Demyelinating patterns of injury in primary central nervous system lymphoma
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1 Asian Biomedicine Vol. 3 No. 3 June 2009; Original article Demyelinating patterns of injury in primary central nervous system lymphoma Jitsupa Treetipsatit a, Thamathorn Assanasen a, Paul S. Thorner a,b, Shanop Shuangshoti a a Department of Pathology, Faculty of Medicine, Chulalongkorn University, Bangkok 10330, Thailand. b Department of Laboratory Medicine and Pathobiology, Hospital for Sick Children and University of Toronto, Toronto, Ontario, M5G1x8, Canada Background: Primary CNS lymphoma (PCNSL) can be confused clinically and pathologically with primary demyelinating disease such as multiple sclerosis, and glucocorticoids are known to modify the histologic picture of lymphoma. Objectives: To evaluate the axon and myelin patterns of parenchymal brain damage and to correlate the patterns with the preoperative administration of corticosteroids. Methods: Twenty two cases of PCNSL, all diffuse large B-cell lymphoma, were evaluated for patterns of axonal and myelin alteration. Results were correlated with preoperative steroid administration. Results: Nine cases (41%) showed myelin loss with axonal preservation, mimicking a primary demyelinating disorder. Loss of both myelin and axon, resembling infarction, was observed in 13 cases (59%). No cases demonstrated preservation of myelin. No significant correlation was found between the demyelinating disease pattern and preoperative steroid treatment (p = 0.696). Conclusion: In PCNSL, different demyelinating patterns of injury are encountered and the pattern is not influenced by glucocorticoid treatment. Awareness of this situation is important when assessing small brain biopsy specimens where tumor cells may not be readily identified. Keywords: Axon, CNS lymphoma, demyelination, multiple sclerosis, myelin. Pathological diagnosis of central nervous system lymphoma is usually straightforward provided representative tissue is obtained. However, the lymphoma cells may escape detection in small biopsy specimens, such as those obtained by stereotactic procedure. Corticosteroid administration prior to biopsy in order to decrease brain edema is another important factor that causes difficulty in making the diagnosis due to its rapid and pronounced lympholytic action [1-9]. In biopsies of primary CNS lymphoma (PCNSL) in which the diagnostic cell is absent, reactive astrocytes adjacent to the main tumor and T-cell infiltrates of varying degrees can be confused with reactive processes encountered in other neurological conditions [1-3]. Primary demyelinating disease, Correspondence to: Shanop Shuangshoti, MD, Department of Pathology, Faculty of Medicine, Chulalongkorn University, Rama IV Rd, Bangkok 10330, Thailand. shanop@ gmail.com especially multiple sclerosis (MS), is one of the diagnostic traps, and a number of case reports as well as small case series have described PCNSL with clinical and pathological features resembling MS [7-13]. Features common to both conditions include the preferential involvement of white matter, gliosis with non-specific inflammation, and demyelination with preservation of axons. In PCNSL after steroid treatment, both the MSlike (myelin loss but preserved axons) and infarctionlike (loss of both axons and myelin) patterns have been noted [9-13]. However, the relative frequency of these two patterns and the correlation between the pattern and steroid treatment has not been well studied. Axonal destruction could either be the result of a direct insult by lymphoma cells or a reactive inflammatory process accompanying the tumor [14-16]. Furthermore, the angiocentric pattern of lymphoma may cause ischemic damage to axons [14, 15]. Since corticosteroids induce apoptosis of lymphoid cells [1-6], as well as reduce the inflammatory response, we hypothesized that
2 262 J. Treetipsatit, et al. preoperative steroid administration might favor axon preservation in PCNSL and lead to a predominance of the MS-like pattern of injury. Therefore, we studied a series of cases of PCNSL to evaluate the axon and myelin patterns of parenchymal brain damage and correlate the patterns with the preoperative administration of corticosteroids. Materials and methods Twenty-two examples of PCNSL along with demographic data were retrieved from the pathology files and medical records of the King Chulalongkorn Memorial Hospital, Bangkok, Thailand. All were reviewed and classified according to the recent WHO classification for hematologic malignancies [17]. Materials from 21 cases were obtained from stereotactic brain biopsy, and one case from open biopsy. Eight- and ten-micrometer-thick sections of formalin-fixed, paraffin-embedded tissue were stained, respectively, with modified Bielschowsky (for axon) [18] and Luxol fast blue (for myelin) [19] protocols. Using normal white matter as a control, the axon density was graded as 1+ to 3+ (stained processes <10%, 10-50%, and >50%, respectively). Axons were considered to be preserved in cases with an axon density >2+. Myelin pallor was recorded as present or absent on the Luxol fast blue myelin stain. Scoring was done on the brain tissue adjacent to the tumor. Results were analyzed using the Statistic Package for the Social Sciences for Windows version 13.0 (SPSS Inc., Chicago, IL, USA). Comparison between groups was made by the Fisher s exact or chi-square test when applicable. A p-value of <0.05 was considered to be significant. Results All 22 PCNSLs were classified as diffuse large B cell lymphoma. Ten patients (45.5%) were male, and 12 (54.5%) were female. The mean age was 60.9 years (median age, 67.5; and age range, 30-79). HIV status was known in 19 cases, 17 were negative; the two positive cases were ages 33 and 37. Twelve patients (73%) had a solitary brain lesion, four (25%) with a frontal lobe mass, four (25%) with a basal ganglion mass, two (12.5%) with a parietal lobe mass, 2 (12.5%) with a corpus callosum mass, and one each with a mass in the occipital lobe, thalamus, periventricular region, and suprasellar region. The remaining six cases (27%) had multiple brain lesions. In general, lymphoma cells were easily identified except for three patients who received preoperative steroids, in whom the malignant cells were sparse. Table 1 summarizes patterns of axonal and myelin changes. Nine of 22 cases (41%) showed myelin loss with axonal preservation (MS-like pattern) (Fig. 1). Loss of both myelin and axon (infarct-like pattern) was observed in 13 cases (59%). No cases demonstrated preservation of myelin. Information regarding preoperative corticosteroid administration was available in 16 cases, and 13 of them received treatment. Treatment was given to reduce brain edema and followed a standard protocol, which meant that all patients received similar amounts of steroids. Axonal preservation was observed in 5/13 patients who received, and 1/3 who did not received steroid. No significant correlation was found between the pattern of injury and preoperative corticosteroid treatment (p=0.696, Fisher s exact). Table 1. Patterns of axon/myelin changes in primary CNS lymphoma (PCNSL). Axon Myelin Number of cases (22) No axonal changes No myelin changes 0 No axonal changes Demyelination 9 (41%) Axonal loss No myelin changes 0 Axonal loss Demyelination 13 (59%)
3 Vol. 3 No. 3 June 2009 MS-like pattern in PCNSL 263 Fig. 1 Histological features of brain parenchyma adjacent to primary CNS lymphoma. Upper row shows the infarct-like pattern with infiltrates of foamy histiocytes and few reactive astrocytes (A). Loss of both axons and myelin is noted (B). Lower row demonstrates the multiple scleosis-like pattern, with reactive astrogliosis and infiltrates of foamy histiocytes (C). Preservation of axon but loss of myelin is evident (D). (A and C: Hematoxylin and eosin stain, x 400; B and D: Modified Bielschowsky s silver stain, x 400). Discussion The incidence of primary central nervous system lymphoma (PCNSL) has increased over the last three decades, not only in immunocompromised but also in immunocompetent patients [1-3]. PCNSL can be confused clinically and pathologically with primary demyelinating disease, such as multiple sclerosis (MS), but only a few reports actually document this [7, 9-13]. According to the PCNSL cases reported by Alarcia et al. [10], Kuroda et al. [11] and Yang et al. [12]; (one case each) all initial brain biopsies showed typical features of MS (demyelination with conservation of axons and perivascular reactive inflammatory cell infiltration). The patients ages were between 33 to 38 years, and one [10] had been treated with dexamethasone prior to stereotactic biopsy in order to decrease brain edema. After the initial biopsy, all patients developed a progressive neurological deficit, an uncommon clinical course for MS. A repeat biopsy in each patient revealed diffuse large B cell lymphoma. In addition to the MS-like morphology, Alderson et al. [13] also noted non-specific inflammation (1 case) and normal brain tissue (one case) in the initial brain biopsies of a series of four immunocompetent patients with PCNSL. It was concluded that the MS-like demyelinating pattern is an early pathological finding of PCNSL that pathologists should be aware of [10, 11-13]. In contrast to findings mentioned above, Choi et al. [4] recently reported pathological findings of four cases of PCNSL treated preoperatively with corticosteroids. All had features of reactive gliosis with axonal loss and myelin destruction (infarct-like pattern), and lymphoma cells were not detected by morphological assessment. In our study, which examined 22 PCNSL cases, lymphoma cells were identified in all cases and both the MS-like demyelinating and infarct-like
4 264 J. Treetipsatit, et al. patterns were noted, involving nine (41%) and 13 (59%) cases, respectively. Although we found no significant correlation between the presence or absence of MS-like pattern and the preoperative corticosteroid treatment, the extent of MS-like pattern could not be assessed since most of our materials were small (most from stereotactic biopsy). Quantitative evaluation of the MS-like pattern, using large tissue samples, and its possible correlation with steroid treatment deserves future study. From a practical standpoint, it should be noted that the prevalence of MS in Eastern Asia is low in terms of the worldwide epidemiology [20] with an estimated cases per 100,000 [21]. Therefore, a diagnosis of MS in these regions of the world has to be made with caution. Morphological assessment alone is insufficient since the MS-like demyelinating pattern is not specific for that disease. Indeed, our study has demonstrated an MS-like morphology in almost half of the cases of PCNSL. Progressive neurological deficit is an uncommon clinical course for MS, and when present, should raise a concern for other diagnoses. The age of onset of the disease is helpful to distinguish MS from PCNSL in immunocompetent patients since PCNSL typically affects older patients than does MS. The mean age of our immunocompetent PCNSL patients of 61.4 years correlates well with the worldwide epidemiologic data of PCNSL in immunocompetent hosts (>60 years, median age=53-57) [2, 3]. The mean age of MS onset across Asia, including the Thai population [22], is younger (between 25 to 33 years) [21] Cases of PCNSL in immunodeficient patients could fall into this age group and could lead to confusion in the diagnosis. In cases for which the diagnosis is in doubt, molecular determination of B-lymphoid clonality (given that the majority of PCNSLs are B-cell [14-16] may enhance detection of lymphoma cells that are not apparent by morphological evaluation [4]. Conclusion MS-like demyelinating pattern and an infarct-like pattern are commonly found in PCNSL. There is no correlation between the patterns of brain parenchymal changes and preoperative corticosteroid treatment, but lymphoma cells can sometimes be difficult to identify after steroid administration. This should always be kept in mind when assessing small brain biopsy specimens, especially in patients at an age uncommon for MS, and in regions where the prevalence of MS is low. Acknowledgement The authors gratefully thank Ms Soisuda Sangprakarn for her excellent technical assistance. The authors have no conflict of interest to report. References 1. Schlegel U, Schmidt-Wolf IGH, Deckert M. Primary CNS lymphoma: clinical presentation, pathological classification, molecular pathogenesis and treatment. J Neurol Sci. 2000; 181: Batchelor T, Loeffler JS. Primary CNS lymphoma. J Clin Oncol. 2006; 24: Hochberg FH, Baehring JM, Hochberg EP. Primary CNS lymphoma. Nat Clin Pract Neurol. 2007; 3: Choi YL, Suh YL, Kim D, Ko YH, Sung CO, Lee JI. Malignant lymphoma of the central nervous system: difficult histologic diagnosis after glucocorticoid therapy prior to biopsy. Clin Neuropathol. 2006; 25: Geppert M, Ostertag CB, Seitz G, Kiessling M. Glucocorticoid therapy obscures the diagnosis of cerebral lymphoma. Acta Neuropathol (Berl). 1990; 80: Weller M. Glucocorticoid treatment of primary CNS lymphoma. J Neurooncol. 1999; 43: Partap S, Spence AM. Spontaneously relapsing and remitting primary CNS lymphoma in an immunocompetent 45-year-old man. J Neurooncol. 2006; 80: Hunt MA, Jahnke K, Murillo TP, Neuwelt EA. Distinguishing primary central nervous system lymphoma from other central nervous system diseases: a neurosurgical perspective on diagnostic dilemmas and approaches. Neurosurg Focus. 2006; 2:E3. 9. Pirotte B, Levivier M, Goldman S, Brucher JM, Brotchi J, Hildebrand J. Glucocorticoid-induced long-term remission in primary cerebral lymphoma: case report and review of the literature. J Neurooncol. 1997; 32: Alarcia R, Ara JR, Marla E, Barrena MR, Gimenez-Mas JA, Capablo JL, Serrano M. Demyelinating pseudotumoral lesion prior to a primary cerebral lymphoma. Rev Neurol. 2000; 31: Kuroda Y, Kawasaki T, Haraoka S, Fujiyama F, Kakigi R, Abe M, et al. Autopsy report of primary CNS B-cell lymphoma indistinguishable from multiple sclerosis: diagnosis with the immunoglobulin gene rearrangements analysis. J Neurol Sci. 1992; 111: Yang JH, Wu SL. Multiple sclerosis preceding CNS lymphoma: a case report. Acta Neurol Taiwan. 2007; 16:92-7.
5 Vol. 3 No. 3 June 2009 MS-like pattern in PCNSL Alderson L, Fetell MR, Sisti M, Hochberg F, Cohen M, Louis DN. Sentinel lesions of primary CNS lymphoma. J Neurol Neurosurg Psychiatr. 1996; 60: Prayson AR, Cohen ML. Practical Differential Diagnosis in Surgical Neuropathology. New Jersey: Humana Press, 2000; p Kleihues P, Cavence WK (eds). World Health Organization Classification of Tumors. Pathology and Genetics of Tumors of the Nervous System. Lyon: IARC Press. 2000; p Fuller GN, Goodman JC. Practical Review of Neuropathology. Philadelphia:Lippincott Williams & Wilkins. 2001; p Jaffe ES, Harris NL, Stein M, Vardiman JW (eds). World Health Organization Classification of Tumors. Pathology and Genetics of Tumors of Hematopoietic and Lymphoid Tissues. IARC Press:Lyon. 2001; p Lowe J. Techniques in neuropathology. In: Bancroft JD and Stevens A (eds). Theory and Practice of Histological Techniques (4th ed). Hong Kong: Churchill Livingston, 1996; p Prophet EB, Mills B, Arrington JB, Sobin LH (eds). Armed Forces Institute of Pathology: Laboratory Methods in Histotechnology. Washington DC: American Registry of Pathology. 1994; p Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG. Multiple sclerosis. N Engl J Med. 2000; 343: Wasay M, Katri IA, Khealani B, Sheerani M. MS in Asian countries. Int MS J. 2006; 13: Siritho S, Prayoonwiwat N. A retrospective study of multiple sclerosis in Siriraj Hospital, Bangkok, Thailand. Can J Neurol Sci. 2007; 34:
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