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Do angiographic data support a detailed classification of hypertensive fundus changes?

Abstract

The eye is a target organ as well as an established prognostic indicator of arterial hypertension. Based on the ophthalmoscopically visible alterations, several classifications, the majority of them grading hypertensive fundus changes into four stages, have been suggested. Moreover, assessment of hypertensive alterations of the perivoveal microcirculation has become possible by means of fluorescein angiography. However, it has not yet been evaluated whether an angiographic equivalent for the ophthalmoscopic classifications exists. We therefore compared the perifoveal microcirculation of hypertensive patients who were staged according to the classification of Neubauer, a modification of the classification of Keith and Wagener, among each other and with that of normal subjects. According to Neubauer, who distinguishes between fundus hypertonicus (stages I–II) and hypertensive retinopathy (stages III–IV), we divided the patients (n = 143) into four groups: stage I (n = 49), stage II (n = 72), stage III (n = 16), and stage IV (n = 6). All patients underwent fluorescein angiography performed with a scanning laser ophthalmoscope. By means of digital image analysis we quantified the following parameters: (1) perifoveal intercapillary area (PIA), (2) the area of the foveal avascular zone (FAZ), and (3) capillary blood velocity (CBV). All patients with arterial hypertension demonstrated a rarefaction of the perifoveal capillary bed and a decrease of capillary blood velocity as compared with normal subjects. Significant changes of PIA (P < 0.05) and CBV (P < 0.05) were seen between mild (I–II) and severe stages (III–IV) of hypertensive retinopathy, but neither between stages I and II nor between stages III and IV. Our findings indicate significant angiographic differences between mild and severe form of hypertensive retinopathy, however, unlike in ophthalmoscopy, a differentiated division into four stages is not possible.

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References

  1. Kannel WB . Fifty years of Framingham Study contributions to understanding hypertension J Hum Hypertens 2000; 14: 83–90

    Article  CAS  PubMed  Google Scholar 

  2. Walsh JB . Hypertensive retinopathy. Description, classification, and prognosis Ophthalmology 1982; 89: 1127–1131

    Article  CAS  PubMed  Google Scholar 

  3. Rath EZ, Frank RN, Shin DH, Kim C . Risk factors for retinal vein occlusions. A case-control study Ophthalmology 1992; 99: 509–514

    Article  CAS  PubMed  Google Scholar 

  4. Klein R, Klein BE, Moss SE . The relation of systemic hypertension to changes in the retinal vasculature: the Beaver Dam Eye Study Trans Am Ophthalmol Soc 1997; 95: 329–348

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Wolf S et al. Retinal hemodynamics inpatients with chronic open-angel glaucoma Ger J Ophthalmol 1995; 4: 279–282

    CAS  PubMed  Google Scholar 

  6. Arend O, Ruffer M, Remky A . Macular circulation inpatients with diabetes mellitus with and without arterial hypertension Br J Ophthalmol 2000; 84: 1392–1396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Wolf S et al. Quantification of retinal capillary density and flow velocity inpatients with essential hypertension Hypertension 1994; 23: 464–467

    Article  CAS  PubMed  Google Scholar 

  8. Neubauer H . Augenhintergrundsbefunde bei arterieller Hypertension? Internist (Berl) 1974; 15: 485–496

    CAS  Google Scholar 

  9. Wolf S, Arend O, Reim M . Measurement of retinal hemodynamics with scanning laser ophthalmoscopy: reference values and variation Surv Ophthalmol 1994; 38: (Suppl): S95–S100

    Article  PubMed  Google Scholar 

  10. Wolf S et al. Retinal capillary blood flow measurement with a scanning laser ophthalmoscope. Preliminary results Ophthalmology 1991; 98: 996–1000

    Article  CAS  PubMed  Google Scholar 

  11. Arend O et al. Macular capillary particle velocities: a blue field and scanning laser comparison Graefes Arch Clin Exp Ophthalmol 1995; 233: 244–249

    Article  CAS  PubMed  Google Scholar 

  12. Littmann H . Zur Bestimmung der wahren Grö eines Objektes auf dem Hintergrund eines lebenden Auges Klin Mbl Augenheilk 1988; 192: 66–67

    Article  CAS  PubMed  Google Scholar 

  13. Holm S . A simple sequentially rejective multiple test procedure Scand J Statist 1979; 6: 65–70

    Google Scholar 

  14. Kagan A, Aureli E, Dobree J . A note on signs in the fundus oculi and arterial hypertension: conventional assessment and significance Bull World Health Organ 1966; 34: 955–960

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Wulle KG et al. Bedeutung der Fundus-Beurteilung bei der Stadieneinteilung der Hochdruck-Krankheit im Vergleich zum Elektrokardiogramm und zur Nierendurchblutung Klin Monatsbl Augenheilkd 1986; 189: 463–466

    Article  CAS  PubMed  Google Scholar 

  16. Palatini P et al. Role of ophthalmoscopy in arterial hypertension: a problem revisited Cardiologia 1991; 36: 713–722

    CAS  PubMed  Google Scholar 

  17. Lund OE . Fundus hypertonicus: Spiegel der Niere oder des Gehirns? MMW Munch Med Wochenschr 1974; 116: 613–616

    CAS  PubMed  Google Scholar 

  18. Kutschbach P et al. Einfluss unterschiedlicher antihypertensive Monotherapien auf die perifoveale Mikrozirkulation bei Patienten mit arterieller Hypertonie Ophthalmologe 1996; 93: 699–702

    Article  CAS  PubMed  Google Scholar 

  19. Remky A et al. Perifoveal capillary network inpatients with acute central retinal vein occlusion Ophthalmology 1997; 104: 33–37

    Article  CAS  PubMed  Google Scholar 

  20. Lafaut BA, De Vriese AS, Stulting AA . Fundus fluorescein angiography ofpatients with severe hypertensive nephropathy Graefes Arch Clin Exp Ophthalmol 1997; 235: 749–754

    Article  CAS  PubMed  Google Scholar 

  21. Spitzer S et al. Koinzidenz zwischen hypertensiven Augenhintergrundveränderungen und Regulationsstörungen der peripheren Mikrozirkulation: Teil I – Haut Klin Monatsbl Augenheilkd 1990; 196: 81–85

    Article  CAS  PubMed  Google Scholar 

  22. Kutschbach P et al. Retinal capillary density inpatients with arterial hypertension: 2-year follow-up Graefes Arch Clin Exp Ophthalmol 1998; 236: 410–414

    Article  CAS  PubMed  Google Scholar 

  23. Antonios TF et al. Structural skin capillary rarefaction in essential hypertension Hypertension 1999; 33: 998–1001

    Article  CAS  PubMed  Google Scholar 

  24. Prewitt RL, Chen II, Dowell R . Development of microvascular rarefaction in the spontaneously hypertensive rat Am J Physiol 1982; 243: H243–H251

    CAS  PubMed  Google Scholar 

  25. Hansen-Smith F, Greene AS, Cowley AW Jr, Lombard JH . Structural changes during microvascular rarefaction in chronic hypertension Hypertension 1990; 15: 922–928

    Article  CAS  PubMed  Google Scholar 

  26. Folkow B . Hypertensive structural changes in systemic precapillary resistance vessels: how important are they for in vivo haemodynamics? J Hypertens 1995; 13: 1546–1559

    CAS  PubMed  Google Scholar 

  27. Bhutto IA, Amemiya T . Vascular changes in retinas of spontaneously hypertensive rats demonstrated by corrosion casts Ophthalmic Res 1997; 29: 12–23

    Article  CAS  PubMed  Google Scholar 

  28. Wagener HPCG, Gipner JF . Classification of retinal lesions in the presence of vascular hypertension Trans Am Ophthalmol Soc 1947; 45: 47–73

    Google Scholar 

  29. Scheie HG . Evaluation of ophthalmoscopic changes of hypertension and arteriolar sclerosis Arch Ophthalmol 1953; 49: 117–118

    Article  CAS  Google Scholar 

  30. Leishman R . The eye in general vascular disease: hypertension and arteriosclerosis Br J Ophthalmol 1957; 41: 641–701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Keith NMWH, Barker NW . Some different types of essential hypertension: their course and prognosis Am J Med Sci 1939; 197: 332–343

    Article  Google Scholar 

  32. Fuchs FD et al. Study of the usefulness of optic fundi examination ofpatients with hypertension in a clinical setting J Hum Hypertens 1995; 9: 547–551

    CAS  PubMed  Google Scholar 

  33. Dimmitt SB et al. Usefulness of ophthalmoscopy in mild to moderate hypertension Lancet 1989; 1: 1103–1106

    Article  CAS  PubMed  Google Scholar 

  34. Schubert HD . Ocular manifestations of systemic hypertension Curr Opin Ophthalmol 1998; 9: 69–72

    Article  CAS  PubMed  Google Scholar 

  35. Dodson PM et al. Hypertensive retinopathy: a review of existing classification systems and a suggestion for a simplified grading system J Hum Hypertens 1996; 10: 93–98

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This investigation was supported by the Deutsche Forschungsgemeinschaft (DFG) grant Re 152/26–2 and Wo 478/8–3.

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Correspondence to M Pache.

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Pache, M., Kube, T., Wolf, S. et al. Do angiographic data support a detailed classification of hypertensive fundus changes?. J Hum Hypertens 16, 405–410 (2002). https://doi.org/10.1038/sj.jhh.1001402

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