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- W2154201863 abstract "For the greater part of the last century, basic science research has been limited to in vitro studies of cellular processes and ex vivo tissue examination from suitable animal models of disease. In the last three decades, however, new techniques have been developed that permit the imaging of live animals using X-rays, radiotracer emissions, magnetic resonance signals, sound waves and optical fluorescence, and bioluminescence. The objective of this review is to provide a broad overview of common animal imaging modalities, with a focus on positron emission tomography (PET), single photon emission computed tomography (SPECT), and computed tomography (CT). Important examples, benefits, and limits of microPET/SPECT/CT technologies in current use, and their central role in improving our understanding of biological behavior and in facilitating the development of treatments from bench to bedside are included. For the greater part of the last century, basic science research has been limited to in vitro studies of cellular processes and ex vivo tissue examination from suitable animal models of disease. In the last three decades, however, new techniques have been developed that permit the imaging of live animals using X-rays, radiotracer emissions, magnetic resonance signals, sound waves and optical fluorescence, and bioluminescence. The objective of this review is to provide a broad overview of common animal imaging modalities, with a focus on positron emission tomography (PET), single photon emission computed tomography (SPECT), and computed tomography (CT). Important examples, benefits, and limits of microPET/SPECT/CT technologies in current use, and their central role in improving our understanding of biological behavior and in facilitating the development of treatments from bench to bedside are included. Animal investigation has been an integral component of biomedical research for the last 100 years, but has been limited to in vitro studies of cellular processes and ex vivo tissue examination from suitable animal models of disease. In the past 30 years, and particularly in the past decade, improvements in computer hardware and software capabilities have enabled whole-body animal imaging to complement the traditional in vitro and ex vivo study techniques. Whole-body imaging using positron emission tomography (PET), single photon emission computed tomography (SPECT), and computed tomography (CT) scanning have revolutionized clinical imaging and with increasing miniaturization of components, these techniques have become available to facilitate small animal research as well. Some of the impetus to develop in vivo imaging has come from recognition of improvements in imaging technologies by the National Institute of Biomedical Imaging and Bioengineering (NIBIB), established by the National Institutes of Health (NIH).1Hendee W.R. Chien S. Maynard C.D. Dean D.J. The National Institute of Biomedical Imaging and Bioengineering: history, status, and potential impact.Radiology. 2002; 222: 12-18Crossref PubMed Scopus (20) Google Scholar It has been understood that longitudinal imaging techniques could permit improvement of the scientific information obtained by using animals as their own controls. The NIBIB explicitly announced that “…Small animal imaging provides the means to address … the non-invasive monitoring of biological processes, disease progression, and response to therapy, with the potential to provide a natural bridge to the clinical environment and contribute substantially to the development of hum an medicine.” [Systems and Methods for Small Animal Imaging (SBIR/STTR), http://grants.nih.gov/grants/guide/rfa-files/RFA-EB-03-002.html, last accessed December 6, 2012]. Another part of the impetus has come from the Association for Assessment and Accreditation of Laboratory Animal Care (AAALAC). This voluntary organization has given voice to the growing consensus that animal research should be performed in a humane manner, considering animal welfare as well as scientific benefit. AAALAC as well as other state and federal agencies adhere to the principles of the three Rs—replacement, reduction, and refinement—first articulated by Russell and Burch.2Russell W. Burch R. The principles of humane experimental technique. London, Methuen1959Google Scholar In this context, imaging devices are seen as technical refinements because they are less invasive than older diagnostic and monitoring techniques. The reduction of animal sacrifice through serial study using the same animals as their own controls simultaneously permits improved statistics of paired observations, thus enhancing the scientific value of the observations. Magnetic resonance imaging (MRI) on a human and animal scale was conceived as an imaginative extrapolation from the use of magnetic resonance spectroscopy performed on small tissue samples. Optical imaging also was used for in vitro cellular imaging, but is now available for whole-animal imaging of fluorescent proteins and bioluminescent markers. By contrast, other small animal imaging devices evolved from similar devices first used clinically in humans. CT, PET, and SPECT were first applied to human subjects before technology advanced sufficiently to permit miniaturization for the purpose of imaging small animals. Superposition of different types of images such as CT and PET is known as image co-registration and can be performed using software that aligns images obtained on separate instruments. More recently, hybrid instruments such as PET/SPECT/CT and PET/MRI have become available, improving the limitations of separate image acquisitions. The co-registration technique has been available in human devices for several years, permitting direct comparison of anatomical and functional findings, and is now also offered on instruments for animal study. Imaging of living animals offers the following three significant advantages over older methods in biomedical investigations:1.By using animals as their own controls, imaging of living animals reduces the number of animals sacrificed, simultaneously improving statistics, with consequential scientific benefit.2.Diagnostic and therapeutic agents can be developed and tested on nearly identical molecular synthesis platforms. Imaging and quantification of these agents can directly identify their biodistribution, pharmacodynamics, and kinetics, thus providing a uniquely straightforward translational paradigm.3.By enabling longitudinal studies, imaging of living animals allows continuous, dynamic, and sometimes nearly instantaneous identification/quantification of disease progression and, in many cases, treatment. These capabilities, especially assessing drug efficacy noninvasively, are major focuses of the NIH/National Cancer Institute (NCI) and provide value added approaches to preclinical studies. PET scanners are in common use in clinical practice particularly for the diagnosis and management of cancers. This familiar application is widely performed today using hybrid PET/CT instruments. The most common radiotracer used in humans is 18F-2-deoxy-2-fluoro-D-glucose (FDG) because of its behavior as a glucose congener. This property allows FDG to provide increased specificity in evaluation of a wide variety of aggressive glycolytic cancers, due to their widespread overexpression of glucose 1 transporters and of hexokinase, causing FDG-phosphate to be trapped within cells. SPECT scanners and, more recently, SPECT/CT scanners are also in common clinical practice using a wide variety of radiotracers for procedures such as bone scans, myocardial perfusion imaging, lung perfusion/ventilation imaging, hepatobiliary imaging, as well as studies of any other organ systems. Similar radioactive tracers can be targeted for in vivo animal imaging in analogous clinical PET/SPECT/CT devices and by the same physiological uptake mechanisms. Therefore, administration of radiotracer molecules, imaged at unrivaled picomolar concentrations,3Gambhir S.S. Molecular imaging of cancer with positron emission tomography.Nat Rev Cancer. 2002; 2: 683-693Crossref PubMed Scopus (1364) Google Scholar provides uniquely noninvasive, nontoxic, quantitative, longitudinal, functional images of physiological health as well as diagnosis and mechanisms of disease, obviously scalable for creatures of widely different sizes. The addition of CT on the same imaging gantry allows precise anatomical co-registration of functional information with anatomy, just as in human-scale instruments. Figure 1 shows the co-registered PET/CT images of a mouse with metastatic breast cancer in the lungs. PET, SPECT, CT, and MRI, whether used separately or together, as described above, now permit high-resolution anatomical and physiological images in small animal models of health and disease. CT provides cross-sectional anatomical imaging with resolution from 100 μm to 50 μm in living animals. A resolution of 20 μm and better must be reserved for terminal experiments because fine resolution comes at the expense of higher radiation–absorbed dose effects on animals, requiring sacrifice of the animals at the conclusion of these experiments. Resolution for PET and SPECT depends on the particulars of instrument specifications, but 1.3 mm or better is not uncommon for modern PET, and less than 1.0 mm resolution can be achieved in certain SPECT configurations. The limit of what can be done biologically depends on the choice and availability of radiotracers. FDG, for PET studies, is widely used as a surrogate for tumor metabolism in animal models of cancer to monitor therapeutic responses noninvasively in serial studies. When coupled with CT, tumor localization can be improved and tumor heterogeneity can also be explored. FDG, as a general marker of metabolism, can also be used in cardiac imaging as well as in inflammation and infectious disease. Sodium fluoride (18F-NaF), a PET bone tracer, in combination with CT is ideal for studying arthritis and general bone and joint diseases. 18F-NaF PET is more sensitive than CT for measuring osteoblast activity, but CT can measure joint space narrowing and can demonstrate osteophyte formation and trabecular bone structure. 3′-Deoxy-3′-18F-fluorothymidine (18F-FLT) can be used to measure cell proliferation, making it a good candidate to monitor stem cell growth, analogous to iododeoxyuridine used in vitro. 124I, naturally, has a role in evaluating thyroid function as well as all organs which express the sodium iodide symporter, including breast tissue, choroid plexus, gastric mucosa, and salivary glands. 64Cu has been used in the evaluation of Wilson’s disease. Both 124I and 64Cu may be conjugated to other biological molecules of interest. The palette of tracers available for SPECT imaging is even broader as they all are used clinically. 99mTechnetium (99mTc) is the most widely used radiotracer in the world. It is a waste product of nuclear reactors (daughter of the decay of 99molybdenum by β decay) and is therefore relatively inexpensive. It is used to label radiotracers including i) methylene diphosphate (MDP) for bone and joint imaging; ii) mebrofenin for hepatocyte function and hepatobiliary excretion; iii) macroaggregated albumin (MAA) for regional organ perfusion and especially pulmonary perfusion; and iv) methyl isobutyl isonitrile (MIBI) for cardiac perfusion experimental models of ischemic heart disease. MIBI has also been used to image and localize parathyroid adenomas. For academic institutions, an on-site or nearby cyclotron as well as the capacity to synthesize organic molecules makes possible an almost infinite variety of radiotracers, especially short-lived compounds labeled with 11C (20 minute half-life), 13N (10 minutes.), and even 15O (2 minutes). Brain receptor imaging with 11C raclopride has achieved wide use for evaluation of schizophrenia due to dopamine 2 (D2) receptor binding. Tropane derivatives are used in Parkinson’s disease, and amyloid-seeking labels are used to monitor Alzheimer’s disease. The variety of uses is constrained only by the limits of organic chemistry synthesis, although the expense of cyclotron use and synthesis is substantial. The potential for neuroscience imaging is enormous when PET is coupled with MRI to provide high-resolution anatomy of the brain, function derived from informed use of magnetic sequences, and metabolism/function from PET tracers. Theranostics, combining diagnostics and therapeutics, has become increasingly important with advances in nanotechnology and molecular imaging. In many ways theranostics is not new to nuclear medicine, as the classic application of radioactive iodine in both diagnosis4Hamilton J.G. Soley M.H. Studie in iodine metabolism by the use of a new radioactive isotope of iodine.Am J Physiol. 1939; 127: 557-572Crossref Google Scholar and therapy5Hamilton J. Lawrence J. Recent clinical developments in the therapeutic application of radio-phosphorus and radioiodine (abstract).J Clin Invest. 1942; 21: 624Google Scholar, 6Seidlin S.M. Marinelli L.D. Oshry E. Radioactive iodine therapy; effect on functioning metastases of adenocarcinoma of the thyroid.J Am Med Assoc. 1946; 132: 838-847Crossref PubMed Scopus (257) Google Scholar of thyroid conditions dates to the 1930s and 1940s. More recent areas of development include targeting neurodegenerative diseases, malignancies,7Dadachova E. Wang X.G. Casadevall A. Targeting the virus with radioimmunotherapy in virus-associated cancers.Cancer Biother Radiopharm. 2007; 22: 303-308Crossref PubMed Scopus (12) Google Scholar and infectious diseases including human immunodeficiency virus and cryptococcus.8Casadevall A. Goldstein H. Dadachova E. Targeting host cells harbouring viruses with radiolabeled antibodies.Expert Opin Biol Ther. 2007; 7: 595-597Crossref PubMed Scopus (20) Google Scholar, 9Dadachova E. Casadevall A. Radioimmunotherapy of infectious diseases.Semin Nucl Med. 2009; 39: 146-153Crossref PubMed Scopus (36) Google Scholar Tracers developed for PET and SPECT may be coupled with tracers for MRI and optical imaging in animal work, and then translated into human theranostic agents. An area of special interest for probe design and theranostic development is cell therapy.10Nohroudi K. Arnhold S. Berhorn T. Addicks K. Hoehn M. Himmelreich U. In vivo MRI stem cell tracking requires balancing of detection limit and cell viability.Cell Transplant. 2010; 19: 431-441Crossref PubMed Scopus (46) Google Scholar, 11Budde M.D. Frank J.A. Magnetic tagging of therapeutic cells for MRI.J Nucl Med. 2009; 50: 171-174Crossref PubMed Scopus (67) Google Scholar While still undifferentiated, stem cells home to diseased organs and take their molecular cues from surrounding tissues to develop into normal tissues, thus offering the potential to repair damaged organs such as the heart, liver, lung, retina, and kidney, without requiring organ transplantation. This potential of stem cell repair remains largely unfulfilled; however, it is at the center of enormous research attention because of its almost unlimited promise. Before attempting such studies in humans, translational research using experimental animal models is absolutely essential. Stem cell therapy has been investigated as a means of recovering cardiac function resulting from chronic damage caused by Trypanosoma cruzi infection both in animal models of Chagas disease and in patients with chagasic cardiomyopathy.12Soares MB, Santos RR: Current status and perspectives of cell therapy in Chagas disease. Mem Inst Oswaldo Cruz 104 Suppl 2009, 1:325–332Google Scholar, 13Campos de Carvalho A.C. Goldenberg R.C. Jelicks L.A. Soares M.B. Dos Santos R.R. Spray D.C. Tanowitz H.B. Cell therapy in Chagas disease.Interdiscip Perspect Infect Dis. 2009; 2009: 484358Crossref PubMed Google Scholar Stem cell therapy has also been shown to extend incubation and survival time in mice infected with a mouse-adapted prion strain.14Relano-Gines A. Lehmann S. Bencsik A. Herva M.E. Torres J.M. Crozet C.A. Stem cell therapy extends incubation and survival time in prion-infected mice in a time window-dependent manner.J Infect Dis. 2011; 204: 1038-1045Crossref PubMed Scopus (19) Google Scholar Other investigators have demonstrated the engraftment of stem cells into the lung in mice with acute Pseudomonas aeruginosa infection.15Rejman J. Colombo C. Conese M. Engraftment of bone marrow-derived stem cells to the lung in a model of acute respiratory infection by Pseudomonas aeruginosa.Mol Ther. 2009; 17: 1257-1265Abstract Full Text Full Text PDF PubMed Scopus (32) Google Scholar Development of noninvasive methods for tracking the temporal and spatial homing of these cells to the diseased tissues is necessary to understand the mechanisms behind their therapeutic actions.16Ankrum J. Karp J.M. Mesenchymal stem cell therapy: two steps forward, one step back.Trends Mol Med. 2010; 16: 203-209Abstract Full Text Full Text PDF PubMed Scopus (484) Google Scholar A number of studies have reported detection of labeled stem cells in cardiac tissue, mostly after direct transplantation into the heart.17Chung J. Yamada M. Yang P.C. Magnetic resonance imaging of human embryonic stem cells.Curr Protoc Stem Cell Biol. 2009; (Chapter 5:Unit 5A.3.)http://dx.doi.org/10.1002/9780470151808.sc05a03s10Crossref PubMed Scopus (16) Google Scholar, 18Tallheden T. Nannmark U. Lorentzon M. Rakotonirainy O. Soussi B. Waagstein F. Jeppsson A. Sjogren-Jansson E. Lindahl A. Omerovic E. In vivo MR imaging of magnetically labeled human embryonic stem cells.Life Sci. 2006; 79: 999-1006Crossref PubMed Scopus (56) Google Scholar, 19Kustermann E. Roell W. Breitbach M. Wecker S. Wiedermann D. Buehrle C. Welz A. Hescheler J. Fleischmann B.K. Hoehn M. Stem cell implantation in ischemic mouse heart: a high-resolution magnetic resonance imaging investigation.NMR Biomed. 2005; 18: 362-370Crossref PubMed Scopus (60) Google Scholar, 20Graham J.J. Foltz W.D. Vaags A.K. Ward M.R. Yang Y. Connelly K.A. Vijayaraghavan R. Detsky J.S. Hough M.R. Stewart D.J. Wright G.A. Dick A.J. Long-term tracking of bone marrow progenitor cells following intracoronary injection post-myocardial infarction in swine using MRI.Am J Physiol Heart Circ Physiol. 2010; 299: H125-H133Crossref PubMed Scopus (25) Google Scholar, 21Shen D. Liu D. Cao Z. Acton P.D. Zhou R. Coregistration of magnetic resonance and single photon emission computed tomography images for noninvasive localization of stem cells grafted in the infarcted rat myocardium.Mol Imaging Biol. 2007; 9: 24-31Crossref PubMed Scopus (20) Google Scholar, 22Ghanem A. Steingen C. Brenig F. Funcke F. Bai Z.Y. Hall C. Chin C.T. Nickenig G. Bloch W. Tiemann K. Focused ultrasound-induced stimulation of microbubbles augments site-targeted engraftment of mesenchymal stem cells after acute myocardial infarction.J Mol Cell Cardiol. 2009; 47: 411-418Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar, 23Doyle B. Kemp B.J. Chareonthaitawee P. Reed C. Schmeckpeper J. Sorajja P. Russell S. Araoz P. Riederer S.J. Caplice N.M. Dynamic tracking during intracoronary injection of 18F-FDG-labeled progenitor cell therapy for acute myocardial infarction.J Nucl Med. 2007; 48: 1708-1714Crossref PubMed Scopus (109) Google Scholar A recent study reports the successful labeling of adipose-derived stem cells with 18F-FDG.24Elhami E. Goertzen A.L. Xiang B. Deng J. Stillwell C. Mzengeza S. Arora R.C. Freed D. Tian G. Viability and proliferation potential of adipose-derived stem cells following labeling with a positron-emitting radiotracer.Eur J Nucl Med Mol Imaging. 2011; 38: 1323-1334Crossref PubMed Scopus (30) Google Scholar Multimodal molecular imaging agents can take advantage of the different strengths of various imaging technologies such as reported by Hwang et al.25Hwang Do W. Ko H.Y. Kim S.K. Kim D. Lee D.S. Kim S. Development of a quadruple imaging modality by using nanoparticles.Chemistry. 2009; 15: 9387-9393Crossref PubMed Scopus (56) Google Scholar In that study, multimodal nanoparticles were developed for studies using fluorescence, bioluminescence, PET, and MRI imaging in vivo. To date, most applications have been nontargeted, and further development of methods to target cells to specific tissue types is required to provide accurate diagnostic staging of disease and to deliver therapeutics. The targeting of labeled cells or the particles themselves to identify specific tissues can be accomplished by attaching antibodies or peptides or through small molecule surface modification or with targeted reporter genes.26Adonai N. Nguyen K.N. Walsh J. Iyer M. Toyokuni T. Phelps M.E. McCarthy T. McCarthy D.W. Gambhir S.S. Ex vivo cell labeling with 64Cu-pyruvaldehyde-bis(N4-methylthiosemicarbazone) for imaging cell trafficking in mice with positron-emission tomography.Proc Natl Acad Sci USA. 2002; 99: 3030-3035Crossref PubMed Scopus (318) Google Scholar, 27Olasz E.B. Lang L. Seidel J. Green M.V. Eckelman W.C. Katz S.I. Fluorine-18 labeled mouse bone marrow-derived dendritic cells can be detected in vivo by high resolution projection imaging.J Immunol Methods. 2002; 260: 137-148Crossref PubMed Scopus (63) Google Scholar, 28Tamura M. Unno K. Yonezawa S. Hattori K. Nakashima E. Tsukada H. Nakajima M. Oku N. In vivo trafficking of endothelial progenitor cells their possible involvement in the tumor neovascularization.Life Sci. 2004; 75: 575-584Crossref PubMed Scopus (41) Google Scholar Exciting areas of development in molecular imaging probe design include the design of aptamers targeted to biologically relevant molecules and the development of activatable molecular probes. The details of these developments are beyond the scope of this article, but a number of excellent reviews have been published.29Majumdar D. Peng X.H. Shin D.M. The medicinal chemistry of theragnostics, multimodality imaging and applications of nanotechnology in cancer.Curr Top Med Chem. 2010; 10: 1211-1226Crossref PubMed Scopus (39) Google Scholar, 30Yan A.C. Levy M. Aptamers and aptamer targeted delivery.RNA Biol. 2009; 6: 316-320Crossref PubMed Scopus (66) Google Scholar, 31Hong H. Goel S. Zhang Y. Cai W. Molecular imaging with nucleic acid aptamers.Current medicinal chemistry. 2011; 18: 4195-4205Crossref PubMed Scopus (88) Google Scholar Aptamers, short single-strand loops of DNA, RNA, or peptides, are generated by computer profiling of random combinations of nucleotides, ribonucleotides or amino acids, respectively. Numerous combinations and permutations are possible depending on aptamer length. Two noteworthy features of aptamers have attracted considerable attention: i) most of them provoke little or no immunological reaction in humans; and ii) they can be designed to target, with antibody-like specificity, desirable molecular targets. These features make them most attractive for development as theranostic agents for targeted delivery of radiotracers and nanoparticles. Activatable molecular probes are another area of interest for development as theranostic agents.32Elias D.R. Thorek D.L. Chen A.K. Czupryna J. Tsourkas A. In vivo imaging of cancer biomarkers using activatable molecular probes.Cancer Biomark. 2008; 4: 287-305Crossref PubMed Scopus (61) Google Scholar, 33Rai P. Mallidi S. Zheng X. Rahmanzadeh R. Mir Y. Elrington S. Khurshid A. Hasan T. Development and applications of photo-triggered theranostic agents.Adv Drug Deliv Rev. 2010; 62: 1094-1124Crossref PubMed Scopus (431) Google Scholar Light has been used as a remote-activation mechanism for drug delivery using photodynamic-, photothermal-, or photo-triggered chemotherapy for several diseases.33Rai P. Mallidi S. Zheng X. Rahmanzadeh R. Mir Y. Elrington S. Khurshid A. Hasan T. Development and applications of photo-triggered theranostic agents.Adv Drug Deliv Rev. 2010; 62: 1094-1124Crossref PubMed Scopus (431) Google Scholar Activatable molecular probes, in combination with specific targeting, have the potential for application as personalized medical treatment for each individual patient. Most small animal imaging studies have focused on mammalian species, particularly mice and rats. Anesthesia is typically required during image acquisition; although, in recent years, special restraining holders for conscious MRI studies of brain function of rodents have been introduced. Biological investigations of ray-finned teleost fish species, on the other hand, have yielded important insights into vertebrate ontologic development (zebrafish), neurological and retinal physiology (goldfish), and physiological balance mechanisms (toadfish), among others. Invertebrate species, especially horseshoe crabs, have also been invaluable models to promote understanding of blood coagulation and immune regulation mechanisms. Fish would appear to have potential value for imaging applications. However, immobilization of fish for serial physiological studies using modern in vivo imaging techniques has proved to be challenging. For example, fish can be immobilized by anesthetizing and suspending them in agar34Ritter D.A. Bhatt D.H. Fetcho J.R. In vivo imaging of zebrafish reveals differences in the spinal networks for escape and swimming movements.J Neurosci. 2001; 21: 8956-8965Crossref PubMed Google Scholar or through injections of muscle relaxants35Rolen S.H. Sorensen P.W. Mattson D. Caprio J. Polyamines as olfactory stimuli in the goldfish Carassius auratus.J Exp Biol. 2003; 206: 1683-1696Crossref PubMed Scopus (90) Google Scholar; however, such studies of the animal are not appropriate for serial studies over a long time frame. Furthermore, these methods are not realistic for physiological PET imaging applications, which may require a living animal to remain motionless for up to 2 hours. A small imaging tank for fish and other aquatic creatures is feasible36Koba W. Fine E. A novel fish imaging aquarium for small animal research.J Nucl Med. 2012; 51: 191Google Scholar and is demonstrated in Figure 2. An outstanding virtue of this technique is that the fish is restrained safely to prevent motion artifacts but remains conscious in an aerated, research aquarium, permitting experiments under physiological conditions. The concept is similar to a flow-through probe designed for 31P NMR studies of fish37van den Thillart G. Korner F. van Waarde A. Erkelens C. Lugtenburg J. A flow-through probe for in vivo 31P NMR spectroscopy of unanesthetized aquatic vertebrates at 9.4 Tesla.J Magn Reson. 1989; 84: 573-579Google Scholar and an animal-holding device for MRI studies of fish.38Van der Linden A. Verhoye M. Portner H.O. Bock C. The strengths of in vivo magnetic resonance imaging (MRI) to study environmental adaptational physiology in fish.Magma. 2004; 17: 236-248Crossref PubMed Scopus (27) Google Scholar Acclimation of the animal before an experiment may be helpful, whether for imaging or nonimaging applications. In summary, the NIH has set the value of longitudinal imaging study as a priority in preclinical research, both as a means to reduce animal sacrifice and to improve science and statistical power using study animals as their own controls. MicroPET/SPECT and CT modalities are noninvasive and offer unique opportunities to study metabolism and function in small animal models of human disease. We thank Dr. Claudia Gravekamp for providing the PET/CT images of a mouse generated in her laboratory as shown in Figure 1." @default.
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