Childhood Non-Hodgkin s Lymphoma in Saudi Arabia
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1 Childhood Non-Hodgkin s Lymphoma in Saudi Arabia Clinical Features of 100 Cases Othman S. Bin Ahmed, MD* and Rajih S. Sabbah, MD * Junior Staff, Department of Pediatrics; Pediatric Hematologist and Oncologist, Chairman, Department of Oncology, King Faisal Specialist Hospital and Research Centre ABSTRACT One hundred children with non-hodgkin s lymphoma (NHL), 80 boys and 20 girls, ranging in age from two to 15 years (median five years), were seen at the King Faisal Specialist Hospital and Research Centre over a period of five years ( ). This constituted 17 percent of all childhood malignancies seen at this Hospital during the same period. Abdominal pain, anorexia, and weight loss were the most frequent presenting complaints. The primary sites of initial involvement included: abdomen in 79 patients, mediastinum in 11 patients, long bones in two patients, neck and skin in one patient each, and undetermined in six patients. According to histologic classification, the following subtypes were seen: lymphoblastic, 11 cases; undifferentiated non-burkitt's, 67 cases; undifferentiated Burkitt s, 17 cases; histiocytic, four cases; and Mediterranean lymphoma, one case. The most useful diagnostic radiographic procedures were sonography of the abdomen and chest radiography. The Burkitt s lymphoma demonstrated space-time clustering but other forms of lymphoma showed rather uniform distribution. The results of this study indicate that childhood NHL is more common in Saudi Arabia than in Europe and in the United States, that it occurs at a much younger age, and that it shows the predominance of the abdominal form. OS Bin Ahmed, RS Sabbah, Childhood Non-Hodgkin s Lymphoma in Saudi Arabia: Clinical Features of 100 Cases. 1982; 2(4): KEYWORDS Lymphoma in infancy and childhood Saudi Arabia Introduction Geographical differences in the incidence of various childhood cancers, especially the lymphomas, are well documented. 1 While this is most evident in the case of Burkitt s lymphoma (BL), remarkable differences exist among countries in relation to the frequency with which the other lymphomas are seen. 2 Non-Hodgkin s lymphoma appears to be at least three times more common in the Middle East than it is in Europe or the United States. 3 In addition, the relative frequency of various histologic types, the sites of involvement and the age groups are believed to be different. The purpose of this report, therefore, is to describe the clinical features in 100 children with non- Hodgkin s lymphoma (NHL) seen at the King Faisal Specialist Hospital and Research Centre over a period of five years. Patients and Methods Children with NHL were referred to the King Faisal Specialist Hospital and Research Centre from various parts of Saudi Arabia. They were prospectively studied according to uniform serial protocols designed to document the clinical, histopathologic, and epidemiologic features of NHL in the Kingdom. Generally, initial evaluation included a history, physical examination, complete blood count, biochemical profile using the SMAC-20 blood analyzer, quantitative immunoglobulins, chest radiography, intravenous pyelography (IVP), radioisotopic scans of the liver, spleen and bones, and sonography of the abdomen. Bone marrow aspiration and lumbar punctures were done routinely. Computerized tomographic (CT) scan of the brain and abdomen were done upon clinical indication. Tissue for diagnosis was obtained by open surgery in 48 cases, Tru- Cut needle biopsy in 30 cases, or fine needle aspiration biopsy (FNA) in 22 cases. 4 Electron microscopic examination was done in 21 cases, 11 on an FNA specimen.
2 Figure 1. Age and sex distribution of 100 children with NHL. The modified Rappaport classification was used for histopathologic characterization of these patients. 5 According to this system, the lymphoma was called lymphoblastic (convoluted or nonconvoluted), undifferentiated (Burkitťs and non-burkitt s) or histiocytic (HL). Immunoproliferative small intestinal disease (IPSID) or Mediterranean lymphoma was added to this classification because it is unique to this part of the world. 6 Results Incidence We saw 100 children with NHL over a period of five years. During the same period the total number of childhood cancers was 587, an NHL incidence of 17 percent. Age and Sex This series includes 80 boys and 20 girls (M : F ratio 4:1). Figure 1. Their ages ranged from two to 15 years (median five years). Boys and girls under the age of three years were equally affected. Thereafter, there was a higher incidence in boys. Histology There were 11 cases of lymphoblastic lymphoma, 17 cases of Burkitťs lymphoma, 67 cases of diffuse undifferentiated lymphoma of the non-burkitt s type, four cases of histiocytic lymphoma, and one case of immunoproliferative small intestinal disease (IPSID) or Mediterranean lymphoma. Geographic and Seasonal Distribution The places of residence of 77 of these patients are shown on the map of the Kingdom of Saudi Arabia. Figure 2. In 23 cases the exact place of residence was not known. The number in brackets indicates cases of Burkitťs lymphoma and the number following the brackets indicates patients with other types of lymphoma who resided in that particular city. While BL occurred primarily in the coastal area of the Red Sea, other types of lymphoma occurred in all parts of the Kingdom. 7 The approximate dates of the onset of the illness reported by the parents are shown in Figure 3. While all types of NHL showed seasonal variation with more cases occurring during the period from December to April, this timeclustering was more evident with BL. Clinical Features The commonest presenting complaints as reported by the parents were swelling of the abdomen, 73 cases; abdominal pain, 72 cases; weight loss, 59 cases; anorexia, 57 cases; constipation, 29 cases; fever, 16 cases; and
3 bleeding, eight cases. Difficulty in chewing due to an intraoral tumor occurred in seven children with BL and in three patients with undifferentiated lymphoma of the non-burkitt s type (UNBL). Five patients presented with respiratory difficulty due to compression of the trachea by a mediastinal mass. Four patients presented with intussusception due to lymphomatous bowel involvement. Most of the patients had severe malnutrition. The sites of involvement at the time of diagnosis are summarized in Table 1. The abdomen was by far the commonest site of involvement. Other organs, such as liver, spleen, kidneys, bone marrow, peripheral lymph nodes, pleura, and testicles became involved as part of disseminated disease. The intra-abdominal tumor consisted of massively enlarged retroperitoneal or mesenteric lymph nodes or of heavily infiltrated bowel wall. Figure 4. The mediastinum was the primary site of involvement in 11 cases. Figure 5. Involvement of the facial bones occurred in seven patients with BL and three patients with UNBL. Solitary involvement of the long bones occurred in two patients. Figure 6. A 12-year-old boy with HL presented with a fungating mass in the right side of the neck. Figure 2. Map of Saudi Arabia showing the geographic distribution for Burkitťs (in brackets) and non-burkitťs lymphoma (the figure after the bracket).
4 Figure 3. Number of cases occurring each month among 100 children with NHL. Table 1. Sites of involvement in 100 children with NHL Site No. of cases Abdomen 79 Lymph nodes 19 Liver 17 Bone marrow 16 Bone 14 Kidneys 12 Mediastinum 11 Spleen 11 Pleura 9 Testes 5 Central nervous system 2 Spine 1
5 Figure 4. Lymphoma infiltrating the wall of the transverse colon in a five-year-old child. Figure 5. Mediastinal lymphoma in an 11-year-old boy.
6 Figure 6. Primary lymphoma in the ulna of a five-year-old boy. The diagnosis was confirmed by electron microscopy. Figure 7. A four-year-old girl with HL had multiple subcutaneous lymphomatous nodules, and thorough investigation failed to reveal other foci of involvement. The kidneys were massively enlarged in seven children with BL. Of these, six patients had acute renal failure at the time of diagnosis. Renal biopsies were done in three of these six patients, and an almost total replacement of parenchymal tissue with BL cells was demonstrated. Figure 7. Histiocytic lymphoma fungating through the skin of a 12-year-old boy. An 11-year-old girl presented with an abdominal mass and hepatosplenomegaly. Alpha heavy chain immunoglobulin was present in her blood and urine. The patient underwent splenectomy, liver biopsy, and resection of the involved bowel. Histology revealed Mediterranean lymphoma (immunoproliferative small bowel disease or IPSID) involving the spleen and liver. After treatment the alpha heavy chain globulin disappeared. A 12-year-old boy presented with an abdominal mass and paraplegia due to a spinal tumor. Biopsy results were diagnostic of BL. Laboratory Investigation Various degrees of bone marrow infiltration with lymphoma cells occurred in 16 patients. We differentiated these cases from leukemia on the basis that extramedullary disease was the predominant feature, lymphoblasts were
7 absent from the peripheral blood, the platelets, neutrophils, and hemoglobin were usually normal, and subsequent relapses occurred in extramedullary sites such as the abdomen, pleura, bones, and mediastinum. Anemia (hemoglobin <10 g/dl) occurred in 20 patients. The creatinine and blood urea nitrogen were elevated in six patients, all of whom had BL. Uric acid was elevated in 17 patients, seven of whom had BL. The transaminases were mildly elevated in 21 patients. Lymphoma cells were seen in the cerebrospinal fluid of two children at the time of diagnosis. Table 2. Results of radiographic body imaging evaluation Test No. of tests Normal Abnormal IVP Chest X-ray Ultrasound of abdomen Liver and splenic scan Bone scan CT brain scan Radiologic Features The result of various radiologic studies performed on these patients are summarized in Table 2. Sonography of the abdomen was the single most useful examination in children with intra-abdominal disease, as it demonstrated hypoechoic abdominal masses which represented enlarged lymph nodes or infiltrated bowel wall. Renal size could be measured in this way as well. Sonography was also useful in choosing a site for a Tru-Cut needle biopsy. The I VP was abnormal in 41 of 86 patients. The abnormalities consisted of deviated ureters or bladder and uniform renal enlargement with or without poor function. Chest radiography was useful in detecting mediastinal enlargement, pleural effusion or inflammatory pulmonary conditions. Liver and splenic scans revealed enlargement of these organs, areas of poor uptake due to tumor masses, or both. The bone scan was useful in detecting lesions in the long bones but was rather insensitive in demonstrating lesions of the facial bones, even in patients where the tumor was clinically evident. Presumably the tumor did not cause significant osteoblastic activity. Comments This study demonstrates that childhood NHL accounts for 17 percent of all childhood malignancies seen in this institution. This relative frequency is much higher than the 8 and 6 percent reported in American white and black children respectively, the 3.16 percent reported in the Manchester Tumour Registry, and the 5.6 percent reported from Japan On the other hand, it is smaller than the 54.8 percent reported from Africa. 11 During the study period ( ) the King Faisal Specialist Hospital and Research Centre in Riyadh served as the major referral center for the treatment of children with cancer. Governmental financial assistance to the families of these children made it possible for them to come from distant places as frequently as needed and to remain in Riyadh as long as necessary. Children who were seen initially elsewhere, including out-of-kingdom institutions, were eventually referred to us for continuation of investigations and therapy. Because of these factors, we believe that there was no significant bias in the referral pattern to our service. The high incidence of NHL among Saudi Arabian children is partly due to the presence of BL (17 percent in this series) in this country. Other possible factors such as genetic, environmental, socioeconomic or infection remain a matter of speculation. Further epidemiologic surveys are warranted to clarify their specific roles. A remarkable feature demonstrated in our patients was the great preponderance of the abdominal form of the lymphoma (79 percent). This incidence is much higher than the 30 to 40 percent reported in other series Parasitic intestinal infestation with subsequent chronic stimulation of the intestinal and mesenteric lymph nodes was proposed as a possible etiology. Nearly all of our patients had parasitic infestations, usually Giardia lamblia, but so did other children with other malignancies; therefore, this correlation was not significant. Another remarkable feature of our patients was their low median age. Sixty of the 100 children were under the age of five years at the time of diagnosis. Considering that, on the average, there was a period of four months between the onset of
8 symptoms and the time of diagnosis, it is reasonable to assume that disease occurred at a younger age. The mediastinal form of the disease showed a tendency to occur in older boys (eight to 13 years). A median age of five years for the onset of the disease in patients in our series is considerably lower than the mean age of eight to 12 years reported in American and Canadian children Another unusual feature seen in our patients was their delayed presentation here when advanced disease was clearly manifested. The majority of patients had disseminated disease, severe malnutrition, electrolyte imbalance, gastrointestinal disturbances, and infections. It is to be noted that in our series the diagnosis was based on material obtained by Tru-Cut needle in 30 cases and FNA of abdominal masses, pleural or peritoneal fluid in 22 cases. Ordinarily, a whole lymph node or a substantial piece of tissue is needed for the diagnosis and subtyping of lymphoma. In children, this issue is less critical because relatively few lymphoma types are seen and the differentiation among these types depends largely on the morphology of the individual cells. Our experience with Tru-Cut needle biopsy has already been published. 4 We have also employed light and electron microscopy to study material obtained by FNA from abdominal masses in our Hospital for over three years. Our experience indicates that this technique is adequate for the diagnosis and subtyping of NHL and other tumors. 16 This proved to be of great value in the management of malnourished children with advanced abdominal disease who are unfit for general anesthesia and surgery. One of the major sources of confusion in studying childhood NHL is the absence of an adequate classification system. This makes comparison among various series an impossible task. Nearly all patients in this series were studied by the same pediatric oncologist and the same team of pathologists. The modified Rappaport classification was adopted for all the patients in this series. Electron microscopy was of great value in differentiating the Burkitt s from the non-burkitt s forms and the lymphoblastic from the non-lymphoblastic types, especially in cases where only FNA was obtained. Again, our experience differs from what has been reported in the specialized literature, indicating that there was a great preponderance of the undifferentiated lymphoma of the Burkitt s and non-burkitt s types. Conclusion Our experience demonstrates that the relative frequency of childhood NHL is three to six times more common in Saudi Arabia than in the Western countries. The disease affects children at a younger age and with a marked initial predominance of the abdominal forms. REFERENCES 1. Davies JNP: The incidence and importance of malignant diseases in childhood. In: Deely TD, ed: Modern Radiotherapy and Oncology Malignant Diseases in Children. London, Butterworth & Co. Ltd 1974 p Burkitt D, O Conor GT: Malignant lymphoma in African children. I. A clinical syndrome. Cancer 14: Salem P (Director of Cancer Program, American University of Beirut): Personal communication Sabbah RS. Ghandour MH, Ali A, et al.: Tru-Cut needle biopsy of abdominal tumors in children. A safe and diagnostic procedure. Cancer 47(10): Byrne GE Jr: Rappaport classification of non-hodgkin's lymphoma: histologic features and clinical significance. Cancer Treat Rep 61 (6): Salem PA, Nasser VH, Shahid MJ, et al. : Mediterranean abdominal lymphoma or immunoproliferative small intestinal disease. Part I: clinical aspects. Cancer 40(6): Sabbah RS, Ali A, Lewall DB, et al. : Burkitťs lymphoma in Saudi Arabia: clinical, pathological, and epidemiological analyses of 16 cases. The King Faisal Specialist Hospital Medical Journal 2(2): Young JL Jr, Miller RW: Incidence of malignant tumors in US children. J Pediatr 8(2): Steward JK: Manchester children s tumour registry. In: Deely TJ, ed: Modern Radiotherapy and Oncology Malignant Diseases in Children. London, Butterworth & Co Ltd 1974 p Birch JM: The epidemiology of childhood tumors. In: Morris Jones PH, ed: Topics in Pediatrics, I Haematology and Oncology. Baltimore, Pitman Med 1978 p Williams AO: Tumors of childhood in Ibadan, Nigeria. Cancer 36(2): Wollner N, Burchenal JH, Lieberman O, et al. : Non-Hodgkin s lymphoma in children. A comparative study of two modalities of therapy. Cancer 37(1): Jenkin RDT: The management of malignant lymphomas in childhood. In: Deely TD, ed: Modern Radiotherapy and Oncology Malignant Diseases in Children. London, Butterworth & Co Ltd 1974 p Murphy SB, Frizzera G, Evans E: A study of childhood non-hodgkin s lymphoma. Cancer 36(6): Dehner LP: Non-Hodgkin s lymphomas and malignant histiocytosis in children. Semin Oncol 4(3): Akhtar M, Ali MA, Owen EW: Application of electron microscopy in the interpretation of fine-needle aspiration biopsies. Cancer 48(11):
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