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  Table of Contents    
ORIGINAL ARTICLE  
Year : 2012  |  Volume : 55  |  Issue : 3  |  Page : 333-338
Kikuchi-Fujimoto disease in fine needle aspiration smears: A clinico-cytologic study of 18 pediatric cases and correlation with 68 adult patients


1 Department of Pathology, Faculty of Medicine, Kuwait University; Cytology Unit, Mubarak Al-Kabeer Hospital, Kuwait
2 Cytology Unit, Mubarak Al-Kabeer Hospital, Kuwait
3 Department of Histopathology, Al-Jahra Hospital, Kuwait

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Date of Web Publication29-Sep-2012
 

   Abstract 

Objective: Kikuchi-Fujimoto disease (KFD) is a self-limiting disorder which usually affects young women. There are only a few studies on pediatric KFD patients and their fine-needle aspiration (FNA) cytodiagnosis. We report a series of pediatric KFD patients diagnosed by FNA cytology and compare them with adults. Materials and Methods: By routine FNA cytology and through retrospective review smears initially diagnosed as reactive hyperplasia of lymph node during the years 2004-2009, 18 pediatric and 68 adult KFD cases were detected. The clinico-cytologic features of these two groups were compared. Results: The age of the pediatric patients ranged from 6 to 18 years with a median of 13.5 years and adult cases were aged 19 to 54 years with a median of 30 years. Only 1 pediatric case (5.6%) and 20 (29.4%) adult cases were initially diagnosed as KFD (P = 0.0604). Arab:non-Arab ratios were 4.3:1 among the pediatric patients and 1:1.5 for the adults (P = 0.0043). FNA smears were highly cellular in 4 (22.2%) pediatric cases and 37 (54.4%) adult cases (P = 0.0180). More than 5% Kikuchi histiocytes was present in 8 (44.4%) pediatric and 49 (72.1%) adult cases (P = 0.0474). No significant difference was observed in male: female ratio, frequency of head & neck lymphadenopathy, time (season) of presentation, and presence of neutrophils and capillary networks, etc. Conclusions: Besides observation and interpretation errors, a significant difference between the two groups in respect of some clinico-cytomorphological features could have influenced the routine cytodiagnosis leading to lower pickup rate of pediatric KFD cases as compared to adults.

Keywords: Fine needle aspiration cytology, histiocytic necrotizing lymphadenitis, Kikuchi-Fujimoto disease, pediatric

How to cite this article:
Das DK, Haji BI, Al-Boijan RA, Sheikh ZA, Pathan SK, Mannan AA. Kikuchi-Fujimoto disease in fine needle aspiration smears: A clinico-cytologic study of 18 pediatric cases and correlation with 68 adult patients. Indian J Pathol Microbiol 2012;55:333-8

How to cite this URL:
Das DK, Haji BI, Al-Boijan RA, Sheikh ZA, Pathan SK, Mannan AA. Kikuchi-Fujimoto disease in fine needle aspiration smears: A clinico-cytologic study of 18 pediatric cases and correlation with 68 adult patients. Indian J Pathol Microbiol [serial online] 2012 [cited 2019 Jul 20];55:333-8. Available from: http://www.ijpmonline.org/text.asp?2012/55/3/333/101739



   Introduction Top


 Kikuchi-Fujimoto disease More Details (KFD) is a subacute necrotizing lymphadenopathy affecting mainly young women, and manifested by cervical lymphadenopathy. [1] The involved lymph nodes in KFD demonstrate foci of apoptotic changes, mostly in the cortex and paracortical region, with abundant karyorrhectic debris and proliferation of histiocytes, plasmacytoid dendritic cells, and lymphocytes, in the absence of neutrophils. [2] KFD, which is rarely reported in children, is a self-limiting disease, and has been misdiagnosed as reactive hyperplasia of lymph node, infectious diseases, or even as malignancy.≠[3],[4],[5] Diagnosis of KFD usually depends upon an excisional biopsy and pathological examination of enlarged lymph nodes. [6],[7] There are only a few studies based on a series of KFD cases in children. [4],[8],[9],[10] Studies highlighting the role of fine needle aspiration (FNA) cytology in KFD are also very few in literature. [3],[11],[12],[13] In the present study, the clinico-cytologic characteristics of 18 pediatric KFD cases, of which only one was detected during routine cytodiagnosis, are reported. We compare the pediatric patients with 68 adults in an attempt to find out the factors that might have contributed to greater degree of failure in the diagnosis of pediatric KFD cases during routine cytodiagnosis.


   Materials and Methods Top


During the years 2004-2009, 1 pediatric (≤18 years) and 20 adult (>18 years) KFD cases were diagnosed by FNA cytology during routine cytodiagnosis. Review of smears diagnosed as reactive hyperplasia during this period revealed additional 17 pediatric and 48 adult cases with KFD. The details of age/sex distribution of the pediatric cases, their nationalities, presenting features, sites of FNA, and initial cytodiagnoses were highlighted. These two groups were compared in respect clinico-epidemiological findings which included male:female ratio, Kuwaiti: non-Kuwaiti ratio, Arab:non-Arab ratio, frequency of lymphadenopathy, presentation during spring, and extended summer months (March to October) in Kuwait and detailed cytomorphologic features such as cellularity (low +, moderate ++, and high +++), count (>5% and >10%) of Kikuchi histiocytes (from among 200 cells each in MGG and Papanicolaou-stained smears), and the presence of capillary networks, interdigitating reticulum cells, tingible body macrophages, and neutrophils. Fisher's exact test was utilized to find out the statistical significance. Histological material, which was available in only 1 of these 18 pediatric cases, was subjected to immunohistochemical studies using antibodies against CD3, CD4, CD8, CD20, CD68, and MPO on the archival material.


   Results Top


Information on age and sex distribution, nationalities, clinical presentation, and limited laboratory data including initial FNA cytodiagnosis of the 18 pediatric KFD cases are shown in [Table 1]. The age of the 18 pediatric patients ranged from 6-18 years with a median of 13.5 years. There were 12 females and 6 males. Analysis of nationalities of pediatric patients revealed that there were 11 Kuwaitis, 2 non-Kuwaiti Arabs/Middle-Eastern people, 2 Indians, and 1 Iranian. In two non-Kuwaiti patients, the exact nationality was not known. These patients presented with left cervical lymphadenopathy in nine, right cervical lymphadenopathy in seven, bilateral cervical lymphadenopathy in one, and left axillary lymphadenopathy in one. Only three patients complained of fever and one had sore throat. The duration of symptoms known in 12 cases ranged from 1 week to 2 years with a median of 3 weeks. The size of lymph node swellings recorded in 17 cases ranged from 1 cm to 4 cm in largest dimension with a median of 2 cm. The lymph node size was ≥2 cm in 9 (50%) cases. The initial (routine) cytodiagnosis was suggestive of KFD in one patient; the remaining 17 cases were diagnosed as reactive hyperplasia of lymph node; however, focal necrosis and ill-defined granuloma were noticed in one case each. Ziehl-Neelsen (Z N) stain for acid-fast bacilli (AFB) was negative in both these cases and culture for Mycobacterium tuberculosis was negative in the case with ill-defined granuloma. Cytologically, the KFD were characterized by the presence of small histiocytes with crescentic nuclei and with or without ingested cell debris dispersed among a polymorphic lymphoid cell populations and scattered apoptotic debris in the background [Figure 1]a and b. Review of FNA smears of the lone case subjected to excision biopsy showed a few Kikuchi histiocytes dispersed among lymphoid cells [Figure 2]a and b. Histopathology of the excised lymph node revealed numerous Kikuchi histiocytes [Figure 2]c. In some fields, extensive karyorrhectic debris and proliferation of large atypical cells, especially around capillaries with endothelial proliferation, were observed [Figure 2]d. Immunohistochemical staining showed that most of the lymphoid cells in the affected foci were positive for pan T-cell marker CD3 [Figure 3]a, negative for helper T-cell marker CD4, positive for suppressor T-cell marker CD8 [Figure 3]b, and negative for B-cell marker CD20; the Kikuchi histiocytes were positive for histiocyte marker CD68 [Figure 3]c, and myeloid marker MPO [Figure 3]d.
Figure 1: FNA smear from 1.5 × 1.5 cm left cervical lymph node of 2 weeks duration in a 17-year-old adolescent Kuwaitiboy. The clinical diagnosis was suspicious of tuberculosis/lymphoma. Initial cytodiagnosis was reactive hyperplasia and reviewed cytodiagnosis was Kikuchi-Fujimoto disease. (a) Numerous Kikuchi histiocytes with crescentic nuclei and ingested cell debris (the count was 25 per 200 cells) are seen along with reactive lymphoid cells and apoptotic bodies (MGG ×400). (b) In the Papanicloaou-stained smears the count of Kikuchi histiocytes was 16 per 200 cells (×400)

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Figure 2: FNA smear and histology of 4 × 3 cm. right cervical lymph node of 2 weeks duration in a 13 year-old Kuwaitiboy with fever. (a) Scattered histiocytes with oval to crescentic nuclei among lymphoid cells. (MGG ×400). (b) Relatively less number of crescentic histiocytes in Papanicolaou-stained smears (×400). (c) The paraffi n section shows large number of Kikuchi histiocytes among lymphoid cell population (Hematoxylin and eosin ×400). (d) Abundant apoptotic debris and proliferation of blastoid cells especially around capillaries (Hematoxylin and eosin ×400)

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Figure 3: Immunohistochemical staining of the paraffi n section of the case described in Figure 2C and D. The lesional lymphoid cells were mostly CD3+, CD20– , CD4– , and CD8+ and histiocytes CD68+ and MPO+. (a) Most of the cells including those around capillaries are CD3+ (×400). (b) The blastoid cells especially around capillaries are positive for CD8 (×400). (c) The Kikuchi histiocytes are positive for CD68 (×400). (d) The Kikuchi histiocytes are also positive for MPO (×400)

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Table 1: Demographic data and clinical information on pediatric Kikuchi-Fujimoto disease cases

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Only 1 (5.6%) out of 18 pediatric cases was diagnosed initially by FNA cytology as suggestive of (S/O) KFD ,whereas 20 (29.4%) of the 68 adult cases (aged 19 to 54 years with a median of 30 years) were initially diagnosed as KFD or S/O KFD (P = 0.0604). The comparison of various clinico-cytologic features of pediatric versus adult KFD cases is depicted in [Table 2]. The male to female ratio in the pediatric age group was 6:12 (1:2) and it was 19:49 (1:2.6) in adult cases (P = 0.7714). The Kuwaiti and non-Kuwaiti ratio among the pediatric patients was 11:7 (1.6:1) and it was 20:48 (1:2.4) among adult cases (P = 0.0160). The Arab: non-Arabs ratio was 13:3 (4.3:1) for the pediatric patients and 25:38 (1:1.5)th for the adults (P = 0.0043). The distribution cases during spring and extended summer season (March to October) versus winter months (November to February) showed that children suffered with equal frequency during both these periods (1.5 per month), whereas the adult cases were more frequent during spring and summer moths (6.5 cases per month during spring and summer and 4.0 cases per month during winter); however, there was no significant difference between the two groups so far as frequency of cases during the spring and extended summer months was concerned (P = 0.5438). The frequency of lymphadenopathy in head and neck region in pediatric age group (94.4%) and adult cases (95.6%) were close (P = 1.0000). The FNA smears were highly cellular in only 4 (22.2%) pediatric cases and 37 (57.4%) adult cases (P = 0.0180). More than 5% Kikuchi cells was present in 8 (44.4%) pediatric cases and 49 (72.1%) adult cases (P = 0.0474). Similarly, when >10% Kikuchi cells were taken into consideration, 16.7% in the pediatric group and 48.5% among adult cases had this feature (P = 0.0167). Neutrophils were present in 10 (55.6%) pediatric cases and 21 (30.9%) of adult patients (P = 0.0604). No significant difference was observed between the two groups in the frequency of capillary networks, tingible body macrophages, and interdigitating reticulum cells although the frequency of capillary networks was higher in adult patients and that of tingible body macrophages and dendritic reticulum cells was higher in the pediatric age group.
Table 2: Pediatric versus adult Kikuchi-Fujimoto Disease: Clinico-cytologic features

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   Discussion Top


KFD or histiocytic necrotizing lymphadenitis (HNL) is a cervical lymphadenitis that occurs rarely in children. [5],[9] Park et al. [4] in a study of 412 pediatric patients with fever and peripheral lymphadenopathy detected 16 (3.9%) patients with KFD, diagnosed by lymph node biopsy. In a report of 2500 lymph node biopsies, Al-Maghrabi and Kanaan [14] observed a much smaller frequency of 4 (0.2%) KFD cases with age ranging from 13 to 17 years. In the present study based on FNA cytology, the frequency of pediatric KFD cases among 2826 lymph node FNAs from all age groups (pediatrics and adults) was 1 (0.04%) at routine cytologic examination but increased to 18 (0.64%) following review of smears initially diagnosed as reactive hyperplasia of lymph nodes. One each of the 17 reactive hyperplasia cases, which turned out to be KFD following review, were found to be showing foci of necrosis and ill formed granuloma , respectively, at initial cytologic examination. During review, these observations were ruled out since the so-called necrotic material was apoptotic debris and ill-defined granulomas were occasional collections/aggregates of Kikuchi histiocytes. The ancillary studies for acid-fast bacilli were negative in these two cases. Our observation indicates that most of our KFD cases were lost due to missed diagnosis at initial cytologic examination due to observation/interpretation errors. Others have also faced similar problems in cytodiagnosis of KFD. In FNA cytologic study of 10 cases of histologically proved KFD by Viguer et al. [3] the initial cytodiagnosis was suggestive of KFD in one case only, the remaining diagnostic labels being nonspecific reactive hyperplasia in 7 cases, necrotizing lymphadenitis in 1case and suspicious of lymphoma in 1 case; even after blind review by 4 investigators, only 4 of the 10 cases were picked up as KFD by all four, 1 case by 3, 1 case by 1, and the remaining 4 cases were missed by all investigators. Whereas only 1 out of our 18 pediatric KFD cases (5.6%) was diagnosed correctly at routine cytodiagnosis, 20 out of 68 adult cases (29.4%) were diagnosed initially; however, the significance of difference was lost marginally (P = 0.0604). The lone pediatric case in our material diagnosed during routine FNA cytodiagnosis was an 18 year-old girl. It has been suggested that some cytopathologists, who are not very conversant with the cytologic features of KFD, may misdiagnose it as reactive hyperplasia of lymph node or tuberculosis in FNA smears. [13]

The present report is based on the comparison of clinico-cytologic features of 18 pediatric and 68 adult cases; these cases had definitive cytodiagnosis of KFD or were suspicious/ suggestive of (S/O) KFD by FNA cytology following review of smears. The upper age limit to define the pediatric population varies among experts/pediatric care organizations ranging from 16 to 21, but the most commonly used upper age limit appears to be 18. The age range of the pediatric group in our material was based on the stipulations of the pediatric regulation of European council (EC) which defines the "pediatric population" as "that part of the population aged between birth and 18 years" but does not divide it further into various groups unlike the ICH Harmonized Tripartite Guidance: Clinical Investigation of medicinal products in the pediatric population E11, as: preterm new born infants, term newborn infants (0 to 27 days), infants and toddlers (28 days to 23 months), children (2 to 11 years), and adolescents (12 to 16-18 years, depending upon the geographic regions). [15] The ratios of pediatric: adult KFD cases were 1:3.8 in our material, which was similar to those of two other studies based on lymph node biopsies, i.e. 1:2.75 and 1:3, respectively. [14],[16] In another FNA cytology-based report none of the 10 histologically proven KFD cases were in pediatric age group, the youngest patient being 19 year old. [3] Comparing of age and sex distribution of the present study with four other studies in children [Table 3] revealed that the age of the patients were either ≤18 years like our material or ≤14 years. [4],[8],[9],[10] In these five studies, the minimum age was 1.5 years; median age ranged from 10.1 to 13.5 years, and male to female ratio showed a wide variation, with a female predominance (in the present study) to equal male:female ratio, and even male predominance. [4],[8],[9],[10] It has been reported earlier that in children, KFD has different gender predominance as compared to adult population, showing a preference for boys in the pediatric age group. [17],[18] There was female predominance in both pediatric and adult patients in our study but no significant difference was observed between the two groups. It was found that there was significantly higher Kuwaiti:non-Kuwaiti ratio (P = 0.0160) as well as Arab:non-Arab ratio (P = 0.0043) among pediatric patients as compared to adults. To the best of our knowledge, similar observation in respect of nationalities of KFD patients has not been reported earlier. In a study by Menasce et al., [19] there was a tendency for the KFD cases to occur predominantly (16/27 biopsies) during the spring and summer months (March to July). Although lesser number of our pediatric cases presented during spring and extended summer months (March to October), there was no significant difference between the two groups (66.7% versus 76.5%, P = 0.5438). As regards site of lymphadenopathy, predominance of cervical lymphadenopathy was a common finding in various reports. [4],[8],[9],[10],[13] The head and neck region was the most common site for lymphadenopathy as has been found in other histological and cytological studies but this was true for both the groups in our study (94.4% in pediatric vs. 95.6% in adults, P = 1.0000). [3],[14],[16]
Table 3: Pediatric Kikuchi-Fujimoto Disease: Clinical features in series with ten or more cases

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In this study, we have attempted to find out which factors could have influenced the difference in pick up rate between pediatric and adult cases by the cytopathologists at initial cytologic examination. It is reported earlier that up to 30% to 40% of KFD can be misdiagnosed, especially in early proliferative phase.≠[20] In a study involving 44 cytologically diagnosed Kikuchi's lymphadenitis cases by FNA, false positive rate was 37.5%, false negative rate 50%, and overall accuracy 56.25%. [21] Differential diagnosis of KFD, both clinically and histologically, include malignant lymphoma, SLE, and infectious diseases such as toxoplasmosis, tuberculosis, cat scratch disease, leprosy,  Yersinia More Details, and viral infections. [22],[23] Especially when the necrotizing process is limited in KFD, the blastic lymphoid cells may dominate the picture causing diagnostic concern; among 17 referral cases received by a center from various hospitals in UK, the diagnosis from out-side hospitals was malignancy in 7; the most common suggested diagnosis was that of a NHL and the KFD was suggested in three cases only. [19] It is also a general belief that KFD is a self-limited condition of young adults, [24] especially in young women in their 20s and 30s from the far-east. [25] A significantly higher number of pediatric patients in our study were Arabs, especially Kuwaiti by nationality. Therefore, the expectation of the cytopathologists to find a KFD case among children, especially children of Arab countries with lymphadenopathy was possibly low. The comparison of cytologic features between the two groups also showed that cytomorphologically the pediatric KFD cases were to some extent different from the adult cases. In a significantly lower number of pediatric KFD cases, there was high cellularity (P = 0.0180), and Kikuchi histiocytes count >5% (P = 0.0474); the significance was even higher (P = 0.0167) when the two groups were compared in respect of >10% Kikuchi histiocytes. The presence of neutrophils, which may be partly due to contamination of blood elements during FNA, was noted in 55.6% of pediatric cases and 33.9% of adult patients; however, the significance of difference was marginally lost (P = 0.0604). Under these circumstances, the chance of missing a case of KFD among children appears to be higher, especially by a cytopathologist who is not very conversant with this entity. One limitation of the present study is the remarkably lower number of subsequent biopsy cases for histopathological examination. Out of 18 pediatric cases, there was subsequent histology in only one which was initially diagnosed as reactive hyperplasia by FNA cytology. The histopathological diagnosis was KFD in this case and it was supported by immunohistochemical findings of CD3+, CD20-, CD4- and CD8+ lymphoid cell populations and CD68+ and MPO+ Kikuchi histiocytes in the affected foci. A similar immunohistochemical reaction pattern in KFD cases has been observed earlier by other investigators. [26],[27],[28] The low frequency of follow-up histology in our material may be attributed to the fact that KFD is a self-limiting disease and moreover, most of these cases were diagnosed as nonspecific reactive hyperplasia during routine cytodiagnosis for which biopsy is not usually done.


   Acknowledgments Top


Part of this study was the material of an oral presentation at the 40 th Annual Conference of the Indian Academy of Cytologists at Kolkata, India during 25 th -28 th November, 2010.

 
   References Top

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Correspondence Address:
Dilip K Das
Department of Pathology, Faculty of Medicine, Kuwait University, P.O. Box: 24923, Safat13110, Kuwait

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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0377-4929.101739

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