Choriocapillaris: Fundamentals and advancements

doi:10.1016/j.preteyeres.2021.100997

Progress in Retinal and Eye Research

Volume 87, March 2022, 100997

https://doi.org/10.1016/j.preteyeres.2021.100997 Get rights and content

Abstract

The choriocapillaris is the innermost structure of the choroid that directly nourishes the retinal pigment epithelium and photoreceptors. This article provides an overview of its hemovasculogenesis development to achieve its final architecture as a lobular vasculature, and also summarizes the current histological and molecular knowledge about choriocapillaris and its dysfunction. After describing the existing state-of-the-art tools to image the choriocapillaris, we report the findings in the choriocapillaris encountered in the most frequent retinochoroidal diseases including vascular diseases, inflammatory diseases, myopia, pachychoroid disease spectrum disorders, and glaucoma. The final section focuses on the development of imaging technology to optimize visualization of the choriocapillaris as well as current treatments of retinochoroidal disorders that specifically target the choriocapillaris. We conclude the article with pertinent unanswered questions and future directions in research for the choriocapillaris.

Introduction

The choroid is the most vascular structure of the eye and has the highest blood flow per unit weight compared to any other tissue in the body (Alm and Bill, 1973). While the choroid has always been of considerable scientific and clinical interest, the recent dramatic increase in the number of publications on choroid is attributable in part to recent advances in imaging technology. Within the choroid, the choriocapillaris plays a critical role in supplying oxygen and nutrition to the outer retinal cells. In this review article, we comprehensively discuss the anatomy, histology, and physiology of the choriocapillaris with a particular emphasis on multimodal imaging. This overview is followed by an in-depth discussion on future avenues for investigation and therapeutic interventions. We conclude our review with pertinent research inquiries for choriocapillaris investigators that may provide insight and advancement for the overall vision science community.

Section snippets

From choroid to choriocapillaris

The choroid is a layered vasculature that provides oxygen and nutrients to the outer retina. It is located between the sclera and the retina, sitting directly below Bruch's Membrane (BM). The majority of the choroid is characterized by its layered vasculature, with stromal tissue occupying only about 20% of its volume (Sohrab et al., 2012). The structure of the choroid is divided into three layers of blood vessels; these layers are classified based on the diameter of the blood vessels. The

Axial length change

Induced myopia leads to compensatory choroidal thickening whereas induced hyperopia is characterized by thinning of the choroid with posterior displacement of the retina in chicks (Wallman et al., 1995). The choroid may also have a role in axial length regulation directly or indirectly via its effects on the sclera. It remains unclear whether the choroidal thickness is involved in emmetropic targets in humans. The regulation of choroidal thickness occurs via widening of capillary fenestrations,

Future imaging approaches

There are many questions which need to be answered about the choriocapillaris. These questions include whether choroidal circuit organization is serial or parallel, whether lobules are effective and if there are shunts between them; whether CNV originate from choriocapillaris, how the choriocapillaris blood flow is regulated, how RPE and the choriocapillaris enable co-survival of each other, and what are the unique features and of the peripheral choroid. Here are described the possible future

Arrangement of the choriocapillaris: is it lobular?

The anatomy of the choriocapillaris anatomy is still debated but the former idea of a continuous monolayer has grown controversial. The main description of the architecture of the choriocapillaris originates from histological studies. (“On Inflammation of the Choroid Coat,” 1830) However, the understanding of the choriocapillaris architecture has been studied using postmortem methods such as casts, as well as in vivo imaging such as fluorescein angiography (Ashton, 1952). The focal void induced

Conclusion

Even though the choriocapillaris represents a relatively small portion of the choroid in terms of volume, it plays an enormous role in the pathogenesis, evolution, and general history of retinochoroidal diseases. Our growing understanding of this unique vasculature will likely impact our overall understanding of many ocular conditions. Advances in imaging have provided novel opportunities to further evaluate the choriocapillaris for effective diagnosis and management in clinical practice. Thus,

Author statement

Raphael Lejoyeux: Writing - Original Draft, Methodology, Jennifer Benillouche: Writing - Original Draft, Joshua Ong: Validation, Writing - Review & Editing, Marie-Hélène Errera: Writing - Original Draft, Ethan A. Rossi: Writing - Original Draft, Resources, Sumit R. Singh: Writing - Original Draft, Kunal K. Dansingani: Validation, Writing - Review & Editing, Susana da Silvada Silvation, Writing - Review & Editing, Debasish Sinha: Validation, Writing - Review & Editing, José-Alain Sahel:

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Citation Excerpt :
The localized BM defects may lead to a local outpouching of the sclera, similar to the occurrence of scleral staphylomas in spatial association with congenital BM defects, as in the case of colobomas, or in association with acquired BM defects in non–highly myopic eyes, such as in the case of toxoplasmotic scarring (Jonas, JB and Panda-Jonas, 2016). The choriocapillaris is a dense, mono-layered capillary network, the basal membrane of which covers the posterior surface of BM (Jonas, JB et al., 2011; Lejoyeux et al., 2022; Schachat et al., 2017) (Fig. 3). The choriocapillaris is the inner layer of the choroid.
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¹: RL 14% JB 8% JO 3% MHE 8% EAR 7% SSR 4% KKD 7% SDS 3% DS 3% JAS 5% KBF 5% SSR 7% GAL 12% JC 14%.

View full text

Choriocapillaris: Fundamentals and advancements

Abstract

Introduction

Section snippets

From choroid to choriocapillaris

Axial length change

Future imaging approaches

Arrangement of the choriocapillaris: is it lobular?

Conclusion

Author statement

Funding

Am. J. Ophthalmol.

Am. J. Ophthalmol.

Am. J. Ophthalmol.

Am. J. Ophthalmol.

Exp. Eye Res.

Exp. Eye Res.

Am. J. Ophthalmol.

Ophthalmology

Am. J. Pathol.

Can. J. Ophthalmol.

Eur. J. Pharm. Biopharm.

Exp. Eye Res.

J. Contr. Release

Mol. Aspect. Med.

Exp. Eye Res.

Neurobiol. Aging

Am. J. Ophthalmol.

Am. J. Pathol.

Surv. Ophthalmol.

Am. J. Ophthalmol.

Microvasc. Res.

Microvasc. Res.

Ophthalmology

Identifying characteristic features of the retinal and choroidal vasculature in choroideremia using optical coherence tomography angiography

Eye

Sequential chorioretinal changes in presumed ocular histoplasmosis syndrome analyzed using spectral domain optical coherence tomography

Ocul. Immunol. Inflamm.

Optical coherence tomography angiography features of paradoxical worsening in tubercular multifocal serpiginoid choroiditis

Ocul. Immunol. Inflamm.

Optical coherence tomography angiography features of bilateral retinopathy associated with Chikungunya fever

Indian J. Ophthalmol.

Retinal vascular perfusion density mapping using optical coherence tomography angiography IN normals and diabetic retinopathy patients

Retina

The role of optical coherence tomography angiography in the diagnosis and management of acute vogt-koyanagi-harada disease

Ocul. Immunol. Inflamm.

Indocyanine green angiography in posterior uveitis

Indian J. Ophthalmol.

Corrosion casts and scanning electron microscopy of choroidal vasculature in rats with inherited hypercholesterolemia

Curr. Eye Res.

Choriocapillaris layer imaging with swept-source optical coherence tomography angiography in lamellar and full-thickness macular hole

Graefes Arch. Clin. Exp. Ophthalmol.

[Choroidal thickness after scleral buckling surgery in macula-off rhegmatogenous retinal detachment]

Ophthalmologe

Indocyanine green angiographic findings in a case of punctate inner choroidopathy

Eur. J. Ophthalmol.

Enhanced depth imaging optical coherence tomography of choroidal metastasis in 14 eyes

Retina

Quantitative OCT angiography of the retinal microvasculature and the choriocapillaris in myopic eyes

Invest. Ophthalmol. Vis. Sci.

Quantitative assessment of choriocapillaris flow voids surrounding choroidal neovascular membranes

Invest. Ophthalmol. Vis. Sci.

Swept-source optical coherence tomography angiography findings in Torpedo maculopathy

Ophthalmic Surg. Lasers Imaging Retina

Synchronized tissue-scale vasculogenesis and ubiquitous lateral sprouting underlie the unique architecture of the choriocapillaris

Dev. Biol.

Intussusceptive vascular remodeling precedes pathological neovascularization

Arterioscler. Thromb. Vasc. Biol.

The distribution of immunoglobulin in the rabbit eye

Arch. Ophthalmol.

Laser-induced macular holes demonstrate impaired choroidal perfusion

Retina

Endothelial cell proliferation in the choriocapillaris during human retinal differentiation

Br. J. Ophthalmol.

Blood flow and oxygen extraction in the cat uvea at normal and high intraocular pressures

Acta Physiol. Scand.

Comparison of retinal and choriocapillaris thicknesses following sitting to supine transition in healthy individuals and patients with age-related macular degeneration

JAMA Ophthalmol.

Subfoveal choroidal vascularity in myopia: evidence from spectral-domain optical coherence tomography

Ophthalmic Surg. Lasers Imaging Retina