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1 NON-HODGKIN S LYMPHOMA IN CHILDREN Correlation of CNS Disease With Initial Presentation. JOHN J. HUTTER, JR., MD,* BLAISE E. FAVARA, MD,+ MICHAEL NELSON, MD (MAJOR),$ AND CHARLENE P. HOLTON, MD The clinical and histopathological findings in 26 children with non-hodgkin s lymphoma without initial marrow involvement are reviewed. A marked male predominance similar to that observed in previous series was noted. Biopsy material was classified according to the recommendations of Rappaport in 22 cases. All have diffuse lymphomas, and 16 of 22 patients had diffuse, poorlydifferentiated,!ymphocytic lymphoma. Twelve of 26 patients had involvement of the mediastinum as part of their initial presentation. Of these 12, 5 developed lymphomatous involvement of the central nervous system prior to the development of leukemic transformation of the bone marrow. This observation suggests that prophylactic therapy against CNS relapse be considered for children with mediastinal non-hodgkin s lymphoma, even in the absence of initial marrow involvement. Cancer 36: , N RECENT YEARS, ADVANCES IN CHEMOTHERAPY I and radiation therapy have led to an improvement in the duration of remission and survival of children with Hodgkin s disease, *18 and acute lymphoblastic leukemia (ALL) Satisfactory guidelines have not been completely developed for the therapy of non-hodgkin s lymphoma (NHL) in children. The reasons for this are multiple and include: 1) the fulminant course of some cases with this disorder; 2) the variety of clinical presentations and extent of disease at the time of diagnosis; 3) a poor correlation between clinical and surgical staging procedures with prognosis as compared to the correlation observed for Hodgkin s disease; 4) the slow development of a standard pathological From the Oncology Center, The Children s Hospital, Denver CO. * Associate Director of Oncology, Oncology Center, The Children s Hospital, Denver, CO. and Junior Faculty Clinical Fellow, American Cancer Society. Pathologist and Director of Laboratories The Children s Hospital Denver, CO. t Resident in Pediatrics, Fitzsimons Army Medical Center, Denver, CO. 5 Director of Oncology, The Children s Hospital, and Clinical Assistant Professor of Pediatrics, The University of Colorado Medical Center, Denver, CO. Address for reprints: John J. Hutter, Jr., MD, Associate Director of Oncology, Oncology Center, The Children s Hospital, 1056 East Nineteenth Avenue, Denver, CO Supported in part by the Pediatric Oncology Center Grant No. 3 PO 2 CA Received for publication November 19, classification; and 5) the small number of cases seen at each center. The comparison of series between centers is difficult because of differences in staging, therapy and pathological classification. In spite of these limitations, an improvement in survival of children with NHL has been observed with the use of supravoltage radiation therapy and intensive chemotherapy.2622 The difference in natural history and epidemiological features between NHL in children and the disease in adults is well-recognized. 7*8*20 Children with NHL have a high incidence of leukemic transformation which has ranges from 15 to 70%.23~5~&411.17~1v-21 Of interest is the question whether the prolongation of survival in children with NHL will lead to an increased incidence of central nervous system relapse such as that previously seen in acute leukemia. The purpose of this report is to document the clinical and pathological findings in 26 children with NHL and to relate these findings to prognosis and the development of central nervous system disease MATERIALS AND METHODS Twenty-six children with NHL were seen at The Children s Hospital, Denver, over a 15-year period from Complete followup information was on all children. Because of the variability in the initial evaluation of patients over this time period, no attempt is
2 No. 6 NON-HODGKIN'S LYMPHOMA IN CHILDREN Hutter et al made to establish clinical staging of disease. All patients had a normal bone marrow aspirate at the time of initial diagnosis, and there were no malignant cells in the peripheral blood. The records of these patients were analyzed and information relating to age, sex, presenting signs and symptoms, central nervous system involvement, local recurrence, conversion to leukemia, and survival were obtained. All biopsy material was reviewed by one of us (BEF) and classified according to the recommendations of Rappaport.13 A bone marrow conversion to leukemia in this report consists of a bone marrow aspirate that contains greater than 5% blast cells. RESULTS Twenty-one patients were male and 5 were female. This marked male predominance is similar to that observed in previous series."." Twelve patients, 9 boys and 3 girls, had involvement of the mediastium as all or part of, or as the single initial presenting sign (Table 1). Pathological material could not be classified in 4 instances: 3 patients had the diagnosis of lymphoma established by the presence of a medias- tinal mass and malignant cells in a pleural effusion, or other non-nodal local tissue. The fourth child had radiation therapy instituted prior to obtaining the biopsy specimen. The remaining 8 had diffuse, poorly-differentiated,, malignant lymphoma. The median survival of the 10 patients with mediastinal presentation who died is 6 months (range 1-31 months). One patient had involvement of the central nervous system at the time of the inital diagnosis and four others developed lymphomatous meningeal involvement documented by lumbar puncture. Bone marrow aspirates performed at the time of CNS involvement revealed no evidence of leukemic conversion. Bone marrow biopsies were not obtained. A sixth patient had symptoms of severe headache and vomiting at a time when the bone marrow showed no leukemic conversion. A diagnostic lumbar puncture was not performed on this latter patient and permission for autopsy was not obtained. None of the 5 children with CNS recurrence received prophylactic central nervous system irradiation. The 2 survivors (J.M., M.S.) with mediastinal presentation at 6+ months had both received early prophylactic cranial irradiation and intrathecal methotrexate. 1 ) 1)s TABLE 1. Children with hledistinal NHL CNS involvement Time from diagnosis prior to marrow to CNS relapse Pt. Age Sex conversion? (Mo.) Histology Survival (months) 2)5.\1* 3) X1H 4) '13 5) I)U 4 M Yes 9 1 M No - 3 M Yes CNS involvement at diagnosis 4 M No - 1 F No - 6) SS 4 F No - 7) JJ 9 F Yes 6 8),11, 5 M Yes 7 9) XIY 8 M Yes' 1 10) c:<; 10 M Yes 3 11) KI' 9 - M No - 12) XIS* 10 M No - Diffuse, poorly differentiated, Diffuse, poorly difrerentiated, Iliffuse, poorly differentiated, IliHuse, poorly differentiated, Diffuse, poorly differentiated, IXffuse, poorly ditferentiated, I)iffuse, poorly dilferentiated, I)iffuse, poorly difrerentiated, * Patients who have received early prophylactic cranial irradiaion t intrathecal methotrexate. ' Clinical evidence of CNS involvement at time of a normal bone marrow. Lumbar puncture not performed I -5 I 8 7 I t
3 2134 CANCER December 1975 Vol. 36 Six of the 12 (50%) children who had initial involvement of the mediastinum eventually developed a bone marrow leukemic conversion. Simultaneous recurrence in the bone marrow and CNS was observed in one child (S.S.). Three of the patients who had CNS involvement prior to marrow leukemia eventually developed bone marrow conversion to leukemia. Nine patients, 8 males and 1 female, presented with lymphoma involving the gastrointestinal tract at time of initial presentation. The age, site of involvement, histopathology and survival of these patients are outlined in Table 2. Four patients (N.C., W.B., A.B., J.U.) had disease confined to the intestine. Following surgical resection of the tumor, the children received radiation therapy and adjuvant chemotherapy. Three of the 4 patients with localized disease had signs or symptoms of intussusception. The fourth (A.B.) presented with a 1 '/2 year history of crampy abdominal pain and poor growth. After therapy of the lymphoma, the chronic abdominal pain regressed completely and his growth has improved markedly. Of the remaining patients with intestinal involvement, marrow conversion to leukemia occurred in only one. The 2 survivors who are disease-free at 18+ and 45+ months both had surgically non-resectable lymphomas with involvement of the mesentery and retroperitoneal nodes. Both survivors received radiation therapy of K to the abdomen, followed by combination chemotherapy with prednisone, vincristine and cyclophosphamide. Chemotherapy was discontinued in S. B. after 36 months, and he remains clinically well. None of the patients with GI lymphoma received prophylactic central nervous system irradiation. The age, site of presentation, histology and survival of the five children with NHL who did not have involvement of the mediastinum or intestine are listed in Table 2. The long-term survivor at 66+ months received 3500 K to the abdominal, pelvic and periaortic nodes followed by two years of chemotherapy with vincristine and cyclophosphamide. Extra-dural involvement of the thoracic spinal cord was observed in one patient (P.H.) after he developed generalization of his disease to include mediastinal and retroperitoneal lymph nodes. The remaining three patients converted to leukemia, and one of the convertors subsequently developed leukemic meningitis. The age of diagnosis in all patients is shown in Fig. 1. The distribution is bimodal with peak incidence in the 4-6 and 8-12 age ranges. There was no correlation observed between age and either the site of origin or histopathology of the tumor. There was also no relationship between the age of onset and tendency to convert to leukemia. Serum uric acid was measured prior to therapy in 7 patients and was elevated in 6. Elevated values ranged from 7.2 to 12.5 mg% (upper limits of normal for our laboratory = 5.3 mg%). DISCUSSION Sixteen of 22 patients in this series had diffuse, poorly-differentiated, lymphomas. The histology of a lymph node with this form of NHL is felt by some to be in- TABLE 2. Children with Gastrointestinal NHL Pt. Age Sex Site Histology Survival (months) 1) LS 15 F Ileum Iliffuse histiocytic lo+ 2)JU 6 M Ileum IlifIuse, poorly diflerentiated, I2+ 3) GR 4 M Sigmoid Iliffuse, poorly differentiated, 2 4) WB 8 M lleocecal IXHuse, poorly dilierentiatcd, 75+ valve 5) SB 9 M Ileum Diffuse, poorly ditlercnti;tted, 4.i+ 6) RB 5 M Duodenum Diffuse, mixed histitxytic- 7 7) DS 9 M Jejunum Diffuse, mixed histiocytic- 6 8) NC 1 M Jejunum Iliffuse, mixed histicxytic ) AB 3 M Ileum Iliffuse, mixed histiocytic- I I+
4 No. 6 NON-HODGKIN'S LYMPHOMA IN CHILDREN Hutter et al TABLE 3. Children with NHL: Sites other than Intestine or Mediastinum Pt. Age Sex Site Histology Survival (months) 1 ) '1W 2) I)L 3) PH 4) I)H 5) bla 10 F Epitrochlear 11 M Cervical nodes + nasopharynx 4 M Cervical nodes 6 M Ketroperitoneal nodes 8 M Inguinal + retroperitoneal nodes Diffuse, poorly differentiated 49 Diffuse, poorly differentiated, 3 I ymp hocy t ic Iliffuse, poorly differentiated, 2 Diffuse, poorly differentiated, 2 Diffuse histiocytic 66+ distinguishable from that seen in acute lymphoblastic leukemia. This similarity, along with the high conversion rate to leukemia of children with NHL, raises the question as to whether these entities are merely different forms of the same disease. Several important differences, however, do stand out. There is a marked male preponderance in children with NHL. Thirteen of the 16 children with diffuse, poorly-differentiated lymphoma in this series were boys, for a M:F ratio of 4.3:l. This ratio, also noted by others,'*'' is much higher than the slight male preponderance observed in children with acute lymphoblastic leukemia. l5 The presence of a mediastinal and/or gastrointestinal mass, which occurs in the majority of children with NHL, is observed much less frequently in ALL. Some patients with diffuse, poorly-differentiated, lymphoma are curable by radiation alone. Finally, recent observations of the frequency of occurrence of cell-surface markers on ALL lymphoblasts indicates that the majority of these cells have neither a T nor B cell One small series of 4 children with lymphoblastic NHL revealed that the malignant cells in each case bound sheep erythrocytes, a characteristic of the T cell. lo Only one other series of non-hodgkin's lymphoma in children utilizing the Rappaport classification has been previously published.' The most frequent pathological type in our series was diffuse,, poorly-differentiated lymphoma (DLPD) with 16 of 22 children having this type of lymphoma. This contrasts with the previous series where 13 of 32 had diffuse, histiocytic lymphoma, and 11 of 32 had DLPD. No patient in our-series, and only 4 in the previous series, had diffuse, undifferentiated lymphoma. Another recent series of NHL classified 30 to 50 children as having diffuse, undifferentiated, non-burkitt's lymphoma. The relation- ship of this latter classification to the Rappaport classification, however, is not entirely clear. A lower predilection for leukemic transformation in children with abdominal presentations of NHL has been previously noted.b'8'21this observation is supported by our experience of a bone marrow conversion rate of 6 of 12 (50%) for mediastinal lymphoma, none of four (0%) for lymphoma confined to the intestine, one of five (20%) for gastrointestinal lymphoma with spread to other abdominal structures, and 3 of 5 (60%) for lymphoma at other sites. Five children had documented evidence of lymphomatous involvement of the central nervous system at a time when bone marrow aspirates revealed no evidence of leukemic transformation in the bone marrow. Bone marrow biopsies have subsequently been shown to be superior to aspirates in demonstrating marrow involvement in lymphoma. ' Unfortunately, marrow biopsies were not obtained on these Age (in years) FIG. 1. Age at diagnosis of 26 children with NHL.
5 2136 CANCER December 1975 Vol. 36 patients. It is possible that all or some of these patients had focal marrow recurrence at time of CNS disease. Only 3 of the 5 subsequently developed an overt leukemic conversion. A sixth who did not receive an LP had a history of severe vomiting and headache compatible with increased intracranial pressure. All 6 had involvement of the mediastinum at the time of diagnosis. This strongly suggests that the mediastinal presentation of childhood NHL has a greater incidence of initial recurrence in the CNS in addition to its greater incidence of leukemic transformation. Detailed staging was not performed in all of our patients, however, and the possibility remains that CNS recurrence may be related to the stage of disease as well as to the initial site. The majority of patients with mediastinal disease at diagnosis also had involvement of peripheral node groups. This observation of initial CNS recurrence of mediastinal NHL has not been described in the of mediastinal NHL in this series at 6+ and 31+ months both received early prophylaxis with 2400 K cranial radiation plus intrathecal methotrexate. Further studies with larger numbers of patients will be required to evaluate the role of prophylactic central nervous system therapy in children with NHL. The value of intensive radiation therapy and chemotherapy in abdominal lymphoma is demonstrated by the response of two patients in this series who had surgically non-resectable tumors with involvement of the mesentery and abdominal nodes. Both of these patients were treated within the last 5 years and are without evidence of disease at the time of this report. A third patient had involvement of the inguinal nodes at the time of diagnosis. Abdominal node dissection revealed the presence of involved retroperitoneal nodes. He was treated with radiation therapy and 2 years of vincristine and cytoxan chemotherapy, and remains well without disolder large series of NHL in ~ hildren,~*~*~,~~ and ease 66+ months later. was also not observed in the more recent series Uric acid nephropathy with renal shutdown utilizing the Rappaport classification.' As more in lymphoma has been described. The elevated effective radiation therapy and chemotherapy uric acid of the patients prior to therapy in this are being used to control the initial presentation series would indicate that, as more intensive of NHL, the CNS may be a sanctuary for this therapy is used in NHL, attention will have to disorder, similar to the experience observed for be paid to the use of proper therapy with hydra- ALL. In the series of Glatstein et al., the CNS tion, allopurinol and urine alkalinization in was not the site of initial relapse for any of their an attempt to reduce the risk of uric acid patients, but only 3 patients had mediastinal nephropathy. diffuse, poorly-differentiated, lym- Central nervous system recurrence prior to phomas. Other series have noted the importance bone marrow transformation in children with of the CNS as a relapse site in NHL.'7s21*22 non-hodgkin's lymphoma of the mediastinum is The administration of 2400 R craniospinal a clinical problem. It would appear warranted radiation or 2400 R cranial irradiation with in- that, in the initial therapy of children with metrathecal methotrexate has been shown to be of diastinal lymphoma of the diffuse value in reducing the incidence of initial recur- type, consideration should be given to the use of rence in the CNS in children with acute leu- prophylactic measures against CNS recurrence, kemia. l5 It is noteworthy that the two survivors even in patients without leukemic conversion. REFERENCES 1. Aghai, E., Hulu, N., Virag, I., et al.: Childhood Non- Hodgkin's lymphoma-a study of 17 cases in Israel. Cancer 33: , Aur, R. J., Hustu, H. O., Simone, J. V., et al.: Therapy of localized and regional lymphosarcoma of childhood. Cancer 27: , Bailey, R. J., Burgert, E. 0. Jr., and Dahlin, D. C.: Malignant lymphoma in children. Pediatrics 28: , Borella, L., Sen, L., and Green, A. A.: Cell surface markers and clinical features in acute leukemia. Proc. Am. Assoc. Ca. Res. 15:122, Dargeon, H. W.: Lymphosarcoma in childhood. Am. 1. Roenlgenol. 85: , Glatstein, E., Kim, H., Donaldson, S. S., et al.: Non- Hodgkin's lymphomas VI. Results of treatment in childhood. Cancer 34: , Grundy, G. W., Creagan, E. T., and Fraumeiri, J. F. : Non-Hodgkin's lymphoma in childhood: epidemiological features. 3. Nail. Cancer Inst. 51 : , 1973.
6 No. 6 NON-HODGKIN S LYMPHOMA IN CHILDREN Hutter et al Jones, B., and Klingberg, W. G.: Lymphosarcoma in children. J. Pediatr. 63:l 1-20, Jones, S. E., Kosenberg, S. A,, and Kaplan, H. S.: Non-Hodgkin s lymphomas. I. Bone marrow involvement. Cancer. 29: , Kaplan, J., Mastrangelo, K., and Peterson, W. D.: Childhood lymphoblastic lymphoma, a cancer of thymusderived lymphocytes. Cancer Res. 34: , I. Maxwell, G. M. : Twelve cases of lymphoblastomata in children. Arch. Ilts. Child. 29: , Pinkel, D.: Five-year follow-up of total therapy of childhood leukemia. J AMA 216:648, Kappaport, H.: Tumors of the hematopoietic system. In Atlas of Tumor Pathology, Section 111, Fascicle 8 (1966). Washington, 11. C., Armed Forces Institute of Pathology, pp Schey, W. L., White, H., Conway, J. J., et al: Lymphosarcoma in children: a roentgenologic and clinical evaluation of 60 children. Am. J. Roentgenol. 117:59-72, Simone, J. V.: Acute leukemia in childhood. Semin. Hematol. 1 1 :25-40, Smith, K. J., Johnson, D., Hustu, O., et al.: Concurrent chemotherapy and radiation therapy in the treatment of childhood and adolescent Hodgkin s disease. Cancer 33:38-46, Sonley, M. J.: Lymphosarcoma in childhood. Paediatriclan 1 : , 1972/ Strum, S. B., and Rappaport, H.: Hodgkin s disease in the first decade of life. Pediahcs 46: , Sullivan, M. P.: Leukemic transformation of lymphosarcoma of childhood. Pehatrics 29: , Sullivan, M. P.: Non-Hodgkin s lymphoma of childhood. In Clinical Pediatric Oncology W. W. Sutow, T. J. Vietti, and D. J. Fernbach, Eds. St. Louis, C. V. Mosby, 1973; pp Watanabe, A., Sullivan, M. P., Sutow, W. W., et al.: Undifferentiated lymphoma, non-burkitt s type, Am. 3. Dis. Child. 125:57-61, Wollner, N., Burchenal, J., Lieberman, P., et al.: Incidence of CNS and bone marrow metastases in non- Hodgkin s lymphoma in children. Proc. Am. Assoc. Cancer Res. 15:107, 1974.
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