Negative Predictive Value of Positron Emission Tomography and Computed Tomography for Stage T1-2N0 Non–Small-Cell Lung Cancer: A Meta-Analysis

doi:10.1016/j.cllc.2011.08.002

Clinical Lung Cancer

Volume 13, Issue 2, March 2012, Pages 81-89

https://doi.org/10.1016/j.cllc.2011.08.002 Get rights and content

Abstract

Background

Nodal staging of non–small-cell lung cancer (NSCLC) is crucial in evaluation of prognosis and determination of therapeutic strategy. This study aimed to determine the negative predictive value (NPV) of combined positron emission tomography and computed tomography (PET-CT) in patients with stage I (T1-2N0) NSCLC and to investigate the possible risk factors for occult nodal disease.

Methods

Studies investigating the performance of PET in conjunction with CT in the nodal staging of stage I NSCLC were identified in the MEDLINE database. The initiative of standards for reporting of diagnostic accuracy (STARD) was used to ensure study quality. Pathologic assessments through mediastinoscopy or thoracotomy were required as the reference standard for evaluation of PET-CT accuracy. Stata-based meta-analysis was applied to calculate the individual and pooled NPVs.

Results

Ten studies with a total of 1122 patients with stage I (T1-2N0) NSCLC were eligible for analysis. The NPVs of combined PET and CT for mediastinal metastases were 0.94 in T1 disease and 0.89 in T2 disease. Including both T1 disease and T2 disease, the NPVs were 0.93 for mediastinal metastases and 0.87 for overall nodal metastases. Adenocarcinoma histology type (risk ratio [RR], 2.72) and high fluorine-18 (¹⁸F) fluorodeoxyglucose (FDG) uptake in the primary lesion were associated with greater risk of occult nodal metastases.

Conclusions

Although overall occult nodal metastases in clinical stage T1-2N0 NSCLC is not infrequent, combined PET and CT provide a favorable NPV for mediastinal metastases in T1N0 NSCLC, suggesting a low yield from routine invasive staging procedures for this subgroup of patients.

Introduction

Lung cancer is the leading cause of cancer deaths worldwide. In 2008 there were an estimated 1.61 million new cases and 1.38 million deaths worldwide,¹ among which 85% were non–small-cell lung cancer (NSCLC). Accurate staging, especially nodal staging, is a crucial factor for evaluation of prognosis and determination of treatment strategy in NSCLC.

Intravenous contrast-enhanced computed tomography (CT) is the most commonly used imaging modality for clinical staging. The predictive ability of CT for mediastinal lymph node metastasis has been well documented, with sensitivity and specificity of 57%-68% and 76-82%, respectively.2, 3, 4, 5, 6 Using the fluorine-18 (¹⁸F) fluorodeoxyglucose (FDG) tracer, positron emission tomography (PET) has much better performance in identification of nodal disease because abnormal metabolic uptake generally precedes anatomic change, providing a sensitivity of 79%-85% and a specificity of 87%-92%.2, 3, 4, 5, 6 Combined PET and CT (PET-CT), in particular integrated PET-CT, could further improve the accuracy of malignant node detection by combining information on spatial resolution, anatomic localization, and metabolic activity of the suspicious lesion.7, 8

Traditionally, mediastinoscopy and systematic lymph node dissection have been regarded as the gold standard for the identification of mediastinal lymph node metastasis by offering pathologic proof of malignancy. The emerging transesophageal ultrasound-guided fine-needle aspiration (EUS-FNA) and endobronchial ultrasound-guided transbronchial needle aspiration (EBUS-TBNA) may serve as alternatives to mediastinoscopy but have not yet been validated.9, 10, 11 Nevertheless, all these modalities are invasive and highly dependent on operator expertise.

In theory, tumors in the early stage behave less aggressively and may have a lower risk of lymph node involvement. The reported presence of mediastinal lymph node metastasis in patients with stage I NSCLC determined by CT ranged from 6%-21%; this was verified by mediastinoscopy-based or thoracotomy-based lymph node sampling or dissection.12, 13, 14 The relatively low rate of nodal involvement calls into question how much benefit can be gained from routine invasive staging for patients with PET-CT–identified small primary lesions and negative nodal findings. We performed a meta-analysis to evaluate the negative predictive value (NPV) of PET-CT in patients with stage I NSCLC (AJCC 6th edition stage T1-2N0M0) and further investigate the potential risk factors for nodal involvement.

Section snippets

Study Eligibility and Identification

We attempted to identify all studies that investigated the diagnostic performance of combined FDG-PET and CT, either integrated or visually correlated, for nodal staging in patients with stage I (T1-2N0) NSCLC. Computerized search of the MEDLINE database was performed using the following keywords: positron emission tomography, non–small-cell lung cancer, stage I, lymph node. Mediastinoscopy, thoracotomy-based lymph node dissection, or lymph node sampling was required to verify mediastinal

Study Identification and Quality

Sixty-seven English-language articles were retrieved in our initial literature search. After reviewing these articles and corresponding references, 10 studies were identified as eligible for this analysis.24, 25, 26, 27, 28, 29, 30, 31, 32, 33 Results of the methodology quality assessment for all studies are shown in Table 1. Quality scores in the series ranged from 10 to 16, with both mean and median values of 13. The worst described item was technical specifications of imaging, with a total

Discussion

In this meta-analysis of 10 studies including 1122 patients with PET-CT–determined stage I (T1-2N0) NSCLC, the summary estimated NPV was 0.93 for mediastinal metastasis. The NPVs for mediastinal metastases in T1 and T2 subgroups were 0.94 and 0.89, respectively. In terms of the overall nodal metastases, the summary estimated NPV of PET-CT was 0.87 for stage I NSCLC. To our knowledge, this is the first combined study systemically evaluating the diagnostic performance of combined FDG-PET and CT

Conclusions

In summary, combined PET and CT provide a favorable NPV for mediastinal metastases in clinical T1N0 NSCLC, and the presence of occult mediastinal involvement is around 6%, inferring a low yield from routine invasive staging procedures for this group of patients. Patients with T2 disease, adenocarcinoma histology, or high FDG uptake in primary lesions have a higher risk of nodal metastases, and the invasive staging procedures are recommended before the initiation of any active treatment.

Disclosure

All authors report that they have no relevant relationships to disclose.

Acknowledgments

We would like to thank Dr. Morand Piert and Dr. Kirk Frey for their valuable comments. We also thank Matthew Schipper for his comments on statistical analysis. We are appreciative of the efforts of Paul Stanton for editing the manuscript.

This work was funded in part by R21CA127057 and R01 CA142840.

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Video-assisted mediastinoscopic lymphadenectomy (VAMLA): Mature results for staging non–small cell lung cancer with normal mediastinum
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The aim of this study is to analyze the accuracy of video-assisted mediastinoscopic lymphadenectomy (VAMLA) and the unsuspected (u) N2/3 rates in patients with non–small cell lung cancer (NSCLC) and normal mediastinum by integrated positron emission tomography-computed tomography.
Prospective observational single-center study of 603 consecutive VAMLAs from 2010 to 2022. Exclusion criteria: other indications (n = 32), tumors different from NSCLC (n = 91), and clinical (c) N2/3 tumors by positron emission tomography-computed tomography (n = 46). Systematic nodal dissection was the gold standard to validate negative VAMLAs. Those patients with negative VAMLA and missing reference standard test were excluded. uN2/3 rates were analyzed in the global series and in the subgroups of tumors according to their clinical nodal and tumor categories. Pathologic findings were reviewed, and staging values were calculated.
Three hundred eighty-three patients with cN0/1 NSCLC underwent VAMLA. Staging values of VAMLA were: sensitivity, 0.98 (95% CI, 0.92-0.99); negative predictive value, 0.99 (95% CI, 0.98-1); and diagnostic accuracy, 0.99 (95% CI, 0.98-1). The uN2/3 rate for the whole series (N = 383) was 18.8%. The uN2/3 rates according to presurgical nodal and tumor categories determined by positron emission tomography computed tomography were: 3.6% (4 out of 111) in cT1N0; 16.3% (18 out of 110) in cT2N0; 10.25% (4 out of 39) in cT3N0; and 32% (7 out of 22) in cT4N0. Forty-two percent (39 out of 93) in cN1; complication rate was 7%.
This series of NSCLC with normal mediastinum staged by VAMLA demonstrates a high accuracy of this technique and a high rate of uN2/3 disease (specially in cN1 and cT4N0). VAMLA could be considered the reference staging procedure for staging cN0/1 NSCLC.
Bilan d'extension du cancer bronchique et classification TNM des CBNPC
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Le diagnostic de certitude de cancer du poumon repose sur l’examen anatomopathologique. Les prélèvements tissulaires (par biopsie), ou cellulaires (par lavage, cytoponction) sont réalisés à partir de la tumeur, des adénopathies associées ou d’un site métastatique accessible. Il existe différentes méthodes d’abord diagnostique d’une opacité suspecte de cancer bronchique. Des recommandations pour chacune des techniques ont été émises afin d’en maximiser le rendement diagnostique et de permettre des analyses immunohistochimiques ou de biologie moléculaire ou qui modifient la stratégie thérapeutique. Le premier objectif de ce propos est d’exposer les différentes méthodes diagnostiques et de proposer des pistes pour optimiser le diagnostic des cancers broncho-pulmonaires.
Définir le cTNM repose sur un bilan précis et rigoureux. Le second objectif de cet article est de présenter les modalités du bilan d’extension des CBNPC, en abordant les indications des examens d’imagerie ainsi que leurs limites. Le bilan des CPC est traité dans un chapitre spécifique. L’examen clinique reste essentiel. Le scanner thoracique avec injection de produit de contraste iodée est systématique, sauf contre-indication. La taille de la tumeur, son extension pleurale, pariétale, endobronchique et médiastinale directe doivent être précisées de même que l’extension ganglionnaire. La TEP-TDM au 18FDG n’est pas indiquée en première intention mais elle est indispensable chez les patients potentiellement éligibles à un traitement curatif. L’imagerie cérébrale est indiquée, même chez les patients asymptomatiques. Le respect des recommandations et une organisation adéquate optimisent la prise en charge des patients. La classification internationale TNM, acceptée conjointement par l’UICC et l’AJCC est utilisée en routine pour les cancers bronchiques non à petites cellules. Le but de cet article est de présenter la 8^e classification TNM, son implication en pratique ainsi que les propositions émanant du IASLC Staging Committee concernant certaines situations cliniques particulières. La base de données qui va servir à l’élaboration de la 9^ème classification est décrite en attendant la publication de la.prochaine révision
1877-1203/© 2023 SPLF. Publié par Elsevier Masson SAS. Tous droits réservés.
The definitive diagnosis of lung cancer relies on pathological examination. Tissue samples (by biopsy), or cell samples (by washing, cytopuncture) are collected from the tumor, associated lymphadenopathy or from an accessible metastatic site. There are different methods of diagnostic access to an opacity suspect of bronchial cancer. Guidelines have been published for each of the techniques in order to maximize their diagnostic efficiency and to allow or immunohistochemical or molecular analyses that modify the therapeutic strategy. The first objective of this topic is to describe the different diagnostic methods and to suggest ways to optimize the diagnosis of broncho-pulmonary cancers.
Establishing cTNM relies on a precise and rigorous evaluation. The second objective of this article is to present the modalities of NSCLC extension assessment, addressing the indications of imaging exams as well as their limitations. SCLC management is discussed in a specific chapter. Clinical examination remains essential. Chest Computed- Tomography (CT) scan with iodine contrast injection is systematic, unless contraindicated. The size of the tumor, its pleural, parietal, endobronchial and direct mediastinal extension should be specified as well as the lymph node extension. 18FDG PET-CT is not indicated as a first line but is essential in patients potentially eligible for curative treatment. Brain imaging is indicated, even in asymptomatic patients. Compliance with the recommendations and proper organisation optimise management of patients.
The international TNM classification, accepted by both UICC and AJCC, is routinely used for non-small cell lung cancer management. The aim of this article is to review the 8^th TNM classification, its practical implications and the IASLC Staging Committee proposals regarding some specific clinical situations. The new database that will inform the ninth TNM classification is discribed awiating publication of the next revision.
1877-1203/© 2023 SPLF. Published by Elsevier Masson SAS. All rights reserved.
Results in mediastinal lymph node staging of surgical lung cancer: Data from the prospective cohort of the Spanish Video-Assisted Thoracic Surgery Group
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El objetivo del estudio es valorar el rendimiento diagnóstico de la tomografía computarizada (TC) y la tomografía por emisión de positrones (PET) en la estadificación clínica mediastínica del cáncer pulmonar quirúrgico según los datos de la cohorte prospectiva del Grupo Español de Cirugía Torácica Videoasistida (GEVATS).
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El acierto global de la TC y PET en conjunto es del 82,9% con VPP y VPN de 0,21 y 0,93. En tumores mayores de 3 cm y a mayor SUVmax del mediastino, el acierto es menor, OR de 0,59 (0,44 – 0,79) y 0,71 (0,66 – 0,75), respectivamente. En el abordaje VATS el acierto es mayor, OR de 2,04 (1,52 – 2,73). El riesgo de pN2 inesperado aumenta con el número de los factores cN1, tumor central o tamaño mayor de 3 cm: entre el 4,5% (0 factores) y 18,8% (3 factores), pero no hay diferencias significativas con la realización de prueba invasiva.
La TC y PET en conjunto tienen un elevado valor predictivo negativo. Su acierto global es menor en tumores mayores de 3 cm y SUVmax del mediastino elevado, y mayor en el abordaje VATS. El riesgo de pN2 inesperado es mayor si cN1, tumor central o mayor de 3 cm y no varía significativamente con prueba invasiva.
The objective of this study was to assess the diagnostic performance of combined computerised tomography (CT) and positron emission tomography (PET) in mediastinal staging of surgical lung cancer based on data obtained from the prospective cohort of the Spanish Group for Video-Assisted Thoracic Surgery (GEVATS).
A total of 2782 patients underwent surgery for primary lung carcinoma. We analysed diagnostic success in mediastinal lymph node staging (cN2) using CT and PET. Bivariate and multivariate analyses were performed of the factors involved in this success. The risk of unexpected pN2 disease was analysed for cases in which an invasive testing is recommended: cN1, the tumour centrally located or the tumour diameter >3 cm.
The overall success of CT together with PET was 82.9% with a positive predictive value of 0.21 and negative predictive value of 0.93. If the tumour was larger than 3 cm and for each unit increase in mediastinal SUVmax, the probability of success was lower with OR 0.59 (0.44–0.79) and 0.71 (0.66–0.75), respectively. In the video-assisted thoracic surgery (VATS) approach, the probability of success was higher with OR 2.04 (1.52–2.73). The risk of unexpected pN2 increased with the risk factors cN1, the tumour centrally located or the tumour diameter >3 cm: from 4.5% (0 factors) to 18.8% (3 factors) but did not differ significantly as a function of whether invasive testing was performed.
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Lung cancer: Diagnostic techniques
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The prevalence of lung cancer and its associated health care burden have increased significantly over the past 100 years. The annual number of deaths from lung cancer in the United States now exceeds the combined death toll from breast, colon, and prostate cancer. A systematic approach to the diagnosis and management of lung cancer will remain a pressing medical need for the coming several decades. Early detection and diagnosis of lung cancer play a pivotal role in decreasing mortality from this disease. In this chapter, we present an overview of current techniques, approaches, and guidelines used in the diagnosis and staging of lung cancer.
Bilan du cancer broncho-pulmonaire non à petites cellules : quel bilan anatomique ?
2022, Revue des Maladies Respiratoires Actualites
Le diagnostic de certitude de cancer du poumon repose sur l’examen anatomopathologique. Les prélèvements tissulaires (par biopsie), ou cellulaires (par lavage, cytoponction) sont réalisés à partir de la tumeur, des adénopathies associées ou d’un site métastatique accessible. Il existe différentes méthodes d’abord diagnostique d’une opacité suspecte de cancer bronchique. Des recommandations pour chacune des techniques ont été émises afin d’en maximiser le rendement diagnostique et de permettre des analyses immunohistochimiques ou de biologie moléculaire qui modifient la stratégie thérapeutique. Le premier objectif de ce propos est d’exposer les différentes méthodes diagnostiques et de proposer des pistes pour optimiser le diagnostic des cancers broncho-pulmonaires.
Définir le cTNM nécessite un bilan précis et rigoureux. Le second objectif de cet article est de présenter les modalités du bilan d’extension des CBNPC, en abordant les indications des examens d’imagerie ainsi que leurs limites. L’examen clinique reste essentiel. Le scanner thoracique avec injection de produit de contraste iodée est systématique. La taille de la tumeur, son extension pleurale, pariétale, endobronchique et médiastinale directe doivent être précisées de même que l’extension ganglionnaire. La TEP-TDM au 18FDG n’est pas indiquée en première intention mais est indispensable chez les patients potentiellement éligibles à un traitement curatif. L’imagerie cérébrale est indiquée, même chez les patients asymptomatiques. Le respect des recommandations et une organisation adéquate optimisent la prise en charge des patients.
1877-1203/© 2022 SPLF. Publié par Elsevier Masson SAS. Tous droits réservés.
The definitive diagnosis of lung cancer relies on pathological examination. Tissue samples (by biopsy), or cell samples (by washing, cytopuncture) are collected from the tumor, associated lymphadenopathy or from an accessible metastatic site. There are different methods of diagnostic access to an opacity suspect of bronchial cancer. Guidelines have been published for each of the techniques in order to maximize their diagnostic efficiency and to allow either immunohistochemical or molecular analyses that modify the therapeutic strategy. The first objective of this topic is to describe the different diagnostic methods and to suggest paths to optimize the diagnosis of broncho-pulmonary cancers. Establishing cTNM relies on a precise and rigorous evaluation.
The second objective of this article is to present the modalities of NSCLC extension assessment, addressing the indications of imaging exams as well as their limitations. Clinical examination remains essential. Chest Computed-Tomography (CT) scan with iodine contrast injection is systematic. The size of the tumor, its pleural, parietal, endobronchial and direct mediastinal extension should be specified as well as the lymph node extension. ¹⁸FDG PET-CT is not indicated frontline, but is essential in patients potentially eligible for curative treatment. Brain imaging is indicated, even in asymptomatic patients. Compliance with such recommendations and proper organisation is needed to optimise patients management.
1877-1203/© 2022 SPLF. Published by Elsevier Masson SAS. All rights reserved.
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Lung cancer management guidelines strive to improve outcomes. Theoretically, thorough staging promotes optimal treatment selection. We examined the association between guideline-concordant invasive mediastinal nodal staging, guideline-concordant treatment, and non-small cell lung cancer survival.
What is the current practice of invasive mediastinal nodal staging for patients with lung cancer in a structured multidisciplinary care environment? Is guideline-concordant staging associated with guideline-concordant treatment? How do they relate to survival?
We evaluated patients with nonmetastatic non-small cell lung cancer diagnosed from 2014 through 2019 in the Multidisciplinary Thoracic Oncology Program of the Baptist Cancer Center, Memphis, Tennessee. We examined patterns of mediastinal nodal staging and stage-stratified treatment, grouping patients into cohorts with guideline-concordant staging alone, guideline-concordant treatment alone, both, or neither. We evaluated overall survival with Kaplan-Meier curves and Cox proportional hazards models.
Of 882 patients, 456 (52%) received any invasive mediastinal staging. Seventy-four percent received guideline-concordant staging; guideline-discordant staging decreased from 34% in 2014 to 18% in 2019 (P < .0001). Recipients of guideline-concordant staging were more likely to receive guideline-concordant treatment (83% vs 66%; P < .0001). Sixty-one percent received both guideline-concordant invasive mediastinal staging and guideline-concordant treatment; 13% received guideline-concordant staging alone; 17% received guideline-concordant treatment alone; and 9% received neither. Survival was greatest in patients who received both (adjusted hazard ratio [aHR], 0.41; 95% CI, 0.26-0.63), followed by those who received guideline-concordant treatment alone (aHR, 0.60; 95% CI, 0.36-0.99), and those who received guideline-concordant staging alone (aHR, 0.64; 95% CI, 0.37-1.09) compared with neither (P < .0001, log-rank test).
Levels of guideline-concordant staging were high, were rising, and were associated with guideline-concordant treatment selection in this multidisciplinary care cohort. Guideline-concordant staging and guideline-concordant treatment were complementary in their association with improved survival, supporting the connection between these two processes and lung cancer outcomes.

View all citing articles on Scopus

: This study was presented as a Mini oral presentation at the 14th World Conference on Lung Cancer, Amsterdam, Netherland, (July 3-7, 2011).

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PerspectiveNegative Predictive Value of Positron Emission Tomography and Computed Tomography for Stage T1-2N0 Non–Small-Cell Lung Cancer: A Meta-Analysis

Abstract

Background

Methods

Results

Conclusions

Introduction

Section snippets

Study Eligibility and Identification

Study Identification and Quality

Discussion

Conclusions

Disclosure

Acknowledgments

Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 10 [Internet]

Combining independent studies of diagnostic fluorodeoxyglucose positron-emission tomography and computed tomography in mediastinal lymph node staging for non-small cell lung cancer

Tumori

Meta-analysis of positron emission tomographic and computed tomographic imaging in detecting mediastinal lymph node metastases in nonsmall cell lung cancer

Ann Thorac Surg

Test performance of positron emission tomography and computed tomography for mediastinal staging in patients with non-small-cell lung cancer: a meta-analysis

Ann Intern Med

Noninvasive staging of non-small cell lung cancer: a review of the current evidence

Chest

Metastases from non-small cell lung cancer: mediastinal staging in the 1990s—meta-analytic comparison of PET and CT

Radiology

Staging of non-small-cell lung cancer with integrated positron-emission tomography and computed tomography

N Engl J Med

The accuracy of integrated PET-CT compared with dedicated PET alone for the staging of patients with nonsmall cell lung cancer

Ann Thorac Surg

Mediastinoscopy vs endosonography for mediastinal nodal staging of lung cancer: a randomized trial

JAMA

Mediastinoscopy in patients with lung cancer and negative endobronchial ultrasound guided needle aspiration

Ann Thorac Surg

The true false negative rates of esophageal and endobronchial ultrasound in the staging of mediastinal lymph nodes in patients with non-small cell lung cancer

Ann Thorac Surg

Mediastinoscopy in patients with clinical stage I non-small cell lung cancer

Ann Thorac Surg

T1 lung cancer: prevalence of mediastinal nodal metastases and diagnostic accuracy of CT

Radiology

N2 disease in T1 non-small cell lung cancer

Ann Thorac Surg

Towards complete and accurate reporting of studies of diagnostic accuracy: the STARD initiative

Fam Pract

The combination of estimates from different experiments

Biometrics

An evaluation of homogeneity tests in meta-analyses in pain using simulations of individual patient data

Pain

Quantifying heterogeneity in a meta-analysis

Stat Med

Measuring inconsistency in meta-analyses

BMJ

Methods for Meta-Analysis in Medical Research

Meta-analysis in clinical trials

Control Clin Trials

Statistical aspects of the analysis of data from retrospective studies of disease

J Natl Cancer Inst

Estimators of the Mantel-Haenszel variance consistent in both sparse data and large-strata limiting models

Biometrics

Non-small cell lung cancer: FDG PET for nodal staging in patients with stage I disease

Radiology

Mediastinal lymph node staging by FDG-PET in patients with non-small cell lung cancer: analysis of false-positive FDG-PET findings

Respiration

Perspective
Negative Predictive Value of Positron Emission Tomography and Computed Tomography for Stage T1-2N0 Non–Small-Cell Lung Cancer: A Meta-Analysis