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J Curr Ophthalmol
J Curr Ophthalmol
JCO
J Curr Ophthalmol
Journal of Current Ophthalmology
2452-2325
Wolters Kluwer - Medknow India

JCO-35-320
10.4103/joco.joco_207_23
Original Article
Low Ocular Perfusion Pressure Values at Rest and during Resistance Exercise in Offspring of Glaucoma Patients
Andrade Diana de Medeiros 1
Oliveira Jordane Benedito Vargas 2
Lacordia Marta Halfeld Ferrari Alves 2
Laterza Mateus Camaroti 1
Martinez Daniel Godoy 1
1 Cardiovascular Research Unit and Exercise Physiology, Federal University of Juiz de Fora, Minas Gerais, Brazil
2 Ophthalmology Service of the University Hospital of the Federal University of Juiz de Fora, Juiz de Fora, Minas Gerais, Brazil
Address for correspondence: Diana de Medeiros Andrade, Federal University of Juiz de Fora, José Lourenço Kelmer, S/N – São Pedro, 36036 900, Juiz de Fora, Minas Gerais, Brazil. E-mail: dianaandrade.fisio@gmail.com
Oct-Dec 2023
10 8 2024
35 4 320325
19 9 2023
24 11 2023
25 11 2023
Copyright: © 2024 Journal of Current Ophthalmology
2024
https://creativecommons.org/licenses/by-nc-sa/4.0/ This is an open access journal, and articles are distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as appropriate credit is given and the new creations are licensed under the identical terms.
Purpose:

To compare the ocular perfusion pressure (OPP) response during physical exercise in individuals with and without a family history (FH+, FH−) of glaucoma.

Methods:

Thirty-four subjects, divided into FH+ and FH− groups, realized 3 min at rest, 3 min of isometric handgrip exercise at 30% of maximal voluntary contraction, followed by 3 min of recovery. Blood pressure (Dixtal® automatic device) and intraocular pressure (Goldmann applanation tonometer) were measured during rest, exercise, and recovery. The mean OPP (mOPP) was calculated.

Results:

In the FH+ group (17 subjects), baseline mOPP values were significantly lower than in the FH− group (17 subjects) (right eye: P < 0.001, left eye: P < 0.001, respectively). During exercise, both the FH+ and FH− groups showed a similar increase in mOPP in both eyes (right eye: FH+: 38 ± 4 mmHg vs. 51 ± 7 mmHg, FH−: 48 ± 5 mmHg vs. 57 ± 9 mmHg, P < 0.001; left eye: FH+: 39 ± 3 mmHg vs. 51 ± 7 mmHg; FH−: 46 ± 5 mmHg vs. 58 ± 8 mmHg, P < 0.001, respectively). However, the FH+ group maintained significantly lower mOPP values compared to the FH− group in the right and left eyes (group effect: P = 0.002, P = 0.002, respectively). The percentage of increase in mOPP in the FH+ group was greater compared to the FH− group during exercise (right eye: 34.1% ± 15.9% vs. 22.1% ± 13.2%, respectively; P = 0.025; left eye: 33.2% ± 17.7% vs. 22.4% ± 13.7%, respectively, P = 0.056).

Conclusions:

mOPP increased during physical exercise in both groups, but the FH+ group had lower absolute values. In addition, the FH+ group appears to demonstrate a higher percentage increase in mOPP compared to the FH− group.

Exercise
Glaucoma
Heredity
Ocular physiological phenomena
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pmcINTRODUCTION

The main risk factor for primary open-angle glaucoma (POAG) is increased intraocular pressure (IOP).1 Age, race, atherosclerosis, corneal thickness, and positive family history (FH+) of POAG also contribute.1 First-degree relatives have a 9-fold higher risk of developing POAG.23 Epidemiological studies have correlated low mean ocular perfusion pressure (mOPP) values with the incidence of POAG.456789

It is unknown how exercise affects OPP in individuals with FH+. Thus, we aimed to compare the mOPP at baseline and during physical exercise in individuals with FH+ and without a family history (FH-) of glaucoma.

METHODS

As criteria for sample inclusion, volunteers should be between 18 and 55 years old. A total of 34 volunteers of both genders were included, divided into two groups: FH+ for POAG (17 subjects) and FH− for POAG (17 subjects). The groups were age-matched.

Exclusion criteria included the presence of cardiovascular and ocular diseases, prior ocular surgeries, the use of antihypertensive and antidiabetic medications, IOP ≥21 mmHg, and musculoskeletal abnormalities that would prevent the execution of the handgrip exercise.

The present study protocol was conducted in accordance with the Declaration of Helsinki and was approved by the Research Ethics Committee under approval number 3.177.330. All individuals included in the study participated voluntarily and signed the informed consent form.

The experimental protocol consisted of anamnesis, which included information on the volunteer’s clinical data and the presence or absence of glaucoma in their parents, as well as anthropometry for measuring body weight and height. For this purpose, a Filizola scale with an accuracy of 0.1 kg and a stepped stadiometer with an accuracy of 0.5 cm attached to it were used, respectively. Body mass index (BMI) was calculated by dividing body weight by height squared (kg/m2). All these variables were measured according to the criteria described by the American College of Sports Medicine.10

Systolic blood pressure (SBP), diastolic blood pressure (DBP), and mean arterial pressure (MAP) were measured in the seated position using an automatic oscillometric method, with the DIXTAL 2023® automatic device (Biomédica Indústria e Comércio Ltda), with the cuff placed on the nondominant upper limb of the volunteer.

Both eyes had their IOP measured using the Goldmann applanation tonometer performed by the ophthalmologist. For this purpose, anesthetic eye drops containing 4 mg/mL of oxybuprocaine hydrochloride and dye eye drops containing 1% sodium fluorescein were used. Subsequently, the mOPP was calculated as follows: ⅔MAP – IOP.11

The physical exercise protocol consisted of three stages: 3 min of rest, 3 min of isometric exercise at 30% of maximum voluntary contraction (MVC), and 3 min of recovery. For the exercise stage, a Jamar® Hand Dynamometer (Jamar Hand Dynamometer – Hydraulic - 200 lb Capacity/Fabrication) was used. Initially, the maximum isometric handgrip strength was calculated by taking the arithmetic mean of three MVC attempts on the dominant limb. At the end of the 3rd min of each stage, SBP, DBP, MAP, heart rate (HR), and IOP of both eyes were measured, and subsequently, the mOPP of both eyes was calculated.

After the protocol, the volunteers were instructed to rate their level of physical exertion during the handgrip maneuver using the Borg Scale for ratings of perceived exertion.12

The statistical analysis of the data was performed using SPSS® (IBM Corp. Released 2019. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY: IBM Corp). Data were presented as mean ± standard deviation and absolute values. The assumption of sphericity was assessed using Mauchly’s test, and when violated, Greenhouse–Geisser correction was applied. A comparison between groups regarding demographic and baseline characteristics as well as the percentage change of mOPP during exercise was conducted using the independent samples t-tests, after testing for equality of variances (Levene’s test). Cohen’s D was used for effect size, considering reference values (small: 0.2–0.5/medium: 0.5–0.8/large: Above 0.8). To investigate potential differences in BP, HR, IOP, and mOPP during the entire experimental protocol, a two-way repeated measures analysis of variance was used, followed by the Bonferroni post hoc tests. The Fisher exact test or Chi-square test, when appropriate, was used to compare categorical variables. A significance level of P ≤ 0.05 was adopted.

RESULTS

The demographic, baseline hemodynamic, and ocular pressure characteristics of both the FH+ group (17 subjects) and the FH− group (17 subjects) are shown in Table 1. Age, height, body weight, HR, and BMI were similar between the FH+ and FH− groups. However, the baseline variables SBP, DBP, MAP, and mOPP in the right eye and mOPP in the left eye were significantly lower in the FH+ group when compared to the FH− group. There was no significant difference in IOP (right and left eye) between the groups.

Table 1 Baseline demographic, hemodynamic, and ocular pressure characteristics of the with and without a family history groups

	FH+ (17)	FH- (17)	P	Cohen’s D	
Men/women	3/14	6/11	-	-	
Age (years)	32±10	29±7	0.327	0.35	
Height (m)	1.67±0	1.65±0	0.606	0.02	
Weight (Kg)	71±11	66±14	0.253	0.40	
BMI (Kg/m²)	25±4	24±3	0.215	0.28	
SBP (mmHg)	111±11	124±9	0.001	-1.29	
DBP (mmHg)	64±6	74±7	0.000	-1.53	
MAP (mmHg)	79±6	91±7	0.000	-1.84	
HR (bpm)	79±2	75±7	0.473	0.78	
IOP_R (mmHg)	14±3	14±3	0.487	0.00	
IOP_L (mmHg)	14±3	14±2	0.817	0.00	
mOPP_R (mmHg)	38±4	46±5	0.000	-1.77	
mOPP_L (mmHg)	39±3	46±5	0.000	-1.70	
FH+: With a family history, FH-: Without a family history, BMI: Body mass index, SBP: Systolic blood pressure, DBP: Diastolic blood pressure, MAP: Mean arterial pressure, HR: Heart rate, IOP_R: Intraocular pressure-right eye, IOP_L: Intraocular pressure-left eye; mOPP_R: Mean ocular perfusion pressure-right eye, mOPP_L: Mean ocular perfusion pressure-left eye. The test used to obtain the P values was the unpaired t-tests (P≤0.05)

During exercise, SBP, DBP, MAP, and HR variables increased similarly between the groups. SBP, DBP, and MAP return to baseline values during the recovery period. However, the FH+ group consistently exhibited significantly lower SBP, DBP, and MAP values throughout the entire experimental protocol (group effect: P = 0.015; P = 0.001; P = 0.002, respectively) [Figure 1a-c]. HR increased during exercise and decreased after the recovery period to values below baseline for both groups remaining similar between the groups [Figure 1d].

Figure 1 Response of (a) systolic blood pressure, (b) diastolic blood pressure, (c) mean arterial pressure, and (d) heart rate at rest, during handgrip exercise, and in postexercise recovery. *P < 0.05 versus baseline, †P < 0.05 versus group, ‡P < 0.05 versus exercise. MAP: Mean arterial pressure, SBP: Systolic blood pressure, DBP: Diastolic blood pressure, FH: Family history

There was no increase in IOP in the right eye during exercise in both groups (time effect: P = 0.109). On the other hand, the IOP of the left eye increased significantly and similarly in both the FH+ and FH− groups (14 ± 3 mmHg vs. 15 ± 3 mmHg; 14± 2 mmHg vs. 15 ± 2 mmHg, time effect: P = 0.022, group effect = 0.967; interaction effect = 0.772, respectively). However, during the recovery period, the IOP of both eyes, in both the FH+ and FH− groups, significantly decreased compared to baseline (right eye: FH+:14 ± 4 mmHg vs. 13 ± 3 mmHg, FH−: 14 ± 2 mmHg vs. 13 ± 2 mmHg, time effect: P = 0.028; left eye: FH+: 14 ± 3 mmHg vs. 13 ± 3 mmHg; FH−: 14 ± 2 mmHg vs. 13 ± 2 mmHg, time effect: P = 0.017, respectively [Figure 2]).

Figure 2 Response of intraocular pressure at rest, during handgrip exercise, and in postexercise recovery in the (a) right and (b) left eyes. *P < 0.05 versus baseline, †P < 0.05 versus group, ‡P < 0.05 versus exercise. IOP: Intraocular pressure, FH: Family history

During the physiological handgrip maneuver, both the FH+ and FH− groups showed a similar increase in mOPP in both eyes (right eye: FH+: 38 ± 4 mmHg vs. 51 ± 7 mmHg, FH−: 48 ± 5 mmHg vs. 57 ± 9 mmHg, P = 0.000; left eye: FH+: 39 ± 3 mmHg vs. 51 ± 7 mmHg; FH−: 46 ± 5 mmHg vs. 58 ± 8 mmHg, P = 0.000, respectively). However, throughout the entire experimental protocol, the FH+ group maintained significantly lower mOPP values compared to the FH− group in both the right and left eyes (group effect: P = 0.002, P = 0.002, respectively). During the recovery period, mOPP returned to baseline values in both the right and left eyes (right eye: FH+: 41 ± 6 mmHg vs. 38 ± 4 mmHg, FH−: 45 ± 5 mmHg vs. 48 ± 5 mmHg, P = 1.000; left eye: FH+: 41 ± 5 mmHg vs. 39 ± 3 mmHg; FH−: 45 ± 5 mmHg vs. 46 ± 5 mmHg, P = 1.000, respectively [Figure 3]).

Figure 3 Response of mean ocular perfusion pressure at rest, during handgrip exercise, and in postexercise recovery in the (a) right and (b) left eyes. *P < 0.05 versus baseline; †P < 0.05 versus group; ‡P < 0.05 versus exercise. mOPP: Mean ocular perfusion pressure, FH: Family history

Furthermore, the percentage of increase in mOPP in the FH+ group was greater compared to the FH− group during physical exercise (right eye: 34.1% ± 15.9% vs. 22.1% ± 13.2%, respectively; P = 0.025; left eye: 33.2% ± 17.7% vs. 22.4% ± 13.7%, respectively, P = 0.056).

DISCUSSION

The main finding of this study was that healthy individuals with a positive FH of glaucoma exhibited a preserved response of increased mOPP during resistance exercise. However, the absolute mOPP values were significantly lower compared to the FH− group throughout the entire experimental protocol.

Several epidemiological studies have investigated the relationship between OPP and glaucoma, and they have observed that reduced OPP is a risk factor for the prevalence, incidence, and progression of the condition.456789131415

The Barbados Eye Study7 was a longitudinal study that assessed the incidence of glaucoma after 9 years of follow-up. The study indicated that participants with mOPP lower than 40 mmHg had a 2.6 times higher risk of developing glaucoma.7 In the present study, the FH+ group exhibited mOPP values, in both eyes, below 40 mmHg, which increases the risk of glaucoma development for these individuals.

In addition, during physical exercise, there was a significant increase in mOPP in both groups, in line with data from various studies1617181920212223242526 that demonstrate that resistance exercise increases mOPP. Consequently, the FH+ group, during exercise, reached absolute mOPP values above those cited as a risk for glaucoma,7 although after recovery, the values of the variables in both groups returned to baseline values.

Another relevant finding of the present study was that the FH+ group exhibited a higher percentage of increase compared to the FH− group, particularly in the right eye. An important fact is that Movaffaghy et al. conducted a study on healthy individuals to investigate the effect of increasing OPP on ocular blood flow through squatting exercise. The authors observed that blood flow in the optic nerve head remained unchanged until mOPP increased by approximately 34% in relation to baseline.27 In the present study, the FH+ group demonstrated a 34% increase in the right eye and 33% in the left eye, aligning with the threshold identified by Movaffaghy et al. for the consistent maintenance of blood flow.

Autoregulation, defined as the vascular bed’s ability to adjust its vascular resistance to changes in OPP, is crucial for maintaining relatively constant blood flow, thereby stabilizing tissue perfusion and capillary hydrostatic pressure during normal variations in BP. In a nonautoregulated vascular bed, any alteration in OPP directly affects perfusion.24

Although our study utilized handgrip exercise, which requires less muscle recruitment compared to squats, we observed a greater variation in the percentage of increase in the FH+ group. This suggests that there could be more significant fluctuations in blood flow within the FH+ group during routine physical activities, potentially posing risks for a population with impaired autoregulation.

Physical exercise plays an important role in the regulation of ocular BP.28 As it is already known, acute resistance exercise can increase BP through sympathetic stimulation.28 However, this increase in BP is directly related to the exercise intensity, the number of sets, the load mobilized, and the muscle groups involved.29 Typically, during strength exercise, both SBP and DBP tend to rise, resulting in a significant increase in MAP, even if only for a short period.30 Similarly, mOPP also increases during physical exercise.1617181920212223242526

It can be inferred that low mOPP values presented by individuals with a FH of glaucoma put this population at a higher risk of developing glaucoma when compared to those without an FH.

Given the potential influence of genetic factors on glaucoma, it is important to note that the sample being discussed has a high level of admixture, likely referring to a mix of different genetic backgrounds or ancestries. There is a known higher risk of POAG among individuals of African descent.1 Siesky et al., examining ocular blood flow disparities between individuals of African and European descent with open-angle glaucoma, found notably lower blood flow in individuals of African descent compared to their European counterparts. These findings imply that the role of ocular blood flow in the progression of the disease may differ between these ethnic groups.31 Consequently, it is essential to refrain from generalizing our findings to all populations.

The handgrip exercise performed by the volunteers is related to functionality since manual grip is part of daily life and is essential for maintaining daily activities. The intensity of the exercise performed by the study population can be considered “moderately strong” for the FH− group (4) and “strong” for the FH+ group (5) according to the Borg Scale for Ratings of Perceived Exertion.12

Our study presented some limitations. Regarding the volunteers, the age range was broad (18–55 years old), but the mean age of both the FH+ and FH− groups was similar, reflecting young adults (FH+: 32 ± 10 vs. FH−: 29 ± 7 years; P = 0.327). The results may not be representative of older age groups or other demographic characteristics. Generalizing the findings to a broader population may require caution. The number of participants in the study may be limited; however, the mOPP response during exercise exhibited significant statistical power for group comparison (HF+ vs. HF−) with values of 0.895 for the right eye and 0.917 for the left eye. Furthermore, we achieved a statistical power of 1.000 when comparing rest and exercise.

As an exclusion criterion, we excluded individuals with no history of cardiovascular and ocular diseases because both conditions could impact IOP and OPP values. Our aim was to evaluate healthy individuals unaffected by systemic and ocular diseases. Our sample does not fully represent the diversity of individuals with an FH of glaucoma. This could limit the external validity of the findings.

Our study calculated mOPP using a single measurement during each stage of the exercise protocol. Continuous monitoring of mOPP could provide a more comprehensive understanding of its dynamic changes during exercise. Furthermore, the subjective nature of self-reported physical exertion using the Borg Scale introduces an element of subjectivity. However, the protocol used was 30% of the MVC in both groups. Even so, objective measures of exercise intensity could contribute to understanding the results. The study primarily focuses on acute responses to resistance exercise. A longer-term follow-up could provide insights into the chronic effects of exercise on mOPP and the potential impact on the development or progression of glaucoma.

In our study, we did not evaluate peak oxygen consumption. However, in the anamnesis, we observed that 11 volunteers in the HF+ group and 6 volunteers in the HF− group reported practicing physical activity, with no difference in the proportion distribution between groups (Chi-square, P = 0.17). Only two volunteers in the HF− group were using medication for anxiety. Six women in the HF+ group and four women in the HF− group were using oral contraceptives with no difference in the proportion distribution between groups (Fisher’s exact test, P = 1.00).

Thus, we conclude that mOPP increased acutely during physical exercise in both groups, but the FH+ group exhibited lower absolute values throughout the entire experimental protocol. In addition, the FH+ group appears to demonstrate a higher percentage increase in mOPP compared to the FH− group. However, more controlled and randomized clinical trials are needed to observe the acute and chronic effects of resistance exercise on mOPP, as well as clinical pharmacological and nonpharmacological strategies for increasing mOPP in individuals with a positive FH of POAG.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.
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REFERENCES

1 Jonas JB Aung T Bourne RR Bron AM Ritch R Panda-Jonas S Glaucoma Lancet 2017 11 2183 93
2 Awadalla MS Fingert JH Roos BE Chen S Holmes R Graham SL Copy number variations of TBK1 in Australian patients with primary open-angle glaucoma Am J Ophthalmol 2015 159 124 30.e1 25284765
3 Wolfs RC Klaver CC Ramrattan RS van Duijn CM Hofman A de Jong PT Genetic risk of primary open-angle glaucoma. Population-based familial aggregation study Arch Ophthalmol 1998 116 1640 5 9869795
4 Quigley HA West SK Rodriguez J Munoz B Klein R Snyder R The prevalence of glaucoma in a population-based study of Hispanic subjects: Proyecto VER Arch Ophthalmol 2001 119 1819 26 11735794
5 Memarzadeh F Ying-Lai M Chung J Azen SP Varma R Los Angeles Latino Eye Study Group Blood pressure, perfusion pressure, and open-angle glaucoma: The Los Angeles Latino eye study Invest Ophthalmol Vis Sci 2010 51 2872 7 20089880
6 Bonomi L Marchini G Marraffa M Bernardi P Morbio R Varotto A Vascular risk factors for primary open angle glaucoma: The egna-neumarkt study Ophthalmology 2000 107 1287 93 10889099
7 Leske MC Wu SY Hennis A Honkanen R Nemesure B BESs Study Group Risk factors for incident open-angle glaucoma: The Barbados eye studies Ophthalmology 2008 115 85 93 17629563
8 Mitchell P Lee AJ Rochtchina E Wang JJ Open-angle glaucoma and systemic hypertension: The blue mountains eye study J Glaucoma 2004 13 319 26 15226661
9 Zheng Y Wong TY Mitchell P Friedman DS He M Aung T Distribution of ocular perfusion pressure and its relationship with open-angle glaucoma: The Singapore Malay eye study Invest Ophthalmol Vis Sci 2010 51 3399 404 20164462
10 ACMS American College of Sports Medicine (ACSM) Guidelines for Exercise Testing and Prescription 9th ed Guanabara Koogan 2014
11 Leske MC Ocular perfusion pressure and glaucoma: Clinical trial and epidemiologic findings Curr Opin Ophthalmol 2009 20 73 8 19240538
12 Borg GA Psychophysical bases of perceived exertion Med Sci Sports Exerc 1982 14 377 81 7154893
13 Omoti AE Enock ME Okeigbemen VW Akpe BA Fuh UC Vascular risk factors for open angle glaucoma in African eyes Middle East Afr J Ophthalmol 2009 16 146 50 20142982
14 Tielsch JM Katz J Sommer A Quigley HA Javitt JC Hypertension, perfusion pressure, and primary open-angle glaucoma. A population-based assessment Arch Ophthalmol 1995 113 216 21 7864755
15 Xu L Wang YX Jonas JB Ocular perfusion pressure and glaucoma: The Beijing eye study Eye (Lond) 2009 23 734 6 18989341
16 Banerjee A Indukhurana Dhull CS Effect of ocular perfusion pressure to isometric handgrip test in patients with primary open angle glaucoma (POAG): a test for autonomic activity Int J Curr Res 2016 8 33064 7
17 Beck D Harris A Evans D Martin B Ophthalmic arterial hemodynamics during isometric exercise J Glaucoma 1995 4 317 21 19920693
18 Boltz A Schmidl D Werkmeister RM Lasta M Kaya S Palkovits S Regulation of optic nerve head blood flow during combined changes in intraocular pressure and arterial blood pressure J Cereb Blood Flow Metab 2013 33 1850 6 23921903
19 Boltz A Told R Napora KJ Palkovits S Werkmeister RM Schmidl D Optic nerve head blood flow autoregulation during changes in arterial blood pressure in healthy young subjects PLoS One 2013 8 e82351 24324774
20 Kiss B Dallinger S Polak K Findl O Eichler HG Schmetterer L Ocular hemodynamics during isometric exercise Microvasc Res 2001 61 1 13 11162191
21 Popa-Cherecheanu A Schmidl D Werkmeister RM Chua J Garhöfer G Schmetterer L Regulation of choroidal blood flow during isometric exercise at different levels of intraocular pressure Invest Ophthalmol Vis Sci 2019 60 176 82 30640970
22 Ramya CM Nataraj SM Rajalakshmi R Smitha MC Changes in ocular perfusion pressure in response to short term isometric exercise in young adults Niger J Physiol Sci 2018 33 101 3 30091740
23 Riva CE Hero M Titze P Petrig B Autoregulation of human optic nerve head blood flow in response to acute changes in ocular perfusion pressure Graefes Arch Clin Exp Ophthalmol 1997 235 618 26 9349945
24 Schmidl D Boltz A Kaya S Werkmeister R Dragostinoff N Lasta M Comparison of choroidal and optic nerve head blood flow regulation during changes in ocular perfusion pressure Invest Ophthalmol Vis Sci 2012 53 4337 46 22661477
25 Witkowska KJ Bata AM Calzetti G Luft N Fondi K Wozniak PA Optic nerve head and retinal blood flow regulation during isometric exercise as assessed with laser speckle flowgraphy PLoS One 2017 12 e0184772 28898284
26 Zhang Y San Emeterio Nateras O Peng Q Rosende CA Duong TQ Blood flow MRI of the human retina/choroid during rest and isometric exercise Invest Ophthalmol Vis Sci 2012 53 4299 305 22661466
27 Movaffaghy A Chamot SR Petrig BL Riva CE Blood flow in the human optic nerve head during isometric exercise Exp Eye Res 1998 67 561 8 9878218
28 Kilbom A Brundin T Circulatory effects of isometric muscle contractions, performed separately and in combination with dynamic exercise Eur J Appl Physiol Occup Physiol 1976 36 7 17 1001318
29 Polito MD Farinatti PT Heart rate, blood pressure, and rate pressure product during resistive exercises: a review of the literature Rev Port Ciências Desporto 2003 3 79 91
30 MacDougall JD Tuxen D Sale DG Moroz JR Sutton JR Arterial blood pressure response to heavy resistance exercise J Appl Physiol (1985) 1985 58 785 90 3980383
31 Siesky B Harris A Racette L Abassi R Chandrasekhar K Tobe LA Differences in ocular blood flow in glaucoma between patients of African and European descent J Glaucoma 2015 24 117 21 23807346
