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Imaging and Cancer: a Review MOLECULAR ONCOLOGY 2 (2008) 115–152 available at www.sciencedirect.com www.elsevier.com/locate/molonc Review Imaging and cancer: A review Leonard Fassa,b,* aGE Healthcare, 352 Buckingham Avenue, Slough, SL1 4ER, UK bImperial College Department of Bioengineering, London, UK ARTICLE INFO ABSTRACT Article history: Multiple biomedical imaging techniques are used in all phases of cancer management. Im- Received 6 March 2008 aging forms an essential part of cancer clinical protocols and is able to furnish morpholog- Received in revised form ical, structural, metabolic and functional information. Integration with other diagnostic 28 April 2008 tools such as in vitro tissue and fluids analysis assists in clinical decision-making. Hybrid Accepted 29 April 2008 imaging techniques are able to supply complementary information for improved staging Available online 10 May 2008 and therapy planning. Image guided and targeted minimally invasive therapy has the promise to improve outcome and reduce collateral effects. Early detection of cancer Keywords: through screening based on imaging is probably the major contributor to a reduction in Imaging mortality for certain cancers. Targeted imaging of receptors, gene therapy expression Cancer and cancer stem cells are research activities that will translate into clinical use in the Diagnosis next decade. Technological developments will increase imaging speed to match that of Staging physiological processes. Targeted imaging and therapeutic agents will be developed in Therapy tandem through close collaboration between academia and biotechnology, information Tracers technology and pharmaceutical industries. Contrast ª 2008 Federation of European Biochemical Societies. Published by Elsevier B.V. All rights reserved. 1. Introduction The future role of imaging in cancer management is shown in Figure 2 and is concerned with pre-symptomatic, minimally Biomedical imaging, one of the main pillars of comprehensive invasive and targeted therapy. Early diagnosis has been the cancer care, has many advantages including real time monitor- major factor in the reduction of mortality and cancer manage- ing, accessibility without tissue destruction, minimal or no in- ment costs. vasiveness and can function over wide ranges of time and size Biomedical imaging (Ehman et al., 2007) is playing an ever scales involved in biological and pathological processes. Time more important role in all phases of cancer management (Hill- scales go from milliseconds for protein binding and chemical man, 2006; Atri, 2006). These include prediction (de Torres reactions to years for diseases like cancer. Size scales go from et al., 2007), screening (Lehman et al., 2007; Paajanen, 2006; molecular to cellular to organ to whole organism. Sarkeala et al., 2008), biopsy guidance for detection (Nelson The current role of imaging in cancer management is et al., 2007), staging (Kent et al., 2004; Brink et al., 2004; Shim shown in Figure 1 and is based on screening and symptomatic et al., 2004), prognosis (Lee et al., 2004), therapy planning disease management. (Ferme´ et al., 2005; Ciernik et al., 2003), therapy guidance * Corresponding author. Tel.: þ44 7831 117132; fax: þ44 1753 874578. E-mail address: [email protected] 1574-7891/$ – see front matter ª 2008 Federation of European Biochemical Societies. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.molonc.2008.04.001 116 MOLECULAR ONCOLOGY 2 (2008) 115–152 membrane antigen (PSMA), MC-1 receptor, somatostatin re- Developing Initial Disease progression Molecular symptoms ceptors, transferrin receptors and folate receptors have been Signature developed. In vitro, cellular, preclinical and clinical imaging are used Screening Diagnosis & Treatment & Follow-up Staging Monitoring in the various phases of drug discovery (Figure 3) and inte- grated in data management systems using IT (Hehenberger et al., 2007; Czernin et al., 2006; Frank and Hargreaves, 2003; Imaging Imaging Surgery Imaging Mammography Endoscopy Cath Lab Non specific Tatum and Hoffman, 2000). Colonography Cath Lab Radio, markers In vitro imaging techniques such as imaging mass spec- Non specific Biopsies Thermal & trometry (IMS) can define the spatial distribution of peptides, markers Chemo Therapy proteins and drugs in tumour tissue samples with ultra high resolution. This review will mainly consider the clinical imag- Figure 1 – Current role of imaging in cancer management. ing techniques. The development of minimally invasive targeted therapy and locally activated drug delivery will be based on image (Ashamalla et al., 2005), therapy response (Neves and Brindle, guidance (Carrino and Jolesz, 2005; Jolesz et al., 2006; Silver- 2006; Stroobants et al., 2003; Aboagye et al., 1998; Brindle, 2008) man et al., 2000; Lo et al., 2006; Hirsch et al., 2003). recurrence (Keidar et al., 2004) and palliation (Belfiore et al., Most clinical imaging systems are based on the interaction 2004; Tam and Ahra, 2007). of electromagnetic radiation with body tissues and fluids. Ul- Biomarkers (Kumar et al., 2006) identified from the genome trasound is an exception as it is based on the reflection, scat- and proteome can be targeted using chemistry that selectively tering and frequency shift of acoustic waves. Ultrasound also binds to the biomarkers and amplifies their imaging signal. interacts with tissues and can image tissue elasticity. Cancer Imaging biomarkers (Smith et al., 2003) are under develop- tissues are less elastic than normal tissue and ultrasound ment in order to identify the presence of cancer, the tumour elastography (Hui Zhi et al., 2007; Lerner et al., 1990; Miyanaga stage and aggressiveness as well as the response to therapy. et al., 2006; Pallwein et al., 2007; Tsutsumi et al., 2007) shows Various pharmaceutical therapies are under development promise for differential diagnosis of breast cancer, prostate for cancer that are classed as cytotoxic, antihormonal, molec- cancer and liver fibrosis. ular targeted and immunotherapeutic. The molecular tar- Endoscopic ultrasound elastography (Sa˜ftoiu and Vilman, geted therapies lend themselves to imaging for control of 2006) has potential applications in imaging of lymph nodes, their effectiveness and include signal transduction inhibitors, pancreatic masses, adrenal and submucosal tumours to avoid angiogenesis inhibitors, apoptosis inducers, cell cycle inhibi- fine needle aspiration biopsies. tors, multi-targeted tyrosine kinase inhibitors and epigenetic Ultrasound can be used for thermal therapy delivery and is modulators. also known to mediate differential gene transfer and expres- In order to obtain the health benefit from understanding sion (Tata et al., 1997). the genome and proteome requires spatial mapping at the The relative frequencies of electromagnetic radiation are whole body level of gene expression and molecular processes shown in Figure 4. High frequency electromagnetic radiation within cells and tissues. Molecular imaging in conjunction using gamma rays, X-rays or ultraviolet light is ionizing and with functional and structural imaging is fundamental to can cause damage to the human body leading to cancer (Pierce achieve this result. Various targeted agents for cancer et al., 1996). Dosage considerations play an important part in markers including epidermal growth factor receptor (EGFR) re- the use of imaging based on ionizing radiation especially for ceptors, avb3 integrin, vascular endothelial growth factor paediatric imaging (Brix et al., 2005; Frush et al., 2003; Byrne (VEGF), carcinoembryonic antigen (CEA), prostate stimulating and Nadel, 2007; Brenner et al., 2002; Slovis, 2002). Future Genetic DNA Pre- Disease Bench to Bedside Predisposition mutation symptomatic regression Basic Hypothesis therapy research generation Diagnosis & Treatment & Follow-up Screening Target Lead Staging Monitoring Target ID Lead ID validation Optimization In vivo/In vitro Animal Phase 0 Toxicology Specific Molecular Image guided Non-invasive efficacy Models markers imaging min-invasive quantitative & Molecular Quantitative surgery & functional Bedside to Bench Phase I Phase II Phase III Diagnostics & functional local/targeted imaging (MDx) whole-body drug delivery Molecular imaging Drug tracking imaging Manufacturing Distribution Cellular Imaging Comp Aided Tissue analysis Molecular diagnostics Diagnostics Molecular Preclinical imaging Sales & Diagnostics (MDx) Phase IV Mrketinga 10 (MDx) Clinical imaging Figure 2 – Future role of imaging in cancer management. Figure 3 – Imaging in the drug discovery process. MOLECULAR ONCOLOGY 2 (2008) 115–152 117 NIRF Ultrasound OCT ODIS Imaging NM/PET PAT DYNOT TV satellite dish 100keV 10keV Micro Ultra- Milli- X Ray Visible Infrared THz Gap -wave violet metre and RF 1019Hz 1018Hz 1017Hz 1016Hz 1015Hz 1014Hz 1013Hz 1012Hz 1011Hz 1010Hz Frequency Terahertz Pulse Imaging TPI X Ray/CT Magnetic Resonance Imaging Ionizing Non-Ionizing Imaging MRI Figure 4 – Frequency spectrum of electromagnetic radiation imaging technologies. systems may need to integrate genetic risk, pathology risk and The concept of only using tumour volume as a measure scan radiation risk in order to optimize dose during the exam. of disease progression has been shown to be inadequate as Non-ionizing electromagnetic radiation imaging tech- it only can show a delayed response to therapy and no indi- niques such as near infrared spectroscopy, electrical imped- cation of metabolism and other parameters. This has led to ance spectroscopy and tomography, microwave imaging the
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