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Orbit, 26:83–88, 2007
Copyright c 2007 Informa Healthcare
ISSN: 0167-6830
DOI: 10.1080/01676830601169148
RESEARCH ARTICLE
Ocular Adnexal Lymphoma Classified using Histology and Stage, but also Gender is a Marjolijn B. Plaisier
Department of Ophthalmology,
ABSTRACT Introduction: Ocular adnexal lymphomas (OAL) belong to the
most common malignancies of the orbit and eyelids and are now classified according to the WHO classification system. MALT lymphoma appears to be Downloaded By: [University of Maastricht] At: 12:49 6 August 2007 Daisy M.D.S. Sie-Go
the most frequent OAL. Histology type and stage of OAL have been found predictors of patient survival. Purpose: To evaluate the outcome of a cohort of patients with OAL using the WHO classification and to compare outcome predictors with those of other studies using the WHO classification. Design:Retrospective, cohort study. Materials and methods: Clinical profile at presen- Tos T.J.M. Berendschot
University Eye Clinic
tation, initial complaints and findings, classification and stage, treatment and outcome of 54 patients with biopsy proven and re-analyzed OAL seen between1 January 1992 and 1 January 2002 at the UMC Utrecht, NL, were evaluated.
Eefke J. Petersen
Kaplan-Meier survival analysis and multivariate Cox-regression survival analysis were applied to assess predictors of outcome. Results: Forty nine patients were University Medical CenterUtrecht, The Netherlands found to have primary and five secondary lymphomas. Of those with primaryOAL, 27 had MALT, eight diffuse large B-cell, six mantle cell and eight follic- Maarten P. Mourits
ular cell lymphoma. Histology and stage showed a significant association with survival (Log-rank test: p = 0.001 and p = 0.002, respectively). A multivariate Cox-regression survival analysis showed histological type to be the only signif- Utrecht and Academic MedicalCenter Amsterdam, The icant predictor for outcome. Looking at the dichotomy full remission versus not completely cured, gender was found to be a significant predictor (Log-ranktest: p = 0.005). Conclusion: This study showed that not only histology type andstage, but also gender is a predictor of outcome.
KEYWORDS Non-hodgkin lymphoma; WHO-classification; MALT lymphoma; staging;
histology
Received 31 May 2006;Accepted 24 August 2006.
Address correspondence to Prof. dr.
INTRODUCTION
M.P. Mourits, MD PhD, Department ofOphthalmology, Academic Medical Ocular adnexal lymphoma (OAL) is the most common malignant tumor of the eyelids, conjunctiva and orbit, accounting for about 8% of all tumors seen Amsterdam, The Netherlands. E-mail:m.p.mourits@amc.uva.nl Patient care requires rapid explanation of diagno- Retroseptal tumors predominantly outside the lacrimal sis and prognosis of disease and the question is how gland were classified as ‘orbital’, predominantly within this can be achieved in the management of a tumor as the lacrimal gland as ‘lacrimal,’ predominantly presep- variable as AOL. Studies using the Revised European- tal tumors as ‘eyelid’ and tumors largely confined to American classification of Lymphomas (REAL) already the conjunctiva, the classical ‘salmon patch’ lesions, as showed that survival of patients with OAL is related ‘conjunctival’. The histological diagnosis was based on to the stage and histology type of the disease.2−6 The paraffin tissue biopsies and the use of immunohisto- introduction, however, of the World Health Organiza- tion (WHO) modification of the REAL classification,7 For classification and staging, the WHO modifica- required a re-appraisal of these assessments. Studies us- tion of the REAL classification was used. All patients ing the WHO classification confirmed that histolog- were referred to a hemato-oncologist (EJP) for staging.
ical subtype and stage are predictors of patient mor- For staging, the Ann Arbor classification was used. We bidity and survival.8−10 Jenkins et al.,9 in the largest classified patients with bilateral orbital, but without series till present, assessed that also other factors, like extra-orbital involvement as Ann Arbor stage I. We con- deep localization (especially those lymphomas located sidered patients to have primary disease if there was no in the lacrimal gland), the presence of a Relative Affer- evidence of systemic disease prior to the diagnosis of ent Pupillary Defect and old age are related to a less favorable outcome. However, in none of these studies Treatment options applied were: observation, radio- a relationship has been found between prognosis and therapy, chemotherapy or a combination of radio- and gender. In this study, we evaluated the clinical profile chemotherapy. Local radiotherapy treatment consisted at presentation including the time relapse between on- of a total dosage of 30–40 Gy in multiple sessions in set of complaints and diagnosis, initial complaints and almost all cases. Chemotherapy treatment ranged from clinical findings, classification, whether the tumor pre- oral chloorambucil to C(H)OP (cyclofosfamide, dox- Downloaded By: [University of Maastricht] At: 12:49 6 August 2007 sented uni- or bilaterally, stage of the disease, treatment orubicin, vincristine and prednisolone) regimens. The and outcome of 54 patients with OAL, referred to a outcome measures we used were: alive with no remis- tertiary referral center, classified and re-classified using sion, alive with remission (active disease), death due the WHO classification, and compared our results with to lymphoma, death due to other cause and lost to other studies using the WHO classification.
Statistical Analysis
METHOD AND MATERIAL
For statistical analysis, SPSS software, version 13.0 We retrieved computer stored data from the Depart- was used. To assess the predictive value of age, gen- ment of Pathology of all patients diagnosed with an der, presenting complaints and findings, histology type, OAL at the University Medical Center Utrecht, the stage, and treatment on the outcome, Kaplan-Meier sur- Netherlands, between 1 January 1992 and 1 January vival and Cox-multivariate regression survival analysis 2002. We only included biopsy proven lymphomas with involvement of the orbit, eyelids, conjunctivaand lacrimal gland. For the purpose of this study, all biopsies were re-examined and reclassified according Clinical Characteristics
to the WHO classification system by one pathologist(DMDSS-G).
Fifty four patients were diagnosed with OAL in the From the patients thus collected, we evaluated the period between 1 January 1992 and 1 January 2002. Of time elapsed between onset of complaints and histo- these patients, 25 were male and 29 were female. Forty logical diagnosis, age, gender, initial complaints and nine patients had primary disease; in five patients (9%) signs and symptoms, mono- or bilaterality, the histolog- the orbital lymphoma developed secondary to systemic ical classification, the staging of the disease, the treat- disease. At presentation, patients ranged in age from ment given and the outcome in terms of survival and 24 to 89 years with a mean age of 64 years (Table 1).
alive with disease. Clinical findings and CT- and MRI- The mean follow-up period was 46 months (range 7– scans served to determine localization of the tumor: 129). The interval between symptoms and the time of M.B. Plaisier et al.
TABLE 1 Comparison of different features of ocular adnexal lymphomas (Percentages between brackets, n = number, y = years, mo =
months)

Downloaded By: [University of Maastricht] At: 12:49 6 August 2007 diagnosis ranged from one to 72 months, the mean in- help was swelling and or proptosis. The most common terval being 13 months. There was no significant differ- findings were palpable mass, proptosis, motility distur- ence of the time period elapsed between the onset of bance, ptosis and globe displacement. Localization of complaints and the histological diagnosis between the the tumor involved the orbit in 23 cases, the conjunc- histology subgroups of the primary OAL. For the whole tiva in 16 cases, the lacrimal gland in nine cases and the group, the most common reason for seeking medical eyelid(s) in six cases. In 27 of 49 patients with primary Ocular Adnexal Lymphoma
FIGURE 1 Survival function for different diagnoses.
disease the diagnosis according to the WHO classifica- died due to other causes (Figs. 1 and 2). Three patients Downloaded By: [University of Maastricht] At: 12:49 6 August 2007 tion was MALT lymphoma. Eight patients had diffuse large B cell lymphoma and another eight had follicular Of patients with secondary disease, two of them lymphoma (grade 1–3). In six patients the diagnosis was showed complete remission, one patient was alive with mantle cell lymphoma. Ann Arbor staging stage I was disease and two patients died of lymphoma. The mean assessed in 61% of cases, whereas 22% of patients had follow-up in patients with secondary lymphoma was stage IV disease. The following subtypes of OAL’s in pa- tients with secondary disease were found: one follicular Patients with primary disease had an average follow- lymphoma, grade 1, two follicular lymphomas, grade up of 45 months. Most patients (n = 30, 61%) were clas- 3, one peripheral T-cell lymphoma, and one secondary sified as stage I according to the Ann Arbor classifica- tion. Of these patients, 19 showed complete remission,five were alive with disease and one patient died of lym- Treatment and Outcome
phoma (three died of a non-OAL related cause, two One patient with primary (MALT cell) lymphoma were lost to follow-up). Eleven patients had stage IV was observed. Twenty three patients with primary dis- disease, of these patients one reached a remission, three ease were treated with radiotherapy alone, 17 patients patients were alive with disease and five patients died with chemotherapy alone, eight patients received a combination of radiotherapy and chemotherapy. Of Statistical analysis of the following parameters, gen- the five patients with secondary disease, one patient der, age, time elapse between onset of complaints and was treated with radiotherapy alone, two patients re- final diagnosis, localization, whether the presentation ceived chemotherapy and two patients a combination was uni- or bilateral, WHO-subtype, and stage of the of radio- and chemotherapy. Of all patients (primary disease, of the 49 patients with primary disease revealed and secondary), 27 (50%) responded well to treatment the following: Using univariate Kaplan-Meier survival and showed complete remission after an average follow- analysis, diagnosis and stage showed a significant as- up period of 46 months. At the end point of our study, sociation with outcome (Log-rank test p = 0.001 and 11 patients (20%) were alive with disease, nine patients p = 0.002, respectively, see Figs. 1 and 2). A multivari- (17%) died due to the lymphoma, while four patients ate Cox-regression forward conditional survival analysis M.B. Plaisier et al.
FIGURE 2 Survival function for different stages.
Downloaded By: [University of Maastricht] At: 12:49 6 August 2007 showed diagnosis to be the only independent signifi- site, and duration. Also, in a recent study with a lim- cant predictor. We also looked at the dichotomy com- ited number of patients (n = 24), no correlation of these plete remission versus not completely cured (death due parameters with survival could be assessed.11 All these to OAL plus alive with OAL). Gender yielded to be the studies, however, were unanimous in their conclusion only significant predictor (Log-rank test p = 0.005. Lym- that OAL’s are most frequently found within the or- phoma related death rate and/or recurrence rate was bit. Jenkins et al.,9 in the largest series described till significantly higher in females than in males (p = 0,03).
present, found bilateral disease and lacrimal gland lo-calization at presentation correlated with a higher rate DISCUSSION
of disseminated disease and systemic disease, bilateral This study confirms previous studies stating that tu- disease, and deep orbital localization correlated with a mor subtype (WHO classification) and stage of the worse prognosis. Relative old age and (slightly) worse disease (Ann Arbor classification) are decisive determi- prognosis were found to be related with each other. A nants of survival. With respect to the most common long history of disease, however, was found to be re- OAL subtypes, patients with a MALT type OAL have lated to a smaller chance of dissemination and a better the best, patients with a mantle cell type the worst and prognosis, apparently because a long history of disease those with a diffuse large B-cell or follicular cell type reflects milder pathology subtype. Sullivan et al.,10 in a an intermediate prognosis. As far as we could retrieve, series of 69 patients, found stage at presentation, tumor our study is the first to show that female patients with histology, primary or secondary status, and whether the an OAL have a worse prognosis. Of 46 patients with tumor was uni- or bilateral, determinants of survival.
primary disease at the final evaluation, 5 of 23 males In general, not unlike any malignant tumor, more ag- versus 12 of 23 females had died of the lymphoma or gressive tumor histology together with stage (bilateral were living with a recurrence (p = 0.03).
disease can be considered as more advanced disease) de- Whereas studies in the pre-WHO classification termines the outcome of OAL. Old age, deep localiza- era,2,3,5,6 already showed that histological subtype and tion and female gender, as found in our series, may also stage of the disease determined the outcome, these stud- influence the outcome in a worse direction. The fact ies failed to demonstrate the role of gender, anatomic that our study did not confirm that age, duration of the Ocular Adnexal Lymphoma
disease prior to the diagnosis, localization and whether [2] Knowles DM, Jakobiec FA, McNally L, Burke JS. Lympoid hyperplasia the presentation was uni- or bilateral were related to and malignant lymphoma occurring in the ocular adnexa (Orbit,conjunctiva, and eyelids); A prospective, multiparametric analysis the outcome can be explained by the relatively small of 108 cases during 1977 to 1987. Hum Pathol. 1990; 21:959– numbers as compared to some other studies.4,9 [3] Coupland SE, Krause L, Delecluse HJ, Anagnostopoulos I, Foss It is therefore interesting, that—as far as we could HD, Hummel M, Bornfeld N, Lee WR, Stein H. Lymphoprolifera- retrieve—this study showed a relationship between out- tive lesions of the ocular adnexa. Ophthalmology 1998; 105:1430– come and gender for the first time. We assessed this [4] Jenkins Ch, Rose GE, Bunce C, Wright JE, Cree IA, Plowman N, relationship by grouping together patients who either Lightman S, Moseley I, Norton A. Histological features of ocular had a tumor related death or a recurrence, which has adnexal lymphoma (REAL classification) and their association withpatient morbidity and survival. B J Ophthalmol. 2000; 84:907– Other studies have shown, that patients with a MALT [5] Auw-Haedrich C, Coupland SE, Kapp A, Schmitt-Gr ¨aff, Buchen R, or follicular cell OAL perform an excellent prognosis for Witschel H. Long term outcome of ocular adnexal lymphoma sub-typed according to the REAL classification. B J Ophthalmol 2001; life, although MALT lymphomas are known for their high distant relapse rate.8,12 In this study, relapse rates [6] McKelvie PA, McNab A, Francis IC, Fox R, O’Day J. Ocular adnexal lymphoproliferative disease: a series of 73 cases. Clin Experiment for primary MALT and follicular cell subtypes were 14 and 50% after a mean follow up of 50 and 56 months [7] Jaffe ES, Harris NL, Diebold J. et al. World Health Organization clas- respectively. In spite of the normal protocol of local sification of neoplastic diseases of the mematopoietic and lymphoidtissues. Am J Clin Pathol. 1999; 111(suppl):S8–12.
therapy of 30–40 Rad radiotherapy, two patients with a [8] Fung CY, Tarbell NJ, Lucarelli MJ, Goldberg SI, Linggood RM, Harris primary MALT lymphoma (7%), one with a B-cell, three NL, Ferry JA. Ocular adnexal lymphoma: Clinical behaviour of distinctWorld Health Organization classification subtypes. Int J Radiat Oncol with a mantle cell and one with a primary follicular cell Biol Phys. 2003; 57:1382–91.
lymphoma (13%) died following disseminated disease.
[9] Jenkins C, Rose GE, Bunce C, Cree I, Norton A, Plowman PN, In conclusion, next to histological subtype and stage, Mosely I, Wright. Clinical features associated with survival of pa-tients with lymphoma of the ocular adnexa. Eye. 2003; 17:809– and next to known clinical parameters as localization Downloaded By: [University of Maastricht] At: 12:49 6 August 2007 and uni- or bilateral presentation, gender seems to be a [10] Sullivan TJ, Whitehead K, Williamson R, Grimes D, Schlect D, Brown I, Dickie G.Lymphoproliferative diasease of the ocular Adnexa: A predictor of outcome in ocular adnexal lymphoma.
clinical and pathological study with statiscal analysis of 69 patients.
Orbit. 2005; 3:177–184.
REFERENCES
[11] Nola M, Lukenda A, Bollman M, Kalauz M, Petrovecki M, Bollmann R. Outcome and prognostic factors in ocular adnexal lymphoma.
[1] Rootman J, Chang W, Jones D. Distribution and differential diag- Croat Med J. 2004; 45:328–332.
noses of orbital disease. In: Rootman J, editor. Diseases of the orbit: [12] Cahill M, Barnes C, Moriarty P, Daly P, Kennedy S. Ocular adnexal A multidisciplinary approach. 2nd edition. Philadelphia: Lippincott lymphoma – comparison of MALT lymphoma with other histological Williams & Wilkins. 2003; 53–84.
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M.B. Plaisier et al.

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