State of the art in vivo imaging techniques for laboratory animals

In recent decades, imaging devices have become indispensable tools in the basic sciences, in preclinical research and in modern drug development. The rapidly evolving high-resolution in vivo imaging technologies provide a unique opportunity for studying biological processes of living organisms in real time on a molecular level. State of the art small-animal imaging modalities provide non-invasive images rich in quantitative anatomical and functional information, which renders longitudinal studies possible allowing precise monitoring of disease progression and response to therapy in models of different diseases. The number of animals in a scientific investigation can be substantially reduced using imaging techniques, which is in full compliance with the ethical endeavours for the 3R (reduction, refinement, replacement) policies formulated by Russell and Burch; furthermore, biological variability can be alleviated, as each animal serves as its own control. The most suitable and commonly used imaging modalities for in vivo small-animal imaging are optical imaging (OI), ultrasonography (US), computed tomography (CT), magnetic resonance imaging (MRI), and finally the methods of nuclear medicine: positron emission tomography (PET) and single photon emission computed tomography (SPECT).

[1]  M. Pourfathi,et al.  The use of hyperpolarized carbon‐13 magnetic resonance for molecular imaging☆ , 2017, Advanced drug delivery reviews.

[2]  M. Carminati,et al.  Development of clinical simultaneous SPECT/MRI , 2017, The British journal of radiology.

[3]  J. Varagić,et al.  Photoacoustic Imaging for the Detection of Hypoxia in the Rat Femoral Artery and Skeletal Muscle Microcirculation , 2016, Shock.

[4]  Song Hu Emerging concepts in functional and molecular photoacoustic imaging. , 2016, Current opinion in chemical biology.

[5]  Yajing Liu,et al.  Photoacoustic Molecular Imaging: From Multiscale Biomedical Applications Towards Early-Stage Theranostics. , 2016, Trends in biotechnology.

[6]  Hans Herzog,et al.  Advances in Clinical PET/MRI Instrumentation. , 2016, PET clinics.

[7]  J. Franconi,et al.  Free-breathing 3D diffusion MRI for high-resolution hepatic metastasis characterization in small animals , 2015, Clinical & Experimental Metastasis.

[8]  Jennifer L. West,et al.  In vivo small animal micro-CT using nanoparticle contrast agents , 2015, Front. Pharmacol..

[9]  Markus Piel,et al.  Positron emission tomography in CNS drug discovery and drug monitoring. , 2014, Journal of medicinal chemistry.

[10]  K. Karlinger,et al.  Demonstration of Metabolic and Cellular Effects of Portal Vein Ligation Using Multi-Modal PET/MRI Measurements in Healthy Rat Liver , 2014, PloS one.

[11]  Domingos Vieira,et al.  Preclinical Imaging: an Essential Ally in Modern Biosciences , 2013, Molecular Diagnosis & Therapy.

[12]  Jean-Noël Hyacinthe,et al.  Hyperpolarization without persistent radicals for in vivo real-time metabolic imaging , 2013, Proceedings of the National Academy of Sciences.

[13]  M. Lisanti,et al.  Imaging of small-animal models of infectious diseases. , 2013, The American journal of pathology.

[14]  Arion F. Chatziioannou,et al.  Instrumentation for Molecular Imaging in Preclinical Research , 2012 .

[15]  C. Alberti,et al.  From molecular imaging in preclinical/clinical oncology to theranostic applications in targeted tumor therapy. , 2012, European review for medical and pharmacological sciences.

[16]  Hans C. Gerritsen,et al.  Fluorescence Spectroscopy, Imaging and Probes: New Tools in Chemical, Physical and Life Sciences , 2012 .

[17]  T. Richards Multinuclear Magnetic Resonance Spectroscopic Imaging , 2012 .

[18]  Vasilis Ntziachristos,et al.  Opto-acoustic imaging of drug discovery biomarkers. , 2012, Current pharmaceutical biotechnology.

[19]  Sepideh Shokouhi,et al.  Advances in Preclinical SPECT Instrumentation , 2012, The Journal of Nuclear Medicine.

[20]  Sven Diederichs,et al.  The hallmarks of cancer , 2012, RNA biology.

[21]  Sanjiv S Gambhir,et al.  A molecular imaging primer: modalities, imaging agents, and applications. , 2012, Physiological reviews.

[22]  Lihong V. Wang,et al.  Photoacoustic Tomography: In Vivo Imaging from Organelles to Organs , 2012, Science.

[23]  A. Brunetti,et al.  Ultrasound Biomicroscopy in Small Animal Research: Applications in Molecular and Preclinical Imaging , 2011, Journal of biomedicine & biotechnology.

[24]  L. Furenlid,et al.  SPECT detectors: the Anger Camera and beyond , 2011, Physics in medicine and biology.

[25]  P. Beard Biomedical photoacoustic imaging , 2011, Interface Focus.

[26]  M. Wylezinska-Arridge,et al.  Imaging technologies for preclinical models of bone and joint disorders , 2011, EJNMMI research.

[27]  Erik L Ritman,et al.  Current status of developments and applications of micro-CT. , 2011, Annual review of biomedical engineering.

[28]  Kami Kim,et al.  Imaging devices for use in small animals. , 2011, Seminars in nuclear medicine.

[29]  G. Antoni,et al.  18F-ML-10, a PET Tracer for Apoptosis: First Human Study , 2011, The Journal of Nuclear Medicine.

[30]  M. Khalil,et al.  Molecular SPECT Imaging: An Overview , 2011, International journal of molecular imaging.

[31]  J. Pratte,et al.  Simultaneous assessment of rodent behavior and neurochemistry using a miniature positron emission tomograph , 2011, Nature Methods.

[32]  G. Nikiforidis,et al.  In vivo small animal imaging: current status and future prospects. , 2010, Medical physics.

[33]  J. Willmann,et al.  Molecular ultrasound imaging: current status and future directions. , 2010, Clinical radiology.

[34]  C. W. G. M. Löwik,et al.  ‘In vivo’ optical approaches to angiogenesis imaging , 2010, Angiogenesis.

[35]  Ciprian Catana,et al.  Small-Animal Molecular Imaging Methods , 2010, Journal of Nuclear Medicine.

[36]  S. Emelianov,et al.  Detection of lipid in atherosclerotic vessels using ultrasound-guided spectroscopic intravascular photoacoustic imaging , 2010, Optics express.

[37]  M. Rodriguez-Porcel In Vivo Imaging and Monitoring of Transplanted Stem Cells: Clinical Applications , 2010, Current cardiology reports.

[38]  Quing Zhu,et al.  A real-time photoacoustic tomography system for small animals. , 2009, Optics express.

[39]  J. Voigt Ultrasound molecular imaging. , 2009, Methods.

[40]  Markus Rudin,et al.  Noninvasive structural, functional, and molecular imaging in drug development. , 2009, Current opinion in chemical biology.

[41]  D. Kraitchman,et al.  Recent Advances in Small-Animal Cardiovascular Imaging , 2009, Journal of Nuclear Medicine.

[42]  M. Pomper,et al.  Serial imaging of human embryonic stem-cell engraftment and teratoma formation in live mouse models , 2009, Cell Research.

[43]  G. Johnson,et al.  In vivo small-animal imaging using micro-CT and digital subtraction angiography , 2008, Physics in medicine and biology.

[44]  P. Acton,et al.  Small-Animal SPECT and SPECT/CT: Important Tools for Preclinical Investigation* , 2008, Journal of Nuclear Medicine.

[45]  A. Rotondo,et al.  Genomics, proteomics, MEMS and SAIF: which role for diagnostic imaging? , 2008, La radiologia medica.

[46]  Markus Schwaiger,et al.  Imaging of integrin αvβ3 expression , 2008, Cancer and Metastasis Reviews.

[47]  B. Pichler,et al.  Positron emission tomography/magnetic resonance imaging: the next generation of multimodality imaging? , 2008, Seminars in nuclear medicine.

[48]  Lihong V. Wang,et al.  Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries. , 2008, Optics letters.

[49]  B. Biswal,et al.  Detection and scaling of task-induced fMRI-BOLD response using resting state fluctuations , 2008, NeuroImage.

[50]  H. Daldrup-Link,et al.  Labeling stem cells with fluorescent dyes for non-invasive detection with optical imaging. , 2008, Journal of visualized experiments : JoVE.

[51]  S. Achilefu,et al.  Multimodality Molecular Imaging with Combined Optical and SPECT/PET Modalities , 2008, Journal of Nuclear Medicine.

[52]  Sushil K. Sharma,et al.  SPECT neuroimaging in translational research of CNS disorders , 2008, Neurochemistry International.

[53]  A. Constantinesco,et al.  SPECT Low-Field MRI System for Small-Animal Imaging , 2007, Journal of Nuclear Medicine.

[54]  Jason S. Lewis,et al.  Cu-ATSM: a radiopharmaceutical for the PET imaging of hypoxia. , 2007, Dalton transactions.

[55]  Antoine Geissbuhler,et al.  Improved Visualization of Vessels and Hepatic Tumors by Micro-Computed Tomography (CT) Using Iodinated Liposomes , 2007, Investigative radiology.

[56]  Hans-Ulrich Gremlich,et al.  In Vivo mouse imaging and spectroscopy in drug discovery , 2007, NMR in biomedicine.

[57]  David B. Stout,et al.  MicroCT Liver Contrast Agent Enhancement Over Time, Dose, and Mouse Strain , 2007, Molecular Imaging and Biology.

[58]  Habib Zaidi,et al.  Current Trends in Preclinical PET System Design. , 2007, PET clinics.

[59]  F. Beekman,et al.  Submillimeter total-body murine imaging with U-SPECT-I. , 2007, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[60]  G. Parker,et al.  DCE-MRI biomarkers in the clinical evaluation of antiangiogenic and vascular disrupting agents , 2007, British Journal of Cancer.

[61]  Lihong V. Wang,et al.  Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging , 2006, Nature Biotechnology.

[62]  B. Esmaeli,et al.  Ultrasound biomicroscopy for estimation of tumor thickness for conjunctival melanoma , 2006, Journal of clinical ultrasound : JCU.

[63]  R. Weissleder,et al.  An Albumin‐Activated Far‐Red Fluorochrome for In Vivo Imaging , 2006, ChemMedChem.

[64]  Wolfgang A Weber,et al.  Molecular imaging in the development of cancer therapeutics. , 2006, Annual review of medicine.

[65]  S. Meikle,et al.  Small animal SPECT and its place in the matrix of molecular imaging technologies , 2005, Physics in medicine and biology.

[66]  Martin G Pomper,et al.  Small animal imaging in drug development. , 2005, Current pharmaceutical design.

[67]  P. Sundgren,et al.  Magnetic resonance spectroscopy. , 2005, Journal of neuro-ophthalmology : the official journal of the North American Neuro-Ophthalmology Society.

[68]  Aaron Fenster,et al.  Three-dimensional ultrasound biomicroscopy for xenograft growth analysis. , 2005, Ultrasound in medicine & biology.

[69]  S. Siegel,et al.  Performance evaluation of the microPET focus: a third-generation microPET scanner dedicated to animal imaging. , 2005, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[70]  B. Cornelissen,et al.  A review of small animal imaging planar and pinhole spect Gamma camera imaging. , 2005, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[71]  Wolfhard Semmler,et al.  Volumetric computed tomography (VCT): a new technology for noninvasive, high-resolution monitoring of tumor angiogenesis , 2004, Nature Medicine.

[72]  Roger Lecomte,et al.  Technology challenges in small animal PET imaging , 2004 .

[73]  Gary D Hutchins,et al.  Small animal PET imaging. , 2004, ILAR journal.

[74]  J. Boone,et al.  Small-animal X-ray dose from micro-CT. , 2004, Molecular imaging.

[75]  D. Dione,et al.  Noninvasive imaging of myocardial angiogenesis following experimental myocardial infarction. , 2004, The Journal of clinical investigation.

[76]  Hyunsuk Shim,et al.  Magnetic Resonance Spectroscopic Imaging of Tumor Metabolic Markers for Cancer Diagnosis, Metabolic Phenotyping, and Characterization of Tumor Microenvironment , 2004, Disease markers.

[77]  H. Kung,et al.  Characterization of IMPY as a potential imaging agent for β-amyloid plaques in double transgenic PSAPP mice , 2004, European Journal of Nuclear Medicine and Molecular Imaging.

[78]  A. Kassner,et al.  Molecular Imaging of Angiogenesis in Nascent Vx-2 Rabbit Tumors Using a Novel ανβ3-targeted Nanoparticle and 1.5 Tesla Magnetic Resonance Imaging , 2003 .

[79]  S. Gambhir,et al.  Optical bioluminescence and positron emission tomography imaging of a novel fusion reporter gene in tumor xenografts of living mice. , 2003, Cancer research.

[80]  S. Gambhir,et al.  Molecular imaging in living subjects: seeing fundamental biological processes in a new light. , 2003, Genes & development.

[81]  R. Weissleder,et al.  Optical-based molecular imaging: contrast agents and potential medical applications , 2003, European Radiology.

[82]  R. Blasberg PET imaging of gene expression. , 2002, European journal of cancer.

[83]  Donald W. Wilson,et al.  Quantitative analysis of acute myocardial infarct in rat hearts with ischemia-reperfusion using a high-resolution stationary SPECT system. , 2002, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[84]  M E Easterly,et al.  A review of high-resolution X-ray computed tomography and other imaging modalities for small animal research. , 2001, Lab animal.

[85]  T G Turkington,et al.  Introduction to PET instrumentation. , 2001, Journal of nuclear medicine technology.

[86]  Yann Hode,et al.  Brain Pharmacokinetics and Tissue Distribution In Vivo of Fluvoxamine and Fluoxetine by Fluorine Magnetic Resonance Spectroscopy , 2000, Neuropsychopharmacology.

[87]  H. Genant,et al.  Micro CT and Micro MR imaging of 3D architecture of animal skeleton. , 2000, Journal of musculoskeletal & neuronal interactions.

[88]  Yu-Chung N. Cheng,et al.  Magnetic Resonance Imaging: Physical Principles and Sequence Design , 1999 .

[89]  Roger N. Gunn,et al.  Pharmacological constraints associated with positron emission tomographic scanning of small laboratory animals , 1998, European Journal of Nuclear Medicine.

[90]  J. Vogel Measurement of cardiac output in small laboratory animals using recordings of blood conductivity. , 1997, American journal of physiology. Heart and circulatory physiology.

[91]  H. Wagner Nuclear medicine: 100 years in the making. , 1996, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[92]  Susan Wray Imaging , 1994, Between Auschwitz and Tradition.

[93]  Ferenc A. Jolesz,et al.  MR‐Guided Focused Ultrasound Surgery , 1992, Journal of computer assisted tomography.

[94]  David J. Schlyer,et al.  Graphical Analysis of Reversible Radioligand Binding from Time—Activity Measurements Applied to [N-11C-Methyl]-(−)-Cocaine PET Studies in Human Subjects , 1990, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[95]  R J Jaszczak,et al.  Single photon emission computed tomography (SPECT). Principles and instrumentation. , 1985, Investigative radiology.

[96]  C S Patlak,et al.  Graphical Evaluation of Blood-to-Brain Transfer Constants from Multiple-Time Uptake Data , 1983, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[97]  Albert Gjedde,et al.  Calculation of cerebral glucose phosphorylation from brain uptake of glucose analogs in vivo: A re-examination , 1982, Brain Research Reviews.

[98]  Pat Zanzonico,et al.  Noninvasive Imaging for Supporting Basic Research , 2011 .

[99]  Ananth Annapragada,et al.  Evaluation of tumor microenvironment in an animal model using a nanoparticle contrast agent in computed tomography imaging. , 2011, Academic radiology.

[100]  A. Drzezga,et al.  Imaging in Neurology Research II: PET Imaging of CNS Disorders , 2011 .

[101]  A. Rehemtulla,et al.  Molecular Imaging , 2009, Methods in Molecular Biology.

[102]  D. Boas,et al.  Laser speckle contrast imaging in biomedical optics. , 2010, Journal of biomedical optics.

[103]  Christoph Groden,et al.  Application of micro-CT in small animal imaging. , 2010, Methods.

[104]  Xiaoyuan Chen,et al.  PET Imaging of Angiogenesis. , 2009, PET clinics.

[105]  Xu Xiao Photoacoustic imaging in biomedicine , 2008 .

[106]  Wolfhard Semmler,et al.  Fundamentals of optical imaging. , 2008, Handbook of experimental pharmacology.

[107]  T. Blackwell,et al.  Bioluminescence imaging. , 2005, Proceedings of the American Thoracic Society.

[108]  N. Volkow,et al.  RatCAP: miniaturized head-mounted PET for conscious rodent brain imaging , 2004, IEEE Transactions on Nuclear Science.

[109]  Dianna D Cody,et al.  In vivo respiratory-gated micro-CT imaging in small-animal oncology models. , 2004, Molecular imaging.

[110]  M. Blomley,et al.  The role of ultrasound in molecular imaging. , 2003, The British journal of radiology.

[111]  P. Herscovitch Single-Photon Emission Computed Tomography (SPECT) , 2003 .

[112]  A. Szalay,et al.  Imaging of light emission from the expression of luciferases in living cells and organisms: a review. , 2002, Luminescence : the journal of biological and chemical luminescence.

[113]  R. Weissleder,et al.  Fluorescence imaging with near-infrared light: new technological advances that enable in vivo molecular imaging , 2002, European Radiology.

[114]  C. Zippe,et al.  Evaluation of preoperative ProstaScint™ scans in the prediction of nodal disease , 2002, Prostate Cancer and Prostatic Diseases.

[115]  E. Croteau,et al.  Cardiac PET imaging of blood flow, metabolism and function in normal and infarcted rats , 2002, 2002 IEEE Nuclear Science Symposium Conference Record.

[116]  R. Weissleder Scaling down imaging: molecular mapping of cancer in mice , 2002, Nature Reviews Cancer.

[117]  R. Coatney,et al.  Ultrasound imaging: principles and applications in rodent research. , 2001, ILAR journal.

[118]  M J Paulus,et al.  High resolution X-ray computed tomography: an emerging tool for small animal cancer research. , 2000, Neoplasia.

[119]  F A Jolesz,et al.  A clinical, noninvasive, MR imaging-monitored ultrasound surgery method. , 1996, Radiographics : a review publication of the Radiological Society of North America, Inc.

[120]  R A Kruger,et al.  Photoacoustic ultrasound. , 1994, Medical physics.

[121]  W. Rogers,et al.  SPECT instrumentation. , 1992, American journal of physiologic imaging.

[122]  H. Anger,et al.  Recent applications of the scintillation camera. , 1967, Strahlentherapie. Sonderbande.