Is digital image compression acceptable within diabetic retinopathy screening? Digital Short Report report image compression and DR screening? A. Basu et al. Oxford, Diabetic DME Blackwell 1464-5491 20 UK Medicine Publishing Science Ltd,Ltd. 2003 A. Basu, A. D. Kamal, W. Illahi*, M. Khan*, P. Stavrou* and R. E. J. Ryder Abstract City Hospital and *Midland Eye Centre, Birmingham, UK Accepted 21 March 2003 Aims The National Screening Committee (NSC), whilst recommending the use of digital mydriatic retinal photography for diabetic retinopathy screening, has not yet accepted the use of digitally compressed images for grading. By greatly reducing the file size, however, compression of images is invaluable for storage and for its rapid transmission across computer networks. We undertook a study to compare the different levels of JPEG compression with the original bit-mapped image to determine whether there was any loss of clinical detail following compression. Methods Three hundred and thirty images were analysed in this study. These images had been captured from 66 eyes consecutively photographed in a diabetic retinopathy screening programme, using a Sony DXC-950 P 3CCD colour video camera mounted on a Canon CR6-45NMf fundus camera. Single 45° macula-centred images were taken from each eye. The images were compressed using the JPEG algorithm within Adobe Photoshop (version 4.0) and then displayed with a Sony Trinitron colour monitor. Four different levels of compression were used, JPEG-1, JPEG-2, JPEG-3, JPEG-4, and an objective analysis was undertaken using ‘lesion counts’. The compressed images were assessed separately and blindly and the results compared with their original BMP images. Results Eight BMP images could not be evaluated (five right eye and three left eye). A total of 290 images were therefore used in the final evaluation. All the JPEG-1 images with file sizes between 16 and 24 kb were found to be ‘pixelated’, while the JPEG-4 images (66–107 kb) appeared similar to the original BMP (1.3 Mb) images. Both JPEG-2 and JPEG-3 images had significantly lower counted lesions than the BMP images. Conclusions From our findings we can conclude that only some degree of image compression (compression ratios of 1 : 20 to 1 : 12) with file sizes of 66–107 kb is permissible using JPEG format, whereas the images obtained after higher compression ratios may not be suitable for diabetic retinopathy screening. Diabet. Med. 20, 766–771 (2003) Keywords digital imaging, retinal screening, image compression, JPEG Abbreviations CCD, charge-coupled device; JPEG, Joint Photographic Experts Group Introduction Correspondence to: Dr A. Basu, Clinical Research Fellow and Specialist Registrar in Diabetes, Department of Diabetes, Endocrinology and Metabolism, City Hospital, Dudley Road, Birmingham B18 7QH, UK. E-mail: [email protected] 766 The National Screening Committee (NSC) recommends the use of digital mydriatic retinal photography for diabetic retinopathy screening. It does not, however, recommend the use of digitally compressed images for grading [1]. Digital retinal © 2003 Diabetes UK. Diabetic Medicine, 20, 766–771 Short report 767 photography has distinct advantages over conventional 35mm photography despite a lower resolution of the acquired image, and has proved to be an effective screening modality in patients with established or partially treated diabetic retinopathy [2]. It allows instantaneous viewing of the retinal images, and provides an inexpensive way of printing hard copies of the images [3] that are often superior to Polaroid prints [4]. Image manipulation using a variety of image editing software may be used to improve lesion detection during the screening process [5]. More recently, computer-assisted image analysis is being used for the development of computer software that may allow automated retinopathy grading in the future [6– 9]. One of the models of diabetic retinopathy screening process which arises from the NSC recommendations envisages images captured out in the field being transmitted electronically to central grading centres for evaluation [1]. One of the limitations of such transmission over networks is the significant time delay involved in transmitting large files, which becomes increasingly problematic as higher resolution images are generated by the digital cameras. High-resolution images generate large file sizes (as more data per pixel get stored) that slow transmission and also occupy significant computer memory space during archiving. One of the solutions to this problem is to allow some degree of image compression that will maintain as much clinically relevant detail as the parent image. Among a variety of compression techniques available, the JPEG compression format is often used for graphical data as the loss of data is in the form of colour information, which may not be of clinical significance [10]. We therefore undertook a study to ascertain whether compressed digital retinal images lose clinically relevant details when compared with the parent uncompressed image, i.e. do retinal details get altered when images are digitally compressed? This allowed uniformity in the image compression ratios for all the images. This resulted in five groups of images: BMP, JPEG-1, JPEG-2, JPEG-3, JPEG-4; BMP represented the original raw image while JPEG-1, JPEG-2, JPEG-3, and JPEG-4 were image sets that had maximum, high, medium and low levels of compression, respectively. The four JPEG groups were evaluated separately from their bitmaps and these had been blinded to the grader (A.B.). A lesion count was performed under the following categories: microaneurysms (MA), haemorrhages (HGES), ‘cotton wool spots’ (CWS), and hard exudates (HE) for each of the images. A strategy using lesion counts to differentiate the images compared with conventional grading of the images was used as it was assumed that evaluation of a compressed digital image from its parent would involve subtle changes in character of the lesions rather than a change in the overall grade. For example, an image with four microaneurysms only, correctly classified as non-proliferative retinopathy, would retain the same grade even if only three out of the four microaneurysms were visible after compression. This is extremely important, as it implies a loss of clinically relevant information and must be taken into consideration in any study that attempts to evaluate digitally compressed images. The lesion counts obtained in each of the JPEG categories were compared separately with their original BMP images. For each of these categories, up to six lesions were counted; any lesion with counts ≥ 6 were labelled as ‘≥ 6’. This was done as we realized that accurate counting of microaneurysms and haemorrhages is not possible when they appear in clusters. An ‘agreement’ between a pair of images was defined only when identical lesion counts in each of the above categories (MA, HGES, CWS, HE) were found. Any discrepancy in this count between the JPEG image and its parent BMP was defined as a ‘disagreement’ in the retinopathy. Lesion counts to determine difference between colour photographs and fluorescein angiograms in detecting diabetic retinopathy have been used before [11]. We have used a similar approach. Patients and methods Results Sixty-six right and left eye images were captured from 33 consecutive patients using a Sony DXC-950 P 3CCD colour video camera mounted on a Canon CR6-45NMf camera. The patients were part of the routine attendance at diabetes retinal screening clinics at City Hospital, Birmingham, UK. The median age was 57 years (range 27–81 years). Most had Type 2 diabetes (n = 31). They were of mixed ethnicity: 14 Caucasians, 11 Asians and eight Afro-Caribbeans. Informed verbal consent was obtained from all patients. All patients had checks of visual acuity and instillation of mydriatic drops (1% Tropicamide) prior to photography. Single 45° macula-centred images were taken from each eye. The images were captured using ‘EyeCap’ software (Orion Imaging Ltd, Cumbran, UK) and a Pentium III PC and saved in Windows Bitmap (BMP) format on CD-ROM. For the purposes of this study the images were displayed using a Sony colour monitor [display resolution 1024 × 768 pixels and 24-bit (True Colour) colour display] and viewed using Adobe Photoshop (version 4.0) image editing software. This software was used to compress each individual image into four levels of JPEG compression (low, medium, high, maximum) using the JPEG compression algorithm specified within the software. Of the 66 BMP images, eight could not be graded (two BMP images had been incorrectly saved and six images had significant cataracts rendering them ungradable). A total of 290 images were therefore evaluated. The retinopathy grades for these 66 BMP images are shown in Table 1. © 2003 Diabetes UK. Diabetic Medicine, 20, 766–771 Objective assessment of images using lesion counts All the JPEG-1 images were found to be ‘pixelated’, which did not allow clear definition of lesion or vessel margins. These Table 1 Retinopathy grades (n = 66) Retinopathy grade Number of images No diabetic retinopathy Non-proliferative retinopathy Proliferative retinopathy Not gradable 26 26 6 8 768 Digital image compression and DR screening? • A. Basu et al. Agreement Disagreement Total number of pixelated images JPEG-1 16 –24 kb JPEG-2 24 –33 kb JPEG-3 37– 61 kb JPEG-4 66–107 kb 0 (0) 0 (0) 58 (100%) 36 (62%) 9 (16%) 13 (22%) 52 (90%) 6 (10%) 0 (0) 58 (100%) 0 (0) 0 (0) Table 2 Comparison of compressed images with Bitmap images (1270 kb) Numbers within cells represent the number of images. Table 3 a. Frequency of BMP images among the different lesion types Lesion count categories Lesion types ≤2 3–5 ≥6 Microaneurysms (MA) Haemorrhages (HGES) Cotton wool spots (CWS) Hard exudates (HE) 8 11 1 2 5 4 1 0 11 8 0 4 b. Reasons for disagreements Reasons for disagreement—lesion counts JPEG/BMP Number of images JPEG-2 JPEG-3 MA HGES Right eye Left eye Total 2 7 9/58 MA 3/≥ 6; MA 4/5 MA 3/6; MA 1/3; MA 2/3; MA 2/5; MA 2/3 HGES 3/4; HGES 2/3 Right eye Left eye Total 1 5 6/58 MA 4/≥ 6 MA 4/6; MA 2/3; MA 5/6; MA 4/5 HGES 1/2 Numbers within cells represent the number of images within each category. images had files sizes of 16–24 kb and were as a result of 1 : 52 to 1 : 79 compression. On the other hand, none of the JPEG-3 and JPEG-4 images was found to have been ‘pixelated’. Difference in images (disagreement based on lesion counts + total number of pixelated images) was noticed in 22/58 JPEG-2 images and 6/58 JPEG-3 images (Table 2). The data are expressed as a proportion of images in agreement or disagreement/total number of images. As this is not a k × k grading system but rather a 1 × k grading system (‘1’ representing the BMP and ‘k’ the different categories of JPEG compression), the κ statistic cannot be used. The ‘agreement’ between the images here is based on having identical lesion counts in different categories (MA, HGES, CWS, HE) between the pair of images (a ‘BMP’ and a ‘JPEG’), where the BMP image is the ‘reference standard’. Microaneurysms and haemorrhages were the predominant lesions encountered in our data set of images (Table 3a). The disagreement noted was predominantly due to reduced counting of microaneurysms in the JPEG-2 and JPEG3 images compared with their original BMP image; in JPEG-2 images 7/9 images and in JPEG-3 5/6 were as a result of a reduced counting of microaneurysms (Table 3b). This is not surprising, as small red lesions such as microaneurysms and small haemorrhages are normally difficult to detect against a red background, and it is still more likely to be the case when the images are compressed. Although the total number of images with hard exudates and cotton wool spots was less than those with microaneurysms and haemorrhages, little difference was noticeable in these lesions after compression. This may be because these lesions, being white, are better contrasted against a red retinal background and therefore more easily detectable. JPEG-1 images of course could not be compared, as they were all universally ‘pixelated’. Side-by-side comparison of the original BMP images and the JPEG-4 images revealed that they were identical as far as could be assessed by the human eye. This was confirmed after careful scrutiny of the images by several of the authors (A.B., R.E.J.R., W.I., A.D.K.) ( Figs 1 and 2). Discussion Digital images can be stored in a variety of compressed file formats. Broadly these are categorized as ‘lossy’ compression or ‘lossless’ compression formats. With ‘lossy’ compression techniques, e.g. JPEG, it is impossible to recreate the original image from the compressed image due to loss of mathematical information. In some instances the compression algorithm used © 2003 Diabetes UK. Diabetic Medicine, 20, 766–771 Short report Figure 1 Image compression of a single retinal image. © 2003 Diabetes UK. Diabetic Medicine, 20, 766–771 769 770 Digital image compression and DR screening? • A. Basu et al. Figure 2 Corresponding areas from the images cropped to focus on the subtle changes. Finer details of vessels and lesions, especially around their edges, are lost with progressive compression, whilst the grade of retinopathy remains unaltered. may be completely reversed so that the decompressed image is ‘digitally’ identical to the original—this is described as ‘lossless’ compression, e.g. TIFF. Despite being a ‘lossy’ compression technique, JPEG compression has a number of advantages. It maintains brightness and contrast information (to which the human eye is very sensitive) at the expense of some colour definition, and is therefore useful for images from film or video [12]. Second, the user can conveniently define the amount of compression necessary by adjusting certain compression parameters. Although this allows the user to trade off file size against output image quality, this difference in quality may not be noticeable to the human eye up to a certain level of compression. For this reason the JPEG algorithm is the one most commonly used for images transmitted over the internet. A number of studies have looked at digital compression of medical images with relative preservation of image quality following compression [13 –15]. Digital image compression (JPEG) of retinal and optic nerve head images for the purposes of tele-ophthalmology has been studied before on a per-lesion basis [16,17]. A study [18] attempting to evaluate the effect of image compression in the context of diabetic retinopathy screening using digitized 35-mm slides not surprisingly found that the sensitivity reduced with increasing degrees of JPEG compression. However, one of the limitations of this study was in the use of digitized images whose quality is dependent on the scanning technique and the scanners used to generate the slides. It is therefore difficult to draw any definitive conclusions from their results. In the case of digitally acquired images as are generated by modern digital retinal cameras, the image quality is specified at the time of capture. In our study we used digitally acquired images, as would be expected during routine retinopathy screening. We also emphasize that while it is important to detect changes in individual lesions following compression, viewing these changes within the context of the entire retinal image is necessary rather than the component parts in isolation as has been done before [17]. In other words, whilst it may be possible to detect hard exudates clearly in one image, it may not be possible to detect a small microaneurysm in the same image, and this is undoubtedly important from the grader’s perspective. Although the total number of images in our data set was small, 40% (23/58) of the images had a large number (≥ 6) of lesions per image. However, the numbers of images with hard exudates and cotton wool spots were few, and whilst we feel that our findings are unlikely to be different even if a larger data set were used, this could be further confirmed using images with many such lesions per image. In this study we used a specific range of compressions and analysed their effects on diabetic retinopathy lesions. Therefore, whilst we can conclude that some degree of image compression may be acceptable [such as the JPEG-4 images with file sizes of 66–107 kb (compression ratios of 1 : 20 to 1 : 12)], we cannot use our study results to specify the optimum compression ratio that can be accepted as a standard across the board. We also recognize that some grading centres may have large computer storage capacities and have transmission lines that allow a broad bandwith, in which case such image compression may not be necessary. However, with the availability of less expensive high-resolution digital cameras (such as the Canon D-30), large image file sizes will be inevitable and one may then need to consider carefully some © 2003 Diabetes UK. Diabetic Medicine, 20, 766–771 Short report image compression options. The optimum JPEG compression ratios for these higher resolution images, however, need to be studied separately. Our study may open an opportunity for diabetic retinopathy screening centres to evaluate JPEG compressed images at a local level, and decide their optimum method for archiving and transmission of such images electronically and could also perhaps be carefully considered within the national screening guidelines. Appendix 1: useful definitions [12,19] Pixel: This is the short for ‘picture elements’; it represents the smallest point in a graphic image. Pixelated: The appearance of pixels in a bit-mapped image— when an image is displayed or printed too large the individual square pixels are discernible to the naked eye. Bit-mapped image: The representation of an image as rows and columns of dots, in the computer’s memory. The value of each dot (whether it is filled in or not) is stored in one or more ‘bits’ of data. The density of the dots, known as the resolution, determines how sharply the image is represented. This is often expressed in dots per inch (dpi) or simply by the number of rows and columns, such as 640 × 480. These bit-mapped images can be stored as a BMP (MS Windows environment), TIFF (tagged image file format) or PCX files. JPEG image ( Joint Photographic Experts Group): JPEG (pronounced ‘jay-peg’) is a standardized image compression mechanism. This compression algorithm is now available in most image-editing software, and in our study we used Adobe Photoshop (version 4.0). 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