Skip to main content
Erschienen in: Japanese Journal of Ophthalmology 1/2021

11.11.2020 | Clinical Investigation

Relationships between the vascular structure and neural function of the macula in patients with diabetes mellitus

verfasst von: Satoshi Ebihara, Shigeki Machida, Yuji Hara, Atsushi Tada, Masahiko Ishizuka, Mana Gonmori, Tomoharu Nishimura

Erschienen in: Japanese Journal of Ophthalmology | Ausgabe 1/2021

Einloggen, um Zugang zu erhalten

Abstract

Purpose

To determine the significance of the correlation between the vascular structure and neural function of the macula in patients with diabetes mellitus.

Study design

Single-center observational study.

Patients and methods

Ninety eyes of 90 diabetic patients with an average (SD) age of 63.5 (3.8) years were studied. Fifty of the eyes had no clinically apparent diabetic retinopathy (non-DR), and 40 eyes had mild-to-moderate nonproliferative DR (NPDR). Thirty age-matched healthy individuals were also studied in the same way. Swept-source optical coherence tomography angiography (OCTA) was performed to obtain 3 × 3-mm en face images of the posterior pole of the eye. The vascular densities (VDs) of the superficial capillary plexus (SCP) and the deep capillary plexus (DCP) were determined. The focal macular electroretinograms (ERGs) elicited by a 15° circular stimulus centered on the fovea were recorded. The amplitudes of the a- and b-waves, sum of the oscillatory potentials (ΣOPs), photopic negative response (PhNR), and implicit times of the individual OPs (OP1-OP3) were measured.

Results

The VDs of the SCP and DCP were reduced in eyes with advanced DR (P < .01 for SCP). The implicit times of OP1-OP3 were significantly prolonged in eyes with a lower VD of the SCP and DCP in the non-DR group (P < .05). The amplitudes of the ΣOPs were significantly smaller in eyes with a reduced VD of the SCP and DCP in the NPDR group (P < .05). The correlation coefficients were higher for the OP implicit times than for the ΣOP amplitudes in the non-DR group.

Conclusions

The OPs of the focal macular ERG are smaller with prolonged implicit times in association with capillary loss in the macula of diabetic patients. The implicit times are the most sensitive functional parameter that reflects the early changes of the microvasculature in the macula caused by diabetes.
Literatur
1.
Zurück zum Zitat Wong TY, Cheung CMG, Larsen M, Sharma S, Simó R. Diabetic retinopathy. Nat Rev Dis Primers. 2016;2:16012.CrossRef Wong TY, Cheung CMG, Larsen M, Sharma S, Simó R. Diabetic retinopathy. Nat Rev Dis Primers. 2016;2:16012.CrossRef
2.
Zurück zum Zitat Yonemura D, Aoki T, Tsuzuki K. Electroretinogram in diabetic retinopathy. Arch Ophthalmol. 1962;68:19–24.CrossRef Yonemura D, Aoki T, Tsuzuki K. Electroretinogram in diabetic retinopathy. Arch Ophthalmol. 1962;68:19–24.CrossRef
3.
Zurück zum Zitat Shirao Y, Kawasaki K. Electrical responses from diabetic retina. Prog Retin Eye Res. 1998;17:59–76.CrossRef Shirao Y, Kawasaki K. Electrical responses from diabetic retina. Prog Retin Eye Res. 1998;17:59–76.CrossRef
4.
Zurück zum Zitat Yonemura D, Tsuzuki K, Aoki T. Clinical importance of the oscillatory potential in the human ERG. Acta Ophthalmol. 1962;Suppl 70:115–23. Yonemura D, Tsuzuki K, Aoki T. Clinical importance of the oscillatory potential in the human ERG. Acta Ophthalmol. 1962;Suppl 70:115–23.
5.
Zurück zum Zitat Wachtmeister L. Oscillatory potentials in the retina: what do they reveal. Prog Retin Eye Res. 1998;17:485–521.CrossRef Wachtmeister L. Oscillatory potentials in the retina: what do they reveal. Prog Retin Eye Res. 1998;17:485–521.CrossRef
6.
Zurück zum Zitat Kawasaki K. Preretinopathic changes in the oscillatory potential in diabetic retina: interpretation and significance. Article in Japanese. Nippon Ganka Gakkai Zasshi. 1998;102:813–36.PubMed Kawasaki K. Preretinopathic changes in the oscillatory potential in diabetic retina: interpretation and significance. Article in Japanese. Nippon Ganka Gakkai Zasshi. 1998;102:813–36.PubMed
7.
Zurück zum Zitat Spaide RF, Fujimoto JG, Waheed NK, Sadda SR, Staurenghi G. Optical coherence tomography angiography. Prog Retin Eye Res. 2018;64:1–55.CrossRef Spaide RF, Fujimoto JG, Waheed NK, Sadda SR, Staurenghi G. Optical coherence tomography angiography. Prog Retin Eye Res. 2018;64:1–55.CrossRef
8.
Zurück zum Zitat Takase N, Nozaki M, Kato A, Ozeki H, Yoshida M, Ogura Y. Enlargement of foveal avascular zone in diabetic eyes evaluated by en face optical coherence tomography angiography. Retina. 2015;35:2377–83.CrossRef Takase N, Nozaki M, Kato A, Ozeki H, Yoshida M, Ogura Y. Enlargement of foveal avascular zone in diabetic eyes evaluated by en face optical coherence tomography angiography. Retina. 2015;35:2377–83.CrossRef
9.
Zurück zum Zitat Ishibazawa A, Nagaoka T, Takahashi A, Omae T, Tani T, Sogawa K, et al. Optical coherence tomography angiography in diabetic retinopathy: a prospective pilot study. Am J Ophthalmol. 2015;160:35–44.CrossRef Ishibazawa A, Nagaoka T, Takahashi A, Omae T, Tani T, Sogawa K, et al. Optical coherence tomography angiography in diabetic retinopathy: a prospective pilot study. Am J Ophthalmol. 2015;160:35–44.CrossRef
10.
Zurück zum Zitat Salz DA, de Carlo TE, Adhi M, Moult E, Choi W, Baumal CR, et al. Select features of diabetic retinopathy on swept-source optical coherence tomographic angiography compared with fluorescein angiography and normal eyes. JAMA Ophthalmol. 2016;34:644–50.CrossRef Salz DA, de Carlo TE, Adhi M, Moult E, Choi W, Baumal CR, et al. Select features of diabetic retinopathy on swept-source optical coherence tomographic angiography compared with fluorescein angiography and normal eyes. JAMA Ophthalmol. 2016;34:644–50.CrossRef
11.
Zurück zum Zitat Couturier A, Rey P-A, Erginay A, Lavia C, Bonnin S, Dupas B, et al. Widefield OCT-angiography and fluorescein angiography assessments of nonperfusion in diabetic retinopathy and edema treated with anti-vascular endothelial growth factor. Ophthalmology. 2019;126:1685–94.CrossRef Couturier A, Rey P-A, Erginay A, Lavia C, Bonnin S, Dupas B, et al. Widefield OCT-angiography and fluorescein angiography assessments of nonperfusion in diabetic retinopathy and edema treated with anti-vascular endothelial growth factor. Ophthalmology. 2019;126:1685–94.CrossRef
12.
Zurück zum Zitat Miyake Y, Yanagida K, Kondo K, Ota I. Subjective scotometry and recording of local electroretinogram and visual evoked response: system with television monitor of the fundus. Jpn J Ophthalmol. 1981;25:439–48. Miyake Y, Yanagida K, Kondo K, Ota I. Subjective scotometry and recording of local electroretinogram and visual evoked response: system with television monitor of the fundus. Jpn J Ophthalmol. 1981;25:439–48.
13.
Zurück zum Zitat Miyake Y. Studies on local macular ERG. Acta Soc Ophthalmol Jpn. 1988;92:1419–49. Miyake Y. Studies on local macular ERG. Acta Soc Ophthalmol Jpn. 1988;92:1419–49.
14.
Zurück zum Zitat Miyake Y. Macular oscillatory potentials in humans: macular OPs. Doc Ophthalmol. 1990;75:111–24.CrossRef Miyake Y. Macular oscillatory potentials in humans: macular OPs. Doc Ophthalmol. 1990;75:111–24.CrossRef
15.
Zurück zum Zitat Miyake Y, Shiroyama N, Horiguchi M, Ota I. Asymmetry of focal ERG in human macular region. Invest Ophthalmol Vis Sci. 1989;30:1743–9.PubMed Miyake Y, Shiroyama N, Horiguchi M, Ota I. Asymmetry of focal ERG in human macular region. Invest Ophthalmol Vis Sci. 1989;30:1743–9.PubMed
16.
Zurück zum Zitat Yoon IH, Shiroyama N, Miyake Y, Awaya S. Oscillatory potentials of local macular ERG in diabetic retinopathy. Korean J Ophthalmol. 1990;4:40–5.CrossRef Yoon IH, Shiroyama N, Miyake Y, Awaya S. Oscillatory potentials of local macular ERG in diabetic retinopathy. Korean J Ophthalmol. 1990;4:40–5.CrossRef
17.
Zurück zum Zitat Wilkinson CP, Ferris FL, Klein RE, Lee PP, Agardh CD, Davis M, et al. Proposed international diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003;110:1677–82.CrossRef Wilkinson CP, Ferris FL, Klein RE, Lee PP, Agardh CD, Davis M, et al. Proposed international diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003;110:1677–82.CrossRef
18.
Zurück zum Zitat Sawada O, Ichiyama Y, Obata S, Ito Y, Kakinoki M, Sawada T, et al. Comparison between wide-angle OCT angiography and ultra-wide field fluorescein angiography for detecting non-perfusion areas and retinal neovascularization in eyes with diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol. 2018;256:1275–80.CrossRef Sawada O, Ichiyama Y, Obata S, Ito Y, Kakinoki M, Sawada T, et al. Comparison between wide-angle OCT angiography and ultra-wide field fluorescein angiography for detecting non-perfusion areas and retinal neovascularization in eyes with diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol. 2018;256:1275–80.CrossRef
19.
Zurück zum Zitat Hirano T, Kakihara S, Toriyama Y, Nittala MG, Murata T, Sadda S. Wide-field en face swept-source optical coherence tomography angiography using extended field imaging in diabetic retinopathy. Br J Ophthalmol. 2018;102:1199–203.CrossRef Hirano T, Kakihara S, Toriyama Y, Nittala MG, Murata T, Sadda S. Wide-field en face swept-source optical coherence tomography angiography using extended field imaging in diabetic retinopathy. Br J Ophthalmol. 2018;102:1199–203.CrossRef
20.
Zurück zum Zitat Zeng Y, Cao D, Yu H, Yang D, Zhuang X, Hu Y, et al. Early retinal neurovascular impairment in patients with diabetes without clinically detectable retinopathy. Br J Ophthalmol. 2019;103:1747–52.PubMed Zeng Y, Cao D, Yu H, Yang D, Zhuang X, Hu Y, et al. Early retinal neurovascular impairment in patients with diabetes without clinically detectable retinopathy. Br J Ophthalmol. 2019;103:1747–52.PubMed
21.
Zurück zum Zitat Zeng Y, Cao D, Yang D, Zhuang X, Hu Y, He M, et al. Retinal vasculature-function correlation in non-proliferative diabetic retinopathy. Doc Ophthalmol. 2020;140:129–38.CrossRef Zeng Y, Cao D, Yang D, Zhuang X, Hu Y, He M, et al. Retinal vasculature-function correlation in non-proliferative diabetic retinopathy. Doc Ophthalmol. 2020;140:129–38.CrossRef
22.
Zurück zum Zitat Kondo M, Sieving PA. Primate photopic sine-wave flicker ERG: vector modeling analysis of component origins using glutamate analogs. Invest Ophthalmol Vis Sci. 2001;42:305–12.PubMed Kondo M, Sieving PA. Primate photopic sine-wave flicker ERG: vector modeling analysis of component origins using glutamate analogs. Invest Ophthalmol Vis Sci. 2001;42:305–12.PubMed
23.
Zurück zum Zitat Kondo M, Sieving PA. Post-photoreceptoral activity dominates primate photopic 32-Hz ERG for sine-, square-, and pulsed stimuli. Invest Ophthalmol Vis Sci. 2002;43:2500–7.PubMed Kondo M, Sieving PA. Post-photoreceptoral activity dominates primate photopic 32-Hz ERG for sine-, square-, and pulsed stimuli. Invest Ophthalmol Vis Sci. 2002;43:2500–7.PubMed
25.
Zurück zum Zitat Vujosevic S, Muraca A, Gatti V, Masoero L, Brambilla M, Cannillo B, et al. Peripapillary microvascular and neural changes in diabetes mellitus: an OCT-angiography study. Invest Ophthalmol Vis Sci. 2018;59:5074–81.CrossRef Vujosevic S, Muraca A, Gatti V, Masoero L, Brambilla M, Cannillo B, et al. Peripapillary microvascular and neural changes in diabetes mellitus: an OCT-angiography study. Invest Ophthalmol Vis Sci. 2018;59:5074–81.CrossRef
26.
Zurück zum Zitat Viswanathan S, Frishman LJ, Robson JG, Harwerth RS, Smith EL 3rd. The photopic negative response of the macaque electroretinogram: reduction by experimental glaucoma. Invest Ophthalmol Vis Sci. 1999;40:1124–36.PubMed Viswanathan S, Frishman LJ, Robson JG, Harwerth RS, Smith EL 3rd. The photopic negative response of the macaque electroretinogram: reduction by experimental glaucoma. Invest Ophthalmol Vis Sci. 1999;40:1124–36.PubMed
27.
Zurück zum Zitat Viswanathan S, Frishman LJ, Robson JG, Walter JW. The photopic negative response of the flash electroretinogram in primary open angle glaucoma. Invest Ophthalmol Vis Sci. 2001;42:514–22.PubMed Viswanathan S, Frishman LJ, Robson JG, Walter JW. The photopic negative response of the flash electroretinogram in primary open angle glaucoma. Invest Ophthalmol Vis Sci. 2001;42:514–22.PubMed
28.
Zurück zum Zitat Gotoh Y, Machida S, Tazawa Y. Selective loss of the photopic negative response in patients with optic nerve atrophy. Arch Ophthalmol. 2004;122:341–6.CrossRef Gotoh Y, Machida S, Tazawa Y. Selective loss of the photopic negative response in patients with optic nerve atrophy. Arch Ophthalmol. 2004;122:341–6.CrossRef
29.
Zurück zum Zitat Machida S, Gotoh Y, Toba Y, Ohtaki A, Kaneko M, Kurosaka D. Correlation between photopic negative response and retinal nerve fiber layer thickness and optic disc topography in glaucomatous eyes. Invest Ophthalmol Vis Sci. 2008;49:2201–7.CrossRef Machida S, Gotoh Y, Toba Y, Ohtaki A, Kaneko M, Kurosaka D. Correlation between photopic negative response and retinal nerve fiber layer thickness and optic disc topography in glaucomatous eyes. Invest Ophthalmol Vis Sci. 2008;49:2201–7.CrossRef
31.
Zurück zum Zitat Kondo M, Kurimoto Y, Sakai T, Koyasu T, Miyata K, Ueno S, et al. Recording focal macular photopic negative response (PhNR) from monkeys. Invest Ophthalmol Vis Sci. 2008;49:3544–50.CrossRef Kondo M, Kurimoto Y, Sakai T, Koyasu T, Miyata K, Ueno S, et al. Recording focal macular photopic negative response (PhNR) from monkeys. Invest Ophthalmol Vis Sci. 2008;49:3544–50.CrossRef
32.
Zurück zum Zitat Machida S, Toba Y, Ohtaki A, Gotoh Y, Kaneko M, Kurosaka D. Photopic negative response of focal electoretinograms in glaucomatous eyes. Invest Ophthalmol Vis Sci. 2008;49:5636–44.CrossRef Machida S, Toba Y, Ohtaki A, Gotoh Y, Kaneko M, Kurosaka D. Photopic negative response of focal electoretinograms in glaucomatous eyes. Invest Ophthalmol Vis Sci. 2008;49:5636–44.CrossRef
33.
Zurück zum Zitat Machida S, Tamada K, Oikawa T, Yokoyama D, Kaneko M, Kurosaka D. Sensitivity and specificity of photopic negative response of focal electroretinogram to detect glaucomatous eyes. Br J Ophthalmol. 2010;94:202–8.CrossRef Machida S, Tamada K, Oikawa T, Yokoyama D, Kaneko M, Kurosaka D. Sensitivity and specificity of photopic negative response of focal electroretinogram to detect glaucomatous eyes. Br J Ophthalmol. 2010;94:202–8.CrossRef
34.
Zurück zum Zitat Tamada K, Machida S, Yokoyama D, Kurosaka D. Photopic negative response of full-field and focal electroretinograms in patients with optic nerve atrophy. Jpn J Ophthalmol. 2009;53:608–14.CrossRef Tamada K, Machida S, Yokoyama D, Kurosaka D. Photopic negative response of full-field and focal electroretinograms in patients with optic nerve atrophy. Jpn J Ophthalmol. 2009;53:608–14.CrossRef
35.
Zurück zum Zitat Tamada K, Machida S, Oikawa T, Miyamoto H, Nishimura T, Kurosaka D. Correlation between photopic negative response of focal electroretinograms and local loss of retinal neurons in glaucoma. Curr Eye Res. 2010;35:155–64.CrossRef Tamada K, Machida S, Oikawa T, Miyamoto H, Nishimura T, Kurosaka D. Correlation between photopic negative response of focal electroretinograms and local loss of retinal neurons in glaucoma. Curr Eye Res. 2010;35:155–64.CrossRef
36.
Zurück zum Zitat Kizawa J, Machida S, Kobayashi T, Gotoh Y, Kurosaka D. Changes of oscillatory potentials and photopic negative response in patients with early diabetic retinopathy. Jpn J Ophthalmol. 2006;50:367–73.CrossRef Kizawa J, Machida S, Kobayashi T, Gotoh Y, Kurosaka D. Changes of oscillatory potentials and photopic negative response in patients with early diabetic retinopathy. Jpn J Ophthalmol. 2006;50:367–73.CrossRef
37.
Zurück zum Zitat Siliprandi R, Canella R, Carmignoto G, Schiavo N, Zanellato A, Zanoni R, et al. N-methyl-D-aspartate-induced neurotoxicity in the adult rat retina. Vis Neurosci. 1992;8:567–73.CrossRef Siliprandi R, Canella R, Carmignoto G, Schiavo N, Zanellato A, Zanoni R, et al. N-methyl-D-aspartate-induced neurotoxicity in the adult rat retina. Vis Neurosci. 1992;8:567–73.CrossRef
38.
Zurück zum Zitat Spix NJ, Liu LL, Zhang Z, Hohlbein JP, Prigge CL, Chintala S, et al. Vulnerability of dopaminergic amacrine cells to chronic ischemia in a mouse model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci. 2016;57:3047–57.CrossRef Spix NJ, Liu LL, Zhang Z, Hohlbein JP, Prigge CL, Chintala S, et al. Vulnerability of dopaminergic amacrine cells to chronic ischemia in a mouse model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci. 2016;57:3047–57.CrossRef
39.
Zurück zum Zitat Luu CD, Szental JA, Lee S, Lavanya R, Wong TY. Correlation between retinal oscillatory potentials and retinal vascular caliber in type 2 diabetes. Invest Ophthalmol Vis Sci. 2010;51:482–6.CrossRef Luu CD, Szental JA, Lee S, Lavanya R, Wong TY. Correlation between retinal oscillatory potentials and retinal vascular caliber in type 2 diabetes. Invest Ophthalmol Vis Sci. 2010;51:482–6.CrossRef
Metadaten
Titel
Relationships between the vascular structure and neural function of the macula in patients with diabetes mellitus
verfasst von
Satoshi Ebihara
Shigeki Machida
Yuji Hara
Atsushi Tada
Masahiko Ishizuka
Mana Gonmori
Tomoharu Nishimura
Publikationsdatum
11.11.2020
Verlag
Springer Japan
Erschienen in
Japanese Journal of Ophthalmology / Ausgabe 1/2021
Print ISSN: 0021-5155
Elektronische ISSN: 1613-2246
DOI
https://doi.org/10.1007/s10384-020-00784-7

Weitere Artikel der Ausgabe 1/2021

Japanese Journal of Ophthalmology 1/2021 Zur Ausgabe

Neu im Fachgebiet Augenheilkunde

Ophthalmika in der Schwangerschaft

Die Verwendung von Ophthalmika in der Schwangerschaft und Stillzeit stellt immer eine Off-label-Anwendung dar. Ein Einsatz von Arzneimitteln muss daher besonders sorgfältig auf sein Risiko-Nutzen-Verhältnis bewertet werden. In der vorliegenden …

Operative Therapie und Keimnachweis bei endogener Endophthalmitis

Vitrektomie Originalie

Die endogene Endophthalmitis ist eine hämatogen fortgeleitete, bakterielle oder fungale Infektion, die über choroidale oder retinale Gefäße in den Augapfel eingeschwemmt wird [ 1 – 3 ]. Von dort infiltrieren die Keime in die Netzhaut, den …

Bakterielle endogene Endophthalmitis

Vitrektomie Leitthema

Eine endogene Endophthalmitis stellt einen ophthalmologischen Notfall dar, der umgehender Diagnostik und Therapie bedarf. Es sollte mit geeigneten Methoden, wie beispielsweise dem Freiburger Endophthalmitis-Set, ein Keimnachweis erfolgen. Bei der …

So erreichen Sie eine bestmögliche Wundheilung der Kornea

Die bestmögliche Wundheilung der Kornea, insbesondere ohne die Ausbildung von lichtstreuenden Narben, ist oberstes Gebot, um einer dauerhaften Schädigung der Hornhaut frühzeitig entgegenzuwirken und die Funktion des Auges zu erhalten.   

Update Augenheilkunde

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.