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Annals of Oncology Advance Access originally published online on September 5, 2007
Annals of Oncology 2007 18(11):1851-1855; doi:10.1093/annonc/mdm340
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© 2007 European Society for Medical Oncology

CNS tumors

Primary intraocular lymphoma: an International Primary Central Nervous System Lymphoma Collaborative Group Report

S. A. Grimm1, J. S. Pulido2, K. Jahnke3, D. Schiff4, A. J. Hall5, T. N. Shenkier6, T. Siegal7, N. D. Doolittle8, T. Batchelor9, U. Herrlinger10, E. A. Neuwelt8,11, N. Laperriere12, M. C. Chamberlain13, J. Y. Blay14, A. J. M. Ferreri14, A. M. P. Omuro15, E. Thiel3 and L. E. Abrey1,*

1 Memorial Sloan-Kettering Cancer Center, New York
2 Mayo Clinic, Rochester
3 Charité University Medicine Berlin, Campus Benjamin Franklin, Berlin, Germany
4 University of Virginia, Charlottesville
5 Royal Melbourne Hospital and Royal Victorian Eye and Ear Hospital, Melbourne, Australia
6 British Columbia Cancer Agency, Vancouver, Canada
7 Hadassah Hebrew University Hospital, Jerusalem, Israel
8 Oregon Health & Sciences University, Portland
9 Massachusetts General Hospital, Boston
10 University of Tuebingen, Tuebingen, Germany
11 Portland VA Medical Center, Portland
12 Princess Margaret Hospital, Toronto, Canada
13 Moffitt Cancer Center, Tampa
14 On behalf of the International Extranodal Lymphoma Study Group
15 Hospital Pitie-Salpetriere, Paris, France

* Correspondence to: Dr L. E. Abrey, Department of Neurology, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10021, USA. Tel: +1-212-639-5122; Fax: +1-917-432-2310; E-mail: abreyl{at}mskcc.org


   Abstract
Top
 Abstract
introduction
 patients and methods
 results
 discussion
 appendix
 Acknowledgements
 References
 
Background: Primary intraocular lymphoma (PIOL) is an uncommon subset of primary central nervous system lymphoma. Because it is rare and difficult to diagnose, the natural history and optimal management are unknown.

Patients and methods: A retrospective study of 83 HIV negative, immunocompetent PIOL patients was assembled from 16 centers in seven countries.

Results: Median age at diagnosis was 65. Median ECOG performance status was 0. Presenting symptoms included blurred vision, decreased visual acuity, and floaters. Median time to diagnosis was 6 months. Diagnosis was made by vitrectomy (74), choroidal/retinal biopsy (6) and ophthalmic exam (3). Eleven percent had positive CSF cytology. Initial treatment was categorized as focal in 23 (intra-ocular methotrexate, ocular radiotherapy) or extensive in 53 (systemic chemotherapy, whole brain radiotherapy). Six received none; details are unknown in one. Forty-seven relapsed: brain 47%, eyes 30%, brain and eyes 15%, and systemic 8%. Median time to relapse was 19 months. Focal therapy alone did not increase risk of brain relapse. Median progression free (PFS) and overall survival (OS) were 29.6 and 58 months, respectively, and unaffected by treatment type.

Conclusion: Treatment type did not affect relapse pattern, median PFS or OS. Focal therapy may minimize treatment toxicity without compromising disease control.

Key words: Ocular lymphoma, primary CNS lymphoma


   introduction
Top
 Abstract
 introduction
patients and methods
 results
 discussion
 appendix
 Acknowledgements
 References
 
Primary intraocular lymphoma (PIOL) is a rare hematopoietic tumor that arises in the retina, vitreous, subretinal pigment epithelial space or optic nerve head [1]. It is an uncommon subset of primary central nervous system lymphoma (PCNSL) that has been reported to have a high risk of ocular and central nervous system (CNS) relapse. Statistical data regarding the incidence of PIOL is lacking, but it has been estimated that in the past 3 years there were at least 100 new cases in the United States [2]. At presentation, PIOL is often misdiagnosed as uveitis and may respond initially to corticosteroids, resulting in a delay of definitive diagnosis [3]. Often a diagnosis is not made until there is brain progression at which time the prognosis is poor. Because the disease is rare and difficult to diagnose, true incidence and natural history are not well characterized. Optimal treatment is unknown, and a variety of local ocular and systemic therapies have been reported. Local ocular treatments include ocular radiotherapy (RT) [4, 5] and intravitreal methotrexate [6]. Extensive treatments include whole brain RT (which includes the posterior retina) as well as intravenous and/or intrathecal chemotherapy.

The International Primary Central Nervous System Lymphoma Collaborative Group (IPCG) is a multidisciplinary group from North America, Europe, and Australia established in 2002 under the sponsorship of the International Extranodal Lymphoma Study Group. Given its rarity, PIOL was identified as an area for which collaborative work would further understanding of the disease [7].


   patients and methods
Top
 Abstract
 introduction
 patients and methods
results
 discussion
 appendix
 Acknowledgements
 References
 
A retrospective chart review was conducted at 16 participating IPCG institutions from seven countries to collect information on HIV negative, immunocompetent patients with intra-ocular lymphoma diagnosed between 1977 and 2005; patients with systemic lymphoma at diagnosis were excluded. Patient characteristics, diagnosis, treatment, site and date of progression, salvage treatment, treatment toxicity and survival were obtained. Histological diagnosis was reviewed at each participating institution by an experienced hematopathologist. Available pathology reports were submitted for central review. The patients identified were separated into two groups: those with isolated intra-ocular lymphoma, reported here, and those with brain and spinal cord involvement in addition to ocular lymphoma at diagnosis, who will be reported separately. Local Institutional Review Board or Ethics Board approval was obtained by each participating center.

statistical considerations
Progression-free survival (PFS) and overall survival (OS) were calculated from date of ocular lymphoma diagnosis to date of first relapse, progression, or death. Surviving patients were censored at date of last follow-up. Survival curves were drawn using the Kaplan Meier product-limit method [8], and comparisons were examined by the log rank test. Analysis of discrete variables was performed using the {chi}2 method with Yates correction for expected values less than 5. Given the descriptive nature of this analysis, there were no a priori power estimates.


   results
Top
 Abstract
 introduction
 patients and methods
 results
discussion
 appendix
 Acknowledgements
 References
 
clinical features
A total of 83 patients were identified; all had disease confined to the eyes at diagnosis with no evidence of brain, systemic or spinal cord lymphoma. Twenty-nine cases included in this cohort were previously reported [9–12]. Patient characteristics and diagnostic details are summarized in Table 1. The median age at diagnosis was 63 (24–85) years; 57% were women. The median Eastern Cooperative Oncology Group performance status was 0; only three patients had a score greater than 1. Fifteen patients had a prior malignancy other than lymphoma; the site of origin was available for nine patients and included breast, squamous cell of the pharynx, papillary thyroid, immunocytoma, renal (two), skin, cutaneous T-cell lymphoma and melanoma.


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  		Table 1. Patient characteristics

 
All patients had a histological diagnosis of lymphoma. Eighty patients were diagnosed on the basis of vitrectomy (74) or direct choroidal/retinal biopsy (6). One patient with a positive slit lamp exam was diagnosed by positive cerebrospinal fluid (CSF) cytology. Two patients were initially diagnosed with ocular lymphoma by slit lamp/ophthalmic exam and definitive pathology was not obtained until time of tumor progression and brain biopsy. Specific histological subtypes included large B-cell (55), T-cell (five), subtype not specified (seven); 16 pathology reports were not available for review.

The mean duration of symptoms prior to diagnosis was 6 months (0–36). The presenting symptoms were blurred vision in 33 patients, decreased visual acuity in 23, floaters in 19 and not specified in 20. Data regarding the incidence of bilateral versus unilateral disease were unavailable. Neuro-imaging (enhanced brain MRI or CT scan) showed no evidence of intracranial tumor at diagnosis of intraocular lymphoma. Sixty patients had a staging lumbar puncture performed which revealed positive CSF cytology in nine patients (15%).

therapeutic management
Treatment details are summarized in Table 2. Forty-four patients received either systemic or intraocular steroids; however, the response was rarely evaluated. Twenty-three received only local ocular therapy at diagnosis and 53 received more extensive treatment including various combinations of systemic chemotherapy, ocular chemotherapy, whole brain radiotherapy (WBRT), and ocular RT. Systemic chemotherapy was methotrexate-based in 37 (70%). All patients with positive CSF cytology received more extensive treatment including systemic chemotherapy in nine, intrathecal chemotherapy in four and WBRT in one. Six patients received no definitive treatment and complete treatment details were unavailable in one. Median follow-up of surviving patients was 32 months.


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  		Table 2. Treatment summary

 
outcome
Median PFS and OS for the entire cohort were 29.6 and 58 months, respectively (Figure 1). Excluding those patients with positive CSF cytology did not significantly impact the survival analysis. There was no statistically significant difference in PFS or OS regardless of the treatment modality (Figures 2 and 3). At last follow-up, 33 patients had died. The cause of death was CNS lymphoma (19), other cancer (3), pneumonia (one), stroke (one), neurotoxicity (one) and unknown (eight).


Figure 1
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  		Figure 1. Kaplan–Meier curve showing progression-free survival (dashed line) and overall survival (solid line) for all 83 patients with primary intraocular lymphoma.

 

Figure 2
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  		Figure 2. Kaplan–Meier curve showing progression-free survival for primary intraocular lymphoma patients treated with dedicated ocular therapy (dashed line) and WBRT and/or systemic chemotherapy (solid line).

 

Figure 3
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  		Figure 3. Kaplan–Meier curve showing overall survival for primary intraocular lymphoma patients treated with dedicated ocular therapy (dashed line) and WBRT and/or systemic chemotherapy (solid line).

 
Forty-seven patients (56%) relapsed at a median of 19 months (0.5–180) after initial therapy. Risk of relapse was similar in the two treatment groups; 56% of those in the focal treatment group relapsed versus 60% in the extensive treatment group (P = 0.8). Sites of relapse included brain in 22 patients (47%), eyes in 14 (30%), brain and eyes in seven (15%) and systemic in four (8%). Patients treated with ocular therapy alone did not have an increased risk of failing in the brain (P = 0.4). Patterns of recurrence were similar in the nine patients with positive CSF cytology.

Information on treatment-related neurotoxicity was available in 45 patients. The complications reported included none (37), dementia (three), leukoencephalopathy (two), gait disorder (one), hemiparesis (one) and stroke (one). All patients with treatment-related neurotoxicity received more extensive therapy either at diagnosis or relapse. Ocular sequelae were reported in 20 patients; 32% of patients who received ocular RT had a reported complication and 36% of those who received intraocular chemotherapy had a reported complication. These included decreased visual acuity (seven), cataracts (seven), retinopathy (two), dry eyes (one), glaucoma (one), retinal artery occlusion (one) and amaurosis (one).


   discussion
Top
 Abstract
 introduction
 patients and methods
 results
 discussion
appendix
 Acknowledgements
 References
 
Because of its rarity, PIOL has been a difficult disease to study. In previously published series, patients with isolated ocular lymphoma were reported as a subset of patients with ocular involvement from brain lymphoma or at ocular relapse of brain or systemic lymphoma [4, 10–12]. This report represents the largest exclusive series of PIOL in the literature to date.

The average duration of symptoms preceding definitive diagnosis was only 6 months; this is substantially shorter than the 13–24-month latency reported in other series [10, 12]. However, our results support other studies in the literature that suggest that definitive diagnosis could be established in 80% of patients between 6 and 12 months [11, 13]. Vitrectomy was the procedure most frequently used to make a definitive diagnosis. The most common immunophenotype observed was B-cell; however, a small percentage of patients had a primary T-cell PIOL. This distribution is similar to that seen in brain lymphoma.

Extent-of-disease workup found positive CSF cytology in nine of 60 (15%) patients at the time of ocular lymphoma diagnosis. We included these nine patients with concomitant CSF and ocular lymphoma in this report to underscore the need for complete extent-of-disease evaluation [15]. If CSF dissemination is not diagnosed and treated as part of the initial disease process, it will persist as a reservoir of untreated lymphoma that will compromise disease control and survival. Moreover, these nine patients had a similar prognosis and pattern of treatment failure as the rest of the group so that inclusion did not impact our analysis.

Optimally, treatment of PIOL should eradicate disease in the eye and prevent spread to the brain, CSF or systemic compartments. The patients included in this series received a heterogeneous array of treatments. The more focused therapy may have been chosen to minimize toxicity, while more extensive therapy was likely chosen to eradicate microscopic, and otherwise undetectable sites of systemic or CNS lymphoma. Our comparison of these two general treatment strategies did not reveal any significant difference with regard to sites of relapse, PFS or OS. Comparison of more specific elements of treatment (e.g. dose or intrathecal administration of methotrexate) was not possible in this retrospective data set with limited sample size for specific treatment paradigms.

Previous reports have suggested that approximately 80% of patients with PIOL will subsequently develop brain lymphoma [13, 16, 17]. In our series, only 56% of patients ultimately progressed. While it is possible that this is an underestimate because of incomplete follow up and the limits of retrospective data, this suggests that some fraction of patients may achieve prolonged control with or without aggressive initial therapy. It may be that patients with PIOL have a relatively less aggressive form of lymphoma than patients presenting with brain lymphoma, or that a much smaller volume of disease is required within the eye to produce symptoms, resulting in earlier presentation. The majority of patients failed in the brain and eyes (92%); however, 8% relapsed systemically. Our data underscores the need for ongoing careful follow-up of all patients treated for PIOL. Patients should have routine follow-up eye examinations, as well as neurological follow-up with periodic MRI scans and prompt investigation of new systemic symptoms.

This study has several limitations. Our data was based on retrospective information abstracted from the medical records by the submitting physician. Patient evaluation and management were heterogeneous across the participating institutions; while this accurately reflects the varied approach to PIOL in academic and community practices, it limits our ability to perform detailed analyses. Central review of pathology was not possible; however, all centers submitting cases have expert lymphoma pathologists who reviewed or confirmed the diagnosis on submitted cases.

In summary, PIOL is a rare subset of PCNSL with a high risk of relapse in the brain and/or eyes despite treatment. Specific treatment recommendations cannot be made on the basis of this analysis; however, our results suggest that focused ocular therapy with close patient follow-up at the completion of active therapy and deferral of more aggressive therapy, such as WBRT or systemic chemotherapy to time of tumor progression may be appropriate. This strategy has the advantage of minimizing or delay treatment-associated toxicity, and does not appear to compromise disease control or survival. Perhaps most importantly, this report highlights the need for ongoing international collaboration to further our understanding and management of rare malignancies such as PIOL.


   appendix
Top
 Abstract
 introduction
 patients and methods
 results
 discussion
 appendix
Acknowledgements
 References
 

IPCG members Affiliation
Abrey, Lauren Memorial Sloan-Kettering Cancer Center
Armitage, James O. University of Nebraska Medical Center
Baars, Joke W. Antoni van Leeuwenhoek ZHS
Batchelor, Tracy Massachusetts General Hospital
Bessell, Eric Nottingham City Hospital
Betensky, Rebecca Harvard School of Public Health
Bierman, Philip Jay University of Nebraska Medical Center
Blay, Jean-Yves Hopital Edouard Herriot/Centre Leon Berard
Borisch, Bettina HUG Geneva Switzerland
Cavalli, Franco Oncology Institute of Southern Switzerland
Chan, Chi-Chao National Eye Institute
Child, Tony The General Infirmary at Leeds
Colombat, Philippe Service d'oncologie medicale
Connors, Joseph M. BC Cancer Agency Vancouver Clinic
D'Addario, Giannicola Kantonsspital St Gallen
DeAngelis, Lisa M. Memorial Sloan-Kettering Cancer Center
Delattre, Jean-Yves CHO Pitie-Salpetriere
Desablens, Bernard Maladies du Sang
Doolittle, Nancy Oregon Health and Science University
Doorduijn, Jeannette K. Erasmus MC, Daniel den Hoed
Dorfman, Molly Massachusetts General Hospital
Ferreri, Andrés San Raffaele Scientific Institute
Fine, Howard National Institutes of Health
Finke, Jürgen University of Freiburg Medical Center
Gilles Salles Centre Hospitalier Lyon-Sud
Girinsky, Théo Institut Gustav Roussy
Glasmacher, Axel University of Bonn
Glass, Jon Fox Chase Cancer Center
Gospodarowicz, Mary Princess Margaret Hospital
Graus, Francesc Hospital Clinic/Barcelona
Grigg, Andrew Royal Melbourne Hospital
Grossman, Stuart Johns Hopkins Oncology Center
Guttenberger, Roland Freiburg, Germany
Haaxma-Reiche, Hanny University Hospital Groningen
Hansen, Mads Rigshospitalet
Harris, Nancy Massachusetts General Hospital
Herrlinger, Ulrich University of Tuebingen
Hoang-Xuan, Khé CHO Pitie-Salpetriere
Hochberg, Fred Massachusetts General Hospital
Hodson, Dan West Anglia Cancer Network Lymphoma Group
Hofer, Silvia Deutsche Kultur Und Familie
Illerhaus, Gerald University of Freiburg Medical Center
Jahnke, Kristoph Charite Universitatsmedizin Berlin
Jean Pierre, Armand Institut Gustav Roussy
Kluin-Nelemans, Hanneke Universitair Ziekenhuis Groningen
Korfel, Agnieszka Charite–Universitaetsmedizin Berlin
Laperriere, Normand The Gerry & Nancy Pencer Brain Tumor Centre
Lister, Andrew St. Bartholomew's Hospital
Levy-Clarke, Grace National Eye Institute
Lugtenburg, Elly University Hospital Rotterdam
Marcus, Robert West Anglia Cancer Network Lymphoma Group
Mason, Warren Princess Margaret Hospital
Neuwelt, Edward A. Oregon Health and Science University
O'Brien, Peter Newcastle Mater Hospital
O'Neill, Brian P. Mayo Clinic and Foundation
Ossenkoppele, Gert van Vrije Universiteit Medisch Centrum
Pels, Hendrik Neurologische Klinik
Ponzoni, Maurilio S. Raffaele H. Scientific Institute
Poortmans, Philip Dr. Bernard Verbeeten Instituut
Pulczynski, Elisa University Hospital Aarhus
Raemaekers, John Radboud U Nijmegen Medical Center
Raizer, Jeffrey Northwestern University
Reni, Michele S. Raffaele H. Scientific Institute
Rosenthal, Mark Royal Melbourne Hospital
Rosta, András Országos Onkológiai Intézet
Rozewicz, Cynthia M. European Organization for Research and Treatment of Cancer
Rubenstein, James L. University of California, San Francisco
Scepanovic, Danijela Clinical Centre of Montenegro
Schiff, David University of Virginia
Schlegel, Uwe University of Bochum
Schmidt-Wolf, Ingo University of Bonn
Sebban, Catherine Centre Leon Berard
Seymour, John Peter MacCallum Cancer Centre
Shenkier, Tamara BC Cancer Agency Vancouver Clinic
Siegal, Tali Hadassah Hebrew University Hospital
Stupp, Roger CHG-Meaux
Swinnen, Lode University Hospital CHUV
Teodorovic, Ivana The Bunting-Blaustein Cancer Research Building
Thiel, Eckhard European Organization for Research and Treatment of Cancer
Thomas, José Charite–Universitaetsmedizin Berlin
Tsang, Richard UZ-Gasthuisberg
van den Bent, Martin Princess Margaret Hospital
van Glabbeke, Martine European Organization for Research and Treatment of Cancer
van Hoof, Achiel European Organization for Research and Treatment of Cancer
van Imhoff, Gustaaf AZ St Jan
Weller, Michael Universitair Ziekenhuis Groningen
Yahalom, Joachim University of Tuebingen
Zucca, Emanuele Memorial Sloan-Kettering Cancer Center Oncology Institute of Southern Switzerland


   Acknowledgements
Top
 Abstract
 introduction
 patients and methods
 results
 discussion
 appendix
 Acknowledgements
References
 
The authors wish to thank the data managers, physicians, nurses and others who contributed to the care and evaluation of the patients, and Judith Lampron for her editorial support. Results presented in part at the American Society of Clinical Oncology Annual Meeting in 2006 and the American Academy of Neurology Annual Meeting in 2007.

Received for publication May 25, 2007. Accepted for publication May 30, 2007.


   References
Top
 Abstract
 introduction
 patients and methods
 results
 discussion
 appendix
 Acknowledgements
 References
 
1. Levy-Clarke GA, Chan CC, Nussenblatt RB. Diagnosis and management of primary intraocular lymphoma. Hematol Oncol Clin N Am (2005) 19:739–749. viii.[CrossRef][Web of Science][Medline]

2. Chan CC, Buggage RR, Nussenblatt RB. Intraocular lymphoma. Curr Opin Ophthalmol (2002) 13:411–418.[CrossRef][Medline]

3. Rothova A, Ooijman F, Kerkhoff F, et al. Uveitis masquerade syndromes. Ophthalmology (2001) 108:386–399.[CrossRef][Web of Science]

4. Freeman LN, Schachat AP, Knox DL, et al. Clinical features, laboratory investigations, and survival in ocular reticulum cell sarcoma. Ophthalmology (1987) 94:1631–1639.[Web of Science]

5. Berenbom A, Davila RM, Lin HS, Harbour JW. Treatment outcomes for primary intraocular lymphoma: implications for external beam radiotherapy. Eye (2006) [Q2].

6. Smith JR, Rosenbaum JT, Wilson DJ, et al. Role of intravitreal methotrexate in the management of primary central nervous system lymphoma with ocular involvement. Ophthalmology (2002) 109:1709–1716.[CrossRef][Web of Science][Medline]

7. Nussenblatt RB, Chan CC, Wilson WH, et al. International Central Nervous System and Ocular Lymphoma Workshop: recommendations for the future. Ocul Immunol Inflamm (2006) 14:139–144.[CrossRef][Web of Science][Medline]

8. Kaplan E, Meir P. Nonparametric estimation from incomplete observations. J Am Statist Assoc (1958) 53:457–481.[CrossRef][Web of Science]

9. Ferreri AJ, Blay JY, Reni M, et al. Relevance of intraocular involvement in the management of primary central nervous system lymphomas. Annl Oncol (2002) 13:531–538.[CrossRef]

10. Hoffman PM, McKelvie P, Hall AJ, et al. Intraocular lymphoma: a series of 14 patients with clinicopathological features and treatment outcomes. Eye (2003) 17:513–521.[CrossRef][Web of Science][Medline]

11. Hormigo A, Abrey L, Heinemann MH, DeAngelis LM. Ocular presentation of primary central nervous system lymphoma: diagnosis and treatment. Br J Haematol (2004) 126:202–208.[CrossRef][Web of Science][Medline]

12. Jahnke K, Korfel A, Komm J, et al. Intraocular lymphoma 2000–2005: results of a retrospective multicentre trial. Graefes Arch Clin Exp Ophthalmol (2006) 244:663–669.[CrossRef][Web of Science][Medline]

13. Char DH, Ljung BM, Miller T, Phillips T. Primary intraocular lymphoma (ocular reticulum cell sarcoma) diagnosis and management. Ophthalmology (1988) 95:625–630.[Web of Science]

14. Akpek EK, Ahmed I, Hochberg FH, et al. Intraocular-central nervous system lymphoma: clinical features, diagnosis, and outcomes. Ophthalmology (1999) 106:1805–1810. [Q3].[CrossRef][Web of Science][Medline]

15. Abrey LE, Batchelor TT, Ferreri AJ, et al. Report of an international workshop to standardize baseline evaluation and response criteria for primary CNS lymphoma. J Clin Oncol (2005) 23:5034–5043.[Abstract/Free Full Text]

16. Peterson K, Gordon KB, Heinemann MH, DeAngelis LM. The clinical spectrum of ocular lymphoma. Cancer (1993) 72:843–849.[CrossRef][Web of Science][Medline]

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S. A. Grimm, C. A. McCannel, A.M.P. Omuro, A. J.M. Ferreri, J. -Y. Blay, E. A. Neuwelt, T. Siegal, T. Batchelor, K. Jahnke, T. N. Shenkier, et al.
Primary CNS lymphoma with intraocular involvement: International PCNSL Collaborative Group Report
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