CASE REPORT. Abstract. Introduction
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1 CASE REPORT Myelodysplstic Syndrome with Ph Negtive Monosomy 7 Chromosome following Trnsient Bone Mrrow Dysplsi during Imtini Tretment for Chronic Myeloid Leukemi Kori Krimt 1, Msyoshi Msuko 2, Tkshi Ushiki 1, Tkshi Kozki 1, Ysuhiko Shiski 1, Toshio Yno 1, Tkshi Ae 1, Msto Moriym 1, Ken To 1, Ttsuo Furukw 2 nd Yoshifus Aizw 1 Astrct We descrie 60-yer-old Jpnese ptient with chronic myeloid leukemi (CML) who developed myelodysplstic syndrome (MDS) with Ph negtive monosomy 7 chromosome following trnsient one mrrow dysplsi during imtini tretment. Most cses tht developed chromosoml normlity in Ph negtive cells during imtini therpy were reported to hve less clinicl implictions, while rre cses developed MDS/ AML. The present cse suggested tht metphse kryotype nlysis nd one mrrow exmintion should e performed for the long term follow-up under imtini tretment in cses showing cytopeni. The results lso suggested tht monosomy 7 in Ph negtive cells my e n indictor of poor prognosis. Key words: CML, MDS, monosomy 7, Ph negtive cells (Intern Med 50: , 2011) () Introduction Chronic myeloid leukemi (CML) is clonl hemtopoietic disorder chrcterized y the presence of Phildelphi chromosome (Ph) resulting in trnsloction t (9; 22) (q34; q11), which leds to the formtion of the BCR-ABL1 fusion gene (1). The BCR-ABL1 fusion gene encodes chimeric protein which increses tyrosine kinse ctivity nd plys centrl role in the leukemogenesis of CML (2). Imtini mesylte is potent tyrosine kinse inhiitor which inds to the ATP-inding site of BCR-ABL1. It induces complete cytogenetic response (CCyR) in more thn 90% of newly dignosed CML ptients, therefore it is now the first-line therpy for CML ptients, replcing the role of interferonα (3, 4). Recently, second-genertion tyrosine kinse inhiitors, such s nilotini nd dstimi, hve ecome ville for ptients who re intolernt or resistnt to imtini (5). Therefore, the ssessment nd mngement of the dverse effects nd efficcy re importnt to improve the prognosis of CML ptients. Cytopeni is one of the common dverse effects of imtin. In the erly phse of imtini therpy, neutropeni is ssocited with the elimintion of Ph clones, nd recovery ccording to norml hemtopoiesis is oserved. In the lte phse under norml hemtopoietis, myelosuppression including grde 3/4 neutropeni, nemi, nd thromocytopeni occur in out 10% of ptients (6). Most such ptients, improve on the withdrwl or dose reduction of imtini. Some ptients with cytopeni show myelodysplstic chnge in Ph-negtive lood cells, ut the clinicl course of such ptients is not well-recognized. Severl reports showed tht CML ptients develop chromosoml normlity in Ph-negtive cells during imtini therpy (7-13). The clinicl implictions of such phenomenon re still uncler. Clinicl courses in such ptients were reported to usully e similr to ptients without chromosoml errtion, nd some re trnsient (14). However rre Division of Hemtology, Niigt University Medicl nd Dentl Hospitl, Jpn nd Division of Stem Cell Trnsplnttion, Niigt University Medicl nd Dentl Hospitl, Jpn Received for puliction Septemer 3, 2010; Accepted for puliction Octoer 21, 2010 Correspondence to Dr. Msyoshi Msuko, mmsuko@med.niigt-u.c.jp 481
2 Figure 1. Morphology of one mrrow cells in My, My-Giems stin..) 400..) 600. Dysplsi in erythrolsts s meglolstic chnge without the prolifertion of myelolsts is shown. cses with chromosoml normlity developed myelodysplstic syndrome (MDS) or cute myelolstic leukemi (AML) (15-18). We report CML ptient who developed MDS with Ph-negtive monosomy 7 chromosome following trnsient one mrrow dysplsi without chromosoml normlity during imtini tretment. Cse Report A 60-yer-old Jpnese mn ws referred to our hospitl ecuse of mrked leukocytosis nd thromocytosis in My He hd een pointed out s showing leukocytosis on medicl check-ups from Peripherl lood nlysis reveled white lood cell count of 20,670/μL with 0.5% myelolst, 7.5% myelocytes, 3.0% metmyelocytes, 9.5% sted-form neutrophiles, 51.0% segmented form neutrophils, 13.5% lymphocytes, 0.5% monocytes, 2.0% eosinophils, 12.5% sophils. The hemogloin concentrtion ws 14.5 g/dl nd the pltelet count ws /μl. The neutrophil lkline phosphtse stin (NAP) score ws 72 nd rte ws 40%. Bone mrrow nlysis reveled hyperplstic mrrow with myeloid hyperplsi. G-nd kryotype nlysis of one mrrow cells showed 46XY, t (9; 22) (q34; q11) in ll of the 20 nlyzed metphse cells. FISH nlysis of one mrrow cells using cr/l trnsloction DNA proe showed tht 97.3% of cells were positive for fusion signl. RT-PCR using primers for 32 were positive. An dominl echogrm showed splenomegly. He ws dignosed with chronic phse chronic myeloid leukemi, nd the Socl score ws He ws treted with 500 mg of hydroxyure nd 600 MU of interferon-α. He showed no cytogenetic response to hydroxyure nd interferon-α on 6 months fter strting tretment, thus we chnged to tretment with 400 mg of imtini in April He chieved CCyR sed on kryotype nlysis of 12 months fter strting imtini tretment. Becuse pncytopeni ws clssed s grde II sed on CTC criteri, s n dverse effect of imtini, he continued to receive 200 to 300 mg of imtini fter chieving CCyR, nd quntitive RT-PCR reveled round 3-log reduction level. In My 2005, he ws pointed out s hving severe thromocytopeni of grde III sed on CTC criteri on regulr checkup. The white lood cell count of 2,220/μL comprised 9.5% sted-form neutrophiles, 21.5% segmented-form neutrophils, 64.0% lymphocytes, 4.0% monocytes, 1.0% eosinophils, nd 0% sophils. The hemogloin concentrtion ws 10.9 g/dl nd the pltelet count ws /μl. Reticulr erythrocytes mde up 2.1%. MCV nd MCH were fl, nd 38.0 pg, respectively. Bone mrrow nlysis showed mrked erythroid hyperplsi with meglolstic morphologicl chnge (Fig. 1). G-nd kryotype nlysis of one mrrow cells showed 46,XY in the 20 cells nlyzed. FISH nlysis of one mrrow cells using cr/l FS proe showed cells were negtive for fusion signl. Quntittive RT-PCR using peripherl lood cells showed 83 copies/μg RNA, which corresponded to the moleculr level of mjor moleculr response (MMR). He discontinued imtini tretment for one month. Then, pncytopeni improved (white lood cell count of 3,140/μL, hemogloin concentrtion of 11.6 g/dl nd the pltelet count of /μl), nd the dysplsi of one mrrow cells disppered. Although FISH nlysis reveled CCyR, quntittive RT- PCR using peripherl lood cells showed n increse to 970 copies/μg RNA. So, he ws re-strted on tretment with 200 mg of imtini. In Novemer 2007, his pltelet count decresed gin to /μl. This time, the hemogloin concentrtion ws 11.3 g/dl nd the white lood cell count ws 2,420/μL with 0.5% myelolsts, 1% myelocytes, 5% sted-form neutrophiles, 12.5% segmented-form neutrophils, 62.0% lymphocytes, 19.0% monocytes, 0% eosinophils, nd 0% sophils. MCV nd MCHC were fl, nd 34.9 pg, respectively. We discontinued imtini gin, ut pltelet counts showed no recovery. Bone mrrow nlysis showed dysplsi in three lineges without lst prolifertion (Fig. 2). Kryotype nlysis reveled tht Ph chromosome presence ws negtive, ut monosomy 7 ws oserved in 16 of 20 nlyzed cells (Fig. 3). FISH nlysis reveled tht the cr/l fusion 482
3 c Figure 2. Morphology of one mrrow cells in Novemer, My-Giems stin ) Multinuculeted erythrolst.) Multinucleted megkryocyte c.) Pseudo Pelger normlity in neutrophils. signl ws negtive lthough 83.0 % of one mrrow cells hd monosomy 7 (Fig. 4, ). Quntittive PCR of cr/l in peripherl lood showed 99 copis/μg RNA. We dignosed him with MDS (RCMD: refrctory cytopeni with multilinege dysplsi). Four months fter the termintion of imtini, FISH nlysis showed tht 88.0% of peripherl lood cells were monosomy 7 positive nd negtive for cr/ l. Becuse quntittive PCR showed elevtion up to 5,500 copies/g RNA, we re-strted 100 mg of imtini. His MDS progressed to AML, nd he died of AML in CCyR of CML fter 2.5 yers. Discussion Severl reports hve descried the occurrence of clonl chromosoml normlity in Ph-negtive cells (7-14). Previous studies reported n incidence of chromosoml normlity of 2-17%. The mjority of normlities re trisomy 8, monosomy 7, nd 20q-, which re often present in MDS. However, most cses with chromosoml normlity were not ssocited with myelodysplsi or AML development nd some seemed to e trnsient. Also, the prognosis of cses with chromosome normlity ws similr to tht of those without n normlity. This suggested tht chromosoml normlity during imtini therpy my hve different clinicl implictions from those ssocited with other cytotoxic chemotherpies. Only rre cses showing chromosoml normlity during imtini therpy developed MDS/ AML (15-18). In the revised recommendtions of Europen LeukemiNet chromosoml normlity in Ph negtive cells t ny time is ctegorized into wrning ctegory (19). However, it is not cler whether or not ech kind of chromosoml normlity hs different implictions regrding the clinicl course. The present cse suggested tht monosomy 7 in Ph-negtive cells should e orne in mind s risk fctor for MDS/AML development. The mechnisms of MDS development during imtini tretment remin uncler. Becuse most cses of MDS during imtini tretment hve een reported in CML ptients, imtini hs een generlly considered to hve no direct mutgenic effect on Ph-negtive cells, nd Ph-negtive cells themselves show genetic instility in CML ptients (16). However, it ws recently reported tht gstrointestinl stroml tumor (GIST) ptient developed MDS with monosomy 7 during imtini tretment, suggesting tht imtini plys direct role in cusing MDS (20). Imtini is potent tyrosine kinse inhiitor which inds to the ATP-inding site of BCR-ABL s well s c-kit nd the PDGF receptor. Deficiency of the c-kit signl led the impired hemtopoietic reconstitution of hemtopoietic stem cells in myelolted nimls. Also, the mice with mutnt c-kit develop severe mcrocytic nemi (21). Tken together, the inhiition of signl trnsduction in molecules other thn BCR-ABL in norml hemtopoietic stem cells my cuse MDS during imtini tretment. Chromosoml normlity hs lso een reported in ptients treted with nilotini or dstini (22-24). Fur- 483
4 Intern Med 50: , 2011 Figure 3. Chromosoml kryotype nlysis of one mrrow cells. Monosomy 7 (indicted y n rrow) ws oserved in 16 of 20 nlyzed cells. Ph chromosome ws not oserved in ny cells. Figure 4. FISH nlysis of one mrrow cells. ) BCR/ABL ES proe. Arrows indicte BCR gene nd rrowheds indicte the ABL gene. The cr/l fusion signl ws negtive. ) Monosomy 7 nlysis using the D7S486/D7Z1 proe. One D7S486 (long rrow) signl nd one D7Z1 (rrowhed) signl in cell revel monosomy 7. A totl of 83.0% of one mrrow cells showed monosomy 7 pttern. ther study is needed to elucidte the cuse of chromosoml normlity during tretment with tyrosine kinse inhiitors. Cytopeni is one of the common dverse effects of imtin. In the lte phse under norml hemtopoietis, myelosuppression, including grde 3/4 neutropeni, nemi, nd thromocytopeni occurs in out 10% of ptients (6). Most ptients improve on the trnsient withdrwl of imtini, nd cn restrt imtini tretment. Some ptients with cytopeni show dysplstic chnges in Ph-negtive one mrrow cells, ut few reports hve descried the long term clinicl course of such ptients. The trnsient cytopeni with mrked meglolstic chnge in the present ptient my re- flect genetic dmge to Ph-negtive one mrrow cells, nd the susequent development of MDS with monosomy 7 could e cused y second hit in norml hemtopoietic stem cells. During tretment with imtini, one mrrow morphologicl exmintion nd metphse kryotype nlysis should e conducted even fter chieving CCyR over long-term follow-up in CML ptients showing cytopeni. The uthors stte tht they hve no Conflict of Interest (COI). 484
5 References 1. Deininger MW, Goldmn JM, Melo JV. The moleculr iology of chronic myeloid leukemi. Blood 96: , Lugo TG, Pendergst AM, Muller AJ, Witte ON. Tyrosine kinse ctivity nd trnsformtion potency of cr-l oncogene products. Science 247: , Druker BJ, Tlpz M, Rest DJ, et l. Efficcy nd sfety of specific inhiitor of the BCR-ABL tyrosine kinse in chronic myeloid leukemi. N Engl J Med 344: , Hughes TP, Ked J, Brnford S, et l. Frequency of mjor moleculr responses to imtini or interferon lf plus cytrine in newly dignosed chronic myeloid leukemi. N Engl J Med 349: , Kntrjin H, Shh NP, Hochhus A, et l. Dstini versus imtini in newly dignosed chronic-phse chronic myeloid leukemi. N Engl J Med 362: , Bccrni M, Sglio G, Goldmn J, et l. Evolving concepts in the mngement of chronic myeloid leukemi: recommendtions from n expert pnel on ehlf of the Europen LeukemiNet. Blood 108: , O Dwyer ME, Gtter KM, Loriux M, et l. Demonstrtion of Phildelphi chromosome negtive norml clones in ptients with chronic myelogenous leukemi during mjor cytogenetic responses induced y imtini mesylte. Leukemi 17: , Bumm T, Müller C, Al-Ali HK, et l. Emergence of clonl cytogenetic normlities in Ph- cells in some CML ptients in cytogenetic remission to imtini ut restortion of polyclonl hemtopoiesis in the mjority. Blood 101: , Medin J, Kntrjin H, Tlpz M, et l. Chromosoml normlities in Phildelphi chromosome-negtive metphses ppering during imtini mesylte therpy in ptients with Phildelphi chromosome-positive chronic myelogenous leukemi in chronic phse. Cncer 98: , Terre C, Eclche V, Rousselot P, et l. Report of 34 ptients with clonl chromosoml normlities in Phildelphi-negtive cells during imtini tretment of Phildelphi-positive chronic myeloid leukemi. Leukemi 18: , Aruzzese E, Gozzetti A, Glimerti S, et l. Chrcteriztion of Ph-negtive norml clones emerging during imtini therpy. Cncer 109: , Lin Y, Bruyère H, Horsmn DE, et l. Phildelphi-negtive clonl hemtopoiesis following imtini therpy in ptients with chronic myeloid leukemi: report of nine cses nd nlysis of predictive fctors. Cncer Genet Cytogenet 170: 16-23, Deininger MW, Cortes J, Pquette R, et l. The prognosis for ptients with chronic myeloid leukemi who hve clonl cytogenetic normlities in Phildelphi chromosome-negtive cells. Cncer 110: , Jour E, Kntrjin HM, Aruzzo LV, et l. Chromosoml normlities in Phildelphi chromosome negtive metphses ppering during imtini mesylte therpy in ptients with newly dignosed chronic myeloid leukemi in chronic phse. Blood 110: , Kovitz C, Kntrjin H, Grci-Mnero G, Aruzzo LV, Cortes J. Myelodysplstic syndromes nd cute leukemi developing fter imtini mesylte therpy for chronic myeloid leukemi. Blood 108: , Nvrro JT, Feliu E, Gru J, et l. Monosomy 7 with severe myelodysplsi developing during imtini tretment of Phildelphipositive chronic myeloid leukemi: two cses with different outcome. Am J Hemtol 82: , Hcknson B, Rückert A, Lüert M. Hyperleukocytotic secondry cute myeloid leukemi (AML) with sole monosomy 7 s sequel of Phildelphi-chromosome positive chronic myeloid leukemi (CML). Eur J Hemtol 83: , Bccrni M, Cortes J, Pne F, et l. Europen LeukemiNet. Chronic myeloid leukemi: n updte of concepts nd mngement recommendtions of Europen LeukemiNet. J Clin Oncol 27: , Pitini V, Arrigo C, Sut MG, Altvill G. Myelodysplstic syndrome ppering during imtini mesylte therpy in ptient with GIST. Leuk Res 33: e143-e144, Lymn SD, Jcosen SE. c-kit lignd nd Flt3 lignd: stem/progenitor cell fctors with overlpping yet distinct ctivities. Blood 91: , Zeidn A, Kkti S, Anderson B, Brcos M, Wetzler M. Monosomy 7 in t(9;22)-negtive cells during nilotini therpy in n imtini-resistnt chronic myeloid leukemi cse. Cncer Genet Cytogenet 176: , Conchon MR, Bendit I, Ferreir P, et l. Emergence of norml clone with monsomy 7 in Phildelphi negtive cells of CML ptients treted with tyrosine kinse inhiitors. Int J Hemtol 89: , Lrsson N, Billström R, Lilljejörn H, et l. Genetic nlysis of dstini-treted chronic myeloid leukemi rpidly developing into cute myeloid leukemi with monosomy 7 in Phildelphinegtive cells. Cncer Genet Cytogenet 199: 89-95, The Jpnese Society of Internl Medicine 485
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