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Published online before print October 19, 2007, 10.1148/radiol.2453062116
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(Radiology 2007;245:881-887.)
© RSNA, 2007

Thoracic Imaging

Pulmonary Nodules: 3D Volumetric Measurement with Multidetector CT—Effect of Intravenous Contrast Medium1

Osamu Honda, MD, PhD, Takeshi Johkoh, MD, PhD, Hiromitsu Sumikawa, MD, Atsuo Inoue, MD, PhD, Noriyuki Tomiyama, MD, PhD, Naoki Mihara, MD, PhD, Yuka Fujita, MD, Mitsuko Tsubamoto, MD, PhD, Masahiro Yanagawa, MD, Tadahisa Daimon, MD, Javzandulam Natsag, MD, and Hironobu Nakamura, MD, PhD

1 From the Departments of Radiology (O.H., H.S., A.I., N.T., N.M., Y.F., M.T., M.Y., T.D., J.N., H.N.) and Medical Physics (T.J.), Osaka University Graduate School of Medicine, 1-7 Yamadaoka, Suita, Osaka 565-0871, Japan. From the 2006 RSNA Annual Meeting. Received December 12, 2006; revision requested February 13, 2007; revision received March 10; accepted March 23; final version accepted May 22. Address correspondence to O.H. (e-mail: ohonda{at}radiol.med.osaka-u.ac.jp).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATION FOR PATIENT CARE
 References
 
Purpose: To retrospectively evaluate the effect of contrast medium on the three-dimensional volumetric measurement of pulmonary nodules.

Materials and Methods: The study was approved by the local institutional review committee, with waiver of informed consent. Sixty pulmonary nodules in 60 patients (17 women, 43 men; age range, 29–82 years) were imaged before and after administration of contrast medium with a 64-channel multidetector computed tomographic (CT) scanner; reconstructed images with a section thickness of 0.625 mm were obtained by using a bone algorithm and a standard algorithm. Volumetric measurements of pulmonary nodules were performed by using commercially available software, and the postcontrast volume ratio was calculated by dividing the postcontrast volume by the precontrast volume. Precontrast and postcontrast volumes were then analyzed by using a Wilcoxon signed rank test.

Results: The median measured volumes of pulmonary nodules were 817 mm3 (precontrast imaging, bone algorithm), 887 mm3 (postcontrast imaging, bone algorithm), 812 mm3 (precontrast imaging, standard algorithm), and 855 mm3 (postcontrast imaging, standard algorithm). The measured volumes obtained with the bone algorithm were significantly larger than those obtained with the standard algorithm, both before and after administration of contrast medium (P < .01); with both the standard algorithm and the bone algorithm, the measured postcontrast volumes were significantly larger than the precontrast volumes (P < .01). The postcontrast volume ratio was more than 1.0 in 45 cases (75%) when the bone algorithm was used and in 53 cases (88%) when the standard algorithm was used. The mean postcontrast volume ratio was 1.054 with the bone algorithm and 1.065 with the standard algorithm.

Conclusion: The measured volume of pulmonary nodules obtained by using three-dimensional volumetric software increased after administration of contrast medium. Moreover, the measured volume of pulmonary nodules that was obtained with the bone algorithm was larger than that obtained with the standard algorithm, regardless of whether contrast medium was used.

© RSNA, 2007


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATION FOR PATIENT CARE
 References
 
The pulmonary nodule is a common finding at computed tomography (CT) that may be due to primary or secondary malignancy but also to benign conditions, including granulomatous diseases and other infectious processes. The morphologic imaging diagnosis of a pulmonary nodule can be performed, with special attention paid to the nodule's margin or internal structure and to its relationships to surrounding structures (1–3). In addition, the degree of enhancement or the pattern of enhancement seen with administration of contrast medium at CT is useful for differentiating malignant from benign nodules (4–6). If a pulmonary nodule might be malignant, further examination with, for example, positron emission tomography (PET), PET/CT, biopsy, or CT is performed. At follow-up CT, it is important to determine whether the pulmonary nodule has grown and, if so, how fast it has grown. The doubling time of a pulmonary nodule is one of the clues used to differentiate malignant from benign nodules; the majority of malignant pulmonary nodules double in volume between 20 and 400 days (7).

Two-dimensional CT measurement is not reliable in the evaluation of small, noncalcified pulmonary nodules (8). However, three-dimensional (3D) volumetric measurement software is now available, and the volumes of a pulmonary nodule can be objectively measured with CT (9,10). Three-dimensional volumetric measurement enables calculation of the doubling time of pulmonary nodules more accurately than can two-dimensional CT, thereby improving diagnosis (11,12). However, there are some limitations to correctly measuring the volume of pulmonary nodules—namely, the reconstruction algorithm, the tube current-time product, the section thickness, and the segmentation threshold (13,14). Moreover, to our knowledge, the effect of contrast medium on 3D volumetric measurement has not been reported. The purpose of our study, therefore, was to retrospectively evaluate the effect of contrast medium on the 3D volumetric measurement of pulmonary nodules.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATION FOR PATIENT CARE
 References
 
Patients
This retrospective study was approved by the local institutional review committee, with waiver of informed consent. CT images obtained in 60 patients (43 men, 17 women; mean age, 62.1 years; age range, 29–82 years) who underwent CT between August 2005 and February 2006 were evaluated. CT was performed for clinical indications in all patients. Nodules found at CT were included in our retrospective study. Patients who underwent CT only with or only without administration of contrast medium were excluded from this study. All patients had one or more pulmonary nodules less than 3 cm in diameter at CT, and postcontrast CT scans had been obtained just after precontrast CT scans. We performed precontrast CT to assess calcification and postcontrast CT to assess lymphadenopathy and nodule enhancement and/or to enable CT angiography. That is why we repeated chest CT with contrast medium just after performing precontrast CT. Data in patients with ground-glass nodules or part-solid nodules were not included in this study. Nodules that contained calcification or cavities were also excluded.

We enrolled 60 patients with 60 nodules during a 7-month period, and no patients were excluded. The 60 pulmonary nodules consisted of pulmonary metastases (n = 35), lung cancer (n = 10), and nodules of unknown etiology (n = 15). Of the 45 patients who received a diagnosis, the diagnosis was based on surgery in 13 patients, transbronchial biopsy in six patients, CT-guided needle biopsy in two patients, and clinical course in 24 patients. All diagnoses based on clinical course were pulmonary metastases, and pulmonary nodules showed interval growth at sequential scanning.

Contrast Medium
The types, total amount, and injection rates of the contrast medium varied because CT was performed not only for patients known or suspected to have nodules but also for patients with incidental pulmonary nodules. Ioversol (Optiray 320 [320 mg iodine per milliliter]; Yamanouchi, Tokyo, Japan) was used in 22 patients, and iohexol (Omnipaque 300 [300 mg iodine per milliliter]; Daiichi, Tokyo, Japan) was used in 38 patients. The total amount of contrast medium ranged from 40 to 150 mL (mean, 91.4 mL ± 19.5 [standard deviation]), and the injection rate ranged from 0.7 to 3 mL/sec. Contrast medium was administered through a 20- to 22-gauge needle, which was placed into a superficial vein in the antecubital fossa or forearm. The contrast medium was administered by using a power injector (Dual Shot GX; Nemoto Kyorindo, Tokyo, Japan). The scan delay also varied, ranging from 25 to 65 seconds (mean, 59.2 seconds ± 8.3).

Acquisition of CT Images
CT images were acquired by using 64-channel multidetector CT scanners (LightSpeed VCT; GE Healthcare, Milwaukee, Wis). Whole-lung CT images before and after administration of contrast medium were obtained with the following parameters: detector collimation, 0.625 mm; field of view, 34.5 cm; pitch, 1.375; gantry speed, 0.4 second per rotation; automatic selection of the milliampere setting (range, 128–750 mA); and noise index, 10. The target nodules were retrospectively selected from precontrast CT images with 5-mm section thickness, and image reconstructions were performed for the target nodules from both precontrast and postcontrast CT data. If a patient had more than one nodule, the largest nodule less than 3 cm in diameter was selected as a target nodule.

Target nodules were selected and reconstructed by one investigator (O.H., who had 10 years of experience with interpretation of thoracic CT images). The target nodules were placed in the center of the reconstruction area on the z-axis and in the x-y plane; thus, the reconstructed images were obtained in a range sufficient to contain the target nodules. The CT images were reconstructed with a 9.6-cm field of view, 0.625-mm section thickness, and 0.625-mm reconstruction interval from the original scan data. Both the bone algorithm (high-spatial-frequency algorithm) and the standard algorithm (low-spatial-frequency algorithm) were used for image reconstruction.

The bone algorithm has been recommended for the evaluation of pulmonary nodules because it helps improve the spatial resolution and delineation of nodule structure (15). On the other hand, the standard algorithm is useful in evaluating the inner part of the nodule because use of the bone algorithm can lead to erroneous diagnosis of calcification because of edge-enhancement artifacts, especially in a small uncalcified nodule (16). In addition, the standard algorithm is commonly used to evaluate nodule enhancement caused by contrast medium (17). Thus, we used two reconstruction algorithms in our study.

Analysis of CT Images
All reconstructed thin-section CT images were transferred to a workstation (Advantage Workstation 4.2; GE Healthcare), and the volumetric measurements were then automatically obtained by using CT lung analysis software (ALA: Advanced Lung Analysis; GE Healthcare). This software segments images of pulmonary nodules by combining watershed segmentation and shape-analysis techniques (9). The postcontrast volume ratio was calculated by dividing the postcontrast volume by the precontrast volume.

The nodule diameters were measured to investigate the influence of nodule size on the postcontrast volume ratio. With use of the bone algorithm, the short- and long-axis diameters of each nodule were measured on the workstation by using the lung window setting (width, 1200 HU; level, –700 HU). Those diameters were measured on the section with the largest cross-sectional area according to the workstation ruler. The attenuation values of the pulmonary nodules were also measured on the workstation by using thin-section CT images reconstructed with both the bone algorithm and the standard algorithm. The difference in attenuation between the precontrast and the postcontrast images for each pulmonary nodule was quantified in Hounsfield units by one investigator (O.H.). The region-of-interest diameters were approximately 70% of the lung nodule's short- and long-axis diameters, as measured at mediastinal window settings (width, 300 HU; level, 10 HU) on transverse images (5). The attenuation values of the main pulmonary artery and left atrium were also quantified on postcontrast CT images (section thickness, 5 mm) obtained with the standard algorithm. For measurement of these attenuation values, the images that showed the largest areas of the main pulmonary artery or left atrium were selected. The region-of-interest diameters were approximately 70% of the short-axis diameters of the main pulmonary artery or left atrium.

Statistical Analysis
Because the measured volumes did not follow normal distribution, nonparametric tests were used in this study. The Wilcoxon signed rank test was used to compare the measured pulmonary nodule volumes obtained with both the bone algorithm and the standard algorithm. In addition, Bland-Altman analysis was used to determine the agreement between the bone algorithm and the standard algorithm for both precontrast and postcontrast nodule volumes (18). The nodule volumes measured before and after contrast medium administration were also analyzed by using the Wilcoxon signed rank test. Simple linear regression analysis was used to evaluate the correlation between the postcontrast volume ratio of the bone algorithm and that of the standard algorithm.

The Spearman rank correlation coefficient was used to evaluate the correlation between the postcontrast volume ratio and the attenuation values of the pulmonary artery or left atrium. Correlation between the postcontrast volume ratio and either the diameter or the degree of enhancement of pulmonary nodules was also evaluated with the Spearman rank correlation coefficient. Statistical software (StatMate II; ATMS, Tokyo, Japan) was used to perform analysis. P < .05 was considered to indicate a significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATION FOR PATIENT CARE
 References
 
Median Volumes
The median volumes of pulmonary nodules (Table) measured with the volumetric software were 817 mm3 (precontrast imaging, bone algorithm; volume range, 29–7043 mm3), 887 mm3 (postcontrast imaging, bone algorithm; volume range, 32–7087 mm3), 812 mm3 (precontrast imaging, standard algorithm; volume range, 25–6998 mm3), and 855 mm3 (postcontrast imaging, standard algorithm; volume range, 29–7052 mm3). With the bone algorithm, the mean increased volume after administration of contrast medium was 50 mm3 ± 104 (range, –144 to 546 mm3). With the standard algorithm, the mean increased volume after administration of contrast medium was 58 mm3 ± 112 (range, –39 to 757 mm3). The measured volumes obtained with the bone algorithm were significantly larger than those obtained with the standard algorithm both before (P < .01) and after (P < .01) administration of contrast medium. The measured volumes at postcontrast imaging were significantly larger than those at precontrast imaging for both the bone algorithm (P < .01) and the standard algorithm (P < .01) (Fig 1).


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  		Nodule Volumes according to 3D Volumetric Measurement

 

Figure 1
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  		Figure 1: A, D, Transverse CT images obtained without administration of contrast medium and with, A, the bone algorithm and, D, the standard algorithm show solid nodule (located at anatomic level for both A and D). B, C, E, and F show volume-rendered images of the same solid nodule. B, Image reconstructed from precontrast data with bone algorithm. C, Image reconstructed from postcontrast data with bone algorithm. E, Image reconstructed from precontrast data with standard algorithm. F, Image reconstructed from postcontrast data with standard algorithm. Surface of the nodule seen with the standard algorithm (E, F) is smoother than that seen with the bone algorithm (B, C). According to the software, measured nodule volumes were 1073 mm3 (B), 1165 mm3 (C), 1054 mm3 (E), and 1147 mm3 (F). The volume obtained with the bone algorithm is larger than that obtained with the standard algorithm, and the volume obtained with administration of contrast medium is larger than that obtained without administration of contrast medium.

 
The agreement between the bone algorithm and the standard algorithm for both precontrast (Fig 2) and postcontrast (Fig 3) CT was determined by using the Bland-Altman method. At precontrast CT, the mean difference between the measured volume obtained with the bone algorithm and that obtained with the standard algorithm was 33 mm3. The limits of agreement were –107 and 172 mm3. At postcontrast CT, the mean difference between the measured volume obtained with the bone algorithm and that obtained with the standard algorithm was 24 mm3. The limits of agreement were –115 and 163 mm3. We found that the difference in measured volume between the bone and the standard algorithms could go in either direction, and the difference between the two algorithms was large for both precontrast and postcontrast CT.


Figure 2
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  		Figure 2: Graph shows results of Bland-Altman analysis of nodule volumes obtained with bone and standard algorithms at precontrast CT. Y-axis shows difference between nodule volumes obtained with the bone algorithm and those obtained with the standard algorithm; x-axis shows mean volumes. Dashed line = mean difference in volume, dotted-and-dashed line = mean difference ± 2 standard deviations (SDs).

 

Figure 3
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  		Figure 3: Graph shows results of Bland-Altman analysis of nodule volumes obtained with bone and standard algorithms at postcontrast CT. Y-axis shows difference between nodule volumes obtained with the bone algorithm and those obtained with the standard algorithm; x-axis shows mean volumes. Dashed line = mean difference in volume, dotted-and-dashed line = mean difference ± 2 standard deviations (SDs).

 
Volume Ratios
The postcontrast volume ratio (postcontrast nodule volume divided by precontrast nodule volume) was more than 1.0 in 75% (45 of 60) of nodules assessed with the bone algorithm and in 88% (53 of 60) of nodules assessed with the standard algorithm (Fig 4). The mean postcontrast volume ratio obtained with the bone algorithm was 1.054 ± 0.10 (range, 0.913–1.434). The mean postcontrast volume ratio obtained with the standard algorithm was 1.065 ± 0.089 (range, 0.881–1.471). According to simple regression analysis, the postcontrast volume ratio obtained with the bone algorithm correlated significantly with the ratio obtained with the standard algorithm (r = 0.612; P < .01) (Fig 4).


Figure 4
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  		Figure 4: Scatterplot shows correlation between postcontrast volume ratio obtained with the bone algorithm and that obtained with the standard algorithm. The postcontrast volume ratio obtained with the bone algorithm was more than 1.0 in 45 of 60 cases (75%), whereas that obtained with the standard algorithm was more than 1.0 in 53 of 60 cases (88%). The solid line is the linear regression line given by the expression y = 0.468 + (0.567 · x) (r = 0.612; P < .01).

 
Attenuation in Main Pulmonary Artery and Left Atrium
The mean attenuation of the main pulmonary artery with administration of contrast medium was 263 HU ± 69 (range, 129–502 HU). The mean attenuation of the left atrium was 240 HU ± 54 (range, 135–389 HU). Neither the postcontrast volume ratio obtained with the bone algorithm nor that obtained with the standard algorithm correlated significantly with the attenuation value of the pulmonary artery (bone algorithm, P = .74; standard algorithm, P = .79) or the attenuation value of the left atrium (bone algorithm, P = .92; standard algorithm, P = .36).

Nodule Diameter
The mean short-axis diameter of the pulmonary nodules was 10.0 mm ± 4.5 (range, 3.7–22.4 mm). The mean long-axis diameter was 12.4 mm ± 5.6 (range, 4.1–29.1 mm). Neither the postcontrast volume ratio obtained with the bone algorithm nor that obtained with the standard algorithm correlated significantly with the short-axis diameter (bone algorithm, P = .64; standard algorithm, P = .37) or the long-axis diameter (bone algorithm, P = .32; standard algorithm, P = .45) of the pulmonary nodules.

Enhancement
For each pulmonary nodule, the mean degrees of enhancement were 30.9 HU ± 31.4 (range, –14 to 208 HU) with the bone algorithm and 29.4 HU ± 31.4 (range, –19 to 198 HU) with the standard algorithm. Neither the postcontrast volume ratio obtained with the bone algorithm nor that obtained with the standard algorithm correlated significantly with the degree of enhancement for each pulmonary nodule (bone algorithm, P = .62; standard algorithm, P = .92).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
 IMPLICATION FOR PATIENT CARE
 References
 
In our study, the measured pulmonary nodule volumes obtained with postcontrast CT were significantly larger than those obtained with precontrast CT using 3D measurement. The reasons for this are unknown, but there are two possibilities: enhancement of the nodule itself and enhancement of the structures surrounding the nodule. We measured the attenuation values of the inner parts of the pulmonary nodules before and after administration of contrast medium and found that the postcontrast volume ratio was not related to the degree of enhancement of the pulmonary nodule. However, the peripheral attenuation value of a pulmonary nodule is more important than the inner attenuation for the segmentation of pulmonary nodules when 3D volumetric measurement is used. If the peripheral part of the nodule is enhanced with contrast medium, the difference in the attenuation value between the pulmonary nodule and the pulmonary parenchyma becomes larger, and the segmentation border may shift to the outer border of the nodule. Peripheral enhancement of the pulmonary nodule may make the measured volume larger. Further investigation is required to explain the relationship between nodule enhancement and the measured volume.

The structures surrounding the nodule are also important factors that affect the outcome of the 3D volumetric measurement. The presence of vessels around a nodule has been shown to lead to an increase in the mean absolute error of volumetric measurement in a chest phantom study (19). When the nodules were located adjacent to blood vessels, segmentation of the nodules became more difficult, and it was assumed that the volumes measured with 3D imaging contained parts of blood vessels (19). With use of contrast medium, the attenuation value of blood vessels increases, and, thus, 3D volumetric measurement software may depict increased nodule volume by including the enhanced vessels that were not included as part of the nodule at precontrast CT.

The bone (high-spatial-frequency) algorithm is recommended for 3D measurement of pulmonary nodule volume. It has been reported that nodule volume measured on images reconstructed with the bone algorithm is more precise than that measured on images reconstructed with the standard (low-spatial-frequency) algorithm (14). In our study, the measured volumes obtained with the bone algorithm were larger than those obtained with the standard algorithm not only before but also after administration of contrast medium. It is speculated that this phenomenon is related to the attenuation value of the nodule edge. The software we used for 3D nodule measurement utilized watershed segmentation and shape-analysis techniques (9). With the bone algorithm, the edge of the pulmonary nodule has a high attenuation value and a sharp margin, and the calculated volume is more precise. With the standard algorithm, however, the edge of the pulmonary nodule is less well defined and the segmented margin can shift inward. This shifting, in turn, leads to a smaller volume than that obtained with the bone algorithm.

Our study had some limitations. CT was performed for clinically indicated reasons in all patients, and the protocols for administration of contrast medium varied: Two types of contrast medium were used, and the amount and the injection rate of contrast medium differed. To avoid the effects of these differences, we measured the CT attenuation of the main pulmonary artery and the left atrium and evaluated the interaction between the attenuation of these structures and the measured nodule volumes. It is presumed that the attenuation of the pulmonary vessels and pulmonary parenchyma around a pulmonary nodule are important for the change in measured nodule volume. However, it is difficult to precisely measure the CT attenuation of small pulmonary vessels or pulmonary parenchyma around a nodule. In our study, the measured nodule volume obtained with the bone algorithm increased after administration of contrast medium by a mean of 5.4%, whereas that obtained with the standard algorithm increased by a mean of 6.5%. In one study of eight nodules, the pulmonary nodule volume on a delayed scan showed a mean 2.0% decrease and the volume on further delayed scans showed a 7.2% decrease after administration of contrast medium (20). Although the degree of the change in measured nodule volume might be affected by the method of contrast medium administration, the nodule volumes obtained with 3D volumetric measurement will increase after administration of contrast medium.

Another limitation was that the CT images were obtained with only one CT scanner, and we used only one type of software. We do not know whether our findings are generalizable to other scanners and software.

In summary, the pulmonary nodule volume calculated with 3D volumetric software is significantly larger after administration of contrast medium. In addition, the measured volume of pulmonary nodules assessed with the bone algorithm is larger than that assessed with the standard algorithm at 3D volumetric measurement, not only before but also after administration of contrast medium. Therefore, care should be taken in the use of contrast medium and in the choice of reconstruction algorithm when follow-up CT is performed to evaluate the interval change in nodule size with 3D volumetric measurement.


   ADVANCES IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
IMPLICATION FOR PATIENT CARE
 References
 


   IMPLICATION FOR PATIENT CARE
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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATION FOR PATIENT CARE
References
 


   FOOTNOTES
 

Abbreviations: 3D = three-dimensional

Guarantor of integrity of entire study, O.H.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, O.H.; clinical studies, O.H., H.S., A.I., N.T., N.M., Y.F., M.T., M.Y., T.D., J.N.; experimental studies, O.H.; statistical analysis, O.H.; and manuscript editing, O.H., T.J., H.N.

Authors stated no financial relationship to disclose.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 IMPLICATION FOR PATIENT CARE
 References
 

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