Review ArticleReviewsR

Optical Coherence Tomography of Choroid in Common Neurological Diseases

FEDERICO DI STASO, MARCO CIANCAGLINI, SOLMAZ ABDOLRAHIMZADEH, FABIAN D'APOLITO and GIANLUCA SCUDERI
In Vivo September 2019, 33 (5) 1403-1409; DOI: https://doi.org/10.21873/invivo.11617

Abstract

The choroid is involved directly and indirectly in many pathological conditions such as age-related macular degeneration, myopia-related chorioretinal atrophy and central serous chorioretinopathy. Optical coherence tomography (OCT) has gradually become a fundamental part of modern resources in the hands of ophthalmologists. The enhanced depth imaging technique and swept-source OCT make a great contribution to conventional in vivo choroid assessment. This review focuses on the most common neurological conditions in which choroid assessment by OCT may provide help in early diagnosis and be used as an interdisciplinary follow-up tool. In order to avoid evaluation biases and misdiagnosis, the main and most common physiological and para-physiological conditions in which the choroid may show alterations are also reviewed.

Optical coherence tomography (OCT) has gradually become a fundamental part of modern resources in the hands of the ophthalmologists. As this technology improves, the nature of the choroid layer of the eye is becoming clearer and better characterized. The choroid vascular section consists of two parts: the outer layer of larger blood vessels called Haller's layer; and the inner layer of smaller arteries, arterioles and veins dedicated to the capillary network called Sattler's layer.

Considering unit per weight, the choroid has the highest blood flow ratio of all anatomical structures (1). The choroid is the only metabolic source for the avascular zone of the fovea (2). It also responsible for the vascular supply of the retinal pigment epithelium and outer retinal layers; furthermore, some portion of the optic nerve may also be supplied by the choroid (3).

The choroid is involved directly and indirectly in many pathological conditions such as age-related macular degeneration (4), myopia-related chorioretinal atrophy (5), central serous chorioretinopathy (6) and others, mostly because any choroid anomaly may lead dysregulation of blood flow and blood supply, with consequent photoreceptor death and vision loss (7).

The enhanced depth imaging technique (EDI) and swept source (SS) OCT have made a great contribution to conventional in vivo choroid assessment (8, 9), once achievable only through indocyanine green angiography and ultrasonography, both methods limited by low repeatability and low image resolution (10).

In 2016, Tan et al. showed in their review that any vascular disease can hypothetically affect the choroid (11) and tried to identify health conditions for which the choroid can be used as an indicator of systemic involvement.

This review focuses on the most common neurological conditions in which choroid assessment by OCT may provide help in early diagnosis or be used as an interdisciplinary follow-up tool.

In order to avoid evaluation biases and misdiagnosis, the following section reviews the main and most common physiological and para-physiological conditions in which the choroid may show alterations: Gender, age-related and circadian choroid variability.

Gender Choroid Variability

A large number of studies have reported statistically significant differences between males and females in choroidal thickness/volume. In 2011, Li et al. reported a higher choroidal thickness in males than in females (12), similar to the results of two other studies conducted in 2012 by Barteselli et al. (13) and Zeng et al. (14). A large study conducted by Wei et al. in 2013, involving more than 3,000 individuals, showed male gender to be associated with a thicker choroid, in particular, the mean subfoveal choroidal thickness was 254±107 μm. It is also worth mentioning that the mean age of the study subjects was 65 years (15). In contrast, in 2014, Sanchez-Cano et al. showed no statistically significant difference between genders (16); in the same year, Ruiz Medrano et al. Similarly found no difference. It is important to note that this study was conducted using SS-OCT (17). In 2015, other studies (18, 19) once again showed that the choroid is thicker in males than females using/comparing SD-OCT data.

In conclusion, the difference in choroidal thickness between males and females should be considered when studying the choroid layer, taking into account that different techniques may lead to different results.

Age-related Choroid Variability

One of the main factors influencing the choroidal thickness seems to be age. In 2009, Margolis et al. studied the choroidal thickness of more than 50 healthy eyes at various points using the EDI OCT technique. The results showed a 15.6 μm subfoveal decrease in choroidal thickness for each decade of life (20). In 2010, Ikuno et al. showed a significant negative association between choroidal thickness and age in healthy Japanese (21). In the same year, Manjunath et al. found a trend for an age-related decrease in choroidal thickness in testing 34 participants (22). In 2012, Barteselli et al. demonstrated a negative correlation between age and axial length (13). Furthermore, in 2014, Rhodes et al. showed a lower age-related choroid peripapillary thickness in a group of African descent and one of European descent (23). In 2015, Gupta and colleagues analyzed more than 500 participants ranging in age from 45 to 85 years using new automated choroidal segmentation software in order to provide the best reliability. In a multiple linear regression model, younger age was significantly associated with a thicker subfoveal choroid (24).

Circadian Choroid Variability

Choroidal thickness seems to be subject to diurnal variations. In 2011, Chakraborty et al. observed significant variation in choroidal thickness during the day, with no difference between myopic and emmetropic patients; the choroid was found to be thinner in the morning (25). In 2012, Tan et al. found a significant diurnal choroidal thickness variation with mean diurnal difference of 33.7 μm associated with a progressive decrease from 9 a.m. to 5 p.m. (26).

Another similar study conducted by Usui et al. showed a similar pattern of variation in thickness in 38 eyes of 19 healthy volunteers (27). In contrast, during the same year, Toyokawa et al. found that the diurnal variation of choroidal thickness may be insignificant in some individuals and variable in others, however, with good correlation between their two eyes (28). In 2013, Osmanbasoglu et al. again reported no significant variation choroidal thickness from 9 a.m. to 4 p.m. (29). Since there is no consensus on the choroid diurnal variation, assessing choroidal thickness at different times in the same individual may help to find a hypothetic pattern in individual variation.

Materials and Methods

Literature search. MEDLINE/PubMed was the primary database source used for this research. Terms pertinent to OCT of the choroid in neurological diseases were used (e.g. OCT choroid, choroid, Alzheimer, dementia, Parkinson, multiple sclerosis, phacomatosis, neurological disease) as well as abbreviations, synonyms and alternative spellings (e.g. phacomatosis). The final search was performed on 16th March 2019.

Results

Alzheimer's disease. Alzheimer's disease (AD) is a common pathology and the most common form of dementia (30). In the last years, many causes and mechanisms have been elucidated in the pathogenesis of this disease, such as microvascular factors (31).

Given that many embryological, physiological and even anatomical properties are shared between cerebral small vessel circulation and retinal circulation (32), many authors have conducted extensive studies in order to find correlation between choroidal thickness and AD. Bayhan et al. in 2014 used an RTVue OCT system to obtain, among other parameters, the choroidal thickness with a cross line retinaI scan pattern, analyzing the chorioretinal interface adjacent to the zero delay zone of 31 consecutive patients with AD and 30 controls (33). The mean measurements of choroidal thickness at each location were significantly lower in patients with AD than controls, except measurements 3.0 mm temporal to the fovea (p=0.067).

The study conducted by Gharbiya et al. (34) on 42 eyes of 21 patients (mean age=73.1±6.9 years) with a diagnosis of mild to moderate AD and 42 eyes of 21 age-matched controls (34) was performed using spectral domain (SD)-OCT images obtained by EDI modality. All measurements were made of the subfoveal choroid, at 500 and 1,500 μm starting from the center of the fovea. The choroidal thickness was significantly thinner at each zone in those with AD than in control eyes (p<0.05).

In 2016, Bulut et al. used EDI-OCT to study the choroidal thickness in patients with AD and in patients with mild cognitive impairment (Figure 1) (35). Mild cognitive impairment is considered a transitional phase towards dementia, with a similar pathogenesis to that of AD (36). The measurements were obtained from the outer edge of the hyper-reflective retinal pigment epithelium to the inner sclera at seven locations: at the fovea; at 500, 1,500, and 3,000 μm temporal to the fovea; and at 500, 1,500, and 3,000 μm nasal of the fovea. Each measurement was repeated three times in order to calculate the average value. There was statistically significant choroidal thinning in AD and patients with mild cognitive impairment compared to the controls.

Figure 1.
Figure 1.

Measurement of choroidal thickness in healthy (top) and patients with Alzheimer's disease (bottom) revealed a statistically significant difference at each location (35).

Another important aspect is atrophy of choroidal capillaries due to normal aging (37). This may lead to doubts about choroidal thinning in patients with AD patients since in the majority of cases, the patients under consideration are elderly. Cunha et al. in 2017 (38) used the SD-OCT in EDI mode to examine 50 patients with a diagnosis of mild AD (mean age=73.1 years), 152 patients without AD (mean age=71.03 years), and 50 elderly without AD (mean age=82.14 years). In the patients with AD, the choroidal thickness was lower in all the examined locations (p<0.001) compared with the age-matched, and elderly groups. Choroidal thinning was even more pronounced temporally to the fovea. Choroidal thinning was found to be more pronounced in elderly compared to younger patients (38); nonetheless, in patients with AD, the choroid was significantly thinner even when compared with an elderly control group.

Parkinson's Disease

The second most common neurodegenerative disease affecting the central nervous system is Parkinson's disease (PD). Although the causes remain unknown, there is progressive degeneration of extrapyramidal dopaminergic neurons. Common findings are Lewy bodies accumulated in the central, peripheral and autonomic nervous system (39). Eraslan et al. hypothesized in 2016 that a choroidal involvement in PD may be due to blood flow irregularities or phenomena of atrophy. They examined the lamina cribrosa and choroidal thicknesses in 44 eyes of 22 patients with PD and 50 eyes of 25 healthy individuals using EDI-OCT (40). The choroidal thickness of the PD group was significantly less compared to the controls, in the subfoveal region, and 1.5 mm temporal and 1.5 mm nasal to the fovea. In 2017, Moschos and Chatziralli used EDI-OCT to analyze the retinal and choroidal thickness of 31 patients with PD compared to 25 healthy controls. The results were similar to those of Eraslan et al., showing a statistically significant thinning in all the examined zones: nasal, temporal, inferior and superior at 1.5 mm and 3 mm from the fovea. According to the authors, the large difference in choroidal thickness between the PD and control groups gives more credit to the involvement of vascular changes besides the neurodegenerative process, both potentially responsible for clinical risk and disease progression (41).

In 2018, Satue et al. used different resources to investigate choroidal thickness in patients with PD SS-OCT (42). Fifty eyes of 50 patients were examined and compared to 54 eyes of 54 healthy controls following the macular) and peripapillary area. They showed that the EDI SD-OCT technique has a limited reliability, mostly because the inner and outer border of the choroid are determined manually by the observer; furthermore, SS-OCT, can easily overcome the choroid light scattering (43) of SD-OCT. The final results showed a thickened macular and peripapillary choroid, in contrast to the previous studies. Although vascular changes may be involved (44), the authors themselves suggest alterations in perivascular connective tissue density as a cause and not hypoperfusion alone.

Multiple Sclerosis

Multiple sclerosis (MS) is a disease with inflammatory and chronic axonal demyelination and subsequent degeneration, which may involve the optic nerve (45-47). Esen et al. in 2015, conducted a study on choroidal vascular changes in MS-affected patients using EDI-OCT (48). The study was conducted taking into account and comparing a positive or negative history/clinical report of optic neuritis episodes. Each measurement was taken at the fovea and at 500-μm intervals temporal and nasal to the fovea up to a total of six intervals per patient. The choroidal thickness at all measured locations was significantly less in patients with MS compared to healthy controls regardless of history of optic neuritis. The authors suggested that choroidal thinning may be the result of a perfusion impairment due to a systemic inflammatory response (49). It has been hypothesized that endothelin-1 (ET1), found to be increased in patients with MS (50), may play a role in this scenario, given its vasoconstrictive effect.

Phakomatoses

Phakomatoses are a group of hereditary multisystem disorders characterized by a pattern of inheritance, variable severity and higher risk of malignant transformation (51) and include neurofibromatosis, tuberous sclerosis and von Hippel Lindau disease (52). These three neurocutaneous diseases share the same aforementioned characteristics and can be defined as true phacomatoses (53).

Neurofibromatosis type I (NF1) is an autosomal dominant disease due to 17p11.2 gene deletion or suppression (54), with several ophthalmic features included in the diagnostic criteria such as Lisch nodules and optic glioma (55). It is often difficult to find choroidal alteration via fundus examination in NF1, on the other hand, the use of the OCT may show choroidal nodules whose number is correlated with the number of Lisch nodules on the iris (56). In 2012, Viola et al. found choroidal nodules in 82% of 190 examined eyes using near-infrared reflectance (NIR) and proposed choroidal nodules be included in the diagnostic criteria for NF1 (57). Many other choroidal features have been found using OCT, such as thickness changes in the retina overlying the nodules (58) and loss of lucency in the choroid over nodules (59). From the point of view of choroidal thickness, Abdolrahimzadeh et al. showed generalized choroidal and retinal thinning in patients with NF1 (60). Furthermore, in the same study, NIR-detected nodules were shown to be related to two different types of hyper-reflective choroidal nodules detected by EDI-OCT: round-shaped and well-defined NIR nodules with dome-shaped hyper-reflective alteration on EDI-OCT, and poorly defined NIR nodules with flat, irregular nodules on EDI-OCT.

Tuberus sclerosis complex is a genetic disorder due to TSC complex subunit 1 (TSC1) and TSC2 gene mutations characterized by shagreen patches, facial angiofibroma, ungula fibroma, skin lesions, cortical tubers and retinal lesions (61). Sometimes additional features may be present such as epilepsy, mental retardation, autism and other behavioral disorders (62). The retinal lesions are defined as retinal astrocytic hamartomas, identifiable in approximately 50% of patients (63-65). In 2016, Pichi et al. classified these hamartomas into four groups using SD-OCT (66), taking into consideration morphology, retinal layer involvement, tumor margins and other parameters. To the best of our knowledge, there are no specific choroidaI alteration in tuberus sclerosis complex.

von Hippel Lindau disease is an autosomal dominant genetic disease due to 3p25-26 tumor-suppressor gene variation (52). The most common presentation of this condition is the presence of vascular tumors of the central nervous system (hemangioblastoma) and retinal capillary hemangioblastoma (53). The most common and early presentation is retinal hemangioblastoma, which may occur in up to 85% of cases (67) and it is made up of capillary spaces with pericytes and stromal cells. Shields et al. showed and described the main OCT characteristics of retinal hemangioblastoma (68) but there are not enough data in literature about choroidal involvement.

Sturge–Weber Syndrome

Sturge–Weber syndrome is a neuro-oculo-dermal disease that affects the normal development of certain blood vessels in the brain, skin and eyes from birth (69). Choroidal hemangioma is a frequent condition in this syndrome; it may cause choroidal thickening and a diffuse red appearance on fundus examination (70). In 2016, Abdolrahimzadeh et al. studied 12 patients with Sturge–Weber syndrome and found that the overall mean choroidal thickness in affected and fellow eyes was significantly higher than in control eyes (266.5 μm) (71). To the best of our knowledge, there are no other reports in literature about the choroidal thickness comparing between patients with Sturge–Weber syndrome and healthy controls.

Conclusion

Difference in choroidal thickness between males and females should be considered when studying the choroidal layer, even age seems to play a role in subfoveal choroidal thickness because a younger age is associated with a thicker subfoveal choroid. In AD, many authors have conducted extensive studies in order to find a correlation between choroidal thickness and this pathology. In AD, the choroid was thinner even when compared with a control group of advanced age. In patients with Parkinson's disease, the choroid was thinner as long as the EDI-OCT method was used. Using SS-OCT the results showed a thickened choroid in patients with Parkinson's, showing that different techniques may lead to different results.

In MS, the choroid seems to be thinner but literature is scarce. Patients with phakomatoses may show several alterations on OCT but from the point of view of choroidal thickness, the choroid was thicker in neurofibromatosis type 1. Even in this case, the literature is scarce. For tuberous sclerosis complex and von Hippel Lindau syndrome, there are not enough data in literature to establish a general consensus about choroid thickness.

In Sturge–Weber syndrome the literature is limited, however, choroid thickness seems to be significantly higher compared to controIs.

OCT technology has become a fundamental instrument in the hands of the ophthalmologist, this is why the choroid layer is becoming increasingly more characterized. Despite constant progress in OCT technology and diagnostic capabilities, certain fields remain unclear. In neurological diseases, OCT may play an important role as a diagnostic and follow-up tool. In common neurological pathologies, such as AD and Parkinson's disease, the literature offers limited, but good resources for better understanding choroidal characteristics on OCT. In rare pathologies, such as phakomatosis, the literature is too limited and further studies are needed.

Footnotes

  • This article is freely accessible online.

  • Received May 14, 2019.
  • Revision received July 7, 2019.
  • Accepted July 12, 2019.

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Optical Coherence Tomography of Choroid in Common Neurological Diseases
FEDERICO DI STASO, MARCO CIANCAGLINI, SOLMAZ ABDOLRAHIMZADEH, FABIAN D'APOLITO, GIANLUCA SCUDERI
In Vivo Sep 2019, 33 (5) 1403-1409; DOI: 10.21873/invivo.11617
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