The Anatomy of the Choroid – a Review

Revista Română de Anatomie funcţională şi clinică, macro- şi microscopică şi de Antropologie

Vol. XV – Nr. 4 – 2016 UPDATES

THE ANATOMY OF THE CHOROID – A REVIEW

Şt. Oprea1*, C.M. Pantu1, F.M. Filipoiu1, Raluca Tulin1, Gabriela Diana Oprea2 1. University of Medicine and Pharmacy “Carol Davila” Bucharest Discipline of Anatomy 2. Universitary Emergency Central Military „Carol Davila“ Hospital, Bucharest

THE ANATOMY OF THE CHOROID – A REVIEW (Abstract): The choroid is an important structure of the eye which can be involved in a lot of pathologies. Its great importance is given by functions like vascularization, thermoregulation and production of growth factors. A good knowl- edge of this element of the eye will help the ophthalmology specialists, especially the young ones, to understand better the pathological substrate of the diseases involving the choroid like diabetic retinopathy, age related macular degeneration wet form, choroid detachment etc. The choroid covers to the interior the fibrous tunic of the eye. It represents the posterior portion of the uvea, the anterior being represented by a thicker region, ciliary zone. Histological, choroid shows the 5 layers, from sclera to the retina: outer pigment layer, suprachoroid; two Vascular layers, one external (called Haller) and one internal, Sattler; choriocapillar layer and Bruch’s membrane. The choroid blood supply is ensured by posterior ciliary arteries (PCA), branches of the ophthalmic artery. Venous drainage is achieved through vorticity veins. Choroid’s Innervation is double, sympathetic and parasympathetic through dense perivascular plexus. Key words: THE CHOROID, DIABETIC RETINOPATHY, POSTERIOR CILIARY ARTERIES

INTRODUCTION optical ditches appear in the cranial neural The choroid represents the main structure folds. After merging neural folds, optical vesi- of the eye which ensures the blood supply of cles are formed, shaped as diverticula from the external layers of the retina, consisting for forebrain wall. After lens vesicles formation on the most part of it from blood vessels. Except the surface ectoderm, optic vesicles invaginate vascularization which is the main function, we and form the optic cups which present a double can mention other equally important functions: wall. The lens vesicles then enter the optical of thermoregulation, adjust retinal position in cavity cups. Mesenchymal surrounding the op- relation with choroidal thickness, production of tic cups differentiate to get an internal and an growth factors. These growth factors appear to external layer. The inner layer will form the play an important role in eye’s emmetropia, in choroid and the external layer the sclera. Mean- the processes of changing the form of the eye while with the development of choroid, the in order to correct the myopia or hyperopia. melanocyte precursors migrate from the neural One area still in research and incompletely crest toward the choroid (fig. 1). These precur- known is the relationship between growth fac- sors will differentiate into pigmented melano- tors and structure changes that occur in the cytes starting with 7-8 month of gestation (1). choroid (1). 2. Anatomy of the choroid ANATOMY AND DEVELOPMENT OF The choroid covers to the interior the fibrous THE CHOROID tunic of the eye. It represents the posterior por- 1. Development of the choroid tion of the uvea, the anterior being represented The choroid is the middle layer of the eye by a thicker region, ciliary zone. The two re- is located in the posterior uveal. Eye develop- gions are separated at the Equator of the eye ment starts at the end of the 4th week when by ora serrata, shaped as a scalloped line.

380 The Anatomy of the Choroid – A Review

Fig. 1. H.E. coloration ob. 4x. Sagittal section Fig. 2. Schematic representation of branching through the eye where can be seen the choroid pattern of medial and lateral PCAs. between the retina and the sclera, the cornea, the lens, the vitrous and the fibers of the optic nerve entering the retina. lateral and the rest of the PCA branches will form short PCAs, between 10 and 20. The medial and lateral PCAs ensure the blood supply for Choroid shows two faces: external which is the medial and lateral part of the choroid (2). convex and is solidarized with the sclera through PCAs branches will continue the branching vessels, ciliary nerves and lax connective tissue ensuring a systematic blood supply for the cho- (lamina fusca); internal is concave and that fits roid. Finally, each choroidal arteriole will cap- the retina without adherence to it. ilarize and will serve a choriocapilar lobule (4). Also choroid has two openings, one anterior with ora serrata as demarcation and one poste- 4. Choroid’s Innervation rior that passes through optic nerve. Choroid’s innervation is double, sympathetic and parasympathetic through dense perivascu- 3. Choroid blood supply lar plexus. Parasympathetic innervation comes Choroid blood supply is ensured by poste- from the pterigopalatin ganglion (5) through rior ciliary arteries (PCA), branches of the fiber mainly cholinergic rich in nitric oxide (6). ophthalmic artery. Venous drainage is achieved Some studies also indicate the presence of par- through vorticity veins (fig. 2). asympathetic fibers which originate in the cili- Posterior ciliary arteries (PCA) originate in ary ganglion (7). the ophthalmic artery. Their number is variable The Sympathetic innervation of the choroid being described several anatomical variants: originates from the superior cervical ganglion. one posterior ciliary artery (3%), two (48%), The fibers are noradrenergic and cause vaso- three (39%), four (8%) or five posterior ciliary constriction (8). arteries (2%). Nomenclature can sometimes by Sensory innervation is realized by related problematic, but classicaly the posterior ciliary sensory fibers that reach the ophthalmic nerve arteries have been named in relation to the via long ciliary nerves in the trigeminal gan- optic nerve: Medial PCA – localized medial to glion Gasser. It has been demonstrated that the optic nerve and usually there is one (70%); these fibers represent the basis of vasodilatation Lateral PCA - lateral side of the optic nerve reflex mediated by peptide as P substance and and it might be one (75 %) or two (20%); calcitonin gene-related peptide (9). Superior PCA- in 9% of cases and is small (3). Different PCA will divide in many smaller HISTOLOGICAL STRUCTURE OF branches that, together with the optic nerve will THE CHOROID perforate the sclera. Medial and lateral branch- Histologically, in literature for the choroid es of the PCA will form long PCAs medial and were described variable between 4 and 6 layers,

381 Şt. Oprea et al. depending if the vascular layer is considered a single or double layer and if lamina fusca is considered belonging to the choroid or sclera (1). Classically, as described by Hogan, choroid shows the 5 layers, from sclera to the retina: outer pigment layer, suprachoroid; two Vascu- lar layers, one external (called Haller) and one internal, Sattler; choriocapilar layer and Bruch’s membrane (fig. 3). At birth, choroid thickness is measuring about 200um and with age its thickness decreases to get 80um at 90 years (10).

1. External pigment layer or the suprachoroid – is a transition zone between the scle- Fig. 3. H.E. coloration ob. 40x ra and the choroid. It consists of elastic con- This photomicrograph highlights the well-vascu- nective tissue and collagen fibers arranged in larized choroid which abuts the sclera. thin lamellae, fibroblasts and melanocytes. The outer layer is called the lamina fusca and consists of fibroblasts and flattened fusiform mel- melanocytes localized perivascular. Also, there anocytes. This layer contains also myelinated can be found mast cells, macrophages and lym- axons disposed in bunches (11). phocytes (13).

2. Choroidal vascular layers – are two: 3. Choriocapilar layer – consists of branch- the outer layer of Haller and the inner layer of ing of choroidal vessels forming an extensive Sattler, outer layer of Haller consists of large capillary network. Each arteriole capilarize forming separate hexagonal region (1). Capil- vessels, especially vortex veins. They form spi- laries are large in size, between 20 and 40 um, rals in their pathway and finally confluence in but in the foveal region, where is the highest four spiraled venous trunks located in the most density of capillaries, these measures only 10um superficial place of the vascular layer. The loca- in diameter (14). Due to this vast network of tion of these trunks is posterior to the equator capillaries, the speed of red blood cells drops and are systematized in two upper trunks and to 77% compared to speed in retinal capillaries two lower trunks (nasal and temporal). These (15). Capillaries shows high permeability to trunks perforates the sclera and drains into the proteins in order to maintain an increased on- ophthalmic vein. Vortex veins do not have a cotic pressure in extravascular stroma. This segmental distribution (3). Sometimes has been contributes to facilitating the fluid exchange described also the chorio-vaginal vein leaving between the retina and choroid (1). the choroid and perforating the sclera with the Choriocapilars are located in a single plane optic nerve and draining into venous plexus of as a continuous layer forming a continuous the optic nerve (3). anastomotic network which stretches along the Various studies have shown by post-mortem entire choroid (3). injection the existence of arterio-arterial and arteriovenous anastomoses in the choroid. Inter 4. Bruch Membrane – is a transparent layer arterial anastomoses are made between branches with homogeneous appearance mainly repre- of anterior and posterior ciliary arteries at the sented by an endothelial basement membrane of equator. Because of these anastomosis occlu- the capillars from the choriocapilars layer (1). sion of a vessel does not produce the infarction choroid (12). CONCLUSIONS Settler inner layer consists of medium and Due to its huge importance in pathology we small caliber vessels, especially by arteries consider that knowing very well all the things that originate in the short posterior ciliary ar- about this structure of the eye, will help espe- teries (1). cially the young specialist to increase the qual- Extravascular stroma consists of fibroblasts, ity and accuracy of their medical atitude in front elastin fibers, smooth muscle fibers and giant of the pathologies involving the choroid.

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Corresponding author

Şt. Oprea e-mail: [email protected]

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