Methotrexate-associated Lymphoproliferative Disorder of the Stomach Presumed to Be Mucosa-associated Lymphoid Tissue Lymphoma
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1 doi: /internlmedicine Intern Med 57: , CASE REPORT Methotrexte-ssocited Lymphoprolifertive Disorder of the Stomch Presumed to Be Mucos-ssocited Lymphoid Tissue Lymphom Sho Ishigki 1, Ttsuhiro Msok 1, Hisko Kmeym 1,MihoKwid 2, Kori Kmeym 2, Tkehiko Mori 3 nd Tknori Kni 1 Astrct: The numer of ptients with methotrexte-ssocited lymphoprolifertive disorder (MTX-LPD) is incresing. We descrie cse of MTX-LPD of the stomch. After tretment with methotrexte for rheumtoid rthritis, the ptient developed left cervicl lymphdenopthy nd n ulcertive lesion in the stomch, which ws presumed to e mucos-ssocited lymphoid tissue (MALT) lymphom. However, we suspected MTX- LPD, sed on the clinicl course nd the positivity of in situ hyridiztion for the detection of the Epstein- Brr encoding region. After the cesstion of MTX, the left cervicl lymphdenopthy nd the gstric lesion disppered. This is first report of gstric MTX-LPD tht ws presumed to e MALT lymphom. Key words: methotrexte, lymphoprolifertive disorder, rheumtoid rthritis, MALT lymphom (Intern Med 57: , 2018) () Introduction Rheumtoid rthritis (RA) is the most common utoimmune inflmmtory rthritis in dults (1). Methotrexte (MTX) hs ecome the initil drug of choice for treting most ptients with RA (2). Both the usge nd dosge of MTX hve incresed consistently (3). Lymphoprolifertive disorders (LPDs) occsionlly develop in individuls with immunodeficiency disorders, such s primry immune disorders, humn immunodeficiency virus infection, or itrogenic immunosuppression following solid orgn or one mrrow llogrft trnsplnttion, or itrogenic immunosuppression in ssocition with the dministrtion of MTX (4). Itrogenic immunodeficiency-ssocited LPD is ctegorized s n immunodeficiency-ssocited LPD in the Revised 4th version of World Helth Orgniztion clssifiction of lymphoid neoplsms (5). The popultion with RA is incresing in Jpn; this cn e ttriuted to the incresing of ging popultion (6). Along with this chnge, the numer of ptients with MTX- LPD is incresing (7). The most common presenting symptom of MTX-LPD is superficil lymphdenopthy (33.3%), followed y the presence of extrnodl msses (27.0%) ndmuch less frequently-dominl or one pin, fever, cough, nd thromocytopeni (4). However, MTX-LPD of the stomch is uncommon (8). We herein report cse of MTX-LPD of the stomch. Cse Report The ptient ws n 83-yer-old womn who hd een undergoing medicl tretment for RA (4 mg/week of MTX) since 200X nd who hd een followed up t the Deprtment of Rheumtology t our hospitl. She ws concurrently dignosed with nonsteroidl nti-inflmmtory drug-induced gstric ulcer t the Deprtment of Gstroenterology nd Heptology. Oservtion with yerly esophgogstroduodenoscopy (EGD) ws susequently initited. In June 200X+7, she complined of left cervicl lymphdenopthy without Division of Gstroenterology nd Heptology, Deprtment of Internl Medicine, Keio University School of Medicine, Jpn, Deprtment of Dignostic Pthology, Keio University School of Medicine, Jpn nd Division of Hemtology, Deprtment of Internl Medicine, Keio University School of Medicine, Jpn Received for puliction Jnury 19, 2018; Accepted for puliction April 17, 2018 Correspondence to Dr. Ttsuhiro Msok, msok@keio.jp 3249
2 Figure 1. Cervicl non-contrst computed tomogrphy () nd cervicl non-contrst T2-weighted mgnetic resonnce imging () scns reveling left cervicl lymphdenopthy. The re of lymphdenopthy is circled. 7 month fter cesstion of MTX c d Figure 2. In July 200X+9, n ulcertive lesion ws found in the lesser curvture of the stomch y esophgogstroduodenoscopy (, ). Seven months fter the cesstion of methotrexte, scrring of the previous ulcertive lesion ws confirmed y esophgogstroduodenoscopy (c, d). other symptoms (e.g., morning stiffness, fever, weight loss, or night swets). A physicl exmintion reveled left cervicl lymphdenopthy of pproximtely 3 3 cm in dimeter. Computed tomogrphy nd mgnetic resonnce imging scns of the ody nd neck were immeditely tken nd reveled left cervicl nd suprclviculr lymphdenopthy (Fig. 1 nd ). Lortory tests reveled norml lood cell count, elevted immunogloulin (Ig)M (1,204 mg/dl; reference rnge, mg/dl), nd n elevted solule interleukin-2 receptor level (652 U/mL; reference rnge, U/mL). Bsed on these findings, MTX-LPD ws suspected nd tretment with MTX ws discontinued in June. In July 200X+7, follow-up EGD for the exmintion of the gstric ulcer reveled n ulcertive lesion t the lesser curvture of the stomch (Fig. 2 nd ). Biopsy specimens of the ulcertive lesion showed lymphoid cell infiltrtion 3250
3 c MALT1 trnsloction. Bsed on these results, pthologicl dignosis of mucos-ssocited lymphoid tissue (MALT) lymphom ws mde. In the sme month, we prescried vonoprzn [20 mg, twice dily (.i.d.)], clrithromycin (400 mg,.i.d.), nd moxicillin (750 mg,.i.d.) for 7 dys to tret gstric MALT lymphom ecuse positive ure reth test (19.3%, stndrd rnge 0-2.4%) result indicted Helicocter pylori infection (9, 10). However, on the sis of the ptient s clinicl history, MTX-LPD ws considered s one of the differentil dignoses. Using iopsy specimen otined during the first EGD procedure, in situ hyridiztion ws retrospectively performed to detect the Epstein-Brr encoding region (EBER). The result ws positive, indicting Epstein-Brr virus (EBV) infection (Fig. 5). In Septemer 200X+7, 3 months fter the discontinution of MTX tretment, physicl exmintion reveled tht the left cervicl lymphdenopthy hd disppered. At the sme time, the incresed serum level of IgM hd decresed to within the reference rnge (Fig. 6). In Novemer 200X+7, t 4 months fter tretment for H. pylori infection, H. pylori erdiction ws confirmed y negtive H. pylori stool ntigen test result. In Ferury 200 X+8, t 7 months fter the first EGD procedure, second EGD procedure reveled scrring t the previous site of the ulcertive lesion (Fig. 2c nd d). According to previous report, fter the erdiction of H. pylori in ptients with MALT lymphom, remission from lymphom ws chieved within medin time of 5 months (11). This ws in line with our cse. However, cse of EBV-positive gstric MALTom hs een reported (12), the rte of EBV infection in gstric MALTom hs previously een reported to e low (13). Conversely, the rte of EBV infection in gstric MTX-LPD hs lso een reported to e high (14). Bsed on the ptient s entire clinicl course nd previous reports, which were grounds for the dignosis of MTX-LPD, we finlly dignosed the ptient with MTX-LPD nd not MALT lymphom. 200 Figure 3. Lymphoid cell infiltrtion in the lmin propri with Hemtoxylin nd Eosin stining in low-power field (: 40), middle-power field (: 100) nd high-power field (c: 400). Scle r indictes 20 μm (), 50 μm (), nd 200 μm (c), respectively. into the lmin propri (Fig. 3-c) In these specimens, CD 20-positive (Fig. 4) nd CD79α-positive (Fig. 4) B lymphocytes were predominnt, while CD3-positive T lymphocytes (Fig. 4c) nd CD5-positive T lymphocytes (Fig. 4d) were less predominnt. Moreover, the specimens were CD 10- nd CD 21-negtive (Fig. 4e nd f). The κ/λ rtio of the B lymphocytes showed no dissocition (Fig. 4g nd h). The iopsy specimen ws not exmined to evlute t(11;18)/api Discussion In our cse, without dditionl informtion out the ptient s clinicl course nd EBER positivity the presumed pthologicl dignosis would hve een MALT lymphom. MTX-LPD cn exhiit ny morphology. Although the suclssifiction of MTX-LPD hs not een estlished, diffuse lrge B cell lymphom (DLBCL) is the most common sutype of MTX-LPD. Other types of B cell lymphom include Folliculr lymphom, MALT lymphom, Burkitt lymphom, nd sometimes even peripherl T-cell lymphom or Hodgkin lymphom (14). EBV infection is n importnt fctor for the clinicl course nd development of MTX-LPD. Among cses of MTX-LPD, the rte of EBV positivity in ptients who showed spontneous regression ws significntly higher thn tht in ptients without regression (15). Moreover, EBV positivity cn e considered fvorle prognostic fctor for 3251
4 c d e f g h 100 Figure 4. Immunohistochemistry of the iopsy specimen otined from the ulcerted lesion. CD20 (), CD79α (), CD3 (c), CD5 (d), CD10 (e), CD21 (f),κ light chin (g) nd λ light chin stining (h). All scle rs indicte 100 μm. The mgnifiction of these imges is 200. spontneous regression. The spontneous regression of MTX-LPD nd EBV infection in our cse were in line with the findings of previous report (4). MTX cn ctivte the relese of infectious EBV from ltently infected cells. In this mnner, EBV persistence nd rectivtion my underlie the pthogenesis of LPD (15). Since our ptient ws EBERpositive, EBV re-ctivtion might hve occurred. Furthermore, in our cse, in ddition to remission in the left cervicl lymph nodes nd the stomch, the cesstion of MTX led to the normliztion of the serum level of IgM. A compliction of type 2 cryogloulinemi hs een reported in ptient with MTX-LPD (16). In the ner future, invsive tests such s EGD will e difficult to perform in our ptient ecuse of her dvnced ge. In such cses, the serum level of 3252
5 IgM my e good non-invsive mrker of disese progression. In this cse, the improvement of the cervicl lesion nd the normliztion of the serum IgM level were chieved t 3 months fter cesstion of MTX (2 months fter tretment for H. pylori infection). These effects re not reported to hve resulted from H. pylori erdiction. H. pylori erdiction ws considered to hve plyed miniml role in the clinicl course of this cse nd it ws considered tht MTX- LPD would hve developed, even in the sence of H. pylori infection. We serched PuMed for the key words MTX, LPD, nd stomch to find reports on gstric MTX-LPD. We found two reports from Jpn. In one cse, gstric lesion presumed to e gstric cncer ws reported (7). In the other cse, n extr-gstric lesion in the medistinum nd chest 200 Figure 5. In situ hyridiztion to detect the the Epstein-Brr encoding region (EBER) indicted the Epstein-Brr virus in infiltrting lymphocytes. EBER-positive cells re circled. The scle r indictes 200 μm. The mgnifiction of this imge is 400. wll ws reported, which ws presumed to e DLBCL (8). Thus, our report is the first cse of MTX-LPD tht ws presumed to e MALT lymphom. MTX is commonly used in the tretment of RA. According to previous report, the men durtion of MTX tretment nd men cumultive dose of the development of MTX-LPD were 5.2 yers (rnge, yers) nd 2,200 mg (rnge 500-5,200 mg), respectively (17). Our ptient ws treted with MTX (4 mg per week) for 7 yers. This durtion nd dose were in line with those in previous report. Complete remission generlly occurs within 4 weeks fter the cesstion of MTX nd ppers to persist for n verge of 15 months. If no remission is chieved-even fter the withdrwl of MTX-tretment for mlignnt lymphom, dditionl tretment such s chemotherpy, should e considered (18). Approximtely 60% of ptients who re EBER-positive cn chieve remission fter the withdrwl of MTX (10). According to Ichikw et l., recurrence nd/or residul disese were oserved in 46% of ptients with MTX-LPD who chieved complete or prtil remission fter the cesstion of MTX (15). Thus, our ptient should e strictly followed up to detect recurrence nd/or residul disese. In conclusion, we experienced cse of MTX-LPD tht ws presumed to e MALT lymphom. MTX-LPD cn mnifest s ny pthologicl stte nd my occur in ny extrnodl orgn. When gstric lesion is encountered during MTX tretment, physicins should consider MTX-LPD s differentil dignosis. Author s disclosure of potentil Conflicts of Interest (COI). Ttsuhiro Msok: Honorri, Tked Phrmceuticl. Finncil Support This study ws supported y Keio Gijuku Acdemic Develop- MTX 4mg/week Neck CT Neck MRI 1st EGD Tretment for H. pylori erdiction Lymphdenopthy disppered 2nd EGD Serum IgM (mg/dl) 1,400 1,200 1, Mr. Apr. My Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jn. Fe. 200X+7 200X+8 Figure 6. The ptient s clinicl course. 3253
6 ment Funds (T.M.). References 1. Helmick CG, Felson DT, Lwrence RC, et l. Estimtes of the prevlence of rthritis nd other rheumtic conditions in the United Sttes. Prt I. Arthritis Rheum 58: 15-25, Upchurch KS, Ky J. Evolution of tretment for rheumtoid rthritis. Rheumtology (Oxford) 51 (Suppl): vi28-vi36, Ymnk H, Inoue E, Tnk E, et l. Influence of methotrexte dose on its efficcy nd sfety in rheumtoid rthritis ptients: evidence sed on the vriety of prescriing pproches mong prcticing Jpnese rheumtologists in single institute-sed lrge oservtionl cohort (IORRA). Mod Rheumtol 17: , Hoshid Y, Xu JX, Fujit S, et l. Lymphoprolifertive disorders in rheumtoid rthritis: clinicopthologicl nlysis of 76 cses in reltion to methotrexte mediction. J Rheumtol 34: , Swerdlow SH, Cmpo E, Hrris NL, et l. WHO Clssifiction of Tumours of Hemtopoietic nd Lymphoid Tissues. Revised 4th ed. WHO Press, Genev, 2017: Kto E, Swd T, Thr K, et l. The ge t onset of rheumtoid rthritis is incresing in Jpn: ntionwide dtse study. Int J Rheum Dis 20: , Stoh K, Yoshid N, Imizumi K, et l. Reversile methotrextessocited lymphoprolifertive disorder resemling dvnced gstric cncer in ptient with rheumtoid rthritis. Am J Med Sci 338: , Iked K, Nkmur T, Kinoshit T, et l. Methotrexte-relted lymphoprolifertive disorder of the stomch in ptient with rheumtoid rthritis: cse of disese regression fter methotrexte cesstion. Clin J Gstroenterol 9: 17-21, Nishizw T, Suzuki H, Fujimoto A, et l. Effects of ptient ge nd choice of ntisecretory gent on success of erdiction therpy for Helicocter pylori infection. J Clin Biochem Nutr 60: , Murkmi K, Skuri Y, Shiino M, Funo N, Nishimur A, Ask M. Vonoprzn, novel potssium-competitive cid locker, s component of first-line nd second-line triple therpy for Helicocter pylori erdiction: phse III, rndomised, doule-lind study. Gut 65: , Zullo A, Hssn C, Cristofri F, et l. Effects of Helicocter pylori erdiction on erly stge gstric mucos-ssocited lymphoid tissue lymphom. Clin Gstroenterol Heptol 8: , Ok K, Shinong M, Ngym R, et l. Coexistence of primry pulmonry Hodgkin lymphom nd gstric MALT lymphom ssocited with Epstein-Brr virus infection: cse report. Pthol Int 60: , Chn WY, Chn EK, Chow JH. Epstein-Brr virus-ssocited gstric lymphoms re distinct from mucos-ssocited lymphoid tissue-type lymphoms: genetic normlities of p53 gene. Dign Mol Pthol 10: , Hsserjin RP, Chen S, Perkins SL, et l. Immunomodultor gent-relted lymphoprolifertive disorders. Mod Pthol 22: , Ichikw A, Arkw F, Kiysu J, et l. Methotrexte/itrogenic lymphoprolifertive disorders in rheumtoid rthritis: histology, Epstein-Brr virus, nd clonlity re importnt predictors of disese progression nd regression. Eur J Hemtol 91: 20-28, Mtsui Y, Miur Y, Sugino N, Kneko H, Wtne M, Tsudo M. Methotrexte-ssocited lymphoplsmcytic lymphom complicted with type 2 cryogloulinemi. Int J Hemtol 93: , Mriette X, Czls-Htem D, Wrszwki J, et l. Lymphoms in rheumtoid rthritis ptients treted with methotrexte: 3-yer prospective study in Frnce. Blood 99: , Sito S, Kneko Y, Ymok K, Tokuhir M, Tkeuchi T. Distinct ptterns of lymphocyte count trnsition in lymphoprolifertive disorder in ptients with rheumtoid rthritis treted with methotrexte. Rheumtology (Oxford) 56: , The Internl Medicine is n Open Access journl distriuted under the Cretive Commons Attriution-NonCommercil-NoDerivtives 4.0 Interntionl License. To view the detils of this license, plese visit ( y-nc-nd/4.0/) The Jpnese Society of Internl Medicine Intern Med 57: ,
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