Preoperative mediastinal and hilar nodal staging with diffusion-weighted magnetic resonance imaging and fluorodeoxyglucose positron emission tomography/computed tomography in patients with non–small-cell lung cancer: Which is better?

doi:10.1016/j.jss.2012.03.074

Journal of Surgical Research

Volume 178, Issue 1, November 2012, Pages 304-314

https://doi.org/10.1016/j.jss.2012.03.074 Get rights and content

Abstract

Background

To compare the diagnostic capability of diffusion-weighted magnetic resonance imaging (DWI) and ¹⁸F-fluorodeoxyglucose positron emission tomography/computed tomography (¹⁸F-FDG PET/CT) in the N stage assessment in patients with non–small-cell lung cancer.

Methods

We performed a meta-analysis of all available studies of the diagnostic performance of DWI and ¹⁸F-FDG PET/CT in the N stage assessment of patients with non–small-cell lung cancer. We determined the sensitivity and specificity across studies, calculated the positive and negative likelihood ratios (LR+ and LR−, respectively), and constructed the summary receiver operating characteristic curves using hierarchical regression models. The methodologic quality was assessed using the Quality Assessment of Diagnostic Accuracy Studies tool.

Results

A total of 19 studies met the inclusion criteria and included a total of 2845 pathologically confirmed patients. No publication bias was found. The methodologic quality was relatively high. The pooled sensitivity estimate of DWI (0.72, 95% confidence interval [CI] 0.63–0.80) was not significantly difference between PET/CT (0.75, 95% CI 0.68–0.81; P = 0.09). The pooled specificity estimate for DWI (0.95, 95% CI 0.85–0.98) was significantly greater than ¹⁸F-FDG PET/CT (0.89, 95% CI 0.85–0.91; P = 0.02). For DWI, the overall LR+ was 13.80 (95% CI 4.54–41.95) and the LR− was 0.29 (95% CI 0.21–0.40). For ¹⁸F-FDG PET/CT, LR+ was 6.67 (95% CI 5.20–8.56) and LR− was 0.28 (95% CI 0.22–0.37).

Conclusions

Our study has confirmed that DWI has a high specificity for N staging of non–small-cell lung cancer compared with ¹⁸F-FDG PET/CT and has the potential to be a reliable alternative noninvasive imaging method for the preoperative staging of mediastinal and hilar lymph nodes in patients with non–small-cell lung cancer.

Introduction

Lung cancer is the leading cause of cancer death in both men and women worldwide [1]. Non–small-cell lung cancer (NSCLC) accounts for 80% of all cases of lung cancer, and it can be cured with surgery if it is detected at an early stage [2]. In patients with NSCLC, involvement of the mediastinal lymph nodes is an important prognostic factor because accurate disease staging is needed to limit surgery or multimodality treatment to only those patients who might benefit from such treatment [3], [4], [5].

Various diagnostic techniques and procedures, such as computed tomography (CT), magnetic resonance imaging (MRI), bronchoscopy, mediastinoscopy, and positron emission tomography (PET), are used for the preoperative staging of lung cancer. CT is the most commonly used method for lymph node staging. However, its limitation is that it relies on the size of the lymph node to differentiate benign from malignant. The sensitivity and specificity of CT in this regard are approximately 60%, which is not optimal for clinical decision making [6], [7], [8], [9], [10].

PET is a functional imaging modality that can potentially detect tumor activity in nonenlarged structures and allow earlier detection of metastatic disease [11]. From a number of trials, PET combined with CT is now widely used for the staging of NSCLC [12], [13], [14], [15], [16] and offers some advantage over CT alone in assessing the mediastinal nodes [17].

Recent advances in MRI gradient technology have allowed acquisition of diffusion-weighted MRI (DWI), which provides excellent tissue contrast because of the difference in the diffusion of water molecules among tissues and is different from ordinary T₁- and T₂-weighted images. Furthermore, diffusion-weighted MRI has been put forward in the past few years as a new technique with which to differentiate metastatic lymph nodes from nonmetastatic lymph nodes in patients with NSCLC [18], [19]. The technique yields qualitative and quantitative information that reflects changes at a cellular level and provides unique insights about tumor cellularity and the integrity of cell membranes [20]. When apparent diffusion coefficients are assessed with DWI, there is a significant difference in apparent diffusion coefficients between malignant and benign lesions.

To our knowledge, however, no one has directly compared the diagnostic capability for N stage assessment of DWI and ¹⁸F-FDG PET/CT in patients with NSCLC using a meta-analysis. In the present study, we performed a meta-analysis to evaluate N staging of NSCLC using DWI compared with ¹⁸F-FDG PET/CT.

Section snippets

Data search

A comprehensive search of studies on human subjects was performed by 1 observer to identify reports on the diagnostic performance of DWI, ¹⁸F-FDG PET/CT in the N stage assessment of patients with NSCLC. The Medline and Embase databases, from January 2000 to December 2011, were used for English studies with the following keywords: “diffusion-weighted magnetic resonance imaging” OR “DWI” AND “positron emission tomography/computed tomography” OR “PET/CT” OR “PET-CT” AND “lung cancer” OR “nonsmall

Data search and study selection

After the comprehensive computerized search was performed, and the reference lists were extensively cross-checked, our research yielded 1178 primary studies, of which 1135 were excluded after reviewing the title and abstract. Then, 23 studies were excluded after reviewing the full report because the aim of the studies was not to reveal ¹⁸F-FDG PET/CT or DWI for N staging of NSCLC [23], [24] or because too few data reported to permit construction of a 2 × 2 table of true-positive,

Discussion

In the present study, we compared the diagnostic ability of DWI with ¹⁸F-FDG PET/CT for mediastinal and hilar nodal staging in patients with NSCLC. Our meta-analysis, which included data from 2845 patients, has shown that a superiority of DWI to ¹⁸F-FDG PET/CT for N staging in patients with NSCLC because of improved specificity in the former, although the pooled sensitivity is similar. False-negative diagnosis with ¹⁸F-FDG PET/CT caused by concurrent lymphadenitis is well known for N staging in

Conclusions

Despite some limitations, our study has confirmed that DWI has a high specificity for N staging of NSCLC compared with ¹⁸F-FDG PET/CT and has the potential to be a reliable alternative noninvasive imaging method for the preoperative staging of mediastinal and hilar lymph node in patients with NSCLC. However, we believe it is too early to call for broad application of this method in clinical practice. We speculate that additional improvement of the technology will increase its role in the

Acknowledgments

The authors thank Yan-Yan Song (Faculty of Department of Medical Statistics, Shanghai Jiao Tong University School of Medicine, Shanghai, China) for critical review and correction of our report. The authors also thank the Shanghai Leading Academic Discipline Project (grant S30203) and Shanghai Jiaotong University School of Medicine Leading Academic Discipline Project for supporting our study.

References (67)

C.M. Free et al.
Lung cancer outcomes at a UK cancer unit between 1998–2001
Lung Cancer
(2007)
M. Okada et al.
Is segmentectomy with lymph node assessment an alternative to lobectomy for nonsmall cell lung cancer of 2 cm or smaller?
Ann Thorac Surg
(2001)
N. Martini et al.
Comparative merits of conventional, computed tomographic, and magnetic resonance imaging in assessing mediastinal involvement in surgically confirmed lung carcinoma
J Thorac Cardiovasc Surg
(1985)
H. Van Tinteren et al.
Effectiveness of positron emission tomography in the preoperative assessment of patients with suspected non small cell lung cancer: The PLUS multicentre randomized trial
Lancet
(2002)
H. Nomori et al.
Diffusion weighted magnetic resonance imaging can be used in place of positron emission tomography for N staging of non-small cell lung cancer with fewer false-positive results
J Thorac Cardiovasc Surg
(2008)
W. Chen et al.
Whole-body diffusion-weighted imaging vs. FDG-PET for the detection of non–small-cell lung cancer: How do they measure up?
Magn Reson Imaging
(2010)
L.P. Liu et al.
Preliminary study of ¹⁸F-FDG PET-CT in defining lymph node radiation target volume for non–small-cell lung cancer patients
Zhonghua Zhong Liu Za Zhi
(2007)
A.S. Bryant et al.
The clinical stage of non-small cell lung cancer as assessed by means of fluorodeoxyglucose-positron emission tomographic/computed tomographic scanning is less accurate in cigarette smokers
J Thorac Cardiovasc Surg
(2006)
R. Kanzaki et al.
Occult mediastinal lymph node metastasis in NSCLC patients diagnosed as clinical N0-1 by preoperative integrated FDG-PET/CT and CT: Risk factors, pattern, and histopathological study
Lung Cancer
(2011)
K. Usuda et al.
Diffusion-weighted imaging is superior to positron emission tomography in the detection and nodal assessment of lung cancers
Ann Thorac Surg
(2011)

R. Sánchez Sánchez et al.

Utility of PET/CT for mediastinal staging of non-small cell lung cancer in stage III (N2)

Rev Esp Med Nucl

(2011)

B. Hwangbo et al.

Application of endobronchial ultrasound-guided transbronchial needle aspiration following integrated PET/CT in mediastinal staging of potentially operable non-small cell lung cancer

Chest

(2009)

G.E. Darling et al.

Positron emission tomography-computed tomography compared with invasive mediastinal staging in non-small cell lung cancer: Results of mediastinal staging in the early lung positron emission tomography trial

J Thorac Oncol

(2011)

M. Sanli et al.

Reliability of positron emission tomography-computed tomography in identification of mediastinal lymph node status in patients with non-small cell lung cancer

J Thorac Cardiovasc Surg

(2009)

W.F. Yang et al.

Value of PET/CT versus enhanced CT for locoregional lymph nodes in non-small cell lung cancer

Lung Cancer

(2008)

B.E. Lee et al.

Advances in positron emission tomography technology have increased the need for surgical staging in non-small cell lung cancer

J Thorac Cardiovasc Surg

(2007)

B.S. Halpern et al.

Presurgical staging of non-small cell lung cancer: Positron emission tomography, integrated positron emission tomography/CT, and software image fusion

Chest

(2005)

P.F. Roberts et al.

Factors associated with false positive staging of lung cancer by positron emission tomography

Ann Thorac Surg

(2000)

A. Jemal et al.

Recent trends in lung cancer mortality in the United States

J Natl Cancer Inst

(2001)

H. Onishi et al.

Stereotactic hypofractionated high-dose irradiation for stage I nonsmall cell lung carcinoma: Clinical outcomes in 245 subjects in a Japanese multiinstitutional study

Cancer

(2004)

K. Nakamura et al.

A phase III randomized trial of lobectomy versus limited resection for small-sized peripheral non-small cell lung cancer (JCOG0802/WJOG4607L)

Jpn J Clin Oncol

(2010)

G.M. Glazer et al.

The mediastinum in non-small cell lung cancer: CT-surgical correlation

AJR Am J Roentgenol

(1984)

G.M. Glazer et al.

Imaging of the pulmonary hilum: A prospective comparative study in patients with lung cancer

AJR Am J Roentgenol

(1985)

D. Musset et al.

Primary lung cancer staging: Prospective comparative study of MR imaging with CT

Radiology

(1986)

F. Laurent et al.

Bronchogenic carcinoma staging: CT versus MR imaging-assessment with surgery

Eur J Cardiothorac Surg

(1988)

K.B. Nolop et al.

Glucose utilization in vivo by human pulmonary neoplasms

Cancer

(1987)

R.C. Viney et al.

Randomized controlled trial of the role of positron emission tomography in the management of stage I and II non small cell lung cancer

J Clin Oncol

(2004)

G.J. Herder et al.

Traditional versus up front [¹⁸F]fluorodeoxyglucose-positron emission tomography staging of non small cell lung cancer: A Dutch cooperative randomized study

J Clin Oncol

(2006)

B. Fischer et al.

Preoperative staging of lung cancer with combined PET-CT

N Eng J Med

(2009)

D.E. Maziak et al.

Positron emission tomography in staging early lung cancer: A randomized trial

Ann Intern Med

(2009)

D. Lardinois et al.

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

N Engl J Med

(2003)

D.M. Koh et al.

Diffusion-weighted MRI in the body: Applications and challenges in oncology

AJR Am J Roentgenol

(2007)

P. Whiting et al.

The development of QUADAS: A tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews

BMC Med Res Methodol

(2003)

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Whole-body MRI (WB-MRI) could be an alternative to multimodality staging of colorectal cancer, but its diagnostic accuracy, effect on staging times, number of tests needed, cost, and effect on treatment decisions are unknown. We aimed to prospectively compare the diagnostic accuracy and efficiency of WB-MRI-based staging pathways with standard pathways in colorectal cancer.
The Streamline C trial was a prospective, multicentre trial done in 16 hospitals in England. Eligible patients were 18 years or older, with newly diagnosed colorectal cancer. Exclusion criteria were severe systemic disease, pregnancy, contraindications to MRI, or polyp cancer. Patients underwent WB-MRI, the result of which was withheld until standard staging investigations were complete and the first treatment decision made. The multidisciplinary team recorded its treatment decision based on standard investigations, then on the WB-MRI staging pathway (WB-MRI plus additional tests generated), and finally on all tests. The primary outcome was difference in per-patient sensitivity for metastases between standard and WB-MRI staging pathways against a consensus reference standard at 12 months, in the per-protocol population. Secondary outcomes were difference in per-patient specificity for metastatic disease detection between standard and WB-MRI staging pathways, differences in treatment decisions, staging efficiency (time taken, test number, and costs), and per-organ sensitivity and specificity for metastases and per-patient agreement for local T and N stage. This trial is registered with the International Standard Randomised Controlled Trial registry, number ISRCTN43958015, and is complete.
Between March 26, 2013, and Aug 19, 2016, 1020 patients were screened for eligibility. 370 patients were recruited, 299 of whom completed the trial; 68 (23%) had metastasis at baseline. Pathway sensitivity was 67% (95% CI 56 to 78) for WB-MRI and 63% (51 to 74) for standard pathways, a difference in sensitivity of 4% (−5 to 13, p=0·51). No adverse events related to imaging were reported. Specificity did not differ between WB-MRI (95% [95% CI 92–97]) and standard pathways (93% [90–96], p=0·48). Agreement with the multidisciplinary team's final treatment decision was 96% for WB-MRI and 95% for the standard pathway. Time to complete staging was shorter for WB-MRI (median, 8 days [IQR 6–9]) than for the standard pathway (13 days [11–15]); a 5-day (3–7) difference. WB-MRI required fewer tests (median, one [95% CI 1 to 1]) than did standard pathways (two [2 to 2]), a difference of one (1 to 1). Mean per-patient staging costs were £216 (95% CI 211–221) for WB-MRI and £285 (260–310) for standard pathways.
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Citation Excerpt :
WB-MRI could also accelerate staging, thereby increasing efficiency by reducing additional tests, staging time, and costs. Meta-analyses suggest accuracy of WB-MRI in detecting metastatic disease for metastatic disease is equivalent to, or might exceed, standard technologies,7–18 but most reports combine disparate cancers7–9,11,12,14,15 or those considering lung cancer alone focus on metastasis detection in a single organ, typically bone.10,13,16–18 Primary studies of WB-MRI in lung cancer staging are predominantly small, single site, explanatory studies with WB-MRI interpretation by a few highly experienced radiologists, which is unlike real-world pathways.4
Whole-body magnetic resonance imaging (WB-MRI) could be an alternative to multi-modality staging of non-small-cell lung cancer (NSCLC), but its diagnostic accuracy, effect on staging times, number of tests needed, cost, and effect on treatment decisions are unknown. We aimed to prospectively compare the diagnostic accuracy and efficiency of WB-MRI-based staging pathways with standard pathways in NSCLC.
The Streamline L trial was a prospective, multicentre trial done in 16 hospitals in England. Eligible patients were 18 years or older, with newly diagnosed NSCLC that was potentially radically treatable on diagnostic chest CT (defined as stage IIIb or less). Exclusion criteria were severe systemic disease, pregnancy, contraindications to MRI, or histologies other than NSCLC. Patients underwent WB-MRI, the result of which was withheld until standard staging investigations were complete and the first treatment decision made. The multidisciplinary team recorded its treatment decision based on standard investigations, then on the WB-MRI staging pathway (WB-MRI plus additional tests generated), and finally on all tests. The primary outcome was difference in per-patient sensitivity for metastases between standard and WB-MRI staging pathways against a consensus reference standard at 12 months, in the per-protocol population. Secondary outcomes were difference in per-patient specificity for metastatic disease detection between standard and WB-MRI staging pathways, differences in treatment decisions, staging efficiency (time taken, test number, and costs) and per-organ sensitivity and specificity for metastases and per-patient agreement for local T and N stage. This trial is registered with the International Standard Randomised Controlled Trial registry, number ISRCTN50436483, and is complete.
Between Feb 26, 2013, and Sept 5, 2016, 976 patients were screened for eligibility. 353 patients were recruited, 187 of whom completed the trial; 52 (28%) had metastasis at baseline. Pathway sensitivity was 50% (95% CI 37–63) for WB-MRI and 54% (41–67) for standard pathways, a difference of 4% (−7 to 15, p=0·73). No adverse events related to imaging were reported. Specificity did not differ between WB-MRI (93% [88–96]) and standard pathways (95% [91–98], p=0·45). Agreement with the multidisciplinary team's final treatment decision was 98% for WB-MRI and 99% for the standard pathway. Time to complete staging was shorter for WB-MRI (13 days [12–14]) than for the standard pathway (19 days [17–21]); a 6-day (4–8) difference. The number of tests required was similar WB-MRI (one [1–1]) and standard pathways (one [1–2]). Mean per-patient costs were £317 (273–361) for WBI-MRI and £620 (574–666) for standard pathways.
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The conventional method of usual clinical practice with which MRI was compared was PET or CT separately and, in few studies with PET/CT (both combined). WU et al.35 included 19 studies where they compared DW-MRI with FDG PET/CT but only in 3 of the 19 studies patients underwent DW-MRI, in the remaining 16, they only underwent FDG PET/CT. Finally, PEERLINGS et al.11 included only 12 studies with very strict selection criteria.
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MRI has shown at least similar or better results in diagnostic accuracy to differentiate metastatic from non-metastatic mediastinal lymph nodes. This suggests that MRI could play a significant role in mediastinal NSCLC staging.
El objetivo de este trabajo es evaluar el potencial diagnóstico de las imágenes por resonancia magnética (RM) para identificar nódulos linfáticos metastásicos frente aquellos no metastásicos en pacientes con cáncer de pulmón no microcítico (CPNM) en comparación con la tomografía computarizada (TC), la tomografía por emisión de positrones con ¹⁸F-fluorodesoxiglucosa (PET-FDG) o ambas técnicas combinadas.
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Se observó que la RM presentaba mayor sensibilidad, especificidad y precisión en la estadificación ganglionar (N) y el diagnóstico de nódulos linfáticos metastásicos o no metastásicos en pacientes con CPNM en comparación con la TC y el PET. Ningún estudio consideró a la RM inferior con respecto a otras técnicas convencionales (TC, PET y PET/TC). Otros resultados destacables de esta revisión son que con la RM se originaron menos falsos positivos en comparación con el PET, y su superioridad respecto al PET/TC en la detección de tumores de pulmón no operables, en el diagnóstico de infiltración en estructuras adyacentes o metástasis cerebrales, así como en la detección de nódulos de pequeño tamaño.
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Oncology/endocrinePreoperative mediastinal and hilar nodal staging with diffusion-weighted magnetic resonance imaging and fluorodeoxyglucose positron emission tomography/computed tomography in patients with non–small-cell lung cancer: Which is better?

Abstract

Background

Methods

Results

Conclusions

Introduction

Section snippets

Data search

Data search and study selection

Discussion

Conclusions

Acknowledgments

Lung Cancer

Ann Thorac Surg

J Thorac Cardiovasc Surg

Lancet

J Thorac Cardiovasc Surg

Magn Reson Imaging

Zhonghua Zhong Liu Za Zhi

J Thorac Cardiovasc Surg

Lung Cancer

Ann Thorac Surg

Rev Esp Med Nucl

Chest

J Thorac Oncol

J Thorac Cardiovasc Surg

Lung Cancer

J Thorac Cardiovasc Surg

Chest

Ann Thorac Surg

Recent trends in lung cancer mortality in the United States

J Natl Cancer Inst

Stereotactic hypofractionated high-dose irradiation for stage I nonsmall cell lung carcinoma: Clinical outcomes in 245 subjects in a Japanese multiinstitutional study

Cancer

A phase III randomized trial of lobectomy versus limited resection for small-sized peripheral non-small cell lung cancer (JCOG0802/WJOG4607L)

Jpn J Clin Oncol

The mediastinum in non-small cell lung cancer: CT-surgical correlation

AJR Am J Roentgenol

Imaging of the pulmonary hilum: A prospective comparative study in patients with lung cancer

AJR Am J Roentgenol

Primary lung cancer staging: Prospective comparative study of MR imaging with CT

Radiology

Bronchogenic carcinoma staging: CT versus MR imaging-assessment with surgery

Eur J Cardiothorac Surg

Glucose utilization in vivo by human pulmonary neoplasms

Cancer

Randomized controlled trial of the role of positron emission tomography in the management of stage I and II non small cell lung cancer

J Clin Oncol

Traditional versus up front [18F]fluorodeoxyglucose-positron emission tomography staging of non small cell lung cancer: A Dutch cooperative randomized study

J Clin Oncol

Preoperative staging of lung cancer with combined PET-CT

N Eng J Med

Positron emission tomography in staging early lung cancer: A randomized trial

Ann Intern Med

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

N Engl J Med

Diffusion-weighted MRI in the body: Applications and challenges in oncology

AJR Am J Roentgenol

The development of QUADAS: A tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews

BMC Med Res Methodol

Oncology/endocrine
Preoperative mediastinal and hilar nodal staging with diffusion-weighted magnetic resonance imaging and fluorodeoxyglucose positron emission tomography/computed tomography in patients with non–small-cell lung cancer: Which is better?

Traditional versus up front [¹⁸F]fluorodeoxyglucose-positron emission tomography staging of non small cell lung cancer: A Dutch cooperative randomized study