European Journal of Radiology

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1 European Journal of Radiology 72 (2009) Contents lists available at ScienceDirect European Journal of Radiology journal homepage: Review Dual energy subtraction: Principles and clinical applications Peter Vock, Zsolt Szucs-Farkas Dept. of Diagnostic, Interventional and Paediatric Radiology, University of Bern, Inselspital, CH-3010 Bern, Switzerland article info abstract Article history: Received 1 March 2009 Accepted 23 March 2009 Keywords: Energy subtraction Chest radiography Calcification Nodule Two technical solutions using single or dual shot offer different advantages and disadvantages for dual energy subtraction. The principles of these are explained and the main clinical applications with results are demonstrated. Elimination of overlaying bone and proof or exclusion of calcification are the primary aims of energy subtraction chest radiography, offering unique information in different clinical situations Published by Elsevier Ireland Ltd. 1. Introduction Among all radiographic projection examinations, chest radiography is most frequently performed worldwide. Despite its general information about many thoracic organs, it has become obvious during the last three decades that alternative examinations often are superior to chest radiography in answering specific questions, such as echocardiography and ultrasonography for cardiac pathology and pleural effusions respectively, or CT for pulmonary and mediastinal disease. But often, it is not justified medically, ethically and economically to perform several different chest examinations, e.g. when the suspicion for one specific disease is not high enough. Radiation exposure as well as cost may be good reasons against these alternative modalities as well. Chest radiography, therefore, still plays an exquisite part among all imaging examinations, and it seems appropriate to optimise this basic imaging examination of the chest by integrating technical advances. The most important development has been the introduction of digital radiography which is characterised by excellent density resolution and allows for easy archiving, transportation to any place by the internet and for post-processing [1]. While maximum geometric resolution of digital examinations still does not reach analogue values, the advantages of the digital technique, such as the linear signal increase over a large range of increasing exposure, vastly compensate for this limitation. Digital post-processing is widely available and used, above all the windowing technique; computer-aided diagnosis (CAD) techniques are currently developed for many specific clinical questions Corresponding author. Tel.: ; fax: addresses: peter.vock@insel.ch (P. Vock), zsolt.szuecs@insel.ch (Z. Szucs-Farkas). and will soon be integrated in the ordinary diagnostic process: nodule detection and temporal subtraction to increase the sensitivity for a new lesion are typical examples and are discussed in other articles of this issue. Other post-processing applications, such as tomosynthesis and energy subtraction radiography (ES), will not as fast become a standard component of daily work since they require additional hardware and, thus, will not be available to the majority of clinical users until their value has been proven by evidence-based clinical research. 2. Methods: two principles of energy subtraction radiography Energy subtraction physically is based on the fact that X- ray attenuation of materials differs depending on the energy of roentgen-photons [1 3]. At higher X-ray energies (roughly >100 kvp), Compton scatter prevails, and absorption is less different for bone and soft tissues than at lower energies where photoelectric absorption is the most important mechanism. Photoelectric absorption, however, is much more effective with atoms of high atomic number (such as calcium) than with hydrogen, carbon and oxygen, the dominant atoms in soft tissues. Despite the fact that X-ray tubes produce spectra rather than monoenergetic photons, using different kvp will significantly influence X-ray absorption. Both technical approaches currently used for energy subtraction radiography produce two radiographs, one at higher and one at lower kvp Single-shot ES radiography The single-shot technique uses a single exposure to produce a normal chest radiograph, a bone image and a soft tissue image (Fig. 1). The cassette contains a thin copper filter sandwiched between two phosphor computed radiography (CR) plates. The X/$ see front matter 2009 Published by Elsevier Ireland Ltd. doi: /j.ejrad

2 232 P. Vock, Z. Szucs-Farkas / European Journal of Radiology 72 (2009) Fig. 1. The principle of single exposure dual energy subtraction radiography. Fig years old female patient with bronchioloalveolar carcinoma of the left upper lobe. (a/b) PA and lateral chest radiographs: note the difficulty of detecting the lesion in the left upper lobe. (c) ES soft tissue image: the density is easily seen after subtraction of the left clavicle and the 1st/5th ribs. (d) CT confirms a mixed, mostly solid density lesion. X-ray beam reaching the first CR plate produces a normal chest radiograph containing bones and soft tissues. The second plate is reached by a smaller number of mostly high energy roentgen photons which have passed the first image plate and the filter. Due to the high energy and low photon count, the image generated on the second plate has low bone contrast and is also noisier than the normal image on the first plate. The higher noise of single-shot radiographs compared to dual-shot images is partially compensated by noise suppression during image postprocessing. To generate a bone image, the signal of the high-energy image on the second plate is enhanced till the intensity from the soft tissues reaches that on the low-energy image on the first plate; weighted subtraction of these images results in canceling the soft tissue signal, leaving only bones and calcified structures visible (bone image). To generate the soft tissue image, the signals of the high-energy image on the second plate are adjusted to equalize the intensity of bones on both plates; weighted subtraction of these images again produces the soft tissue image. Table 1 Energy subtraction (ES) radiography: single vs. dual shot technique. Single-shot ES Double-shot ES Advantage Usual radiation exposure Lower image noise No motion artefacts Better subtraction Disadvantage Noisier image Motion artefacts Limited energy separation Slightly elevated radiation exposure

3 P. Vock, Z. Szucs-Farkas / European Journal of Radiology 72 (2009) Fig years old male patient after kidney transplantation. (a) PA chest radiograph and (b) soft tissue image of PA chest radiograph show diffuse interstitial, mostly reticular densities with some ground glass component. In this situation, ES does not detect but better demonstrate the distribution of diffuse lung disease Dual-shot ES radiography In the dual-shot technique, the high and low energy radiographs are generated by two exposures. The system uses a flat panel detector with superior detective quantum efficiency (DQE), as compared to the phosphor plates. The detector is consecutively exposed twice at two different energy levels, typically at 120 and 60 kv, generating two radiographs and allowing for weighted subtraction. The use of the highly sensitive digital detector results in a superb image quality with high contrast and low image noise. Furthermore, the energy spectra of the two images are better separated than by the copper filter in the single-shot technique, resulting in a very good bone subtraction. However, the short interval of ms between the two successive exposures renders the images susceptible to cardiac, respiratory and muscular motion artifacts. Thus, postprocessing is necessary to reduce these artifacts which are most expressed at the heart border, the level of the diaphragm and the hilar vessels. Table 1 shows the relative advantages and disadvantages of singleand dual-shot ES radiography Dose aspects in ES radiography In the single-shot approach, the first CR plate needs an exposure identical to chest radiography without ES; in order to get a better signal-to-noise ratio of the second plate, however, the mas value is slightly increased by many users. Dual-shot ES radiography, by definition, needs a second low-energy exposure in addition to the ordinary high-energy projection, increasing exposure [2,3]. However, the portion of this extra radiation equals only about 15% of an ordinary biplanar chest radiograph, since the flat panel detector is more sensitive than the phosphor plate and requires a lower mas for a single exposure to reach the same image quality. Since exposure is low on posteroanterior projections as compared to lateral projections, most users argue that the difference is negligible and may be compensated by minimally lowering mas of the lateral projection and by the high DQE of flat panel detectors. Exposure, however, is the reason for not using ES with lateral projections. Fig. 4. Preoperative chest radiograph in a female patient of 82 years of age with lumbar spinal stenosis. PA chest radiographs: (a) standard view, (b) bone and (c) soft tissue image. Numerous calcified foci of a few millimetres of diameter are detected on (a) and more obvious on (b) but disappear on (c). In addition, there are also numerous calcified hilar and mediastinal lymph nodes; the combination corresponds to tuberculous calcified primary complexes.

4 234 P. Vock, Z. Szucs-Farkas / European Journal of Radiology 72 (2009) Fig years old man with Ewing s sarcoma. (a c) PA chest radiograph using ES, (d) CT image at left upper lobe. Note that calcification (c) of this pulmonary metastatic nodule is seen despite the overlap of the left clavicle, and it is confirmed by CT. Currently, due to the special hardware needed, even large departments usually either do not offer ES radiography at all, or they have just one of the two techniques available. This is also true for our department, and all illustrations of this article will be based on single-shot ES. 3. Applications of energy subtraction radiography From the beginning, it has been the principle aim of energy subtraction to eliminate overlaying bones that often make the detection of pulmonary pathology difficult [4] (Table 2). For example, Austin et al. showed that 81% of missed lung cancers were located in the upper lobes [5] where ribs and clavicles often obscure the visualisation of the lung; in 23 of 27 missed cancers, ribs were a major reason for the failure of detection, often combined with the clavicles or major lung vessels. Successful elimination of the bones, therefore, is pointed out as the major advantage of ES and reason for a better sensitivity in most articles [3,6 9]. The most obvious advantage results for nodule detection [10 14], as needed in primary lung cancer and in haematogenous lung metastases (Fig. 2). Similarly, tiny benign lesions often are better visible after bone subtraction; this is true for the detection of active versus scarred tuberculosis or invasive aspergillosis in immunocompromised patients [15]. ES improves the characterization of focal and the visualisation of distribution of diffuse lung disease and, thus, may help in their differentiation [3] (Fig. 3). It shows the central tracheobronchial tree in continuity and enhances the recognition of stenosis and mediastinal masses [2,15]. Beyond the elimination of superimposed bone, ES is a sensitive tool to prove or exclude calcification [2,3]. Calcified nodules most often are of benign origin, representing granuloma, hamartoma or a scar (Fig. 4). The exception is pulmonary metastasis in case of a calcified or ossified primary neoplasm; however, this is usually Fig years old female with dyspnoea and a history of tuberculosis many decades ago. (a c) PA and lateral chest radiographs clearly show the post-infectious shrinkage of the left chest due to pleuritic scarring and calcification.

5 P. Vock, Z. Szucs-Farkas / European Journal of Radiology 72 (2009) Fig. 7. Postinterventional radiograph after implantation of a defibrillator electrode and a pacemaker in a male of 77 years. Standard PA radiograph (a) and corresponding bone image (b) show a slight protrusion of the left cardiac border with a rim of calcification, corresponding to a false aneurysm after myocardial infarction. Fig. 8. Pseudonodule in a 62 years old female patient with rheumatoid arthritis. (a) PA chest radiograph shows a rounded density projecting in a right-sided lower or middle lobe location; on the lateral projection (b) there is no correlate. On the soft tissue image (c), the nodule fades away, and on the bone image (d) calcified callus is identified, due to a fracture of the 9th rib.

6 236 P. Vock, Z. Szucs-Farkas / European Journal of Radiology 72 (2009) Table 2 Clinical applications of ES chest radiography. 1. To avoid overlap of thoracic bones To detect pulmonary lesions To characterise the density and morphology of pulmonary lesions To show the tracheobronchial lumen To detect a mediastinal mass 2. To prove calcification/ossification In lung nodule (granuloma, hamartoma, scar, metastasis of calcified neoplasm) In lymph nodes In pleural location In mediastinum: vascular, cardiac, cartilage In soft tissues including breast Callus after rib fractures, osteophytes etc. 3. To analyse the bone In congenital malformations In acquired bone disease 4. To localise foreign bodies Metallic devices/foreign bodies Indwelling devices (catheters, ports, drains) Silicon breast implants known which simplifies the recognition of malignant calcification (Fig. 5). Calcified lymph nodes are often seen in hilar or mediastinal location. Pleural calcification is enhanced and its distribution often helps in determining the etiology, both asbestos exposure [2], postinflammatory (Fig. 6) or posttraumatic. Since penetration is minimal for the mediastinum, the bone image often is very noisy here; still, it is possible to identify cardiovascular calcifications [2,15] (Fig. 7). Posttraumatic callus formation and osteophytes may simulate lung nodules; ES is an excellent tool in clarifying this situation (Fig. 8). Although this is not the primary goal, bone images from radiographs taken at 120 kvp often improve the visualisation of congenital and acquired bone disease (Fig. 9). Finally, ES easily identifies many foreign bodies and devices [2,15], whether metallic, of silicon or plastic (Fig. 10). 4. Obstacles to a wider dissemination of ES The cost of additional hardware and additional archiving space (three images instead of one) are probably the main reasons for the currently limited application of ES in radiology departments. Since it is not easy to upgrade an existing X-ray unit to ES, the Fig. 9. Pseudotumour in clavicular pseudarthrosis. 76 years old man. Ordinary (a), soft tissue (b) and bone-weighted PA chest radiographs (c). At (a), it is not easy to exclude a pulmonary apical mass or infection. The lateral projection did not reveal the lesion that was clearly shown to represent a pure clavicular problem at (c) without pulmonary pathology (b). decision has to be made with the purchase. Once ES is available and radiologists have adapted to noisy images whether young or experienced they like to use it and also feel more confident than just using ordinary radiography [12]. At the beginning, one has to adapt to elevated noise and to artifacts caused by misregistration, both potential reasons for misinterpretation. We use two commercially available high definition Fig. 10. Ordinary (a) and bone-weighted (b) PA chest radiographs in a 57 years old female with silicon breast implants. Note their detectability on the bone image, due to the fact that silicon is denser than soft tissues. This is not easily seen on the standard radiograph.

7 P. Vock, Z. Szucs-Farkas / European Journal of Radiology 72 (2009) liquid crystal display monitors for image analysis. One monitor shows the three stacked PA chest images, enabling easier lesion detection and characterization by scrolling over the normal, bone and soft-tissue images, and the other monitor displays the lateral view. To fully exploit the advantages of ES, all images are routinely analyzed. In our experience, increased reading time is not a relevant factor, due to enhanced confidence. Data are scarce in the literature on whether the specificity deteriorates with ES. In an analysis of 200 pulmonary lesions in 77 patients, we found that even experienced readers detected more false positive findings on the soft tissue images than on the normal chest radiographs [13] while Ricke et al. reported higher specificity with ES in 20 patients [12]. We think that this issue will have to be clarified by further research in large patient populations. 5. Future developments of ES techniques An immediately available gain in performance might be achieved by combining ES with a CAD system for lung nodule detection. In our initial experience, it is worth while to evaluate this approach for its clinical impact. In a few years, X-ray spectra might be replaced by specific gamma energies for gammametry and material decomposition; this might significantly improve the differentiation, diminish noise and, thus, improve the diagnostic gain. However, this needs major technical development. 6. Conclusion Energy subtraction is a valuable optional feature of chest radiography; it is ideal to eliminate overlaying bone and to recognise or exclude calcification in lesions of most anatomic locations. Hardware requirements currently limit its dissemination in the radiological community. References [1] McAdams HP, Samei E, Ill JD, Tourassi GD, Ravin CE. Recent advances in chest radiography. Radiology 2006;241(3): [2] Kuhlman JE, Collins J, Brooks GN, Yandow DR, Broderick LS. Dual-energy subtraction chest radiography: what to look for beyond calcified nodules. Radiographics 2006;26: [3] MacMahon H, Li F, Engelmann R, Roberts R, Armato S. Dual energy subtraction and temporal subtraction chest radiography. J Thorac Imaging 2008;23(2): [4] Samei E, Flynn MJ, Peterson E, William RE. Subtle lung nodules: influence of local anatomic variations on detection. Radiology 2003;228: [5] Austin JHM, Romney BM, Goldsmith LS. Missed bronchogenic carcinoma: radiographic findings in 27 patients with potentially resectable lesion evident in retrospect. Radiology 1992;182: [6] Ide K, Mogami H, Murakami T, Yasuhara Y, Miyagawa M, Mochizuki T. Detection of lung cancer using single-exposure dual-energy subtraction chest radiography. Radiat Med 2007;25(5): [7] Ishigaki T, Sakuma S, Ikeda M. One-shot dual-energy subtraction chest imaging with computed radiography: clinical evaluation of film images. Radiology 1988;168: [8] Kido S, Ikezoe J, Naito H, et al. Single-exposure dual-energy chest images with computed radiography. Evaluation with simulated pulmonary nodules. Invest Radiol 1993;28(6): [9] Kido S, Nakamura H, Ito W, Shimura K, Kato H. Computerized detection of pulmonary nodules by single-exposure dual-energy computed radiography of the chest (part 1). Eur J Radiol 2002;44(3): [10] Li F, Engelmann R, Doi K, MacMahon H. Improved detection of small lung cancers with dual-energy subtraction chest radiography. AJR 2008;90: [11] Niklason LT, Hickey NM, Chakraborty DP, et al. Simulated pulmonary nodules: detection with dual-energy digital versus conventional radiography. Radiology 1986;160: [12] Ricke J, Fischbach F, Freund T, et al. Clinical results of Csl-detector-based dualexposure dual energy in chest radiography. Eur Radiol 2003;13(12): [13] Szucs-Farkas Z, Patak MA, Yuksel-Hatz S, et al. Single-exposure dual-energy subtraction chest radiography: detection of pulmonary nodules and masses in clinical practice. Eur Radiol 2008;18: [14] Uemura M, Miyagawa M, Yasuhara Y, et al. Clinical evaluation of pulmonary nodules with dual-exposure dual-energy subtraction chest radiography. Radiat Med 2005;23(6): [15] Gilkeson RC, Sachs PB. Dual energy subtraction digital radiography: technical considerations, clinical applications, and imaging pitfalls. J Thorac Imaging 2006;21(4):

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