KIKUCHI-FUJIMOTO DISEASE: A CASE REPORT
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1 KIKUCHI-FUJIMOTO DISEASE: A CASE REPORT Chih-Hung Lee and Shih-Tsung Cheng Department of Dermatology, Kaohsiung Medical University, Kaohsiung, Taiwan. We describe a rare but typical case of Kikuchi-Fujimoto disease (KFD). Two subcutaneous nodules appeared suddenly on the right of the neck of a 15-year-old girl. Microscopy of a surgical specimen of the larger nodule showed necrotizing lymphadenitis. Prompt treatment with mepirizole resulted in the disappearance of the smaller nodule. No recurrence was noted during 6 months of follow-up. KFD is a rare, self-limiting, necrotizing histiocytic lymphadenitis that needs to be differentiated from malignant lymphoma. Any nodal biopsy showing fragmented nuclei, necrosis, and karyorrhexis without prominent neutrophils should alert the physician to consideration of KFD, especially in a young woman presenting with cervical lymphadenopathy. Key Words: Kikuchi-Fujimoto disease, necrotizing histiocytic lymphadenitis (Kaohsiung J Med Sci 2003;19:246 51) Kikuchi-Fujimoto disease (KFD), also called histiocytic necrotizing lymphadenitis, was first recognized by both Kikuchi [1] and Fujimoto et al [2] in It is a self-limiting, rare, necrotizing form of lymphadenitis that most commonly affects young women. The pathogenesis is still poorly understood but is thought to include a hyperimmune reaction induced by different antigenic stimuli or an autoimmune-mediated process in which apoptosis plays a major role. The most frequent clinical manifestations are fever and painless cervical lymphadenitis. Menasce et al documented 25 cases and found the age of patients ranged from 13 to 47 years (mean, 29 years) [3]. There was a predominance of female patients. Received: January 3, 2003 Accepted: March 4, 2003 Address correspondence and reprint requests to: Dr. Shih- Tsung Cheng, Department of Dermatology, Kaohsiung Medical University, 100 Shih-Chuan 1 st Road, Kaohsiung 807, Taiwan. keithche@ms13.hinet.net 246 CASE PRESENTATION A 15-year-old girl came to our dermatology clinic because of the appearance of two subcutaneous nodules along the belly of the right sternoclavicomastoid muscle; they had been enlarging for the previous 2 weeks (Figure 1). The larger nodule measured 1.5 x 1.5 cm and the smaller one measured 1.3 x 1.2 cm. They were both firm in consistency and moved freely with mild tenderness. There was no fever or any other constitutional symptoms, nor were epistaxis, nasal obstruction, blood-tinged sputum, odynophagia, or hoarseness noted. Physical examination, including complete dermatologic inspection, showed no other remarkable findings. The tentative diagnosis was lymphadenitis of the neck. The larger nodule was completely removed. On deep dissection to the fascia, the nodule appeared to be a well circumscribed, faintly bluish, round subfascial tumor. Under microscopy, hypercellular areas alternating with hypocellular areas showed that it was a necrotizing lymph node. A few germinal centers and areas of hemorrhage were noted (Figure 2A). There were fragmented nuclei, many histiocytes, and necrosis without prominent neutrophils in the hypocellular area (Figure 2B). Sheets of lymphoid cells and histiocytes were present in the 2003 Elsevier. All rights reserved.
2 Kikuchi-Fujimoto disease Figure 1. Two tender and indurated subcutaneous nodules on the right of the neck. The bigger nodule was removed completely by surgery. After 1 week of mepirizole therapy, the smaller nodule (arrow) disappeared in 1 month. hypercellular area (Figure 2C). There were red blood cell extravasations with clusters of lymphoid cells and histiocytes in the areas of hemorrhage (Figure 2D). The pathologic diagnosis was histiocytic necrotizing lymphadenitis, or KFD. The patient was then admitted for general survey. There was adenoid formation in the nasopharyngeal area with no other remarkable abnormalities in the ear-nose-throat field. Neither premature hematopoietic cells nor atypical monocytes appeared in peripheral blood. The complete hemogram and routine blood biochemistry were within normal limits. Test for antinuclear antibody (ANA) was negative. Serum C-reactive protein was mildly elevated (3.67 μg/ml, normal < 0.06 μg/ml). The serum titer of antistreptolysin O was not elevated (31.4 IU/mL, normal < 125 IU/mL). Serum levels of immunoglobulin M (IgM) antibody to herpes simplex virus 1 (HSV-1), herpes simplex virus 2 (HSV-2), varicella- C A B D Figure 2. (A) Gross view of the node shows hypercellular areas alternating with hypocellular areas. A few germinal centers and hemorrhage are evident. (B) Fragmented nuclei, many histiocytes, and necrosis without prominent neutrophils are evident in the hypocellular areas (x 400, H & E). (C) Sheets of lymphoid cells and histiocytes are present in the hypercellular areas (x 400, H & E). (D) Red blood cell extravasation with clusters of lymphoid cells and histiocytes in areas of hemorrhage (x 400, H & E). H & E = Hematoxylin and eosin. 247
3 zoster virus (VZV), and viral capsid antigen (IgM anti- VCA) of Epstein-Barr virus (EBV) were not elevated. Although the titer of IgG anti-vca was elevated initially (1:16), there was no further increase after 4 weeks (1:16). Polymerase chain reaction (PCR) for parvovirus B19 DNA in blood was negative. Gynecologic ultrasonography showed no gross lesion. There was normal increased activity in the growth plate on bone scan. No active cardiopulmonary disease was demonstrated on chest roentgenography and there were no space-occupying lesions on abdominal ultrasonography. Tumor markers, including alphafetoprotein, CA-125, CA-19-9, tissue polypeptide antigen, and squamous cell carcinoma antigen, were all within normal limits. The final diagnosis was KFD, with pure nodal involvement without skin manifestation. Prompt treatment with mepirizole (Mebron, Daiichi company, Taipei, Taiwan) for 1 week decreased the size of the smaller nodule. Complete disappearance of the nodule took 1 month. No recurrence occurred during 6 months of follow-up. DISCUSSION 248 KFD was first described in 1972 by Kikuchi [1] and Fujimoto et al [2] as lymphadenitis with focal proliferation of reticular cells accompanied by nuclear debris and numerous phagocytes. It is a benign, selflimiting condition that more commonly affects females (male to female ratio, 1:4) under the age of 30 years (mean, 29 years) [3]. The most common clinical manifestation is cervical lymphadenopathy with or without fever. Sore throat, weight loss, sweating, chills, myalgia, arthralgia, splenomegaly, and skin rash may accompany the lymphadenopathy. Laboratory findings may include leukopenia, and elevated serum transaminase and serum lactate dehydrogenase (LDH) [4,5]. The course is benign and is followed by complete recovery within 1 to 3 months in almost all cases. Recurrences may occur but are infrequent, and fatalities are exceptional [4,6 8]. The typical nodal KFD lesion is paracortical and composed of patchy zones of eosinophilic fibrinoid necrosis with nuclear dust surrounded by a mixed lymphohistiocytic infiltrate composed of debris-laden macrophages, foamy histiocytes, immunoblasts, and atypical mononuclear cells with irregular twisted nuclei [4]. Additional important histologic findings include the absence of granulocytes, granuloma and multinucleated giant cells, the rarity of plasma cells, and the presence of clusters of unusual plasmacytoid monocytes [4,9]. Immunohistochemical studies indicate that these lesions are composed primarily of CD15+ histiocytes, early-stage CD4+ T cells, and late-stage CD8+ T cells, with relatively few B cells and natural killer cells [4,10,11]. Kuo classified the morphologic changes of KFD into three histologic subtypes proliferative, necrotizing, and xanthomatous according to the absence or presence of coagulative necrosis and predominance of foamy histiocytes [12]. The pathogenesis of KFD is poorly understood. The clinical manifestation of fever, chills, lymphadenitis, rash, arthralgia, and myalgia in young women is certainly suggestive of an infectious or autoimmune disease. Imamura et al first suggested that KFD might be a lupus-like autoimmune disease triggered by viral infection [13]. In fact, it may be difficult to distinguish the histologic features of KFD in some cases from those of systemic lupus erythematosus (SLE) [4,14]. Given the similarities of KFD lymphadenitis with lupus lymphadenitis, KFD-like lymphadenitis in SLE or other autoimmune diseases may simply represent an abnormal autoimmune reaction [15]. Although SLE is more prevalent in young females, in this case, there was no malar rash, discoid rash, or oral ulcer suggestive of SLE, and a test for ANA was negative. Another possible cause of KFD is infection. Some viral infections have been proposed as etiologic factors in KFD. Arguably, the most commonly detected infectious agent in KFD is EBV. A study conducted by Chiu et al in Taiwan to detect viral DNA, RNA, and proteins in surgical lymph node specimens revealed EBV-encoded RNA by in situ hybridization in all 10 cases, EBV-DNA by PCR in nine cases, and EBVencoded protein by immunohistochemistry in only one case [16]. Neither human T cell leukemia virus-1 nor parvovirus B19 were detected. The fact that many patients with KFD have elevated antibody titer to EBV argues for the involvement of EBV in the pathogenesis of KFD [16]. However, Hollingsworth et al [17] and Anagnostopoulos et al [18] argued against EBV as the causative agent because it is commonly detected in reactive lymphoid tissue. Although EBV DNA, RNA, and proteins in lymph nodes were not examined, negative IgM-VCA and no later seroconversion of IgG-
4 Kikuchi-Fujimoto disease VCA did not support EBV involvement in the etiology of KFD in this case. Normal levels of serum IgM antibody to HSV-1, HSV-2, and VZV indicated that these viruses did not contribute to KFD in this case. Nor could we demonstrate positive parvovirus B19 DNA in blood by PCR. In KFD specimens, human herpes virus-6 (HHV-6) DNA was detected in 26 of 27 cases by PCR and 10 of 10 cases by in situ hybridization [19]. However, the negative results of southern blot and the common existence of HHV-6 in reactive lymphoid tissue does not support HHV-6 as a causative agent [19]. The presence of fragmented nuclei suggests the involvement of apoptosis [20]. The Fas-Fas ligand system may play an important role in the occurrence of apoptosis in KFD, as evidenced by positive Fas reactivity in many lymph node cells in KFD [16,20]. The perforin pathway may also play a role in apoptosis in KFD [21]. DNA-end labeling (TUNEL) [19] and transmission electron microscopy (TEM) study [21] have also demonstrated the presence of apoptosis in the fragmented nuclei. In this case, no skin manifestation occurred apart from neck lymph node enlargement. It has been reported that % of patients with KFD have skin eruptions [14,22 24]. Yasukawa et al recently reviewed the 11 KFD cases with skin manifestations to date [25]. The cutaneous manifestation of KFD included macules, papules, plaques, and nodules distributed on the face, arms, and upper trunk. However, no clinical skin lesion was specific for KFD. All 11 cases resolved spontaneously or after treatment with oral prednisolone [25]. The pathologic findings were also variable. Some showed nonspecific perivascular dermatitis while others showed patchy infiltration of lymphoid cells, histiocytes, and nuclear debris, similar to the affected lymph node [25]. When there was heavy cell infiltration including large atypical lymphoid cells, it was difficult to differentiate KFD from cutaneous lymphoma [26]. Biopsy of the involved skin should be at the most indurated lesion. KFD patients with skin lesions are more likely to suffer from high fever and liver dysfunction than those without [25,27]. In this case, pure nodal KFD without cutaneous involvement might suggest a benign course and rapid recovery. Nodal KFD needs to be differentiated clinically from other causes of cervical lymphadenitis such as tuberculosis, SLE, non-hodgkin s lymphoma (NHL), sarcoidosis, and Kawasaki s disease. Pathologic differentiation includes SLE, Toxoplasma gondii, Yersinia enterocolitica, Bartonella henselae, EBV, HIV-1, infectious mononucleosis, and cat-scratch disease [4], although the major differentiation is NHL. Misdiagnosis of KFD as NHL may lead to unnecessary lymph node dissection or chemotherapy. Clinical information, abundant histiocytes, and lack of monoclonality in proliferating cells could differentiate KFD from NHL. The presence of plasmacytoid monocytes may provide another clue [4]. Fine needle aspiration cytology may provide an alternative to open nodal biopsy to establish the diagnosis [28]. However, it is not always conclusive [29]. The mainstay of management is usually symptomatic treatment using aspirin or nonsteroidal anti-inflammatory drugs (NSAIDs) and allowing the disease to run its course [30]. Systemic corticosteroids can be used as an effective option in cases unresponsive to initial use of aspirin or NSAIDs, or in cases with elevated levels of LDH and ANA to help early recovery from KFD [31]. In conclusion, the diagnosis of KFD merits active consideration in any nodal biopsy showing fragmentation, necrosis, and karyorrhexis, especially in young women presenting with cervical lymphadenopathy. It is important both clinically and pathologically to differentiate KFD from malignant lymphoma because of differences in treatment choice and clinical outcome. REFERENCES 1. Kikuchi M. Lymphadenitis showing focal reticulum cervical hyperplasia with nuclear debris and phagocytes. Acta Hematol Jpn 1972;35: Fujimoto Y, Kojima Y, Yamaguchi K. Cervical subacute necrotizing lymphadenitis. Naika 1972;30: Menasce LP, Banerjee SS, Edmondson D, Harris M. Histiocytic necrotizing lymphadenitis (Kikuchi-Fujimoto disease): continuing diagnostic difficulties. Histopathology 1998;33: Dorfman RF, Berry GJ. Kikuchi s histiocytic necrotizing lymphadenitis: an analysis of 108 cases with emphasis on differential diagnosis. Semin Diagn Pathol 1988;5: Chamulak GA, Brynes RK, Nathwani BN. Kikuchi-Fujimoto disease mimicking malignant lymphoma. Am J Surg Pathol 1990;14: Chan JK, Wong KC, Ng CS. A fatal case of multicentric Kikuchi s histiocytic necrotizing lymphadenitis. Cancer 1989; 63: O Neill D, O Grady J, Variend S. Child fatality associated with 249
5 pathological features of histiocytic necrotizing lymphadenitis (Kikuchi-Fujimoto disease). Pediatr Pathol Lab Med 1998;18: Tsai MK, Huang HF, Hu RH, et al. Fatal Kikuchi-Fujimoto disease in transplant recipients: a case report. Transplant Proc 1998;30: Facchetti F, de Wolf-Peeters C, van den Oord JJ, et al. Plasmacytoid monocytes (so-called plasmacytoid T cells) in Kikuchi s lymphadenitis: an immunohistologic study. Am J Clin Pathol 1989;92: Ali MH, Horton LWL. Necrotizing lymphadenitis without granulocytic infiltration (Kikuchi s disease). J Clin Pathol 1985; 38: Ohshima K, Kikuchi M, Sumiyoshi Y, et al. Proliferating cells in histiocytic necrotizing lymphadenitis. Virchows Arch B Cell Pathol Incl Mol Pathol 1991;61: Kuo TT. Kikuchi s disease (histiocytic necrotizing lymphadenitis). A clinical pathologic study of 79 cases with an analysis of histologic subtypes, immunohistology, and DNA ploidy. Am J Surg Pathol 1995;19: Imamura M, Uenio H, Matsumura A, et al. An ultrastructural study of subacute necrotizing lymphadenitis. Am J Pathol 1982;107: Eimoto T, Kikuchi M, Mitsui T. Histiocytic necrotizing lymphadenitis: an ultrastructural study in comparison with other types of lymphadenitis. Acta Pathol Jpn 1983;33: Sever CE, Leith CP, Appenzeller J, Foucar K. Kikuchi s histiocytic necrotizing lymphadenitis associated with ruptured silicone breast implant. Arch Pathol Lab Med 1996;120: Chiu CF, Chow KC, Lin TY, et al. Virus infection in patients with histiocytic necrotizing lymphadenitis in Taiwan. Am J Clin Pathol 2000;113: Hollingsworth HC, Peiper SC, Weiss LM, et al. An investigation of the viral pathogenesis of Kikuchi-Fujimoto disease. Lack of evidence for Epstein-Barr virus or human herpes virus type 6 as the causative agents. Arch Pathol Lab Med 1994; 118: Anagnostopoulos I, Hummel M, Korbjuhn P, et al. Epstein- Barr virus in Kikuchi-Fujimoto disease. Lancet 1993;341: Huh J, Kang GH, Gong G, et al. Kaposi s sarcoma-associated herpes virus in Kikuchi s disease. Hum Pathol 1998;29: Ura H, Yamada N, Torii H, et al. Histiocytic necrotizing lymphadenitis (Kikuchi s disease): the necrotic appearance of the lymph node cells is caused by apoptosis. J Dermatol 1999; 26: Ohshima K, Shimazaki K, Kume T, et al. Perforin and Fas pathways of cytotoxic T-cells in histiocytic necrotizing lymphadenitis. Histopathology 1998;33: Kikuchi M, Takeshita M, Tashiro K, et al. Immunohistological study of histiocytic necrotizing lymphadenitis. Virchows Arch A Pathol Anat Histopathol 1986;409: Kuo TT. Cutaneous manifestation of Kikuchi s histiocytic necrotizing lymphadenitis. Am J Surg Pathol 1990;14: Seno A, Torigoe R, Shimoe K, et al. Kikuchi s disease (histiocytic necrotizing lymphadenitis) with cutaneous involvement. J Am Acad Dermatol 1994;30: Yasukawa K, Matsumura T, Sato-Matsumura KC, et al. Kikuchi s disease and the skin: case report and review of the literature. Br J Dermatol 2001;144: Chamulk GA, Brynes RK, Nathwani BN. Kikuchi-Fujimoto disease mimicking malignant lymphoma. Am J Surg Pathol 1990;14: Sumiyoshi Y, Kikuchi M, Takeshita M, et al. Immunohistological study of skin involvement in Kikuchi s disease. Virchows Arch B Cell Pathol Incl Mol Pathol 1992;62: Hsueh EJ, Ko WS, Hwang WS, Yam LT. Fine needle aspiration of histiocytic necrotizing lymphadenitis (Kikuchi s disease). Diagn Cytopathol 1993;9: Bhat NA, Hock YL, Turner NO, Das Gupta AR. Kikuchi s disease of the neck (histiocytic necrotizing lymphadenitis). J Laryngol Otol 1998;112: Garcia CE, Girdhar GHV, Dorfman DM. Kikuchi-Fujimoto disease of the neck. Update. Ann Otol Rhinol Laryngol 1993;102: Jang YJ, Park KH, Seok HJ. Management of Kikuchi s disease using glucocorticoid. J Laryngol Otol 2000;114:
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