Hematopathology VII Acute Lymphoblastic Leukemia, Chronic Lymphocytic Leukemia, And Hairy Cell Leukemia



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John L. Kennedy, M.D. UIC College of Medicine Associate Professor of Clinical Pathology M2 Pathology Course Lead Pathologist, VA Chicago Health Care System Lecture #43 Phone: (312) 569-6690 Thursday, November 13, 2003 e-mail: John.Kennedy@med.va.gov 9:30 a.m. Important Concepts of Acute Leukemia and ALL 1. Leukemia definition and types: lymphocytic vs myeloid, acute vs chronic. 2. Presenting signs and symptoms of acute leukemia. 3. Features of the L1 lymphoblast vs the myeloblast and the L3 lymphoblast. 4. Cytochemical staining pattern of lymphoblasts. 5. Three immunologic phenotypes with important markers: CD19, CD20, CD10, SIgM, CD7, CD2, CD5, relative frequency of each type, and associated prognosis. 6. Specific cytogenetic abnormalities associated with a poor prognosis. 7. Clinical risk factors. 8. Features of T-cell ALL vs B-cell precursor ALL. LEUKEMIA Leukemia can be defined as an accumulation of neoplastic hematopoietic cells in the marrow with varying numbers of circulating neoplastic cells in the peripheral blood and sometimes soft tissue involvement e.g., splenomegaly, hepatomegaly, and lymphadenopathy. It is an intrinsic bone marrow disease with malignant cells representing lineages normally found in the bone marrow. Leukemia is generally divided into two major groups lymphocytic and myeloid (granulocytic). Both of these are subdivided into acute and chronic leukemia. Acute leukemia is characterized by an accumulation of primitive hematopoietic cells in the bone marrow which are termed blasts, lymphoblasts in acute lymphoblastic leukemia (ALL) and myeloblasts in acute myeloid leukemia (AML). Chronic leukemia is composed of more mature elements e.g., lymphocytes in chronic lymphocytic leukemia or myelocytes to segmented neutrophils in chronic myelogenous leukemia. Page 1 of 13

ACUTE LEUKEMIA Acute leukemia typically presents with signs and symptoms of bone marrow failure. Fatigue and pallor associated with anemia due to depressed erythropoiesis is usually present. Bleeding, commonly due to thrombocytopenia, is a reflection of decreased megakaryocytes in the bone marrow. Infection may be related to neutropenia as a result of depressed granulopoiesis. The combination of anemia, thrombocytopenia, and neutropenia is termed pancytopenia. The white blood cell count (WBC) is variable in acute leukemia and may be decreased, normal, or increased which it is in over half of the patients (sometimes markedly to 300,000 per ul); however, some residual circulating normal leukocytes are most often present in low normal to decreased numbers. One may see a leukoerythroblastic reaction (the presence of immature granulocytes and nucleated RBC's in the peripheral blood due to bone marrow infiltration) which can make the distinction between ALL and acute myeloid leukemia (AML) difficult. When faced with a patient with acute leukemia the most important diagnostic distinction which must be made is to identify the leukemia as being either ALL or AML. The blast cell morphology particularly in the bone marrow can be helpful in this separation. Lymphoblasts Myeloblasts Size Medium size: Medium to large: 15 um. in diameter. 15-20 um. in diameter. Nuclear Round to oval; Round to oval to Configuration may be indented. polygonal; may be indented, folded, or lobulated. Chromatin Pattern Slight chromatin Finely distributed clumping. chromatin. Nucleoli Often absent; 2-5 usually may have 1-2 usually prominent nucleoli. inconspicuous nucleoli. Cytoplasm Scanty, agranular. Relatively abundant; may contain azurophilic granules and/or Auer rods. Unfortunately these cytologic parameters are not always definitive in the distinction between ALL and AML. Page 2 of 13

ACUTE LYMPHOBLASTIC LEUKEMIA Acute lymphoblastic leukemia (ALL) is the most common malignancy of childhood. 75% of all cases of ALL occur in children below the age of 6 years (about 3,200 new cases per year in the U.S.). A group of French, American, and British hematologists devised a morphologic classification of ALL which was published in the mid 1970's termed the F.A.B. classification. ALL was divided into three types based upon nuclear and cytoplasmic features as well as cell size. Only bone marrow aspirate smears not peripheral blood are used for this classification. L1 L2 L3 Size Medium size. Variable with large Large. cells greater than twice the diameter of small lymphocytes. Nuclear Round or angular Uniform to lobulated Oval to round and Configuration nuclei; may have nuclear contours. regular. narrow clefts or folds which do not distort the regular nuclear outline. Nucleoli Absent or small Large prominent Usually multiple inconspicuous nucleoli often with prominent nucleoli. nucleoli. a peripheral chromatin condensation. Cytoplasm Narrow rim of Cytoplasm >20% of Moderately abundant cytoplasm which cell surface area. cytoplasm with may be limited intense basophilia to a small portion (dark blue color) of the cell perimeter. and clear sharply demarcated vacuoles. About 75% of cases of ALL fall into the L1 category which are primarily concentrated in the younger patients aged 1 to 6 years. One should note that the L2 category demonstrates many of the morphologic features of myeloblasts and thus must differentiated from AML using other techniques such as flow cytometry. Page 3 of 13

ALL is diagnosed and categorized based upon immunologic phenotype with some distinctive morphologic, cytogenetic, and clinical features. The various immunologic subtypes of ALL have been identified as representing specific stages of normal B-cell or T-cell maturation. Precursor B Lymphoblastic Leukemia B-lineage surface antigens including CD19, CD20, CD22 Burkitt Leukemia B-lineage surface antigens plus monoclonal surface IgM Precursor T Lymphoblastic Leukemia T-lineage surface antigens including CD7, CD5, CD2 The first evidence of B-cell lineage identifiable is the rearrangement of the immunoglobulin heavy chain gene on chromosome 14. Although one might assume that this DNA programming for immunoglobulin production would be specific for B-cells, it is not. Frequent cases of T-cell ALL show a heavy chain rearrangement and even in AML rare cases with immunoglobulin heavy chain gene rearrangements have been identified. Light chain gene rearrangements are present in about 40% of B-cell precursor ALL with kappa genes always preceding lambda genes in the sequential hierarchy of immunoglobulin gene rearrangements. Light chain rearrangements appear to be quite specific for B-cell lineage and have been identified in non-b cells only exceedingly rarely. Many antigenic markers are recognized on the surface of normal and leukemic cells identified by monoclonal antibodies. CD19 and CD20 are B-cell markers present on virtually 100% and 50% of Precursor B Lymphoblastic Leukemia cases respectively. Burkitt Leukemia is defined by the presence of surface immunoglobulin almost always of IgM type(sigm). A sequence of the appearance of various B-cell markers on the cell surface of developing B-cell precursors in relation to the immunophenotype of B-lineage ALL is seen below. CD19 [ CD20 [ CD22 [ cigm [ sigm Precursor B Lymphoblastic Leukemia Burkitt Leukemia A small proportion of ALL patients (7%) demonstrate one or more myeloid antigens (CD13 or CD33) on the surface of the lymphoblasts. No effect on prognosis has been identified. T cell maturation in the thymus is divided into three stages: early thymocyte, common thymocyte, and mature thymocyte. Although cases of Precursor T Lymphoblastic Leukemia can be assigned to a particular stage of maturation, specific antigens normally present may be missing in individual cases. Early thymocytes are characterized by the presence of CD7 on the cell surface. This is an important marker because it is present on the cells of virtually all T-cell ALL and absent in non T-cell ALL. Early thymocytes are primitive cells which frequently also Page 4 of 13

demonstrate CD2 and/or CD5. The next detectable event in T-cell maturation is rearrangement of the T-beta and T-gamma chain genes of the T-cell antigen receptor which is analogous to immunoglobulin gene rearrangements in B cells. This apparently occurs during the later part of early thymocyte maturation. Common thymocytes are characterized by the presence of CD1, CD4, and CD8. Mature or late thymocytes can be identified as being of either CD4 (helper) or CD8 (suppressor) phenotype. CD3 marks these cells as being mature thymocytes. Phenotypic expression of CD3 occurs in association with the presence of T-beta or T-gamma chain gene products on the cell surface to form the T-cell antigen receptor. Precursor T Lymphoblastic Leukemia Early thymocyte CD7, CD5, CD2 Common thymocyte Mature thymocyte CD1, CD4, CD8 (CD7, CD5, CD2) CD3, CD4 or CD8 (CD7, CD5, CD2) Various age groups reveal some differences with regard to the distribution of immunologic phenotypes. The incidence of T-cell ALL increases with age. Infants Children Adolescents Adults Precursor B 90% 85% 76% 74% Lymphoblastic Leukemia Precursor T 6% 14% 23% 22% Lymphoblastic Leukemia Burkitt Leukemia 4% 1% 1% 4% The prognosis of ALL has been related to the immunologic phenotype as follows from worst to best. PROGNOSIS Precursor B Lymphoblastic Leukemia Best Precursor T Lymphoblastic Leukemia Intermediate Burkitt Leukemia - Worst Cytogenetic study has become an important part of the evaluation of ALL. More than 90% of cases of ALL have karyotype abnormalities. Chromosomes from metaphases are studied using banding techniques to identify clonal cell populations which must demonstrate the identical chromosomal abnormality in two or more metaphases (dividing cells). These studies are performed on peripheral blood if sufficient circulating blasts are available but more commonly Page 5 of 13

on bone marrow, either immediately or after short term (24 hour) culture. A hyperdiploid cell population in ALL with greater than 50 chromosomes is characterized by a gain of whole chromosomes in addition to an intact complement of 46 original chromosomes. Structurally abnormal chromosomes are the exception in this group which has the best prognosis in both children and adults. Other good prognostic factors such as a low WBC at diagnosis, absence of a mediastinal mass, absence of CNS disease at diagnosis, and ALL of other than T- cell type have been associated with the hyperdiploid greater that 50 group. The hyperdiploid group with 47-50 chromosomes has a less favorable prognosis particularly in adults. Certain specific karyotypic abnormalities have a particularly bad prognosis such as the Philadelphia chromosome t(9;22) (4% of childhood ALL, 10-20% of adult ALL). The t(8;14) translocation of Burkitt Leukemia transfers the c-myc oncogene from chromosome 8 to the heavy chain gene locus on chromosome 14 correlating with the IgM surface immunoglobulin expression in these cells. One important additional translocation associated with a poor prognosis is t(4;11) seen in ALL in the first year of life. A number of risk factors for ALL with a poor prognosis have been identified using clinical, laboratory, and physical examination data. Clinical Risk Factors WBC > 50,000 Age < 1 or > 10 years Male gender Mediastinal mass Pretreatment CNS disease Hepatomegaly, splenomegaly, and/or massive peripheral lymphadenopathy The most important risk factor is a high WBC. It is an independent risk factor which cuts across the immunologic phenotypic groups of ALL such that Precursor B Lymphoblastic Leukemia with a high WBC has a prognosis similar to Precursor T Lymphoblastic Leukemia. A high WBC, mediastinal mass, lymphadenopathy, and hepatosplenomegaly probably all reflect a large tumor burden. Age is the second most important risk factor, particularly in patients less than one year of age who do quite poorly. Other risk factors include severe thrombocytopenia, hypogammaglobulinemia, and L2 morphology. However, 25% of the high risk patients do achieve long term survival. Page 6 of 13

T-cell ALL has a few rather distinctive clinical features some of which have been associated with poor prognosis of this group in general. The table below contrasts Precursor B Lymphoblastic Leukemia, Precursor T Lymphoblastic Leukemia T-cell, and Burkitt Leukemiacell ALL in terms of risk factors. Precursor B Precursor T Burkitt Lymphoblastic Lymphoblastic Leukemia Leukemia Leukemia Median WBC 12,500/mm 3 63,000/mm 3 30,000/mm 3 Median age 4 yrs. 9 yrs. 8 yrs. Male gender 54% 68% 67% Mediastinal mass 1% 52% 0% Lymphadenopathy 3% 20% 24% Cytogenetics 29% 2% 0% Hyperdiploid >50 chromosomes The typical patient with Precursor T Lymphoblastic Leukemia is an adolescent male with a somewhat lymphomatous presentation (mediastinal mass and/or peripheral lymphadenopathy) and a high WBC. These features are usually lacking in Precursor B Lymphoblastic Leukemia. Burkitt Leukemia patients are often older children with lymphadenopathy and CNS involvement. The overall prognosis of ALL is fairly good with a 70% 5-year survival. 70% of children are cured with modern therapy and achieve a long term disease free survival. Therapy for ALL is determined by the risk factors identified in the individual patient and is termed standard risk, intermediate risk, or high risk therapy. Induction chemotherapy utilizes the standard drugs used in ALL including vincristine, prednisone, L-asparaginase, and usually an anthracycline such as daunorubicin. With this regimen virtually all children and 70-80% of adults with ALL attain complete remission. For intermediate risk and high risk ALL induction therapy utilizes additional drugs and is repeated one or more times after achievement of complete remission, a process called consolidation. The challenge of ALL treatment is the maintenance of complete remission. In the past CNS relapse was a major problem occurring in over 50% of patients who were otherwise in remission. This has been reduced to less than 5% through the institution of CNS prophylaxis which usually consists of triple intrathecal therapy utilizing methotrexate, hydrocortisone, and cytosine arabinoside with or without cranial irradiation. After induction therapy and CNS prophylaxis, patients are continued on maintenance chemotherapy for three years from diagnosis if relapse does not occur. At that time therapy is discontinued and is not reinstituted unless relapse occurs. If a patient relapses while on therapy or during the first year after coming off therapy, the possibility of long term survival is markedly reduced unless successful bone marrow transplantation can be performed. If a patient relapses greater than a year after therapy is discontinued, reinduction and attainment of a second long disease-free interval can often be obtained with the same drugs used initially. Most relapses occurring after therapy is discontinued happen during the first year after the cessation of drug therapy. Thus with each year of disease-free survival off therapy, the probability of relapse becomes increasingly remote. Page 7 of 13

References: 1. FAB classification of acute leukemia. Brit. J. Haematol. 33:451, 1976 2. Morphologic classification of ALL. Brit. J. Haematol. 47:553, 1981. 3. Adult ALL. N.E.J.M. 311:1219, 1984. 4. DNA studies in ALL. N.E.J.M. 313:1033, 1985 and J. Clin. Invest. 71:301, 1983. 5. CALLA. Blood 61:628, 1983. 6. Immunologic phenotype in ALL. Cancer Research 41:4752, 1981, Med. Pediat. Onc. 14:135, 1986, Blood 82:343, 1993. 7. Immunologic markers in T-cell ALL. Proc. Natl. Acad. Sci. 77:1588, 1980, Blood 68:134, 1986, Blood 69:1062, 1987, and Cancer 59:2020, 1987. 8. Immunologic markers in ALL in relation to normal lymphoid maturation. Blood 56:1120, 1980, and J. Clin. Invest 74:332, 1984. 9. Cytogenetic in ALL. Blood 60:864, 1982, N.E.J.M. 313:640, 1985, Cancer Gen. and Cytogen. 11:233, 1984, and Blood 70:247, 1987. 10. Risk factors in ALL. Am. J. Ped. Hem./Onc. 5:243, 1983, and Med. Pediat. Onc. 14:124, 1986. Page 8 of 13

Important Concepts of CLL 1. Clinical features. 2. PB morphology. 3. Typical immunologic phenotype: CD19, CD5, SIgM/IgD. 4. Prognosis in general and as related to clinical stage CHRONIC LYMPHOCYTIC LEUKEMIA Chronic lymphocytic leukemia (CLL) is the most common leukemia in the United States comprising 30% of all leukemia in this country. It is a disease of adults with a median age at diagnosis of 60 years. Males are affected more often than females by ratio of 2:1. CLL is characterized by an accumulation mature-appearing lymphocytes in the peripheral blood, bone marrow, and lymph nodes. The neoplastic lymphocytes are small (8-10 um. in diameter) with clumped nuclear chromatin and small to moderate amounts of cytoplasm. An absolute lymphocytosis of >4,000 lymphocytes per ul is invariably present with the WBC typically ranging between 20,000 and 100,000. The marrow is infiltrated by small lymphocytes which represent >30% of the cellular elements in the marrow. Anemia if present is usually mild and the platelet count is usually normal at diagnosis. Mild lymphadenopathy is common and splenomegaly, if detected, is modest. This is an indolent disease and many CLL patients are completely asymptomatic with the diagnosis being made on a routine CBC. Although the prognosis is fairly good with a median survival of 5 years, a staging scheme has been developed to assess the extent of disease and correlate with survival. International Workshop on CLL Clinical Staging Proposal Clinical Stage A Clinical Stage B Clinical Stage C areas No anemia or thrombocytopenia and less than three areas of lymphoid enlargement. No anemia or thrombocytopenia with three or more involved areas. Anemia and/or thrombocytopenia regardless of the number of of lymphoid enlargement. Anemia is defined as a hemoglobin <10g/dL and thrombocytopenia is defined by a platelet count <100,000 per ul. Five areas are assessed for lymphoid enlargement: liver, spleen, cervical, axillary, and inguinal lymph nodes. Involvement is defined by organomegaly or lymphadenopathy whether unilateral or bilateral. Median survival does correlate with clinical stage. Page 9 of 13

Distribution of CLL Cases and Median Survival by Clinical Stage Clinical Stage A 66% not reached Clinical Stage B 30% 54 months Clinical Stage C 4% 22 months The five year survival for Clinical Stage A was 79% The influence of stage on survival reveals a clinical problem that many patients face eventually, which is cytopenia. Bone marrow function becomes compromised as it is progressively infiltrated by the small lymphocytes. Infection is the major cause of death. This is not only related to neutropenia but also to hypogammaglobulinemia observed in about 50% of CLL patients. Greater than >95% of cases of CLL demonstrate a B-cell immunophenotype. The neoplastic lymphocytes characteristically display small amounts of monoclonal IgM on the cell surface often accompanied by IgD of the same idiotype. Other commonly observed surface markers include CD19, CD20, and CD23. Interestingly, one pan T-cell antigen, CD5, is identified in almost all cases of CLL. Trisomy 12 is the most frequent cytogenetic abnormality seen in CLL although a normal karyotype is identified in about one third of the patients. Trisomy 12 is seen in over half of the patients with an abnormal karyotype but is often accompanied by other karyotypic chromosomal changes. Survival is significantly worse for patients with trisomy 12 plus other abnormalities than for patients with only trisomy 12 or with a normal karyotype. Because of the indolent nature of the disease, CLL is usually not treated until the patient becomes symptomatic. Treatment is typically initiated with single agent chemotherapy such as chlorambucil or fludarabine. Indications for therapy include: a markedly elevated lymphocyte count, progressive anemia or thrombocytopenia, symptomatic lymphadenopathy or organomegaly, and complications such as recurrent infections, hemolytic anemia, or transformation to a more aggressive phase of disease. Transformation in CLL is heralded by fever, progressive asymmetric lymphadenopathy, and organomegaly. Histologically the lymph nodes show conversion from an infiltration by small lymphocytes to large cell lymphoma. This phenomenon has been termed Richter's syndrome. Rapid progression to death is the typical course after transformation. CLL does not convert into an acute leukemia thus a blast crisis is not observed in this disease. Page 10 of 13

References: 1. Biology of CLL. Sem. Hematol. 24:209-29, 1987. 2. Clinical staging of CLL. Cancer 48:198, 1981 and Semin. Hematol. 24:275, 1987. 3. Cytogenetics in CLL. N.E.J.M. 310:288-92, 1984. 4. Transformation of CLL (Richter's syndrome). Cancer 46:118-34, 1980 and Cancer 48:1302, 1981. Page 11 of 13

Important Concepts of HCL 1. Clinical features. 2. B-cell immunophenotype of hairy cells. HAIRY CELL LEUKEMIA (Leukemic Reticuloendotheliosis) Hairy cell leukemia (HCL) is an uncommon form of chronic leukemia characterized by an insidious onset, massive splenomegaly without lymphadenopathy, pancytopenia, dry bone marrow aspiration, and the presence of abnormal circulating mononuclear cells. Males predominate in this disease which tends to appear in the sixth decade. The number of circulating leukemic cells is variable but usually the WBC is decreased due to neutropenia. The neoplastic cells are termed hairy cells because of numerous hair-like cytoplasmic projections around the periphery of the cytoplasm. The nuclei are round to oval or slightly indented with chromatin which is more finely clumped than that of a mature lymphocyte. The most distinctive feature is the abundant cytoplasm which is pale blue and appears delicate. Because only low numbers of leukemic cells are often present in the peripheral blood, the diagnosis is usually made on the bone marrow biopsy. The histologic picture is one of a normal to hypercellular bone marrow with partial replacement of the normal marrow elements by an infiltrate of bland-appearing cells with abundant cytoplasm. The nuclei resemble those of lymphocytes and the abundant cytoplasm appears clear in the biopsy sections giving the cells a "fried egg" appearance. Increased reticulin is present in the bone marrow causing the dry tap with attempted aspiration. The pancytopenia relates to marrow infiltration as well as hypersplenism due to the massive splenomegaly. The spleen, which may be removed for therapeutic purposes, is markedly enlarged with an average weight of 1800g (nl 150-200g). The splenomegaly is due to expansion of the red pulp by a diffuse infiltration of hairy cells similar in appearance to the bone marrow. The pulp cords are widened and occasional dilated blood-filled spaces are seen which have been termed pseudosinuses or red cell lakes. The classic cytochemical test used to confirm the presence of hairy cells is the tartrate resistant acid phosphatase (TRAP) reaction. While the great majority of patients with HCL show persistent acid phosphatase positivity despite pretreatment of the smears with tartrate, it is not specific for hairy cell leukemia, and positive reactions are observed occasionally in some other disease states such as CLL. HCL is a B-cell leukemia at a more mature stage of maturation than CLL. This is demonstrated by the presence of more advanced isotypes of monoclonal immunoglobulin on the cell surface, specifically IgG and IgA. In fact, many cases of HCL appear to be arrested in maturation at the point of immunoglobulin heavy chain switching with multiple heavy chain isotypes including Page 12 of 13

IgG, IgA, IgM, and/or IgD on the cell surface simultaneously with a single light chain type indicating monoclonality. In addition, it has a somewhat distinctive pattern of surface markers: CD19, CD20, CD22, CD11c, CD25, FMC7, and CD103. Some patients with HCL have indolent disease requiring no specific therapy. In the past when therapy has been indicated due to massive splenomegaly, severe pancytopenia, or recurrent infection, splenectomy was the therapy of choice. This resulted in significant improvement of peripheral counts in about 50% or patients. Patients with progressive disease post-splenectomy remained major therapeutic problems, and the median survival for all HCL patients was about 4 years. Today alpha interferon or 2-CdA is administered producing often prompt reduction in spleen size and improvement or normalization of peripheral counts with many long term survivors, obviating the need for splenectomy in patients today. References: 1. Clinicopathologic features of HCL. Cancer 33:1399-1410, 1974, A.J.C.P. 70:876-84; 1978; A.J.C.P. 67:415-26, 1977. 2. Cytochemistry of HCL. A.J.C.P. 68:268-72, 1977. 3. Immunology of HCL. Blood 59:52-60, 1982, Blood 59:609-14, 1982. 4. Therapy of HCL. N.E.J.M. 310:15-18, 1984, N.E.J.M. 307:495-6, 1982, Blood 68:493-7, 1986. Page 13 of 13