Layer-specific blood-flow MRI of retinitis pigmentosa in RCS rats

Experimental Eye Research

Volumn 101, Issue , 2012, Pages 90-96

  Li, Guang ^a   De La Garza, Bryan ^a   Shih, Yen Yu I ^a,c   Muir, Eric R ^a   Duong, Timothy Q ^a,b  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b SOUTH TEXAS VETERANS HEALTH CARE SYSTEM   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Arterial spin labeling; Blood flow; Choroid; Retina; Retinal degeneration; Retinitis pigmentosa

Indexed keywords

ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOROID; CONTROLLED STUDY; DISEASE COURSE; HISTOPATHOLOGY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; RETINA BLOOD FLOW; RETINA DEGENERATION; RETINITIS PIGMENTOSA;

ANIMALS; BLOOD FLOW VELOCITY; CHOROID; DISEASE MODELS, ANIMAL; MAGNETIC RESONANCE IMAGING; RATS; RATS, LONG-EVANS; RATS, MUTANT STRAINS; REGIONAL BLOOD FLOW; RETINAL VESSELS; RETINITIS PIGMENTOSA;

EID: 84864302474     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2012.06.006     Document Type: Article

References (58)

1. Akyol N., Kukner S., Celiker U., Koyu H., Luleci C. Decreased retinal blood flow in retinitis pigmentosa. Can. J. Ophthalmol. 1995, 30:28-32.
2. Aleman T.S., Cideciyan A.V., Sumaroka A., Windsor E.A.M., Herrera W., White D.A., Kaushal S., Naidu A., Roman A.J., Schwartz S.B., Stone E.M., Jacobson S.G. Retinal laminar architecture in human retinitis pigmentosa caused by rhodopsin gene mutations. Invest. Ophthalmol. Vis. Sci. 2008, 49:1580-1590.
3. Baris Toprak A., Ozbilgin K., Toprak V., Tuglu I., Guler C. A histological analysis of the protective effect of ischemic preconditioning in the rat retina. Curr. Eye Res. 2002, 24:234-239.
4. Berkowitz B.A., Roberts R., Goebel D.J., Luan H. Noninvasive and simultaneous imaging of layer-specific retinal functional adaptation by manganese-enhanced MRI. Invest. Ophthalmol. Vis. Sci. 2006, 47:2668-2674.
5. Berkowitz B.A., Gradianu M., Schafer S., Jin Y., Porchia A., Iezzi R., Roberts R. Ionic dysregulatory phenotyping of pathologic retinal thinning with manganese-enhanced MRI. Invest. Ophthalmol. Vis. Sci. 2008, 49:3178-3184.
6. Bill A., Sperber G.O. Control of retinal and choroidal blood flow. Eye 1990, 4:319-325.
7. Blanks J.C., Johnson L.V. Vascular atrophy in the retinal degenerative rd mouse. J. Comp. Neurol. 1986, 254:543-553.
8. Boughman J.A., Conneally P.M., Nance W.E. Population genetic studies of retinitis pigmentosa. Am. J. Hum. Genet. 1980, 32:223-235.
9. Chang B., Hawes N.L., Pardue M.T., German A.M., Hurd R.E., Davisson M.T., Nusinowitz S., Rengarajan K., Boyd A.P., Sidney S.S., Phillips M.J., Stewart R.E., Chaudhury R., Nickerson J.M., Heckenlively J.R., Boatright J.H. Two mouse retinal degenerations caused by missense mutations in the beta-subunit of rod cGMP phosphodiesterase gene. Vision. Res. 2007, 47:624-633.
10. Chen J., Wang Q., Zhang J., Yang X., Wang J., Berkowitz B.A., Wickline S.A., Song S.K. In vivo quantification of T1, T2, and apparent diffusion coefficient in the mouse retina at 11.74T. Magn. Reson. Imaging 2008, 59:731-738.
11. Chen J., Wang Q., Chen S., Wickline S.A., Song S.K. In vivo diffusion tensor MRI of the mouse retina: a noninvasive visualization of tissue organization. NMR. Biomed. 2010.
12. Cheng H., Nair G., Walker T.A., Kim M.K., Pardue M.T., Thule P.M., Olson D.E., Duong T.Q. Structural and functional MRI reveals multiple retinal layers. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:17525-17530.
13. Cheng H., Duong T.Q. Simplified laser-speckle-imaging analysis method and its application to retinal blood flow imaging. Opt. Lett. 2007, 32:2188-2190.
14. Cioffi G., Granstam E., Alm A. Ocular Circulation 2003, Adler's Physiology of the Eye, 747-784 pp.
15. Detre J.A., Zhang W., Roberts D.A., Silva A.C., Williams D.S., Grandis D.J., Koretsky A.P., Leigh J.S. Tissue specific perfusion imaging using arterial spin labeling. NMR. Biomed. 1994, 7:75-82.
16. Dowling J.E., Sidman R.L. Inherited retinal dystrophy in the rat. J. Cell. Biochem. 1962, 14:73-109.
17. Gal A., Li Y., Thompson D.A., Weir J., Orth U., Jacobson S.G., Apfelstedt-Sylla E., Vollrath D. Mutations in MERTK, the human orthologue o the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat. Genet. 2000, 26:270-271.
18. Grunwald J.E., Maguire A.M., Brucker A.J., Dupont J.C., Riva C.E. Retinal blood-flow and its regulation in patients with retinitis-pigmentosa. Invest. Ophthalmol. Vis. Sci. 1995, 36:S1040.
19. Grunwald J.E., Maguire A.M., Dupont J. Retinal hemodynamics in retinitis pigmentosa. Am. J. Ophthalmol. 1996, 122:502-508.
20. Harris A., Kagemann L., Cioffi G.A. Assessment of human ocular hemodynamics. Surv. Ophthalmol. 1998, 42:509-533.
21. Herscovitch P., Raichle M.E. What is the correct value for the brain-blood partition coefficient for water?. J. Cereb. Blood Flow Metab. 1985, 5:65-69.
22. Jolly C., Jeanny J.C., Behar-Cohen F., Laugier P., Saied A. High-resolution ultrasonograophy of subretinal structure and assessment of retina degeneration in rat. Exp. Eye Res. 2005, 81:592-601.
23. Joly S., Pernet V., Dorfman A.L., Chemtob S., Lachapelle P. Light-induced retinopathy: comparing adult and juvenile rats. Invest. Ophthalmol. Vis. Sci. 2006, 47:3202-3212.
24. Kiel J.W. Choroidal myogenic autoregulation and intraocular pressure. Exp. Eye Res. 1994, 58:529-543.
25. Kiel J.W. The Ocular Circulation 2010, San Rafael (CA): Morgan & Claypool Life Sciences.
26. Langham M.E., Kramer T. Decreased choroidal blood flow associated with retinitis pigmentosa. Eye (Lond) 1990, 4(Pt 2):374-381.
27. Li Y., Cheng H., Shen Q., Kim M., Thule P.M., Olson D.E., Pardue M.T., Duong T.Q. Blood-flow magnetic resonance imaging of retinal degeneration. Invest. Ophthalmol. Vis. Sci. 2009, 50:1824-1830.
28. Matthes M.T., Bok D. Blood vascular abnormalities in the degenerative mouse retina (C57BL/6J-rd le). Invest. Ophthalmol. Vis. Sci. 1984, 25:364-369.
29. Muir E.R., Shen Q., Duong T.Q. Cerebral blood flow MRI in mice using the cardiac-spin-labeling technique. Magn. Reson. Med. 2008, 60:744-748.
30. Muir E.R., Duong T.Q. Layer-specific retinal and choroidal blood-flow MRI of retinitis pigmentosa in mice. Proc. Int. Soc. Magn. Reson. Med. 2011.
31. Muir E.R., Duong T.Q. MRI of retinal and choroidal blood flow with laminar resolution. NMR. Biomed. 2011, 24:216-223.
32. Muir, E.R., De La Garza, B., Duong, T.Q. Blood flow and anatomical MRI in a mouse model of retinitis pigmentosa. Magn. Reson. Med., doi:10.1002/mrm.24232.
33. Nair G., Pardue M.T., Kim M., Duong T.Q. Manganese-enhanced MRI reveals multiple cellular and vascular layers in normal and degenerated retinas. J. Magn. Reson. Imaging 2011, 34:1422-1429.
34. Nair G., Tanaka Y., Kim M., Olson D.E., Thule P.M., Pardue M.T., Duong T.Q. MRI reveals differential regulation of retinal and choroidal blood volumes in rat retina. Neuroimage 2011, 54:1063-1069.
35. Neuhardt T., May C.A., Wilsch C., Eichhorn M., Lutjen-Drecoll E. Morphological changes of retinal pigment epithelium and choroid in rd-mice. Exp. Eye Res. 1999, 68:75-83.
36. Nilsson S.F.E., Maepea O., Alm A., Narfstrom K. Ocular blood flow and retinal metabolism in Abyssinian cats with hereditary retinal degeneration. Invest. Ophthalmol. Vis. Sci. 2001, 42:1038-1044.
37. Padnick-Silver L., Kang Derwent J.J., Giuliano E., Narfstrom K., Linsenmeier R.A. Retinal oxygenation and oxygen metabolism in Abyssinian cats with a hereditary retinal degeneration. Invest. Ophthalmol. Vis. Sci. 2006, 47:3683-3689.
38. Penn J.S., Li S., Naash M.I. Ambient hypoxia reverses retinal vascular attenuation in a transgenic mouse model of autosomal dominant retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci. 2000, 41:4007-4013.
39. Pennesi M.E., Nishikawa S., Matthes M.T., Yasumura D., LaVail M.M. The relationship of photoreceptor degeneration to retinal vascular development and loss in mutant rhodopsin transgenic and RCS rats. Exp. Eye Res. 2008, 87:561-570.
40. Phelan J.K., Bok D. A brief review of retinitis pigmentosa and the identified retinitis pigmentosa genes. Mol. Vis. 2000, 6:116-124.
41. Pouliot M., Deschenes M.C., Hetu S., Chemtob S., Lesk M.R., Couture R., Vaucher E. Quantitative and regional measurement of retinal blood flow in rats using N-isopropyl-p-[C-14]-iodoamphetamine ([C-14]-IMP). Exp. Eye Res. 2009, 89:960-966.
42. Preussner P.R., Richard G., Darrelmann O., Weber J., Kreissig I. Quantitative measurement of retinal blood flow in human beings by application of digital image-processsing methods to television fluorescein angiograms. Graefes Arch. Clin. Exp. Ophthalmol. 1983, 221:110-112.
43. Riva C.E., Cranstoun S.D., Grunwald J.E., Petrig B.L. Choroidal blood flow in the foveal region of the human ocular fundus. Invest. Ophthalmol. Vis. Sci. 1994, 35:4273-4281.
44. Roth S. The effects of halothane on retinal and choroidal blood flow in cats. Anesthesiology 1992, 76:455-460.
45. Sarunic M.V., Yazdanpanah A., Gibson E., Xu J., Bai Y.J., Lee S., Saragovi H.U., Beg M.F. Longitudinal study of retinal degeneration in a rat using spectral domain optical coherence tomography. Opt. Express 2010, 18:23435-23441.
46. Satoh T., Yamaguchi K. Ocular fundus abnormalities detected by fluorescein and indocyanine green angiography in the Royal College of Surgeons dystrophic rat. Exp. Anim. 2000, 49:275-280.
47. Shen Q., Ren H., Cheng H., Fisher M., Duong T.Q. Functional, perfusion and diffusion MRI of acute focal ischemic brain injury. J. Cereb. Blood Flow Metab. 2005, 25:1265-1279.
48. Shen Q., Duong T.Q. Background suppression in arterial spin labeling MRI with a separate neck labeling coil. NMR. Biomed. 2011.
49. Sho K., Takahashi K., Fukuchi T., Matsumura M. Quantitative evaluation of ischemia-reperfusion injury by optical coherence tomography in the rat retina. Jpn. J. Ophthalmol. 2005, 49:109-113.
50. Sicard K.M., Duong T.Q. Effects of hypoxia, hyperoxia and hypercapnia on baseline and stimulus-evoked BOLD, CBF and CMRO2 in spontaneously breathing animals. Neuroimage 2005, 25:850-858.
51. Silva A.C., Zhang W., Williams D.S., Koretsky A.P. Multi-slice MRI of rat brain perfusion during amphetamine stimulation using arterial spin labeling. Magn. Reson. Med. 1995, 33:209-214.
52. Thomas B.B., Arai S., Ikai Y., Qiu G., Chen Z., Aramant R.B., Sadda S.R., Seiler M.J. Retinal transplants evaluated by optical coherence tomography in photoreceptor degenerate rats. J. Neurosci. Methods 2006, 151:186-193.
53. Tilton R.G., Chang K., Weigel C., Eades D., Sherman W.R., Kilo C., Williamson J.R. Increased ocular blood flow and 125I-albumin permeation in galactose-fed rats: inhibition by sorbinil. Invest. Ophthalmol. Vis. Sci. 1988, 29:861-868.
54. Tilton R.G., Chang K.C., LeJeune W.S., Stephan C.C., Brock T.A., Williamson J.R. Role for nitric oxide in the hyperpermeability and hemodynamic changes induced by intravenous VEGF. Invest. Ophthalmol. Vis. Sci. 1999, 40:689-696.
55. Wang Q., Song S.K., Zhang H., Berkowitz B.A., Chen S., Wickline S.A., Chen J. Photoreceptor degeneration changes magnetic resonance imaging features in a mouse model of retinitis pigmentosa. Magn. Reson. Med. 2011, 65:1793-1798.
56. Wang S., Villegas-Perez M., Holmes T., Lawrence J.M., Vidal-Sanz M., Hurtado-Montalban N., Lund R.D. Evolving neurovascular relationships in the RCS rat with age. Curr. Eye Res. 2003, 27:183-196.
57. Yu D.Y., Cringle S.J., Su E.N., Yu P.K. Intraretinal oxygen levels before and after photoreceptor loss in the RCS rat. Invest. Ophthalmol. Vis. Sci. 2000, 41:3999-4006.
58. Yu D.Y., Cringle S.J. Retinal degeneration and local oxygen metabolism. Exp. Eye Res. 2005, 80:745-751.