Relationship between retinal vessel tortuosity and oxygenation in sickle cell retinopathy
Tóm tắt
Reduced retinal vascular oxygen (O2) content causes tissue hypoxia and may lead to development of vision-threatening pathologies. Since increased vessel tortuosity is an early sign for some hypoxia-implicated retinopathies, we investigated a relationship between retinal vascular O2 content and vessel tortuosity indices. Dual wavelength retinal oximetry using a commercially available scanning laser ophthalmoscope was performed in both eyes of 12 healthy (NC) and 12 sickle cell retinopathy (SCR) subjects. Images were analyzed to quantify retinal arterial and venous O2 content and determine vessel tortuosity index (VTI) and vessel inflection index (VII) in circumpapillary regions. Linear mixed model analysis was used to determine the effect of disease on vascular O2 content, VTI and VII, and relate vascular O2 content with VTI and VII. Models accounted for vessel type, fellow eyes, age and mean arterial pressure. Retinal arterial and venous O2 content were lower in SCR (O2A = 11 ± 4 mLO2/dL, O2V = 7 ± 2 mLO2/dL) compared to NC (O2A = 18 ± 3 mLO2/dL, O2V = 13 ± 3 mLO2/dL) subjects (p < 0.001). As expected, O2 content was higher in arteries (15 ± 5 mLO2/dL) than veins (10 ± 4 mLO2/dL) (p < 0.001), but not different between eyes (OD: 12 ± 5 mLO2/dL; OS:13 ± 5 mLO2/dL) (p = 0.3). VTI was not significantly different between SCR (0.18 ± 0.07) and NC (0.15 ± 0.04) subjects, or between arteries (0.18 ± 0.07) and veins (0.16 ± 0.04), or between eyes (OD: 0.18 ± 0.07, OS:0.17 ± 0.05) (p ≥ 0.06). VII was significantly higher in SCR (10 ± 2) compared to NC subjects (8 ± 1) (p = 0.003). VII was also higher in veins (9 ± 2) compared to arteries (8 ± 5) (p = 0.04), but not different between eyes (OD: 9 ± 2; OS: 9 ± 2) (p = 0.2). There was an inverse linear relationship between vascular O2 (13 ± 5 mLO2/dL) content and VII (9 ± 2) (β = −0.5; p = 0.02). The findings augment knowledge of relationship between retinal vascular oxygenation and morphological changes and potentially contribute to identifying biomarkers for assessment of retinal hypoxia due to SCR and other retinopathies.
Tài liệu tham khảo
Saint-Geniez M, D’Amore PA. Development and pathology of the hyaloid, choroidal and retinal vasculature. Int J Dev Biol. 2004;48:1045–58. https://doi.org/10.1387/ijdb.041895ms.
Welch RB, Goldberg MF. Sickle-cell hemoglobin and its relation to fundus abnormality. Arch Ophthalmol. 1966;75:353–62. https://doi.org/10.1001/archopht.1966.00970050355008.
Fadugbagbe AO, Gurgel RQ, Mendonça CQ, Cipolotti R, dos Santos AM, Cuevas LE. Ocular manifestations of sickle cell disease. Ann Trop Paediatr. 2010;30:19–26. https://doi.org/10.1179/146532810X12637745451870.
Shahidi M, Felder AE, Tan O, Blair NP, Huang D. Retinal oxygen delivery and metabolism in healthy and sickle cell retinopathy subjects. Investig Ophthalmol Vis Sci. 2018;59:1905–9. https://doi.org/10.1167/iovs.17-23647.
Siqueira RC, Costa RA, Scott IU, Cintra LP, Jorge R. Intravitreal bevacizumab (Avastin) injection associated with regression of retinal neovascularization caused by sickle cell retinopathy. Acta Ophthalmol Scand. 2006;84:834–5. https://doi.org/10.1111/j.1600-0420.2006.00779.x.
Khansari MM, O’Neill W, Lim J, Shahidi M. Method for quantitative assessment of retinal vessel tortuosity in optical coherence tomography angiography applied to sickle cell retinopathy. Biomed Opt Express. 2017;8:3796. https://doi.org/10.1364/BOE.8.003796.
Alam M, Thapa D, Lim JI, Cao D, Yao X. Quantitative characteristics of sickle cell retinopathy in optical coherence tomography angiography. Biomed Opt Express. 2017;8:1741. https://doi.org/10.1364/BOE.8.001741.
Khansari MM, Garvey SL, Farzad S, Shahidi M. Relationship between retinal vessel tortuosity and oxygenation in normal control and sickle cell retinopathy subjects. Invest Ophthalmol Vis Sci. 2018;59:4651.
Bracher D. Changes in peripapillary tortuosity of the central retinal arteries in newborns—a phenomenon whose underlying mechanisms need clarification. Graefe’s Arch Clin Exp Ophthalmol. 1982;218:211–7. https://doi.org/10.1007/BF02150097.
Sasongko MBB, Wong TYY, Nguyen TTT, Cheung CYY, Shaw JEE, Wang JJ. Retinal vascular tortuosity in persons with diabetes and diabetic retinopathy. Diabetologia. 2011;54:2409–16. https://doi.org/10.1007/s00125-011-2200-y.
Hughes AD, Martinez-Perez E, Jabbar AS, Hassan A, Witt NW, Mistry PD, et al. Quantification of topological changes in retinal vascular architecture in essential and malignant hypertension. J Hypertens. 2006;24:889–94. https://doi.org/10.1097/01.hjh.0000222759.61735.98.
Gelman R, Martinez-Perez ME, Vanderveen DK, Moskowitz A, Fulton AB. Diagnosis of plus disease in retinopathy of prematurity using retinal image multiScale analysis. Investig Ophthalmol Vis Sci. 2005;46:4734–8. https://doi.org/10.1167/iovs.05-0646.
Scott A, Powner MB, Fruttiger M. Quantification of vascular tortuosity as an early outcome measure in oxygen induced retinopathy (OIR). Exp Eye Res. 2014;120:55–60. https://doi.org/10.1016/j.exer.2013.12.020.
Blair NP, Wanek J, Felder AE, Joslin CE, Kresovich JK, Lim JI, et al. Retinal oximetry and vessel diameter measurements with a commercially available scanning laser ophthalmoscope in diabetic retinopathy. Investig Ophthalmol Vis Sci. 2017;58:5556–63. https://doi.org/10.1167/iovs.17-21934.
Lisowska A, Annunziata R, Loh GK, Karl D, Trucco E. An experimental assessment of five indices of retinal vessel tortuosity with the RET-TORT public dataset. 2014 36th Annu Int Conf IEEE Eng Med Biol Soc EMBC 2014. https://doi.org/10.1109/embc.2014.6944850.
Ye DH, Kwon D, Yun ID, Lee SU. Fast multiscale vessel enhancement filtering. Proc SPIE. 2008;6914:691423. https://doi.org/10.1117/12.770038.
Beach JM, Schwenzer KJ, Srinivas S, Kim D, Tiedeman JS. Oximetry of retinal vessels by dual-wavelength imaging: calibration and influence of pigmentation. J Appl Physiol. 1999;86:748–58. https://doi.org/10.1016/j.jacr.2010.07.010.
Trucco E, Azegrouz H, Dhillon B. Modeling the tortuosity of retinal vessels: does caliber play a role? IEEE Trans Biomed Eng. 2010;57:2239–47. https://doi.org/10.1109/TBME.2010.2050771.
Bribiesca E. A measure of tortuosity based on chain coding. Pattern Recognit. 2013;46:716–24. https://doi.org/10.1016/j.patcog.2012.09.017.
Bullitt E, Gerig G, Pizer SM, Lin W, Aylward SR. Measuring tortuosity of the intracerebral vasculature from MRA images. IEEE Trans Med Imaging. 2003;22:1163–71. https://doi.org/10.1109/TMI.2003.816964.
Annunziata R, Kheirkhah A, Aggarwal S, Hamrah P, Trucco E. A fully automated tortuosity quantification system with application to corneal nerve fibres in confocal microscopy images. Med Image Anal. 2016. https://doi.org/10.1016/j.media.2016.04.006.
Werkmeister RM, Schmidl D, Aschinger G, Doblhoff-Dier V, Palkovits S, Wirth M, et al. Retinal oxygen extraction in humans. Sci Rep. 2015. https://doi.org/10.1038/srep15763.
Minvielle W, Caillaux V, Cohen SY, Chasset F, Zambrowski O, Miere A, et al. Macular microangiopathy in sickle cell disease using optical coherence tomography angiography. Am J Ophthalmol. 2016;164(137–144):e1. https://doi.org/10.1016/j.ajo.2015.12.023.
Han IC, Tadarati M, Scott AW. Macular vascular abnormalities identified by optical coherence tomographic angiography in patients with sickle cell disease. JAMA Ophthalmol. 2015;133:1337–40. https://doi.org/10.1001/jamaophthalmol.2015.2824.
Cogan DG, Kuwabara T, Friedman E. Retinal vasculature. Microvasc Res. 1968;1:115–32. https://doi.org/10.1016/0026-2862(68)90012-5.
Muraoka Y, Tsujikawa A, Murakami T, Ogino K, Kumagai K, Miyamoto K, et al. Morphologic and functional changes in retinal vessels associated with branch retinal vein occlusion. Ophthalmology. 2013;120:91–9. https://doi.org/10.1016/j.ophtha.2012.06.054.
Muraoka Y, Tsujikawa A, Kumagai K, Akagi-Kurashige Y, Ogino K, Murakami T, et al. Retinal vessel tortuosity associated with central retinal vein occlusion: an optical coherence tomography study. Invest Ophthalmol Vis Sci. 2014;55:134–41. https://doi.org/10.1167/iovs.13-13201.
Longmuir SQ, Mathews KD, Longmuir RA, Joshi V, Olson RJ, Abrmoff MD. Retinal arterial but not venous tortuosity correlates with facioscapulohumeral muscular dystrophy severity. J AAPOS. 2010;14:240–3. https://doi.org/10.1016/j.jaapos.2010.03.006.
Taylor AM, MacGillivray TJ, Henderson RD, Ilzina L, Dhillon B, Starr JM, et al. Retinal vascular fractal dimension, childhood IQ, and cognitive ability in old age: the Lothian birth cohort study 1936. PLoS One. 2015. https://doi.org/10.1371/journal.pone.0121119.
Hlastala MP. A model of fluctuating alveolar gas exchange during the respiratory cycle. Respir Physiol. 1972;15:214–32. https://doi.org/10.1016/0034-5687(72)90099-0.
Benitez-Aguirre P, Craig ME, Sasongko MB, Jenkins AJ, Wong TY, Wang JJ, et al. Retinal vascular geometry predicts incident retinopathy in young people with type 1 diabetes: a prospective cohort study from adolescence. Diab Care. 2011;34:1622–7. https://doi.org/10.2337/dc10-2419.
Abdu A, Gómez-Márquez J, Aldrich TK. The oxygen affinity of sickle hemoglobin. Respir Physiol Neurobiol. 2008;161:92–4. https://doi.org/10.1016/J.RESP.2007.12.005.
Ar A, Pc C, Fc C. Absorption spectra of normal adults and patients with sickle cell anaemia treated with hydrogen peroxide at two pH values. Adv Biores. 2013;5:129–35.
Nahavandi M, Nichols JP, Hassan M, Gandjbakhche A, Kato GJ. Near-infrared spectra absorbance of blood from sickle cell patients and normal individuals. Hematology. 2009;14:46–8. https://doi.org/10.1179/102453309x385133.
Elagouz M, Jyothi S, Gupta B, Sivaprasad S. Sickle cell disease and the eye: old and new concepts. Surv Ophthalmol. 2010. https://doi.org/10.1016/j.survophthal.2009.11.004.