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Decreased retinal–choroidal blood flow in retinitis pigmentosa as measured by MRI

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Abstract

Purpose

To evaluate retinal and choroidal blood flow (BF) using high-resolution magnetic resonance imaging (MRI) as well as visual function measured by the electroretinogram (ERG) in patients with retinitis pigmentosa (RP).

Methods

MRI studies were performed in 6 RP patients (29–67 years) and 5 healthy volunteers (29–64 years) on a 3-Tesla scanner with a custom-made surface coil. Quantitative BF was measured using the pseudo-continuous arterial spin-labeling technique at 0.5 × 0.8 × 6.0 mm. Full-field ERGs of all patients were recorded. Amplitudes and implicit times of standard ERGs were analyzed.

Results

Basal BF in the posterior retinal-choroid was 142 ± 16 ml/100ml/min (or 1.14 ± 0.13 μl/mm2/min) in the control group and was 70 ±19 ml/100ml/min (or 0.56 ± 0.15 μl/mm2/min) in the RP group. Retinal–choroidal BF was significantly reduced by 52 ± 8 % in RP patients compared to controls (P<0.05). ERG a- and b-wave amplitudes of RP patients were reduced, and b-wave implicit times were delayed. There were statistically significant correlations between a-wave amplitude and BF value (r=0.9, P<0.05) but not between b-wave amplitude and BF value (r =0.7, P=0.2).

Conclusions

This study demonstrates a novel non-invasive MRI approach to measure quantitative retinal and choroidal BF in RP patients. We found that retinal–choroidal BF was markedly reduced and significantly correlated with reduced amplitudes of the a-wave of the standard combined ERG.

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References

  1. Hartong DT, Berson EL, Dryja TP (2006) Retinitis pigmentosa. Lancet 368:1795–1809

    Article  PubMed  CAS  Google Scholar 

  2. Vámos R, Tátrai E, Németh J, Holder GE, DeBuc DC, Somfai GM (2011) The structure and function of the macula in patients with advanced retinitis pigmentosa. Invest Ophthalmol Vis Sci 52:8425–8432

    Article  PubMed  Google Scholar 

  3. Gundogan F, Tas A, Sobaci G (2011) Electroretinogram in hereditary retinal disorders. In: Belusic G (ed) Electroretinograms. doi:10.5772/21704

  4. Berson EL, Rosner B, Sandberg MA, Hayes KC, Nicholson BW, Weigel-DiFranco C, Willett W (1993) A randomized trial of vitamin A and vitamin E supplementation for retinitis pigmentosa. Arch Ophthalmol 111:761–772

    Article  PubMed  CAS  Google Scholar 

  5. Herscovitch P, Markham J, Raichle ME (1983) Brain blood flow measured with intravenous H2(15)O. I. Theory and error analysis. J Nucl Med 24:782–789

    PubMed  CAS  Google Scholar 

  6. Machida S, Kondo M, Jamison JA, Khan NW, Kononen LT, Sugawara T, Bush RA, Sieving PA (2000) P23H rhodopsin transgenic rat: correlation of retinal function with histopathology. Invest Ophthalmol Vis Sci 41:3200–3209

    PubMed  CAS  Google Scholar 

  7. Wang R, Jiang C, Ma J, Young MJ (2012) Monitoring morphological changes in the retina of rhodopsin −/− mice with spectral domain optical coherence tomography. Invest Ophthalmol Vis Sci 53:3967–3972

    Article  PubMed  CAS  Google Scholar 

  8. Marc RE, Jones BW, Watt CB, Strettoi E (2003) Neural remodeling in retinal degeneration. Prog Retin Eye Res 22:607–655

    Article  PubMed  Google Scholar 

  9. Ma Y, Kawasaki R, Dobson LP, Ruddle JB, Kearns LS, Wong TY, Mackey DA (2012) Quantitative analysis of retinal vessel attenuation in eyes with retinitis pigmentosa. Invest Ophthalmol Vis Sci 53:4306–4314

    Article  PubMed  Google Scholar 

  10. Merin S, Auerbach E (1976) Retinitis pigmentosa. Surv Ophthalmol 20:303–346

    Article  PubMed  CAS  Google Scholar 

  11. Grunwald JE, Maguire AM, Dupont J (1996) Retinal hemodynamics in retinitis pigmentosa. Am J Ophthalmol 122:502–508

    PubMed  CAS  Google Scholar 

  12. Akyol N, Kukner S, Celiker U, Koyu H, Luleci C (1995) Decreased retinal blood flow in retinitis pigmentosa. Can J Ophthalmol 30:28–32

    PubMed  CAS  Google Scholar 

  13. Beutelspacher S, Serbecic N, Barash H, Burgansky-Eliash Z, Grinvald A, Krastel H, Jonas J (2011) Retinal blood flow velocity measured by retinal function imaging in retinitis pigmentosa. Graefes Arch Clin Exp Ophthalmol 249:1855–1858

    Article  PubMed  Google Scholar 

  14. Best M, Galin MA, Blumenthal M, Toyofuku H (1971) Fluorescein angiography during induced ocular hypertension in retinitis pigmentosa. Am J Ophthalmol 71:1226–1230

    PubMed  CAS  Google Scholar 

  15. Best M, Toyofuku H, Galin MA (1972) Ocular hemodynamics in retinitis pigmentosa. Arch Ophthalmol 88:123–130

    Article  PubMed  CAS  Google Scholar 

  16. Falsini B, Anselmi GM, Marangoni D, D’Esposito F, Fadda A, Di Renzo A, Campos EC, Riva CE (2011) Subfoveal choroidal blood flow and central retinal function in retinitis pigmentosa. Invest Ophthalmol Vis Sci 52:1064

    Article  PubMed  Google Scholar 

  17. Langham ME, Kramer T (1990) Decreased choroidal blood flow associated with retinitis pigmentosa. Eye (Lond) 4(Pt 2):374–381

    Article  Google Scholar 

  18. Schmidt KG, Pillunat LE, Kohler K, Flammer J (2001) Ocular pulse amplitude is reduced in patients with advanced retinitis pigmentosa. Br J Ophthalmol 85:678–682

    Article  PubMed  CAS  Google Scholar 

  19. Maleki N, Dai W, Alsop DC (2011) Blood flow quantification of the human retina with MRI. NMR Biomed 24:104–111

    Article  PubMed  Google Scholar 

  20. Peng Q, Zhang Y, Nateras OS, van Osch MJ, Duong TQ (2011) MRI of blood flow of the human retina. Magn Reson Med 65:1768–1775

    Article  PubMed  Google Scholar 

  21. Zhang Y, Nateras OSE, Peng Q, Rosende CA, Duong TQ (2012) Blood flow MRI of the human retina/choroid during rest and isometric exercise. Invest Ophthalmol Vis Sci 53:4299–4305

    Article  PubMed  Google Scholar 

  22. Potsidis E, Berson EL, Sandberg MA (2011) Disease course of patients with unilateral pigmentary retinopathy. Invest Ophthalmol Vis Sci 52:9244–9249

    Article  PubMed  Google Scholar 

  23. Zhang Y, Peng Q, Kiel JW, Rosende CA, Duong TQ (2011) Magnetic resonance imaging of vascular oxygenation changes during hyperoxia and carbogen challenges in the human retina. Invest Ophthalmol Vis Sci 52:286–291

    Article  PubMed  Google Scholar 

  24. Zhang Y, Nateras OS, Peng Q, Kuranov RV, Harrison JM, Milner TE, Duong TQ (2011) Lamina-specific anatomic magnetic resonance imaging of the human retina. Invest Ophthalmol Vis Sci 52:7232–7237

    Article  PubMed  Google Scholar 

  25. Chalela JA, Alsop DC, Gonzalez-Atavales JB, Maldjian JA, Kasner SE, Detre JA (2000) Magnetic resonance perfusion imaging in acute ischemic stroke using continuous arterial spin labeling. Stroke 31:680–687

    Article  PubMed  CAS  Google Scholar 

  26. Herscovitch P, Raichle ME (1985) What is the correct value for the brain–blood partition coefficient for water? J Cereb Blood Flow Metab 5:65–69

    Article  PubMed  CAS  Google Scholar 

  27. Lu H, Clingman C, Golay X, van Zijl PC (2004) Determining the longitudinal relaxation time (T1) of blood at 3.0 Tesla. Magn Reson Med 52:679–682

    Article  PubMed  Google Scholar 

  28. Stanisz GJ, Odrobina EE, Pun J, Escaravage M, Graham SJ, Bronskill MJ, Henkelman RM (2005) T1, T2 relaxation and magnetization transfer in tissue at 3T. Magn Reson Med 54:507–512

    Article  PubMed  Google Scholar 

  29. Wu WC, Fernandez-Seara M, Detre JA, Wehrli FW, Wang J (2007) A theoretical and experimental investigation of the tagging efficiency of pseudocontinuous arterial spin labeling. Magn Reson Med 58:1020–1027

    Article  PubMed  Google Scholar 

  30. Garcia DM, Duhamel G, Alsop DC (2005) Efficiency of inversion pulses for background suppressed arterial spin labeling. Magn Reson Med 54:366–372

    Article  PubMed  Google Scholar 

  31. Cheng H, Nair G, Walker TA, Kim MK, Pardue MT, Thule PM, Olson DE, Duong TQ (2006) Structural and functional MRI reveals multiple retinal layers. Proc Natl Acad Sci U S A 103:17525–17530

    Article  PubMed  CAS  Google Scholar 

  32. Marmor M, Fulton A, Holder G, Miyake Y, Brigell M, Bach M (2009) ISCEV standard for full-field clinical electroretinography (2008 update). Doc Ophthalmol 118:69–77

    Article  PubMed  CAS  Google Scholar 

  33. Bill A (1984) Circulation in the eye. In: Renkin EM, Michel CC (eds) Handbook of Physiology: Cardiovascular. American Physiological Society, Bethesda

    Google Scholar 

  34. Duong TQ, Pardue MT, Thule PM, Olson DE, Cheng H, Nair G, Li Y, Kim M, Zhang X, Shen Q (2008) Layer-specific anatomical, physiological and functional MRI of the retina. NMR Biomed 21:978–996

    Article  PubMed  Google Scholar 

  35. Duong TQ, Muir ER (2009) Magnetic resonance imaging of the retina. Jpn J Ophthalmol 53:352–367

    Article  PubMed  Google Scholar 

  36. Li Y, Cheng H, Shen Q, Kim M, Thule PM, Olson DE, Pardue MT, Duong TQ (2009) Blood flow magnetic resonance imaging of retinal degeneration. Invest Ophthalmol Vis Sci 50:1824

    Article  PubMed  Google Scholar 

  37. Muir ER, De La Garza B, Duong TQ (2013) Blood flow and anatomical MRI in a mouse model of retinitis pigmentosa. Magn Reson Med 69:221–228

    Google Scholar 

  38. Neuhardt T, May CA, Wilsch C, Eichhorn M, Lutjen-Drecoll E (1999) Morphological changes of retinal pigment epithelium and choroid in rd-mice. Exp Eye Res 68:75–83

    Article  PubMed  CAS  Google Scholar 

  39. Flannery JG, Farber D, Bird AC, Bok D (1989) Degenerative changes in a retina affected with autosomal dominant retinitis pigmentosa. Invest Ophthalmol Vis Sci 30:191–211

    PubMed  CAS  Google Scholar 

  40. Nilsson SFE, Mäepea O, Alm A, Narfström K (2001) Ocular blood flow and retinal metabolism in Abyssinian cats with hereditary retinal degeneration. Invest Ophthalmol Vis Sci 42:1038–1044

    PubMed  CAS  Google Scholar 

  41. May CA, Narfstrom K (2008) Choroidal microcirculation in Abyssinian cats with hereditary rod-cone degeneration. Exp Eye Res 86:537–540

    Article  PubMed  CAS  Google Scholar 

  42. Ben-Zion I, Harris A, Weizman Y, Ehrlich R, Rechtman E (2008) An updated review of methods for human retinal oximetry measurements and current applications. Harefuah 147(812–817):836

    Google Scholar 

  43. Harris A, Dinn RB, Kagemann L, Rechtman E (2003) A review of methods for human retinal oximetry. Ophthalmic Surg Lasers Imag 34:152–164

    Google Scholar 

  44. Jacobson SG, Roman AJ, Aleman TS, Sumaroka A, Herrera W, Windsor EA, Atkinson LA, Schwartz SB, Steinberg JD, Cideciyan AV (2010) Normal central retinal function and structure preserved in retinitis pigmentosa. Invest Ophthalmol Vis Sci 51:1079–1085

    Article  PubMed  Google Scholar 

  45. Shen Q, Cheng H, Pardue MT, Chang TF, Nair G, Vo VT, Shonat RD, Duong TQ (2006) Magnetic resonance imaging of tissue and vascular layers in the cat retina. J Magn Reson Imag 23:465–472

    Article  Google Scholar 

  46. De La Garza BH, Muir ER, Shih YY, Duong TQ (2012) 3D magnetic resonance microscopy of the ex vivo retina. Magn Reson Med 67:1154–1158

  47. Chen J, Wang Q, Zhang H, Yang X, Wang J, Berkowitz BA, Wickline SA, Song SK (2008) In vivo quantification of T(1), T(2), and apparent diffusion coefficient in the mouse retina at 11.74T. Magn Reson Med 59:731–738

    Article  PubMed  Google Scholar 

  48. Muir ER, Duong TQ (2011) Layer-specific functional and anatomical MRI of the retina with passband balanced SSFP. Magn Reson Med 66:1416–1421

    Article  PubMed  Google Scholar 

  49. Berkowitz BA, Roberts R, Luan H, Bissig D, Bui BV, Gradianu M, Calkins DJ, Vingrys AJ (2007) Manganese-enhanced MRI studies of alterations of intraretinal ion demand in models of ocular injury. Invest Ophthalmol Vis Sci 48:3796–3804

    Article  PubMed  Google Scholar 

  50. De La Garza BH, Li G, Shih YY, Duong TQ (2012) Layer-specific manganese-enhanced MRI of the retina in light and dark adaptation. Invest Ophthalmol Vis Sci 53:4352–4358

    Article  Google Scholar 

  51. Nair G, Kim M, Pardue MT, Duong TQ (2011) Manganese-enhanced MRI reveals multiple cellular and vascular layers. J Magn Reson Imag 34:1422–1429

    Article  Google Scholar 

  52. Chan KC, Fan SJ, Zhou IY, Wu EX (2012) In vivo chromium-enhanced MRI of the retina. Magn Reson Med 68:1202–1210

    Article  PubMed  CAS  Google Scholar 

  53. Shih YY, Muir ER, Li G, De La Garza BH, Duong TQ (2012) High-resolution 3D MR microangiography of the rat ocular circulation. Radiology 264:234–241

    Article  PubMed  Google Scholar 

  54. Duong TQ, Ngan S-C, Ugurbil K, Kim S-G (2002) Functional magnetic resonance imaging of the retina. Invest Ophthalmol Vis Sci 43:1176–1181

    PubMed  Google Scholar 

  55. De La Garza BH, Muir ER, Li G, Shih YY, Duong TQ (2011) Blood oxygenation level-dependent (BOLD) functional MRI of visual stimulation in the rat retina at 11.7 T. NMR Biomed 24:188–193

    Article  Google Scholar 

  56. Nair G, Tanaka Y, Kim M, Olson DE, Thule PM, Pardue MT, Duong TQ (2011) MRI reveals differential regulation of retinal and choroidal blood volumes in rat retina. Neuroimage 54:1063–1069

    Article  PubMed  Google Scholar 

  57. Shih YY, De la Garza BH, Muir ER, Rogers WE, Harrison JM, Kiel JW, Duong TQ (2011) Lamina-specific functional MRI of retinal and choroidal responses to visual stimuli. Invest Ophthalmol Vis Sci 52:5303–5310

    Article  PubMed  Google Scholar 

  58. Bissig D, Berkowitz BA (2011) Same-session functional assessment of rat retina and brain with manganese-enhanced MRI. Neuroimage 58:749–760

    Article  PubMed  Google Scholar 

  59. Bissig D, Berkowitz BA (2012) Light-dependent changes in outer retinal water diffusion in rats in vivo. Mol Vis 18:2561–2577

    PubMed  Google Scholar 

  60. Li G, De La Garza B, Shih YY, Muir ER, Duong TQ (2012) Layer-specific blood-flow MRI of retinitis pigmentosa in RCS rats. Exp Eye Res 101:90–96

    Google Scholar 

  61. Nair G, Shen Q, Duong TQ (2010) Relaxation time constants and apparent diffusion coefficients of rat retina at 7 tesla. Int J Imag Syst Tech 20:126–130

    Google Scholar 

  62. Zhang Y, Wey HY, Nateras OS, Peng Q, De La Garza BH, Duong TQ (2011) Anatomical, blood oxygenation level-dependent, and blood flow MRI of nonhuman primate (baboon) retina. Magn Reson Med 66:546–554

    Google Scholar 

  63. Nair G, Pardue MT, Kim M, Duong TQ (2011) Manganese-enhanced MRI reveals multiple cellular and vascular layers in normal and degenerated retinas. J Magn Reson Imag 34:1422–1429

    Google Scholar 

  64. Shih YY, Li G, Muir ER, De La Garza BH, Kiel JW, Duong TQ (2012) Pharmacological MRI of the choroid and retina: blood flow and BOLD responses during nitroprusside infusion. Magn Reson Med 68:1273–1278

    Google Scholar 

  65. Lavery WJ, Muir ER, Kiel JW, Duong TQ (2012) Magnetic resonance imaging indicates decreased choroidal and retinal blood flow in the DBA/2J mouse model of glaucoma. Invest Ophthalmol Vis Sci 53:560–564

    Google Scholar 

  66. Muir ER, Renteria RC, Duong TQ (2012) Reduced ocular blood flow as an early indicator of diabetic retinopathy in a mouse model of diabetes. Invest Ophthalmol Vis Sci 53:6488–6494.

    Google Scholar 

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Acknowledgments

This work was supported by a Clinical Translational Science Award Pilot Grant and a Translational Technology Resource grant (parent grant UL1TR000149), NIH/NEI (R01 EY014211 and EY018855), and Department of Veterans Affairs MERIT awards to TQD. YZ was supported by a Translational Science Training award through the University of Texas System Graduate Program Initiative.

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Authors and Affiliations

  1. Research Imaging Institute, University of Texas Health Science Center, 8403 Floyd Curl Dr, San Antonio, TX, 78229, USA

    Yi Zhang & Timothy Q. Duong

  2. Department of Ophthalmology, University of Texas Health Science Center, San Antonio, TX, USA

    Joseph M. Harrison, Steven Chalfin & Timothy Q. Duong

  3. Department of Radiology, University of Texas Health Science Center, San Antonio, TX, USA

    Yi Zhang, Oscar San Emeterio Nateras & Timothy Q. Duong

  4. Department of Physiology, University of Texas Health Science Center, San Antonio, TX, USA

    Timothy Q. Duong

  5. South Texas Veterans Health Care System, San Antonio, TX, USA

    Timothy Q. Duong

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  1. Yi Zhang
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Correspondence to Timothy Q. Duong.

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Zhang, Y., Harrison, J.M., Nateras, O.S.E. et al. Decreased retinal–choroidal blood flow in retinitis pigmentosa as measured by MRI. Doc Ophthalmol 126, 187–197 (2013). https://doi.org/10.1007/s10633-013-9374-1

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  • DOI: https://doi.org/10.1007/s10633-013-9374-1

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