1921
Volume 81, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Noninvasive assessment of cardiac structure and function is essential to understand the natural course of murine infection with . Magnetic resonance imaging (MRI) and echocardiography have been used to monitor anatomy and function; positron emission tomography (PET) is ideal for monitoring metabolic events in the myocardium. Mice infected with (Brazil strain) were imaged 15–100 days post infection (dpi). Quantitative F-FDG microPET imaging, MRI and echocardiography were performed and compared. Tracer (F-FDG) uptake was significantly higher in infected mice at all days of infection, from 15 to 100 dpi. Dilatation of the right ventricular chamber was observed by MRI from 30 to 100 dpi in infected mice. Echocardiography revealed significantly reduced ejection fraction by 60 dpi. Combination of these three complementary imaging modalities makes it possible to noninvasively quantify cardiovascular function, morphology, and metabolism from the earliest days of infection through the chronic phase.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.2009.09-0338
2009-11-01
2017-07-23
Loading full text...

Full text loading...

/deliver/fulltext/14761645/81/5/0810900.html?itemId=/content/journals/10.4269/ajtmh.2009.09-0338&mimeType=html&fmt=ahah

References

  1. Tanowitz HB, Machado FS, Jelicks LA, Shirani J, de Carvalho AC, Spray DC, Factor SM, Kirchhoff LV, Weiss LM, 2009. Perspectives on Trypanosoma cruzi-induced heart disease (Chagas disease). Prog Cardiovasc Dis 51: 524–539.
  2. Rossi MA, Ramos SG, Bestetti RB, 2003. Chagas’ heart disease: clinical-pathological correlation. Front Biosci 8: e94–e109.
  3. Higuchi Mde L, Benvenuti LA, Martins Reis M, Metzger M, 2003. Pathophysiology of the heart in Chagas’ disease: current status and new developments. Cardiovasc Res 60: 96–107.
  4. Rochitte CE, Nacif MS, de Oliveira Júnior AC, Siqueira-Batista R, Marchiori E, Uellendahl M, de Lourdes Higuchi M, 2007. Cardiac magnetic resonance in Chagas’ disease. Artif Organs 31: 259–267.
  5. Mukherjee S, Nagajyothi F, Mukhopadhyay A, Machado FS, Belbin TJ, Campos de Carvalho A, Guan F, Albanese C, Jelicks LA, Lisanti MP, Silva JS, Spray DC, Weiss LM, Tanowitz HB, 2008. Alterations in myocardial gene expression associated with experimental Trypanosoma cruzi infection. Genomics 91: 423–432.
  6. Gomes JA, Bahia-Oliveira LM, Rocha MO, Busek SC, Teixeira MM, Silva JS, Correa-Oliveira R, 2005. Type 1 chemokine receptor expression in Chagas’ disease correlates with morbidity in cardiac patients. Infect Immun 73: 7960–7966.
  7. Machado FS, Koyama NS, Carregaro V, Ferreira BR, Milanezi CM, Teixeira MM, Rossi MA, Silva JS, 2005. CCR5 plays a critical role in the development of myocarditis and host protection in mice infected with Trypanosoma cruzi. J Infect Dis 191: 627–636.
  8. Michailowsky V, Celes MR, Marino AP, Silva AA, Vieira LQ, Rossi MA, Gazzinelli RT, Lannes-Vieira J, Silva JS, 2004. Intercellular adhesion molecule 1 deficiency leads to impaired recruitment of T lymphocytes and enhanced host susceptibility to infection with Trypanosoma cruzi. J Immunol 173: 463–470.
  9. Scherrer-Crosbie M, 2006. Role of echocardiography in studies of murine models of cardiac diseases. Arch Mal Coeur Vaiss 99: 237–241.
  10. De Souza AP, Tang B, Tanowitz HB, Araújo-Jorge TC, Jelicks LA, 2005. Magnetic resonance imaging in experimental Chagas disease: a brief review of the utility of the method for monitoring right ventricular chamber dilatation. Parasitol Res 97: 87–90.
  11. Chandra M, Shirani J, Shtutin V, Weiss LM, Factor SM, Petkova SB, Rojkind M, Dominguez-Rosales JA, Jelicks LA, Morris SA, Wittner M, Tanowitz HB, 2002. Cardioprotective effects of verapamil on myocardial structure and function in a murine model of chronic Trypanosoma cruzi infection (Brazil strain): an echocardiographic study. Int J Parasitol 32: 207–215.
  12. Jelicks LA, Chandra M, Shirani J, Shtutin V, Tang B, Christ GJ, Factor SM, Wittner M, Huang H, Weiss LM, Mukherjee S, Bouzahzah B, Petkova SB, Teixeira MM, Douglas SA, Loredo ML, D’Orleans-Juste P, Tanowitz HB, 2002. Cardioprotective effects of phosphoramidon on myocardial structure and function in murine Chagas’ disease. Int J Parasitol 32: 1497–1506.
  13. Jelicks LA, Shirani J, Wittner M, Chandra M, Weiss LM, Factor SM, Bekirov I, Braunstein VL, Chan J, Huang H, Tanowitz HB, 1999. Application of cardiac gated magnetic resonance imaging in murine Chagas’ disease. Am J Trop Med Hyg 61: 207–214.
  14. Johannsen B, 2005. The usefulness of radiotracers to make the body biochemically transparent. Amino Acids 29: 307–311.
  15. Phelps ME, 2000. Inaugural article: positron emission tomography provides molecular imaging of biological processes. Proc Natl Acad Sci USA 97: 9226–9233.
  16. Iida H, Takahashi A, Tamura Y, Ono Y, Lammertsma AA, 1995. Myocardial blood flow: comparison of oxygen-15-water bolus injection, slow infusion and oxygen-15-carbon dioxide slow inhalation. J Nucl Med 36: 78–85.
  17. Araujo LI, Lammertsma AA, Rhodes CG, McFalls EO, Iida H, Rechavia E, Galassi A, De Silva R, Jones T, Maseri A, 1991. Noninvasive quantification of regional myocardial blood flow in coronary artery disease with oxygen-15-labeled carbon dioxide inhalation and positron emission tomography. Circulation 83: 875–885.
  18. Camici P, Araujo LI, Spinks T, Lammertsma AA, Kaski JC, Shea MJ, Selwyn AP, Jones T, Maseri A, 1986. Increased uptake of 18F-fluorodeoxyglucose in postischemic myocardium of patients with exercise-induced angina. Circulation 74: 81–88.
  19. Ratib O, Phelps ME, Huang SC, Henze E, Selin CE, Schelbert HR, 1982. Positron tomography with deoxyglucose for estimating local myocardial glucose metabolism. J Nucl Med 23: 577–586.
  20. Law MP, Osman S, Pike VW, Davenport RJ, Cunningham VJ, Rimoldi O, Rhodes CG, Giardinà D, Camici PG, 2000. Evaluation of [11C]GB67, a novel radioligand for imaging myocardial alpha 1-adrenoceptors with positron emission tomography. Eur J Nucl Med 27: 7–17.
  21. Schäfers M, Dutka D, Rhodes CG, Lammertsma AA, Hermansen F, Schober O, Camici PG, 1998. Myocardial presynaptic and postsynaptic autonomic dysfunction in hypertrophic cardiomyopathy. Circ Res 82: 57–62.
  22. Rajappan K, Livieratos L, Camici PG, Pennell DJ, 2002. Measurement of ventricular volumes and function: a comparison of gated PET and cardiovascular magnetic resonance. J Nucl Med 43: 806–810.
  23. Boyd HL, Gunn RN, Marinho NV, Karwatowski SP, Bailey DL, Costa DC, Camici PG, 1996. Non-invasive measurement of left ventricular volumes and function by gated positron emission tomography. Eur J Nucl Med 23: 1594–1602.
  24. Chatziioannou AF, Cherry SR, Shao Y, Silverman RW, Meadors K, Farquhar TH, Pedarsani M, Phelps ME, 1999. Performance evaluation of microPET: a high-resolution lutetium oxyorthosilicate PET scanner for animal imaging. J Nucl Med 40: 1164–1175.
  25. Cherry SR, Shao Y, Silverman RW, Meadors K, Siegel S, Chatziioannou A, Young JW, Jones W, Moyers JC, Newport D, Boutefnouchet A, Farquhar TH, Andreaco M, Paulus MJ, Binkley DM, Nutt R, Phelps ME, 1997. MicroPET: a high resolution PET scanner for imaging small animals. IEEE Trans Nucl Sci 44: 1161–1166.
  26. Schiller NB, Shah PM, Crawford M, DeMaria A, Devereux R, Feigenbaum H, Gutgesell H, Reichek N, Sahn D, Schnittger I, 1989. Recommendations for quantitation of the left ventricle by two-dimensional echocardiography. American Society of Echocardiography Committee on Standards, Subcommittee on Quantitation of Two-Dimensional Echocardiograms. J Am Soc Echocardiogr 2: 358–367.
  27. Huang H, Chan J, Wittner M, Jelicks LA, Morris SA, Factor SM, Weiss LM, Braunstein VL, Bacchi CJ, Yarlett N, Chandra M, Shirani J, Tanowitz HB, 1999. Expression of cardiac cytokines and inducible form of nitric oxide synthase (NOS2) in Trypanosoma cruzi-infected mice. J Mol Cell Cardiol 31: 75–88.
  28. Cherry SR, Gambhir SS, 2001. Use of positron emission tomography in animal research. ILAR J 42: 219–232.
  29. De Souza AP, Tanowitz HB, Chandra M, Shtutin V, Weiss LM, Morris SA, Factor SM, Huang H, Wittner M, Shirani J, Jelicks LA, 2004. Effects of early and late verapamil administration on the development of cardiomyopathy in experimental chronic Trypanosoma cruzi (Brazil strain) infection. Parasitol Res 92: 496–501.
  30. Goldenberg RC, Jelicks LA, Fortes FS, Weiss LM, Rocha LL, Zhao D, Carvalho AC, Spray DC, Tanowitz HB, 2008. Bone marrow cell therapy ameliorates and reverses chagasic cardiomyopathy in a mouse model. J Infect Dis 197: 544–547.
  31. Hiller KH, Waller C, Haase A, Jakob PM, 2008. Magnetic resonance of mouse models of cardiac disease. Handb Exp Pharmacol 185: 245–257.
  32. Siri FM, Jelicks LA, Leinwand LA, Gardin JM, 1997. Gated magnetic resonance imaging of normal and hypertrophied murine hearts. Am J Physiol 272: H2394–H2402.
  33. Slawson SE, Roman BB, Williams DS, Koretsky AP, 1998. Cardiac MRI of the normal and hypertrophied mouse heart. Magn Reson Med 39: 980–987.
  34. Chandra M, Tanowitz HB, Petkova SB, Huang H, Weiss LM, Wittner M, Factor SM, Shtutin V, Jelicks LA, Chan J, Shirani J, 2002. Significance of inducible nitric oxide synthase in acute myocarditis caused by Trypanosoma cruzi (Tulahuen strain). Int J Parasitol 32: 897–905.
  35. Tanowitz HB, Huang H, Jelicks LA, Chandra M, Loredo ML, Weiss LM, Factor SM, Shtutin V, Mukherjee S, Kitsis RN, Christ GJ, Wittner M, Shirani J, Kisanuki YY, Yanagisawa M, 2005. Role of endothelin 1 in the pathogenesis of chronic chagasic heart disease. Infect Immun 73: 2496–2503.
  36. Rottman JN, Ni G, Brown M, 2007. Echocardiographic evaluation of ventricular function in mice. Echocardiography 24: 83–89.
  37. Scherrer-Crosbie M, 2006. Role of echocardiography in studies of murine models of cardiac diseases. Arch Mal Coeur Vaiss 99: 237–241.
  38. Litwin SE, Katz SE, Morgan JP, Douglas PS, 1994. Serial echocardiographic assessment of left ventricular geometry and function after large myocardial infarction in the rat. Circulation 89: 345–354.
  39. Tanaka N, Dalton N, Mao L, Rockman HA, Peterson KL, Gottshall KR, Hunter JJ, Chien KR, Ross J Jr, 1996. Transthoracic echocardiography in models of cardiac disease in the mouse. Circulation 94: 1109–1117.
  40. Coatney RW, 2001. Ultrasound imaging: principles and applications in rodent research. ILAR J 42: 233–247.
  41. Chapon C, Jackson JS, Aboagye EO, Herlihy AH, Jones WA, Bhakoo KK, 2009. An in vivo multimodal imaging study using MRI and PET of stem cell transplantation after myocardial infarction in rats. Mol Imaging Biol 11: 31–38.
  42. Gyöngyösi M, Blanco J, Marian T, Trón L, Petneházy O, Petrasi Z, Hemetsberger R, Rodriguez J, Font G, Pavo IJ, Kertész I, Balkay L, Pavo N, Posa A, Emri M, Galuska L, Kraitchman DL, Wojta J, Huber K, Glogar D, 2008. Serial noninvasive in vivo positron emission tomographic tracking of percutaneously intramyocardially injected autologous porcine mesenchymal stem cells modified for transgene reporter gene expression. Circ Cardiovas Imaging 1: 94–103.
  43. Handa N, Magata Y, Mukai T, Nishina T, Konishi J, Komeda M, 2007. Quantitative FDG-uptake by positron emission tomography in progressive hypertrophy of rat hearts in vivo. Ann Nucl Med 21: 569–576.
  44. Stegger L, Schäfers KP, Flögel U, Livieratos L, Hermann S, Jacoby C, Keul P, Conway EM, Schober O, Schrader J, Levkau B, Schäfers M, 2005. Monitoring left ventricular dilation in mice with PET. J Nucl Med 46: 1516–1521.
  45. Osman S, Danpure HJ, 1992. The use of 2-[18F]fluoro-2-deoxy-D-glucose as a potential in vitro agent for labelling human granulocytes for clinical studies by positron emission tomography. Int J Rad Appl Instrum B 19: 183–190.
  46. Kubota R, Yamada S, Kubota K, Ishiwata K, Tamahashi N, Ido T, 1992. Intra-tumoral distribution of fluorine-18-fluorodeoxyglu-cose in vivo: high accumulation in macrophages and granulocytes studied by microautoradiography. J Nucl Med 33: 1972–1980.
  47. Kubota R, Yamada S, Kubota K, Ishiwata K, Tamahashi N, Ido T, 1992. Auto-radiographic demonstration of 18F-FDG distribution within mouse FM3A tumour tissue in vivo. Kaku Igaku 29: 1215–1221.
  48. Godino C, Messa C, Gianolli L, Landoni C, Margonato A, Cera M, Stefano C, Cianflone D, Fazio F, Maseri A, 2008. Multifocal, persistent cardiac uptake of [18-f]-fluoro-deoxy-glucose detected by positron emission tomography in patients with acute myocardial infarction. Circ J 72: 1821–1828.
  49. Truijers M, Kurvers HA, Bredie SJ, Oyen WJ, Blankensteijn JD, 2008. In vivo imaging of abdominal aortic aneurysms: increased FDG uptake suggests inflammation in the aneurysm wall. J Endovasc Ther 15: 462–467.
  50. Rudd JH, Myers KS, Bansilal S, Machac J, Pinto CA, Tong C, Rafique A, Hargeaves R, Farkouh M, Fuster V, Fayad ZA, 2008. Atherosclerosis inflammation imaging with 18F-FDG PET: carotid, iliac, and femoral uptake reproducibility, quantification methods, and recommendations. J Nucl Med 49: 871–878.
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.2009.09-0338
Loading
/content/journals/10.4269/ajtmh.2009.09-0338
Loading

Data & Media loading...

Supplementary Data

Uninfected mouse

Infected mouse

  • Received : 18 Jun 2009
  • Accepted : 17 Jul 2009

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error