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RESEARCH ARTICLE
Year : 2007  |  Volume : 6  |  Issue : 3  |  Page : 89-93 Table of Contents     

Ophthalmic manifestations of lymphoma


1 Department of Ophthalmology, University of Benin Teaching Hospital, Benin City, Nigeria
2 Department of Haematology, University of Benin Teaching Hospital, Benin City, Nigeria

Date of Web Publication9-Oct-2009

Correspondence Address:
A E Omoti
Department of Ophthalmology, University of Benin Teaching Hospital, Benin City
Nigeria
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1596-3519.55728

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   Abstract 

Background : Ophthalmic involvement in lymphoma is a relatively rare condition that can result from a primary intraocular lymphoma or an intraocular manifestation of systemic lymphoma. This report reviews the ophthalmic manifestations of lymphoma.
Methods : Review of relevant information from journal articles and Internet search.
Results : Almost all the structures in the orbit, adnexiae and eye can be involved in lymphoma. Lymphoma of the eye and adnexiae are most frequently of B lineage. Most of the ocular manifestations frequently masquerade as other more benign intraocular conditions including allergic or infectious conjunctivitis, uveitis, multiple evanescent white dot syndrome, acute retinal necrosis or herpetic retinitis. Correct diagnosis thus depends on a high index of suspicion and frequently requires radiologic imaging, histologic analysis, particularly vitreous biopsy or flow cytometry, subretinal aspiration and retinal biopsy. Diagnosis is often delayed and may lead to a fatal outcome. Recognition of its modes of presentation facilitates early diagnosis and treatment that may improve prognosis.
Conclusions : It is important to review the ocular manifestations of lymphoma to assist the ophthalmologist to play a pivotal role in the prompt diagnosis and treatment of ocular lymphoma, and the haematologist/oncologist to recognize the need for a complete ophthalmic evaluation in the diagnosis, follow-up and management of lymphoma patients.

   Abstract in French 

Introduction : La participation ophtalmique dans lymphome est une condition rélativement rare qui peut être provoqué par lymphome intraoculaire primaire ou une manifestation intraoculaire du lymphome systématique. Ce rapport fait une rétrospective des manifestation ophtalmique du lymphome.
Méthodes : Une rétrospective des informations pertinentes des articles dans les journaux et des recherches dans l'internet.
Résultats : Prèsque toutes les structures dans l'orbite, adnexiae et l'oeil peuvent participer dans lymphome. Lymphome de l'oeil et d'adnexiae sont le plus souvent du lignage B. La plupart des manifestations oculaires les plus souvent mascarade comme d'autre conditions intraoculaire plus bénigne y compris des infections conjunctivite ou allergique, uveite, syndrome tacheté du blanc évanescent multiple, nécrose aigue rétine ou rétinite herpetique. Donc diagnostique correcte dépend d'index plus élevé du soupçon et l'imaging radiologique est très fréquemment éxigé, analyse histologique, la biopsie vitreouse en particulier ou bien écoulement cytométrie, aspiration sousrétine et la biopsie rétine. Le diagnostique est souvent rétardé et pourrait aboutir à un résultat sérieux. Réconnaissance de son mode de présentation facilitera un diagnostique précoce et un traitement qui pourrait améliorer la prognose.
Conclusion : C'est très important de faire une rétrospective des manifestations oculaires du lymphome afin d'aider l'ophtamologiste de jouer un rôle clef dans un diagnostique précoce et traitement du lymphome oculaire, et pour aider l'hématologiste et oncologiste de réconnaitre le besoin pour une évaluation ophtalmique dans le diagnostique, des soins post-hospitaliers et la prise en charge des patients atteints du lymphome.

Keywords: lymphoma, ophthalmic manifestations, masquerade, vitreous biopsy


How to cite this article:
Omoti A E, Omoti C E. Ophthalmic manifestations of lymphoma. Ann Afr Med 2007;6:89-93

How to cite this URL:
Omoti A E, Omoti C E. Ophthalmic manifestations of lymphoma. Ann Afr Med [serial online] 2007 [cited 2019 Sep 21];6:89-93. Available from: http://www.annalsafrmed.org/text.asp?2007/6/3/89/55728


   Introduction Top


Lymphoid proliferations can affect the eye in various ways. Intraocular and orbital structures can be affected by non-Hodgkin's primary central nervous system lymphoma (PCNSL), reactive lymphoid hyperplasia, and systemic non-Hodgkin's lymphoma.[1],[2],[3],[4],[5],[6],[7] Rare cases of cutaneous T-cell lymphoma (mycosis fungoides and Sezary syndrome) with ocular involvement have also been reported.[8],[9] Hodgkin's lymphoma may also affect the ocular structures.[10]

There are two distinct forms of intraocular lymphoma.[4] One originates within the central nervous system (CNS) and is called primary CNS lymphoma. The second form arises outside the CNS and metastasizes to the eye. When primary CNS lymphoma initially involves the retina, it is named primary intraocular lymphoma (PIOL).

Intraocular lymphoma is probably the most elusive intraocular tumor to diagnose. It frequently masquerades as other more benign ocular lesions.[2],[3],[5],[7],[11] Correct diagnosis thus depends on a high index of suspicion and frequently requires radiologic imaging, histologic analysis, particularly vitreous biopsy or flow cytometry, subretinal aspiration and retinal biopsy.[3],[4],[5],[11] Diagnosis can be difficult and it is frequently delayed as the clinical condition can mimic a number of other ocular conditions.[2],[7] Furthermore, ocular manifestations of lymphoma are generally rare events.[12] It is thus important to review the ocular manifestations of lymphoma to assist the ophthalmologist to play a pivotal role in the prompt diagnosis and treatment of ocular lymphoma which must be regarded as a sight and life threatening condition. It will also assist the haematologist/oncologist to recognize the need for a complete ophthalmic evaluation in the diagnosis, follow-up and management of lymphoma patients.


   Epidemiologic Characteristics Top


Most reports of ocular involvement in lymphoma are case reports or reports of few patients. This may reflect its relative rarity. Since an indeterminate number of unreported and isolated cases have occurred, meaningful data regarding incidence and prevalence are not available. In general, the primary non-Hodgkin's lymphoma of the CNS is rare, accounting for 1% of all non-Hodgkin's lymphomas, 1% of intracranial tumors and less than 1% of all intraocular tumors.[2],[13] It typically affects elderly patients,[2],[12],[14],[15],[16] with mean age around 63 years,[16] but can occur in young children.[1],[17] There is no reported racial predilection. There is no sex predilection.[3]


   Mechanism of Ocular Manifestations Top


Cancer may affect the eye and orbit as a direct result of metastatic neoplastic infiltration, compression, or circulating antibodies involving paraneoplastic retinal degeneration.[18] In the case of lymphoma, ocular involvement may be due to the disease itself, or side effects of the treatment. Most of the ophthalmic manifestations are the consequence of direct infiltration of the adnexiae, intraocular and orbital tissues. Presence of a mass lesion in the orbit can result in compression of orbital tissues and displacement of the eyeball resulting in proptosis.[1],[16] The ocular symptoms may be due to inflammation of the infiltrated tissues and this is largely responsible for the variability of ophthalmic manifestations ranging from typical uveitis to retinitis and vasculitis.[19] Eyes with retinal infiltrates and haemorrhagic retinal necrosis are usually believed to harbor a microbial infection.[20] An acute change of refractive error has been reported to be due to a lymphomatous deposit in the choroid.[21] Lymphomas of the eye and its adnexia are frequently of B lineage but may rarely be affected by non-B-cell non-Hodgkin's lymphoma.[16]


   Ophthalmic Manifestations Top


The lack of pathognomonic features, high clinical variability and the limited value of imaging techniques and histopathological measures often lead to serious delay in diagnosis.[19] Intraocular lymphoma often has a fatal outcome, but recognition of its modes of presentation facilitates early diagnosis and treatment that may improve prognosis.[7] Almost all the ocular tissues may be affected by lymphoma. They will be grouped as the orbit and adnexial structures, anterior segment, posterior segment and neuro-ophthalmic manifestations.

Orbit and adnexial structures

Infiltration of the orbit by lymphoma can result in proptosis.[1],[16] The protrusion may be gross depending on the size of the mass lesion.[16] Infiltration of the eyelids may result in periorbital swelling and ptosis.[21] Lymphoma may also present as a localized eyelid mass or nodule.[16],[22],[23]

Cutaneous T cell lymphoma (mycosis fungoides and Sezary syndrome) may involve the skin of the eyelids and may result in lower eyelid ulceration or cicatricial ectropion.[8],[24] In a report on cutaneous T-cell lymphoma, cicatricial eyelid ectropion was the most common ophthalmic manifestation occurring in 17(40.4%) of the 42 patients studied.[8]

Anterior segment

Infiltration of the conjunctiva may give rise to conjunctival swellings or masses.[16],[22] In a study of 39 children with leukaemias and malignant lymphomas, the most frequent ocular findings were seen in the conjunctiva, occurring in 33.4% of patients.[1] Marked chronic follicular conjunctivitis has been reported in a patient with mantle cell lymphoma.[23] The follicular appearance of the lymphocyte hyperplasia may mimic the clinical picture of infectious or allergic conjunctivitis, and may cause diagnostic difficulties and delay in diagnosis and appropriate treatment.

The cornea may be affected in adult T-cell leukaemia/lymphoma which is caused by Human T-cell lymphotrophic virus type 1 infection (HTLV-1).[25] It is an RNA retrovirus that primarily affects CD4+ T-cells. Corneal involvement in HTLV-1 infection and adult T-cell leukaemia/lymphoma include corneal haze, central corneal opacities with thinning, scarring, bilateral immunoprotein keratopathy, peripheral corneal thinning, scarring and neovascularization.[25] It is believed that the novel corneal findings in these patients are most likely a consequence of the hypergammaglobulinaemia induced by the HTLV-1 infection or the T-cell malignancy. Keratoconjunctivitis sicca has also been reported in adult T-cell leukaemia/lymphoma.[25]

Episcleritis and scleritis may occur following lymphoma infiltration.[25],[26] The differential diagnosis of lymphoma should be considered when scleritis is resistant to corticosteroid therapy.[26] Mucosa-associated lymphoid tissue (MALT) lymphoma has been reported to masquerade as anterior scleritis.[26] The anterior scleritis may be associated with uveal effusion syndrome.[26]

Lymphoma may masquerade as iritis, anterior uveitis or panuveitis.[2],[3],[7],[12], [25],[26],[27] Incorrect diagnosis of the uveitic syndrome may have severe consequences. Uveal involvement may be the initial manifestation of extranodal lymphoma.[12] It is a differential diagnosis of recurrent uveitis-like symptoms evolving to painful blind eye. In a study of 40 patients with uveitic masquerade syndromes identified in a cohort of 828 consecutive patients with uveitis, 19 patients had intraocular malignancy (48% of all with uveitis masquerade syndrome; 2.3% of all with uveitis), mainly intraocular lymphoma (n=13) and leukaemia (n=3).[27] The ophthalmologist was the first to recognize malignant disease in 11 of 19 patients (58%). Uveitis in lymphoma is resistant to corticosterioid therapy[7] and may be associated with hypopyon.[28] An iridic nodular lesion has been reported in the evolution of non-Hodgkin's lymphoma.[17] Vogt-Koyanagi-Harada disease (VKH), an inflammatory ocular disorder characterized by bilateral granulomatous panuveitis and a variety of extraocular manifestations, has been reported to be associated with various immune disorders and recently with malignant lymphoma.[29] There is evidence that VKH can be induced by immune disorders caused by high sIL-2R in malignant lymphoma.[29]

Glaucoma may occur in lymphoma.[2],[28] It may occur secondary to neovascularization of the iris and iridocorneal angle (neovascular glaucoma), [2] or may be due to direct obstruction of the trabecular meshwork by tumor cells.[28]

Posterior segment

The vitreous may be infiltrated by cells[20] or there may be vitritis.[3],[4] In a study of 14 patients with intraocular lymphoma, vitritis was present in 85.7% of cases.[3] The typical clinical presentation include blurred vision and floaters.[4],[15] Vitreous haemorrhage may also occur.[2]

The choroid may be involved by lymphoma either alone[4],[26] or as part of panuveitis.[2],[7],[26] Posterior uveitis may be associated with retinochoroidal infiltration and in more severe cases may be associated with serous retinal detachment.[26] A choroidal tumor has also been reported in large-cell lymphoma.[22]

The retina is frequently involved in ocular lymphoma. The various retinal lesions reported in lymphoma include retinal and subretinal infiltrates,[4],[11],[30] necrotizing granulomatous retinal vasculitis and retinitis,[5],[7],[19],[31] retinal pigmentary degeneration,[14],[25] haemorrhagic retinal necrosis,[20] retinal periphlebitis,[10] and perivascular exudates and sheathing.[20],[32] The retinal and subretinal infiltrates and pigmentary alterations may mimic a diagnosis of multiple evanescent white dot syndrome.[11] The typical yellowish-white infiltrates may occur at the level of the subretinal pigment epithelial layer.[30] Subretinal pigment epithelium tumors may also be seen.[7] However, other presentations may include multiple deep white dots in the retina secondary to tumor infiltration; retinal infiltration causing a necrotizing retinitis; or infiltration of the retinal vasculature causing arterial or venous obstruction[7] The fundus may also show tumorous subretinal lesions suggestive of proliferation of tumor cells.[31] Electrooculogram may show findings suggestive of widespread impairment of the retinal pigment epithelium.[31] In adult T-cell leukaemia/lymphoma, ocular lesions may result from HTLV-1 infection, including direct infiltration by adult T-cell leukaemia/lymphoma cells, cytomegalovirus retinitis and HTLV-1-associated uveitis.[33] The ocular lesion may simulate acute retinal necrosis or herpetic retinitis.[34]

Neuro-ophthalmic manifestations

Primary intraocular lymphoma is a variant of primary central nervous system lymphoma in which lymphoma cells are initially present only in the eyes without evidence of disease in the brain or cerebrospinal fluid.[15] The prognosis is mostly determined by involvement of the central nervous system and/or visceral organ.[19] Completely different extaocular features are induced by long-standing local infiltrates within basal ganglia, a diffuse infiltration of the brain leading to an acute increase in intracranial pressure.[19] These may result in neuro-ophthalmic manifestations. Optic nerve invasion may occur in primary intraocular lymphoma.[7],[10],[28],[35] Optic neuritis can occur due to tumor cell infiltration of the optic nerve,[28],[35] and this may progress to optic atrophy and visual loss.[35] The clinical course may mimic multiple sclerosis.[35] Bilateral optic disc swelling may occur in Hodgkin's disease.[10] The incidence of non-Hodgkins lymphoma of the central nervous system has trebled over the past 15 years.[36] HIV/AIDS and other causes of immunosuppression may be responsible.


   Diagnosis Top


Diagnosis is based on a good history, clinical examination and investigations. A history of systemic lymphoma will raise a suspicion that the ophthalmic disorder may be due to lymphoma. With the aid of a pen torch and slit lamp biomicroscope, anterior segment lesions can be identified. Fundoscopy and fluorescein angiography can identify posterior segment lesions. Orbital and intraocular mass lesions can be identified by radiological examinations such as ultrasound scan, computed tomography scan and magnetic resonance imaging.[11],[35] Definitive diagnosis is based on biopsy of the affected tissue. Diagnosis of the systemic disease is established based on tissue samples that are studied by histological examination of a surgical biopsy from an accessible lymph node site.

Of importance in ocular lymphoma is pars plana vitrectomy and cytology, aqueous tap, subretinal aspiration or retinal biopsy.[11],[14],[30] Lumbar puncture with cytology of the cerebrospinal fluid is important in central nervous system involvement.


   Treatment and Prognosis Top


Treatment of ocular lymphoma is by radiation therapy and this may be combined with chemotherapy in the presence of central nervous system involvement.[11] For non-Hodgkin's lymphoma, chemotherapy involves the use of iv Cyclophosphamide 750mg/m2 on days 1 and 8, iv Adriamycin 45mg/m2 on days 1 and 8, iv Vincristine 1.5mg/m2 on days 1 and 8 and oral Prednisolone 20mg 8 hourly for 10days. For Hodgkin's lymphoma, chemotherapy involves the use of ABVD regimen (iv Adriamycin 25mg/m2 on days 1and15; iv Bleomycin 10U/m2 on days 1and15; iv Vinblastine 6mg/m2 on days 1and15 and iv Dacarbazine 375mg/m2 on days 1and15). High dose methotrexate and Leucovorin rescue may also be used for ocular lymphoma.[2]

Prognosis for visual recovery is good if diagnosis is made early and therapy started on time. Dramatic improvements in visual acuity have been reported in patients with retinal involvement after x-irradiation.[11] Intraocular lymphoma often has a fatal outcome but recognition of its mode of presentation facilitates early diagnosis and treatment that may improve prognosis.[3],[7],[31] Compared with primary intraocular lymphoma, metastatic systemic lymphomas have a better prognosis and is less likely to create a diagnostic dilemma.[15] The survival from the establishment of the diagnosis has been reported to 20.6 months on the average.[3]


   Conclusion Top


Lymphoma of the eye and adnexia are most frequently of B lineage. The lack of pathognomonic features, high clinical variability and the limited value of imaging techniques and histopathological measures often lead to serious delay in diagnosis. Almost all ocular structures can be involved in lymphoma and it frequently masquerades as other more benign intraocular conditions. Diagnosis is thus often delayed and this may lead to a fatal outcome. Early diagnosis and treatment may be facilitated by recognition of its modes of presentation and this may improve prognosis.



 
   References Top

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2.Pache M, Kain H, Buess M, Flammer J, Meyer P. Primary intraocular lymphoma with unusual clinical presentation and poor outcome. Klin Monatsbl Augenheilkd 2004; 221: 401-403  Back to cited text no. 2      
3.Rihova E, Siskova A, Jandusova J, Kovarik Z, Sach J, Adam P. Intraocular lymphoma-a clinical study of 14 patients with non-Hodgkin's lymphoma. Cesk Slov Oftalmol 2004;60: 3-16  Back to cited text no. 3      
4.Chan CC, Buggage RR, Nussenblatt RB. Intraocular lymphoma. Curr Opin Ophthalmol 2002; 13: 411-418  Back to cited text no. 4      
5.Levy-Clarke GA, Buggage RR, Shen D, Vaughn LO, Chan CC, Davis JL. Human T-cell lymphotropic virus type-1 associated T-cell leukaemia/lymphoma masquerading as necrotizing retinal vasculitis. Ophthalmology 2002; 109: 1717-1722  Back to cited text no. 5      
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7.Gill MK, Jampol LM. Variations in the presentation of primary intraocular lymphoma: case reports and a review. Surv Ophthalmol 2001; 45: 463-471.  Back to cited text no. 7      
8.Cook BE Jr, Bartle GB, Pittelkow MR. Ophthalmic abnormalities in patients with cutaneous T-cell lymphoma. Ophthalmology 1999; 106: 1339-1344  Back to cited text no. 8      
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10.Barr CC, Joondeph HC. Retinal periphlebitis as the initial clinical finding in a patient with Hodgkin's disease. Retina 1983; 3: 253-257  Back to cited text no. 10      
11.Fahim DK, Bucher R, Johnson MW. The elusive nature of primary intraocular lymphoma. J Neuroophthalmol 2005; 25: 33-36  Back to cited text no. 11      
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13.Burnier MN Jr, Stockl FA, Dolmetsch AM. Large B-cell lymphoma of the retina and CNS. Presented at the 1994 Annual Meeting of the Eastern Ophthalmic Pathology Society, Boston, October 1994  Back to cited text no. 13      
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15.Buggage RR, Chan CC, Nussenblatt RB. Ocular manifestations of central nervous system lymphoma. Curr Opin Oncol 2001; 13: 137-142  Back to cited text no. 15      
16.Coupland SE, Foss HD, Assaf C et al. T-cell and T/natural killer-cell lymphomas involving ocular and ocular adnexial tissues: a clinicopathologic, immunohistochemical, and molecular study of seven cases. Ophthalmology 1999; 106: 2109-2120  Back to cited text no. 16      
17.Glavici M, Comanescu V, Glavici A. Ocular manifestations in non-Hodgkin's lymphomas. Oftalmologia 1994; 38: 242-246  Back to cited text no. 17      
18.De Potter P, Disneur D, Levecq L, Snyers B. Ocular manifestations of cancer. J Fr Ophtalmol 2002; 25: 194-202  Back to cited text no. 18      
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20.Ridley ME, McDonald HR, Sternberg P Jr, Blumenkranz MS, Zarbin MA, Schachat AP. Retinal manifestations of ocular lymphoma (reticulum cell sarcoma). Ophthalmology 1992; 99: 1153-1160  Back to cited text no. 20      
21.Weisenthal R, Frayer WC, Nichols CW, Eagle RC. Bilateral ocular disease as the initial presentation of malignant lymphoma. Br J Ophthalmol 1988; 72: 248-252  Back to cited text no. 21      
22.Leff SR, Shields JA, Augsburger JJ, Miller RV, Liberatore B. Unilateral eyelid, conjunctival, and choroidal tumuors as initial presentation of diffuse large-cell lymphoma. Br J Ophthalmol 1985; 69: 861-864  Back to cited text no. 22      
23.Amstutz CA, Michel S, Thiel MA. Follicular conjunctivitis caused by mantle cell lymphoma. Klin Monatsbl Augenheilkd 2004; 221: 398-400  Back to cited text no. 23      
24.Garne JA, Davies R. Case report: Mycosis fungoides causing severe lower eyelid ulceration. Clin Experiment Ophthalmol 2002; 30: 369-371  Back to cited text no. 24      
25.Buggage RR, Levy-Clarke GA, Smith JA. New corneal findings in human T-cell lymphotrophic virus type 1 infection. Am J Ophthalmol 2001; 131: 309-313  Back to cited text no. 25      
26.Gaucher D, Bodaghi B, Charlotte F et al. MALT-type B-cell lymphoma masquerading as scleritis or posterior uveitis. J Fr Ophtalmol 2005; 28: 31-38  Back to cited text no. 26      
27.Rothova A, Ooijman F, Kerkhoff F, Van Der Lelij A, Lokhorst HM. Uveitis masquerade syndromes. Ophthalmology 2001; 108: 386-399  Back to cited text no. 27      
28.Furuya T, Yamabayashi S, Okuyama M, Imai M, Tanokura M. A case of malignant lymphoma with various ocular manifestations. Nippon Ganka Gakkai Zasshi 1990; 94: 231-237  Back to cited text no. 28      
29.Hashida N, Kanayama S, Kawasaki A, Ogawa K. A case of Vogt-Koyanagi-Harada disease associated with malignant lymphoma. Jpn J Ophthalmol 2005; 49: 253-256   Back to cited text no. 29      
30.Matsuo T, Yamaoka A, Shiraga F, Matsuo N. Two types of initial ocular manifestations in intraocular-central nervous system lymphoma. Retina 1998; 18: 301-307   Back to cited text no. 30      
31.Noda K, Suzuki S, Ando Y et al. The clinical features of 9 cases of intraocular malignant lymphoma of oculocerebral origin. Nippon Ganka Gakkai Zasshi 1998; 102: 348-354  Back to cited text no. 31      
32.Schanzer MC, Font RL, O'Malley RE. Primary ocular malignant lymphoma associated with the acquired immune deficiency syndrome. Ophthalmology 1991; 98: 88-91  Back to cited text no. 32      
33.Shibata K, Shimamoto Y, Nishimura T, Okinami S, Yamada H, Miyahara M. Ocular manifestations in adult T-cell leukaemia/lymphoma. Ann Hematol 1997; 74: 163-168  Back to cited text no. 33      
34.Kohno T, Uchida H, Inomata H, Fukushima S, Takeshita M, Kikuchi M. Ocular manifestations of adult T-cell leukaemia/lymphoma. A clinicopathologic study. Ophthalmology 1993; 100: 1794-1799   Back to cited text no. 34      
35.Dunker S, Reuter U, Rosler A, Wiegand W. Optic nerve involvement in chronic lymphatic leukaemia of the B-cell series. Ophthalmologe 1996; 93: 351-353   Back to cited text no. 35      
36.Hochberg FH, Miller DC. Primary central nervous system lymphoma. J Neurosurg 1998; 68: 835-853  Back to cited text no. 36      



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