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  • 2020–2021 BCSC Basic and Clinical Science Course™

    Go to Academy Store Learn more and Purchase.

    4 Ophthalmic Pathology and Intraocular Tumors

    Part I: Ophthalmic Pathology

    Chapter 11: Retina and Retinal Pigment Epithelium

    Neoplasia

    The tumors discussed in this chapter arise from tissue derived from the inner layer of the optic cup.

    Retinoblastoma

    Retinoblastoma is the most common primary intraocular malignancy in childhood, occurring in 1 in 14,000–20,000 live births. Chapter 19 discusses the clinical aspects of retinoblastoma. Retinoblastoma is also discussed in BCSC Section 6, Pediatric Ophthalmology and Strabismus.

    Pathogenesis

    Although retinoblastoma was once thought to be of glial origin (eg, lesions clinically simulating retinoblastoma were formerly called pseudogliomas), the tumor’s neuroblastic origin from the nucleated layers of the retina has been well established. In immunohistochemical studies, tumor cells stain positively for neuron-specific enolase, retinal S-antigen, and rhodopsin. Tumor cells also secrete an extracellular substance known as interphotoreceptor retinoid-binding protein (IRBP), which is produced by normal photoreceptors. Retinoblastoma cells grown in culture have expressed red and green photopigments, as well as cone cell α-subunits of transducin. These findings further support the hypothesis that retinoblastoma may be a neoplasm of cone cell lineage. However, immunohistochemical and molecular studies cast some doubt on a single-cell progenitor for retinoblastoma. The presence of small amounts of glial tissue within retinoblastomas suggests that resident glial cells may undergo reactive proliferation or become trapped within the tumor.

    Retinoblastoma develops when both copies of the retinoblastoma gene (RB1) become nonfunctional, either by a deletion error or by mutation. RB1 is located on the long arm of chromosome 13 and encodes for retinoblastoma protein, pRB, which functions as a tumor suppressor. Thus, loss of the gene does not actively cause tumorigenesis but rather leads to loss of tumor suppression, resulting in the development of retinoblastoma (and other tumors, such as osteosarcoma).

    A single normal gene copy is sufficient to suppress the development of retinoblastoma. However, when 1 abnormal gene is present, if a mutation in the remaining normal gene occurs during retinal differentiation, loss of tumor suppression occurs and retinoblastoma is likely to develop.

    Recently, MYCN oncogene amplification was demonstrated in a minority (approximately 3%) of retinoblastomas that lacked RB1 gene mutations. This type of retinoblastoma is associated with very early age (ie, median age of 4.5 months) at diagnosis and unilateral occurrence, as well as more aggressive growth compared to retinoblastoma with RB1 mutations.

    • Rushlow DE, Mol BM, Kennett JY, et al. Characterisation of retinoblastomas without RB1 mutations: genomic, gene expression, and clinical studies. Lancet Oncol. 2013;14(4): 327–334.

    Histologic features

    On hematoxylin-eosin stain, retinoblastoma is histologically distinguished by 3 predominant colors, appreciated best at low magnification: blue, representing the retinoblastoma tumor cells; pink, representing areas of necrosis; and purple, representing areas of calcification. Commonly referred to as a small blue cell tumor, retinoblastoma consists of cells with round or oval nuclei that are approximately twice the size of a lymphocyte. The nuclei are hyperchromatic and surrounded by a scant amount of cytoplasm. The cells are generally tightly packed, and the nuclei can be indented by adjacent cells (nuclear molding). Mitotic activity is usually high, although frequent apoptotic cells may complicate identification of mitoses. As the tumor expands into the vitreous or subretinal space, retinoblastoma cells surround blood vessels for sustenance, creating a characteristic pattern referred to as pseudorosettes (ie, viable tumor cells surrounding a blood vessel) (Fig 11-41). However, they frequently outgrow their blood supply, and regions of ischemic necrosis begin 90–120 µm from the central vessel. Associated with the necrosis are foci of calcification. DNA released from degenerate cells sometimes accumulates in the walls of tumor blood vessels (Fig 11-42) or within vessels in other ocular tissues, such as the iris. Neovascularization of the iris, sometimes resulting in angle closure, may occur in the setting of retinoblastoma (Fig 11-43).

    Small clumps of cells shed from the tumor may remain viable in the vitreous (vitreous seeds) and subretinal space without a blood supply and may eventually develop into focal tumor implants throughout the eye. It may be difficult to determine histologically whether multiple intraocular foci of the tumor represent multiple primary tumors, implying a systemic RB1 mutation, or tumor implants due to intraocular seeding.

    Various forms of differentiation may occur in retinoblastomas. The formation of highly organized Flexner-Wintersteiner rosettes is a characteristic of retinoblastoma that occurs only rarely in other neuroblastic tumors and represents cellular differentiation toward retinal tissue. These rosettes comprise a single row of columnar cells with eosinophilic cytoplasm and peripherally situated nuclei arranged radially (Fig 11-44A). The cells surround a central lumen lined by a refractile membranous structure that corresponds to the external limiting membrane of the retina. A rosette without features of retinal differentiation, known as a Homer Wright rosette, is also found in retinoblastomas as well as in other neuroblastic tumors, such as neuroblastomas and medulloblastomas. Unlike the Flexner-Wintersteiner rosette, the Homer Wright rosette lacks a central lumen and is filled with a tangle of eosinophilic cytoplasmic processes (Fig 11-44B). Evidence of photoreceptor differentiation has also been documented for a form of differentiation known as a fleurette. Fleurettes, which resemble a bouquet of flowers, are curvilinear clusters of cells composed of rod and cone inner segments that are often attached to abortive outer segments (Fig 11-44C). A fleurette expresses a greater degree of retinal differentiation than a Flexner-Wintersteiner rosette. Nevertheless, in a typical retinoblastoma, undifferentiated tumor cells greatly outnumber fleurettes and Flexner-Wintersteiner rosettes, and differentiation is not an important prognostic indicator.

    Figure 11-41 Retinoblastoma. Note the viable tumor cells (asterisk) surrounding a blood vessel (arrow) and the alternating zones of necrosis (N). This histologic arrangement is referred to as a pseudorosette.

    Figure 11-42 Retinoblastoma. Zones of viable tumor (usually surrounding blood vessels) alternate with zones of tumor necrosis (asterisk). Calcification (arrow) occurs in the necrotic areas. The basophilic material surrounding and within the blood vessel walls (arrowheads) is DNA, liberated from degenerating tumor cells.

    Figure 11-43 Retinoblastoma, anterior segment of the globe. Note the thick neovascular membrane (arrow) on the iris surface extending into the angle, resulting in angle closure. Free-floating tumor cells (arrowhead) are present in the anterior chamber.

    Tumors secondary to MYCN amplification demonstrate distinct histologic features such as undifferentiated cells with prominent and multiple nucleoli, necrosis, apoptosis, little calcification, and absence of Flexner-Wintersteiner rosettes and nuclear molding (Fig 11-45). Despite aggressive growth and poor differentiation, these tumors appear unlikely to spread systemically.

    Tumor progression

    Histologic features of retinoblastoma that are associated with higher risk of metastasis and poorer survival include

    • optic nerve invasion (laminar, retrolaminar, or surgical cut end of the nerve)

    • massive choroidal invasion

    • direct extraocular extension

    • anterior chamber involvement

    The most common route for retinoblastoma to extend out of the eye is through the optic nerve. Direct infiltration of the optic nerve can lead to extension into the brain (Fig 11-46). Cells that spread into the leptomeninges can gain access to the cerebrospinal fluid, with the potential for seeding throughout the CNS. Therefore, invasion of the optic nerve is a poor prognostic indicator.

    Massive choroidal invasion (Fig 11-47) is defined as an invasive focus of a tumor with a diameter (in any dimension) of at least 3 mm and the tumor reaching at least the inner fibers of the scleral tissue. Massive choroidal invasion is a poor prognostic factor that is thought to be related to hematogenous spread of tumor via the highly vascular choroid. See Chapter 19 for a discussion of prognosis. Choroidal involvement that is less than 3 mm in any dimension and does not reach the sclera is termed focal choroidal invasion. Focal choroidal invasion is not associated with a worse prognosis in retinoblastoma.

    Figure 11-44 Retinoblastoma differentiation (rosettes).A, Flexner-Wintersteiner rosettes. Note the central lumen (L). B, Homer Wright rosettes. Note the neurofibrillary tangle (arrow) in the center of these structures. C, The fleurette (arrow) demonstrates bulbous extensions of retinoblastoma cells that represent differentiation toward photoreceptor inner segments.

    Figure 11-45 High-magnification photomicrograph of retinoblastoma cells with MYCN oncogene amplification. Tumor cells are very poorly differentiated and highly pleomorphic. Nuclei are often hyperchromatic and enlarged (arrows) or have prominent nucleoli (arrowheads).

    (Courtesy of Nasreen A. Syed, MD.)

    • Sastre X, Chantada GL, Doz F, et al; International Retinoblastoma Staging Working Group. Proceedings of the consensus meetings from the International Retinoblastoma Staging Working Group on the pathology guidelines for the examination of enucleated eyes and evaluation of prognostic risk factors in retinoblastoma. Arch Pathol Lab Med. 2009;133(8):1199–1202.

    Excerpted from BCSC 2020-2021 series: Section 4 - Ophthalmic Pathology and Intraocular Tumors. For more information and to purchase the entire series, please visit https://www.aao.org/bcsc.

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