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Three-dimensional Human Airway Segmentation Methods for Clinical Virtual Bronchoscopy 1 Atilla P. Kiraly, MS, William E. Higgins, PhD, Geoffrey McLennan, MD, PhD Eric A. Hoffman, PhD, Joseph M. Reinhardt, PhD Rationale and Objectives. The segmentation of airways from CT images is a critical first step for numerous virtual broncho- scopic (VB) applications. Automatic or semiautomatic methods are necessary, since manual segmentation is prohibitively time consuming. The methods must be robust and operate within a reasonable time frame to be useful for clinical VB use. The au- thors developed an integrated airway segmentation system and demonstrated its effectiveness on a series of human images. Materials and Methods. The authors’ airway segmentation system draws on two segmentation algorithms: (a) an adaptive region-growing algorithm and (b) a new hybrid algorithm that uses both region growing and mathematical morphology. Images from an ongoing VB study were segmented by means of both the adaptive region-growing and the new hybrid methods. The segmentation volume, branch number estimate, and segmentation quality were determined for each case. Results. The results demonstrate the need for an integrated segmentation system, since no single method is superior for all clin- ically relevant cases. The region-growing algorithm is the fastest and provides acceptable segmentations for most VB applica- tions, but the hybrid method provides superior airway edge localization, making it better suited for quantitative applications. In addition, the authors show that prefiltering the image data before airway segmentation increases the robustness of both region- growing and hybrid methods. Conclusion. The combination of these two algorithms with the prefiltering options allowed the successful segmentation of all test images. The times required for all segmentations were acceptable, and the results were suitable for the authors’ VB applica- tion needs. Key Words. Bronchi, CT; bronchoscopy; computed tomography (CT), image processing; computed tomography (CT), three- dimensional; trachea, CT. © AUR, 2002 New multidetector spiral CT scanners can produce three- dimensional (3D) volumetric images of the human airway tree consisting of hundreds of two-dimensional (2D) sec- tions (1,2). A typical 3D image can include 400 or more 512 512 0.6-mm sections. Such images provide an ex- cellent basis for virtual bronchoscopy (VB) applications (3–15) and quantitative airway analysis (8,16 –20). New VB methods also allow for live guided nodule and lymph node biopsies (13,15). A critical first step in these VB applications is the segmentation of the airway tree. Man- ual interactive segmentation has been applied in some cases, but routine manual analysis is impractical for the large 3D images arising from the new scanners (21,22). A variety of semiautomatic airway segmentation techniques have been proposed, but none have been conclusively proved adequate for very large, high-resolution, 3D CT chest images (4,20 –30). Acad Radiol 2002; 9:1153–1168 1 From the Departments of Computer Science and Engineering (A.P.K., W.E.H.), and Electrical Engineering (W.E.H.), Penn State University, Univer- sity Park, Pa; and Departments of Radiology (W.E.H., E.A.H.), Internal Med- icine (G.M.), and Biomedical Engineering (E.A.H., J.M.R.), University of Iowa, 1402 SC, Iowa City, IA 52242. Received June 10, 2002; revision re- quested June 19; revision received and accepted July 9. Supported in part by grants CA74325 and CA91534 from the National Cancer Institute, by National Science Foundation grant 0092758, by a Biomedical Engineering Research Grant from the Whitaker Foundation, and by a National Institutes of Health Bioengineering Research Partnership (NIH-HL-064368). Address correspondence to J.M.R. © AUR, 2002 1153

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Page 1: Three-dimensional Human Airway Segmentation Methods for ... · Three-dimensional Human Airway Segmentation Methods for Clinical Virtual Bronchoscopy1 Atilla P. Kiraly, MS, William

Three-dimensional Human Airway SegmentationMethods for Clinical Virtual Bronchoscopy1

Atilla P. Kiraly, MS, William E. Higgins, PhD, Geoffrey McLennan, MD, PhDEric A. Hoffman, PhD, Joseph M. Reinhardt, PhD

Rationale and Objectives. The segmentation of airways from CT images is a critical first step for numerous virtual broncho-scopic (VB) applications. Automatic or semiautomatic methods are necessary, since manual segmentation is prohibitively timeconsuming. The methods must be robust and operate within a reasonable time frame to be useful for clinical VB use. The au-thors developed an integrated airway segmentation system and demonstrated its effectiveness on a series of human images.

Materials and Methods. The authors’ airway segmentation system draws on two segmentation algorithms: (a) an adaptiveregion-growing algorithm and (b) a new hybrid algorithm that uses both region growing and mathematical morphology. Imagesfrom an ongoing VB study were segmented by means of both the adaptive region-growing and the new hybrid methods. Thesegmentation volume, branch number estimate, and segmentation quality were determined for each case.

Results. The results demonstrate the need for an integrated segmentation system, since no single method is superior for all clin-ically relevant cases. The region-growing algorithm is the fastest and provides acceptable segmentations for most VB applica-tions, but the hybrid method provides superior airway edge localization, making it better suited for quantitative applications. Inaddition, the authors show that prefiltering the image data before airway segmentation increases the robustness of both region-growing and hybrid methods.

Conclusion. The combination of these two algorithms with the prefiltering options allowed the successful segmentation of alltest images. The times required for all segmentations were acceptable, and the results were suitable for the authors’ VB applica-tion needs.

Key Words. Bronchi, CT; bronchoscopy; computed tomography (CT), image processing; computed tomography (CT), three-dimensional; trachea, CT.© AUR, 2002

New multidetector spiral CT scanners can produce three-dimensional (3D) volumetric images of the human airwaytree consisting of hundreds of two-dimensional (2D) sec-

tions (1,2). A typical 3D image can include 400 or more512 � 512 0.6-mm sections. Such images provide an ex-cellent basis for virtual bronchoscopy (VB) applications(3–15) and quantitative airway analysis (8,16–20). NewVB methods also allow for live guided nodule and lymphnode biopsies (13,15). A critical first step in these VBapplications is the segmentation of the airway tree. Man-ual interactive segmentation has been applied in somecases, but routine manual analysis is impractical for thelarge 3D images arising from the new scanners (21,22). Avariety of semiautomatic airway segmentation techniqueshave been proposed, but none have been conclusivelyproved adequate for very large, high-resolution, 3D CTchest images (4,20–30).

Acad Radiol 2002; 9:1153–1168

1 From the Departments of Computer Science and Engineering (A.P.K.,W.E.H.), and Electrical Engineering (W.E.H.), Penn State University, Univer-sity Park, Pa; and Departments of Radiology (W.E.H., E.A.H.), Internal Med-icine (G.M.), and Biomedical Engineering (E.A.H., J.M.R.), University ofIowa, 1402 SC, Iowa City, IA 52242. Received June 10, 2002; revision re-quested June 19; revision received and accepted July 9. Supported in partby grants CA74325 and CA91534 from the National Cancer Institute, byNational Science Foundation grant 0092758, by a Biomedical EngineeringResearch Grant from the Whitaker Foundation, and by a National Institutesof Health Bioengineering Research Partnership (NIH-HL-064368). Addresscorrespondence to J.M.R.

© AUR, 2002

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We present an integrated airway segmentation systemthat includes both region-growing and mathematical mor-phology segmentation algorithms. Our system includes ahybrid method (31) that gives results equivalent to a pre-viously proposed morphology-only approach (22) butgreatly reduces the time required for segmentation. Thehybrid method is based on the results of both region-growing and morphology approaches. We present a com-parison study of the underlying image processing algo-rithms in our segmentation system. This study reveals thata small amount of filtering applied before segmentationcan greatly increase the robustness of all methods in thecase of patient breathing artifacts, stent distortion, andpartial volume artifacts. We will also illustrate the utilityof 3D airway segmentation in VB-assisted peripheral nod-ule analysis and review the airway segmentation problemand previously proposed segmentation methods.

A 3D CT image of the chest, I, comprises a stack of Zcontiguous sections. Each section consists of Xsize � Ysize

voxels (typically 512 � 512). Each voxel (x, y, z) hasintensity value I(x, y, z) and spacing (�x, �y, �z). Thehuman airway tree appears on a 3D image as a set ofconnected, dark, branching tubular structures that tend todecrease in diameter as the branching progresses. CT im-ages are reasonably well calibrated, such that air is atapproximately �1,000 HU (ie, I [x, y, z] � �1,000 for apure air voxel [x, y, z]) while water is at 0 HU. Soft tis-sues, such as those in the mediastinum, are situated inthe range of �100 to 200 HU, and dense bone is near1,000 HU.

Airway-tree segmentation is a challenging problem forseveral reasons. While airway voxels are generally near�1,000 HU, noise and partial volume effects make it im-possible to use a simple threshold to identify all airwayvoxels within an image (18). Whenever mixtures of dif-ferent tissue types comprise a voxel, intermediate gray-level values are the result (32). Voxels straddling air andairway walls typically have values well above �1,000HU. These partial voxels can be resolved into tissue com-ponents through statistical methods (32–35). Moreover,due to the size of the voxel, thin or stenosed airways canappear broken or discontinuous. Finally, image recon-struction artifacts, such as those introduced when a sharphigh-frequency kernel is used, may cause the airways toappear discontinuous (36). Such discontinuities may causeproblems during the segmentation, resulting in both un-der- and oversegmentation errors.

Previously proposed airway segmentation methodshave employed four strategies: (a) knowledge-based tech-

niques (21,23,37), (b) region growing (4,24,25,30,38),(c) central-axis analysis (20,27), and (d) mathematicalmorphology (22,26,28,29). The technique proposed bySonka et al (21,23) uses an anatomic knowledge basedescribing structural relationships between airways andneighboring pulmonary vessels. Initially, 3D seeded re-gion growing is used to identify large airways. Theknowledge-based rules are applied to the image on a sec-tion-by-section basis. A fuzzy logic approach was lateradded by Park et al (37) to improve specificity. Neithermethod was tested on human data. More robust (lessknowledge-dependent) methods exist.

Region-growing-based methods use voxel connectivityand a threshold to identify regions, usually through 26-connectivity (4,24,25,30,38). Summers et al (4) use 3Dseeded region growing and a manually selected thresholdto segment airways for rendering. Schlatholter et al (38)also use a set threshold in addition to other parameters toperform a type of 3D seeded region growing. Region-growing fronts are checked to prevent parenchymal leak-age. The algorithm proposed by Mori et al (25) uses anadaptive 3D region-growing algorithm that automaticallydetermines a threshold through repeated segmentations.Wood et al (24) also employ 26-connected region grow-ing in conjunction with a global threshold as a basis forairway segmentation. Law and Heng (30) use adaptive 3Dregion growing but add a genetic algorithm to identify thecenter of the trachea automatically.

Although 3D region growing is extremely fast, it suf-fers from partial volume effects and noise due to theglobal threshold used during segmentation. The “optimal”thresholds differ for large versus small airways because ofthese factors. The resultant segmentation tends to lackfiner details of the airways and contains rough edges. Allof these similar methods can either lose details, depictincomplete structures, or suffer from parenchymal leakage(“explosion”) to varying degrees.

Segmentation algorithms based on central axis analysisdepend on central axis estimates for computing the seg-mentation (20,27). The segmentation technique proposedby Swift et al (20,27) performs a central axis computationas a basis for airway segmentation. This computation be-gins with a manually selected root site. The surface of anellipsoid positioned at this site is then sampled to deter-mine more sites or to detect the end of a branch. The pro-cess is then repeated for each new site. Further processingproduces a complete central axis tree. Bronchial walls arethen detected along this tree via thresholding. Finally, theunified results of this process determine the segmented

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airway tree. The disadvantage of this method is the criti-cal dependence on the central axis analysis results, whichmay be imperfect or fail for several reasons. Concernsinclude complex dependencies of initial parameters andstopping criteria and the possibility of forming paths out-side the airways.

The field of mathematical morphology involves image-processing operations that focus on shape and gray-scaleproperties (39,40). Airway segmentation methods thatdraw on mathematical morphology tend to have two ormore processing phases (22,26,28,29). First, candidateairways are detected by means of various morphologicoperations. Next, 3D relationships and shape characteris-tics help determine the true airways from false candidates.Bilgen et al (22) proposed an algorithm based on binaryand gray-scale morphologic operations. Two-dimensionaloperators of varying sizes are applied to each section ofthe image to identify candidate airways. Next, false candi-dates are eliminated through 3D reconstruction. Pisupatiet al (26) proposed a similar technique that uses the sameprinciples to detect both pulmonary arteries and veins.Preteux et al (28) use a method based on a combinationof morphologic filtering, connection cost-based marking,and conditional watershed techniques to segment thebronchi of sheep lungs. Three-dimensional tree recon-struction was not considered, since the primary focus was2D airway detection.

Extending this work to 3D airway segmentation andreconstruction, Fetita and Preteux (29) have proposedmethods that use more complex morphologic operationsin addition to fractal analysis of candidate regions. Anupdated selective marking and depth-constrained connec-tion cost operator is used to identify possible airways.

Valid candidates are identified through a 3D reconstruc-tion procedure involving model-based aggregation andfractal analysis. While these methods are promising, theircomputation time tends to be inordinate, particularly forreal clinical scenarios. Variations in the properties of themorphologic operators directly affect the candidates deter-mined. In addition, the reconstruction process, once can-didates are defined, can be complex and unestablished.Further, these methods have received little or no testingon large high-resolution 3D CT chest volumes.

We present a segmentation system that includes adap-tive 3D region growing and mathematical morphology togive fast, robust methods for 3D airway-tree segmentationfor chest CT images.

This article describes our airway segmentation system,presents results obtained by applying our system to hu-man CT data, compares these results with other methods,and demonstrates virtual bronchoscopic (VB) analysis forbronchoscopic planning in a peripheral nodule case.

MATERIALS AND METHODS

This section describes our integrated 3D airway seg-mentation system, which allows the user to choose fromthree segmentation methods: (a) adaptive 3D regiongrowing, (b) morphologic based segmentation, and (c) thehybrid method, which combines features of the other twomethods. Figure 1 shows a layout of these componentalgorithms and how they comprise the system. Adaptivelung region definition and region growing are describedfirst. We will then describe the other two methods and theimage acquisition protocol for our test images.

Lung Region DefinitionThe lungs are identified on the 3D CT image with a

simplified version of the method of Hu et al (41). In thatmethod, lung segmentation is performed in three steps toproduce separated left and right lungs with smoothboundaries. We used a simplified algorithm since we didnot need precise results but only a bounding region forthe lungs.

Lung region definition begins with the determinationof a threshold to use for region growing at the root site.This threshold is large enough that the 3D region growingencompasses the entire lungs. The initial threshold, T0, isset to �1,000 HU. An iterative procedure then determinesthe final threshold. The segmentation threshold at step i,Ti, is used to separate the entire image into voxels greater

Figure 1. System diagram of the hybrid and region-growing air-way segmentation algorithms.

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than Ti and those less than or equal to Ti. The new thresh-old, Ti�1, is set to

Ti�1 ��b � �n

2,

where �b and �n represents the mean gray level of thevoxels greater than Ti and that of all other voxels, respec-tively. This procedure is repeated until the condition Ti �Ti�1 is met. The lung region is then identified by meansof 3D region growing from the root site with threshold Ti.

Adaptive Region GrowingA robust adaptive 3D region-growing method provides

an airway segmentation option in addition to identifyingregions of the image containing the large airways for thehybrid method. We increased the robustness of themethod described in reference 25 to provide good resultsfor a wide variety of images. This section first describesadaptive 3D region growing and then describes our modi-fications to improve robustness.

Three-dimensional region growing uses a threshold Tand a root site (xr, yr, zr) to determine which voxels areadded to the segmentation. In adaptive region growing, anoptimal T is found by repeating 3D region growing withincreasing values of T. For airway segmentation, thethreshold eventually becomes high enough that the regiongrowing breaks through the bronchial wall and enters thelung parenchyma. The total volume V of the segmentationis computed each time the 3D region growing is per-formed, so the breakthrough can be detected by means ofa sharp increase in the volume, or explosion, and deter-mined by a preset value called the explosion parameter,E, set to a value below the expected volume after explo-sion.

Let I be the original gray-scale image, and let IR(x, y,z) � 0, @(x, y, z) � IR. IR will contain the output of the3D region-growing segmentation. Let N26(x, y, z) be the26-connected neighborhood of the voxel (x, y, z), and letT be the region-growing threshold. Given the root site,(xr, yr, zr), each neighbor (x, y, z) � N26(xr, yr, zr) suchthat I(x, y, z) � T and IR(x, y, z) � 1 is added to the seg-mentation; that is, we set IR(x, y, z) � 1. As each voxel isadded, its neighbors are also processed in this fashion.This procedure is repeated until no new voxels are addedto IR. Then the volume V of this segmentation is com-puted. The following steps outline how repeated 3D re-gion-growing operations are used to determine an optimal

threshold: (a) initialize threshold to T � �1,000 HU;(b) perform 3D region growing with root site (xr, yr, zr)and threshold T; (c) calculate the volume of region grow-ing, V, from step 2, ie, V � �x � �y � �z � [�@(x,y,z) �

IR IR(x, y, z)]; (d) if V � E, continue from step 2 withT � T � 1; otherwise, (e) decrease the threshold, T �T � 1, and perform final 3D region growing with thisvalue. Figure 2 is a block diagram of these steps.

We have made two modifications to the adaptive 3Dregion-growing algorithm to increase robustness. The firstmodification is applied to the output segmentation and isrepresented by the “postprocessing” box in Figures 1 and2. The final output of adaptive 3D region growing is un-acceptable in most cases because of cavities in the seg-mentation due to noise in the original image. Addition-ally, the region boundaries in the final segmentation areoften rough. We solve these problems by applying a 2Dcavity filling and a 2D binary closing by a four-connectedneighborhood operator to each section of IR (40).

The second modification is the prefiltering of the data.This option is manually applied as needed on a case-by-case basis. Prefiltering is necessary when even the mini-mal initial threshold creates an explosion into the paren-chyma. Applying a 2D median filter to each sectionsolves this problem (40). Two mask sizes are used, de-pending on the severity of the explosion. The first maskis a four-connected neighborhood and the second is a 3 �3 mask. The effects of these filters on region growing aredescribed in Results.

Figure 2. Block diagram of adaptive 3D region growing.

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Morphology-based SegmentationIn the hybrid method, a modified form of the morpho-

logic segmentation method proposed by Bilgen et al (22)accounts for most of the processing. The method of Bil-gen et al has two steps. First, 2D morphologic operationsare performed to determine candidate airway locations.This step uses gray-scale reconstruction followed bythresholding applied to each section. Next, 3D reconstruc-tion is performed to recover the airway tree from thesecandidate locations. These steps are depicted in Figure 1.The result is a binary segmented volume of the air-ways, IS.

Candidate airway locations are determined on a 2Dbasis by means of gray-scale reconstruction followed bythresholding. The basis operator for the reconstruction isgiven by a binary four-connected neighborhood, B4, thesmallest element used in the process. Larger elements arecomputed with repeated dilations of B4 as follows:

B4b � bB4 � B4 � B4 � . . . � B4

,(1)

b � 1) dilations

where bB4 is the bth-order homothetic of B4.An operator B4

b is applied to each individual section asdescribed below. Given the original image I, each sectionz � 1, . . . , Z, of I is windowed (�1,000, 0) to form anew 2D image S,

Sx,y � � Ix,y,z if Ix,y,z � 00 otherwise.

Windowing is used to eliminate the effect of variationsin more dense structures, such as bone. Figure 3a shows

an example of a windowed section. A marker image forgray-scale reconstruction, J1, is then obtained from thegray-scale closing of S with structuring element B4

b,

J 1b � S � B4

b � S � B4b � B4

b. (2)

Hence, J1b is computed from the gray-scale dilation by

means of B4b followed by an erosion by the same operator.

Next, J2b is computed from J1

b with the following:

J k�1b � maxJ k

b � B4,S, (3)

where max(. , .) computes the voxel-by-voxel gray-levelmaximum. Equation (3) is repeated until no furtherchanges occur; that is,

J �b x,y � J k�1

b x,y � J kbx,y, � x,y � J k

b, (4)

where J�b represents the final gray-scale reconstructed im-

age with structuring element B4b. In this image, local min-

ima smaller than B4b in S are filled in with a gray-level

value proportional to the difference between the maxi-mum and minimum gray levels computed within a B4

b-sized neighborhood of the minima. An example image ofJ�

b is shown in Figure 3b.A gray-scale difference image is then computed be-

tween J�b and S and thresholded:

Cbx,y � � 1, if J �b x,y � S � TM.

0, otherwise.

The difference image is bright where local minima existin the image S. We use a value of 20% of the difference

Figure 3. Demonstration of 2D candidatelabeling for case h016, section 283. (a) Origi-nal section is windowed to (� 1,000, 0).(b) Gray-scale reconstruction is performed onthe image in a with a operator of a specificsize (J�

b for a specific b � 7). (c) Images band a are subtracted and then thresholded bya value TM to produce a binary image of thecandidate airways. (d) The union of binaryimages acquired through each operator istaken to define all candidate airways.

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between the maximum and minimum possible values forthe parameter TM. In this case, since the data were win-dowed between 0 and �1,000, the threshold value is 200.Figure 3c gives an example of Cb, a binary section ofpotential airways identified by operator B4

b.To identify airways of various sizes, the above process

is repeated for each element B4b, b � 1, 2, . . . , M, where

BM4 is the maximum-sized operator. The union of this

series of images is taken to form the final output C forthe section z:

Cx,y � �b�1

M

Cbx,y. (5)

The segmented section C contains all potential airwaysacquired through all the operators. An example of C isshown in Figure 3d. C is then inserted into IS to definecandidate airway locations for section z:

ISx,y,z � Cx,y, � x,y � C. (6)

This process is repeated for each section z of I.Once the candidate airway locations are in IS, the 3D

airway tree is reconstructed by using a closed space dila-tion with a unit kernel radius, as described in reference22. Three-dimensional region growing with six-connectiv-ity, rooted at the trachea, is used in this process, whicheliminates most false candidates, leaving only the airwaysin IS. An example is shown in Figure 4. Simpler recon-struction methods are also possible. A closing followedby region growing at the root site provides better truecandidate recovery at the cost of greater false candidates.

An opening before this simpler reconstruction allows forbetter recovery of stenosed branches. In both of theseoperations, the operator used was a discrete sphere ofradius 1.

Segmentation methods using morphologic operationscan be computationally expensive. Reference 22 describesthe use of operators of various sizes to detect airways ofcorresponding sizes. These costly operators need not beapplied to the entire image, however, but only to the ap-proximate locations of the airways, because they have notheoretical relevance to other portions of the volume. Thehybrid approach uses lung segmentation and adaptive 3Dregion growing to create masks that greatly constrain thevolume where these operators are applied.

Hybrid Lung Segmentation AlgorithmA diagram of the hybrid algorithm is shown in Figure

1. The inputs are the 3D CT image of the chest and thelocation of the proximal end of the trachea, or the rootsite. The hybrid algorithm requires four parameters: (a) E,the explosion parameter for adaptive 3D region growing;(b) s, the maximal operator size considered “small”;(c) M, the maximal operator size for morphologic opera-tions; and (d) TM, the preset threshold used by the mor-phologic operator segmentation method. The final outputis the segmented image of the airways, IS.

The original image and root site are used throughoutthe method. The goal of the method is to provide thesame quality of segmentation as an existing technique(22) but with an order of magnitude reduction in compu-tation time. This increase in speed is achieved by usingan adaptive 3D region-growing method (introduced inreference 25) combined with lung region definition. More

Figure 4. Coronal projections of the candi-date labeled image and the image after 3Dreconstruction.

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specifically, we identify the locations of larger airways byusing 3D region growing. Computationally expensivemorphologic operators for large airways are then appliedonly to these identified regions. Areas of the lungs aremasked by using lung region definition. Operators forsmaller airways are applied in the restricted region en-compassing only this area. These operators are character-ized by their integer size, b. Several other segmentationapproaches make use of morphologic operations followedby reconstruction (26,28,29). These approaches can alsobe improved with our method.

Lung region definition creates a 3D mask of the datathat defines the subvolume of the image containing thelungs. Once the lung region is segmented, the maximumbounding 3D parallelopiped of the segmentation, WL, isused as a mask for smaller morphologic operators, b � 1,. . . , s. The Morphology-based Segmentation section de-scribes how these operators of smaller sizes are appliedon a section-by-section basis.

Adaptive 3D region growing uses an optional prefilteralong with a specified explosion parameter, E, to providea segmentation of the airways, IR. The E parameter sim-ply ensures that an acceptable volume is segmented. Thissegmentation is used to provide a set of more refinedmasks for each section of the image, WR

i , I � 1, . . . , Z.These masks are then used by the remaining larger opera-tors, b � s � 1, . . . , M. Although adaptive 3D regiongrowing is fast, the segmentation does not always capturefine details on the order of one or two voxels, but it doesgive an excellent estimate of the location of larger air-ways. The computation time of this segmentation is smallcompared with that of any method employing morpho-logic operations. In summary, 3D region growing is usedto create a rough segmented volume of the airways, IR.For each section I � IR, a maximum bounding 2D regionencompassing the segmented airways, WR

i , is determined.Each window is then expanded by the radius of the larg-est operator to ensure proper detection of large airwayson the boundaries.

Once the masks, WL and WR, are computed, the recon-struction proceeds according the gray-scale reconstructionmethod described in Morphology-based Segmentation, butthe operators are applied only to the regions dictated bythese masks.

Image AcquisitionThirty 3D CT images, obtained with either an MX8000

(Philips Medical Systems, Best, Netherlands) or an Aquil-ion (Toshiba America Medical Systems, Tustin, Calif)

multisection CT scanner, were used to test the system.The subjects were studied under a protocol approved bythe University of Iowa’s Institutional Review Board. Thescanning parameters for the Philips scanner included thefollowing: 120 kVp, 100 mAs with a multisection pitchof 5 (equivalent to a single pitch of 1.25), 0.5-second ro-tation time, 0.6-mm table increment, 180° scan angle, and1.3-mm section thickness. The images obtained with thisscanner included four airway images, two lung noduleimages, seven mediastinal lymph node images, and sixother images, all obtained with a D reconstruction kernel.In addition, eight images obtained with the MX8000scanner were used to compare the A, B, and D recon-struction kernels. Three images from the Toshiba scannerwere used to test the robustness of the system with a dif-ferent scanner. All images were 512 � 512 pixels in thetransverse plane but varied in resolution and the numberof sections. Table 1 lists the testing images in detail.

RESULTS

In this section we present the results of the segmenta-tion system applied to the test images. Various compo-nents of the system are compared, and the effects of fil-tering are presented. We then demonstrate the applicationof these methods to human VB analysis of a peripheralnodule. Adaptive region growing, morphologic recon-struction, and the hybrid method were compared for theimages listed in Table 1. In each case, the root site wasmanually identified. Computation times were determinedon a 933-MHz Xeon PIII personal computer (Dell Preci-sion 620; Dell Computer, Austin, Tex) with two centralprocessing units and 2 GB of memory. The explosionparameter, E, was set to 50,000 mm3 for all but one case.The threshold parameter for the morphologic method waskept at TM � 200 for all cases. The largest operator clas-sified as small, s, was determined from the smallest air-way 3D region growing can segment continually. A valueof 3 was used for s since airways with cross sectionslarger than B3

4 are hardly influenced by partial volumeeffects. The largest operator, M, is based on the size ofthe largest airway on the image. We found that settingM � 18 adequately captures all the airways in our datasets.

The morphology and hybrid methods were first com-pared in terms of average execution time for 10 of theimages in Table 1. In each case, the region-growing inputto the hybrid method was checked to make sure that nomajor parenchymal leakage occurred. Minimal manual

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interaction was required to assure this condition. The hy-brid method performed labeling more than 20 times fasteron average (641 vs 13,751 seconds), and the 3D recon-struction time was also improved by 8% (737 vs 799 sec-onds).

Next, the adaptive region-growing and hybrid methodswere compared. Two main factors were analyzed: robust-ness and execution time. Robustness was defined as themethod’s ability to complete a visually acceptable seg-mentation. Qualities such as segmentation volume andnumber of branches were also compared. The hybrid andregion-growing methods were compared according tothese criteria for all the images.

Table 2 shows the quality of segmentations accordingto the methods and filtering levels. It also divides the im-

ages into those reconstructed with the D kernel and thosereconstructed with the A and B kernels. All of the imageswere successfully segmented by both methods, althoughin some cases prefiltering was required for a successfulsegmentation. The quality of the segmentations was deter-mined subjectively according to the quality of thebranches segmented. Table 3 lists the mean segmentationtimes for both methods, with standard deviations andranges. The average volumes were computed for all suc-cessful segmentations. There was a general decrease involume with increasing filtering for both methods. Thisdecrease was greater with the region-growing method. Forthe region-growing method, the average volumes droppedby approximately 20% and 21% for the star median and3 � 3 median filters, respectively. The hybrid method

Table 1Images Used in Testing the Algorithms Making up the 3D Airway Segmentation System

Image Z �x �y �z Comments

h017 239 0.56 0.56 0.50 Toshibah022 280 0.58 0.58 0.50 Toshibah023 100 0.60 0.60 3.00 Toshibah010 535 0.69 0.69 0.60 Philips, D kernelh015 476 0.57 0.57 0.60 Philips, D kernelh018frc 448 0.57 0.57 0.60 Philips, D kernelh018tlc 475 0.57 0.57 0.60 Philips, D kernelh001a 414 0.57 0.57 0.60 Philips, A kernelh008 389 0.59 0.59 0.60 Philips, A kernelh026 502 0.76 0.76 0.60 Philips, A kernelh026b 502 0.76 0.76 0.60 Philips, B kernelh001 414 0.57 0.57 0.60 Philips, D kernel, lung noduleh019 597 0.74 0.74 0.60 Philips, D kernel, lung noduleh003 210 0.66 0.66 0.60 Philips, D kernel, airway caseh009 492 0.69 0.69 0.60 Philips, D kernel, airway caseh012 149 0.62 0.62 0.60 Philips, D kernel, airway case—papillomah016 556 0.72 0.72 0.60 Philips, D kernel, airway caseh002 515 0.59 0.59 0.60 Philips, D kernel, mediastinal lymph nodeh004 262 0.59 0.59 0.60 Philips, D kernel, mediastinal lymph nodeh005 479 0.59 0.59 0.60 Philips, D kernel, mediastinal lymph nodeh006 574 0.72 0.72 0.60 Philips, D kernel, mediastinal lymph nodeh007 488 0.65 0.65 0.60 Philips, D kernel, mediastinal lymph nodeh008 389 0.59 0.59 0.60 Philips, D kernel, mediastinal lymph nodeh014 411 0.66 0.66 0.60 Philips, D kernel, mediastinal lymph nodeh028Afrc 370 0.68 0.68 0.60 Philips, A kernelh028Bfrc 370 0.68 0.68 0.60 Philips, B kernelh028Dfrc 370 0.68 0.68 0.60 Philips, D kernelh029Afrc 412 0.66 0.66 0.60 Philips, A kernelh029Bfrc 412 0.66 0.66 0.60 Philips, B kernelh029Dfrc 412 0.66 0.66 0.60 Philips, D kernel

Note.—Images are listed by case number. Z � number of sections, �x and �y � axial plane resolutions, and �z � section thickness.Comments indicate the scanner used (Philips MX8000 or Toshiba Aquilon), the reconstruction kernel, and case details (see Image Acqui-sition for additional information).

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showed average volume drops of 1.2% and 2.5% for thesame filters and also demonstrated 4% greater averagevolumes for nonfiltered segmentations compared to theregion-growing method. Finally, the number of branchesof segmentations considered “excellent,” as listed in Ta-ble 2, were counted by an automatic path-planning algo-rithm (42). The region-growing segmentations had an av-erage of 55 branches, while the hybrid method segmenta-tions had an average of 74 branches.

Figures 5, 6, and 7a show the maximum-intensity pro-jection views of airways segmented with the three meth-ods. Figures 7b and 8 show surface renderings based onthe segmentation results.

Figure 5 shows case h007 segmented with the threedifferent segmentation methods and three levels of filter-ing. The filtering enables segmentations to be completedsuccessfully. All three methods displayed comparable seg-mentation quality, but the hybrid method showed nosmall explosion artifacts and achieved acceptable segmen-tation with less filtering than the region-growing methodrequired. Figure 8 shows the surface renderings of theairways segmented with the 3 � 3 median filter.

Figure 7a shows the results in case h006, without fil-tering. The 3D region-growing and hybrid methods hadsimilar results. Each method missed airways recovered bythe other. With the region-growing method there was aminor explosion in the segmentation. Filtering or lower-ing the explosion parameter can correct this problem, butsince the explosion volume is small, it would be difficultto determine the proper setting according to the volumechange during region growing. Figure 7b displays a sur-face-shaded view based on the hybrid segmentation re-sults.

Figure 6 displays the results obtained without filteringin case h008. The hybrid method was the only successfulone. Region growing failed because a low gray-levelvoxel directly linked the airways to the parenchyma. Themathematical morphology method failed because larger

Table 2Results with the Hybrid and Region-growing Algorithmswith Various Filters

Method and Filter

No. of Images

Excellent

MinorBranchFusion

MajorBranchFusion Failure

Region-growingNo filter 14 8 4 4Star median 21 3 5 13 � 3 median 23 6 1 0

HybridNo filter 12 14 1 3Star median 17 8 2 33 � 3 median 17 9 1 3

Region-growing ABNo filter 6 1 0 0Star median 6 1 0 03 � 3 median 7 0 0 0

Hybrid ABNo filter 4 3 0 0Star median 5 1 1 03 � 3 median 6 1 0 0

Region-growing DNo filter 8 7 4 4Star median 15 2 5 13 � 3 median 16 6 1 0

Hybrid DNo filter 8 11 1 3Star median 11 7 1 33 � 3 median 10 8 1 3

Note.—The quality of the segmentation was subjectively deter-mined according to the fusing of branches. Images rated as ex-cellent had no noticeable fusion. The next two categories in-cluded images with fusion of small peripheral branches and thosewith fusion of larger branches. Finally, failure was defined as largesections fused or incorrectly segmented images. The first sixrows give results for all images, while the remaining rows giveresults for images reconstructed with the A or B and the D kernel,respectively. For path planning for navigational purposes, all im-ages are acceptable except for those considered failures. Figure9a is an example of major branch fusion, and Figure 9b shows asegmentation classified as excellent. The segmentation on the leftin Figure 7a shows minor branch fusion.

Table 3Timing Comparisons for Region-growing and Hybrid Methods

Method Mean Time (sec)

Region growingNo filter 19 � 12 (5–67)Star median 70 � 18 (17–92)3 � 3 median 116 � 29 (28–158)

HybridNo filter Lab: 761 � 357 (198–1,561)

Rec: 947 � 571 (113–2,365)Star median Lab: 745 � 332 (184–1,478)

Rec: 835 � 509 (90–2,247)3 � 3 median Lab: 730 � 303 (176–1,383)

Rec: 719 � 408 (90–1,604)

Note.—Only successfully segmented images were consideredin these statistics. Times are given as means � standard devia-tions, with ranges in parentheses. Lab � labeling time, Rec � re-construction time. The region-growing method is considerablyfaster than the hybrid method, but both are acceptable for clinicaluse.

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structuring elements identified candidates that eventuallylinked airways to the parenchyma. Filtering preventedfailure in the latter two methods.

We have applied the segmentation method to over 30human cases thus far, using an integrated VB system(11,20,44,45). The system permits assessment of 3D CTimages and live guidance of follow-up bronchoscopy.Reference 45 illustrates the system’s use for phantomstudies, while reference 20 describes preliminary effortsto assess 3D CT images in human subjects.

Figures 9 and 10 illustrate the use of our segmentationmethod and the VB system in a peripheral nodule case.The initial 3D CT image was obtained with a PhilipsMX8000 multidetector helical CT scanner and consistedof 414 sections (512 � 512; section thickness, 0.6 mm;axial plane resolution, 0.566 mm). Figure 9 illustratesairway-tree segmentation results with and without filter-ing. After segmentation, we used an automated algorithmto compute the centerline paths for the segmented tree(42). Twelve generations of airway branches were ex-

Figure 5. Maximum-intensity projection images of different segmentations of a 512 � 512 CT image of the chest (case h007) (488 sec-tions; voxel spacing, � x � �y � 0.654297 mm, �z � 0.599976 mm; image size, 244 MB. The three segmentation algorithms are shownin the columns, and the different levels of filters in the rows. Filtering the image before processing increases the robustness of the seg-mentation methods, but it also tends to remove smaller branches or identify nonairway regions, depending on the algorithm used (rootsite � [266, 221, 0], E � 50,000 mm3, TM � 200).

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tracted, which included 182 branches and 93 paths (seereference 20 for definitions); some paths toward the pe-riphery are false. The segmentation step took 2 minutes26 seconds, compared with 3 minutes 19 seconds for thepath analysis. All processing was done on a Dell Inspiron(Dell Computer) 3800 laptop computer (700-MHz centralprocessing unit, 512-MB RAM).

Figure 10 gives a composite VB system view for thecase. A peripheral nodule is clearly visible on the coronalprojection view in the right lung. We manually definedthe nodule with the system’s built-in editing tools. Wethen created a surface file by using a custom surface-dila-tion procedure and a standard marching cubes algorithm(46). All tools clearly show the nodule, while the endolu-minal renderer shows an interior view in the right mainbronchus. These data could be used for planning fol-low-up biopsy.

DISCUSSION

We have presented an airway segmentation systembased on region-growing and mathematical morphologyalgorithms for segmentation. We have evaluated the un-derlying algorithms by testing the system with a group of30 images. The results show that no single method is su-perior in all respects, demonstrating a need for a multifac-eted segmentation system. The use of two methods alongwith filtering allows all the images to be successfully seg-mented. In this section we discuss the effects of filteringon segmentation robustness and quality, the different re-construction kernels, and the results of the hybrid algo-rithm compared with the other methods.

Filtering the image before segmentation increases therobustness of the algorithms by helping eliminate low-density voxels that connect the airways to the paren-

Figure 6. Maximum-intensity projections of three different segmentation algorithms fora 512 � 512 CT image of the chest (case h008) (389 sections; voxel spacing, �x ��y � 0.585938 mm, �z � 0.599976 mm; image size, 194 MB). The left image was ob-tained with adaptive 3D region growing, the center image with the hybrid algorithm, andthe right image with the standard morphologic algorithm (failed). All three images werecomputed without filtering (root site � [242, 211, 0], E � 50,000 mm3, TM � 200).

Figure 7. (a) Maximum-intensity projections of three different segmentation algorithms for a 512 � 512 CT image of the chest (caseh006) (574 sections; voxel spacing, �x � �y � 0.724609 mm, �z � 0.599976 mm; original image size, 287 MB). The left image was ob-tained with adaptive 3D region growing, the center image with the hybrid algorithm, and the right image with the standard morphologicalgorithm. All three images were computed without filtering. The center image was used to mask the original gray-scale data. (b) Themarching-cubes algorithm with a threshold of �600 HU was then applied to the masked gray-scale data to create the surface shown(root site � [273, 248, 0], E � 50,000 mm3, TM � 200).

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chyma. In most of the cases shown in Table 2, the num-ber of excellent segmentations increased with greater fil-tering.

Filtering has predictable effects on the region-growingsegmentation. In the column for the region-growingmethod in Figure 5, there are two noticeable effects ofincreased filtering. The first is successful segmentation.The second effect is negative, in that smaller branches areeliminated. The hybrid and morphologic methods do notrespond as predictably to filtering. This behavior is due tothe more complex two-step process used in computing the

segmentation. Filtering has a less predictable effect on themorphologic operations but can still result in improve-ments in some cases. A trend toward more segmentationsclassified as excellent is noticeable for both methods inTable 2.

The hybrid method tends to be more robust againstfailure than the original morphology method or the re-gion-growing method when filtering is not used. The useof filtering benefits the region-growing algorithm themost, since the hybrid algorithm is less prone to leaksinto the parenchyma. Since filtering tends to reduce the

Figure 8. Surface renderings based on the segmented images from Figure 5 obtained with the 3 � 3 median filter and (a) the region-growing, (b) hybrid, and (c) morphology methods. The segmentations were dilated by three voxels and used as a mask on the originalgray-level data. The marching-cubes algorithm with a threshold of �800 HU was then used on the masked data (43).

Figure 9. Coronal maximum-intensity pro-jection images of a segmented airway treeobtained with 3D CT of a peripheral nodule(see text for image details). (a) Image ob-tained with region growing and no filtering(root site � [273, 292, 0]; E � 50,000 mm3).Note the extraneous noisy extensions. (b) Im-age obtained with the same segmentationparameters as in a but with a star medianfilter (five-point windows, including the centralpixel and its four neighboring pixels along thevertical and horizontal axes); the view ismarkedly cleaner.

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number of peripheral branches, the segmentation volumetends to decrease. The hybrid method, however, is lessinfluenced by filtering.

In summary, filtering increases the robustness of thesealgorithms but comes at the cost of losing smallerbranches or identifying additional nonairway structures.For several images, segmentation with adaptive regiongrowing was unsuccessful, but prefiltering solved theproblem in each case. The four-connected neighborhoodmedian filter eliminates the finer branches, and the 3 � 3median filter eliminates thicker ones.

The assortment of images included several differentreconstruction kernels. Table 2 distinguishes images re-

constructed with the D kernel and those reconstructedwith the A or B kernel. The images are classified intofour levels of quality, from excellent to failure. The ratioof excellent images to other quality levels is higher forimages reconstructed with the A or B kernel. This prop-erty is seen for both reconstruction methods. The D ker-nel has more instances of branch fusion and failures. Itoffers a sharp reconstruction for more pronounced edges.This quality also produces more noise and strengthensartifacts, reducing the segmentation quality. Voxels thatmake up the airway walls in the peripheral airways arealtered more with the D kernel, creating a fusion of pe-ripheral branches. These results suggest that an A or B

Figure 10. Composite view in a VB system for the peripheral nodule case shown in Figure 9. The 3D surface tool shows the renderedairway tree and precomputed airway centerlines. One path that leads closest to a peripheral nodule is highlighted. Arrows on the varioustools indicate the location of the nodule. The coronal projection view is a half-sized maximum-intensity projection of all data betweenY � 150 and Y � 400. It shows the nodule and the highlighted (white) path closest to it. The Coronal Front-to-Back Slab depicts adepth-weighted maximum view near the nodule (field of view � 30, depth of vision � 40, viewing window � [�1,024, 196]) (47). TheTransverse and Coronal Slicer views show original section data in the transverse and coronal directions; a mediastinal viewing windowwas used (WL � �40, WW � 400). Finally, the Endoluminal Renderer shows an interior airway view approaching the end of the rightmain bronchus; this site is shown by the ball on the 3D surface view and the termination of the white path on the coronal projection view(case h001) (root site � [273, 292, 0], region growing, star median filter, E � 50,000 mm3, slab � [focus � 20, vision � 30, maxwin �400]).

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reconstruction kernel would be more appropriate for seg-mentation. Reinhardt et al (18) also found that a normalreconstruction kernel is better suited for quantitative pur-poses.

As previously mentioned, neither method is superior.The adaptive region-growing and hybrid methods eachhave distinct advantages. The hybrid method, however, issuperior to the morphology method in that it substantiallyreduces execution times while producing very similar re-sults. These conclusions are discussed below.

Adaptive 3D region growing proved to be the fastestmethod for obtaining an airway segmentation, but severalairways can be missed and the lumen edge definitiontends to be poor. Figure 11 demonstrates the superioredge localization of the hybrid method. Although fusionof the branches increases the segmented volume slightlyand the hybrid tended to have more fusion cases, the edgelocalization is probably why its segmentation volumetended to be greater. Furthermore, for the images classi-fied as excellent, those segmented with the hybrid method

had more branches on average than those segmented withregion growing: 74 versus 55.

As one case demonstrates, however, adaptive regiongrowing is a necessary method of the system for propersegmentation. Case h012 is an image obtained from apatient with the papilloma virus, which creates sacs thatare valid portions of the airways. A rendering and crosssection are shown in Figure 12. Since the sacs occupy asubstantial volume, the explosion parameter, E, was set to70,000 mm3. Morphology-based methods such as the hy-brid method tend to fail due to their inability to identifythe shape and consistency of the sacs.

The hybrid algorithm considerably reduced the timerequired for segmentation compared with the morphologymethod, suiting it for clinical use. The outputs of thesetwo methods are similar, but in addition to the speed ad-vantage, the hybrid method has better use of larger opera-tors. These operators are only applied to locations withairways of similar sizes. Again, the larger operators haveno theoretical relevance in locations where there are no

Figure 11. Sections of gray-scale 3D CTdata with overlays of the resultant segmenta-tions obtained with region-growing and hybridmethods. The hybrid method demonstratesbetter edge localization since it capturesmore of the airway lumen than the region-growing method. This property partly explainswhy the hybrid method results in greater seg-mentation volumes. This feature also makeshybrid segmentation better for quantitativeanalysis.

Figure 12. (a) Surface rendering of the air-way from a patient with papilloma (caseh012). Region growing was the only success-ful method. (b) Magnified view shows a win-dowed (�1,000, 0) section of the data. Themorphology method does not segment thecavity successfully due to the cavity’s oddsize, shape, and contents. This case demon-strates the necessity of the region-growingmethod in a clinical environment (root site �[266, 221, 0], region growing, star median fil-ter, E � 70,000 mm3, TM � 200).

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similarly sized airways. Hence, the hybrid method is lesslikely to produce as many false candidates, making recon-struction faster and the output more successful. The hy-brid method was more than 20 times faster than the mor-phology method for labeling and about 8% faster for re-construction.

These results indicate that adaptive 3D region growingis appropriate when a fast segmentation is needed for pathplanning. The hybrid approach offers better edge localiza-tion at the cost of more computation time. Both methodsare necessary for clinical use, however. Additionally,given the choice of reconstruction kernel, the A and Bkernels tend to produce better results.

Although human intervention is required to select pre-filtering of the data, the use of the median filter beforesegmentation increases the robustness of all three algo-rithms. Adaptive region growing benefits the most fromprefiltering, since region growing is prone to parenchymalleakage. The median filter helps to reduce the number ofconnections between airways and the parenchyma.

The system described here is being used as part of aVB analysis system to guide path selection and treatmentplanning (11,15). The ability to segment the airways of-fers a basis for variety of image analysis methods. Pathcalculations, rendering, and quantitative analysis all de-pend on accurate airway segmentation.

ACKNOWLEDGMENTS

The authors thank Jered Sieren for help with the imageacquisition and Janice Cook-Granroth, BS, and AngelaDelsing for help with the image processing.

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