Small Pulmonary Nodules: Our Preliminary Experience in Volumetric Analysis of Doubling Times

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1 Small Pulmonary Nodules: Our Preliminary Experience in Volumetric Analysis of Doubling Times Andrea Borghesi, MD Davide Farina, MD Roberto Maroldi, MD Department of Radiology University of Brescia Brescia, Italy Corresponding author: Andrea Borghesi, MD Department of Radiology University of Brescia Piazzale Spedali Civili Brescia, Italy aborghesi@sirm.org Introduction Pulmonary nodules are a frequent incidental finding in chest computed tomography (CT), but their prevalence in the general population is not known precisely [1, 2]. With the improvement in resolution and broad availability of multi-detector row CT (MDCT), an increasing number of small pulmonary nodules are being detected. Although many of these small pulmonary nodules are benign (i.e. hamartoma, granuloma), nodules frequently remain undetermined. In fact, only fully calcified and fat-containing nodules can be considered benign lesions. The goal of the radiological evaluation of small solitary pulmonary nodules is to differentiate benign from malignant lesions noninvasively and as accurately as possible. Contrast-enhanced CT is applicable for the diagnosis of nodules larger than 5 mm, but its specificity is only 58% [3]. Fluorine-18 FDG PET is inaccurate for the diagnosis of nodules smaller than 10 mm in diameter [4, 5]. Moreover, less than 1% of nodules smaller than 5 mm and 23% of those between 5 and 10 mm are malignant [6]. For these reasons, in small, noncalcified, undetermined pulmonary nodules, the only indicator of malignancy is growth rate (i.e. doubling time). It is estimated that the doubling time of malignant tumors is generally between 30 and 500 days, with a mean of 100 days [7]. In other words, if growth is detected (i.e. doubling time < 500 days), the nodule should be studied by means of percutaneous biopsy, videothoracoscopy or thoracic surgery. The determination of growth rate by comparing size on current and prior images is an important and cost-effective step in the evaluation of small pulmonary nodules. Changes of the maximal transverse diameter of the nodule, as detected on 2D images, are used to estimate the growth rate between the previous CT scan and the follow-up study. A limitation of this type of measurement is the possibility of asymmetric growth, resulting in minimal changes in the maximal diameter but in increase of the overall volume of the lesion. Moreover, manual measurements of small nodules are not sufficiently reproducible. To overcome these limitations, it has been proposed that the growth rate in small nodules be assessed using serial volume measurements rather than diameter [8] (Figure 1).

2 Figure 1: 64-year-old woman with three pulmonary nodules. SAT module evaluation of a nodule in the left upper lobe. Top left: Global view providing the location of the nodules: the one under analysis is marked with a pink circle, the other nodules are marked with green circles. Top right and bottom right panels show the nodule under analysis on coronal MPR and axial scan images. Bottom left: Three-dimensional surface-shaded rendering. The purpose of our study was to evaluate the accuracy of software-calculated growth rate of small pulmonary nodules for differentiating benign from malignant nodules. We assessed nodule volume doubling time using the Aquarius Workstation from TeraRecon, Inc. (San Mateo, CA, U.S.A.). Materials and Methods The study population consisted of 29 (19 men and 10 women) non-consecutive patients who were identified with a keyword search in our departmental PACS from November, 2006 to September, We selected only solid, noncalcified nodules with a diameter between 4 and 15 mm. Groundglass opacities were discarded. This study was retrospective and did not affect patient management. Age of the patients ranged from 47 to 82 years, with a mean of 63 years. Nine of the 29 patients were heavy smokers. In 11/29 (38%) of the patients, chest CT had been performed during follow-up of thoracic or extrathoracic malignancies, while 18/29 (62%) of the patients had been scanned for non-neoplastic lesions (i.e. emphysema, pulmonary embolism, cardiomyopathy or thoracic aortic aneurysm). An overall number of 40 small, noncalcified nodules were found in 29 patients; 21/29 (73%) had one nodule, 6/29 (20%) had two nodules, 1/29 (3%) had three nodules and 1/29 (3%) had four nodules.

3 All patients underwent chest CT using a 16 multi-detector row CT scanner with a collimation of 16 x 0.75 mm. Thin sections (with 1 mm slice thickness) were reconstructed with an increment of 0.75 mm by using a high-resolution reconstruction algorithm with standardized window level and width settings for the lung parenchyma. The same technique was applied for baseline and follow-up CT studies. The nodule volume doubling time was calculated on the Aquarius Workstation (TeraRecon, Inc.) with the segmentation, analysis and tracking (SAT) module. The SAT module is used to segment, analyze and track pulmonary nodules. To calculate pulmonary nodule volume using SAT, the New Findings button was selected and the nodule center was marked with a mouse click. The goal of this evaluation was to use the software to compare nodule volumes between the baseline and follow-up CT scans and to calculate doubling time when growth was detected (Figures 2 and 3). If nodule volume decreased, the doubling time could not be calculated (Figure 4). On the basis of the literature [9], we considered a doubling time of less than 500 days indicative of a malignant lesion. Conversely, nodules were considered benign when they were decreased in size, unchanged or showed a doubling time greater than 500 days at the follow-up CT. Figure 2: Small nodule in a 64-year-old man, heavy smoker. Top left: Unenhanced CT shows 5.99 mm nodule with smooth margins in the middle lobe. Bottom left: Threedimensional surface-rendering from baseline CT. Top and bottom right: On follow-up CT examination, acquired 473 days later, a small increase in size (3%) is demonstrated (estimated doubling time of more than 28 years) suggesting benign nature.

4 Figure 3: 67-year-old man treated for a laryngeal neoplasm 11 years prior. Top: Transverse CT images from baseline (left) and 103-day follow-up scans (right). Bottom: Nodule segmentation from baseline and follow-up scans. Relative volume variation is only 1% (estimated doubling time of 7647 days) suggesting benign nature.

5 Figure 4: Small nodule in a 57-year-old man. Transverse CT images from baseline (left) and 180-day follow-up scans (right). Volumetric nodule reduction (2%) is demonstrated. Results Segmentation was successful for all nodules. The maximum diameter of 40 noncalcified, undetermined, pulmonary nodules selected on the baseline CT scans ranged from 4.59 mm to mm (mean = 7.46 mm). Nodule volumes ranged from 36.9 mm 3 to mm 3 (mean = 184 mm 3 ). Two nodules were smaller than 5 mm; 31 ranged between 5 mm and 10 mm, seven were greater than 10 mm. The interval between the baseline and the last follow-up CT scan ranged from 95 to 1139 days with a mean of 369 days and a median of 301 days. Volume increased in 19/40 (47.5%) of the nodules (the relative variation ranged from 1% to 201%); in these cases, the software-calculated doubling time ranged between 96 and days (mean = 4227 days; median = 3094 days). Two nodules remained unchanged at 95 and 539 days, respectively. Volume decreased in 19/40 (47.5%) of the nodules (the relative variation ranged from 1 to 15%). On the basis of doubling time, 5/40 (12.5%) of the nodules were considered potentially malignant; in these cases, the software-calculated doubling time ranged between 96 and 335 days (mean = days). A pathologic diagnosis (based on surgical specimens) was obtained only in four nodules (Table). In one nodule measuring mm ( mm 3 ) at baseline CT, with a doubling time of 96 days, a final diagnosis of pulmonary adenocarcinoma was rendered (Figure 5). Two nodules measuring 4.99 mm (44.67 mm 3 ) and 5.1 mm (61.65 mm 3 ) at baseline CT, with a doubling time of 312 and

6 284 days respectively, turned out to be non-neoplastic intrapulmonary lymph nodes (IPLNs) (Figure 6). IPLNs are found along the subpleural lymphatic chain, usually located inferior to the carina; they may increase in size over time [10] and thus be confused with metastatic or primary lung cancer in up to 18% of cases [11]. The fourth nodule measuring 14.2 mm ( mm 3 ) at follow-up CT was incorrectly considered increased in size (solely on the basis of 2D measurement) and surgically removed. In this case, pathologic analysis showed a hamartoma. In fact, retrospective 3D evaluation of the nodule showed decreased volume (Figure 7). The diagnosis of another nodule (diameter = mm) considered benign on the basis of doubling time (2492 days) was confirmed using PET- CT (no FDG uptake) (Figure 8). TABLE Nodule type Diameter (mm) Volume (mm 3 ) Followup (day) Size (increased/ decreased) Volume variation (%) Doubling time (days) Benign increased IPLN* Final Diagnosis Benign increased IPLN* Benign decreased 1 - Hamartoma Malignant increased Pulmonary adenocarcinoma *IPLN: Intrapulmonary Lymph Node Figure 5: 68-year-old man who received left upper lobe resection for pulmonary adenocarcinoma four years earlier. Transverse CT images from baseline (left) and 153- day follow-up scans (right). The SAT module calculated a doubling time of 96 days, suggesting malignancy. The nodule was surgically removed and proved to be a metachronous pulmonary adenocarcinoma.

7 Figure 6: 69-year-old woman already treated for a pulmonary malignancy. Transverse CT images from baseline (left) and 328-day follow-up scans (right). The SAT module calculated a relative volume variation of 123% (estimated doubling time of 284 days) suggesting malignancy. The nodule was surgically removed, and pathologic analysis revealed an intrapulmonary lymph node (IPLN).

8 Figure 7: 54-year-old woman, smoker. Baseline (left) and 98-day follow-up (right) CT scans. The SAT module revealed volumetric nodule decrease in spite of increase in 2D size. The final diagnosis on pathologic examination was hamartoma.

9 Figure 8: 66-year-old man, smoker. Transverse CT images from baseline (left) and 182- day follow-up (right) scans. The SAT module calculated a relative volume variation of 5% (estimated doubling time of 2492 days) suggesting benign nature. This was confirmed by PET-CT (no FDG uptake). Conclusion The characterization of small, noncalcified, pulmonary nodules remains a diagnostic challenge for the radiologist. Generally, they are monitored by means of CT follow-up and considered malignant when significant growth is demonstrated over time. Increase in size of the nodule can be demonstrated by measuring its maximal diameter on 2D images; however, this is not sufficiently reproducible to detect small variations. Moreover, manual measurements may be extremely imprecise, especially when performed on small nodules with only minimal growth. An alternative approach is to measure volumetric changes with the aid of software-calculated growth rate. This automated 3D measurement is more reproducible [12], though it may be influenced by the respiratory phase. With the aid of the Aquarius Workstation (TeraRecon, Inc.) with the SAT module, we have calculated the doubling time retrospectively of 40 random, noncalcified, small pulmonary nodules. The SAT module is an extremely intuitive and user-friendly interface that allows data to be obtained easily and quickly. In our preliminary experience, the mean time to perform 3D measurements and compare nodule volumes on baseline and follow-up CT scans was never greater than 5 minutes. Though the number of nodules evaluated is low, our results demonstrate that the SAT module provides reliable and reproducible calculations of the volume of small nodules, in

10 agreement with previous literature reports [13]. Three-dimensional volumetric measurement with the SAT module has the potential to modify the decision-making algorithms for the management of small pulmonary nodules detected with MDCT. References 1. Henschke CI, McCauley DI, Yankelevitz DF, et al. Early Lung Cancer Action Project: overall design and findings from baseline screening. Lancet 1999; 354: Swensen SJ, Jett JR, Sloan JA, et al. Screening for lung cancer with low-dose spiral computed tomography. Am J Respir Crit Care Med 2002; 165: Swensen SJ, Viggiano RW, Midthun DE, et al. Lung nodule enhancement at CT: multicenter study. Radiology 2000; 214: Detterbeck FC, Falen S, Rivera MP, Halle JS, Socinski MA. Seeking a home for a PET: part 1. Defining the appropriate place for positron emission tomography imaging in the diagnosis of pulmonary nodules or masses. Chest 2004; 125: Nomori H, Watanabe K, Ohtsuka T, Naruke T, Suemasu K, Uno K. Evaluation of F-18 fluorodeoxyglucose (FDG) PET scanning for pulmonary nodules less than 3 cm in diameter, with special reference to the CT images. Lung Cancer 2004; 45: Henschke CI, Yankelevitz DF, Naidich DP, et al. CT screening for lung cancer: suspiciousness of nodules according to size on baseline scans. Radiology 2004; 231: Geddes DM. The natural history of lung cancer: areview based on rates of tumour growth. Br J Dis Chest 1979; 73: Yankelevitz DF, Reeves AP, Kostis WJ, Zhao B, Henschke CI. Small pulmonary nodules: volumetrically determined growth rates based on CT evaluation. Radiology 2000; 217: Hasegawa M, Sone S, Takashima S, et al. Growth rate of small lung cancers detected on mass CT screening. Br J Radiol 2000; 73: Houk ZN, Osborne DP, Subvisceral pleural lymph node presenting as an expanding intrapulmonary nodule. Am Rev Respir Dis 1965; 91: Bankoff MS, McEniff NJ, Bhadelia RA, et al. Prevalence of pathologically proven intrapulmonary lymph nodes and their appearance on CT. AJR 1996;167: Revel MP, Lefort C, Bissery A, et al. Pulmonary nodules: preliminary experience with three-dimensional evaluation. Radiology 2004; 231: Revel MP, Merlin A, Peyrard S, Triki R, Couchon S, Chatellier G, Frija G. Software volumetric evaluation of doubling times for differentiating benign versus malignant pulmonary nodules. AJR Am J Roentgenol Jul;187(1):135-42

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