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(Chest. 2003;123:129S-136S.)
© 2003 American College of Chest Physicians

Diagnosis of Lung Cancer*

The Guidelines

M. Patricia Rivera, MD, FCCP; Frank Detterbeck, MD, FCCP and Atul C. Mehta, MD, FCCP

* From the Departments of Medicine (Dr. Rivera) and Surgery (Dr. Detterbeck), The University of North Carolina at Chapel Hill, Chapel Hill, NC; and the Department of Medicine (Dr. Mehta), The Cleveland Clinic Foundation, Cleveland OH.

Correspondence to: M. Patricia Rivera, MD, FCCP, Assistant Professor of Medicine, University of North Carolina at Chapel Hill, 420 Burnett-Womack Blvd, CB No. 7020, Chapel Hill, NC 27599; e-mail: mprivera{at}med.unc.edu


   Abstract
TOP
 Abstract
Introduction
 General Approach to Diagnosis
 Diagnosis of Primary Tumor
 Conclusion
 Summary of Recommendations
 References
 
Lung cancer is usually suspected in individuals who have abnormal chest radiograph findings or have symptoms caused by either local or systemic effects of the tumor. The method of diagnosis of suspected lung cancer depends on the type of lung cancer (ie, small cell lung cancer or non-small cell lung cancer), the size and location of the primary tumor, the presence of metastasis, and the overall clinical status of the patient. Achieving a diagnosis and staging are usually done in concert because the most efficient way to make a diagnosis often is dictated by the stage of the cancer. The best sequence of studies and interventions in a particular patient involves careful judgment of the probable reliability of a number of presumptive diagnostic issues, so as to maximize the sensitivity and to avoid performing multiple or unnecessary invasive procedures. In this article, we consider all manner of clinical presentations of lung cancer in light of currently available diagnostic procedures. Published data supporting a particular diagnostic approach is weighed based on the quality of the benefit as well as the estimated net benefit. Recommendations are graded in terms of strength to provide clinicians with guidance as to the most efficient and approach to the diagnosis of lung cancer in individual patients.

Key Words: bronchoscopy • lung neoplasm • sensitivity • specificity • sputum cytology • transthoracic needle aspiration


   Introduction
TOP
 Abstract
 Introduction
General Approach to Diagnosis
 Diagnosis of Primary Tumor
 Conclusion
 Summary of Recommendations
 References
 
The radiographic findings and clinical presentation usually allow a presumptive differentiation between small cell lung cancer (SCLC) and non-SCLC (NSCLC). Massive lymphadenopathy and direct mediastinal invasion are well-recognized phenomena in SCLC.1 2 A mass in, or adjacent to, the hilum is a particular characteristic of SCLC and is seen in about 78% of cases.1 2 Not infrequently, patients with SCLC present with paraneoplastic syndromes.3 These include the syndrome of inappropriate antidiuretic hormone, ectopic adrenocorticotrophic hormone production, and the Lambert-Eaton syndrome. If SCLC is suspected, the diagnosis should be achieved by whatever means is easiest (ie, sputum cytology, thoracentesis if an accessible pleural effusion is present, fine needle aspirate [FNA] of a supraclavicular node or metastatic site, bronchoscopy with or without transbronchial needle aspiration [TBNA] of mediastinal nodes or submucosal process). If the diagnosis of SCLC is established on a biopsy of the primary lesion, the distinction between limited or extensive disease then is made radiographically.

In patients who are suspected of having NSCLC, the method of achieving a diagnosis is usually dictated by the presumed stage of the disease. Patients with suspected lung cancer who present with a pleural effusion should undergo thoracentesis first in order to differentiate between a malignant effusion (ie, one due to malignant involvement of the pleura) and a paramalignant effusion (ie, one due to other factors such as lymphatic blockade, atelectasis, or hypoproteinemia). Distinction between the two is important because the finding of malignant cells in the pleural fluid alters the stage and treatment of the particular patient. Because pleural metastases are more common in the visceral pleura4 and tend to be focal when there is involvement of the parietal pleura, pleural fluid cytology is a more sensitive diagnostic test than percutaneous pleural biopsy, the latter being a blind sampling procedure.5 6 7 When three separate pleural fluid specimens from a patient with malignant pleural disease are submitted to an experienced cytologist, one should expect a positive diagnosis in about 80% of patients.7 8 Percutaneous, closed pleural biopsy is reported6 to be diagnostic for malignancy in about 50% of cases. Thoracoscopic biopsy of the pleura is safe and can provide a definitive diagnosis with a high degree of accuracy and minimal risk to the patient.9 10 The reported sensitivity rate is 0.80 to 1, the specificity rate is 1, and the negative predictive value is 0.93.9 11 12 13 False-negative test results are more common with mesothelioma than with primary lung carcinoma.11

Patients with metastatic NSCLC (stage IV disease) usually present with constitutional symptoms (ie, fatigue and weight loss), organ-specific symptoms (ie, bone pain and neurologic symptoms), and/or abnormal laboratory findings (ie, anemia, elevated alkaline phosphatase levels, and/or elevated liver enzyme levels). In many of these patients, a FNA or a needle biopsy of a site of metastasis represents the most efficient way both to make a diagnosis and to confirm the stage. In some cases, however, the metastatic site may be technically difficult to biopsy. If metastatic disease can be predicted with a high degree of accuracy on the basis of radiographic findings (ie, multiple brain, liver, or bone lesions), it may be more efficient to achieve a diagnosis of the primary lung lesion by whatever method is easiest for the patient (ie, sputum cytology, bronchoscopy, or transthoracic needle aspiration [TTNA]). This decision must be made by weighing the technical considerations involved in each approach as well as the reliability of diagnosing an extrathoracic lesion as a site of metastasis based on radiographic appearances alone (see the article on clinical/noninvasive staging elsewhere in this supplement). A joint decision among the radiologist, the pulmonologist, and the medical or radiation oncologist is the desirable approach.

NSCLC can present with extensive infiltration of the mediastinum. In such patients, the diagnosis should be achieved by the method that has the most favorable risk/benefit ratio. Bronchoscopy with TBNA for cytologic or histologic examination of mediastinal lymph nodes has been shown to be a safe procedure.14 15 16 17 Technical aspects that are frequently emphasized to be important in achieving a high success rate include accurate preparation of the specimen, rapid on-site evaluation by a cytopathologist, and using the larger 19-gauge needles, which provide better tissue samples for histologic evaluation.18 19 The overall sensitivity of TBNA is 0.76, and the overall specificity is 0.96.14 15 16 17 18 19 20 21 22 (The reader is referred to the article on invasive clinical staging of non-small cell lung cancer elsewhere in this supplement for a more detailed review on the performance characteristics of TBNA for staging the mediastinum.) The negative predictive value of TBNA (0.71) is not high enough to obviate the need for a further confirmation of negative results. Mediastinoscopy is warranted in patients with nondiagnostic results.

CT-guided TTNA of mediastinal masses or nodes (ie, nodes < 1.5 cm in size) can be performed safely.23 The role of TTNA in patients with extensive mediastinal disease (defined as such extensive invasion of the mediastinum by the tumor that discrete lymph nodes can no longer be discerned) is usually to confirm SCLC, or in patients with NSCLC who are not surgical candidates because of the extent of mediastinal disease.

In the case of a small (ie, < 3 cm), solitary, peripheral lung lesion that is suspicious for lung cancer in a patient who appears to have early-stage disease and is a surgical candidate, the diagnostic dilemma generally centers around whether or not to obtain a biopsy to confirm the diagnosis of cancer before surgical resection is carried out. When the lesion is moderately to highly suspicious for lung cancer, an excisional biopsy performed via thoracoscopy has a much higher sensitivity than TTNA and is the most definitive method of diagnosing a peripheral lung nodule. TTNA has no role in patients with a solitary lesion that is moderately or highly suspicious for lung carcinoma who appear to have early stage-disease and are candidates for surgical resection. (The reader is referred to the article on solitary pulmonary nodules elsewhere in this supplement for a more detailed review on the diagnostic approach to the solitary pulmonary nodule.)


   General Approach to Diagnosis
TOP
 Abstract
 Introduction
 General Approach to Diagnosis
Diagnosis of Primary Tumor
 Conclusion
 Summary of Recommendations
 References
 
Recommendations

  1. In patients suspected of having SCLC based on the radiographic and clinical findings, the diagnosis should be obtained by whatever method is easiest (ie, sputum cytology, thoracentesis, FNA, or bronchoscopy, including TBNA), as dictated by the patient’s presentation. Level of evidence, fair; benefit, moderate; grade of recommendation, B
  2. In patients suspected of having lung cancer who have an accessible pleural effusion, a definitive diagnosis of the pleural effusion via thoracentesis should be made first. Level of evidence, fair; benefit, substantial; grade of recommendation, B
  3. In a patient with an accessible pleural effusion, if pleural fluid cytology is negative (after at least two thoracentesis procedures), thoracoscopy should be performed as the next step. Level of evidence, fair; benefit, moderate; grade of recommendation, B
  4. In patients suspected of having lung cancer who have a solitary extrathoracic site suspicious of a metastasis, the diagnosis should be obtained by a fine-needle aspiration or biopsy of the distant site. Level of evidence, fair; benefit, substantial; grade of recommendation, B
  5. In patients suspected of having lung cancer who present with lesions in multiple distant sites that are typical for metastases but in whom biopsy of a metastatic site would be technically difficult, a diagnosis of the primary lung lesion should be obtained by whatever method is easiest and safest (ie, sputum cytology, bronchoscopy, or TTNA). Level of evidence, poor; benefit, moderate; grade of recommendation, C
  6. In patients suspected of having lung cancer who have no known distant metastases or pleural effusions but have extensive infiltration of the mediastinum based on radiographic studies, a diagnosis should be obtained from the mediastinal tissue by whatever method is most efficacious (ie, bronchoscopy with TBNA, TTNA, or mediastinoscopy) as dictated by the location of the tumor. Level of evidence, fair; benefit, moderate; grade of recommendation, B
  7. A patient with a solitary peripheral lesion that is even moderately suspicious for lung cancer, who appears to have early-stage disease (ie, negative findings of chest CT scan and 18F-2-fluoro-2-deoxy-D-glucose [FDG] positron emission tomography [PET] scan of the mediastinum) and is a surgical candidate, should undergo excisional biopsy and subsequent lobectomy if a resectable lung cancer is confirmed. Level of evidence, poor; benefit, substantial; grade of recommendation, C


   Diagnosis of Primary Tumor
TOP
 Abstract
 Introduction
 General Approach to Diagnosis
 Diagnosis of Primary Tumor
Conclusion
 Summary of Recommendations
 References
 
A variety of techniques (eg, sputum cytology, flexible bronchoscopy, and TTNA) are available as methods of achieving a definitive diagnosis. The selection of the most appropriate test is best performed in a multidisciplinary fashion. Four key questions on the diagnostic workup of patients with lung cancer were formulated and answered by a comprehensive review of the published literature performed by the Duke University Center for Clinical Health Policy Research. (Please refer to a previous article in this supplement entitled: "Performance Characteristics of Different Modalities for Diagnosis of Suspected Lung Cancer: Summary of Published Evidence," which hereafter is referred to as the background article, for the detailed review and tables.) The following section summarizes the results of the data and provides recommendations based on a critical review of the published evidence.

Sputum Cytology
What Are the Performance Characteristics of Sputum Cytology for the Diagnosis of Lung Cancer With Special Consideration for the Location of the Tumor? Sputum cytology is the least invasive means of obtaining a diagnosis in a patient who is suspected of having lung cancer. The diagnostic accuracy of sputum cytology is dependent on rigorous specimen sampling (at least three specimens) and preservation techniques, as well as on the location and size of the tumor (ie, central vs peripheral). Unfortunately, many institutions do not have an established program for sputum collection and processing, and therefore sputum analysis has a much lower sensitivity than that indicated in the data presented here (which come from institutions with well-established sputum analysis programs). Sputum cytology is particularly useful in patients who present with centrally located tumors (ie, SCLC or squamous call carcinoma) and in those who present with hemoptysis. The sampling of sputum specimens should certainly be the first step in a patient who presents with a central lesion with or without radiographic evidence of metastatic disease, in whom a semi-invasive procedure such as bronchoscopy or TTNA might pose a higher risk. A systematic literature review by the Duke University Center for Clinical Health Policy Research found 16 studies that provided data on the performance characteristics of sputum cytology for the diagnosis of suspected lung cancer (see Table 1 in the background article). The results of these studies revealed the average sensitivity and specificity rate of sputum cytology to be 0.66 and 0.99, respectively. Eight studies provided data on the sensitivity of prebronchoscopy sputum analysis in patients who were suspected of having lung cancer (see evidence Table 2 in the background article) and revealed a prebronchoscopy sputum sensitivity ranging from 0.10 to 0.74, with an average sensitivity of 0.22. Seventeen studies that addressed the effect of location of the lesion on the sensitivity of sputum cytology were identified (see Table 3 in the background article). The sensitivity of sputum cytology for central lesions is 0.71 and decreases to 0.49 for peripheral lesions.

Recommendations

Flexible Bronchoscopy
What Are the Performance Characteristics of Flexible Bronchoscopy and Its Ancillary Procedures for the Diagnosis of Central Tumors (Endobronchial), as Opposed to Peripheral Tumors, and to Peripheral Tumors < 2 cm and > 2 cm in Size? Flexible bronchoscopy with its attendant procedures is a valuable diagnostic procedure in the workup of a patient who is suspected of having lung cancer. A comprehensive literature search conducted by the Duke University Center for Clinical Health Policy Research revealed 44 studies, each with > 50 patients, that reported on the sensitivity of flexible bronchoscopy for the diagnosis of lung cancer.

The decision about whether to perform a diagnostic bronchoscopy for a lesion that is suspicious for lung cancer largely depends on the location of the lesion (ie, central vs peripheral). Central lesions can present as an exophytic endobronchial mass, submucosal spread, or a peribronchial tumor causing extrinsic compression. Thirty of the 44 studies that were found reported on the sensitivity of bronchoscopy for central, endobronchial lesions (see Table 4 in the background article). Among a total of 3,754 patients, the overall sensitivity of flexible bronchoscopy was 0.88. Direct forceps biopsy of visible central lesions is the technique used most frequently, and the sensitivity of this test by itself was 0.74. At least three forceps biopsies of the visible lesion are recommended. The sensitivity from washings and brushings is somewhat lower (0.48 and 0.59, respectively), but these tests often are combined with forceps biopsies. The addition of TBNA to obtain cytology or histology samples when there is submucosal tumor spread or peribronchial tumor causing extrinsic compression increases the sensitivity of bronchoscopy.24 25

Peripheral lesions are defined in most studies as lesions that are not visible in the main or lobar airways, and thus it is not surprising that the sensitivity of flexible bronchoscopy for diagnosing peripheral lung cancers is lower than that for central lesions. Thirty of the 44 studies also reported on the sensitivity of flexible bronchoscopy for peripheral lesions (see Table 5 in the background article). Among a total of 4,136 patients, the average sensitivity of flexible bronchoscopy for peripheral lesions was 0.69. A few points must be made in order to interpret the results of bronchoscopy in the diagnosis of peripheral lung cancers. First, most of the studies used fluoroscopy routinely for peripheral lesions, which increases the reported sensitivity of bronchoscopy.26 Second, the number of transbronchial biopsy samples obtained is important, with a sensitivity of 0.45 for one sample and 0.70 for six samples being reported in one study.27

The sensitivity of bronchoscopy for peripheral lesions is most affected by the size of the lesion. Eight studies that reported on the sensitivity of flexible bronchoscopy based on the size of the peripheral lesion were identified by the Duke University Center for Clinical Health Policy Research (see Table 6 in the background article). In 879 patients with lesions that were > 2 cm in size, the sensitivity of bronchoscopy was 0.62, whereas in 341 patients with lesions < 2 cm in size, the sensitivity was only 0.33. The sensitivity of bronchoscopy is reported to be higher if a CT scan shows a bronchus extending to the lesion (0.60 vs 0.25, respectively).28 29

The false-negative (FN) rate for bronchoscopy results has not yet been defined. Most clinicians would pursue the diagnosis further in the case of a nondiagnostic bronchoscopy of a visible endobronchial abnormality. The FN rate can be estimated to be fairly high in the case of peripheral lesions, especially smaller ones, because of the relative low sensitivity in this setting. Bronchoscopy has an important role in the diagnosis of benign conditions, but the chance of finding a benign condition in a patient who is clinically suspected of having lung cancer is only 1%.30

Recommendations

TTNA
What Are the Performance Characteristics for TTNA as a Diagnostic Modality With Particular Emphasis on the Size and Location of the Suspected Cancer? A meta-analysis of 47 studies and an additional 19 studies focusing on the performance characteristics of TBNA or biopsy for the diagnosis of localized pulmonary lesions were analyzed by the Duke University Center for Clinical Health Policy Research. Five studies with < 50 patients included in the meta-analysis were excluded from the final analysis (see Table 8 in the background article). Among 11,279 patients, the overall sensitivity and specificity of TTNA for diagnosing peripheral lung cancers were 0.90 and 0.97, respectively. The difference between the sensitivity of TTNA in lesions that were > 2 cm in size and those that were < 2 cm in size was not statistically different (0.95 and 0.91, respectively).

TTNA of a peripheral lung lesion can be performed under either fluoroscopic or CT scan guidance. Studies using CT scan guidance show a higher sensitivity (0.92) than those using fluoroscopy guidance (0.88). For peripheral lung lesions, the sensitivity of TTNA is higher than that of bronchoscopy. In patients who have lung cancer, TTNA has approximately a 90% chance of providing confirmation of the diagnosis. Furthermore, given the false-positive rate of 0.01 to 0.02, a TTNA result that is positive for cancer is reliable. On the other hand, the FN test result rate of TTNA is high (range, 0.20 to 0.30).31 Thus, TTNA is generally not useful in ruling out cancer. As such, TTNA has no role in patients who have lesions that are even moderately suspicious for lung cancer, and who appear to have early-stage disease and are candidates for surgical resection. Although a test that could reliably rule out lung cancer might be useful in this setting, the high FN rate of TTNA makes reliance on a negative result untenable.

Establishing a specific benign diagnosis such as tuberculosis, fungal infection, or hamartoma, using TTNA is quite valuable, particularly in patients in whom the clinical and radiologic findings strongly suggest a benign diagnosis. In such cases, a specific benign diagnosis using TTNA further decreased the risk of missing a cancer.

PET scanning using FDG has proven to be an excellent modality for evaluating solitary pulmonary nodules. In a recently published meta-analysis32 of the available data on FDG-PET scanning, the average sensitivity and specificity of FDG-PET scanning for detecting a malignancy were reported to be 0.97 and 0.78, respectively. Like any test, PET scanning has some limitations. The current generation of PET scanners can miss lesions that are < 1 cm in size,32 33 34 and FN results can occur when dealing with carcinoid tumors or bronchoalveolar carcinomas.32 34 35 False-positive results may be seen with certain inflammatory or infectious lesions such as tuberculomas, histoplasmomas, and rheumatoid nodules.32 34 (The reader is referred to the article on solitary pulmonary nodule elsewhere in this supplement for a more detailed discussion of FDG-PET scanning in the evaluation of the solitary pulmonary nodules.)

Recommendations

Cell Type Accuracy
What Is the Diagnostic Error When Differentiating Between NSCLC and SCLC Generated by Various Diagnostic Techniques (Bronchoscopy, TTNA, and Sputum Cytology)? In a patient with lung cancer, distinguishing between SCLC and NSCLC is of paramount importance as each of these cancers is treated in a radically different manner. The distinction between SCLC and NSCLC on sputum cytology, TTNA cytology, and bronchoscopic washings, brushings, and BAL cytology is quite reliable. Twenty-one studies with a total of 6,305 patients were systematically reviewed for the analysis of the diagnostic accuracy of various techniques in differentiating NSCLC from SCLC (see Table 9 in the background article). Indeed, the chance that a preoperative diagnosis of NSCLC is in error (ie, that the tumor is actually SCLC) is 0.02 (range, 0.01 to 0.07). On the other hand, the error rate of a diagnosis of SCLC (ie, that the tumor is actually NSCLC) is on average 0.09, with individual studies ranging from 0 to 0.33.

Recommendations


   Conclusion
TOP
 Abstract
 Introduction
 General Approach to Diagnosis
 Diagnosis of Primary Tumor
 Conclusion
Summary of Recommendations
 References
 
A variety of techniques is available to assist the clinician in achieving a definitive diagnosis of lung cancer. Selection of the most appropriate test is best done in a multidisciplinary fashion with input from a pulmonologist, chest radiologist, and thoracic surgeon. Furthermore, the most appropriate test is usually determined by the type of lung cancer (ie, SCLC or NSCLC), the size and location of the tumor, and the presumed stage of the cancer.

A diagnosis should be obtained by whatever method is easiest in patients who are presumed to have SCLC or who have very clear evidence of advanced NSCLC (ie, large pleural effusions or metastatic disease). Sputum cytology is a reasonable first step in patients with central lesions, but diagnostic accuracy depends of the rigorous acquisition, handling, and interpretation of samples. Flexible bronchoscopy is the most useful test for central lesions, whereas in the case of peripheral lesions, the sensitivity of TTNA is higher than that of bronchoscopy.


   Summary of Recommendations
TOP
 Abstract
 Introduction
 General Approach to Diagnosis
 Diagnosis of Primary Tumor
 Conclusion
 Summary of Recommendations
References
 
General Approach to Diagnosis

  1. In patients suspected of having SCLC based on the radiographic and clinical findings, the diagnosis should be obtained by whatever method is easiest (ie, sputum cytology, FNA, and bronchoscopy, including TBNA), as dictated by the patient’s presentation. Level of evidence, fair; benefit, moderate; grade of recommendation, B
  2. In patients suspected of having lung cancer who have an accessible pleural effusion, a definitive diagnosis of the pleural effusion via thoracentesis should be made first. Level of evidence, fair; benefit, substantial; grade of recommendation, B
  3. In a patient with an accessible pleural effusion, if the results of pleural fluid cytology are negative (after at least two thoracentesis procedures), thoracoscopy should be performed as the next step. Level of evidence, fair; benefit, moderate; grade of recommendation, B
  4. In patients who are suspected of having lung cancer and who have a solitary extrathoracic site that is suspicious of metastasis, the diagnosis should be obtained by a fine-needle aspiration or biopsy of the distant site. Level of evidence, fair; benefit, substantial; grade of recommendation, B
  5. In patients who are suspected of having lung cancer and who present with lesions in multiple distant sites that are typical for metastases, but in whom biopsy of a metastatic site would be technically difficult, a diagnosis of the primary lung lesion should be obtained by whatever method is easiest and safest (ie, sputum cytology, bronchoscopy, or TTNA). Level of evidence, poor; benefit, moderate; grade of recommendation, C
  6. In patients who are suspected of having lung cancer and who have no known distant metastases or pleural effusions but have extensive infiltration of the mediastinum based on radiographic studies, a diagnosis should be obtained from the mediastinal tissue by whatever method is most efficacious (ie, bronchoscopy with TBNA, TTNA, or mediastinoscopy) as dictated by the location of the tumor. Level of evidence, fair; benefit, moderate; grade of recommendation, B
  7. A patient with a solitary peripheral lesion that is even moderately suspicious for lung cancer, who appears to have early-stage disease (ie, negative findings on a chest CT of the mediastinum) and is a surgical candidate, should undergo excisional biopsy and subsequent lobectomy if a resectable lung cancer is confirmed. Level of evidence, poor; benefit, substantial; grade of recommendation, C

Diagnosis of Primary Tumor


   Footnotes
 
Abbreviations: FDG = 18F-2-fluoro-2-deoxy-D-glucose; FN = false negative; FNA = fine needle aspirate; NSCLC = non-small cell lung cancer; PET = positron emission tomography; SCLC = small cell lung cancer; TBNA = transbronchial needle aspiration; TTNA = transthoracic needle aspiration


   References
TOP
 Abstract
 Introduction
 General Approach to Diagnosis
 Diagnosis of Primary Tumor
 Conclusion
 Summary of Recommendations
 References
 

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