Subfoveal choroidal thickness and peripapillary retinal nerve fiber layer thickness in young obese males

Abstract

Objective:

Regarding the effect of obesity on subfoveal choroidal thickness (CT) and peripapillary retinal nerve fiber layer (RNFL) thickness, controversial results have been reported in different patient groups. This study aimed to evaluate the effect of obesity on these parameters among young male subjects in comparison with age-matched non-obese healthy males.

Methods:

This prospective, cross-sectional study included both eyes of 50 obese young males and 50 healthy non-obese young males. The obese and the non-obese groups included subjects with a BMI of ⩾30 and ⩽25 kg/m², respectively. Subfoveal choroidal thickness and RNFL analyses were conducted by spectral domain optical coherence tomography (SD-OCT).

Results:

Subfoveal choroidal thickness (321.0 ± 46.7 vs 338.4±35.3, p = 0.002) and RNFL thickness at temporal quadrant (73.4 ± 9.9 vs 76.4 ± 9.3, p = 0.008) was significantly lower in the obese group when compared to the non-obese group. The groups did not differ regarding peripapillary RNFL thickness at other quadrants (superior, inferior, or nasal) or regarding mean peripapillary RNFL thickness.

Conclusion:

Findings of this study demonstrated a negative correlation of obesity with subfoveal choroidal thickness and temporal quadrant peripapillary RNFL thickness. Larger studies on different patient groups with longer-term follow-up are warranted to better elucidate the ophthalmological effects of obesity.

Keywords

Subfoveal choroidal thickness retinal nerve fiber layer obesity young males optical coherence tomography

Introduction

Obesity, a complex multifactorial disease, currently represents a global health issue. Rates of obesity have been on the rise due to poor eating habits, sedentary lifestyle, and increasing use of food additives. Recent estimates have suggested that nearly 40% of the US population is obese, while a prevalence rate of 32% places Turkey among one of the highest prevalence countries in Europe.^1,2

Studies on obesity have consistently shown that obesity frequently coexists with many systemic disorders such as diabetes mellitus, hypertension, dyslipidemia, atherosclerosis, and cardiac diseases.^3–5 Although the correlation between obesity and ophthalmologic diseases is not well documented, obesity is commonly associated with cataracts, glaucoma, diabetic retinopathy, and age-related macular degeneration.⁶

The choroidal tissue is a vascular layer between the retina and the sclera, extending from the optic nerve head to the ora serrata. While the inner retinal layers are supplied with blood flow from the central retinal artery, the outer retinal layers and the prelaminar part of the optic nerve are fed through the choroid. The choroid has a much higher blood flow rate than other tissues and organs of the body per tissue volume. Peripapillary retinal nerve fiber layer (RNFL) thickness is a parameter that is obtained through averaging multiple measurements on a peripapillary circle placed around the optic disc. Although this parameter has an important role in monitoring patients with glaucoma, it has also been shown to be diminished under the influence of a number of factors including advanced age, male gender, short axial length, cataract surgery, and high BMI in males irrespective of intraocular pressure.⁷

Controversial results have been reported in different patient groups (e.g. pediatric patients, obese females, or morbidly obese subjects) regarding the effect of obesity on subfoveal choroidal thickness (CT) and peripapillary RNFL thickness, with some studies reporting increase or no change in contrast with others reporting decrease with increasing severity of obesity.^8–14 On the other hand, data for obese young males are still lacking.

Optical coherence tomography (OCT) is a non-contact, non-invasive, and easily performed imaging method developed by Huang in 1991. OCT rapidly provides information about the retinal layers and the assessment can be performed frequently, as it does not involve radiation exposure.¹⁵ In 2008, Spaide et al.¹⁶ defined a novel technique termed as enhanced depth imaging-OCT (EDI-OCT) that enabled a more detailed examination of the eye, allowing the thickness of the choroid, retina, and RNFL to be measured.

This study aimed to evaluate the effect of obesity on subfoveal choroidal thickness and peripapillary RNFL thickness using OCT among young male subjects in comparison with age-matched non-obese healthy males.

Methods

Patients

This prospective, cross-sectional study included both eyes of 50 obese young males (100 eyes) and 50 healthy non-obese young males (100 eyes) who were referred to the ophthalmology clinic between September 2018 and June 2019. Participants had to be between 19 and 32 years of age. Male individuals who applied for exemption from military service due to obesity constituted the obese group. As a part of exemption evaluation procedures, ophthalmological examination is routinely performed. Young male patients admitted to the outpatient clinic of the ophthalmology department for the examination of refractive errors who were not obese constituted the non-obese group. Groups were defined according to the criteria set by the World Health Organization. The obese and the non-obese groups included subjects with a BMI of ⩾30 and ⩽25 kg/m², respectively. Subjects with a BMI of <20 (underweight individuals) were excluded from the non-obese group. All participants had a detailed ophthalmologic examination before enrollment and those who had systemic diseases other than obesity, disorders of the eyes such as strabismus, cataract or glaucoma, incomplete vision in both eyes, history of ophthalmic trauma or surgery, refraction error that could affect measurements (myopia or hyperopia ⩾ 2.00, astigmatism ⩾ 1.50), and a short or long axial length (shorter than 22.0 mm or longer than 25.0 mm) were excluded. Obese patients as well as controls had to be free from chronic diseases and chronic medication use. The study was conducted in accordance with the Declaration of Helsinki and approved by the ethics committee of GOP Taksim Training and Research Hospital (March 7, 2018, number, 28). Participants provided written informed consent prior to study entry.

OCT measurements

Primary and secondary outcome measures were subfoveal choroidal thickness and peripapillary RNFL thickness, respectively. Peripapillary mean RNFL thickness and RNFL thicknesses in each of four quadrants (i.e. superior, inferior, nasal, and temporal) were measured. Subfoveal choroidal thickness and RNFL analyses were conducted by spectral domain optical coherence tomography (SD-OCT) (3D OCT-2000 FA plus, version 8.20, Topcon, Tokyo, Japan). The 3D macular scanning protocol (6 mm × 6 mm, 512 × 128 A-scans) and the 3D optic disc protocol (6 mm × 6 mm, 512 × 128 A-scans) was used for choroidal thickness and RNFL measurements, respectively. In addition, the axial length was measured by IOL (intraocular lens) Master (Carl Zeiss AG, Oberkochen, Germany) in each participant. After the completion of the process, the subfoveal choroidal thickness was manually measured with the assistance of calipers, marking the distance between the outer edge of the retinal pigment epithelium and the choroid-scleral junction. All measurements and manual calculations were done by the same person. OCT measurements were done at roughly the same time of day (9:00–11:00 am) after dilatation by tropicamide. Measurements were repeated until a sufficiently high signal was obtained, while paying attention to the head position and internal fixation point of the participants.

Statistical analysis

Statistical Package for Social Sciences (SPSS) version 24.0 for Windows (SPSS Inc., Chicago, IL) was used for the analysis of data. Normality of distribution was tested using Kolmogorov–Smirnov test. Intergroup comparisons of continuous variables were done using student t test for independent samples or Mann–Whitney U test, depending on the distribution of data. A two-tailed p value <0.05 was considered indication of statistical significance.

Results

Table 1 shows the characteristics of the participants in the two groups, which did not differ in terms of age, height, and axial length (p > 0.05 for all). As expected from the definition of the groups, body weight and BMI were significantly higher in the obese group (p = 0.001 for both). Based on full ophthalmologic examination, the best corrected visual acuity was bilateral 20/20, intraocular pressure values were within the normal limits (⩽20 mm Hg), pachymetry measurements were in the range of 530–550 µm, and the anterior segment and fundus examinations were normal in all participants. A total of nine patients (18 eyes) were morbidly obese in the obese patient group, BMI ranging from 40.4 to 43.6 kg/m².

Table 1.

Characteristics of the participants.

	Obese group	Non-obese group	p-value*
Age, years	24.6 ± 3.3	24.0 ± 3.1	0.289
Body weight, kg	122.6 ± 14.7	74.7 ± 7.3	0.001
Height, cm	176.8 ± 6.9	178.3 ± 6.5	0.072
BMI, kg/m²	39.2 ± 4.4	23.4 ± 1.2	0.001
Axial length, mm	23.9 ± 0.9	23.6 ± 0.7	0.200

BMI: body mass index.

All p-values are from Mann–Whitney U test. Data presented as mean ± standard deviation. Each group included 50 participants. Axial length measurements were done in both eyes (i.e. 100 eyes in each group).

Table 2 shows the comparison of the two groups in terms of subfoveal choroidal thickness and peripapillary RNFL thickness. Subfoveal choroidal thickness (321.0 ± 46.7 vs 338.4 ± 35.3, p = 0.002) and RNFL thickness at temporal quadrant (73.4 ± 9.9 vs 76.4 ± 9.3, p = 0.008) was significantly lower in the obese group when compared to the non-obese group. The groups did not differ regarding peripapillary RNFL thickness at other quadrants (superior, inferior, or nasal) or regarding mean peripapillary RNFL thickness.

Table 2.

Comparison of the groups in terms of subfoveal choroidal thickness and peripapillary RNFL thickness.

	Obese group	Non-obese group	p-value
Subfoveal choroidal thickness	321.0 ± 46.7 (320.0, 209.0–400.0)	338.4 ± 35.3 (340.5, 201.0–412.0)	0.002*
Peripapillary RNFL thickness
Mean RNFL thickness	102.6 ± 6.8 (102, 90–122)	101.1 ± 8.2 (100, 85–125)	0.107*
Superior quadrant	123.7 ± 9.2 (124.5, 98–146)	120.3 ± 14.2 (120.5, 48–158)	0.050^†
Inferior quadrant	128.1 ± 11.0 (128.5, 98–151)	125.5 ± 14.8 (125, 86–171)	0.159^†
Temporal quadrant	73.4 ± 9.9 (73, 48–101)	76.4 ± 9.3 (76, 42–99)	0.008*
Nasal quadrant	84.5 ± 10.7 (84, 56–116)	81.9 ± 10.9 (83, 58–107)	0.087^†

RNFL: retinal nerve fiber layer.

All measurements are in micrometers. Data presented as mean ± standard deviation (median, range). Each group included 100 eyes of 50 participants.

Student t test for independent samples.

†

Mann-Whitney U test.

Discussion

In this study comparing subfoveal choroidal thickness, average peripapillary RNFL thickness, and four-quadrant (superior, inferior, nasal, and temporal) RNFL thickness between young obese males and age- and sex-matched healthy individuals, the former group has been found to have thinner subfoveal choroidal thickness and peripapillary temporal quadrant RNFL thickness as compared to controls. To the best of our knowledge, this study is the first to assess changes in subfoveal choroidal thickness and peripapillary RNFL thickness measurements in obese versus non-obese healthy young males.

The choroid has a much higher blood flow rate than other tissues and organs of the body per tissue volume. Several studies have been published regarding the correlations between choroid thickness and obesity in different patient groups, with inconsistent results. While increased subfoveal choroidal thickness has been reported in obese females,¹⁰ it has been found to be diminished in morbidly obese people, with a subsequent increase following laparoscopic sleeve gastrectomy.^6,17 While Panon et al.¹³ found similar subfoveal choroidal thickness measurements among obese and normal subjects, Yılmaz et al.¹¹ in their 160-patient series with varying BMI values, found a reduced choroid thickness among those with a BMI of greater than 25 kg/m², suggesting that this observation could be due to an imbalance between vasodilator and vasoconstrictor mediators resulting from obesity. Similarly, mixed results have been reported among pediatric patients.^8,9 In the current study, we found diminished subfoveal choroidal thickness measurements in young obese males as compared to healthy controls.

Peripapillary RNFL thickness decreases mainly due to glaucoma. Changes in RNFL thickness that are not particularly due to glaucoma can be influenced by many factors. In a study conducted by the EPIC-Norfolk Eye Study group on 11,030 healthy eyes, it was reported that the RNFL measurements were thinner in those with advanced aged, male sex, short axial length, history of cataract surgery, and high BMI (in males only), but there was no correlation between intraocular pressure and RNFL measurements.⁷ Also, several previous studies investigated the association between RNFL thickness and obesity in varying patient groups. In one such study, Panon et al.¹³ found no difference in RNFL thickness between obese and non-obese individuals, while Dogan et al.⁶ observed reduced RNFL thickness in morbidly obese subjects. Again, in another study in morbidly obese subjects, reduced RNFL thickness was detected in the temporal quadrant.¹² In a study by Pacheco-Cervera et al.,¹⁸ a negative correlation has been shown between RNFL thickness and BMI, leptin, and interleukin‑6 levels among overweight and obese children; however, RNFL thickness at the temporal quadrant did not differ between normal weight, overweight, obese and severely obese children, although these values were significantly different for other quadrants. Although this was attributed to the critical role of inflammatory factors in the retinal cell damage, authors did not provide any reasonable explanations of how inflammatory cytokines affect some quadrants, sparing others.¹⁸ In the present study however, young obese males had reduced peripapillary RNFL thickness in their temporal quadrant.

It is currently well known that a high BMI is associated with many systemic and ocular disorders, resulting in macrovascular and microvascular structural changes. Obese individuals have been shown to have reduced choroidal thickness and ocular pulse amplitude, which may indicate reduced ocular blood flow and choroid perfusion.¹⁹ Stapleton et al.²⁰ found that obese individuals have decreased nitric oxide (NO) levels, which could result in impaired dilatation of the vasculature. In addition, increased levels of some vasoconstrictor molecules such as endothelin-1 and angiotensin-II have been reported to be associated with higher BMI.²¹ NO plays an important role in the regulation of ocular perfusion on the retina, optic nerve and choroidal tissue.²² Experimental studies in animals showed a positive correlation between choroidal thickness and levels of retinal dopamine and choroid-originated NO, which is secreted by retinal dopamine stimulation.^23–25 Dopamine of retinal origin that has a role in NO secretion may also be reduced in association with the NO levels, which have been shown to be decreased in obese individuals. It has also been shown that systemic inhibition of nitric oxide synthase reduces total choroidal blood flow in humans, whereas exogenous dopamine administration reduces vascular resistance, thereby creating vasodilation and increased choroidal blood flow in rabbits.^26,27

Potential effects of obesity on retinal microvascular circulation have been examined in different age groups; and narrowing of retinal arterioles and dilatation of retinal venules have been reported in both children/adolescents and adults.^28,29 In obese individuals who underwent bariatric surgery, the observed increase in arteriolar caliber and decrease in venular caliber suggest that obesity may have effect on retinal microvascular structures.³⁰ In pediatric obese cases, wider retinal venules, narrower retinal arterioles, and lower subfoveal choroidal thickness have been associated with microvascular impairments.⁹ Agarwall et al.³¹ examined the changes in choroid thickness measurements and retinal arteriole/venule ratio following treatment with respect to normal individuals in obese patients who underwent bariatric surgery or received conservative management. The study found that choroid thickness increased in the bariatric surgery group compared to baseline, whereas in the conservative management group, retinal arteriole/venule ratio increased; and authors suggested arteriole to venule ratio as an indication of preclinical changes in cerebral and coronary microcirculation. Nitric oxide levels, which are shown to decrease in obese individuals, might have role in such changes of subfoveal choroidal thickness as well as retinal microvascular structures. Hanssen et al. examined obese and lean athletes after a 10-week training program. Training improved retinal arteriole to venule ratio in both groups and induced retinal arteriolar dilatation in obese athletes. The authors suggested a possible key role for nitric oxide/asymmetric dimethylarginine (ADMA) pathway in this microvascular improvement.³² Further studies on adults with a high BMI are warranted to elucidate the correlation between the changes in choroidal thickness and retinal arteriole/venule diameters and the pathogenesis of such changes.

Several hypotheses have been proposed regarding the mechanisms of the thinning of peripapillary RNFL, which may be detected in individuals with high BMI. A previous study suggested that visceral fat accumulation and reduction in lipoprotein lipase activity may induce neurodegenerative retinal disorders and a subsequent decline in RNFL thickness, especially on the nasal side.³³ Detection of reduced RNFL thickness measurements in nasal, temporal, superior temporal, and inferior quadrants independent of age, gender, and obesity-related comorbidities in obese subjects with subclinical idiopathic intracranial hypertension suggests that this finding may represent a potential marker for optic nerve neurodegeneration and thus, for systemic neurodegeneration.³⁴ Obesity is known to be associated with low levels of systemic inflammation, which leads to another theory that chronic inflammation may induce RNFL thinning.^35–37 Low-grade inflammation, oxidative stress, and endothelial dysregulation has been reported to cause an initial axonal injury with subsequent RNFL thinning in pediatric obese subjects.³⁸ Another theory points out to a negative correlation between blood pressure measurements and RNFL thickness, particularly in the temporal quadrant. In patients who had undergone gastric bypass surgery, an increase in RNFL thickness have been observed in both eyes, together with a significant improvement in blood pressure as well as decreased BMI at 3 months and 1 year after surgery.³⁹ Although the mechanisms of the diminished RNFL thickness in the temporal quadrant in our study may be related with the hypotheses stated above, it should be noted that these studies have been carried out with the participation of pediatric cases or mixed gender cohorts, with predominance of females in some. On the other hand, the reported RNFL thinning without reference to the quadrant in males with high BMI in the EPIC-Norfolk Eye Study Group study evaluating the factors influencing RNFL is partly in line with our observations.

These two parameters (subfoveal choroidal thickness and RNFL thickness) may represent early markers both for local and systemic vascular complications in obese people with increased cardiovascular risk and also for the neuronal injury underlying the pathogenesis of glaucoma that may coexist with obesity.

Certain limitations of our study deserve to be mentioned. Firstly, the sample size was small, which may interfere with the generalizability of the findings. Larger studies may allow detection of alterations of peripapillary RNFL thickness in quadrants other than the temporal quadrant. Low statistical power due to small sample size in this study may be accounted for marginal but insignificant p values for RNFL thicknesses in superior, nasal, and inferior quadrants. There may be some degree of variability owing to the manual measurements done in this study using SD-OCT, which may be considered another limitation. Long-wavelength SS-OCT on the other hand, which is a novel and less available device, has the potential to better delineate the sclerochoroidal junction owing to its higher acquisition speed and deeper tissue penetration.⁴⁰ Its superiority is particularly evident in cases with a thick choroid.⁴¹ Nevertheless, both devices are recommended for the measurement of choroidal thickness.⁴² In the present study, SD-OCT was used since SS-OCT was not available. In addition, we believe that future studies would benefit from the use of newly identified parameters such as the choroidal vascular index.⁴³ Another limitation is the cross-sectional design, which does not provide an idea on the effects of BMI changes over time. In addition, lack of discrimination between fat deposition and muscle hypertrophy, especially in such a young male population, may be a source of bias. However, there was no such an additional evaluation procedure other than BMI during the routine military exemption procedure, neither clinically nor legally. Recent guidelines on obesity do not provide definite criteria for such a discrimination as well.

On the other hand, there are several strengths of the study, including the use of homogeneous groups in terms of age, sex, axial length measurements, refractive errors, and the absence of any other ocular or systemic disorders.

In conclusion, our results showed a negative correlation of obesity with subfoveal choroidal thickness and temporal quadrant RNFL thickness measurements in young males. Larger studies with longer-term follow-up with different groups of patients are warranted to better elucidate the ophthalmological effects of obesity.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Ceylan Uslu Dogan

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