About this Journal Submit a Manuscript Table of Contents
Journal of Biomedicine and Biotechnology
Volume 2012 (2012), Article ID 519238, 14 pages
http://dx.doi.org/10.1155/2012/519238
Review Article

Ultrasound Biomicroscopy in Small Animal Research: Applications in Molecular and Preclinical Imaging

1Department of Biomorphological and Functional Sciences, University of Naples “Federico II”, 80131 Naples, Italy
2CEINGE-Biotecnologie Avanzate, s.c.ar.l., 80145 Naples, Italy
3Institute of Biostructure and Bioimaging, Italian National Research Council (CNR), 80131 Naples, Italy
4SDN Foundation Instituto di Ricovero e Cura a Carattere Scientifico (M.M.), 80131 Naples, Italy
5Department of Biochemistry and Microbiology, Joan C. Edwards School of Medicine, Marshall University, Huntington, WV 25755, USA
6Department of Surgery, Joan C. Edwards School of Medicine, Marshall University, Huntington, WV 25755, USA

Received 1 August 2011; Accepted 12 August 2011

Academic Editor: Monica Fedele

Copyright © 2012 A. Greco et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. B. Hinton, C. M. Alfieri, S. A. Witt et al., “Mouse heart valve structure and function: echocardiographic and morphometric analyses from the fetus through the aged adult,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 294, no. 6, pp. H2480–H2488, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. M. Mancini, E. Vergara, G. Salvatore et al., “Morphological ultrasound microimaging of thyroid in living mice,” Endocrinology, vol. 150, no. 10, pp. 4810–4815, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. Z. P. Shen, A. A. Brayman, L. Chen, and C. H. Miao, “Ultrasound with microbubbles enhances gene expression of plasmid DNA in the liver via intraportal delivery,” Gene Therapy, vol. 15, no. 16, pp. 1147–1155, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. F. S. Foster, M. Zhang, A. S. Duckett, V. Cucevic, and C. J. Pavlin, “In vivo imaging of embryonic development in the mouse eye by ultrasound biomicroscopy,” Investigative Ophthalmology and Visual Science, vol. 44, no. 6, pp. 2361–2366, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. C. F. Spurney, C. W. Lo, and L. Leatherbury, “Fetal mouse imaging using echocardiography: a review of current technology,” Echocardiography, vol. 23, no. 10, pp. 891–899, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. D. H. Turnbull, T. S. Bloomfield, H. S. Baldwin, F. S. Foster, and A. L. Joyner, “Ultrasound backscatter microscope analysis of early mouse embryonic brain development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 6, pp. 2239–2243, 1995. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Greco, A. Di Benedetto, C. M. Howard et al., “Eradication of therapy-resistant human prostate tumors using an ultrasound-guided site-specific cancer terminator virus delivery approach,” Molecular Therapy, vol. 18, no. 2, pp. 295–306, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. H. C. Manning, N. B. Merchant, A. C. Foutch et al., “Molecular imaging of therapeutic response to epidermal growth factor receptor blockade in colorectal cancer,” Clinical Cancer Research, vol. 14, no. 22, pp. 7413–7422, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. M. L. Springer, R. E. Sievers, M. N. Viswanathan et al., “Closed-chest cell injections into mouse myocardium guided by high-resolution echocardiography,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 289, no. 3, pp. H1307–H1314, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  10. Y. Q. Zhou, L. Davidson, R. M. Henkelman et al., “Ultrasound-guided left-ventricular catheterization: a novel method of whole mouse perfusion for microimaging,” Laboratory Investigation, vol. 84, no. 3, pp. 385–389, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. A. Greco, S. E. Kelly, P. P. Claudio, M. Salvatore, and A. Brunetti, “Ultrasound Contrast Agents for imaging and gene therapy,” in Proceedings of the AISAL Symposium “Imaging and Translational Medicine, p. 25, 2010.
  12. F. S. Foster, M. Y. Zhang, Y. Q. Zhou et al., “A new ultrasound instrument for in vivo microimaging of mice,” Ultrasound in Medicine and Biology, vol. 28, no. 9, pp. 1165–1172, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. J. W. Xuan, M. Bygrave, H. Jiang et al., “Functional neoangiogenesis imaging of genetically engineered mouse prostate cancer using three-dimensional power Doppler ultrasound,” Cancer Research, vol. 67, no. 6, pp. 2830–2839, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. O. Balogun, G. D. Cole, R. Huber, D. Chinn, T. W. Murray, and J. B. Spicer, “High-spatial-resolution sub-surface imaging using a laser-based acoustic microscopy technique,” IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control, vol. 58, no. 1, pp. 226–233, 2011. View at Publisher · View at Google Scholar · View at PubMed
  15. B. E. Treeby, E. Z. Zhang, A. S. Thomas, and B. T. Cox, “Measurement of the ultrasound attenuation and dispersion in whole human blood and its components from 0–70 MHz,” Ultrasound in Medicine and Biology, vol. 37, no. 2, pp. 289–300, 2011. View at Publisher · View at Google Scholar · View at PubMed
  16. M. Tamaki, K. Kidoguchi, T. Mizobe et al., “Carotid artery occlusion and collateral circulation in C57Black/6J mice detected by synchrotron radiation microangiography,” Kobe Journal of Medical Sciences, vol. 52, no. 5, pp. 111–118, 2006. View at Scopus
  17. K. C. Graham, L. A. Wirtzfeld, L. T. MacKenzie et al., “Three-dimensional high-frequency ultrasound imaging for longitudinal evaluation of liver metastases in preclinical models,” Cancer Research, vol. 65, no. 12, pp. 5231–5237, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. L. A. Wirtzfeld, K. C. Graham, A. C. Groom et al., “Volume measurement variability in three-dimensional high-frequency ultrasound images of murine liver metastases,” Physics in Medicine and Biology, vol. 51, no. 10, pp. 2367–2381, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. J. R. Lindner, “Microbubbles in medical imaging: current applications and future directions,” Nature Reviews Drug Discovery, vol. 3, no. 6, pp. 527–532, 2004. View at Scopus
  20. F. S. Villanueva, R. J. Jankowski, S. Klibanov et al., “Microbubbles targeted to intercellular adhesion molecule-1 bind to activated coronary artery endothelial cells,” Circulation, vol. 98, no. 1, pp. 1–5, 1998. View at Scopus
  21. B. Walzog, D. Schuppan, C. Heimpel, A. Hafezi-Moghadam, P. Gaehtgens, and K. Ley, “The leukocyte integrin Mac-1 (CD11b/CD18) contributes to binding of human granulocytes to collagen,” Experimental Cell Research, vol. 218, no. 1, pp. 28–38, 1995. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. M. Mancini, A. Greco, A. Speranza, and M. Salvatore, “Ultrasound molecular imaging by targeted microbubble contrast agents,” Minerva Biotecnologica, vol. 21, no. 2, pp. 97–110, 2009. View at Scopus
  23. H. D. Liang and M. J. K. Blomley, “The role of ultrasound in molecular imaging,” British Journal of Radiology, vol. 76, no. 2, pp. S140–S150, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. S. L. Huang, “Liposomes in ultrasonic drug and gene delivery,” Advanced Drug Delivery Reviews, vol. 60, no. 10, pp. 1167–1176, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. C. K. Holland and D. D. McPherson, “Echogenic lipsomes for targeted drug delivery,” in Proceedings IEEE International Symposium of Biomedical Imaging (ISBI '09), pp. 755–758, July 2009. View at Publisher · View at Google Scholar
  26. G. M. Lanza and S. A. Wickline, “Targeted ultrasonic contrast agents for molecular imaging and therapy,” Progress in Cardiovascular Diseases, vol. 44, no. 1, pp. 13–31, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. O. Couture, P. D. Bevan, E. Cherin, K. Cheung, P. N. Burns, and F. S. Foster, “Investigating perfluorohexane particles with high-frequency ultrasound,” Ultrasound in Medicine and Biology, vol. 32, no. 1, pp. 73–82, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. N. Reznik, R. Williams, and P. N. Burns, “Investigation of vaporized submicron perfluorocarbon droplets as an ultrasound contrast agent,” Ultrasound in Medicine and Biology, vol. 37, no. 8, pp. 1271–1279, 2011. View at Publisher · View at Google Scholar · View at PubMed
  29. R. Bekeredjian, S. Behrens, J. Ruef et al., “Potential of gold-bound microtubules as a new ultrasound contrast agent,” Ultrasound in Medicine and Biology, vol. 28, no. 5, pp. 691–695, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. H. A. Bardelmeijer, T. Buckle, M. Ouwehand, J. H. Beijnen, J. H. M. Schellens, and O. van Tellingen, “Cannulation of the jugular vein in mice: a method for serial withdrawal of blood samples,” Laboratory Animals, vol. 37, no. 3, pp. 181–187, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. P. Haag, F. Frauscher, J. Gradl et al., “Microbubble-enhanced ultrasound to deliver an antisense oligodeoxynucleotide targeting the human androgen receptor into prostate tumours,” Journal of Steroid Biochemistry and Molecular Biology, vol. 102, no. 1–5, pp. 103–113, 2006. View at Publisher · View at Google Scholar · View at PubMed
  32. Y. Miyake, K. Ohmori, J. Yoshida et al., “Granulocyte colony-stimulating factor facilitates the angiogenesis induced by ultrasonic microbubble destruction,” Ultrasound in Medicine and Biology, vol. 33, no. 11, pp. 1796–1804, 2007. View at Publisher · View at Google Scholar · View at PubMed
  33. J. C. Slevin, L. Byers, M. Gertsenstein et al., “High resolution ultrasound-guided microinjection for interventional studies of early embryonic and placental development in vivo in mice,” BMC Developmental Biology, vol. 27, no. 6, p. 10, 2006. View at Publisher · View at Google Scholar · View at PubMed
  34. D. Guo, X. Li, P. Sun et al., “Ultrasound/microbubble enhances foreign gene expression in ECV304 cells and murine myocardium,” Acta Biochimica et Biophysica Sinica, vol. 36, no. 12, pp. 824–831, 2004.
  35. J. K. Willmann, A. M. Lutz, R. Paulmurugan et al., “Dual-targeted contrast agent for US assessment of tumor angiogenesis in vivo,” Radiology, vol. 248, no. 3, pp. 936–944, 2008. View at Publisher · View at Google Scholar · View at PubMed
  36. A. Lyshchik, A. C. Fleischer, J. Huamani, D. E. Hallahan, M. Brissova, and J. C. Gore, “Molecular imaging of vascular endothelial growth factor receptor 2 expression using targeted contrast-enhanced high-frequency ultrasonography,” Journal of Ultrasound in Medicine, vol. 26, no. 11, pp. 1575–1586, 2007.
  37. C. M. Howard, F. Forsberg, C. Minimo, J. B. Liu, D. A. Merton, and P. P. Claudio, “Ultrasound guided site specific gene delivery system using adenoviral vectors and commercial ultrasound contrast agents,” Journal of Cellular Physiology, vol. 209, no. 2, pp. 413–421, 2006. View at Publisher · View at Google Scholar · View at PubMed
  38. M. R. Böhmer, A. L. Klibanov, K. Tiemann, C. S. Hall, H. Gruell, and O. C. Steinbach, “Ultrasound triggered image-guided drug delivery,” European Journal of Radiology, vol. 70, no. 2, pp. 242–253, 2009. View at Publisher · View at Google Scholar · View at PubMed
  39. R. Pla, V. Borrell, N. Flames, and O. Marín, “Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling,” Journal of Neuroscience, vol. 28, no. 26, pp. 6924–6934, 2006. View at Publisher · View at Google Scholar · View at PubMed
  40. C. Punzo and C. L. Cepko, “Ultrasound-guided in utero injections allow studies of the development and function of the eye,” Developmental Dynamics, vol. 237, no. 4, pp. 1034–1042, 2008. View at Publisher · View at Google Scholar · View at PubMed
  41. J. C. Pezold, K. Zinn, M. A. Talbert, R. Desmond, and E. L. Rosenthal, “Validation of ultrasonography to evaluate murine orthotopic oral cavity tumors,” ORL, vol. 68, no. 3, pp. 159–163, 2006. View at Publisher · View at Google Scholar · View at PubMed
  42. C. P. Chang, L. Chen, and G. R. Crabtree, “Sonographic staging of the developmental status of mouse embryos in utero,” Genesis, vol. 36, no. 1, pp. 7–11, 2003. View at Publisher · View at Google Scholar · View at PubMed
  43. M. Zollo, N. Marino, A. Greco, et al., “In vivo imaging methodologies applied to the murine xenografts of human breast cancer: a pre-clinical h-prune animal model,” in Proceedings of the European Symposium of Molecular Imaging, p. 38, Naples, Italy, May 2007.
  44. B. Banihashemi, R. Vlad, B. Debeljevic, A. Giles, M. C. Kolios, and G. J. Czarnota, “Ultrasound imaging of apoptosis in tumor response: novel preclinical monitoring of photodynamic therapy effects,” Cancer Research, vol. 68, no. 20, pp. 8590–8596, 2008. View at Publisher · View at Google Scholar · View at PubMed
  45. J. Folkman, “What is the evidence that tumors are angiogenesis dependent?” Journal of the National Cancer Institute, vol. 82, no. 1, pp. 4–6, 1990.
  46. C. Dazzi, A. Cariello, P. Maioli et al., “Prognostic and predictive value of intratumoral microvessels density in operable non-small-cell lung cancer,” Lung Cancer, vol. 24, no. 2, pp. 81–88, 1999. View at Publisher · View at Google Scholar
  47. M. Scherrer-Crosbie and H. B. Thibault, “Echocardiography in translational research: of mice and men,” Journal of the American Society of Echocardiography, vol. 21, no. 10, pp. 1083–1092, 2008. View at Publisher · View at Google Scholar · View at PubMed
  48. J. Stypmann, M. A. Engelen, C. Troatz, M. Rothenburger, L. Eckardt, and K. Tiemann, “Echocardiographic assessment of global left ventricular function in mice,” Laboratory Animals, vol. 43, no. 2, pp. 127–137, 2009. View at Publisher · View at Google Scholar · View at PubMed
  49. R. C. Fentzke, C. E. Korcarz, S. G. Shroff et al., “Evaluation of ventricular and arterial hemodynamics in anesthetized closed-chest mice,” Journal of the American Society of Echocardiography, vol. 10, no. 9, pp. 915–925, 1997.
  50. P. Krishnamurthy, J. Rajasingh, E. Lambers, G. Qin, D. W. Losordo, and R. Kishore, “IL-10 inhibits inflammation and attenuates left ventricular remodeling after myocardial infarction via activation of STAT3 and suppression of HuR,” Circulation Research, vol. 104, no. 2, pp. e9–e18, 2009. View at Publisher · View at Google Scholar · View at PubMed
  51. J. Takagawa, Y. Zhang, M. L. Wong et al., “Myocardial infarct size measurement in the mouse chronic infarction model: comparison of area- and length-based approaches,” Journal of Applied Physiology, vol. 102, no. 6, pp. 2104–2111, 2007. View at Publisher · View at Google Scholar · View at PubMed
  52. T. P. Abraham, M. Jones, K. Kazmierczak et al., “Diastolic dysfunction in familial hypertrophic cardiomyopathy transgenic model mice,” Cardiovascular Research, vol. 82, no. 1, pp. 84–92, 2009. View at Publisher · View at Google Scholar · View at PubMed
  53. L. Gavish, C. Rubinstein, A. Bulut et al., “Low-level laser irradiation inhibits abdominal aortic aneurysm progression in apolipoprotein E-deficient mice,” Cardiovascular Research, vol. 83, no. 4, pp. 785–792, 2009. View at Publisher · View at Google Scholar · View at PubMed
  54. M. Ni, M. Zhang, S. F. Ding, W. Q. Chen, and Y. Zhang, “Micro-ultrasound imaging assessment of carotid plaque characteristics in apolipoprotein-E knockout mice,” Atherosclerosis, vol. 197, no. 1, pp. 64–71, 2008. View at Publisher · View at Google Scholar · View at PubMed
  55. M. Walker, B. R. Campbell, K. Azer et al., “A novel 3-dimensional micro-ultrasound approach to automated measurement of carotid arterial plaque volume as a biomarker for experimental atherosclerosis,” Atherosclerosis, vol. 204, no. 1, pp. 55–65, 2009. View at Publisher · View at Google Scholar · View at PubMed
  56. G. Bragagni, F. Lari, G. Magenta, R. Brogna, and G. Zoli, “Echocardiographic evaluation of anti-tumor necrosis factor-α therapy with infliximab in patients without cardiac pathologies,” Recenti Progressi in Medicina, vol. 101, no. 7-8, pp. 289–292, 2010. View at Publisher · View at Google Scholar
  57. J. Grönros, J. Wikström, U. Brandt-Eliasson et al., “Effects of rosuvastatin on cardiovascular morphology and function in an ApoE-knockout mouse model of atherosclerosis,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 295, no. 5, pp. H2046–H2053, 2008. View at Publisher · View at Google Scholar · View at PubMed
  58. B. A. Kaufmann, M. Lankford, C. Z. Behm et al., “High-resolution myocardial perfusion imaging in mice with high-frequency echocardiographic detection of a depot contrast agent,” Journal of the American Society of Echocardiography, vol. 20, no. 2, pp. 136–143, 2007. View at Publisher · View at Google Scholar · View at PubMed
  59. S. Srinivasan, H. S. Baldwin, O. Aristizabal et al., “Noninvasive, in utero imaging of mouse embryonic heart development with 40-MHz echocardiography,” Circulation, vol. 98, no. 9, pp. 912–918, 1998.
  60. C. K. L. Phoon, R. P. Ji, O. Aristizábal et al., “Embryonic heart failure in NFATc1-/- mice novel: mechanistic insights from in utero ultrasound biomicroscopy,” Circulation Research, vol. 95, no. 1, pp. 92–99, 2004. View at Publisher · View at Google Scholar · View at PubMed
  61. N. Corrigan, D. P. Brazil, and F. M. Auliffe, “High-frequency ultrasound assessment of the murine heart from embryo through to juvenile,” Reproductive Sciences, vol. 17, no. 2, pp. 147–157, 2010. View at Publisher · View at Google Scholar · View at PubMed
  62. D. H. Turnbull, J. A. Ramsay, G. S. Shivji et al., “Ultrasound backscatter microscope analysis of mouse melanoma progression,” Ultrasound in Medicine and Biology, vol. 22, no. 7, pp. 845–853, 1996. View at Publisher · View at Google Scholar
  63. M. Russo, L. Meomartino, A. Greco et al., “Pregnancy detection in mice using ultrasound,” Veterinary Record, vol. 160, no. 13, pp. 446–447, 2007.
  64. J. Mu, J. C. Slevin, D. Qu, S. McCormick, and S. L. Adamson, “In vivo quantification of embryonic and placental growth during gestation in mice using micro-ultrasound,” Reproductive Biology and Endocrinology, vol. 12, no. 6, p. 34, 2008. View at Publisher · View at Google Scholar · View at PubMed
  65. D. H. Turnbull, “In utero ultrasound backscatter microscopy of early stage mouse embryos,” Computerized Medical Imaging and Graphics, vol. 23, no. 1, pp. 25–31, 1999. View at Publisher · View at Google Scholar
  66. E. Bentley, P. E. Miller, and K. A. Diehl, “Use of high-resolution ultrasound as a diagnostic tool in veterinary ophthalmology,” Journal of the American Veterinary Medical Association, vol. 223, no. 11, pp. 1617–1622, 2003. View at Publisher · View at Google Scholar
  67. A. M. Flenniken, L. R. Osborne, N. Anderson et al., “A Gja1 missense mutation in a mouse model of oculodentodigital dysplasia,” Development, vol. 132, no. 19, pp. 4375–4386, 2005. View at Publisher · View at Google Scholar · View at PubMed
  68. N. Nissirios, J. Ramos-Esteban, and J. Danias, “Ultrasound biomicroscopy of the rat eye: effects of cholinergic and anticholinergic agents,” Graefe's Archive for Clinical and Experimental Ophthalmology, vol. 243, no. 5, pp. 469–473, 2005. View at Publisher · View at Google Scholar · View at PubMed
  69. S. W. M. John, R. S. Smith, O. V. Savinova et al., “Essential iris atrophy, pigment dispersion, and glaucoma in DBA/2J mice,” Investigative Ophthalmology and Visual Science, vol. 39, no. 6, pp. 951–962, 1998.