Hepatitis A Virus Infection Associated with Hemophagocytic Syndrome: Report of TwoCases
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1 CASE REPORT Hepatitis A Virus Infection Associated with Hemophagocytic Syndrome: Report of TwoCases Masaaki Watanabe, Akitaka Shibuya, Junko Okuno, Tadanobu Maeda*, Shunpei Tamamaand Katsunori Saigenji Abstract Virus-associated hemophagocytic syndrome (VAHS) is reported to be a rare complication in hepatitis A virus infections. Weencountered two patients with hepatitis Avirus-associated hemophagocytic syndrome (HAV-AHS).Although hemophagocytosisassociated with other types of virus infections is fatal, the present patients with HAV-AHS recovered well without any treatment. Thrombocytopenia is an initial important finding ofvahswhich is not rare in patients with acute hepatitis A. If bone marrowaspiration is performed more frequently, more HAV-AHSwill be diagnosed. Further investigations are necessary to clarify the clinical features of HAV-AHSin more patients. (Internal Medicine 41: , 2002) Key words: thrombocytopenia, macrophage, bone marrow aspiration, cytokine disease Introduction Virus-associated hemophagocytic syndrome (VAHS)is a severe illness characterized by persistent fever, peripheral blood cytopenia, hyperferritinemia, high serum lactate dehydrogenase (LDH) level and hemophagocytosis. The main cause of VAHSis a herpes virus group infection, especially one by Epstein-Barr virus (EBV) (1). Other viruses, such as cytomegalovirus (CMV), dengue virus, herpes simplex virus, parvovirus B 19, adenovirus type 1 1, measles, coxsackie virus A9, rubella, influenza A, varicella zoster virus, and human immunodeficiency virus were also reported to cause VAHS(2). However, there are few reports in the literature about hepatitis A virus (HAV)-associated hemophagocytic syndrome (HAV- AHS). Recently, we encountered two patients with acute hepatitis A who had thrombocytopenia due to hemophagocytic syndrome (HPS). Thrombocytopenia is not a rare complication of hepatitis A virus infection; and HPSis one of the possible causes of thrombocytopenia in patients with acute hepatitis A. Case Reports Patient 1 A 45-year-old manwas admitted to Kitasato University East Hospital on May 1, 2001, because of headache, fatigue, and fever up to 39 C for 7 days. He had no history of serious illness, had not received a blood transfusion and had no habit of alcohol intake. Laboratory examination on admission showed high serum transaminase and LDH. Leukopenia and thrombocytopenia were also seen (Table 1). IgM class anti-hav antibody was positive. Serological markers for hepatitis B virus (HBV), hepatitis C virus (HCV), and EBVinfection were all negative. Serum ferritin and soluble interleukin-2 receptor (sil- 2R) levels were markedly elevated (Table 1). Bone marrow aspiration was performed in order to investigate the cause of cytopenia. It showed hemophagocytosis characterized by macrophages ingesting erythrocytes, platelets and nuclear cells (Fig. 1 ). The aspiration fluid was contaminated with peripheral blood and the ratio of phagocytic cell to nuclear cell count was 1.3%. Dysplastic cells werenot observed. Wemadea diagnosis of HAV-AHS.The general condition, biochemical data, and platelet and white blood cell counts improved on bed rest without treatment. After recovery from blood cytopenia, the second bone marrow aspiration was performed on the 28th hospital day, but revealed hemophagocytosis was not detected. The patient was discharged on the 30th hospital day (Fig. 2). Patient 2 A 41-year-old man with a past history of intravenous drug abuse was admitted to our hospital on October 3, 2001, because of fever and liver abnormality. He began to suffer fatigue, and a fever of up to 38.5 C persisted for 7 days. He has been positive for anti-hcv antibody for two years, but the serumtransaminase levels were within the normal range. Four months before admission, the serum HCV-RNAvalue was 1700 From the Department of Gastroenterology and *the Clinical Laboratory Branch, Kitasato University East Hospital, Sagamihara Received for publication May 1 3, 2002; Accepted for publication August 24, 2002 Reprint requests should be addressed to Dr. Masaaki Watanabe, the Department of Gastroenterology, Kitasato University East Hospital, Asamizodai, Sagamihara, Kanagawa
2 Hemophagocytosis in Acute Hepatitis A Table 1. Laboratory Data of the Two Patients on Admission Normal ranges and units Patient 1 Patient! Hematology White blood cell 4,000-9,000/ il 2,000 3,700 Red blood cell x1 04/ il Hemoglobin g/dl Platelets xlo4/ il Coagulation Prothrombin time >70% Active partial thromboplastin time >70% Hepaplastin test % Fibrinogen mg/dl D-dimer Fibrinogen <0 ig/ml degradation products < 1 0 ig/ml 1 0 Serum chemistry Total protein g/dl Albumin Total bilirubin g/dl mg/dl Direct bilirubin <0.4 mg/dl Asparatate aminotransferase TU/l 8,660 2,982 Alanine Lactate aminotransferase dehydrogenase ^80 TU/l IU// 6,210 15,600 2,661 2,882 Alkaline phosphatase IU// y-glutamyltransferase IU// Ferritin 5-80 ng/ml 1,298 5,800 Serology IgM anti-hav 2.1(+) 6.2(+) HBs Ag (-) (_) HCV Ab (-) (+) HCV-RNA <0.5 kcopies/ml 68 SIL-2R U/ml 4,870 2,590 kcopies/ml and the HCVgenotype was lb. On admission, laboratory examinations showed marked elevation of transaminases and LDH levels (Table 1). IgM class anti-hav antibody was positive and serological markers of HBV,EBV, or CMVwere all negative. Wemadea diagnosis of HAVsuperinfection in a healthy HCVcarrier. The peripheral platelets and white blood cell counts decreased to 7x104/ ll1 and 1,005/jil, respectively. The serum ferritin, and SIL-2R were markedly elevated (Table 1). Bone marrowaspiration showedseveral hemophagocytic cells (2.1% of a normal nuclear cell count of 8.3xlO4/ il). The serum HCV-RNAconcentration decreased to 68 kcopies/ml on admission, which fell below the detectable limit on the 12th hospital day. The liver function test and the peripheral blood cell count gradually improved without any special treatments being administered. After recovery from the HAVinfection, the serum HCV-RNAbecame positive again (Fig. 2). Discussion VAHSis defined as a secondary hemophagocytic syndrome (HPS) characterized by histiocytic proliferation with marked hemophagocytosis associated with active viral infection (3). VAHSis a fatal disease and frequently complicates multiple organ failure or disseminated intravascular coagulopathy (DIC). Its mortality rate is reported to be 20-40% (4, 5). Imashuku described the diagnostic criteria for secondary HPS as follows (2): persistent high fever (seven days or more with a peak temperature of 38.5 C or higher), peripheral blood cytopenia (affecting two or more of three lineages), hyperferritinemia, hyper- LDH-nemia,and hemophagocytosis in the bone marrow, spleen, or lymph nodes. In the present patients, all of these clinical and laboratory features were satisfied. A hemophagocytic cell ratio of over 2 or 3%of bone marrow nuclear cell count is regarded as HPSin diagnostic criteria (5-7), however, the ratio in patient 1 was 1.3%. This is probably due to peripheral Figure 1. A: Bone marrow aspiration of patient 1 showing hemophagocytosis of red blood cells, nucleated red cells, and platelets (May-Giemsa stain, x600). B: In the same patient, proliferation of hemophagocytic cells (arrows) could be found. (May-Giemsa stain, x200). 1189
3 Watanabe et al T.bil ALT Admission pit (mg/dl) (IU//) I 1st bone marrow aspiration (xiovao 7 7,000r+4 1 ^ Z ^^» 'p^ji 2nd bone marrow aspiration 6 6,000 *M Jr*"*"*'* \. i ,000 )/* «ft: M\ /\ * 4 4,000 / \ / -V ,000 wfr~jr ^"y^ ^^^_,0 ~~^^^~ 2,000 pyr \ A10 1 1,000»^^ N» -r^ 2001 May 1 May 6 May ll May 16 May 21 May 26 B T.bil ALT Admission ^ plt (mg/dl) (IU//) Bone marrow aspiration ( X 10V//1) 3, j30 ik^^s^alt ^J* a 10 2,500 f 5S- W -X- 8 2,000 \C \ II * ^-^^, ,500 \i >V^^ \ «S/\ \Tbil 4 1,000 W^ \ \ Jan. 9 Oct. 3 Oct. 9 Oct. 18 Nov. 1 Dec. 3 HCV-RNA g50 170Q 6g L1 <Q5 <05 <05 5Q0 660 (kcopies/ml) Figure 2. A: Clinical course of the patient 1. B: Clinical course of the patient 2. (pit: platelets, ALT: alanine aminotransferase, T.bil: total bilirubin). blood contamination in the bone marrow aspiration fluid. When it is unexpectedly difficult to prove the presence of hemophagocytic cells in the bone marrow, the lymph node or spleen biopsy or several bone marrowaspirations are recommended (7). Unfortunately, the second bone marrow aspiration after recovery in patient 1 revealed no hemophagocytosis. Manyviruses have been reported to cause VAHS,but to our knowledge, there are only nine case reports, including the two presented herein, regarding HAV-AHS (Table 2) (4, 8-1 3). Two of the nine patients (22.2%) died of DIC or multiple organ failure, but four (44.4%) recovered without any treatment. It is important to clarify the risk factors associated with the prognosis of HAV-AHSbut the clinical features of HAV-AHSare not well known. In the present study, a superinfection of HAV on the HCVcarrier and a high serum level of SIL-2R were observed. 1190
4 Hemophagocytosis in Acute Hepatitis A Table 2. Case Reports of HAVAssociated Hemophagocytic Syndrome rhg-csf*: recombinant human granulocyte colony stimulating factor, HDF**: hemodiafiltration, combination chemotherapy* * * : cyclophosphamide+vincristine+prednisolone. HAVsuperinfection in patients with chronic HCVinfection maymakethe clinical findings more severe and complex (14). In the present patient 2, it is interesting that the serum HCV- RNAlevel fell below the detectable limit after the onset of HAV-AHSand increased again after recovery from HAVinfection. This suggests that HAVinfection suppresses the activity of HCV.The association between the superinfection and VAHSis not clarified but another HAV-AHSpatient with chronic HCVinfection has also been reported (case 4 in Table 2)(ll). A high serum level of SIL-2R was observed in the present patients. Authors of recent studies regard hemophagocyticsyndrome as a cytokine disease (2, 5). Various cytokines such as IFN-y, TNF-a, IL-2, and IL-6 following T-cell and macrophage activation may play an important role in the pathogenetic mechanismof this syndrome. Hypercytokinemia induces phagocytosis and the suppression of hematopoiesis (5). Imashuku et al proposed the serum concentration of SIL-2R as a prognostic marker for hemophagocytic syndrome (15); thus, a poor prognosis for patients with high serum concentrations of SIL-2R was reported. But it does not apply to the present patients. Although our patients showed higher serum levels of SIL-2R compared with the previously reported patients with HAV-AHS(Table 2), our patients recovered well without any special treatment. Thrombocytopenia is an initial important finding of VAHS which is not rare in patients with acute hepatitis A. The mechanisms of thrombocytopenia have been reported to be aplastic anemia, idiopathic thrombocytopenic purpura or the presence of circulating immune complex ( 1 6). Another important mechanism of thrombocytopenia is DIC. It was reported that hypercytokinemia in hemophagocytic syndrome may also induce DIC (5). In an animal model, DICmay cause sinusoidal microcirculation failure indicating massive and severe hepatocyte necrosis (17). A subclinical DIC cannot be ruled out in the present patients but the clinical features and laboratory findings did not support an overt DIC. No standard specific therapy for VAHShas yet been established. In keeping with the proposed pathogenetic mechanism, a T-cell suppressive agent maybe considered. In fact, some successful treatments of VAHSusing high-dose corticosteroid therapy have been documented (2, 4, 5, 1 3). Carcinostatic agents such as vincristine (VCR), etoposide (VP- 16), and cyclosporine A (CPA) were also administered with corticosteroid. Plasma exchange and hemodiafiltration maybe useful for eliminating cytokines. But as demonstrated in this report, some patients with HAV-AHShave recovered well without any treatment for hypercytokinemi a. As this report indicates, VAHSis a possible mechanismof thrombocytopenia in patients with acute hepatitis A. If bone marrow aspiration is performed more frequently in patients with HAVinfection whoshowsigns of thrombocytopenia, more HAV-AHSwill be diagnosed. Further investigations are necessary to clarify the clinical features of HAV-AHS. References 1) Sullivan JL, Woda BA, Herrod HG, Koh G, Rivara FP, Mulder C. Epstein- Barr virus-associated hemophagocytic syndrome: virological and immunopathological studies. Blood 65: , ) Imashuku S. Differential diagnosis of hemophagocytic syndrome: underlying disorders and selection of the most effective treatment. Int J Hematol 66: , ) Risdall RJ, McKenna RW, Nesbit ME, et al. Virus-associated hemophagocytic syndrome: a benign histiocytic proliferation distinct from malignant histiocytosis. Cancer 44: , ) Onaga M, Hayashi K, Nishimagi T, et al. A cause of acute hepatitis A with marked hemophagocytosis in bone marrow. Hepatol Res 17: , ) Tsuda H. Hemophagocytic syndrome (HPS) in children and adults. Int J Hematol 65: , ) Imashuku S. The clinic of histiocytosis. Nihon Iji Shinpo (Jpn Med J) 3650: 27-34, 1994 (in Japanese). 7) Henter JI, Elinder G, Ost A, et al. Diagnostic guidelines for hemophagocytic lymphohistiocytosis. The FHL Study Group of the Histiocyte Society. Semin Oncol 18: 29-33, ) Kishimoto N, Shirai T, Koake E, Ohno J, Tsuji M. A case of hemophago- 1191
5 Watanabe et al cytic syndromeregarded as associating with hepatitis A. Nihon Naika Gakkai Zasshi (J Jpn Soc Intern Med) 77: 1299, 1988 (in Japanese). 9) McPeake JR, Hirst WJR, Brind AM, Williams R. Hepatitis A causing a second episode of virus-associated haemophagocytic lymphohistiocytosis in a patient with Still's disease. J Med Virol 39: , ) Kondo H, Date Y. Effects of simultaneous rhg-csf and methylprednisolone pulse therapy on hepatitis A virus-associated haemophagocytic syndrome [letter]. Eur J Haematol 54: , ll) Wu CS, Chang KY, Dunn P, Lo TH. Acute hepatitis A with coexistent hepatitis C virus infection presenting as a virus-associated hemophagocytic syndrome: a case report [see comments]. AmJ Gastroenterol 90: , ) Kyoda K, Nakamura S, Machi T, Kitagawa S, Ohtake S, Matsuda T. Acute hepatitis A virus infection-associated hemophagocytic syndrome [letter; comment]. Am J Gastroenterol 93: , ) Yamagishi Y, Katho S, Matsunaga S, et al. A case offulminant hepatitis A with hemophagocytic syndrome (HPS). Kanzo (Acta Hepatol JPN) 41: , 2000 (in Japanese). 14) Vento S, Garofano T, Renzini C, et al. Fulminant hepatitis associated with hepatitis A virus superinfection in patients with chronic hepatitis C. N Engl J Med 338: , ) Imashuku S, Hibi S, Sako M, et al. Soluble interleukin-2 receptor: a useful prognostic factor for patients with hemophagocytic lymphohistiocytosis [letter]. Blood 86: , ) Mashiko N. Study about thrombocytopenia associated with hepatitis A. Kanzo (Acta Hepatol Jpn) 29: , 1988 (in Japanese). 17) Mochida S, Fujiwara K. Symposiumon clinical aspects in hepatitis virus infection. 2. Recent advances in acute and fulminant hepatitis in Japan. Intern Med 40: ,
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