Location via proxy:   [ UP ]  
[Report a bug]   [Manage cookies]                
Skip to main content
SpringerLink
Log in

Ultrasound Imaging in Inflammation Research

  • Chapter
  • First Online:
Imaging Inflammation

Part of the book series: Progress in Inflammation Research ((PIR,volume 91))

  • 518 Accesses

Abstract

Ultrasound is a well-established and widely used tool for both clinical diagnosis and preclinical research. In this chapter, we review the physics behind and applications of 2D, Doppler, and contrast-enhanced ultrasound. Our focus will be the research applications of contrast-enabled molecular imaging of inflammatory mediators as a tool for understanding atherosclerosis and ischemic memory. We will also cover the use of ultrasound in the diagnosis of and research on inflammatory conditions including rheumatoid arthritis and renal failure. Our work and others’ demonstrate the continued place of ultrasound at the cutting edge of biomedical practice and research.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Bushberg JT, Seibert JA Jr, Boone EMLJM. The essential physics of medical imaging. 3rd ed. Third, Nor. Philadelphia: LWW; 2011.

    Google Scholar 

  2. Wettlaufer J. Physical principles of medical imaging. 2nd ed. Radiology, vol. 200. Radiological Society of North America; 1996. p. 504. https://doi.org/10.1148/radiology.200.2.504.

    Book  Google Scholar 

  3. Pellett AA, Kerut EK. The doppler equation. Echocardiography. 2004;21:197–8. https://doi.org/10.1111/j.0742-2822.2004.03146.x.

    Article  PubMed  Google Scholar 

  4. Baker DW, Rubenstein SA, Lorch GS. Pulsed doppler echocardiography: principles and applications. Am J Med. 1977;63:69–80. https://doi.org/10.1016/0002-9343(77)90119-X.

    Article  CAS  PubMed  Google Scholar 

  5. Lee C, Jeon M, Kim C. Photoacoustic imaging in nanomedicine. In: Hamblin MR, Avci P, editors. Appl Nanosci Photomed. Elsevier; 2015. p. 31–47. https://doi.org/10.1533/9781908818782.31.

    Chapter  Google Scholar 

  6. van den Berg PJ, Daoudi K, Bernelot Moens HJ, Steenbergen W. Feasibility of photoacoustic/ultrasound imaging of synovitis in finger joints using a point-of-care system. Photo-Dermatology. 2017;8:8–14. https://doi.org/10.1016/j.pacs.2017.08.002.

    Article  Google Scholar 

  7. Jayaweera AR, Edwards N, Glasheen WP, Villanueva FS, Abbott RD, Kaul S. In vivo myocardial kinetics of air-filled albumin microbubbles during myocardial contrast echocardiography. Comparison with radiolabeled red blood cells. Circ Res. 1994;74:1157–65. https://doi.org/10.1161/01.RES.74.6.1157.

    Article  CAS  PubMed  Google Scholar 

  8. Lindner JR, Song J, Jayaweera AR, Sklenar J, Kaul S. Microvascular rheology of Definity microbubbles after intra-arterial and intravenous administration. J Am Soc Echocardiogr. 2002;15:396–403. https://doi.org/10.1067/mje.2002.117290.

    Article  PubMed  Google Scholar 

  9. Kaufmann BA, Wei K, Lindner JR. Contrast echocardiography. Curr Probl Cardiol. 2007;32:51–96. https://doi.org/10.1016/j.cpcardiol.2006.10.004.

    Article  PubMed  Google Scholar 

  10. de Jong N, Hoff L, Skotland T, Bom N. Absorption and scatter of encapsulated gas filled microspheres: theoretical considerations and some measurements. Ultrasonics. 1992;30:95–103. https://doi.org/10.1016/0041-624X(92)90041-J.

    Article  PubMed  Google Scholar 

  11. Qin S, Caskey CF, Ferrara KW. Ultrasound contrast microbubbles in imaging and therapy: physical principles and engineering. Phys Med Biol. 2009;54:R27–57. https://doi.org/10.1088/0031-9155/54/6/R01.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Seol S-H, Davidson BP, Belcik JT, Mott BH, Goodman RM, Ammi A, et al. Real-time contrast ultrasound muscle perfusion imaging with intermediate-power imaging coupled with acoustically durable microbubbles. J Am Soc Echocardiogr. 2015;28:718–726.e2. https://doi.org/10.1016/j.echo.2015.02.002.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Kutty S, Biko DM, Goldberg AB, Quartermain MD, Feinstein SB. Contrast-enhanced ultrasound in pediatric echocardiography. Pediatr Radiol. 2021;51:2408–17. https://doi.org/10.1007/s00247-021-05119-3.

    Article  PubMed  Google Scholar 

  14. Grønholdt M-LM, Nordestgaard BG, Schroeder TV, Vorstrup S, Sillesen H. Ultrasonic Echolucent carotid plaques predict future strokes. Circulation. 2001;104:68–73. https://doi.org/10.1161/hc2601.091704.

    Article  PubMed  Google Scholar 

  15. Petersen C, Peçanha PB, Venneri L, Pasanisi E, Pratali L, Picano E. The impact of carotid plaque presence and morphology on mortality outcome in cardiological patients. Cardiovasc Ultrasound. 2006;4:16. https://doi.org/10.1186/1476-7120-4-16.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Meola M, Samoni S, Petrucci I. Imaging in chronic kidney disease. Ultrasound imaging acute chronic kidney dis. Karger Publishers; 2016. p. 69–80. https://doi.org/10.1159/000445469.

    Book  Google Scholar 

  17. Bigé N, Lévy PP, Callard P, Faintuch J-M, Chigot V, Jousselin V, et al. Renal arterial resistive index is associated with severe histological changes and poor renal outcome during chronic kidney disease. BMC Nephrol. 2012;13:139. https://doi.org/10.1186/1471-2369-13-139.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Sugiura T, Wada A. Resistive index predicts renal prognosis in chronic kidney disease. Nephrol Dial Transplant. 2009;24:2780–5. https://doi.org/10.1093/ndt/gfp121.

    Article  PubMed  Google Scholar 

  19. O’Neill WC. Renal relevant radiology: use of ultrasound in kidney disease and nephrology procedures. Clin J Am Soc Nephrol American Society of Nephrology. 2014;9:373–81. https://doi.org/10.2215/CJN.03170313.

    Article  Google Scholar 

  20. Nomura G, Kinoshita E, Yamagata Y, Koga N. Usefulness of renal ultrasonography for assessment of severity and course of acute tubular necrosis. J Clin Ultrasound. 1984;12:135–9. https://doi.org/10.1002/jcu.1870120304.

    Article  CAS  PubMed  Google Scholar 

  21. O’Neill WC, Baumgarten DA. Ultrasonography in renal transplantation. Am J Kidney Dis. 2002;39:663–78. https://doi.org/10.1053/ajkd.2002.31978.

    Article  PubMed  Google Scholar 

  22. Thölking G, Schuette-Nuetgen K, Kentrup D, Pawelski H, Reuter S. Imaging-based diagnosis of acute renal allograft rejection. World J Transplant. 2016;6:174. https://doi.org/10.5500/wjt.v6.i1.174.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Naesens M, Heylen L, Lerut E, Claes K, De Wever L, Claus F, et al. Intrarenal resistive index after renal transplantation. N Engl J Med. 2013;369:1797–806. https://doi.org/10.1056/NEJMoa1301064.

    Article  CAS  PubMed  Google Scholar 

  24. Grantham JJ. Pathogenesis of renal cyst expansion: opportunities for therapy. Am J Kidney Dis. 1994;23:210–8. https://doi.org/10.1016/S0272-6386(12)80974-7.

    Article  CAS  PubMed  Google Scholar 

  25. Pei Y, Obaji J, Dupuis A, Paterson AD, Magistroni R, Dicks E, et al. Unified criteria for ultrasonographic diagnosis of ADPKD. J Am Soc Nephrol. 2009;20:205–12. https://doi.org/10.1681/ASN.2008050507.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Lee J, Darcy M. Renal cysts and urinomas. Semin Intervent Radiol. 2011;28:380–91. https://doi.org/10.1055/s-0031-1296080.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Heidari B. Rheumatoid arthritis: early diagnosis and treatment outcomes. Caspian J Intern Med. 2011;2:161–70.

    PubMed  PubMed Central  Google Scholar 

  28. Naredo E, Bonilla G, Gamero F, Uson J, Carmona L, Laffon A. Assessment of inflammatory activity in rheumatoid arthritis: a comparative study of clinical evaluation with grey scale and power Doppler ultrasonography. Ann Rheum Dis. 2005;64:375–81. https://doi.org/10.1136/ard.2004.023929.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Newman JS, Adler RS, Bude RO, Rubin JM. Detection of soft-tissue hyperemia: value of power doppler sonography. Am J Roentgenol. 1994;163:385–9. https://doi.org/10.2214/ajr.163.2.8037037.

    Article  CAS  Google Scholar 

  30. Hubac J, Gilson M, Gaudin P, Clay M, Imbert B, Carpentier P. Ultrasound prevalence of wrist, hand, ankle and foot synovitis and tenosynovitis in systemic sclerosis, and relationship with disease features and hand disability. Jt Bone Spine. 2020;87:229–33. https://doi.org/10.1016/j.jbspin.2020.01.011.

    Article  Google Scholar 

  31. Massignan Â, da Silva M, Chakr R, Bueno P, de Andrade N, Brenol CV. Synovitis and tenosynovitis on ultrasound as predictors of DMARD tapering failure in patients with long-standing rheumatoid arthritis in clinical remission or low disease activity. J Ultrasound Med. 2021;40:2549–59. https://doi.org/10.1002/jum.15640.

    Article  PubMed  Google Scholar 

  32. Wakefield RJ, Gibbon WW, Conaghan PG, O’Connor P, McGonagle D, Pease C, et al. The value of sonography in the detection of bone erosions in patients with rheumatoid arthritis: a comparison with conventional radiography. Arthritis Rheum. 2000;43:2762–70. https://doi.org/10.1002/1529-0131(200012)43:12%3C2762::aid-anr16%3E3.0.co;2-#.

    Article  CAS  PubMed  Google Scholar 

  33. Kawashiri S, Fujikawa K, Nishino A, Okada A, Aramaki T, Shimizu T, et al. Ultrasound-detected bone erosion is a relapse risk factor after discontinuation of biologic disease-modifying antirheumatic drugs in patients with rheumatoid arthritis whose ultrasound power Doppler synovitis activity and clinical disease activity are wel. Arthritis Res Ther. 2017;19:108. https://doi.org/10.1186/s13075-017-1320-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Sundin U, Sundlisater NP, Aga A-B, Sexton J, Nordberg LB, Hammer HB, et al. Value of MRI and ultrasound for prediction of therapeutic response and erosive progression in patients with early rheumatoid arthritis managed by an aggressive treat-to-target strategy. RMD Open BMJ Specialist Journals. 2021;7:e001525. https://doi.org/10.1136/rmdopen-2020-001525.

    Article  Google Scholar 

  35. Chamberland DL, Wang X, Roessler BJ. Photoacoustic tomography of carrageenan-induced arthritis in a rat model. J Biomed Opt. 2008;13:011005. https://doi.org/10.1117/1.2841028.

    Article  PubMed  Google Scholar 

  36. Rajian JR, Shao X, Chamberland DL, Wang X. Characterization and treatment monitoring of inflammatory arthritis by photoacoustic imaging: a study on adjuvant-induced arthritis rat model. Biomed Opt Express. 2013;4:900. https://doi.org/10.1364/BOE.4.000900.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Jo J, Tian C, Xu G, Sarazin J, Schiopu E, Gandikota G, et al. Photoacoustic tomography for human musculoskeletal imaging and inflammatory arthritis detection. Photo-Dermatology. 2018;12:82–9. https://doi.org/10.1016/j.pacs.2018.07.004.

    Article  Google Scholar 

  38. Takiuchi S, Rakugi H, Honda K, Masuyama T, Hirata N, Ito H, et al. Quantitative ultrasonic tissue characterization can identify high-risk atherosclerotic alteration in human carotid arteries. Circulation. 2000;102:766–70. https://doi.org/10.1161/01.CIR.102.7.766.

    Article  CAS  PubMed  Google Scholar 

  39. Sano K, Kawasaki M, Ishihara Y, Okubo M, Tsuchiya K, Nishigaki K, et al. Assessment of vulnerable plaques causing acute coronary syndrome using integrated backscatter intravascular ultrasound. J Am Coll Cardiol. 2006;47:734–41. https://doi.org/10.1016/j.jacc.2005.09.061.

    Article  PubMed  Google Scholar 

  40. Nair A, Kuban BD, Tuzcu EM, Schoenhagen P, Nissen SE, Vince DG. Coronary plaque classification with intravascular ultrasound radiofrequency data analysis. Circulation. 2002;106:2200–6. https://doi.org/10.1161/01.CIR.0000035654.18341.5E.

    Article  PubMed  Google Scholar 

  41. Nair A, Kuban BD, Obuchowski N, Vince DG. Assessing spectral algorithms to predict atherosclerotic plaque composition with normalized and raw intravascular ultrasound data. Ultrasound Med Biol. 2001;27:1319–31. https://doi.org/10.1016/S0301-5629(01)00436-7.

    Article  CAS  PubMed  Google Scholar 

  42. Nasu K, Tsuchikane E, Katoh O, Vince DG, Virmani R, Surmely J-F, et al. Accuracy of in vivo coronary plaque morphology assessment. J Am Coll Cardiol. 2006;47:2405–12. https://doi.org/10.1016/j.jacc.2006.02.044.

    Article  PubMed  Google Scholar 

  43. König A, Klauss V. Virtual histology. Heart. 2007;93:977–82. https://doi.org/10.1136/hrt.2007.116384.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Gogas BD, Farooq V, Serruys PW, Garcìa-Garcìa HM. Assessment of coronary atherosclerosis by IVUS and IVUS-based imaging modalities: progression and regression studies, tissue composition and beyond. Int J Cardiovasc Imaging. 2011;27:225–37. https://doi.org/10.1007/s10554-010-9791-0.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Stone GW, Maehara A, Lansky AJ, de Bruyne B, Cristea E, Mintz GS, et al. A prospective natural-history study of coronary atherosclerosis. N Engl J Med. 2011;364:226–35. https://doi.org/10.1056/NEJMoa1002358.

    Article  CAS  PubMed  Google Scholar 

  46. Calvert PA, Obaid DR, O’Sullivan M, Shapiro LM, McNab D, Densem CG, et al. Association between IVUS findings and adverse outcomes in patients with coronary artery disease. JACC Cardiovasc Imaging. 2011;4:894–901. https://doi.org/10.1016/j.jcmg.2011.05.005.

    Article  PubMed  Google Scholar 

  47. Cheng JM, Garcia-Garcia HM, de Boer SPM, Kardys I, Heo JH, Akkerhuis KM, et al. In vivo detection of high-risk coronary plaques by radiofrequency intravascular ultrasound and cardiovascular outcome: results of the ATHEROREMO-IVUS study. Eur Heart J. 2014;35:639–47. https://doi.org/10.1093/eurheartj/eht484.

    Article  PubMed  Google Scholar 

  48. Ophir J, Céspedes I, Ponnekanti H, Yazdi Y, Li X. Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrason Imaging. 1991;13:111–34. https://doi.org/10.1177/016173469101300201.

    Article  CAS  PubMed  Google Scholar 

  49. Maurice RL, Brusseau É, Finet G, Cloutier G. On the potential of the Lagrangian speckle model estimator to characterize atherosclerotic plaques in endovascular elastography: in vitro experiments using an excised human carotid artery. Ultrasound Med Biol. 2005;31:85–91. https://doi.org/10.1016/j.ultrasmedbio.2004.07.009.

    Article  PubMed  Google Scholar 

  50. Schaar JA, de Korte CL, Mastik F, Strijder C, Pasterkamp G, Boersma E, et al. Characterizing vulnerable plaque features with intravascular elastography. Circulation. 2003;108:2636–41. https://doi.org/10.1161/01.CIR.0000097067.96619.1F.

    Article  PubMed  Google Scholar 

  51. Lindner JR, Coggins MP, Kaul S, Klibanov AL, Brandenburger GH, Ley K. Microbubble persistence in the microcirculation during ischemia/reperfusion and inflammation is caused by integrin- and complement-mediated adherence to activated leukocytes. Circulation. 2000;101:668–75. https://doi.org/10.1161/01.CIR.101.6.668.

    Article  CAS  PubMed  Google Scholar 

  52. Anderson D, Tsutsui J, Xie F, Radio S, Porter T. The role of complement in the adherence of microbubbles to dysfunctional arterial endothelium and atherosclerotic plaque. Cardiovasc Res. 2007;73:597–606. https://doi.org/10.1016/j.cardiores.2006.11.029.

    Article  CAS  PubMed  Google Scholar 

  53. Lindner JR, Song J, Xu F, Klibanov AL, Singbartl K, Ley K, et al. Noninvasive ultrasound imaging of inflammation using microbubbles targeted to activated leukocytes. Circulation. 2000;102:2745–50. https://doi.org/10.1161/01.CIR.102.22.2745.

    Article  CAS  PubMed  Google Scholar 

  54. Bachmann C, Klibanov AL, Olson TS, Sonnenschein JR, Rivera-Nieves J, Cominelli F, et al. Targeting mucosal Addressin cellular adhesion molecule (MAdCAM)-1 to noninvasively image experimental Crohn’s disease. Gastroenterology. 2006;130:8–16. https://doi.org/10.1053/j.gastro.2005.11.009.

    Article  CAS  PubMed  Google Scholar 

  55. Kaufmann BA, Sanders JM, Davis C, Xie A, Aldred P, Sarembock IJ, et al. Molecular imaging of inflammation in atherosclerosis with targeted ultrasound detection of vascular cell adhesion Molecule-1. Circulation. 2007;116:276–84. https://doi.org/10.1161/CIRCULATIONAHA.106.684738.

    Article  CAS  PubMed  Google Scholar 

  56. Weller GER, Villanueva FS, Klibanov AL, Wagner WR. Modulating targeted adhesion of an ultrasound contrast agent to dysfunctional endothelium. Ann Biomed Eng. 2002;30:1012–9. https://doi.org/10.1114/1.1513565.

    Article  PubMed  Google Scholar 

  57. Villanueva FS, Jankowski RJ, Klibanov S, Pina ML, Alber SM, Watkins SC, et al. Microbubbles targeted to intercellular adhesion Molecule-1 bind to activated coronary artery endothelial cells. Circulation. 1998;98:1–5. https://doi.org/10.1161/01.CIR.98.1.1.

    Article  CAS  PubMed  Google Scholar 

  58. Lankford M, Behm CZ, Yeh J, Klibanov AL, Robinson P, Lindner JR. Effect of microbubble ligation to cells on ultrasound signal enhancement. Investig Radiol. 2006;41:721–8. https://doi.org/10.1097/01.rli.0000236825.72344.a9.

    Article  Google Scholar 

  59. Dayton PA, Chomas JE, Lum AFH, Allen JS, Lindner JR, Simon SI, et al. Optical and acoustical dynamics of microbubble contrast agents inside neutrophils. Biophys J. 2001;80:1547–56. https://doi.org/10.1016/S0006-3495(01)76127-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Lindner JR, Song J, Christiansen J, Klibanov AL, Xu F, Ley K. Ultrasound assessment of inflammation and renal tissue injury with microbubbles targeted to P-selectin. Circulation. 2001;104:2107–12. https://doi.org/10.1161/hc4201.097061.

    Article  CAS  PubMed  Google Scholar 

  61. Carr CL, Qi Y, Davidson B, Chadderdon S, Jayaweera AR, Belcik JT, et al. Dysregulated selectin expression and monocyte recruitment during ischemia-related vascular remodeling in diabetes mellitus. Arterioscler Thromb Vasc Biol. 2011;31:2526–33. https://doi.org/10.1161/ATVBAHA.111.230177.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Hamilton AJ, Huang S-L, Warnick D, Rabbat M, Kane B, Nagaraj A, et al. Intravascular ultrasound molecular imaging of atheroma components in vivo. J Am Coll Cardiol. 2004;43:453–60. https://doi.org/10.1016/j.jacc.2003.07.048.

    Article  PubMed  Google Scholar 

  63. Schumann PA, Christiansen JP, Quigley RM, McCreery TP, Sweitzer RH, Unger EC, Lindner JR, et al. Targeted-microbubble binding selectively to GPIIb IIIa receptors of platelet thrombi. Investig Radiol. 2002;37:587–93. https://doi.org/10.1097/00004424-200211000-00001.

    Article  CAS  Google Scholar 

  64. Lanza GM, Abendschein DR, Hall CS, Scott MJ, Scherrer DE, Houseman A, et al. In vivo molecular imaging of stretch-induced tissue factor in carotid arteries with ligand-targeted nanoparticles. J Am Soc Echocardiogr. 2000;13:608–14. https://doi.org/10.1067/mje.2000.105840.

    Article  CAS  PubMed  Google Scholar 

  65. Wang X, Hagemeyer CE, Hohmann JD, Leitner E, Armstrong PC, Jia F, et al. Novel single-chain antibody-targeted microbubbles for molecular ultrasound imaging of thrombosis. Circulation. 2012;125:3117–26. https://doi.org/10.1161/CIRCULATIONAHA.111.030312.

    Article  CAS  PubMed  Google Scholar 

  66. Latifi Y, Moccetti F, Wu M, Xie A, Packwood W, Qi Y, et al. Thrombotic microangiopathy as a cause of cardiovascular toxicity from the BCR-ABL1 tyrosine kinase inhibitor ponatinib. Blood. 2019;133:1597–606. https://doi.org/10.1182/blood-2018-10-881557.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Ozawa K, Packwood W, Varlamov O, Qi Y, Xie A, Wu MD, et al. Molecular imaging of VWF (von Willebrand factor) and platelet adhesion in postischemic impaired microvascular reflow. Circ Cardiovasc Imaging. 2018;11:e007913. https://doi.org/10.1161/CIRCIMAGING.118.007913.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Pope JH, Aufderheide TP, Ruthazer R, Woolard RH, Feldman JA, Beshansky JR, et al. Missed diagnoses of acute cardiac ischemia in the emergency department. N Engl J Med. 2000;342:1163–70. https://doi.org/10.1056/NEJM200004203421603.

    Article  CAS  PubMed  Google Scholar 

  69. McEver RP, Beckstead JH, Moore KL, Marshall-Carlson L, Bainton DF. GMP-140, a platelet alpha-granule membrane protein, is also synthesized by vascular endothelial cells and is localized in Weibel-Palade bodies. J Clin Invest. 1989;84:92–9. https://doi.org/10.1172/JCI114175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Bevilacqua MP, Nelson RM. Selectins. J Clin Invest. 1993;91:379–87. https://doi.org/10.1172/JCI116210.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Chukwuemeka AO, Brown KA, Venn GE, Chambers DJ. Changes in P-selectin expression on cardiac microvessels in blood-perfused rat hearts subjected to ischemia-reperfusion. Ann Thorac Surg. 2005;79:204–11. https://doi.org/10.1016/j.athoracsur.2004.06.105.

    Article  PubMed  Google Scholar 

  72. Kaufmann BA, Lewis C, Xie A, Mirza-Mohd A, Lindner JR. Detection of recent myocardial ischaemia by molecular imaging of P-selectin with targeted contrast echocardiography. Eur Heart J. 2007;28:2011–7. https://doi.org/10.1093/eurheartj/ehm176.

    Article  PubMed  Google Scholar 

  73. Villanueva FS, Lu E, Bowry S, Kilic S, Tom E, Wang J, et al. Myocardial ischemic memory imaging with molecular echocardiography. Circulation. 2007;115:345–52. https://doi.org/10.1161/CIRCULATIONAHA.106.633917.

    Article  PubMed  PubMed Central  Google Scholar 

  74. Davidson BP, Chadderdon SM, Belcik JT, Gupta S, Lindner JR. Ischemic memory imaging in nonhuman primates with echocardiographic molecular imaging of selectin expression. J Am Soc Echocardiogr. 2014;27:786–93.e2. https://doi.org/10.1016/j.echo.2014.03.013.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Davidson BP, Kaufmann BA, Belcik JT, Xie A, Qi Y, Lindner JR. Detection of antecedent myocardial ischemia with multiselectin molecular imaging. J Am Coll Cardiol. 2012;60:1690–7. https://doi.org/10.1016/j.jacc.2012.07.027.

    Article  CAS  PubMed  Google Scholar 

  76. Christiansen JP, Leong-Poi H, Klibanov AL, Kaul S, Lindner JR. Noninvasive imaging of myocardial reperfusion injury using leukocyte-targeted contrast echocardiography. Circulation. 2002;105:1764–7. https://doi.org/10.1161/01.CIR.0000015466.89771.E2.

    Article  PubMed  Google Scholar 

  77. Mott B, Packwood W, Xie A, Belcik JT, Taylor RP, Zhao Y, et al. Echocardiographic ischemic memory imaging through complement-mediated vascular adhesion of phosphatidylserine-containing microbubbles. JACC Cardiovasc Imaging. 2016;9:937–46. https://doi.org/10.1016/j.jcmg.2015.11.031.

    Article  PubMed  Google Scholar 

  78. Davidson BP, Hodovan J, Layoun ME, Golwala H, Zahr F, Lindner JR. Echocardiographic ischemic memory molecular imaging for point-of-care detection of myocardial ischemia. J Am Coll Cardiol. 2021;78:1990–2000. https://doi.org/10.1016/j.jacc.2021.08.068.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Libby P, Ridker PM, Hansson GK. Inflammation in atherosclerosis. J Am Coll Cardiol. 2009;54:2129–38. https://doi.org/10.1016/j.jacc.2009.09.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Kaufmann BA, Carr CL, Belcik JT, Xie A, Yue Q, Chadderdon S, et al. Molecular imaging of the initial inflammatory response in atherosclerosis. Arterioscler Thromb Vasc Biol. 2010;30:54–9. https://doi.org/10.1161/ATVBAHA.109.196386.

    Article  CAS  Google Scholar 

  81. Chadderdon SM, Belcik JT, Bader L, Kirigiti MA, Peters DM, Kievit P, et al. Proinflammatory endothelial activation detected by molecular imaging in obese nonhuman primates coincides with onset of insulin resistance and progressively increases with duration of insulin resistance. Circulation. 2014;129:471–8. https://doi.org/10.1161/CIRCULATIONAHA.113.003645.

    Article  CAS  PubMed  Google Scholar 

  82. Shim CY, Liu YN, Atkinson T, Xie A, Foster T, Davidson BP, et al. Molecular imaging of platelet–endothelial interactions and endothelial von Willebrand Factor in early and mid-stage atherosclerosis. Circ Cardiovasc Imaging. 2015;8:e002765. https://doi.org/10.1161/CIRCIMAGING.114.002765.

    Article  PubMed  Google Scholar 

  83. Moccetti F, Brown E, Xie A, Packwood W, Qi Y, Ruggeri Z, et al. Myocardial infarction produces sustained proinflammatory endothelial activation in remote arteries. J Am Coll Cardiol. 2018;72:1015–26. https://doi.org/10.1016/j.jacc.2018.06.044.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Liu Y, Davidson BP, Yue Q, Belcik T, Xie A, Inaba Y, et al. Molecular imaging of inflammation and platelet adhesion in advanced atherosclerosis effects of antioxidant therapy with NADPH oxidase inhibition. Circ Cardiovasc Imaging. 2013;6:74–82. https://doi.org/10.1161/CIRCIMAGING.112.975193.

    Article  PubMed  Google Scholar 

  85. Hamilton A, Huang S-L, Warnick D, Stein A, Rabbat M, Madhav T, et al. Left ventricular thrombus enhancement after intravenous injection of echogenic immunoliposomes. Circulation. 2002;105:2772–8. https://doi.org/10.1161/01.CIR.0000017500.61563.80.

    Article  PubMed  Google Scholar 

  86. Cohen D, Colvin RB, Daha MR, Drachenberg CB, Haas M, Nickeleit V, et al. Pros and cons for C4d as a biomarker. Kidney Int. 2012;81:628–39. https://doi.org/10.1038/ki.2011.497.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Liao T, Zhang Y, Ren J, Zheng H, Zhang H, Li X, et al. Noninvasive quantification of intrarenal allograft C4d deposition with targeted ultrasound imaging. Am J Transplant. 2019;19:259–68. https://doi.org/10.1111/ajt.15105.

    Article  CAS  PubMed  Google Scholar 

  88. Grabner A, Kentrup D, Mühlmeister M, Pawelski H, Biermann C, Bettinger T, et al. Noninvasive imaging of acute renal allograft rejection by ultrasound detection of microbubbles targeted to T-lymphocytes in rats. Ultraschall der Medizin – Eur J Ultrasound. 2015;37:82–91. https://doi.org/10.1055/s-0034-1385796.

    Article  Google Scholar 

  89. Xie F, Li Z-P, Wang H-W, Fei X, Jiao Z-Y, Tang W-B, et al. Evaluation of liver ischemia-reperfusion injury in rabbits using a nanoscale ultrasound contrast agent targeting ICAM-1. Gracia-sancho J, editor. PLoS One. 2016;11:e0153805. https://doi.org/10.1371/journal.pone.0153805.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Xie F, Zhang S-H, Cheng J, Wang H-W, Fei X, Jiao Z-Y, et al. Evaluation of hepatic vascular endothelial injury during liver storage by molecular detection and targeted contrast-enhanced ultrasound imaging. IUBMB Life. 2016;68:51–7. https://doi.org/10.1002/iub.1459.

    Article  CAS  PubMed  Google Scholar 

  91. Yu Z, Hu M, Li Z, Dan X, Zhu L, Guo Y, et al. Anti-G250 nanobody-functionalized nanobubbles targeting renal cell carcinoma cells for ultrasound molecular imaging. Nanotechnology. 2020;31:205101. https://doi.org/10.1088/1361-6528/ab7040.

    Article  CAS  PubMed  Google Scholar 

  92. Abou-Elkacem L, Wang H, Chowdhury SM, Kimura RH, Bachawal SV, Gambhir SS, et al. Thy1-targeted microbubbles for ultrasound molecular imaging of pancreatic ductal adenocarcinoma. Clin Cancer Res. 2018;24:1574–85. https://doi.org/10.1158/1078-0432.CCR-17-2057.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Bam R, Daryaei I, Abou-Elkacem L, Vilches-Moure JG, Meuillet EJ, Lutz A, et al. Toward the clinical development and validation of a Thy1-targeted ultrasound contrast agent for the early detection of pancreatic ductal adenocarcinoma. Investig Radiol. 2020;55:711–21. https://doi.org/10.1097/RLI.0000000000000697.

    Article  CAS  Google Scholar 

  94. Foygel K, Wang H, Machtaler S, Lutz AM, Chen R, Pysz M, et al. Detection of pancreatic ductal adenocarcinoma in mice by ultrasound imaging of thymocyte differentiation antigen 1. Gastroenterology. 2013;145:885–94.e3. https://doi.org/10.1053/j.gastro.2013.06.011.

    Article  CAS  PubMed  Google Scholar 

  95. Rojas JD, Lin F, Chiang Y-C, Chytil A, Chong DC, Bautch VL, et al. Ultrasound molecular imaging of VEGFR-2 in clear-cell renal cell carcinoma tracks disease response to antiangiogenic and notch-inhibition therapy. Theranostics. 2018;8:141–55. https://doi.org/10.7150/thno.19658.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Wei S, Fu N, Sun Y, Yang Z, Lei L, Huang P, et al. Targeted contrast-enhanced ultrasound imaging of angiogenesis in an orthotopic mouse tumor model of renal carcinoma. Ultrasound Med Biol. 2014;40:1250–9. https://doi.org/10.1016/j.ultrasmedbio.2013.12.001.

    Article  PubMed  Google Scholar 

  97. Korpanty G, Carbon JG, Grayburn PA, Fleming JB, Brekken RA. Monitoring response to anticancer therapy by targeting microbubbles to tumor vasculature. Clin Cancer Res. 2007;13:323–30. https://doi.org/10.1158/1078-0432.CCR-06-1313.

    Article  CAS  PubMed  Google Scholar 

  98. Baron Toaldo M, Salvatore V, Marinelli S, Palamà C, Milazzo M, Croci L, et al. Use of VEGFR-2 targeted ultrasound contrast agent for the early evaluation of response to sorafenib in a mouse model of hepatocellular carcinoma. Mol Imaging Biol. 2015;17:29–37. https://doi.org/10.1007/s11307-014-0764-x.

    Article  CAS  PubMed  Google Scholar 

  99. Lucas VS, Burk RS, Creehan S, Grap MJ. Utility of high-frequency ultrasound. Plast Surg Nurs. 2014;34:34–8. https://doi.org/10.1097/PSN.0000000000000031.

    Article  PubMed  PubMed Central  Google Scholar 

  100. Hu C, Feng Y, Huang P, Jin J. Adverse reactions after the use of SonoVue contrast agent. Medicine (Baltimore). 2019;98:e17745. https://doi.org/10.1097/MD.0000000000017745.

    Article  PubMed  Google Scholar 

  101. Dijkmans P, Visser C, Kamp O. Adverse reactions to ultrasound contrast agents: is the risk worth the benefit? Eur J Echocardiogr. 2005;6:363–6. https://doi.org/10.1016/j.euje.2005.02.003.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Knight Cardiovascular Institute, Oregon Health & Science University, Portland, OR, USA

    Matthew Muller, Jonathan R. Lindner & Matthew W. Hagen

  2. Oregon National Primate Research Center, Oregon Health & Science University, Portland, OR, USA

    Jonathan R. Lindner

  3. Robert M. Berne Cardiovascular Research Center, University of Virginia Health System, Charlottesville, VA, USA

    Jonathan R. Lindner

  4. Cardiovascular Division, University of Virginia Health System, Charlottesville, VA, USA

    Jonathan R. Lindner

Authors
  1. Matthew Muller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jonathan R. Lindner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthew W. Hagen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jonathan R. Lindner .

Editor information

Editors and Affiliations

  1. Institute of Pharmaceutical Science, King#x2019;s College London, London, UK

    Francis Man

  2. Department of Medicine, University of California, San Francisco, San Francisco, CA, USA

    Simon J. Cleary

Ethics declarations

Funding: Dr. Lindner is supported by grants R01-HL078610, R01-HL130046, and P51-OD011092 from the National Institutes of Health (NIH), Bethesda, MD, and grant 18-18HCFBP_2-0009 from NASA.

Conflict of Interest: The authors have no conflicts of interest to declare.

Ethical approval: Images obtained from human subjects were acquired during studies approved by the Institutional Review Board of Oregon Health and Science University.

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Muller, M., Lindner, J.R., Hagen, M.W. (2023). Ultrasound Imaging in Inflammation Research. In: Man, F., Cleary, S.J. (eds) Imaging Inflammation. Progress in Inflammation Research, vol 91. Springer, Cham. https://doi.org/10.1007/978-3-031-23661-7_4

Download citation

Publish with us

Policies and ethics

Search

Navigation