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Stem Cells International
Volume 2016 (2016), Article ID 4058656, 8 pages
http://dx.doi.org/10.1155/2016/4058656
Review Article

Molecular Imaging of Stem Cell Transplantation for Liver Diseases: Monitoring, Clinical Translation, and Theranostics

1Molecular Imaging Laboratory, MGH/MIT/HMS Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02129, USA
2Department of Thoracic Surgery, European Institute of Oncology, Via Ripamonti 435, 20141 Milan, Italy
3Postgraduation School in Radiodiagnostics, Università degli Studi di Milano, Via Festa del Perdono 7, 20122 Milan, Italy
4Department of Radiology, European Institute of Oncology, Via Ripamonti 435, 20141 Milan, Italy
5Department of Oncology, University of Milan, Via Festa del Perdono 7, 20142 Milan, Italy

Received 26 September 2016; Accepted 1 November 2016

Academic Editor: Gary E. Lyons

Copyright © 2016 Ping Wang 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. D. Schuppan and N. H. Afdhal, “Liver cirrhosis,” The Lancet, vol. 371, no. 9615, pp. 838–851, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Berardis, P. D. Sattwika, M. Najimi, and E. M. Sokal, “Use of mesenchymal stem cells to treat liver fibrosis: current situation and future prospects,” World Journal of Gastroenterology, vol. 21, no. 3, pp. 742–758, 2015. View at Publisher · View at Google Scholar · View at Scopus
  3. T. K. Kuo, S.-P. Hung, C.-H. Chuang et al., “Stem cell therapy for liver disease: parameters governing the success of using bone marrow mesenchymal stem cells,” Gastroenterology, vol. 134, no. 7, pp. 2111–2121.e3, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. Z. Zhang and F. S. Wang, “Stem cell therapies for liver failure and cirrhosis,” Journal of Hepatology, vol. 59, no. 1, pp. 183–185, 2013. View at Publisher · View at Google Scholar
  5. M. R. Lucey, N. Terrault, L. Ojo et al., “Long-term management of the successful adult liver transplant: 2012 practice guideline by the American Association for the Study of Liver Diseases and the American Society of Transplantation,” Liver Transplantation, vol. 19, no. 1, pp. 3–26, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. P. P. Wang, J. H. Wang, Z. P. Yan et al., “Expression of hepatocyte-like phenotypes in bone marrow stromal cells after HGF induction,” Biochemical and Biophysical Research Communications, vol. 320, no. 3, pp. 712–716, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. J. M. Luk, P. P. Wang, C. K. Lee, J. H. Wang, and S. T. Fan, “Hepatic potential of bone marrow stromal cells: development of in vitro co-culture and intra-portal transplantation models,” Journal of Immunological Methods, vol. 305, no. 1, pp. 39–47, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. V. Volarevic, J. Nurkovic, N. Arsenijevic, and M. Stojkovic, “Concise review: therapeutic potential of mesenchymal stem cells for the treatment of acute liver failure and cirrhosis,” Stem Cells, vol. 32, no. 11, pp. 2818–2823, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. M.-E. M. Amer, S. Z. El-Sayed, W. A. El-Kheir et al., “Clinical and laboratory evaluation of patients with end-stage liver cell failure injected with bone marrow-derived hepatocyte-like cells,” European Journal of Gastroenterology and Hepatology, vol. 23, no. 10, pp. 936–941, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. H. Salama, A.-R. N. Zekri, A. A. Bahnassy et al., “Autologous CD34+ and CD133+ stem cells transplantation in patients with end stage liver disease,” World Journal of Gastroenterology, vol. 16, no. 42, pp. 5297–5305, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Nikeghbalian, B. Pournasr, N. Aghdami et al., “Autologous transplantation of bone marrow-derived mononuclear and CD133+ cells in patients with decompensated cirrhosis,” Archives of Iranian Medicine, vol. 14, no. 1, pp. 12–17, 2011. View at Google Scholar · View at Scopus
  12. M. El-Ansary, I. Abdel-Aziz, S. Mogawer et al., “Phase II trial: undifferentiated versus differentiated autologous mesenchymal stem cells transplantation in Egyptian patients with HCV induced liver cirrhosis,” Stem Cell Reviews and Reports, vol. 8, no. 3, pp. 972–981, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. A.-R. N. Zekri, H. Salama, E. Medhat et al., “The impact of repeated autologous infusion of haematopoietic stem cells in patients with liver insufficiency,” Stem Cell Research and Therapy, vol. 6, no. 1, article 118, 2015. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Mohamadnejad, K. Alimoghaddam, M. Bagheri et al., “Randomized placebo-controlled trial of mesenchymal stem cell transplantation in decompensated cirrhosis,” Liver International, vol. 33, no. 10, pp. 1490–1496, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. R. P. H. Meier, Y. D. Müller, P. Morel, C. Gonelle-Gispert, and L. H. Bühler, “Transplantation of mesenchymal stem cells for the treatment of liver diseases, is there enough evidence?” Stem Cell Research, vol. 11, no. 3, pp. 1348–1364, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Mohamadnejad, K. Alimoghaddam, M. Mohyeddin-Bonab et al., “Phase 1 trial of autologous bone marrow mesenchymal stem cell transplantation in patients with decompensated liver cirrhosis,” Archives of Iranian Medicine, vol. 10, no. 4, pp. 459–466, 2007. View at Google Scholar · View at Scopus
  17. Z. Zhang, H. Lin, M. Shi et al., “Human umbilical cord mesenchymal stem cells improve liver function and ascites in decompensated liver cirrhosis patients,” Journal of Gastroenterology and Hepatology, vol. 27, no. s2, pp. 112–120, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Peng, D.-Y. Xie, B.-L. Lin et al., “Autologous bone marrow mesenchymal stem cell transplantation in liver failure patients caused by hepatitis B: short-term and long-term outcomes,” Hepatology, vol. 54, no. 3, pp. 820–828, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. H. Salama, A.-R. N. Zekri, E. Medhat et al., “Peripheral vein infusion of autologous mesenchymal stem cells in Egyptian HCV-positive patients with end-stage liver disease,” Stem Cell Research and Therapy, vol. 5, no. 3, article no. 70, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. L. Xu, Y. Gong, B. Wang et al., “Randomized trial of autologous bone marrow mesenchymal stem cells transplantation for hepatitis B virus cirrhosis: regulation of Treg/Th17 cells,” Journal of Gastroenterology and Hepatology, vol. 29, no. 8, pp. 1620–1628, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Shi, Z. Zhang, R. Xu et al., “Human mesenchymal stem cell transfusion is safe and improves liver function in acute-on-chronic liver failure patients,” Stem Cells Translational Medicine, vol. 1, no. 10, pp. 725–731, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Vosough, S. Moossavi, S. Mardpour et al., “Repeated intraportal injection of mesenchymal stem cells in combination with pioglitazone in patients with compensated cirrhosis: a clinical report of two cases,” Archives of Iranian Medicine, vol. 19, no. 2, pp. 131–136, 2016. View at Google Scholar · View at Scopus
  23. X.-N. Pan, L.-Q. Zheng, and X.-H. Lai, “Bone marrow-derived mesenchymal stem cell therapy for decompensated liver cirrhosis: a meta-analysis,” World Journal of Gastroenterology, vol. 20, no. 38, pp. 14051–14057, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. X.-R. Ma, Y.-L. Tang, M. Xuan, Z. Chang, X.-Y. Wang, and X.-H. Liang, “Transplantation of autologous mesenchymal stem cells for end-stage liver cirrhosis: a meta-analysis based on seven controlled trials,” Gastroenterology Research and Practice, vol. 2015, Article ID 908275, 10 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. G. Kim, Y. W. Eom, S. K. Baik et al., “Therapeutic effects of mesenchymal stem cells for patients with chronic liver diseases: systematic review and meta-analysis,” Journal of Korean Medical Science, vol. 30, no. 10, pp. 1405–1415, 2015. View at Publisher · View at Google Scholar · View at Scopus
  26. N. N. Than, C. L. Tomlinson, D. Haldar, A. L. King, D. Moore, and P. N. Newsome, “Clinical effectiveness of cell therapies in patients with chronic liver disease and acute-on-chronic liver failure: a systematic review protocol,” Systematic Reviews, vol. 5, no. 1, article 100, 2016. View at Publisher · View at Google Scholar
  27. H. Yukawa, M. Watanabe, N. Kaji et al., “Monitoring transplanted adipose tissue-derived stem cells combined with heparin in the liver by fluorescence imaging using quantum dots,” Biomaterials, vol. 33, no. 7, pp. 2177–2186, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. E. Akhan, D. Tuncel, and K. C. Akcali, “Nanoparticle labeling of bone marrow-derived rat mesenchymal stem cells: their use in differentiation and tracking,” BioMed Research International, vol. 2015, Article ID 298430, 9 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Wang, L. Cheng, H. Xu, and Z. Liu, “Towards whole-body imaging at the single cell level using ultra-sensitive stem cell labeling with oligo-arginine modified upconversion nanoparticles,” Biomaterials, vol. 33, no. 19, pp. 4872–4881, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. Z. Li, X. Hu, J. Mao et al., “Optimization of mesenchymal stem cells (MSCs) delivery dose and route in mice with acute liver injury by bioluminescence imaging,” Molecular Imaging and Biology, vol. 17, no. 2, pp. 185–194, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. J. J. Liu, X. J. Hu, Z. R. Li et al., “In Vivo bioluminescence imaging of transplanted mesenchymal stromal cells and their rejection mediated by intrahepatic NK cells,” Molecular Imaging and Biology, 2016. View at Google Scholar
  32. C.-G. Wu, J.-C. Zhang, C.-Q. Xie et al., “In vivo tracking of human placenta derived mesenchymal stem cells in nude mice via14C-TdR labeling,” BMC Biotechnology, vol. 15, no. 1, article no. 55, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Bos, Y. Delmas, A. Desmoulière et al., “In vivo MR imaging of intravascularly injected magnetically labeled mesenchymal stem cells in rat kidney and liver,” Radiology, vol. 233, no. 3, pp. 781–789, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. A. S. Arbab, E. K. Jordan, L. B. Wilson, G. T. Yocum, B. K. Lewis, and J. A. Frank, “In vivo trafficking and targeted delivery of magnetically labeled stem cells,” Human Gene Therapy, vol. 15, no. 4, pp. 351–360, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Cai, X. Zhang, X. Wang, C. Li, and G. Liu, “In vivo MR imaging of magnetically labeled mesenchymal stem cells transplanted into rat liver through hepatic arterial injection,” Contrast Media & Molecular Imaging, vol. 3, no. 2, pp. 61–66, 2008. View at Google Scholar · View at Scopus
  36. S. Ju, G.-J. Teng, H. Lu et al., “In vivo MR tracking of mesenchymal stem cells in rat liver after intrasplenic transplantation,” Radiology, vol. 245, no. 1, pp. 206–215, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Ju, G.-J. Teng, H. Lu et al., “In vivo differentiation of magnetically labeled mesenchymal stem cells into hepatocytes for cell therapy to repair damaged liver,” Investigative Radiology, vol. 45, no. 10, pp. 625–633, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. D. Choi, J. H. Kim, M. Lim et al., “Hepatocyte-like cells from human mesenchymal stem cells engrafted in regenerating rat liver tracked with in vivo magnetic resonance imaging,” Tissue Engineering Part C: Methods, vol. 14, no. 1, pp. 15–23, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Zhong, Z. Tang, R. Xu et al., “Effect of transplantation route on stem cell migration to fibrotic liver ofrats via cellular magnetic resonance imaging,” Cytotherapy, vol. 15, no. 10, pp. 1266–1274, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. T. H. Kim, J. K. Kim, W. Shim, S. Y. Kim, T. J. Park, and J. Y. Jung, “Tracking of transplanted mesenchymal stem cells labeled with fluorescent magnetic nanoparticle in liver cirrhosis rat model with 3-T MRI,” Magnetic Resonance Imaging, vol. 28, no. 7, pp. 1004–1013, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. H.-L. Shuai, R.-L. Yan, H. Song, D.-L. Chen, and X. Luo, “Analysis of feasibility of in vitro nuclear magnetic resonance tracking human umbilical cord mesenchymal stem cells by Gd-DTPA labeled,” Magnetic Resonance Imaging, vol. 32, no. 7, pp. 934–940, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. H. Shuai, C. Shi, J. Lan, D. Chen, and X. Luo, “Double labelling of human umbilical cord mesenchymal stem cells with Gd-DTPA and PKH26 and the influence on biological characteristics of hUCMSCs,” International Journal of Experimental Pathology, vol. 96, no. 1, pp. 63–72, 2015. View at Publisher · View at Google Scholar · View at Scopus
  43. H. Pan, J. Lan, X. Luo, J. Gao, X. Xie, and H. Guo, “Biologic properties of gadolinium diethylenetriaminepentaacetic acid-labeled and PKH26-labeled human umbilical cord mesenchymal stromal cells,” Cytotherapy, vol. 16, no. 1, pp. 74–83, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. E. J. Ribot, J. M. Gaudet, Y. Chen, K. M. Gilbert, and P. J. Foster, “In vivo MR detection of fluorine-labeled human MSC using the bSSFP sequence,” International Journal of Nanomedicine, vol. 9, no. 1, pp. 1731–1739, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. E. T. Ahrens, R. Flores, H. Xu, and P. A. Morel, “In vivo imaging platform for tracking immunotherapeutic cells,” Nature Biotechnology, vol. 23, no. 8, pp. 983–987, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. B. M. Helfer, A. Balducci, A. D. Nelson et al., “Functional assessment of human dendritic cells labeled for in vivo 19F magnetic resonance imaging cell tracking,” Cytotherapy, vol. 12, no. 2, pp. 238–250, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. J. M. Janjic and E. T. Ahrens, “Fluorine-containing nanoemulsions for MRI cell tracking,” Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, vol. 1, no. 5, pp. 492–501, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Chen, G. M. Lanza, and S. A. Wickline, “Quantitative magnetic resonance fluorine imaging: today and tomorrow,” Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, vol. 2, no. 4, pp. 431–440, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. B. Zheng, T. Vazin, P. W. Goodwill et al., “Magnetic particle imaging tracks the long-term fate of in vivo neural cell implants with high image contrast,” Scientific Reports, vol. 5, Article ID 14055, 2015. View at Publisher · View at Google Scholar · View at Scopus
  50. B. Zheng, M. P. von See, E. Yu et al., “Quantitative magnetic particle imaging monitors the transplantation, biodistribution, and clearance of stem cells in vivo,” Theranostics, vol. 6, no. 3, pp. 291–301, 2016. View at Publisher · View at Google Scholar
  51. Y. Ito-Fujishiro, H. Koie, H. Shibata et al., “Tracking cells implanted into cynomolgus monkeys (Macaca fascicularis) using MRI,” Experimental Animals, vol. 65, no. 3, pp. 311–318, 2016. View at Publisher · View at Google Scholar
  52. X.-L. Shi, J.-Y. Gu, B. Han, H.-Y. Xu, L. Fang, and Y.-T. Ding, “Magnetically labeled mesenchymal stem cells after autologous transplantation into acutely injured liver,” World Journal of Gastroenterology, vol. 16, no. 29, pp. 3674–3679, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Spriet, G. B. Hunt, N. J. Walker, and D. L. Borjesson, “Scintigraphic tracking of mesenchymal stem cells after portal, systemic intravenous and splenic administration in healthy beagle dogs,” Veterinary Radiology and Ultrasound, vol. 56, no. 3, pp. 327–334, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Gholamrezanezhad, S. Mirpour, M. Bagheri et al., “In vivo tracking of 111In-oxine labeled mesenchymal stem cells following infusion in patients with advanced cirrhosis,” Nuclear Medicine and Biology, vol. 38, no. 7, pp. 961–967, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. F. Defresne, T. Tondreau, X. Stéphenne et al., “Biodistribution of adult derived human liver stem cells following intraportal infusion in a 17-year-old patient with glycogenosis type 1A,” Nuclear Medicine and Biology, vol. 41, no. 4, pp. 371–375, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. S. S. Kelkar and T. M. Reineke, “Theranostics: combining imaging and therapy,” Bioconjugate Chemistry, vol. 22, no. 10, pp. 1879–1903, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. S. M. Janib, A. S. Moses, and J. A. MacKay, “Imaging and drug delivery using theranostic nanoparticles,” Advanced Drug Delivery Reviews, vol. 62, no. 11, pp. 1052–1063, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. J. V. Jokerst and S. S. Gambhir, “Molecular imaging with theranostic nanoparticles,” Accounts of Chemical Research, vol. 44, no. 10, pp. 1050–1060, 2011. View at Publisher · View at Google Scholar
  59. X. Ma, Y. Zhao, and X. J. Liang, “Theranostic nanoparticles engineered for clinic and pharmaceutics,” Accounts of Chemical Research, vol. 44, no. 10, pp. 1114–1122, 2011. View at Publisher · View at Google Scholar
  60. P. Wang and A. Moore, “Theranostic magnetic resonance imaging of type 1 diabetes and pancreatic islet transplantation,” Quantitative Imaging in Medicine and Surgery, vol. 2, no. 3, pp. 151–162, 2012. View at Google Scholar
  61. D. Yoo, J.-H. Lee, T.-H. Shin, and J. Cheon, “Theranostic magnetic nanoparticles,” Accounts of Chemical Research, vol. 44, no. 10, pp. 863–874, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. P. Pang, C. Wu, F. Gong et al., “Nanovector for gene transfection and MR imaging of mesenchymal stem cells,” Journal of Biomedical Nanotechnology, vol. 11, no. 4, pp. 644–656, 2015. View at Publisher · View at Google Scholar · View at Scopus
  63. P. J. Kempen, S. Greasley, K. A. Parker et al., “Theranostic mesoporous silica nanoparticles biodegrade after pro-survival drug delivery and ultrasound/magnetic resonance imaging of stem cells,” Theranostics, vol. 5, no. 6, pp. 631–642, 2015. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Pulavendran, C. Rose, and A. B. Mandal, “Hepatocyte growth factor incorporated chitosan nanoparticles augment the differentiation of stem cell into hepatocytes for the recovery of liver cirrhosis in mice,” Journal of Nanobiotechnology, vol. 9, article no. 15, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. J. Wang, Z. Lu, M. G. Wientjes, and J. L.-S. Au, “Delivery of siRNA therapeutics: barriers and carriers,” AAPS Journal, vol. 12, no. 4, pp. 492–503, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. X. Zhao, Q. Huang, and Y. Jin, “Gold nanorod delivery of LSD1 siRNA induces human mesenchymal stem cell differentiation,” Materials Science and Engineering C, vol. 54, article no. 5448, pp. 142–149, 2015. View at Publisher · View at Google Scholar · View at Scopus
  67. E. Alizadeh, A. Akbarzadeh, M. B. Eslaminejad et al., “Up regulation of liver-enriched transcription factors HNF4a and HNF6 and liver-specific microRNA (miR-122) by inhibition of let-7b in mesenchymal stem cells,” Chemical Biology and Drug Design, vol. 85, no. 3, pp. 268–279, 2015. View at Publisher · View at Google Scholar · View at Scopus
  68. K. D. Chen, K. T. Huang, C. C. Lin et al., “MicroRNA-27b enhances the hepatic regenerative properties of adipose-derived mesenchymal stem cells,” Molecular Therapy. Nucleic Acids, vol. 5, article e285, 2016. View at Publisher · View at Google Scholar
  69. R. S. M. Gomes, R. P. D. Neves, L. Cochlin et al., “Efficient pro-survival/angiogenic miRNA delivery by an MRI-detectable nanomaterial,” ACS Nano, vol. 7, no. 4, pp. 3362–3372, 2013. View at Publisher · View at Google Scholar · View at Scopus
  70. J. Zhao, J. Vykoukal, M. Abdelsalam et al., “Stem cell-mediated delivery of SPIO-loaded gold nanoparticles for the theranosis of liver injury and hepatocellular carcinoma,” Nanotechnology, vol. 25, no. 40, Article ID 405101, 2014. View at Publisher · View at Google Scholar · View at Scopus
  71. K. von der Haar, A. Lavrentieva, F. Stahl, T. Scheper, and C. Blume, “Lost signature: progress and failures in in vivo tracking of implanted stem cells,” Applied Microbiology and Biotechnology, vol. 99, no. 23, pp. 9907–9922, 2015. View at Publisher · View at Google Scholar · View at Scopus
  72. J. Chung, R. Dash, K. Kee et al., “Theranostic effect of serial manganese-enhanced magnetic resonance imaging of human embryonic stem cell derived teratoma,” Magnetic Resonance in Medicine, vol. 68, no. 2, pp. 595–599, 2012. View at Publisher · View at Google Scholar · View at Scopus
  73. M. Rodriguez-Porcel, “In vivo imaging and monitoring of transplanted stem cells: clinical applications,” Current Cardiology Reports, vol. 12, no. 1, pp. 51–58, 2010. View at Publisher · View at Google Scholar
  74. D. Y. Lee and K. C. P. Li, “Molecular theranostics: a primer for the imaging professional,” American Journal of Roentgenology, vol. 197, no. 2, pp. 318–324, 2011. View at Publisher · View at Google Scholar · View at Scopus