Prevalence and Clinical Characteristics of Myelinated Retinal Nerve Fibers in a Healthy Population: A Big-data Analysis

doi:10.21203/rs.3.rs-4708536/v1

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Prevalence and Clinical Characteristics of Myelinated Retinal Nerve Fibers in a Healthy Population: A Big-data Analysis

https://doi.org/10.21203/rs.3.rs-4708536/v1

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Objective: To analyze the prevalence, clinical characteristics, and related factors of myelinated retinal nerve fibers (MRNFs) in a community-based cohort.

Methods: From March 2017 to June 2020, a total of 10,341 adults undergoing health examinations at Beijing Tongren Hospital received comprehensive systemic and basic eye examinations. Diagnosis of MRNFs was conducted using fundus photography.

Results: Excluding 97 blurred fundus photographs, the final population was 10,244 participants. The average age was 49.5±14.8 years, with 6,225 females (60.8%). 66 patients were diagnosed with MRNFs, showing a prevalence of 0.6±0.3%. In the 73 affected eyes of 66 patients, a total of 86 MRNFs lesions were found, with 64 eyes (87.7%) having a single lesion and 9 eyes (12.3%) having multiple lesions. A significant positive correlation was observed between the prevalence of MRNFs and elevated systolic blood pressure (P=0.025, OR: 1.014). Two eyes had extensive MRNFs connected to the optic disc, but not involving the macular fovea. The visual acuity of the affected eyes was 1.0.

Conclusions: In community-based study in healthy Chinese population, MRNFs were found in 0.6% of cases. They were linked to increased systolic blood pressure. Extensive MRNFs can work for normal visual function while they uncover the macular fovea.

Myelinated retinal nerve fibers (MRNFs) are the congenital myelination of retinal ganglion cells axons, appearing as white or grayish-white patches on the retina, located in the inner layer of the retina, with frayed or feathered borders that can obscure the underlying retinal blood vessels[1]. The reported prevalence of MRNFs ranges from 0.4–1.0% in a general population[1–5]. MRNFs are mostly asymptomatic and usually are incidentally detected by ophthalmoscopy. Clinically, MRNFs are usually connected to the optic nerve, with a 7.7% chance of bilateral involvement [1].

While MRNFs are typically regarded as benign and rare, it is important to note that several associations have been documented concerning visual field defects, myopia, amblyopia, and strabismus[1, 6–9]. Additionally, instances of MRNFs have been noted in correlation with systemic anomalies such as optic disc drusen, Gorlin syndrome or neurofibromatosis[10–15].

However, the majority of previous studies were hospital-based and had limited sample sizes. Therefore, it is crucial to understand the potential correlates of MRNFs and to conduct comprehensive population-based investigations. Consequently, we undertook this investigation to explore the prevalence, clinical characteristics, and concomitant systemic and ocular determinants of MRNFs within a substantial cohort representative of the general population.

The population of this study comes from the people undergoing health check-up at the Beijing Tongren Hospital Physical Examination Center, organized by their institutions or attended voluntarily for health checks. The study population included adults (age ≥ 18 years) undergoing health check-up from March 2017 to June 2020. Our study enrolled 10,341 participants, with an average age of 49.8 ± 15.0 years (range: 21–100 years), including 6,284 females (60.8%). The composition of the participants consisted of corporate staff (32.7%), hospital staff (35.0%), civil servants (20.8%), research personnel (5.5%), and others (6.0%)[16, 17].

The study protocol was approved by the Medical Ethics Committee of Beijing Tongren Hospital confirming that it was adherent to the Declaration of Helsinki. All participants underwent systemic examinations, and a comprehensive ophthalmic examination. Basic systematic data measurement: It included height, weight, waist and hip circumferences, blood pressure, pulse rate, and electrocardiogram. Blood pressure was measured in accordance with the guidelines of the World Health Organization /International Society of Hypertension. The blood pressure examination was conducted by one or two trained personnel. Participants must sit quietly for at least 5 minutes before the examination.

Fasting peripheral blood was drawn for the testing of relevant data, including differentiated blood cell counts and biochemical tests, which included serum glucose, urea nitrogen, creatinine, uric acid, transaminases, bilirubin, bile acids, high-sensitivity C-reactive protein, and lipids (triglyceride fatty acid, total cholesterol, high density lipoprotein, low density lipoprotein, lipoprotein).

The ophthalmologic examinations, conducted by professional technicians and ophthalmologists, encompassed assessments such as measurement of best-corrected visual acuity (BCVA), noncontact tonometry, and slit lamp-based biomorphometry of both the anterior and posterior segments of the eye.

Trained technicians used a color fundus camera (Fundus camera Type Topcon TRG-NW7SF, Topcon, Tokyo, Japan; or Fundus camera Type CR6-45NM, Canon Inc., USA) to perform fundus photography on all participants under non-mydriatic conditions, obtaining retinal images of both eyes. our fundus images were centered between optic disc and fovea. If any abnormalities were found in the fundus, photographs were taken of the quadrant where the abnormality was located (Fig. 1).

Body Mass Index: weight (kg) / height squared (m²). Waist-Hip Ratio: waist circumference (cm) / hip circumference (cm). Hypertension Diagnostic Criteria: systolic blood pressure ≥ 140mmHg and/or diastolic blood pressure ≥ 90mmHg, or previously diagnosed with hypertension or currently on antihypertensive medication. Diabetes Diagnostic Criteria: fasting blood glucose ≥ 7.0 mmol/L, or previously diagnosed with diabetes, or current use of glucose-lowering medications (oral hypoglycemic agents or insulin).

Diagnostic Criteria for MRNFs: visible white or grayish-white patches on the retina with blurred, feather-like boundaries, obscuring the retina and causing the underlying vessels to appear blurred[3, 18]. All fundus photos from the Beijing Tongren Hospital Health Examination Study were independently analyzed by two experienced ophthalmologists (Pan Zhe, Xu Jie) to identify patients with MRNFs. For inconsistent results, the two ophthalmology professionals discussed the images together a second time to reach a unanimous diagnosis.

Statistical analysis was performed using the SPSS statistical software package SPSS 26.0 (SPSS for Windows, version 26.0, IBM-SPSS, Chicago, IL, USA). Mean values (expressed as mean ± standard deviation) were calculated for the primary parameters. Univariate logistic analysis: Using the presence of MRNFs as the dependent variable, with other ocular and systemic factors as independent variables. Multivariate analysis: Using the presence of MRNFs as the dependent variable, with ocular and systemic factors that showed significant association in the univariate analysis as independent variables. Variables no longer meeting the analysis criteria due to collinearity with other parameters, or no longer significantly associated, were removed using a stepwise elimination method. Odds ratio (OR) and 95% confidence intervals (CIs) were calculated. All P-values were based on two-sided tests and considered significant if less than 0.05.

This study included 10,341 adults who underwent health examinations at the Beijing Tongren Hospital Physical Examination Center from March 2017 to June 2020, with a mean age of 49.8 ± 15.0 years (range: 21–100 years). 97 individuals were excluded from the study due to unreadable fundus photographs because of image blurring or other reasons. Ultimately, 10,244 individuals (20,488 eyes) were included in the study, with a mean age of 49.5 ± 14.8 years (21–100 years), and 6,225 of them were women (60.8%). The mean uncorrected visual acuity (UCVA) was 0.6 ± 0.36 (0.4–1.20), the mean BCVA was 0.8 ± 0.36 (0.4–1.20), and the mean intraocular pressure (IOP) was 14.3 ± 3.2 mmHg (7-41mmHg).

In our study, MRNFs were identified in 73 eyes of 66 patients, with a prevalence rate of 0.6 ± 0.3% (95% CI: 0.56–0.73) among people and 0.3 ± 0.2% (95% CI: 0.32–0.40) among eyes. The mean age of the patients was 51.9 ± 13.2 years, ranging from 29 to 91 years, and included 34 females (51.5%). The age and sex distribution of patients with MRNFs is detailed in Table 1. There was no significant difference in prevalence between male and female patients (0.8% and 0.5% respectively, P = 0.122).

Table 1

Age Distribution and Prevalence of Patients with MRNFs.
Age (years)	Participants (n)	MRNFs (n)	Prevalence (%)	95%CI
Below 40	3343	16	0.5	0.4, 0.6
40–49	2249	15	0.7	0.5, 0.9
50–59	1911	15	0.8	0.6, 1.0
60–69	1737	14	0.8	0.6, 1.1
Above 70	1004	6	0.6	0.4, 0.9
Total	10244	66	0.6	0.6, 0.7

The fundamental ocular conditions of the affected eyes, including UCVA, BCVA, and IOP, are presented in Table 2. Among the 66 patients with MRNFs, 89.4% individuals had unilateral involvement, while 10.6% had bilateral involvement. In total, 86 MRNF lesions were found in the 73 affected eyes. Single lesions were present in 64 eyes (87.7%), and multiple lesions (2–4) were found in 9 eyes (12.3%). Specially, 6 eyes had 2 lesions, 2 eyes had 3 lesions, and 1 eye had 4 lesions (Table 3).

Table 2

Basic Ocular Conditions of Eyes with MRNFs.
Parameter	Mean	Standard Deviation	Minimum	Maximum
Uncorrected Visual Acuity	0.60	0.37	0.04	1.20
Corrected Visual Acuity	0.83	0.23	0.40	1.20
Intraocular Pressure (mmHg)	14.2	3.4	9.0	27.0

Table 3

Distribution of Lesions in Eyes with MRNFs.
Lesion (n)	Eyes with MRNFs (n)	Frequency (%)
1	64	87.7
2	6	8.2
3	2	2.7
4	1	1.4
Total	73	100

MRNF was classified based on the relationship between MRNF patches and the optic disc. Among the 73 eyes, 53 eyes (72.6%) had 66 lesions connected to the optic disc. These lesions were further categorized by their location relative to the optic disc, as shown in Table 4: superior, inferior, nasal, temporal, and peripapillary (surrounding the optic disc by more than 180 degrees). Meanwhile, 20 eyes (27.4%) had 20 lesions not connected to the optic disc. These were classified based on their direction relative to the retinal vascular arcades, as listed in Table 4: superior temporal, inferior temporal, superior nasal, and inferior nasal.

Table 4

Location Distribution of MRNFs.
Lesion Location	Lesions (n)	Frequency (%)
Connected to the Optic Disc
Inferior	23	34.8
Superior	20	30.3
Nasal	10	15.2
Temporal	7	10.6
Peripapillary	6	9.1
Not Connected to the Optic Disc
Inferior Temporal	11	55
Superior Nasal	5	25
Superior Temporal	3	15
Inferior Nasal	1	5

Two eyes (in two individuals) were found to have extensive MRNFs, with lesions connected to the optic disc and not involving the macular fovea. The vision and IOP of the affected eyes were essentially normal (Fig. 2A and B). In our study, 5 eyes with MRNFs also had other ocular abnormalities: 1 eye had concurrent diabetic retinopathy, 1 eye had ocular hypertension, and 3 eyes had glaucomatous optic neuropathy (Fig. 2C and D).

Univariate analysis showed that the prevalence of MRNFs was positively correlated with higher systolic blood pressure (P = 0.013, OR: 1.105, 95% CI: 1.003, 1.027), but not significantly associated with age, or other systemic factors such as weight, diastolic pressure, heart rate, hypertension, diabetes, alkaline phosphatase concentration, total cholesterol level, height, blood glucose concentration, C-reactive protein level, lipoprotein level, triglyceride level, low density lipoprotein cholesterol level, and high density lipoprotein cholesterol level (Table 5); also not significantly associated with UCVA (P = 0.521), BCVA (P = 0.860) and IOP (P = 0.569) .

Table 5

Results of Univariate Analysis on Prevalence of MRNFs and Systemic Factors.
	Univariate Analysis			Age-Adjusted Univariate Analysis
Parameter	P-value	Regression Coefficient B	95.0%CI	P-value	Regression Coefficient B	95.0%CI
Age (years)	0.180	1.011	0.995, 1.027	/	/	/
Sex (Male/Female)	0.125	1.461	0.900, 2.372	0.149	1.429	0.880, 2.323
Weight (kg)	0.161	1.013	0.995, 1.031	0.149	1.013	0.995, 1.032
Height (cm)	0.241	1.018	0.988, 1.048	0.154	1.022	0.992, 1.052
Heart Rate (bpm)	0.173	0.978	0.948, 1.010	0.172	0.978	0.948, 1.010
Hypertension (Yes/No)	0.191	0.722	0.442, 1.177	0.478	0.813	0.459, 1.440
Diabetes (Yes/No)	0.185	0.654	0.349, 1.226	0.365	0.734	0.376, 1.433
Systolic Blood Pressure (mmHg)	0.013	1.105	1.003, 1.027	0.042	1.015	1.001, 1.029
Diastolic Blood Pressure (mmHg)	0.055	1.021	1.000, 1.043	0.082	1.019	0.998, 1.042
Creatinine (mmol/L)	0.333	1.003	0.997, 1.010	0.475	1.003	0.995, 1.010
Lipoprotein (mmol/L)	0.890	1.001	0.990, 1.011	0.975	1.000	0.990, 1.011
Glucose (mmol/L)	0.833	1.018	0.863, 1.200	0.887	0.987	0.822, 1.185

Age-adjusted univariate analysis revealed that the prevalence of MRNFs was positively correlated with higher systolic pressure, with no significant association with sex or other systemic factors (Table 5).

In the multivariate analysis, the prevalence of MRNFs was used as the dependent variable, with ocular and systemic factors identified in the univariate analysis as independent variables (P < 0.10). A stepwise elimination method was used to remove variables no longer associated with the prevalence of MRNFs, resulting in the sequential removal of age (P = 0.782), diastolic pressure (P = 0.584), and alkaline phosphatase concentration (P = 0.209) due to lack of significant association. The prevalence of MRNFs was positively correlated with higher systolic pressure (P = 0.025, OR: 1.014, 95% CI: 1.002, 1.026).

From March 2017 to June 2020, a total of 10,244 participants who met the criteria and with readable fundus photographs were enrolled at the Beijing Tongren Hospital Health Examination Center, with 66 patients diagnosed with MRNFs, yielding a prevalence rate of 0.6 ± 0.3% (95% CI: 0.56–0.73). The prevalence of MRNFs in the population ranges from 0.4–1% [1–5]. Despite being a societally based study, the large sample size makes it one of the most substantial community-based population studies to date. The prevalence rate of MRNFs in this study was 0.6%, which is consistent with the prevalence rates reported in previous literature[3, 18, 19].

Straatsma and colleagues diagnosed 39 individuals (42 eyes) with MRNFs out of 3968 autopsies conducted in the United States, yielding a prevalence of 1%[1]. Kodama and colleagues studied 5789 ophthalmology outpatients at Shimane Medical University Hospital in Japan from 1980 to 1988, diagnosing 33 individuals (35 eyes) with MRNFs through posterior pole photographs, with a prevalence of 0.6%[19]. Elabaz and colleagues found 51 individuals (55 eyes) with MRNFs among 12,906 participants through fundus photography in a local population study in Goettingen, Germany, with a prevalence of 0.4%[20]. Nangia and Jonas diagnosed 46 individuals (52 eyes) with MRNFs among 4485 people in a central Indian population study using fundus photographs, with a prevalence of 1%[18]. The results of the above studies are essentially consistent with those of our study.

Past reports indicate that the probability of bilateral involvement of MRNFs ranges from approximately 7.7–13.0%[1, 18–20]. Straatsma and colleagues found through autopsy that the rate of bilateral disease of MRNFs was 7.7%; Kodama's study in Japan reported a bilateral disease rate of 7.8%; Nangia and Jonas reported a 13.0% rate of bilateral disease of MRNFs in a central Indian population. In this study, among the 66 patients identified during health examinations at Beijing Tongren Hospital, 73 eyes had MRNFs. Out of these, 59 individuals had unilateral involvement, and 7 had bilateral involvement, with a probability of 10.6% for bilateral MRNFs.

Yang Shen and its team, along with Straatsma and colleagues, described that eyes with MRNFs often present with axial myopia, anisometropia, and amblyopia[1, 21], with no significant improvement in vision after treatment for amblyopia. The reason why MRNFs cause axial myopia is not clear, but Moradiand and others speculate that the MRNFs, being opaque, obscures the retina, blurs retinal imaging, and leads to deprivation amblyopia. This form of deprivation amblyopia can cause an increase in the axial length of the eye, resulting in myopia during critical periods of visual development. On the other hand, the elongation of the eye's axial length might also cause the formation of myelin sheaths on retinal nerve fibers. In axial myopia, the elongated lamina cribrosa allows the myelin to extend through an incomplete lamina to the optic disc and retina, forming MRNFs[22]. Straatsma and colleagues found that about 10% of patients with MRNFs have myopia, amblyopia, and anisometropia[21]. In our study, the two patients with extensive MRNFs had essentially normal vision. One patient's vision and IOP were (UCVA 1.0, IOP 10 mmHg), and the other eye was (UCVA 0.6, BCVA 1.0, IOP18 mmHg). The second patient had MRNFs in the left eye and myopia in both eyes (right eye UCVA 0.6, BCVA 1.0; left eye UCVA 0.7, BCVA 1.0), with BCVA at 1.0 for both, and no anisometropia or amblyopia. As Moradiand's theory, the MRNFs in the two patients in our study likely did not affect the macular region, preventing form-deprivation amblyopia and consequently not leading to ipsilateral axial myopia, anisometropia, or amblyopia.

Nangia and Jonas found a positive correlation between the prevalence of MRNFs and hyperopia, with no significant association with age, BCVA, IOP, optic disc area, glaucomatous optic atrophy, or early age-related macular degeneration[18]. Elabaz and colleagues discovered a positive correlation between the prevalence of MRNFs and a history of stroke, with no significant correlation to age, sex, glaucoma, diopter, IOP, BCVA, or central corneal thickness. They speculated that stroke may cause defects in the lamina cribrosa, allowing oligodendrocytes to pass through to the retina and form myelin sheaths; another theory suggests that myelin regeneration may occur after recovery from central nervous system white matter ischemia. The regeneration of myelin might result from increased expression of growth factors and genes for proteolipid proteins that form myelin in the central nervous system, thus explaining why patients with stroke or cerebral ischemia are prone to developing myelinated retinal nerve fibers[20]. Our study found a positive correlation between the prevalence of MRNFs and higher systolic pressure in patients. It is widely accepted that high systolic blood pressure is a clear risk factor for stroke, possibly consistent with Elabaz's results, elevated blood pressure may play a role in damaging the lamina cribrosa, allowing oligodendrocytes to pass through to the retina and to the development of MRNFs. On the other hand, the optic nerve head is subjected to a complex and dynamic biomechanical environment, influenced by blood pressure, IOP anteriorly, and retrolaminar tissue pressure and cerebrospinal fluid pressure posteriorly. Therefore, higher systolic blood pressure can significantly disrupt the dynamic biomechanical environment of the optic nerve head, potentially causing damage. The statistical results may require further evaluation with expanded samples and enriched clinical data due to our limited ocular examinations and systemic information, lack of patient stroke history, and absence of refractive and axial length data.

Our study also has certain limitations. Firstly, in any community research, the selection of the population may affect the results and introduce bias. Although our sample size was large, with 10,244 participants, there is still a certain deviation between the cohort participating in physical examinations and the general population base. Secondly, since the health examination center did not conduct optical coherence tomography for people undergoing health checks, we were unable to assess changes in the thickness of MRNFs. Thirdly, due to the fundus photography covering only one field of view, some myelinated retinal nerve fibers were not completely captured, making it impossible for us to quantify the area of the MRNFs and potentially overlooking peripheral myelinated nerve fibers. Fourthly, since all participants in this study were adults, we were unable to observe the clinical characteristics and changes of MRNFs in adolescents or children. Lastly, this is study also lacks observations on the trends of examination date changes in MRNF patients due to cross-sectional study. A follow-up study of 5 to 10 years is needed, and more analysis and research should be conducted in the future.

The prevalence of MRNFs was 0.6% in this community-based study of a healthy Chinese population. They were associated with higher systolic blood pressure, but no significant associations were found with UCVA, BCVA, or IOP. Extensive MRNFs may still allow for normal visual function as long as they do not cover the macular fovea.

MRNFs	Myelinated retinal nerve fibers
OR	Odds ratio
CIs	Confidence intervals
UCVA	Uncorrected visual acuity
BCVA	Best corrected visual acuity
IOP	Intraocular pressure

Funding:

Supported by the Major Research Plan of the Ministry of Science and Technology of the Peoples’ Republic of China (No. 2023YFC2506104).

Author Contribution

Zhe Pan, Chun Zhang, Dongning Chen designed this study.Dongning Chen and Jie Xu collected data.Zhe Pan, Haocheng Xian，Jinyue Dai have analyzed data.Zhe Pan, linyun Gong, Can Can Xue, Chun Zhang have drafted the work or substantively revised it

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No competing interests reported.

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Prevalence and Clinical Characteristics of Myelinated Retinal Nerve Fibers in a Healthy Population: A Big-data Analysis

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