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Thoracic Imaging |
1 From the Dept of Diagnostic Radiology (S.J.S., T.E.H.) and Div of Pulmonary and Critical Care Medicine and Internal Medicine (D.E.M.), Mayo Clinic and Mayo Foundation, 200 First St SW, Rochester, MN 55905; Div of Pulmonary Medicine (R.W.V.), Dept of Diagnostic Radiology (J.R.M.), and Section of Biostatistics (A.L.W.), Mayo Clinic Scottsdale, Ariz; Dept of Diagnostic Radiology, Vancouver General Hospital, British Columbia, Canada (N.L.M.); Dept of Diagnostic Radiology, Memorial Medical Center, Springfield, Ill (A.S.); Dept of Diagnostic Radiology, Shiga Health Insurance Hospital, Otsu, Japan (K.Y.); Dept of Diagnostic Radiology, New York University Medical Center, NY (D.P.N.); Dept of Diagnostic Radiology, Duke University Medical Center, Durham, NC (E.F.P.). Supported in part by grants from GE Medical Systems, Bracco Diagnostics, and the Mayo Foundation. Recd Sept 22, 1998; revision reqd Nov 10; final revision recd Apr 15, 1999; accepted Apr 22. Address reprint requests to S.J.S.
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Abstract |
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 TOP Abstract IntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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15 HU) at computed tomography (CT) is strongly predictive of benignity. MATERIALS AND METHODS: Five hundred fifty lung nodules were studied. Of these, 356 met all entrance criteria and had a diagnosis. On nonenhanced, thin-section CT scans, the nodules were solid, 5–40 mm in diameter, relatively spherical, homogeneous, and without calcification or fat. All patients were examined with 3-mm-collimation CT before and after intravenous injection of contrast material. CT scans through the nodule were obtained at 1, 2, 3, and 4 minutes after the onset of injection. Peak net nodule enhancement and time-attenuation curves were analyzed. Seven centers participated.
RESULTS: The prevalence of malignancy was 48% (171 of 356 nodules). Malignant neoplasms enhanced (median, 38.1 HU; range, 14.0–165.3 HU) significantly more than granulomas and benign neoplasms (median, 10.0 HU; range, -20.0 to 96.0 HU; P < .001). With 15 HU as the threshold, the sensitivity was 98% (167 of 171 malignant nodules), the specificity was 58% (107 of 185 benign nodules), and the accuracy was 77% (274 of 356 nodules).
CONCLUSION: Absence of significant lung nodule enhancement (15 HU) at CT is strongly predictive of benignity.
Index terms: Lung, CT, 60.12112, 60.12115 • Lung, nodule, 60.281 • Lung neoplasms, CT, 60.12112, 60.12115 • Lung neoplasms, diagnosis, 60.30
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Introduction |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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There are distinct differences in the vascularity and vasculature of benign and malignant modules (6–19). These differences may offer an opportunity to distinguish benign from malignant lung nodules by using radiologic imaging technology. Researchers have shown, with every modality at their disposal, that lung malignancies enhance more than benign lung nodules. This has been shown with angiography (8,11,12,15,20), contrast material–enhanced conventional tomography (21), 2-[fluorine 18]fluoro-2-deoxy-D-glucose positron emission tomography (PET) (22–25), gadolinium-enhanced magnetic resonance imaging (26,27), Doppler ultrasonography (28,29), and contrast-enhanced computed tomography (CT) (30–32). Others have shown that differential nodule enhancement may help to distinguish benign from malignant lesions in the breast (33,34), adrenal gland (35), and kidney (36). Are any of these techniques accurate enough in distinguishing benign from malignant lung nodules to be clinically useful?
A multicenter study was organized to test the following hypothesis: Absence of significant lung nodule enhancement (15 HU) at CT is strongly predictive of benignity.
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MATERIALS AND METHODS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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On nonenhanced, thin-section CT images, the nodules were solid, relatively spherical, homogeneous, and without calcification or fat. They were solitary on chest radiographs but not necessarily on CT images. Nodules measured 5 mm or larger in diameter. The diameter was calculated as a mean of the short- and long-axis diameters at lung-window settings on transverse CT images. All patients were examined with 3-mm-collimation CT before and after the administration of contrast material (2 mL/sec; 300 mg of iodine per milliliter; 420 mg of iodine per kilogram of body weight). A 15-mm z-axis cluster of scans was obtained through the nodule at 1, 2, 3, and 4 minutes after the onset of injection. Peak nodule enhancement and time-attenuation curves were analyzed.
The nodules had to be relatively spherical (ie, short- and long-axis diameters were within a factor of 2 of each other). Nodules were excluded if they had calcification or fat on thin-section (1–3-mm-collimation) CT images (2,37–39). In the judgment of the attending radiologist (including S.J.S., N.L.M., A.S., K.Y., D.P.N., E.F.P., T.E.H., J.R.M.), there was no substantial CT artifact in the region of the nodule (eg, cardiac motion artifact or beam-hardening artifact from adjacent bone). All nodules were relatively homogeneous on preenhancement sections (Fig 1) in the judgment of the attending radiologist (ie, no signs of necrosis, cavitation, calcification, or a low signal-to-noise ratio) (40). Recent (<1-month) transthoracic needle aspiration biopsy of the nodule was an exclusion criterion, because postbiopsy hemorrhage in theory could result in decreased enhancement, which would lead to false-negative results.
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Studies were performed with a HiSpeed Advantage (GE Medical Systems, Milwaukee, Wis) (n = 222), CT-Twin/RTS (Elscint, Hackensack, NJ) (n = 134), or Quantex (GE-Yokogama Medical Systems, Tokyo, Japan) (n = 25) scanner.
Preenhancement analysis consisted of analysis of 3-mm-collimation spiral scans (pitch, 1:1) obtained through the entire nodule. After the administration of contrast material, serial, 5-second, 3-mm-collimation spiral acquisitions were performed at 1-minute intervals, beginning 1 minute after injection onset, for a total of four acquisitions. The following technique was used: 3-mm-collimation spiral scanning with 2-mm reconstruction intervals, 120 kVp, 280 mA, pitch of 1:1, 5-second scanning time, standard reconstruction algorithm, and 15-cm field of view.
We compared the median preenhancement attenuation among three groups: (a) malignant neoplasms, (b) granulomas and benign nodules at observation, and (c) benign neoplasms and other benign nodules.
The dose of iodinated, low-osmolarity, nonionic contrast material administered intravenously was based on patient weight (Table 1). All patients were carefully instructed by a technologist or radiologist (including S.J.S., N.L.M., A.S., K.Y., D.P.N., E.F.P., T.E.H., J.R.M.) that it was important to reproduce precisely the same degree of inspiration. Patients were instructed to "take a small breath in and hold it."
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The region-of-interest diameters were approximately 70% of the lung nodule's short- and long-axis diameters as measured at mediastinal window settings on transverse images. All Hounsfield unit measurements were performed on mediastinal-window images to ensure that partial volume averaging was minimized.
The circular or oval region of interest was centered on the image closest to the nodule equator. The nodule equator was identified by using lung-window settings in which small vessels could be visualized and could be used to locate the same z-axis level for the multiple, serial Hounsfield unit measurements. Nodule enhancement was defined as the difference between the maximum mean Hounsfield unit nodule measurement in the 4 minutes after contrast material administration and the preenhancement mean Hounsfield unit nodule measurement.
For the lung nodule enhancement on the CT study to be considered technically adequate, the following criteria had to be met: (a) no sign at physical examination that there was contrast material extravasation at the site of injection, (b) assessment by a radiologist that there was appropriate enhancement of cardiovascular structures imaged during examination, (c) no clinically important patient reaction to contrast material administration that interfered with image acquisition, (d) administration of the correct dose of contrast material, and (e) satisfactory patient breath holding and respiratory registration so that artifact-free images were produced through the nodule equator. Meticulous attention to the details of this CT enhancement technique was critical.
On the basis of our previous work, we considered a nodule that enhanced 15 HU or less to have not enhanced significantly (32). This was an indication to us that the nodule was likely benign, probably a granuloma.
If any of the images obtained after the injection of contrast material showed enhancement of greater than 15 HU, we considered the examination to be adequate and the nodule to have enhanced significantly. For a nodule to be given an enhancement value of less than or equal to 15 HU, nodule-enhancement images had to be available from each of the 4 minutes after the injection of contrast material. For example, if nodule-enhancement measurements at 1, 3, and 4 minutes after the injection of contrast material were all less than 15 HU but no measurement was available at 2 minutes after injection because of respiratory misregistration or artifact, the entire study was considered technically inadequate. We did this because the peak enhancement theoretically could have been missed at 2 minutes after injection, and the nodule could have been misclassified as "likely benign."
The clinical histories of all patients were reviewed subsequently to determine whether a clinical or histologic diagnosis had been made. Nodules were classified as malignant only if this diagnosis was confirmed histologically or cytologically. All bronchial carcinoid tumors and fibrous tumors of the pleura were classified as malignancies (41). All benign neoplasms (hamartomas) were diagnosed histologically. Nodules were classified as granulomas if this diagnosis was confirmed histologically or if there was radiologic evidence of no growth during at least 2 years of surveillance (2,37,38,42,43).
One hundred sixty-nine of the 550 patients were excluded. We were unable to obtain a clinical or a histologic diagnosis of the nodule in 147 patients, because the surveillance was less than 2 years, the patient was no longer being treated at the respective institution and could not be contacted, or the diagnosis could not be verified after death. These patients were excluded from statistical analysis.
In 19 patients, studies were technically inadequate because the breath hold was inconsistent after injection. No serious reactions to contrast material occurred. One examination was interrupted because of a minor reaction.
One patient was excluded because an incorrect dose of contrast material was administered. The patient weighed 133.9 kg and received an injection of 100 mL of nonionic contrast material. The correct dose should have been 175 mL (Table 1). This patient's 2-cm nodule enhanced 14.3 HU. The diagnosis was melanoma metastasis.
One patient was excluded because the nodule diameter was 3 mm, the same as the CT collimation.
One other patient was excluded because transthoracic needle aspiration biopsy of the nodule recently had been performed. This undiagnosed nodule is being managed with observation. It enhanced 15 HU.
Two patients had multiple examinations performed at different times. Only the first of these was included.
The 25 patients in Shiga, Japan, were examined by using a different enhancement protocol. After the injection of contrast material, images were obtained at 30, 120, and 300 seconds. Because no images were obtained at 60, 180, and 240 seconds after injection, we chose to analyze these data separately.
Thus, there was a clinical or histologic diagnosis and a technically adequate study of lung nodule enhancement in 356 patients.
To analyze the statistical significance and clinical relevance of the data, we divided the patients into two groups: patients with malignant neoplasms and patients with granulomas or benign neoplasms. The distributions of enhancement and diameters were compared for the two groups by using the Wilcoxon rank sum test because the distributions of these variables were nongaussian. The 
2 test was used to analyze nodule distribution. The Spearman rank correlation test was used to compare nodule diameter and enhancement at CT.
Sensitivity, specificity, accuracy, and positive and negative predictive values were calculated, with an enhancement level of greater than 15 HU signifying a positive test result. "Sensitivity" was defined as the percentage of patients with malignant neoplasms who had a level of enhancement greater than 15 HU; "specificity" was defined as the percentage of patients with granulomas or benign neoplasms who had a level of enhancement of 15 HU or less. Ninety-five percent CIs for these diagnostic characteristics were calculated by using an exact method for obtaining a CI for a binomial parameter (44).
Receiver operating characteristic analysis summarized the usefulness of enhancement as a marker for malignant neoplasms (vs granulomas and benign neoplasms). Estimates of the area (and its standard error) under the receiver operating characteristic curves for the current and previously reported series were made with nonparametric methods, which require no distributional assumptions (45). The area measurements obtained from two independent samples were compared by calculating the critical ratio z score, Area1 - Area2/[SE(Area1 - Area2)], where SE is standard error, and by comparing the critical ratio with the table of the normal distribution.
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RESULTS |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The enhancement, preenhancement attenuation, location, and diameter of all nodules are summarized in Table 3. On the basis of the results of the Wilcoxon rank sum test, the median enhancement (Fig 2) and median diameter of the malignant neoplasms were significantly higher than those of the granulomas and benign neoplasms (38.0 vs 10.0 HU, P < .001; 17 vs 13 mm, P < .001, respectively). There was no significant difference between the preenhancement attenuation of benign nodules and that of malignant nodules (Wilcoxon rank sum test [two-sided], P = .244). Malignant nodules were located in the upper lobe more often than were benign nodules (2 test, P = .001).
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level of .05.
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A comparison of the areas under the receiver operating characteristic curves for the current series (area, 0.831 ± 0.023) (Fig 4) and a previously reported series (32) (area, 0.879 ± 0.046) showed no significant difference (P = .351).
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We analyzed the degree of enhancement at each 1-minute interval for the 319 nodules with data recorded at every interval. The profiles of benign and malignant nodules were not significantly different (Fig 5). We found that to maximize sensitivity, enhancement must be measured at each of the four 1-minute intervals (Table 6).
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DISCUSSION |
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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15 HU) at CT is strongly predictive of benignity. We found that our protocol allows satisfactory measurement of the enhancement of pulmonary nodules (5–40 mm in diameter) with iodinated contrast material. Malignant nodules enhanced significantly more than granulomas and benign neoplasms (median enhancement, 38.1 vs 10.0 HU, respectively; P < .001). In the 8 years from August 1989 to June 1997, 626 nodules were evaluated in the current and previous studies (30,32). On the basis of the results of the Wilcoxon rank sum test, the median enhancement and median diameter of the nodules and the median age of patients with malignant neoplasms were significantly greater than those of patients with granulomas and benign neoplasms (40.0 vs 10.0 HU, P < .001; 17 vs 12 mm, P < .001; and 67 vs 64 years, P < .001, respectively).
Yamashita et al (31) reported results of lung nodule enhancement at CT that are similar to ours, even though they examined a different patient population. None of their 18 cases of lung cancer enhanced less than 25 HU. The 10 granulomas and three of four hamartomas in their study enhanced less than 15 HU. Zhang and Kono (46) also reported corroborating results. They found that peak enhancement levels were significantly higher for malignant (42 HU) and inflammatory benign (44 HU) nodules than for non-inflammatory benign nodules (13 HU).
Results of the lung nodule enhancement technique appear to be generalizable. Histoplasmosis, coccidioidomycosis, and tuberculous granulomas appear to have similar lung nodule enhancement characteristics. Younger granulomas with active inflammatory changes generally enhance substantially more than 15 HU. As they mature and become less active and more necrotic, their vascular stroma recedes and they enhance less (Figs 7, 8). We found no significant difference in the precontrast attenuation among lung nodule diagnoses (Fig 6). A small proportion of lung nodules had negative Hounsfield unit values before the administration of contrast material. We speculate that this may be secondary to differences in calibration between scanners at the seven institutions where the study was performed. Another consideration is that some nodules in truth had an attenuation lower than that of water, perhaps from necrosis or a less compact tissue structure. We do not believe that any difference in calibration would have affected the measurement of enhancement, however.
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It appears that comparable results are attainable with 2-[18F]fluoro-2-deoxy-D-glucose PET (48). Because of its inability to depict calcification, limited availability, and expense, use of that modality for initial evaluation of an indeterminate lung nodule is unrealistic.
It is possible that a bias inherent in the study method has led to an underestimation or overestimation of the accuracy of this research. Our previous (32) and present findings show (a) that nodules ultimately diagnosed as benign are more likely to be managed with radiologic observation than with biopsy or surgery and (b) that nonenhancing nodules are more likely to be managed with observation than with intervention. One hundred forty-seven nodules in this cohort are being managed with observation rather than intervention. A disproportionate number of these nodules (71 of 147) enhanced 15 HU or less. We believe that most of the 147 nodules are benign, given stability for periods of less than 2 years, even though they are still radiologically indeterminate. However, it is possible that some of the nonenhancing nodules that are being observed or that were lost to follow-up are, in fact, malignant (ie, false-negative).
It is also possible that a bias inherent in the CT enhancement measurement technique increased the frequency of diagnoses made for enhancing versus nonenhancing nodules and thus affected the accuracy. For 19 nodules, examinations were technically inadequate because of respiratory misregistration. Each of these 19 nodules had net enhancement values of 15 HU or less but did not have adequate equatorial measurements from each of the 4 minutes after injection, and they were therefore excluded. This bias, like the first one acknowledged, disproportionately excluded nonenhancing nodules, some of which could have been malignant.
Four of the 356 study results were false-negative. Case 1 was a 27-mm, left upper lobe primary adenocarcinoma in a 72-year-old man that had a net enhancement value of 14 HU.
Case 2 was a 15-mm, right upper lobe lung adenocarcinoma recurrence in a 71-year-old woman (Fig 1a). Its net enhancement value was 14 HU. The histologic appearance was consistent with lymphangitic metastasis. It had a zone of central necrosis (Fig 1b). Histologically, there was little vascular stroma, which may have been a factor in its relatively low enhancement value (32).
Case 3 was an 11-mm, left upper lobe primary squamous cell carcinoma in a 60-year-old woman that had a net enhancement value of 15 HU.
Case 4 was an 18-mm, right lower lobe squamous cell carcinoma metastasis from a laryngeal primary in a 71-year-old man. Its net enhancement value was 14 HU. There was a second laryngeal metastasis that was studied during the same CT examination that had a net enhancement value of 42 HU.
On the basis of previous findings of lung nodule enhancement at CT (30–32), we prospectively selected 15 HU as the threshold for a positive diagnosis. If we retrospectively select a threshold of 10 HU, the following calculations are obtained: sensitivity, 100% (171 of 171; 95% CI: 97.9%, 100%); specificity, 50.3% (93 of 185; 95% CI: 42.8%, 57.7%); accuracy, 74.2% (264 of 356; 95% CI: 69.3%, 78.6%); positive predictive value, 65.0% (171 of 263; 95% CI: 58.9%, 70.8%); negative predictive value, 100% (93 of 93; 95% CI: 96.1%, 100%). To further minimize the likelihood that a malignant lesion will be classified as benign with this technique, it may be most prudent to use 10 HU as the threshold for a positive diagnosis.
With spiral CT, it is now possible to perform both the lung nodule enhancement technique and an optimally enhanced CT examination of the chest and the abdomen with the same injection of contrast material. To do this, we obtained a spiral series of scans through the chest after a delay of 20 seconds from the onset of the injection of contrast material. Then, at 1 minute after injection onset, we obtained 5 seconds of 3-mm-collimation spiral images through the nodule, with a 1-mm reconstruction interval. Between acquisition of the 1- and 2-minute scans of the nodule, we obtained spiral images through the lower part of the chest and the upper part of the abdomen. This allowed scanning of the liver during optimal enhancement. Finally, the spiral sections through the nodule were obtained at 2, 3, and 4 minutes after injection onset. It was possible to perform CT with this sequence without tube overheating. The majority of the patients were able to tolerate the injection and breath-holding regimen.
We found this method to be useful to optimize CT staging of the chest and abdomen in patients with indeterminate nodules when there was a clinical suspicion of primary lung cancer. The combination of enhanced CT of the chest and abdomen with the lung nodule enhancement protocol did not add expense or substantial time (<5 min) to the complete examination.
The low false-negative rate of the results of the CT nodule enhancement technique is potentially valuable in the treatment of patients. A primary objective is to avoid misclassifying malignant lesions as benign. A nonenhancing lung nodule could be managed with radiologic surveillance alone (in a supportive clinical situation). Enhancing nodules, with the associated higher likelihood of malignancy, could be managed with biopsy or surgical removal. Because of the relatively low specificity, enhancing nodules may be appropriately managed with radiologic surveillance in a clinical situation where the physician's clinical suspicion is extraordinarily low.
It may be most prudent to use the CT lung nodule enhancement technique for nodules with a diameter of 2.0 cm or less. Smaller nodules have a higher likelihood of benignity (49), result in more difficulty in obtaining biopsy specimens successfully (50), and are less likely to contain substantial regions of necrosis (40).
The CT lung nodule enhancement technique may be clinically useful in the evaluation of radiologically indeterminate lung nodules. Absence of significant enhancement is strongly predictive of benignity.
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Footnotes |
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Author contributions: Guarantor of integrity of entire study, S.J.S.; study concepts and design, S.J.S.; definition of intellectual content, S.J.S.; literature research, S.J.S.; clinical studies, all authors; data acquisition, all authors; data analysis, S.J.S., A.L.W.; statistical analysis, S.J.S., A.L.W.; manuscript preparation, editing, and review, all authors.
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TOPAbstractIntroductionMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) on a nodule. The region of interest is positioned centrally, and its shape approximates that of the nodule on the cross-sectional image. Its net enhancement value was 14 HU. This was one of the four false-negative results. (b) Photomicrograph of this adenocarcinoma shows an appearance consistent with lymphangitic metastasis. Note the central zone of necrosis (arrows). There is little vascular stroma, which may have been a factor in its relatively low enhancement value. (Antibody to factor VIII-associated antigen; original magnification, x50.)
