutaneous biopsies and videothoracoscopy. After performing FDG-PET, a more intense uptake was observed in the right cardiophrenic angle region, the site where targeted biopsies were made, revealing a mesothelioma in the examined material.(49)

A similar experience occurred here in Brazil, where a 62-year-old patient was diagnosed with pleural mesothelioma, after marking the biopsy site by FDG-PET. Also in this case, a previous thoracotomy had been unable to lead to the diagnosis of the pleural tumor.(50)

 

Conclusion

Currently, there is already rather significant evidence allowing to assume that, in most situations, FDG-PET in association with a good clinical and tomographic examination, can differentiate, in patients with pulmonary nodules, those which are benign from those which are secondary to neoplasias. It also allows better mediastinal and whole-body staging in non-small-cell pulmonary tumors, besides making it possible to indicate sites for targeted biopsies. There is no evidence so far allowing us to conclude that FDG-PET can be used as the sole test (associated with chest CT) in the staging of non-small-cell pulmonary carcinoma, therefore it should always be associated with routine tests. It is an expensive test that, in Brazil, costs approximately R$ (reais) 1,600.00 (US$ 500.00) when performed in a hybrid equipment, and R$ 2,600.00 (US$ 700.00) when performed in a dedicated chamber. Despite its high cost, a great number of resection surgeries can be prevented, and the test has a good cost/benefit ratio.

 

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Correspondence to
Rua Alves Guimarães, 461, apto. 32
05410-000 – São Paulo, SP, Brazil.
Phone: +55 11 3081-3181 (home); +55 11 3082-7040 (fax); +55 11 9503-8332 (cell).
E-mail: majaco@terra.com.br.

Received for publication on 03/22/03.
Approved, after revision, on 04/11/03.

 

 

* Work performed at the Heart Insitute (Instituto do Coração - InCor), Hospital das Clínicas of the University of São Paulo Medical School (HC-FMUSP).

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