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Translocation t(3;4)(q26;q21) in myelodysplastic syndrome with megakaryoblastic proliferation
Translocation t(3;4)(q26;q21) in Myelodysplastic Syndrome with Megakaryoblastic Proliferation Kazuma Ohyashiki, Yasuhiro Enomoto, Yonosuke Watanabe, Yoshio Nehashi, Junko H. Ohyashiki, and Keisuke Toyama
ABSTRACT: A 74-year-old Japanese male with a 4-year history of refractory anemia with excess of blasts is reported here. Chromosome study revealed the bone marrow cells of this patient to contain a t13;4)(q26;q21). Ultrastructural analysis of platelet peroxidase and immunocytochemical study using monoclonal antibody far platelet antigen revealed a large number of blasts in the bone marrow to be megakaryoblasts. Thus, this case was thought to be one of a myelodysplastic syndrome with excess of blasts including megakaryoblastic proliferation showing chromosome changes at 3q26 and 4q21. The relationship of the anomaly on the long arm of a chromosome #3. especially at band 3q26, to abnormal megakaryoblastic prolifl~.ration is discussed.
INTRODUCTION
Recent immunologic and cytochemical approaches have made possible the determination and accurate identification of megakaryoblasts [1]. According to these findings, acute megakaryoblastic leukemia (M-7 according to FAB criteria) is now recognized as a distinct hematologic entity [2]. Although a specific chromosome aberration in acute megakaryoblatic leukemia has not been established [3, 4], a possible correlation between abnormal megakaryoblastic of megakaryocytic proliferation with elevated platelet counts and chromosomal changes of the long arm of chromosome #3 (3q) is recognized [5-14]. For example, an intrachromosomal inversion [inv(3)(q21q26)] and an interchromosomal insertion of 3q21-q26 region into 3q21 [ins(3)(q21;q21q26)] have been seen in acute myeloid leukemia (AML) and myelodysplastic syndromes (MDS) with elevated platelet counts and abnormal megakaryocyte proliferation in the bone marrow [10]. We encountered a patient with MDS with megakaryoblastic proliferation associated with a chromosome anomaly at 3q26.
From the Department of Internal Medicine, Tokyo Medical College {K. O.. Y. N., J. H. O.. K. T] and th(~ Department of Pathology, School of Medicine, Keio University (Y. E., Y. W.], Tokyo. Japan
Address requests for reprints to Dr. Kazuma Ohyashiki, Department of Internal Medicine. Tokyo Medical College, 6-7-1 Nishishinjuku. Shinjuku-ku, Tokyo 160, Japan. Received December 8, 1987; accepted March 8, 1988.
5 . 1988 Elsevier Science 1J ublishing Co,. Inc. 'c;' 52 Vanderbill Ave., New York, NY 10017
Cancer Genet Cytogenet 34:5-9(1988) 0165 4608"88,'$03.50
6
K. Ohyashiki et al.
CASE REPORT A 74-year-old male was found to be in a bicytopenic stage (anemia and leukopenia) in 1983. Blood tests revealed a red blood cell (RBC) count of 2.62 × 10"/#1, platelet count 318 x 10:~/p~l,and white blood cell (WBC) count 2700/1~1 with 37% stabs and segmented granulocytic cells. 54% lympbocytes, and 9% monocytes. Blood films showed anisocytosis and poikilocytosis. Bone marrow aspirate y i e l d e d a normocellular marrow with 3.2% blasts and 3.6% promyelocytes. He was diagnosed as having refractory anemia (RA) according to FAB criteria. The patient was followed without treatment until 1984, when he was treated with androgenic steroids for 7 months. However, this therapy was d i s c o n t i n u e d because of liver dysfunction and p r e d n i s o l o n e was initiated. In October 1986, blasts and micromegakaryocytes appeared in the peripheral hlood and increased in the bone marrow. The diagnosis of refractory anemia with excess of blasts (RAEB) was made. Some of the blasts (25%) in the bone marrow reacted with a monoclonal antibody specific for platelet glycoprotein IIb/IIIa (GP lib/Ilia) and were positive for platetet peroxidase reaction by electron microscopy. Thus, the patient was thought to be in an RAEB phase with abnormal megakaryoblastic proliferation. However. he has not d e v e l o p e d an overt leukemia and has remained in the RAEB phase. CYTOGENETIC STUDIES For c h r o m o s o m e analysis, Hoechst 33258 and quinacrine mustard double staining was utilized. The first c h r o m o s o m e analysis was made on August 15, 1983. At this time (during the RA stage), all 20 bone marrow cells showed a pseudodiploid karyotype, w h i c h was interpreted as a reciprocal translocation between c h r o m o s o m e s #3 and #4. On February 14, 1986, all 20 bone marrow cells also had a similar c h r o m o s o m e change, i.e., a 46,XY,t(3;4){q26;q21) (Fig. 1). Chromo-
Figure 1 Representative Q-banded partial karyotypes of the bone marrow cells of the patient, showing a t(3;4)(q26;q21). Arrowheads indicate breakpoints at 3q26 and 4q21.
t(3;4) in MDS
7
some analysis of p h y t o h e m a g g l u t i n - s t i m u l a t e d peripheral blood cells showed a normal male d i p l o i d karyotype, indicating that the translocation in the bone marrow cells was an acquired change associated with the hematologic condition of this patient. DISCUSSION
A cytogenetic change of the long arm of a c h r o m o s o m e #3 in hematopoietic disorders was first found in AML with thrombocytosis by Golomb et al. [51, and a possible association between a c h r o m o s o m e change on 3q and abnormal megakaryocytic proliferation with qualitative and quantitive platelet dysfunction was postulated [6]. Subsequently, an intrachromosomal rearrangement of chromosomes #3 at q21 and q26 [inv(3)(q21q26)] and an interchromosomal insertion [ins(3;3)(q21;q21q26)] were found in AML [7-10] and MDS [11, 121 with elevated platelet counts and abnormal megakaryocytic proliferation in the bone marrow. Furthermore, these anomalies, involving 3q21 and 3q26 bands, were found in Phpositive chronic m y e l o i d leukemia (CML) as an additional c h r o m o s o m e change [8, 14]. According to these observations, a c h r o m o s o m e change at 3q was considered to play some role in abnormal megakaryocytic proliferation [10] because these inversions and insertions involving 3q21 and 3q26 were found in MDS, AML, and CML. Furthermore, it has been suggested that leukemias with 3q21 and 3q26 anomalies had a short survival time and did not respond adequately to c h e m o t h e r a p y
[10[. A m o n g the reports dealing with hematopoietic disorders with c h r o m o s o m e change of 3q, most of the cases with abnormal megakaryocytic proliferation showed an involvement of both regions, 3q21 and 3q26, either as an insertion or inversion [10[. On the other hand, some cases of hematopoietic neoplasia with only 3q21 anomalies did not show abnormal megakaryocytic proliferation or elevated platelet counts; also, leukemias and MDS with t(3;5)(q21;q31) [15-18] and t(1;3)(p36;q21) [19-251 usually did not show an apparent megakaryocytic involvement. A salient feature in the present case was that only a 3q26 change resulting in a t(3:4)(q26;q21) was present. It was noteworthy that the bone marrow showed abnormal megakaryoblastic proliferation, although elevated platelet count was not prominent. Thus, a c h r o m o s o m e change at 3q26, either as an insertion [ins(3:3)(q21;q21q26)], inversion [inv{3){q21q26)], or translocation [t(3;4)(q26;q21)] might be associated with abnormal megakaryocytic (or megakaryoblastic) proliferation, whereas changes at 3q21 did not. Chromosome changes in acute megakaryoblastic leukemia (M7 by FAB classification) have not been well recognized so far. Only a few reports have appeared [3, 4] and no consistent a n o m a l y has been established. The main reason for this problem is that it is usually difficult to obtain bone marrow samples from M7 leukemia patients because of bone marrow fibrosis. Thus, an accumulation of c h r o m o s o m e findings in M7 leukemia, as well as in MDS with abnormal megakaryocytic (or megakaryoblastic) involvement, as in this case, might answer the question. Supported by a Grant-in-Aid for Cancer Research and Young Scientists from the Ministry ot Education, Science and Culture, and in part by Grant-in-Aid for Japanese Group Study for Intractable Diseases from the Ministry of Health and Welfare, Japan (K. T.). The authors are grateful to A. Kodama and Y. Mori for their help. Thanks are due to H. Kinoshita (Department of Health Promotion, School of Medicine, Keio University) for supplying previous chromosome data.
8
K. O h y a s h i k i et al.
REFERENCES 1. Koike T (1984): Megakaryoblastic leukemia: The characterization and identification of megakaryoblasts. Blood 64:683-692. 2. Bennett JM, Catovsky D, Daniel MT, Flandrin G, Galton DA, Gralnick HR (1985): Criteria for the diagnosis of acute leukemia of megakaryocyte lineage (M7). A report of the French American-British Cooperative Group. Ann Intern Med 103:460-462. 3. Stoll C, Seiller F, Lutz P, Levy JM (1985): Megakaryoblastic leukemia with bypodiploidy in a girl with trisomy 21. Ann Pediatr 32:21-23. 4. Teyssier JR, Pigion F, Behar C, Pignon B, Blaise AM (1987): Chromosomal subclonal evolution in paroxysmal nocturnal hemoglobinuria evolving into acute megakaryoblastic leukemia. Cancer Genet Cytogenet 25:259-264. 5. Golomb HM, Vardiman J, Rowley, JD (1976): Acute nonlymphocytic leukemia in adults: Correlation with Q banded chromosomes. Blood 48:9-21. 6. Sweet DDL, Golomb HM, Rowley, JD, Vardiman JM (1979): Acute myelogenous leukemia and thrombocythemia associated with an abnormality of chromosome no. 3. Cancer Genet Cytogenet 1:33 37. 7. Bernstein R, Pinto MR, Behr A, Mendelow B (1982): Chromosome 3 abnormalities in acute nonlymphocytic leukemia (ANLL/ with abnormal thrombopoiesis: Report of three patients with a " n e w " inversion normally and a further case of homologous translocation. Blood 60:613-617. 8. Mecucci C, Vermaelen K, Tricot G, Louwagie A, Michaux J-L, Bosly A, Thomas J, Barbieri D, van den Berghe H (1983): 3q , 3q+ anomaly in malignant proliferations in humans. Cancer Genet Cytogenet 9:367-381. 9. Bitter MA, Neilly ME, Le Beau MM, Pearson M, Rowley JD (1985): Rearrangements of chromosome 3 involving bands 3q21 and 3q26 are associated with normal or elevated platelet counts in acute nonlymphocytic leukemia. Blood 66:1362-1370. 10. Pintado T, Ferro MT, San Roman C, Mayayo M, Larana JG (1985): Clinical correlations of the 3q21;q26 cytogenetic anomaly. Cancer 55:535-541. 11. Norrby A, Ridell B, Swolin B, Westin J (1982): Rearrangement of chromosome no. 3 in a case of preleukemia with thrombocytosis. Cancer Genet Cytogenet 5:257-263. 12. Carroll AJ, Poon M-C, Robinson NC, Crist WM (1986): Sideroblastic anemia associated with thrombocytosis and a chromosome 3 abnormality. Cancer Genet Cytogenet 11:183187, 13. Gascoyne RD, Noble MC, Kalousek DK (1986): Translocation t(3;3}(q21;q26) and thrombocytosis. Cancer Genet Cytogenet 22:365. 14. Carbonell F, Foelzer D, Thiel E, Bartl R (1982): Ph-positive CML associated with megakaryocytic hyperplasia and thrombocythemia and an abnormality of chromosome no. 3, Cancer Genet Cytogenet 6:153-161. 15. Werner-Favre C, Engel E, Besis P (1985): Translocation t(3:5) in ANLL. Cancer Genet Cytogenet 16:279. 16. Pi D, Kalousek DK (1986): Translocation t(3;5) in acute myelocytic leukemia type M2. Cancer Genet Cytogenet 20:171. 17. Smadja N, Krulik M, de Gramont A, Sirinelli A, Dray C, Brissaud P, Debray J (1986): Translocation t(3;5) and acute nonlymphocytic leukemia. Cancer Genet Cytogenet 20:173. 18. Sharp RA, Robertson J, Heppleston AD (1987): t(3;5)(q21;q31) in a myelodysplastic syndrome. Leukemia Res 11:629-633. 19. Moir DJ, Jones PAE, Pearson J, Duncan JR, Cook P, Buckle VJ (1984): A new translocation, t(1;3)(p36;q21), in myelodysplastic disorders. Blood 64:553-555. 20. Rios Gonzales A, Salazar J, Moraleda JM, Delcanizo MC (1985): Translocation (1;3) in myelodysplastic disorders. Blood 65:509-510. 21. Bloomfield CD, Garson OM, Volin L, Knuutila S, de la Chapelle (1985): t(1;3)(p36;q21) in acute nonlymphocytic leukemia: A new cytogenetic-clinicopathologic association. Blood 66:1409. 22. Viguie F, Marie J, Poler F, Bernadou A (1986): Three cases of preleukemic myelodysplastic disorders with the same translocation t(1;3). Cancer Genet Cytogenet 19:213.
t(3;4) in M D S
9
23. Atichartakarn V, OPunyammalee B, Wongsasant B, Jootar S (1986): Acute nonlymphocytic leukemia with translocation (1;3)(p36;q21) in an XYY man. Cancer Genet Cytogenet 21:79-83. 24. Scheres JMJC, Hustinx TWJ, Haasjes JG, Haanen C (1986): Specific translocation t(1;'l) in acute myelomonocytic leukemia: Further case. Cancer Genet Cytogenet 22:69 73. 25. Rege-Cambrin G, Mecucci C, van Orshoven A, Tricot G, van den Berghe H (1986): Translocation t(1;3)(p36;q21) in malignant myeloid stem cell disorders. Cancer Genet Cytogenet 22:75-81.
ABSTRACT: A 74-year-old Japanese male with a 4-year history of refractory anemia with excess of blasts is reported here. Chromosome study revealed the bone marrow cells of this patient to contain a t13;4)(q26;q21). Ultrastructural analysis of platelet peroxidase and immunocytochemical study using monoclonal antibody far platelet antigen revealed a large number of blasts in the bone marrow to be megakaryoblasts. Thus, this case was thought to be one of a myelodysplastic syndrome with excess of blasts including megakaryoblastic proliferation showing chromosome changes at 3q26 and 4q21. The relationship of the anomaly on the long arm of a chromosome #3. especially at band 3q26, to abnormal megakaryoblastic prolifl~.ration is discussed.
INTRODUCTION
Recent immunologic and cytochemical approaches have made possible the determination and accurate identification of megakaryoblasts [1]. According to these findings, acute megakaryoblastic leukemia (M-7 according to FAB criteria) is now recognized as a distinct hematologic entity [2]. Although a specific chromosome aberration in acute megakaryoblatic leukemia has not been established [3, 4], a possible correlation between abnormal megakaryoblastic of megakaryocytic proliferation with elevated platelet counts and chromosomal changes of the long arm of chromosome #3 (3q) is recognized [5-14]. For example, an intrachromosomal inversion [inv(3)(q21q26)] and an interchromosomal insertion of 3q21-q26 region into 3q21 [ins(3)(q21;q21q26)] have been seen in acute myeloid leukemia (AML) and myelodysplastic syndromes (MDS) with elevated platelet counts and abnormal megakaryocyte proliferation in the bone marrow [10]. We encountered a patient with MDS with megakaryoblastic proliferation associated with a chromosome anomaly at 3q26.
From the Department of Internal Medicine, Tokyo Medical College {K. O.. Y. N., J. H. O.. K. T] and th(~ Department of Pathology, School of Medicine, Keio University (Y. E., Y. W.], Tokyo. Japan
Address requests for reprints to Dr. Kazuma Ohyashiki, Department of Internal Medicine. Tokyo Medical College, 6-7-1 Nishishinjuku. Shinjuku-ku, Tokyo 160, Japan. Received December 8, 1987; accepted March 8, 1988.
5 . 1988 Elsevier Science 1J ublishing Co,. Inc. 'c;' 52 Vanderbill Ave., New York, NY 10017
Cancer Genet Cytogenet 34:5-9(1988) 0165 4608"88,'$03.50
6
K. Ohyashiki et al.
CASE REPORT A 74-year-old male was found to be in a bicytopenic stage (anemia and leukopenia) in 1983. Blood tests revealed a red blood cell (RBC) count of 2.62 × 10"/#1, platelet count 318 x 10:~/p~l,and white blood cell (WBC) count 2700/1~1 with 37% stabs and segmented granulocytic cells. 54% lympbocytes, and 9% monocytes. Blood films showed anisocytosis and poikilocytosis. Bone marrow aspirate y i e l d e d a normocellular marrow with 3.2% blasts and 3.6% promyelocytes. He was diagnosed as having refractory anemia (RA) according to FAB criteria. The patient was followed without treatment until 1984, when he was treated with androgenic steroids for 7 months. However, this therapy was d i s c o n t i n u e d because of liver dysfunction and p r e d n i s o l o n e was initiated. In October 1986, blasts and micromegakaryocytes appeared in the peripheral hlood and increased in the bone marrow. The diagnosis of refractory anemia with excess of blasts (RAEB) was made. Some of the blasts (25%) in the bone marrow reacted with a monoclonal antibody specific for platelet glycoprotein IIb/IIIa (GP lib/Ilia) and were positive for platetet peroxidase reaction by electron microscopy. Thus, the patient was thought to be in an RAEB phase with abnormal megakaryoblastic proliferation. However. he has not d e v e l o p e d an overt leukemia and has remained in the RAEB phase. CYTOGENETIC STUDIES For c h r o m o s o m e analysis, Hoechst 33258 and quinacrine mustard double staining was utilized. The first c h r o m o s o m e analysis was made on August 15, 1983. At this time (during the RA stage), all 20 bone marrow cells showed a pseudodiploid karyotype, w h i c h was interpreted as a reciprocal translocation between c h r o m o s o m e s #3 and #4. On February 14, 1986, all 20 bone marrow cells also had a similar c h r o m o s o m e change, i.e., a 46,XY,t(3;4){q26;q21) (Fig. 1). Chromo-
Figure 1 Representative Q-banded partial karyotypes of the bone marrow cells of the patient, showing a t(3;4)(q26;q21). Arrowheads indicate breakpoints at 3q26 and 4q21.
t(3;4) in MDS
7
some analysis of p h y t o h e m a g g l u t i n - s t i m u l a t e d peripheral blood cells showed a normal male d i p l o i d karyotype, indicating that the translocation in the bone marrow cells was an acquired change associated with the hematologic condition of this patient. DISCUSSION
A cytogenetic change of the long arm of a c h r o m o s o m e #3 in hematopoietic disorders was first found in AML with thrombocytosis by Golomb et al. [51, and a possible association between a c h r o m o s o m e change on 3q and abnormal megakaryocytic proliferation with qualitative and quantitive platelet dysfunction was postulated [6]. Subsequently, an intrachromosomal rearrangement of chromosomes #3 at q21 and q26 [inv(3)(q21q26)] and an interchromosomal insertion [ins(3;3)(q21;q21q26)] were found in AML [7-10] and MDS [11, 121 with elevated platelet counts and abnormal megakaryocytic proliferation in the bone marrow. Furthermore, these anomalies, involving 3q21 and 3q26 bands, were found in Phpositive chronic m y e l o i d leukemia (CML) as an additional c h r o m o s o m e change [8, 14]. According to these observations, a c h r o m o s o m e change at 3q was considered to play some role in abnormal megakaryocytic proliferation [10] because these inversions and insertions involving 3q21 and 3q26 were found in MDS, AML, and CML. Furthermore, it has been suggested that leukemias with 3q21 and 3q26 anomalies had a short survival time and did not respond adequately to c h e m o t h e r a p y
[10[. A m o n g the reports dealing with hematopoietic disorders with c h r o m o s o m e change of 3q, most of the cases with abnormal megakaryocytic proliferation showed an involvement of both regions, 3q21 and 3q26, either as an insertion or inversion [10[. On the other hand, some cases of hematopoietic neoplasia with only 3q21 anomalies did not show abnormal megakaryocytic proliferation or elevated platelet counts; also, leukemias and MDS with t(3;5)(q21;q31) [15-18] and t(1;3)(p36;q21) [19-251 usually did not show an apparent megakaryocytic involvement. A salient feature in the present case was that only a 3q26 change resulting in a t(3:4)(q26;q21) was present. It was noteworthy that the bone marrow showed abnormal megakaryoblastic proliferation, although elevated platelet count was not prominent. Thus, a c h r o m o s o m e change at 3q26, either as an insertion [ins(3:3)(q21;q21q26)], inversion [inv{3){q21q26)], or translocation [t(3;4)(q26;q21)] might be associated with abnormal megakaryocytic (or megakaryoblastic) proliferation, whereas changes at 3q21 did not. Chromosome changes in acute megakaryoblastic leukemia (M7 by FAB classification) have not been well recognized so far. Only a few reports have appeared [3, 4] and no consistent a n o m a l y has been established. The main reason for this problem is that it is usually difficult to obtain bone marrow samples from M7 leukemia patients because of bone marrow fibrosis. Thus, an accumulation of c h r o m o s o m e findings in M7 leukemia, as well as in MDS with abnormal megakaryocytic (or megakaryoblastic) involvement, as in this case, might answer the question. Supported by a Grant-in-Aid for Cancer Research and Young Scientists from the Ministry ot Education, Science and Culture, and in part by Grant-in-Aid for Japanese Group Study for Intractable Diseases from the Ministry of Health and Welfare, Japan (K. T.). The authors are grateful to A. Kodama and Y. Mori for their help. Thanks are due to H. Kinoshita (Department of Health Promotion, School of Medicine, Keio University) for supplying previous chromosome data.
8
K. O h y a s h i k i et al.
REFERENCES 1. Koike T (1984): Megakaryoblastic leukemia: The characterization and identification of megakaryoblasts. Blood 64:683-692. 2. Bennett JM, Catovsky D, Daniel MT, Flandrin G, Galton DA, Gralnick HR (1985): Criteria for the diagnosis of acute leukemia of megakaryocyte lineage (M7). A report of the French American-British Cooperative Group. Ann Intern Med 103:460-462. 3. Stoll C, Seiller F, Lutz P, Levy JM (1985): Megakaryoblastic leukemia with bypodiploidy in a girl with trisomy 21. Ann Pediatr 32:21-23. 4. Teyssier JR, Pigion F, Behar C, Pignon B, Blaise AM (1987): Chromosomal subclonal evolution in paroxysmal nocturnal hemoglobinuria evolving into acute megakaryoblastic leukemia. Cancer Genet Cytogenet 25:259-264. 5. Golomb HM, Vardiman J, Rowley, JD (1976): Acute nonlymphocytic leukemia in adults: Correlation with Q banded chromosomes. Blood 48:9-21. 6. Sweet DDL, Golomb HM, Rowley, JD, Vardiman JM (1979): Acute myelogenous leukemia and thrombocythemia associated with an abnormality of chromosome no. 3. Cancer Genet Cytogenet 1:33 37. 7. Bernstein R, Pinto MR, Behr A, Mendelow B (1982): Chromosome 3 abnormalities in acute nonlymphocytic leukemia (ANLL/ with abnormal thrombopoiesis: Report of three patients with a " n e w " inversion normally and a further case of homologous translocation. Blood 60:613-617. 8. Mecucci C, Vermaelen K, Tricot G, Louwagie A, Michaux J-L, Bosly A, Thomas J, Barbieri D, van den Berghe H (1983): 3q , 3q+ anomaly in malignant proliferations in humans. Cancer Genet Cytogenet 9:367-381. 9. Bitter MA, Neilly ME, Le Beau MM, Pearson M, Rowley JD (1985): Rearrangements of chromosome 3 involving bands 3q21 and 3q26 are associated with normal or elevated platelet counts in acute nonlymphocytic leukemia. Blood 66:1362-1370. 10. Pintado T, Ferro MT, San Roman C, Mayayo M, Larana JG (1985): Clinical correlations of the 3q21;q26 cytogenetic anomaly. Cancer 55:535-541. 11. Norrby A, Ridell B, Swolin B, Westin J (1982): Rearrangement of chromosome no. 3 in a case of preleukemia with thrombocytosis. Cancer Genet Cytogenet 5:257-263. 12. Carroll AJ, Poon M-C, Robinson NC, Crist WM (1986): Sideroblastic anemia associated with thrombocytosis and a chromosome 3 abnormality. Cancer Genet Cytogenet 11:183187, 13. Gascoyne RD, Noble MC, Kalousek DK (1986): Translocation t(3;3}(q21;q26) and thrombocytosis. Cancer Genet Cytogenet 22:365. 14. Carbonell F, Foelzer D, Thiel E, Bartl R (1982): Ph-positive CML associated with megakaryocytic hyperplasia and thrombocythemia and an abnormality of chromosome no. 3, Cancer Genet Cytogenet 6:153-161. 15. Werner-Favre C, Engel E, Besis P (1985): Translocation t(3:5) in ANLL. Cancer Genet Cytogenet 16:279. 16. Pi D, Kalousek DK (1986): Translocation t(3;5) in acute myelocytic leukemia type M2. Cancer Genet Cytogenet 20:171. 17. Smadja N, Krulik M, de Gramont A, Sirinelli A, Dray C, Brissaud P, Debray J (1986): Translocation t(3;5) and acute nonlymphocytic leukemia. Cancer Genet Cytogenet 20:173. 18. Sharp RA, Robertson J, Heppleston AD (1987): t(3;5)(q21;q31) in a myelodysplastic syndrome. Leukemia Res 11:629-633. 19. Moir DJ, Jones PAE, Pearson J, Duncan JR, Cook P, Buckle VJ (1984): A new translocation, t(1;3)(p36;q21), in myelodysplastic disorders. Blood 64:553-555. 20. Rios Gonzales A, Salazar J, Moraleda JM, Delcanizo MC (1985): Translocation (1;3) in myelodysplastic disorders. Blood 65:509-510. 21. Bloomfield CD, Garson OM, Volin L, Knuutila S, de la Chapelle (1985): t(1;3)(p36;q21) in acute nonlymphocytic leukemia: A new cytogenetic-clinicopathologic association. Blood 66:1409. 22. Viguie F, Marie J, Poler F, Bernadou A (1986): Three cases of preleukemic myelodysplastic disorders with the same translocation t(1;3). Cancer Genet Cytogenet 19:213.
t(3;4) in M D S
9
23. Atichartakarn V, OPunyammalee B, Wongsasant B, Jootar S (1986): Acute nonlymphocytic leukemia with translocation (1;3)(p36;q21) in an XYY man. Cancer Genet Cytogenet 21:79-83. 24. Scheres JMJC, Hustinx TWJ, Haasjes JG, Haanen C (1986): Specific translocation t(1;'l) in acute myelomonocytic leukemia: Further case. Cancer Genet Cytogenet 22:69 73. 25. Rege-Cambrin G, Mecucci C, van Orshoven A, Tricot G, van den Berghe H (1986): Translocation t(1;3)(p36;q21) in malignant myeloid stem cell disorders. Cancer Genet Cytogenet 22:75-81.