Top

Graefe's Archive for Clinical and Experimental Ophthalmology

Published in:

Open Access 24-10-2023 | Diabetic Retinopathy | Retinal Disorders

Relationship between nailfold capillaroscopy parameters and the severity of diabetic retinopathy

Authors: Tatsu Okabe, Hiroshi Kunikata, Masayuki Yasuda, Shinjiro Kodama, Yuta Maeda, Joe Nakano, Dan Takeno, Nobuo Fuse, Toru Nakazawa

Published in: Graefe's Archive for Clinical and Experimental Ophthalmology | Issue 3/2024

Abstract

Purpose

To determine whether non-invasive measurements of the nailfold capillaries (NCs) are associated with the presence and severity of diabetic retinopathy (DR) in patients with type 2 diabetes.

Methods

Eighty-three eyes of 83 patients with type 2 diabetes were enrolled. Sixty-three age-matched non-diabetic subjects served as controls. Diabetic patients were classified by the severity of their DR: non-DR (NDR), non-proliferative DR (NPDR), and proliferative DR (PDR). We used nailfold capillaroscopy to measure NC parameters, including number, length, width, and turbidity.

Results

Four NC parameters in the diabetic patients were significantly lower than in the controls (all P < 0.001). There was a statistically significant decrease in the NC parameters along with the increasing severity of DR (number: P = 0.02; all others: P < 0.001). Logistic regression analysis revealed that combining the systemic characteristics of age, sex, systolic blood pressure, estimated glomerular filtration rate, hemoglobin A1c level, and history of hypertension and dyslipidemia could indicate the presence of DR and PDR (the area under the receiver operating characteristic curve [AUC] = 0.81, P = 0.006; AUC = 0.87, P = 0.001, respectively). Furthermore, the discriminative power of DR was significantly improved (P = 0.03) by adding NC length to the systemic findings (AUC = 0.89, P < 0.001).

Conclusion

NC measurement is a simple and non-invasive way to assess the risk of DR and its severity.

Maldonado G, Guerrero R, Paredes C, Ríos C (2017) Nailfold capillaroscopy in diabetes mellitus. Microvasc Res 112:41–46. https://doi.org/10.1016/j.mvr.2017.03.001CrossRefPubMed

Carratù P, Nazzaro P, Portincasa P (2022) The crucial role of Nailfold capillaroscopy in obstructive sleep apnea syndrome. Microvasc Res 141:104335CrossRefPubMed

Arslan NG, Pancar GS (2021) Nailfold capillaroscopic changes of sleep apnea patients. Microvasc Res 137:104177.https://doi.org/10.1016/j.mvr.2021.104177CrossRefPubMed

Cousins CC, Alosco ML, Cousins HC et al (2018) Nailfold capillary morphology in alzheimer’s disease dementia. Journal of Alzheimer’s Disease 66:601–611. https://doi.org/10.3233/JAD-180658CrossRefPubMed

Ferri C, Pitaro N, Giuggioli D et al (1994) Nailfold capillary microscopy in lacunar infarction. Stroke 25:525–526. https://doi.org/10.1161/01.str.25.2.525CrossRefPubMed

Smith V, Herrick AL, Ingegnoli F et al (2020) Standardisation of nailfold capillaroscopy for the assessment of patients with Raynaud’s phenomenon and systemic sclerosis. Autoimmun Rev 19(3):102458CrossRefPubMed

Shikama M, Sonoda N, Morimoto A et al (2021) Association of crossing capillaries in the finger nailfold with diabetic retinopathy in type 2 diabetes mellitus. J Diabetes Investig 12:1007–1014. https://doi.org/10.1111/jdi.13444CrossRefPubMed

Uyar S, Balkarli A, Erol MK et al (2016) Assessment of the relationship between diabetic retinopathy and nailfold capillaries in type 2 diabetics with a noninvasive method: Nailfold videocapillaroscopy. J Diabetes Res 2016:7592402. https://doi.org/10.1155/2016/7592402CrossRefPubMedPubMedCentral

Abd EL-Khalik DM, Hafez EA, Hassan HE, et al (2022) Nail folds capillaries abnormalities associated with type 2 diabetes mellitus progression and correlation with diabetic retinopathy. Clin Med Insights Endocrinol Diabetes 15:11795514221122828. https://doi.org/10.1177/11795514221122828CrossRefPubMed

10.

Nakajima T, Nakano S, Kikuchi A, Matsunaga YT (2022) Nailfold capillary patterns correlate with age, gender, lifestyle habits, and fingertip temperature. PLoS One 17(6):e0269661. https://doi.org/10.1371/journal.pone.0269661CrossRefPubMedPubMedCentral

11.

Shoji MK, Cousins CC, Saini C, et al (2021) Paired optic nerve microvasculature and nailfold capillary measurements in primary open-angle glaucoma. Transl Vis Sci Technol 10(7):13. https://doi.org/10.1167/tvst.10.7.13

12.

Hammes H-P, Lin J, Renner O et al (2002) Pericytes and the pathogenesis of diabetic retinopathy. Diabetes 51:3107–3112. https://doi.org/10.2337/diabetes.51.10.3107CrossRefPubMed

13.

Beltramo E, Porta M (2013) Pericyte loss in diabetic retinopathy: mechanisms and consequences. Curr Med Chem 20:3218–3225. https://doi.org/10.2174/09298673113209990022CrossRefPubMed

14.

Warmke N, Griffin KJ, Cubbon RM (2016) Pericytes in diabetes-associated vascular disease. J Diabetes Complications 30:1643–1650. https://doi.org/10.1016/j.jdiacomp.2016.08.005CrossRefPubMed

15.

Spencer BG, Estevez JJ, Liu E et al (2020) Pericytes, inflammation, and diabetic retinopathy. Inflammopharmacology 28:697–709. https://doi.org/10.1007/s10787-019-00647-9CrossRefPubMed

16.

Yang J, Liu Z (2022) Mechanistic pathogenesis of endothelial dysfunction in diabetic nephropathy and retinopathy. Front Endocrinol (Lausanne) 13:816400CrossRefPubMed

17.

Huang H (2020) Pericyte-endothelial interactions in the retinal microvasculature. Int J Mol Sci 21:1–18CrossRef

18.

Gui F, You Z, Fu S et al (2020) Endothelial dysfunction in diabetic retinopathy. Front Endocrinol (Lausanne) 11:591CrossRefPubMed

19.

Cyr AR, Huckaby LV, Shiva SS, Zuckerbraun BS (2020) Nitric oxide and endothelial dysfunction. Crit Care Clin 36:307–321CrossRefPubMedPubMedCentral

20.

Toda N, Nakanishi-Toda M (2007) Nitric oxide: ocular blood flow, glaucoma, and diabetic retinopathy. Prog Retin Eye Res 26:205–238CrossRefPubMed

21.

Kowluru RA, Atasi L, Ho YS (2006) Role of mitochondrial superoxide dismutase in the development of diabetic retinopathy. Invest Ophthalmol Vis Sci 47:1594–1599. https://doi.org/10.1167/iovs.05-1276CrossRefPubMed

22.

Vancheeswaran R, Magoulas T, Efrat G et al (1994) Circulating endothelin-1 levels in systemic sclerosis subsets–a marker of fibrosis or vascular dysfunction? J Rheumatol 21:1838–1844PubMed

23.

Manetti M, Allanore Y, Saad M et al (2012) Evidence for caveolin-1 as a new susceptibility gene regulating tissue fibrosis in systemic sclerosis. Ann Rheum Dis 71:1034–1041. https://doi.org/10.1136/annrheumdis-2011-200986CrossRefPubMed

24.

Sambataro D, Sambataro G, Zaccara E et al (2014) Nailfold videocapillaroscopy micro-haemorrhage and giant capillary counting as an accurate approach for a steady state definition of disease activity in systemic sclerosis. Arthritis Res Ther 16(5):462. https://doi.org/10.1186/s13075-014-0462-8CrossRefPubMedPubMedCentral

25.

Yasuda M, Shimura M, Kunikata H et al (2015) Relationship of skin autofluorescence to severity of retinopathy in type 2 diabetes. Curr Eye Res 40:338–345. https://doi.org/10.3109/02713683.2014.918152CrossRefPubMed

26.

Zhang Y-F, Wei W, Li L et al (2015) Sirt1 and HMGB1 regulate the AGE-induced pro-inflammatory cytokines in human retinal cells. Clin Lab 61:999–1008. https://doi.org/10.7754/clin.lab.2015.150141CrossRefPubMed

27.

Li L, Zhang H-N, Chen H-Z et al (2011) SIRT1 acts as a modulator of neointima formation following vascular injury in mice. Circ Res 108:1180–1189. https://doi.org/10.1161/CIRCRESAHA.110.237875CrossRefPubMed

28.

Ma S, Motevalli SM, Chen J et al (2018) Precise theranostic nanomedicines for inhibiting vulnerable atherosclerotic plaque progression through regulation of vascular smooth muscle cell phenotype switching. Theranostics 8:3693–3706. https://doi.org/10.7150/thno.24364CrossRefPubMedPubMedCentral

29.

Dou Y-Q, Kong P, Li C-L et al (2020) Smooth muscle SIRT1 reprograms endothelial cells to suppress angiogenesis after ischemia. Theranostics 10:1197–1212. https://doi.org/10.7150/thno.39320CrossRefPubMedPubMedCentral

30.

Aldámiz-Echevarría L, Andrade F (2012) Asymmetric dimethylarginine, endothelial dysfunction and renal disease. Int J Mol Sci 13:11288–11311CrossRefPubMedPubMedCentral

31.

Ahmed Aziz KM (2018) Association of diabetic retinopathy and maculopathy with elevated HbA1c, blood pressure, serum creatinine, microalbuminuria, spot urine protein, nephropathy and diabetic kidney disease an experience from data analysis of 10,580 diabetic patients. J Endocrinol Diabetes 5:1–11. https://doi.org/10.15226/2374-6890/5/1/00195CrossRef

32.

Wang X, Zhang M, Li T et al (2022) Effect of urinary albumin creatinine ratio on type 2 diabetic retinopathy and is cut-off value for early diabetic retinopathy diagnosis. Prim Care Diabetes 16:698–702. https://doi.org/10.1016/j.pcd.2022.08.002CrossRefPubMed

33.

Li T, Wu Y (2022) Correlation of glucose and lipid metabolism levels and serum uric acid levels with diabetic retinopathy in type 2 diabetic mellitus patients. Emerg Med Int 2022:1–7. https://doi.org/10.1155/2022/9201566CrossRef

34.

Shan Y, Wang Q, Zhang Y et al (2022) High remnant cholesterol level is relevant to diabetic retinopathy in type 2 diabetes mellitus. Lipids Health Dis 21(1):12. https://doi.org/10.1186/s12944-021-01621-7CrossRefPubMedPubMedCentral

35.

Tanaka K, Tani Y, Asai J et al (2012) Skin autofluorescence is associated with severity of vascular complications in Japanese patients with Type2 diabetes. Diabet Med 29:492–500. https://doi.org/10.1111/j.1464-5491.2011.03448.xCrossRefPubMed

36.

Monnier VM, Bautista O, Kenny D et al (1999) Skin collagen glycation, glycoxidation, and crosslinking are lower in subjects with long-term intensive versus conventional therapy of Type 1 diabetes: relevance of glycated collagen products versus HbA 1c as markers of diabetic complications. DCCT Skin Collagen Ancillary Study Group. Diabetes Control and Complications Trial. Diabetes 48(4):870–80CrossRefPubMed

37.

Ichinohasama K, Kunikata H, Ito A et al (2019) The relationship between carotid intima-media thickness and ocular circulation in type-2 diabetes. J Ophthalmol 2019:3421305. https://doi.org/10.1155/2019/3421305CrossRefPubMedPubMedCentral

38.

Eladawi N, Elmogy M, Khalifa F et al (2018) Early diabetic retinopathy diagnosis based on local retinal blood vessel analysis in optical coherence tomography angiography (OCTA) images. Med Phys 45:4582–4599. https://doi.org/10.1002/mp.13142CrossRefPubMed

39.

Cano J, O’neill WD, Penn RD et al (2020) Classification of advanced and early stages of diabetic retinopathy from non-diabetic subjects by an ordinary least squares modeling method applied to OCTA images. Biomed Opt Express 11:4666. https://doi.org/10.1364/boe.394472CrossRefPubMedPubMedCentral

Title: Relationship between nailfold capillaroscopy parameters and the severity of diabetic retinopathy
Authors: Tatsu Okabe
Hiroshi Kunikata
Masayuki Yasuda
Shinjiro Kodama
Yuta Maeda
Joe Nakano
Dan Takeno
Nobuo Fuse
Toru Nakazawa
Publication date: 24-10-2023
Publisher: Springer Berlin Heidelberg
Keywords: Diabetic Retinopathy
Diabetic Retinopathy
Dyslipidemia
Hypertension
Hypertension
Published in: Graefe's Archive for Clinical and Experimental Ophthalmology / Issue 3/2024
Print ISSN: 0721-832X
Electronic ISSN: 1435-702X
DOI: https://doi.org/10.1007/s00417-023-06220-z

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Relationship between nailfold capillaroscopy parameters and the severity of diabetic retinopathy

Abstract

Purpose

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 3/2024

Intraocular pressure spikes after gonioscopy-assisted transluminal trabeculotomy (GATT)

Proliferative vitreoretinopathy: an update on the current and emerging treatment options

Cataract surgery utilization in Parkinson’s disease: the english longitudinal survey on ageing

SGLT2 inhibitors and diabetic retinopathy progression

Graefe’s archive for clinical and experimental surgery—170th anniversary

Associations of quantitative contrast sensitivity with wide-field swept-source optical coherence tomography angiography in retinal vein occlusion