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    REVIEW

    Texture analysis of medical images

    G. Castellano*, L. Bonilha, L.M. Li, F. Cendes

    Neuroimage Laboratory, Faculty of Medical Sciences, State University of Campinas, Brazil

    Received 12 April 2004; received in revised form 5 July 2004; accepted 22 July 2004

    KEYWORDSImages, analysis;Images, processing;Diagnostic radiology;Magnetic resonance(MR), tissue

    characterization;Computedtomography (CT),tissuecharacterization;Ultrasound (US),tissuecharacterization

    The analysis of texture parameters is a useful way of increasing the informationobtainable from medical images. It is an ongoing field of research, with applicationsranging from the segmentation of specific anatomical structures and the detection oflesions, to differentiation between pathological and healthy tissue in differentorgans. Texture analysis uses radiological images obtained in routine diagnosticpractice, but involves an ensemble of mathematical computations performed with

    the data contained within the images. In this article we clarify the principles oftexture analysis and give examples of its applications, reviewing studies of thetechnique.q 2004 The Royal College of Radiologists. Published by Elsevier Ltd. All rightsreserved.

    Introduction

    The texture of images refers to the appearance,

    structure and arrangement of the parts of an objectwithin the image. Images used for diagnosticpurposes in clinical practice are digital. A two-dimensional digital image is composed of littlerectangular blocks or pixels (picture elements), anda three-dimensional digital image is composed oflittle volume blocks called voxels (volumeelements); each is represented by a set of coordi-nates in space, and each has a value, representingthe grey-level intensity of that picture or volumeelement in space. Since most medical images aretwo-dimensional we will restrict the discussion to

    pixels, bearing in mind that the extension to voxelsand volumetric images is straightforward.

    We may attribute the texture concept in a digitalimage to the distribution of grey-level values amongthe pixels of a given region of interest in the image.

    One way of depicting this is to display the digitaldata as a three-dimensional map based on the pixelvalues, as shown in Fig. 1. Thus, texture analysis is

    in principle a technique for evaluating the positionand intensity of signal features, i.e. pixels, andtheir grey-level intensity in digital images. Texturefeatures are, in fact, mathematical parameterscomputed from the distribution of pixels, whichcharacterize the texture type and thus the under-lying structure of the objects shown in the image.

    According to the methods employed to evaluatethe inter-relationships of the pixels, the forms oftexture analyses are categorized as structural,model-based, statistical and transform methods.1

    The structural methods2

    This represents texture by the use of well-definedprimitives. In other words, a square object isrepresented in terms of the straight lines orprimitives that form its border. The advantage ofthese methods are that they provide a goodsymbolic description of the image. On the otherhand,itisbetterforthesynthesisofanimagethanforits analysis. The theory of mathematical morphology3

    is a powerful tool for structural analysis.

    Clinical Radiology (2004) 59, 10611069

    0009-9260/$ - see front matterq 2004 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.doi:10.1016/j.crad.2004.07.008

    * Guarantor and correspondent: G. Castellano, NeuroimageLaboratory, Faculty of Medical Sciences, State University ofCampinas (UNICAMP), 13081-970 Campinas SP, Brazil. Tel.:C55-19-37887292; fax:C55-19-32891395.

    E-mail address: [email protected](G. Castellano).

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    The model-based methods

    Here an attempt is made to represent texture in an

    image using sophisticated mathematical models(such as fractal or stochastic). The model par-ameters are estimated and used for the imageanalysis. The disadvantage is the computationalcomplexity involved in the estimation of theseparameters.

    The statistical approaches2

    These are based on representations of texture usingproperties governing the distribution and rela-tionships of grey-level values in the image. These

    methods normally achieve higher discriminationindexes than the structural or transform methods.

    The transform methods

    The texture properties of the image may be

    analyzed in a different space, such as the frequencyor the scale space. These methods are based on theFourier,4 Gabor5 or Wavelet transform.6 The Wave-let transform is the most widely used because of theease with which it may be adjusted to the problemin question.

    Texture parameters

    Medical images possess a vast amount of textureinformation relevant to clinical practice. For

    example, current magnetic resonance (MR) imagesof tissues are not capable of providing microscopicinformation that can be assessed visually. However,histological alterations present in some illnessesmay bring about texture changes in the MR imagethat are amenable to quantification through textureanalysis. This has been successfully applied to theclassification of pathological tissues from the liver,thyroid, breasts, kidneys, prostate, heart, brain andlungs.715

    We describe the main parameters used intexture analysis, selecting four categories ofparameter from the statistical class (which is

    the most widely used for medical applications),one from the model-based class and one from thetransform class. The structural class is omittedbecause we did not find any example of itsapplication to medical images.

    The most commonly used texture parameterscome from six main categories.

    1. Histogram (statistical class)2. Absolute gradient (statistical class)3. Run-length matrix (statistical class)4. Co-occurrence matrix (statistical class)

    5. Auto-regressive model (model class)6. Wavelets (transform class).

    We describe those categories in more detailbelow, and give examples of the sorts of measures(parameters) that can be obtained from them.

    Histogram

    In digital images, the allowed grey-level values thata pixel may assume are limited. They consist ofinteger numbers ranging from 0 to 2bK1, where bstands for the number of bits of the image (i.e. this

    Figure 1 (a) Coronal slice of T1-weighted cerebral MRI.(b) Corresponding three-dimensional map based on thepixel values.

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    will determine the amount of disk memory occu-pied by each image pixel). For most digital images 8bits are sufficient, and therefore the grey-levelvalues range from 0 to 255; but medical MR imagesnormally use 12 bits (which gives more definition ofthe objects in the image), and therefore the grey-

    level values range from 0 to 4095. Note that theconvention is to attribute lower values to darkergrey levels, and higher values to lighter grey levels.Therefore 0 generally represents black, and white isrepresented by 255 (in an 8 bits image) or 4095 (in a12 bits image). Fig. 2 shows an example of a 3 bitsdigital image, with 5!5 pixels.

    The histogram of an image is the count of howmany pixels in the image possess a given grey-levelvalue. For a 12 bits image, this may be representedby a graph with an x coordinate ranging from 0 to4095, and a y coordinate representing the respect-

    ive pixel count. Fig. 3 shows the histogram of theimage in Fig. 2.From the histogram many parameters may be

    derived, such as its mean, variance and percentiles.The mean of the histogram gives us the mean grey-level value of the image. The variance is a measureof how far from the mean the grey-level values inthe image are distributed. For example, if there isan image with 2 pixels with grey-level values 0 and100, and another image also with 2 pixels withvalues 49 and 51, the mean will be 50 for bothimages. However, in the first case there is a hugevariance, since 0 and 100 are far from the mean,

    whereas in the second case the variance is small,since 49 and 51 are close to the mean value. Apercentile gives the highest grey-level value underwhich a given percentage of the pixels in the imageare contained; for example, if the 1% percentile ofan 8 bits image is 10, the 1% of pixels in the imagehas a grey-level value from 0 to 9.

    Absolute gradient

    The gradient of an image measures the spatialvariation of grey-level values across the image.Thus, if at a point in the image the grey level variesabruptly from black to white, we have a highgradient value at that point; whereas if it variessmoothly from a dark grey to a slightly lighter grey,we have a low gradient value at that point. Thegradient may be positive or negative, depending onwhether the grey level varies from dark to light orfrom light to dark. However, since in general whatis of interest is whether we have an abrupt or asmooth grey-level variation, the absolute gradientis used (i.e. the sign is not taken into consider-ation). Fig. 4(a) shows a coronal slice of a T1-

    weighted cerebral MRI, and Fig. 4(b) shows thecorresponding absolute gradient. Note how thegradient image emphasizes the contours ofthe original one, and how it is strongest (whitest)where the grey-level changes in the original imageare greatest.

    Examples of texture parameters that may becomputed from the absolute gradient are, again, itsmean and its variance. The absolute gradient meanwill thus be a measure of the mean grey-levelvariation across the image, and its variance a

    Figure 2 Example of a digital image. (a) Image with 5!5 pixels, with grey-level values ranging from 0 (black) to 7(white). (b) Numerical representation of the image.

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    measure of how far from the mean these variationsare.

    Run-length matrix

    The run-length matrix is a way of searching theimage, always across a given direction, for runs ofpixels having the same grey-level value. Thus, givena direction (for example, the horizontal direction),the run-length matrix measures for each allowedgrey-level value how many times there are runs of,for example, 2 consecutive pixels with the samevalue. Next it does the same for 3 consecutivepixels, then for 4, 5 and so on. Note that manydifferent run-length matrices may be computed fora single image, one for each chosen direction. Inpractice normally 4 matrices are computed, for thehorizontal, vertical, and two diagonal directions.

    Fig. 5 shows the horizontal and one of the diagonalrun-length matrices corresponding to the exampleimage in Fig. 2. Since this image is small and there isnot much space for runs in it, most of the elementsof the run-length matrices are zero-valued. Theonly non-zero-valued elements correspond to thegrey-level values 0, 2 and 7, which are the onlyvalues giving runs in the selected directions.

    Some parameters that may be computed fromthe run-length matrix are the fraction of image inruns and the short-run emphasis. The fraction ofimage in runs is a measure of the percentage ofimage pixels that are part of any of the runsconsidered for the matrix computing, and the short-run emphasis is a measure of the proportion of runsoccurring in the image that have short length.

    Co-occurrence matrix

    The co-occurrence matrix is a technique that allows

    Figure 3 Histogram of the image shown in Fig. 2.

    Figure 4 (a) Coronal slice of T1-weighted cerebral MRI.(b) Corresponding absolute gradient image.

    Figure 5 Example of horizontal and 458 run-lengthmatrices for the image shown in Fig. 2.

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    for the extraction of statistical information fromthe image regarding the distribution of pairs ofpixels. It is computed by defining a direction and adistance, and pairs of pixels separated by thisdistance, computed across the defined direction,are analyzed. A count is then made of the number of

    pairs of pixels that possess a given distribution ofgrey-level values. Each entry of the matrix thuscorresponds to one such grey-level distribution. Forexample, let us define a distance of 3 pixels in thevertical direction, and let us compute the corre-sponding co-occurrence matrix for an 8 bits image;for such an image, the allowed grey-level valuesrange from 0 to 255. The size of this matrix will thenbe 256!256. Thus the element (0, 10) willcorrespond to the number of pixel pairs that wefind in the image having intensity values 0 and 10respectively, and which are separated by a 3-pixel

    distance in the vertical direction. Conversely theelement (10, 0) will have exactly the same value,since it will correspond to the number of pixel pairsthat we find in the image having intensity values 10and 0, respectively, and which are separated by a 3-pixel distance in the vertical direction.

    As in the case of the run-length matrix, theremay be many co-occurrence matrices computed fora single image, one for each pair of distances anddirections defined. Normally a set of 20 co-occurrence matrices are computed, for distancesranging from 1 to 5 pixels, in the horizontal,vertical, and two diagonal directions. In Fig. 6, a

    co-occurrence matrix for a distance of 2 pixels inthe horizontal direction, for the example image ofFig. 2, is shown. Note that the matrix is symmetri-cal, as expected.

    Since the co-occurrence matrix analyzes thegrey-level distribution of pairs of pixels, it is alsoknown as the second-order histogram.

    Examples of parameters computed from the co-occurrence matrix are the contrast and theentropy. The contrast of an image refers to howmuch difference, or definition, there is betweengrey-level values of different objects in the image.

    The entropy measures the randomness or homogen-eity of the pixel distribution with respect to lengthor orientation, and it will take a higher value for amore random distribution: it is a measure of theamount of disorder in the image.

    Auto-regressive model

    The auto-regressive model assumes a local inter-action between image pixels in that the pixel grey-level value is a weighted sum of the grey-levelvalues of the neighbouring pixels. In simpler words,

    it is a way of describing shapes within the image, byfinding relations between groups of neighbouringpixels. The auto-regressive parameters are simplythe set of weights used to establish these relations.It is expected that these relations are unique for agiven type of object (or shape) in an image and,

    therefore, they may constitute a way of character-izing this object.

    Fig. 7 shows an example neighbourhood (whitepixels) that could be used to characterize the grey-level value of the centre pixel (black) through theauto-regressive model. In that case, the assumptionmade is that everypixel in theimage has itsgrey-level

    Figure 6 Example of a co-occurrence matrix for a 2-pixels distance in the horizontal direction, computed forthe example image of Fig. 2.

    Figure 7 Example of a pixel neighbourhood that couldbe used to compute the parameters of the auto-regressive model.

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    value characterized by the grey-level values ofthe surrounding pixels, according to the patternshown.

    Wavelets

    If a one-dimensional signal varies quickly in time, ithas a high frequency; if slowly, it has a lowfrequency. For example in an electrocardiogramwe see that fast variations are associated with highfrequency, whereas slow variations are associatedwith low frequency. If the grey-level value of a two-dimensional image varies fast, that is has manyvariations within a small piece of the image, weassociate a high spatial frequency to this part of theimage. In turn, if the grey-level value varies slowly,being almost the same throughout a region of theimage, the region has a low spatial frequency. Theconcept of fast or slow grey-level value variations isdependent on the scale of the image region. Anexample is the picture of a forest: if taken by asatellite (very large scale), it looks like an almostconstant green stain; if taken from an aircraft flyingat a low altitude (smaller scale), it shows manyvariations and details. The former picture wouldhave a lower frequency content, and the latterwould have a higher frequency content. In addition,the direction of the variations must be taken intoaccount in two dimensions: an image with stripes inthe horizontal direction is different from an imagewith stripes of the same size but in the verticaldirection.

    Wavelets represent a technique that analyzesthe frequency content of an image within differentscales of that image. This analysis yields a set ofwavelet coefficients corresponding to differentscales and to different frequency directions. Whencomputing the wavelet transform of an image, weassociate to each pixel a set of numbers (thewavelet coefficients) which characterize the fre-quency content of the image at that point over a setof scales. From these coefficients we can compute

    texture parameters. Fig. 8 shows an example of awavelet transform for the image shown in Fig. 4(a).The top left corner of the image shows a low-frequency small-scale version of the original image,whereas all the other parts of the image show high-frequency versions of the original image on differ-ent scales.

    An example of a wavelet-derived parameter isthe wavelet energy associated with a given scaleand direction, so this parameter measures thefrequency content of the image on a given scaleand in a given direction.

    Important considerations

    The parameters described above give an idea of thetype of information that texture analysis mayproduce from an image, depending on whichtexture parameters provide the information sought.Most applications use texture measures as a way of

    classifying regions of interest in images, forexample to differentiate between healthy andpathological tissue, or in order to separate differentanatomical structures. Therefore, the proceduregenerally adopted is to compute a large set oftexture parameters, and then determine which ofthem provides the differentiation required. Thismay be done by simple inspection of the parametervalues, or differentiation by parameter group maybe performed through discriminant analysis.

    There are commercial software packages such asMazda (https://www.eletel.p.lodz.pl/merchant/

    mazda/order1_en.epl), developed by A. Materkaand his group under the Cost project (http://www.eletel.p.lodz.pl/cost/cost_project.html ), whichproduce a large amount of texture parameters fora given region of interest in an image, and there aremany other packages available to perform furtherdata reduction and analysis of the textureparameters.

    The effect of external factors on some textureparameters must be taken into considerationbefore using texture analysis techniques. Anexample of an external factor is the grey-level

    Figure 8 Wavelet transform of the image shown in Fig.4(a). The top left corner of the image shows a low-frequency, small-scale version of the original image,whereas all other parts of the image show high-frequencyversions of the original image on different scales.

    G. Castellano et al.1066

    http://https//www.eletel.p.lodz.pl/merchant/mazda/order1_en.eplhttp://https//www.eletel.p.lodz.pl/merchant/mazda/order1_en.eplhttp://www.eletel.p.lodz.pl/cost/cost_project.htmlhttp://www.eletel.p.lodz.pl/cost/cost_project.htmlhttp://www.eletel.p.lodz.pl/cost/cost_project.htmlhttp://www.eletel.p.lodz.pl/cost/cost_project.htmlhttp://https//www.eletel.p.lodz.pl/merchant/mazda/order1_en.eplhttp://https//www.eletel.p.lodz.pl/merchant/mazda/order1_en.epl
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    tone variation present in MR images due to lack ofhomogeneity of the radio-frequency field, whichresults in different grey-level values for the sametissue type. These changes in grey-level tonesaffect the histogram of the image and its mean.

    Applications

    Texture analysis may be applied in a series of studiesof medical images. One application is the segmenta-tion of a given anatomical structure, based on thetexture characteristics of the structure. However,texture analysis is most important for those cases inwhich change cannot be detected by direct inspec-tion of the image. For example, in some conditionsthe tissue of associated anatomical structures suffersalterations. These can normally be detected by

    histologicalexamination, butsometimes notby visualinspection of the image of the tissue, whereas theymay be demonstrated by statistical analysis of thepixel distribution in the image of the structure.

    Most applications described above have beenperformed on MR images because of the greatamount of detail provided by this technique.Nevertheless, texture analysis of all sorts of imageshas been and may be performed.

    Segmentation of anatomical structures

    SaeedandPuri

    16

    analyzed texture features in order tosegment the cerebellum, using T1-weighted three-dimensional MRI of adult controls and patients. Alejoetal.17 used neighbourhood analysis of texture-basedparameters of MRI for semi-automatic segmentationof the hippocampus and corpus callosum.

    Diagnosis of skeletal muscle dystrophy

    In an earlier study using texture analysis, Herlidouet al.18 compared texture with visual analysis of MRIdata for the diagnosis of skeletal muscle dystrophy.They concluded that texture analysis can provideuseful information contributing to the diagnosis ofskeletal muscle disease.

    Differentiation between healthy andpathological tissue in the human brain

    Kovalev et al.19usedtexture parametersderived fromgradient vectors and from generalized co-occurrencematrices for the characterization of texture of someMR-T2 brain images, in order to demonstrate patho-logical conditions with widespread manifestations,resulting in the change in the textural appearance of

    the brain. They used extended multisort co-occur-rence matrices that involve intensity, gradient andanisotropy image features in a uniform way, forseparation between the brain images of controls andpatients suffering from white-matter encephalopathyand/or Alzheimers disease. They also applied these

    texture features to the segmentation of diffuse brainlesions.20

    Herlidou et al.21 used texture parameters basedon the histogram, co-occurrence matrix, gradientand run-length matrix for the characterization ofhealthy and pathological human brain tissues (whitematter, grey matter, cerebrospinal fluid, tumoursand oedema). They succeeded in distinguishing thedifferent brain tissues, and confirmed that MRimages, including those obtained during routineprocedures in three different MRI units, containtissue-specific texture features which can be

    extracted by mathematical methods.In a series of studies of T1-weighted cerebral MRimages, Bernasconi et al.7 and Antel et al.22,23

    manipulated a combination of texture parameters todetermine cortical thickness and hyperintense T1signal, and to model the blurring of the greymatter/white matter interface. They managed inthat way automatically to detect lesions of focalcortical dysplasia, some of which would have beenmissed by the human eye. They assert that thedeveloped computer-based, automated method maybe usefulin thepresurgical evaluation of patients withsevere epilepsy related to focal cortical dysplasia.23

    Mahmoud et al.24 used the texture analysisapproach based on a three-dimensional co-occur-rence matrix in order to improve brain tumourcharacterization. They carried out a comparativestudy to evaluate the performance of this approachcompared with the two-dimensional approach, usingT1-weighted MRI of 7 patients with glioma todistinguish between solid tumour, necrosis, oedemaand surrounding white matter. With the three-dimensional approach they achieved better discrimi-nation between necrosis and solid tumour as well asbetween oedema and solid tumour. They did not

    manage completely to separate peritumoral whitematter from oedema, nor far ipsilateral matter fromcontralateral white matter, using either of thesemethods. They suggest, however, that the proposedthree-dimensional approach could provide a new toolfor tumour grading and treatment follow-up, as wellas for surgery or radiation therapy planning.

    Hippocampus and epilepsy

    Yu et al.25 performed a study with patients withunilateral temporal lobe epilepsy characterized on

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    MRI by ipsilateral hippocampal sclerosis and anapparently normal contralateral hippocampus.They first ascertained the existence of texturedifferences between normal (control) and sclerotichippocampi. Next they showed that the apparentlynormal contralateral hippocampi could be classified

    into three categories in terms of texture: appar-ently healthy, similar to sclerosis; or different fromeither healthy or sclerotic. They attributed thesefindings to a certain degree of hippocampal altera-tion, requiring further investigation to improvecharacterization. Bonilha et al.8 and Coelhoet al.10 confirmed the findings using textureparameters based on run-length and co-occurrencematrices. A similar study was undertaken by Jafari-Khouzani et al.,26 this time using wavelet-basedtexture features in order to distinguish healthyfrom pathological hippocampal tissue, aiming to aidphysicians in the determination of candidates forepilepsy surgery.

    Multiple sclerosis

    Mathias et al.13 applied texture analysis to MRI ofthe spinal cord in an attempt to quantify patho-logical changes that occur in multiple sclerosis(MS). Texture differences were detected betweennormal controls and relapsing-remitting MS patientsbefore spinal cord atrophy was visually detectable.They also found a significant correlation betweentexture changes and disability.

    Cervix lesions classification

    Ji et al.12 used texture analysis for characterizingand recognizing typical, diagnostically most import-ant, vascular patterns relating to cervical lesionsfrom colposcopic images. They introduced a gen-eralized texture analysis technique, where conven-tional statistical and structural textural analysisapproaches were combined, thus creating a set oftexture measures that described the specificcharacteristics of cervical textures as perceived

    by medical examinations. With those measures theydemonstrated the effectiveness of the proposedapproach in discriminating between cervical tex-ture patterns indicative of different stages ofcervical lesions.

    Obstructive lung diseases

    Chabat et al.15 used 13 texture parameters, derivedfrom the histogram, co-occurrence matrix and run-length matrix categories, to differentiate betweena variety of obstructive lung diseases in thin-section

    (CT) images. A set of CT images was obtained fromhealthy subjects and from patients with panlobularemphysema, centrilobular emphysema and con-strictive obliterative bronchiolitis. They demon-strated the feasibility of textural distinctionbetween those diseases, which cause decreased

    attenuation of the lung parenchyma, and the lungsof healthy subjects. They concluded that theaccuracy of the method was high, and suggestedthat it should be included as one of the main CTfeature extractors for the automated detection ofobstructive lung diseases.

    Conclusions

    We have described here the technique of texture

    analysis in medical images. Texture parameters aresimply a mathematical representation of imagefeatures that can be characterized in words assmooth, rough, grainy and so on. This implies that inprinciple, texture analysis may be applied to any setof image regions that may be differentiated by suchdescription.

    In outlining the main categories of textureparameters, and the several uses of each tech-nique, MRI applications have been emphasizedexcept in the work of Ji et al. with colposcopicimages12 and Chabat et al. with CT.15 MRI appli-

    cations dominate in the literature about thistechnique because, although texture analysis is amethod devised to extract from medical imagesadditional information that is not easily depicted byvisual inspection, such analysis remains limited bythe restricted resolution of images. It is therefore apromising method linked to future improvement inthe quality of medical images.

    However, the technique is by no means limited toMRI, and can be applied in the setting of differentimage applications, taking into consideration thelimitations of each imaging method. Furthermore,the application of texture parameters is not specific

    to the illnesses discussed herein, but is helpful inthe investigation of other pathological conditions inwhich imaging is an appropriate investigationmethod.

    Acknowledgements

    This work was partially supported by a grant fromFundacao de Ampara a Pesquisa do Estado de SaoPaulo (FAPESP) (Proc. N. 02/00275-5).

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