... Experience with Surgery for Thymoma Associated with Pure Red Blood Cell Aplasia* Report of Three Cases
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1 Experience with Surgery for Thymoma Associated with Pure Red Blood Cell Aplasia* Report of Three Cases Shigefumi Fujimura. M.D. F.C.C.P.; Takashi Kondo. M.D.; Atsushi Yamauchi. M.D.; Masashi Handa. M.D.; and Tasuku Nakada. M.D. F.C.C.P. We present three cases of thymoma associated with pure red blood ceo aplasia in which thymomectomy and thymectomy were performed. Case 1, a patient with pure red blood ceo aplasia and hypogammaglobulinemia, was treated after surgery with immunosuppressive agents. She did not show any remission and died eight months after the operation. Case 2, a patient with pure red blood ceu aplasia alone, showed transient erythropoiesis only in the early postoperative period and died one year and seven months after the operation. Patient 3 had pure red blood ceo aplasia alone before surgery and was treated after surgery with prednisolone and 8uoxymesterone. He showed good remission from the aplasia after these treatments; however, myasthenia gravis appeared seven months after the operation. These results seem to show that such combined therapy as applied in case 3 may be effective for some of the patients with pure red blood ceo aplasia and thymoma; however, the elfects of thymomectomy or thymectomy (or both) are still Controversial for the treatment of pure red blood ceo aplasia. Thymoma often is associated with various autoimmune diseases during its natural history. 1 Among them, myasthenia gravis has been proven to be caused by circulating antibody to the acetylcholine receptoi; and the protocol fur treatment is being established; however, the causes of other diseases associated with thymoma. such as pure red blood cell aplasia and hypogammaglobulinemia, are not known nor are their effective treatments. Recently, we had experience with three patients *From the Department of Surgery, the Research Institute fur Chest Diseases and Cancer, Tohoku UniverSity, Sendai, J ~. Supported in part by Japan WelfBre Ministry Board (58-32). Manuscript received Aprll15, 1984; revision accepted January 17. Reprint requests: Dr. Fujimura, Katahiro, Sendal 980, Japan who underwent surgery fur thymoma associated with pure red blood cell aplasia. These cases are presented in order to look fur an effective treatment fur pure red blood cell aplasia with thymoma from a surgical point of view. CASE! CASE REPORTS A y e woman a N ~ lhad d a tumorous shadow of the right mediastinum on a che5t x-ray film at euminatiqn of a mass in Since the winter of1974, she had frequently developed fever and productive cough, and each time, she received antibiotics. 1n 1978, she was hospitalized with pneumonia fur 40 days. 1n August 1978, the patient was readmitted with tonsillitis and pneumonia fur two months. From June 191:10, she noticed vertigo together with breathlessness; she was admitted to Tohoku Univenity Medical Center, where she was 1 FIGURE 1. Preoperative roentgenograms of patients with thymomas associated with pure red blood cell aplasia. Left, Case 1; center, case 2; and right, case CHEST I 88 I 2 I AUGUST,
2 Table l.;_ruulta of Preoperative E:raminatioftl of Peripheral Blood and Bone Marrow Data Case1 Case2 Case3 Peripheral blood RBC, X 10'/J.Ll Hemoglobin, wdl Reticulocytes, percent Platelets, x 10'/J.Ll WBC, /J.Ll 8,400 5,500 11,400 Bone marrow Nucleated cells, x 10'/J.Ll Megakaryocytes, /J.Ll Erythroblasts, percent Myeloblasts, percent Neutrophils, percent Promyelocytes Myelocytes Metamyelocytes Band Segmented Basophils, percent Eosinophils, percent Monocytes, percent Lymphocytes, perceni Plasma cells, percent Others, percent RBC, Red blood cell count; and WBC, white blood cell count. diagnosed as having thymoma, pure red blood cell aplasia and hypogammaglobulinemia. The patient was transferred to our department fur surgical treabnent on Jan 19, Since February 1978, she had had stomatitis. On examination, the patient had a trichophytosis on the nails and hepatosplenomegaly. A chest x-ray film revealed a tumorous mass on the right side behind the sternum (Fig 1). The results of hematologic examinations in the three patients are summarized in Table 1. In patient 1, there was severe anemia without any reticulocytes in the peripheral blood, and there were no erythroblasts, with relative lymphocytosis, but there was some decrease in nucleated cells, and plasma cells in the bone marrow tended to disappear. Biochemical and immunologic investigations of peripheral blood showed an apparent decrease in the serum -y-globulin level, as well as in serum immunoglobulins. B-lymphocyte composition was also decreased ('Th.ble 2). The results of other examinations were reported as decreased lymphocyte blastogenesis to pokeweed mitogen (PWM) and inactive skin tests to purified protein derivative of tuberculin (PPD) and dinitrochlorobenzene. The patient underwent thymomectomy and thymectomy on Feb 10, The tumorous mass was well encapsulated. The specimen measured 9.8 by 12.1 by 8. 7 em. On cut section, there was a smooth parenchymal surface with soft portions slightly separated by fibrous septa (Fig 2). Histologically, the specimen predominantly contained epithelial cells with spindle-shaped nuclei. Lymphocytes were relatively scant (Fig 3). This spindle-cell thymoma showed no malignant nature histologically. After surgery the patient was given immunosuppressive agents such as prednisolone, ACTH, and azathioprine. The patient suddenly died eight months after the operation without any improvement in the hematologic findings. At autopsy the bone marrow had no erythroblasts, and abundant fat. There was diffuse hemosiderosis in the liver, spleen, pancreas, and thyroid gland. Brown atrophy of the myocardium was also remarkable. CASE2 222 A 63-year-old man developed weakness and slight breathlessness Table 2-Ruulta of Preoperative Immunologic E:raminations Data* Case 1 Case2 Case3 TP. wdl Albumin, percent a 1 -globulin, percent ~ I t - g l o b u l i n, percent globulin, percent y-globulin, percent Albumin-globulin ratio IgG, mwdl 660 1, lga, mwdl lgm, mwdl Serum complement, CHSOU/ml Coombs' test, direct/indirect -I- -I- Antinuclear antibodies ( X ) ESR, mmlhr C-reactive protein (2") Lymphocytes Count, /J.Ll 6,432 1,722 2,508 T, percent B, percent OKT-3, percent 85.0 OKT-4, percent 43.2 OKT-8, percent 38.2 OKial, percent 12.8 TP, total protein; and ESR, erythrocytic sedimentation rate. in the spring o An abnormal shadow on the chest x-ray film and anemia were noted in September The patient was transferred to our department via Tohoku University Medical Center with a diagnosis of thymoma and pure red blood cell aplasia on Jan 5, Neither the liver nor the spleen was palpable. The chest x-ray film revealed a tumorous mass on the right mediastinal side near the anterior chest wall (Fig 1). A blood cell count showed the erythrocytes to number 304 X 10'/J.Ll and no reticulocytes (Table 1). On examination, bone marrow revealed no erythroblasts and a decrease in nucleated cells and plasma cell component. Other examinations showed a decrease in surface immunoglobulin-positive lymphocyte levels to 0.2 percent (control, 7.6 percent). Cutaneous reactivity to PPD was normal. The patient underwent thymomectomy and thymectomy on Jan 26, The tumor was well encapsulated. The specimen measured 3.8 by 7.6 by 4.2 em. On cut section, it had a parenchymal surface with soft portions grossly separated by thin fibrous septa (Fig 2). Histologically, epithelial cells had spindle-shaped nuclei with scant lymphocyte migration (Fig 4). There were no malignant patterns in these specimens. The patient received no immunosuppressive therapy after surgery but showed temporary remission in bone marrow findings; the erythroblast level was increased up to 13.2 percent at one month after surgery; however, a decrease in this level began to be progressive thereafter. Finally, the patient died of cerebral softening one year and seven months after surgery. Autopsy was not performed. CASE3 A 58-yeaM>ld man had a history of pneumonia in childhood. Old right-sided pleuritis had been noted roentgenologically fur ten years. The patient presented with loss of appetite and faintness in August 1983, and anemia associated with an abnormal shadow on chest x-ray film was noted. He was admitted into our department on Sept 8, Chest roentgenographic examination revealed a large tumorous lor Thymoma (Fujlmura et Ill) S u r g e ~ y
3 1 2 FIGURE 4. Thymoma showing densely packed spindle-shaped epithelial cells with scant lymphocytes (case 2) (hematoxylin-eosin, original magnification x 100). shadow on the left side behind the anterior chest wall, with old pleuritis on the left (Fig 1). Investigations ofperipheral blood showed anemia without any reticulocytes (Table 1). There were no erythroblasts but normal findings of granulopoiesis in bone marrow. Biochemical and immunologic examinations showed normal levels of -y-globulins and each kind of immunoglobulin ('lahle 2). The indirect Coombs' test was positive. There was a relative decrease in the 8- lymphocyte level, but lymphocyte subsets measured by monoclonal anti-t-cell antibodies were within the normal range. The patient underwent thymomectomy and thymectomy on Nov 17, The tumor had a thickened capsule but seemed to be invasive to the left upper lobe and pericardium; thus, its surgical category was invasive thymoma. The excised specimen measured 8.4 by ll.9 by 7.3 em and was well encapsulated (Fig 2). Histologically, there were two dominant areas in the specimen; a dark area had collections of lymphocytes, and another light portion had an epithelial dominant pattern with scant lymphocytes. Many epithelial cells had spindle-shaped nuclei (Fig 5). Histologically, there was no tumor cell invasion into the capsule. After surgery the patient showed rapid improvement in the hematologic findings; peripheral reticulocyte levels were going up to 8 percent and 78 percent on the 12th and 19th postoperative days, respectively; however, this level decreased to 24 percent five weeks after the operation. Bone marrow showed 9.6 percent erythroblasts at this period. The patient was discharged five weeks after the operation, but was readmitted to our hospital three weeks later, because of progressive breathlessness. On readmission the reticulocyte level was zero, and the red blood cell count was 204 x 10'/f.l.l in the peripheral blood. After readmission, in order to suppress a presumed autoimmune mechanism in the pure red blood cell aplasia and to stimulate bone marrow erythropoiesis simultaneously, we started therapy with FIGURE 3. Thymoma showing densely packed spindle-shaped epithelial cells with lymphocytes (case I) (hematoxylin-eosin, original magnification x 100). FIGURE 5. Thymoma showing two separate areas, one with abundant lymphocytes and another with scant lymphocytes. Epithelial cells are spindle-shaped (case 3) (hematoxylin-eosin, original magnification XlOO). 3 FIGURE 2. Gross features of external and cut surface of thymoma removed from case 1 (top), case 2 (middle) and case 3 (bottom). CHEST I 88 I 2 I AUGUST,
4 prednisolone in combination with ftuoxymesterone (Halotestin). Soon after these treatments began, the patient showed remarkable improwment in the anemic symptoms; the peripheral reticulocyte level became 59 percent, and the bone marrow erythroblast level reached 28.2 percent after one month of the treatmenl The patient was discharged from the hospital after 14 weeks, when his reticulocyte level in the peripheral blood was <J:1 percent and the bone marrow erythroblast level was 24.6 percent. Continued observations of peripheral blood and bone marrow blood have remained improwd; however, seven months after the operation, the patient showed symptoms of myasthenia gravis with a serum anti-acetylcholine receptor antibody level of 5.8 pmoles/ml (normal range, o-0.3 pmoleslml). During the past lour months since the myasthenia gravis appeared, the antibody level has decreased to 3.8 pmoles/ml. The continued treatment so far has consisted of prednisolone (20 mg every other day) and fluoxymesterone (Halotestin; 30 mg daily). DISCUSSION Abnormalities of the thymus, including thymoma, have been associated with various immunologic abnormalities, and are regarded as autoimmune diseases. 1 It has been known that approximately 5 percent of thymomas are associated with pure red blood cell aplasia, and 50 percent of the cases of such aplasia are associated with thymoma. u Pure red blood cell aplasia is presumably related to an autoimmune mechanism. The disease is known to be associated with other autoimmune diseases, such as myasthenia gravis, systemic lupus erythematosus, and pemphigus fuliaceus; the disease is also known to show immunologic abnormalities which are found in autoimmune diseases. 3 4 Krantz and.kao 11 have found that IgG of the serum from a patient with pure red blood cell aplasia is cytotoxic to erythroblasts under complement interaction; however, it is not commonly possible to detect circulating antibody against erythroblasts routinely so far. On the contrary, it is well known that in the case of myasthenia gravis, the patient frequently has a circulating antibody (anti-acetylcholine receptor antibody) which seems to be widely possible to detect in many institutions. Thus, these situations in pure red blood cell aplasia have made it difficult to establish an exact protocol fur treatment of this disease. For the patient who concomitantly has thymoma and pure red blood cell aplasia, treatment should be scheduled fur the thymoma itself and fur the aplasia. Of all the treatments fur thymoma, it is clear that surgery is the first choice. On the contrary, fur patients with pure red blood cell aplasia, surgery has not been widely accepted as the first choice in therapy; however, as it is strongly suggested that the disease has the same etiology as myasthenia gravis, thymomectomy or thymectomy (or both) might be considered to be effective fur pure red blood cell aplasia. This aplasia is a progressive disease.u 7 Hirst and Robertson 6 reported that in approximately 15 percent of the patients with pure red blood cell aplasia, the levels of other elements, including serum globulins, were later de- pressed. The three cases in the present study showed some interesting results. The first patient, who had thymoma, pure red blood cell aplasia, and hypogammaglobulinemia, died eight months after surgery without any remission from the hematologic findings and symptoms of immunodeficiency. There has been no evidence that hypogammaglobulinemia is caused by an autoimmune mechanism. Rather, a recent report suggests that this abnormality is induced by thymoma itself. 8 There have been no reports showing that thymomectomy is effective fur hypogammaglobulinemia. Surgery fur those patients who have pure red blood cell aplasia with severe immunodeficiency s ~ eto mhave s no efficacy fur the marrow depression. The second case with thymoma and pure red blood cell aplasia showed temporary improvement in the aplasia soon after the operation, but the patient died one year and seven months after surgery. The transient improvement following surgery in this patient may well be related to the surgical stress response and an increase in circulating endogenous corticosteroids. The third patient, who had thymoma and pure red blood cell aplasia, showed rapid improvement from the aplasia soon after surgery without any other therapy, which can be explained in the same manner as case 2. Symptoms in patient 3 became worse again, but therapy with prednisolone and fluoxymesterone induced remission fur more than seven months. It is difficult to explain whether the male hormone has a role in remission from pure red blood cell aplasia, but, rather, it is clear that prednisolone was effective against pure red blood cell aplasia in case 3. In this case an appearance of myasthenia gravis during the course of treatment fur pure red blood cell aplasia suggests that the etiology of the aplasia had an autoimmune origin and might have been influenced by the corticosteroid therapy. To summarize the results of our experience with surgery fur thymoma associated with pure red blood cell aplasia, controversy remains about the efficacy of surgery fur these situations; however, it may be effective in some cases of pure red blood cell aplasia to treat with prednisolone after surgery. Until the precise mechanism of pure red blood cell aplasia can be revealed, one can regard corticosteroid therapy following surgery as one of the best treatments required in patients with thymoma. REFERENCES 1 Rosai J, Levine GD. Thmors of the thymus. Washington, DC: Armed Forces Institute of Pathology, Henry K, Farrer-Brown G. A colour atlas of thymus and lymph node: histopathology with ultrastructure. Weert, The Netherlands: Wolfe Medical Publications, 1981: Mackechnie HLN, Squires AH, Platts M, Pruzanski W. Thy- 224
5 moma, myasthenia gravis, erythroblastopenic anemia and systemic lupus erythematosus in one patient. Can Med Assoc J 1973; 109: Cooper A, Wells JV. Pemphigus fuliaceus, myasthenia gravis, and thymoma in a patient with serological evidence ofsle. Aust NZ J Med 1981; 11: Krantz SB, Kao V. Studies on red cell aplasia: 1. demonstration of a plasma inhibitor to heme synthesis and an antibody to erythroblast nuclei. Proc Natl Acad Sci USA 1967; 58: Hirst E, Robertson TI. The syndrome of thymoma and erythroblastopenic anemia: a review of 56 cases including three case reports. Medicine 1967; 46: Rogers BH, Manaligod JR, Blazek WV. Thymoma associated with pancytopenia and hypogammaglobulinemia: report of a case and review of the literature. Am J Med 1968; 44: Hayward AR, Paolucci P, Webster ADB, Kohler P. Pre-8 cell suppression by thymoma patient lymphocytes. Clin Exp Immunol 1982; 48: Heart and Mind: Neurocardlology Update The University of Kansas Medical Center will present this one-day program on September 7 at the Hyatt Regency Hotel, Kansas City, Missouri. For information, contact Ms. Jan Johnston, Office of Continuing Education, University of Kansas Medical Center, 39th and Rainbow Blvd, Kansas City, KS (913: ). Pulmonary and TB Update The St. Paul-Ramsey Medical Center, will present this course at the Radisson Plaza Hotel, St. Paul, September For information, contact: Continuing Medical Education, St. Paul Ramsey Medical Center, 640 Jackson Street, St. Paul (612: ). CHEST I 88 I 2 I AUGUST,
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