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Journal of Diabetes and Its Complications 33 (2019) 641–647

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Journal of Diabetes and Its Complications 33 (2019) 641–647 Journal of Diabetes and Its Complications 33 (2019) 641–647 Contents lists available at ScienceDirect Journal of Diabetes and Its Complications journal homepage: www.jdcjournal.com Retinal vessel reactivity is not attenuated in patients with type 2 diabetes compared with matched controls and is associated with peripheral endothelial function in controls Jonathan Mathias Baier a,⁎, Kristian Løkke Funck a,LinePetersenb, Liv Vernstrøm a, Søren T. Knudsen a, Toke Bek b, Per Løgstrup Poulsen a,EsbenLaugesena a Department of Internal Medicine and Endocrinology, Aarhus University Hospital, DK-8200, Denmark b Department of Ophthalmology, Aarhus University Hospital, DK-8200, Denmark article info abstract Article history: Background and aims: Attenuated retinal vasoreactivity in patients with type 2 diabetes preceding diabetic reti- Received 26 February 2019 nopathy development has been proposed to reflect local endothelial dysfunction. Received in revised form 22 May 2019 Whether retinal vessel reactivity is associated with peripheral endothelial dysfunction and large artery stiffness Accepted 27 May 2019 in patients with type 2 diabetes remains to be elucidated. Available online xxxx Methods: Twenty patients with type 2 diabetes without retinopathy and 20 sex- and age matched controls (dia- betes duration: 9.9 years (range 6.0;12.4), 40% male, age: 66.5 ± 7.3 (diabetes) and 65.2 ± 7.6 years (controls)) Keywords: were included. Endothelial function was assessed using EndoPAT. Arterial stiffness was assessed by carotid- Type 2 diabetes Endothelial dysfunction femoral pulse wave velocity using the SphygmoCor. Retinal blood supply regulation was examined by retinal ar- Diabetic retinopathy teriolar diameter change during 1) isometric exercise (hand-weight lifting), 2) exposure to flickering lights, and Arterial stiffness 3) a combined stimulus of 1) + 2) using the Dynamic Vessel Analyzer. Dynamic vessel analysis Results: No significant differences were observed in retinal vessel reactivity in T2DM patients compared to con- trols. Endothelial function was associated with mean arteriolar diameter change during only the combination in- tervention, (Beta = 0.033 [0.0013;0.064], p = 0.042) in the overall population of patients and controls. When groups were analyzed separately, the associations was statistically significant only in controls. However, formal test for interaction was not statistically significant, p = 0.40. No association was observed between pulse wave velocity and retinal arteriolar %-diameter change in patients or controls. Conclusion: Peripheral endothelial function was associated with retinal arteriolar diameter change in the com- bined sample. The association seemed to be driven primarily by the controls. Our findings indicate that peripheral endothelial function is reflective of endothelial function in the retina mainly in subjects without T2DM, whereas an association in T2DM without retinopathy was not observed. Further studies are needed in T2DM patients with more advanced retinopathy. © 2019 Elsevier Inc. All rights reserved. 1. Introduction The prevalence of type 2 diabetes (T2DM) is growing epidemically.1 Abbreviations: AU, Arbitrary units; cfPWV, Carotid-femoral pulse wave velocity; DR, Type 2 diabetes is associated with development of late complications in Diabetic retinopathy; DVA, Dynamic Vessel Analyzer; FMD, Flow-mediated dilation; both micro- and macrovascular beds. However, the pathogenic mecha- MAP, Mean arterial pressure; OCT, Optical coherence tomography; PAT, Peripheral arterial nisms underlying the development of complications are complex and it tonometry; RH, Reactive hyperaemia; RHI, Reactive hyperaemia index; T2DM, Type 2 dia- remains unsettled whether common disease mechanisms are involved betes mellitus; UACR, Urinary albumin:creatinine ratio. Declaration of competing interest: The authors declare that there is no duality of in- in both micro- and macrovascular complication development. A terest associated with this manuscript. number of recent studies found correlations between micro- and ⁎ Corresponding author at: Department of Endocrinology and Internal Medicine, Aar- macrovascular complications of diabetes, suggesting an interplay be- hus University Hospital, Palle Juul-Jensens Boulevard 99, DK-8200 Aarhus N, Denmark. tween the different vascular beds.2–5 E-mail addresses: [email protected] (J.M. Baier), [email protected] (K.L. Funck), Patients with type 2 diabetes and prediabetes have attenuated [email protected] (L. Petersen), [email protected] (L. Vernstrøm), [email protected] 6–10 (S.T. Knudsen), [email protected] (T. Bek), [email protected] (P.L. Poulsen), vasoreactivity of the retinal vessels. There is no generally accepted [email protected] (E. Laugesen). cut-off value for retinal vasoreactivity, however the retinal https://doi.org/10.1016/j.jdiacomp.2019.05.024 1056-8727/© 2019 Elsevier Inc. All rights reserved. 642 J.M. Baier et al. / Journal of Diabetes and Its Complications 33 (2019) 641–647 vasoreactivity was significantly reduced when compared with control examination and dynamic vessel analysis) on the same day. Participants subjects without diabetes. abstained from intake of any caffeinated beverages and tobacco usage This may reflect dysfunctional autoregulation of the retinal blood on the day of the examinations and were all fasting at least 3 h prior flow and has been suggested to play a role in the development of dia- to the examinations. They did, however, take their prescribed medicine betic retinopathy (DR).11Moreover, decreasing retinal arteriolar diame- as usually. ter has been associated with improvement of diabetic retinopath.12 As the retinal vessel response to diffuse luminance flicker light stim- 2.2. Patient characteristics ulation is at least in part mediated by nitric oxide,13 attenuated re- sponses have been proposed to reflect endothelial dysfunction in the At the 5-year follow-up, all participants underwent assessment of 8 retina. Similarly, type 2 diabetes has been associated with impaired pe- anthropometrics, HbA1C, plasma cholesterol, urinary albumin:creati- ripheral endothelial function,14 which has in turn been associated with nine ratio (UACR), 24-hour blood pressure monitoring, endothelial development of macrovascular complications.15 One study has found function, pulse wave velocity and eye examinations. These data were that flow-mediated dilation of the brachial artery (FMD) is correlated used for baseline characteristics in the present study. with retinal arteriolar diameter response to stimulation with flicker light in patients with hypertension and type 1 diabetes mellitus,16 sug- 2.3. Endothelial function gesting that peripheral endothelial dysfunction is associated with reti- nal vessel dysfunction. Endothelial function was assessed by peripheral arterial tonometry Large artery stiffness is an independent predictor of cardiovascular (PAT) during a reactive hyperaemia (RH) protocol using the EndoPAT mortality and increased aortic stiffness has been found to increase car- 2000 device (Itamar Medical Inc., Caesarea, Israel). The system consists diovascular mortality in patients with type 2 diabetes.17,18 Moreover, of a pneumatic plethysmograph in form of two inflatable digital probes large artery stiffness has also been associated with microvascular com- that detect pressure alterations in the finger probes induced by changes plications in patients with type 2 diabetes, including DR.2,4,19,20 in digital pulse wave amplitude. These digital probes are connected to Whether retinal vasoreactivity is associated with peripheral endo- an inflating device through pneumatic tubes and are controlled by a thelial dysfunction and large artery stiffness in patients with type 2 dia- computer. During the RH protocol, the digital probes were placed on betes remains to be elucidated. both index fingers and a blood pressure cuff (Hokanson SC-12, Bellevue, In the present study, we examined a group of well-regulated pa- WA, USA) was placed on the left upper arm; the right arm served as a tients with type 2 diabetes without retinopathy and a group of sex- control. The examination takes 15 min and was conducted with the sub- and age-matched controls to test the following hypothesis: ject in supine position. After five minutes of baseline measurements ar- Endothelial dysfunction and arterial stiffness are associated with terial blood flow in the left forearm was occluded by inflation of the cuff perturbations of the autoregulation of the retinal blood supply in pa- on the left upper arm to 200 mm Hg or systolic pressure plus 60 mm Hg tients with type 2 diabetes. (whichever was higher) for five minutes after which the measurements proceeded for five minutes. Endothelial function was evaluated via the 1.1. Subjects RH-index (RHI) calculated by the EndoPAT software. The RHI is a ratio of the PAT amplitude post-to-pre occlusion of the tested arm divided We included 20 patients with type 2 diabetes and 20 control subjects by the post-to-pre occlusion ratio of the control arm – a low RHI indi- matched on sex and age. All participants were recruited from an already cates reduced endothelial function. Data are presented as a natural log- established cohort that has been described in detail earlier.19 In brief, arithm of the measured RH-index, LnRHI, as data were skewed. 100 patients with type 2 diabetes were recruited from the outpatient clinic at Aarhus University Hospital, Aarhus, Denmark, while 100 sex- 2.4. Arterial stiffness and age-matched control subjects were recruited through advertise- ment
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