Acute effects of coffee consumption on the microcirculation of macula and optic nerve head

doi:10.21203/rs.3.rs-1605732/v1

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Acute effects of coffee consumption on the microcirculation of macula and optic nerve head

https://doi.org/10.21203/rs.3.rs-1605732/v1

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Purpose: The aim of this study was to evaluate the acute changes in retinal vasculature following coffee consumption.

Methods: This is an interventional case series. The subjects were 22 healthy young adults. They were asked to rest in a silent room for 15 minutes; then, their heart rate (HR), blood pressure (BP), and arterial oxygen saturation pressure (spO2) were measured with a single patient monitoring system. OCT and OCT-A imaging of disc and macula were performed for both eyes of the subjects. These measurements were repeated 45 minutes after drinking a cup of 450 milliliters of coffee containing a standard dose of 130 milligrams of caffeine. Macular and optic nerve head neuro vasculature changes were assessed.

Results: The results of our study didn’t show a significant change in peripapillary retinal nerve fiber layer thickness and neural structural and vascular parameters of the optic nerve head. Although assessments of macular vasculature showed a significant decrement in superficial (p=0.01) and deep vessels density (p=0.05) at parafovea, vessel densities at the fovea and deep capillary plexus at perifovea showed no significant change.

Conclusion: Consuming one cup of coffee (150 mg caffeine) statistically changes central foveal thickness and parafoveal blood flow, but likely does not have a clinical impact in healthy young adults.

Coffee

Macula

Optic disc

Optical imaging

A wide variety of beverages including green tea, black tea, coffee, certain foods, and drugs contain caffeine. Several studies have investigated the vascular and hemodynamic effects of caffeine. Caffeine increases blood pressure acutely in about 15 to 90 minutes after consuming coffee, which persists for 3 to 4 hours.^1,2 This effect is assumed to be due to peripheral vascular stiffness.³ Both tachycardia and bradycardia can be seen in response to caffeine.⁴ Positron emission tomography (PET) has shown a 30% reduction in cerebral blood flow, 30 minutes after oral caffeine intake.⁵

The radial peripapillary capillaries (RPCs) form a special capillary plexus around the ONH which nourishes the more superficial portions of the peripapillary retinal nerve fiber layer (RNFL). They course straight along the RNFL up to 0.5 mm from ONH, lay relatively in the same depth in the retina during their path, rarely anastomose with each other, and are relatively uniform in diameter.^6–10 Macular vessel density (VD), foveal thickness and foveal avascular zone (FAZ) are other important factors that can be imaged and quantified precisely with OCT-A. Microvascular effects of caffeine on retinal or ONH blood flow if do occur, may be detected now thanks to this new technology. Any possible acute or chronic effect of coffee or other caffeine-containing drinks may have significant effects in eyes with compromised structural or microvascular status such as glaucoma or ischemic conditions.

In this study, we aimed to evaluate acute changes in OHN, peripapillary, and macular microvasculature changes after drinking coffee.

This is an interventional case series. It was approved by the institutional review board and ethics committee of the Mashhad University of Medical Sciences ( IR.MUMS.MEDICAL.REC.1397.592) and was designed and conducted in Khatam Eye Hospital. The study protocol adhered to the tenets of the Declaration of Helsinki. The subjects were 22 healthy young adults from the ophthalmology department staff who were not using any drugs at the time of the study. None of them drank coffee as an everyday routine. They were asked to rest in a silent room for 15 minutes; then, their heart rate (HR), blood pressure (BP), and arterial oxygen saturation pressure (spO2) were measured with a single patient monitoring system. OCT and OCT-A imaging of disc and macula were performed for both eyes of the subjects (AngioVue, Version 2017.1.0.151, Optovue, Fremont, CA, USA). After that, each participant drank a cup of 450 milliliters of coffee containing a standard dose of 130 milligrams of caffeine (Frappuccino, Starbucks, Seattle, Washington, US). By resting for another 45 minutes, HR, BP, and spO2 measurements were repeated with the same equipment. OCT and OCT-A measurements were repeated by the same operator and with the same device. All the measurements were performed between 8 to 10 a.m.

To detect the retinal vasculature, vertical and horizontal raster B-scans were done at the desired area. An area of 4.5 × 4.5 mm centered on the optic nerve head (ONH) which included the papillary and peripapillary regions and an area of 3.5 × 3.5 mm centered on the fovea were covered. To obtain the vascular density (VD) of the papillary area, the VD image was merged with the en face OCT image of the ONH region with the built-in software of the device, and the papillary VD was calculated automatically. For the peripapillary area VD measurement, two circles were centered on the center of the ONH on the en face OCT image by a trained operator, one at the margin of the disc and the other at a radius of 2.25 mm from the center of the disc (4.5 mm diameter). The doughnut-shaped area made between them was defined as the peripapillary area. RPC plexus density was measured both as a whole image (360 degrees around the ONH) and superior/inferior semicircles. Foveal VD was defined as the density of the superficial capillary plexus (internal limiting membrane to inner plexiform layer) in a 1mm diameter circle centered on the center of the fovea. Parafoveal VD was defined as the ring occupying the area between the foveal area and the 2.5 × 2.5 mm area centered on the foveal center. Perifoveal VD was defined as the outer ring between the outer border of parafovea and the 3.5 × 3.5 mm diameter on the foveal center. The measurement was performed at superior, inferior, nasal, and temporal quadrants. Retinal nerve fiber layer (RNFL) thickness was measured with the use of built-in software of the instrument- disc mode. To measure the foveal and parafoveal thickness, segmentation of the retinal layers was performed automatically by the instrument software. The inner limiting membrane (ILM) was determined as the inner border and the retinal pigment epithelium (RPE) was determined as the outer border. To measure foveal inner thickness, segmentation lines were automatically put on ILM as the inner border and the inner nuclear layer as the outer border. Vessel density (VD) was defined as the density of the vessels in a 3mm diameter circle centered on the fovea.

Statistical analysis

Statistical analysis was performed using the statistical software package (SPSS for Mac, version 19; IBM-SPSS, Chicago, IL). All the measured values were checked with the Kolmogorov-Smirnov test for normal distribution. Paired samples t-test was used to compare before and after coffee drinking measurements for variables with normal distribution. Wilcoxon signed ranks test was used for the variables with non-normal distribution. All the measurements are presented in mean ± standard deviation (SD).

The mean age ± SD of the 22 study participants was 34 ± 6.8 years. Nine individuals (40.9%) were female. There were no statistically significant difference in systolic and diastolic blood pressure and heart rate between men and women (P > 0.05). SpO2 was higher in females than males by 1.5% (98.9% vs 97.4%, respectively, P = 0.008).

Systemic measurements of participants before and after caffeine consumption are presented in Table 1. There was no significant difference between pre-and post-coffee consumption.

There was no statistically significant difference in the measured OCT and OCT-A values between the right eye and the left eye of any of the participants (t-test for parametric, and Mann Whitney for nonparametric variables, P > 0.05). Randomly, data of the right eye of all the individuals were chosen for analysis.

Table 1

Hemodynamics of participants at baseline and following coffee drinking
	Mean, Baseline	Mean, after coffee drinking	P-value
Systolic blood pressure (mmHg)	104.82	101.30	0.10
Diastolic blood pressure (mmHg)	72.91	71.25	0.42
Heart rate (bit/min)	79.83	82.75	0.24
O2 saturation (%)	98.13	97.16	0.20

Neural structural findings

Peripapillary RNFL thickness was decreased from 113.5 µm to 113.22 µm after coffee drinking; which was not statistically significant (t-test, p = 0.540) (Table 2). Also, foveal thickness showed an increment by about 1.36 micrometer- from 253.54µm to 254.90µm- after coffee drinking which was statistically significant (t-test, P = 0.000). Inner foveal thickness didn’t change significantly after coffee consumption (P = 0.803). Other neural structural assessments of macula and ONH including parafoveal full thickness and inner thickness, and RNFL thickness as a whole and by quadrants showed no significant change following coffee consumption (p > 0.05).

Table 2

Neural structural changes following coffee drinking.
Structural findings		Mean ± SD, baseline	Mean ± SD, after coffee drinking	Change from baseline	P-value
	Peripapillary RNFL thickness	113.50 ± 9.16	113.22 ± 9.02	− 0.28	0.540
	Foveal thickness	253.54 ± 17.31	254.90 ± 17.13	+ 1.36	0.000
	Inner Foveal thickness	50.90 ± 9.11	50.95 ± 9.00	+ 0.05	0.803

Macular vasculature

Macular superficial vessel density (MSVD) of the whole image was significantly decreased after coffee drinking (P = 0.005). Furthermore, decrement in MSVD at the parafoveal area was also statistically significant (P = 0.010). Similarly, changes in macular deep vessels density (MDVD) of the whole image and at the parafovea were statistically significant following coffee consumption (P = 0.03, and P = 0.05 respectively). Vascular parameter assessments at the fovea showed no significant change in MSVD (P = 0.66) and MDVD (P = 0.65) after coffee drinking. Although MSVD was significantly decreased at perifovea (P = 0.04), the decrement of MDVD was not significant (P = 0.79). Macular vascular changes following coffee drinking were summarized in Table 3.

Table 3

Macular vascular changes following coffee drinking
Macular vascular parameters	Mean ± SD, baseline	Mean ± SD, after coffee drinking	Change from baseline	P-value
MSVD- whole image	48.53 ± 2.89	47.28 ± 3.08	− 1.25	0.005
MSVD- superior hemi	48.43 ± 3.01	47.22 ± 3.15	− 1.21	0.015
MSVD- inferior hemi	48.61 ± 2.84	47.30 ± 3.09	− 1.31	0.002
MSVD- fovea	20.41 ± 5.85	20.26 ± 5.41	− 0.15	0.661
MSVD- parafovea	51.37 ± 3.19	50.20 ± 3.15	− 1.17	0.010
MSVD- parafovea superior hemi	51.19 ± 3.19	50.21 ± 3.18	− 0.98	0.065
MSVD- parafovea inferior hemi	51.54 ± 3.28	50.20 ± 3.27	− 1.34	0.002
MSVD- parafovea temporal quad	49.74 ± 3.14	48.57 ± 3.02	− 1.17	0.001
MSVD- parafovea superior quad	52.57 ± 3.74	51.45 ± 3.90	− 1.12	0.093
MSVD- parafovea nasal quad	50.53 ± 3.14	48.91 ± 3.39	− 1.62	0.013
MSVD- parafovea inferior quad	52.66 ± 3.44	51.97 ± 3.25	− 0.69	0.110
MDVD- whole image	53.21 ± 3.09	51.88 ± 3.89	− 1.33	0.034
MDVD- superior hemi	53.36 ± 3.32	51.85 ± 4.35	− 1.51	0.037
MDVD- inferior hemi	53.02 ± 2.91	51.90 ± 3.51	− 1.12	0.015
MDVD- fovea	37.30 ± 5.99	37.11 ± 5.24	− 0.19	0.658
MDVD- parafovea	54.95 ± 3.00	53.78 ± 3.86	− 1.17	0.054
MDVD- parafovea superior hemi	55.13 ± 3.14	53.72 ± 4.29	− 1.41	0.047
MDVD- parafovea inferior hemi	54.77 ± 2.95	53.82 ± 3.54	− 0.95	0.093
MDVD- parafovea temporal quad	55.13 ± 3.05	54.08 ± 3.80	− 1.05	0.053
MDVD- parafovea superior quad	54.85 ± 3.18	53.22 ± 4.73	− 1.63	0.047
MDVD- parafovea nasal quad	55.42 ± 2.92	54.26 ± 3.86	− 1.16	0.089
MDVD- parafovea inferior quad	54.35 ± 3.20	53.54 ± 3.75	− 0.81	0.190
MSVD- perifovea	55.59 ± 3.34	54.39 ± 3.61	− 1.2	0.047
MSVD- perifovea superior hemi	55.99 ± 3.48	55.0 ± 3.64	-0.99	0.119
MSVD- perifovea inferior hemi	55.18 ± 3.56	53.79 ± 3.79	− 1.39	0.029
MSVD- perifovea temporal quad	57.52 ± 4.10	56.18 ± 4.52	− 1.34	0.078
MSVD- perifovea superior quad	55.52 ± 3.52	54.78 ± 3.36	− 0.74	0.178
MSVD- perifovea nasal quad	53.30 ± 4.19	52.37 ± 3.97	− 0.93	0.260
MSVD- perifovea inferior quad	55.45 ± 3.70	53.75 ± 3.91	− 1.7	0.046
MDVD- perifovea	47.45 ± 7.18	47.14 ± 4.47	− 0.31	0.797
MDVD- perifovea superior hemi	48.10 ± 6.82	46.88 ± 5.28	− 1.22	0.538
MDVD- perifovea inferior hemi	47.30 ± 7.46	47.39 ± 4.03	0.09	0.945
MDVD- perifovea temporal quad	49.15 ± 7.27	49.58 ± 5.70	0.43	0.758
MDVD- perifovea superior quad	46.33 ± 7.49	45.59 ± 5.38	− 0.74	0.646
MDVD- perifovea nasal quad	51.05 ± 7.66	50.09 ± 5.23	− 0.96	0.717
MDVD- perifovea inferior quad	42.94 ± 11.65	44.07 ± 4.49	1.13	0.584

MSVD : Macular superficial vessel density

MDVD : Macular deep vessel density

ONH vasculature

The data on changes in the vascular density of the ONH and peripapillary area following coffee consumption are summarized in Table 4. There was no significant change in the capillary plexus density after coffee consumption both at the ONH itself and the peripapillary area.

To evaluate the possible effect of gender in our results, we compared the amount of change from baseline in MSVD and MDVD following coffee consumption between the two genders. The results showed that the difference from baseline in MSVD of the whole image, at the parafovea, and perifovea was significantly higher in the male group. The change from baseline in MDVD was not significantly different between males and females (Table 5).

Table 4

ONH and peripapillary vascular changes following coffee drinking.
ONH and peripapillary vasculature	Mean ± SD, baseline	Mean ± SD, after coffee drinking	Change from baseline	P-value
Small vessels- whole image	49.16 ± 2.54	49.33 ± 1.84	0.17	0.630
small vessels inside disc	49.00 ± 4.70	48.79 ± 4.93	− 0.21	0.806
RPC- small vessels	51.93 ± 2.83	52.12 ± 2.06	0.19	0.668
RPC- small vessels- superior hemi	51.88 ± 3.12	52.01 ± 2.02	0.13	0.787
RPC- small vessels- inferior hemi	51.97 ± 2.85	52.19 ± 2.64	0.22	0.628
All vessels- whole image	55.90 ± 2.26	55.96 ± 2.02	0.06	0.847
All vessels- inside disc	58.46 ± 4.00	58.31 ± 4.61	− 0.15	0.836
All vessels- peripapillary	58.44 ± 2.35	58.54 ± 1.97	0.1	0.763
All vessels- peripapillary- superior hemi	58.72 ± 2.50	58.73 ± 1.86	0.01	0.991
All vessels- peripapillary- inferior hemi	58.14 ± 2.38	58.31 ± 2.45	0.17	0.640

RPC : Radial peripapillary capillary

Table 5

Comparison of MSVD and MDVD change between males and females.
Parameters		Change from baseline (Mean ± SD)	P-Value ( t-test)
MSVD- whole image	Male	1.90 ± 1.99	0.03
MSVD- whole image	Female	0.30 ± 1.23	0.03
MSVD- fovea	Male	0.6 ± 1.46	0.11
MSVD- fovea	Female	-0.5 ± 1.59	0.11
MSVD- parafovea	Male	1.90 ± 2.12	0.028
MSVD- parafovea	Female	.1 ± 1.98	0.028
MSVD- perifovea	Male	− .87 ± 1.36	0.050
MSVD- perifovea	Female	.81 ± 2.01	0.050
MDVD- whole image	Male	2.10 ± 2.91	0.11
MDVD- whole image	Female	.2 ± 2.16	0.11
MDVD- fovea	Male	.65 ± 2.21	0.19
MDVD- fovea	Female	− .47 ± 1.48	0.19
MDVD- parafovea	Male	1.90 ± 2.90	0.13
MDVD- parafovea	Female	.12 ± 2.06	0.13
MDVD- perifovea	Male	-1.30 ± 3.05	0.17
MDVD- perifovea	Female	.51 ± 2.42	0.17

In this study, we investigated the acute effect of drinking coffee on microcirculation and the thickness of the retina and optic nerve head. The results of our study didn’t show a significant change in neural structural parameters. Peripapillary RNFL thickness did not change significantly following coffee drinking. Although the change in foveal thickness (1.36 µm) was statistically significant, it may not be of clinical significance. Because the axial resolution of Angiovue scans is 3–5 µm that means a 1µm difference between baseline thickness and after coffee drinking thickness may be a measurement error. Although assessments of macular vasculature showed a significant decrement in superficial and deep vessels density at parafovea, vessel densities at the fovea and deep capillary plexus at perifovea showed no significant change. Similarly, there was no significant change in ONH and peripapillary capillary plexus. These findings suggest that the changes in microcirculation trends to the superficial vessels and the farther we go from the parafovea to perifovea and peripapillary area, the less impact we encounter. As we showed, vessel density in the deep capillary plexus significantly decreases at the parafovea, but there is no such significant decrement at the perifovea.

In 2001, Mahmud and Feely showed that caffeine increases arterial stiffness, arterial blood pressure, and peripheral vascular resistance.¹¹ In 2010, Mostofsky et al claimed that coffee increases the risk of an ischemic stroke just immediately after drinking it (within 1 hour), particularly among infrequent drinkers, because the plasma caffeine concentration reaches its peak in this period.¹² In 2017, Washio et al showed that although coffee drinking acutely raises arterial stiffness, it doesn’t affect the middle cerebral artery pulsatile stress, so the increased risk of stroke after drinking coffee could be due to other unknown factors.³ This result can be interpreted to the hypothesis that autoregulation plays an important role in preventing pulsatile stress after coffee drinking from large arteries reach to small arteries, arterioles, and capillary beds. Differences in the behavior of the macular vessels and the optic nerve head in response to coffee consumption can be due to different autoregulation responses in these areas. Studies on macular vascular changes in glaucoma indicate a greater impact of this disease on the superficial vascular network.¹³ It seems that the susceptibility of vessels at macula to the environmental insults and their autoregulation mechanisms are different between the superficial and deep layers.¹⁴ ONH and retinal circulation impairment could increase the susceptibility of ganglion cells and nerve fibers to high IOP. It is hypothesized that intraocular pressure (IOP) is not the only determining factor in the development and progression of glaucoma, but retinal nerve fiber and optic nerve head susceptibility to IOP are of the same importance.^{15, 16} Using laser speckle flowgraphy, Okuno et al, reported an increased blood vessel resistance and a decreased blood flow in the human ONH and choroid-retina in response to oral caffeine consumption.¹⁷ In this technique a speckle pattern laser is projected onto the desired area of the retina and a sensor would detect the blurred scattered light coming back from the retina. The square blur rate (SBR) is the value produced in this method to correlate with the retinal blood flow velocity. Unlike Okuno’s study results, we didn’t find a significant change in ONH blood flow in response to coffee consumption. The participants of the Okuno study took a capsule containing 100 milligrams of pure caffeine, but in our study, we used a coffee drink containing 150 milligrams of caffeine. The bioavailability of these two products differs and coffee drink contains many other ingredients which may affect the pharmacokinetics of caffeine. Our purpose was to find out if commercial caffeine-containing drinks could alter ONH and retinal circulation. If we could demonstrate the effect of coffee on retinal circulation in normal individuals with normal ONH blood flow autoregulation, a more significant adverse effect would be expected in patients with impaired ONH blood flow regulation such as in normal-tension glaucoma (NTG).¹⁸ Then some considerations may be necessary to be taken by glaucoma patients in their daily nutritional habits.

In this study, we showed that there is a significant difference in changes of MSVD between the two genders at parafovea and perifovea. Differences in vasoregulation between males and females could be due to variations in responses of vascular endothelial cells to different vasoactive agents.¹⁹

Our study had some limitations. Small sample size, lack of control group and no masking of participants were among these limitations.

Consuming one cup of coffee (150 mg caffeine) statistically changes central foveal thickness and parafoveal blood flow, but likely does not have a clinical impact in healthy young adults.

Ethics approval and consent to participate: This study is in accordance to the decleration of Helsinky and it was approved by the institutional review board and ethics committee of the Mashhad University of Medical Sciences (IR.MUMS.MEDICAL.REC.1397.592).

Consent for publication: Consent for publication was acquired from the patient.

Competing interests: The authors declare that they have no competing interests

Funding: The authors received no funding. It is the authors’ own work, not funded by government or academic institutes.

Author Contributions: All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Nasser Shoeibi, Parisa Rajaei, Mohadese Ghobadi, SeyedehMaryam Hosseini, Mojtaba Abrishami, Mohammad-Reza Ansari-Astaneh, and Mehrdad Motamed Shariati. The first draft of the manuscript was written by Arash Omidtabrizi, and Mehrdad Motamed Shariati. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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No competing interests reported.

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Acute effects of coffee consumption on the microcirculation of macula and optic nerve head

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Abstract

Introduction

Methods

Statistical analysis

Results

Neural structural findings

Macular vasculature

ONH vasculature

Discussion

Conclusion

Declarations

References

Additional Declarations

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