Role of Anti-neutrophil Cytoplasmic Antibodies in Kawasaki Disease
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1 J Med Sci 2012;32(3): Copyright 2012 JMS Fang-Yih Liaw, et al. Role of Anti-neutrophil Cytoplasmic Antibodies in Kawasaki Disease Fang-Yih Liaw 1, Ming-Chih Tsai 2, Jen-Jiuan Liaw 3, Fang-Lin Chang 4, Tung-Wei Kao 1, and Hueng-Chuen Fan 2* 1 Department of Family and Community Health; 2 Department of Pediatrics; 4 Department of Anesthesia, Tri-Service General Hospital, National Defense Medical Center, Taipei; 3 School of Nursing, National Defense Medical Center, Taipei, Taiwan, Republic of China Background: Kawasaki disease (KD) is characterized by systemic vasculitis and may lead to coronary artery ectasia and aneurysm. Autoantibodies, in particular anti-neutrophil cytoplasmic antibodies (ANCAs), have been identified in association with the vasculitis. The relationship between ANCAs and KD is unclear. The purpose of this study is to investigate the role of ANCAs in KD in Taiwan. Methods: We assessed ANCAs in 10 KD patients (6 male and 4 female; age range, 4 months to 3 years) between January and December Results: Cytoplasmic (c)-anca staining was absent in all patients, but 5 patients showed perinuclear (p)-anca staining. C-reactive protein levels were significantly higher in p- ANCA-positive than p-anca-negative KD patients (12.672±3.05 vs ±2.60 mg dl -1, respectively; P < 0.01); there was no significant difference in age, white blood cell count, or clinical presentation. Conclusions: Our data showed that CRP levels were significantly higher in p-anca-positive patients and c-anca was negative in all KD patients. Neither c-anca nor p-anca was linked to coronary artery abnormalities in KD patients, suggesting that ANCAs may play only a minor role in the pathogenesis of KD. Key words: Kawasaki disease, anti-neutrophil cytoplasmic antibodies, clinical presentation INTRODUCTION Kawasaki disease (KD), formerly known as mucocutaneous lymph node syndrome, is an acute systemic inflammatory childhood illness. The disorder occurs worldwide, but is most common in Asian populations. 1-2 The annual reported incidence of KD in Japan was and per 100,000 children, aged 0-4 years, in 2007 and Compared with an annual incidence of 6-9 per 100,000 similarly aged children in the United States 4 and per 100,000 children in Britain 5 and Australia, 6 the annual incidence in Taiwan is 69 per 100,000 children under 5 years old 7, which is 10 times greater than that in Western countries. Received: December 26, 2011; Revised: March 19, 2012; Accepted: April 24, 2012 * Corresponding author: Hueng-Chuen Fan, Department of Pediatrics, Tri-Service General Hospital, National Defense Medical Center, No. 325, Sec. 2, Cheng-gong Road, Taipei 114, Taiwan, Republic of China. Tel: ; Fax: ; fanhuengchuen@yahoo.com.tw If left untreated, the condition may result in coronary artery abnormalities, including vasculitis, ectasia, and aneurysm, in up to 20-25% of patients. 8-9 Severely affected patients may develop coronary artery thrombosis or stenosis, and myocardial infarction, and sudden death may also occur. KD is reportedly the leading cause of acquired heart disease in children in developed countries. However, the etiology of KD remains unknown. Diagnosis of classic KD is based on the presence of characteristic clinical signs, including fever for 5 or more days and 4 or more of the 5 principal clinical features: (1) changes in the hands and feet (erythema, edema, and peeling), (2) polymorphous exanthema, (3) bilateral bulbar conjunctival injection without exudates, (4) changes in lips and oral cavity (erythema and strawberry tongue), and (5) cervical lymphadenopathy, usually unilateral. 4 No definitive laboratory diagnostic tests are available for this vasculitic disorder. Vasculitic disorders such as Wegener s granulomatosis (WG) and polyarteritis nodosa (PAN) are associated with autoantibodies against determinants in neutrophils cytoplasm. Detection of thease antibodies has proved useful for diagnosis Indirect immunofluorescence (IIF) and enzyme-linked immunosorbent assay (ELISA) are the most widely used techniques for ANCA detection. Us- 129
2 ANCA in Kawasaki disease ing IIF on ethanol-fixed neutrophils, 2 staining patterns are recognized: diffuse cytoplasmic (c)-anca staining and perinuclear (p)-anca staining. 12 Because PAN and KD are disseminated vasculitides of unknown causes affecting small- and medium-sized vessels in children, and because autopsy reports have proved that clinical and pathologic findings of infantile PAN are strikingly similar to those of KD 13-14, it was of interest to investigate the role of these circulating autoantibodies in KD. In this study, 10 Taiwanese KD patients were screened and divided into 2 groups according to the expression of ANCAs. The clinical presentations of both groups were analyzed and compared. MATERIAL AND METHODS The medical charts of 10 children, presenting between January and December 2003, who met the criteria for the diagnosis of KD, established by the Japanese Research Committee, were retrospectively reviewed. The criteria for a KD diagnosis included at least 5 days of fever and at least 4 of the 5 primary clinical features described previously. In incomplete or atypical KD, patients have persistent fever but less than four of the five classical signs. In such patients, echocardiographic results and laboratory data can help diagnose the diagnosis. 15 Coronary artery abnormalities were considered if they meet at least one of the following Japanese Ministry of Health criteria 16 : Internal lumen diameter >3 mm in children less than five years of age; Internal diameter of a segment at least 1.5 times the size of an adjacent segment; or, the coronary lumen is clearly irregular. The retrospective reviews of medical charts were approved by the Ethics Committee of the Tri-Service General Hospital, Taiwan. Information from the patient charts indicated that serum samples from all patients were obtained within hours of being admitted. Each patient received intravenous immunoglobulin (IVIG; 2 g kg - 1 d -1 ) within 36 h of admission and also received aspirin (80 mg kg -1 d -1 ). The dose of aspirin was decreased to 5 mg kg -1 d -1 after normalization of C-reactive protein (CRP) levels or fever subsided. The presence of circulating autoantibodies had also been examined by IIF using the IMMCO Diagnostics (Buffalo, NY, USA) ANCA test system. Briefly, neutrophils, isolated from whole blood, were washed twice in phosphate-buffered saline (ph: 7.4) and sedimented on to glass slides using a cytocentrifuge. The slides were dried and fixed in absolute ethanol for 10 min. Patient serum was diluted 1:20 and layered over the neutrophils, followed by the secondary antibody. Interpretation was performed by epi-fluorescence microscopy, according to standard international guidelines. Statistical analysis was performed using SPSS software (version 17.01; SPSS Inc., Chicago, IL, USA). Differences between KD patients groups with and without a positive p-anca were analyzed using the Mann-Whitney test; P values < 0.05 were considered statistically significant. RESULTS The records of 10 children were included in the study, including 6 girls (aged 4-36 months) and 4 boys (aged 5-24 months); half of the patients (5/10) were confirmed to have typical KD and half were confirmed to have atypical KD. The mean age of all patients was 14.8±10.06 months. The most important laboratory findings were leukocytosis and elevated CRP levels. Coronary artery dilatation developed in 6 patients. By IIF, p-ancas were detected in 5 patients at the time of hospital admission; c-ancas were not detected in any of these patients. Figure 1 shows the typical appearance of P-ANCA. The general clinical presentation, laboratory data, and autoantibody profiles of all patients are listed in Table 1. The 10 patients with KD were divided into 2 groups based on the results of p-anca detection, namely, those who were p-anca-positive and those who were p- ANCA-negative. Table 2 shows the comparison between these groups. There was no difference between p-ancapositive and negative KD patients with respect to clinical presentation, age, or white blood cell count. However, CRP levels were significantly higher in p-anca -positive patients than in p-anca- negative patients. DISCUSSION Statistical reports show 50% of patients with KD are younger than 2 years of age and that 80% are younger than 5 years of age; KD seldom occurs in patients older than 12 years of age This same age distribution of KD was observed in the present study, with 50% of the KD-diagnosed children being under 2 years old and 80% being younger than 5 years of age. In addition, population-based studies in several countries have shown that the ratio of male to female patients with KD was 1.5:1 in Japan 17,19 and 1.62:1 in Taiwan. 7 However, KD was predominantly observed in female patients in this study (male/female: 4/6). This discrepancy may have been due to the limited sample size in our study. 130
3 Fang-Yih Liaw, et al. Table 1 Clinical manifestations and laboratory data of KD patients Case Sex F F M F F F M F M M Age 4/M 2/Y 10/M 3/Y 5/M 1/Y 2/Y 1/Y 9/M 1/Y Conjunctival injection Erythema of the oral and pharyngeal mucosa Edema and erythema of the hands and feet Polymorphous exanthema Nonsuppurative cervical lymphadenopathy Dilated coronary artery White blood cell count ( 10 3 cells mm -3 ) Elevated C-reactive protein (mg dl -1 ) p-anca c-anca IVIG treatment p-anca after treatment c-anca after treatment Table 2 Comparison of KD patients with or without positive p-anca p-anca Positive Negative p-value Number of Patients 5 5 / Age (Months) 21.2± ± (10-36 months) (4-12 months) White blood cell count 12.21± ± ( 10 3 cells mm -3 ) C-reactive protein ± ±2.606 <0.05 (mg dl -1 ) Dilated coronary artery 3 3 / Criteria (fulfill 4/5) 4 4 / Conjunctival injection 5 3 / Erythema of the oral and 5 5 / pharyngeal mucosa Edema and erythema of 4 3 / the hands and feet Polymorphous exanthema 5 5 / Nonsuppurative cervical lymphadenopathy 1 1 / In this study, clinical manifestations of patients with KD included fever (100%), lymphadenopathy (20%), rash (100%), conjunctival injection (80%), edema of Fig. 1 Typical appearance of p-anca as determined by indirect immunofluorescence (IIF). the oral and pharyngeal mucosa (100%), and edema and erythema of the hands and feet (100%). Some patients (40%) showed erythema and induration of the bacille Calmette-Guérin (BCG) scar, also an important indicator in the diagnosis of KD Based on the diagnostic criteria for KD, there were 5 typical KD cases (cases 3, 4, 5, 7 and 8), and 3 atypical ones (cases 1, 2 and 9). Cases 6 and10 showed erythema of the oral and pharyngeal mucosa, edema and erythema of the hands and feet, and 131
4 ANCA in Kawasaki disease polymorphous exanthema; however, their persistent fever and other KD-related symptoms subsided after IVIG and aspirin administration. Therefore, we grouped them as atypical KD cases. KD is known to cause coronary artery ectasia and aneurysms, which may lead to more serious cardiac events and sudden death. In Taiwan, a report showed that 7.2% patients with KD developed coronary artery aneurysms. 7 However, in this study, we found 60% of the patients with KD showed dilated coronary arteries by echocardiography. In addition to our limited sample numbers, we think that the discrepancies may be due to the definition of the cardiac involvement. The dilated coronary arteries under echocardiography may only reflect an inflammatory status of this vasculitis. Whether the finding of dilated coronary arteries by echocardiography is equal to coronary artery aneurysms is worthy of further investigation. In fact, none of these patients have developed coronary artery aneurysms in the 8-year follow up. Routine laboratory tests showed an average white blood cell count of ± cells mm -3, an erythrocyte sedimentation rate (ESR) of 78±29.34 mm h -1 (normal range: 3-13 mm h -1 ), and CRP levels of 8.43±5.21 mg dl -1 (normal: <0.5 mg dl -1 ). These laboratory data also highlight the generalized immune activation and inflammation associated with this disease. Several studies have proposed that immune activation and the secretion of cytokines may contribute to the pathogenesis of KD Although the gene-dosage effect on the risk of KD was observed among patients more than 1 year old and in the female subjects 26, no association between individual cytokine genetic polymorphisms and susceptibility of KD has so far been detected. Suzuki et al. 27 discovered that sera from Churg Strauss syndrome (CSS) patients reacted to the Ha and Hf epitopes of the myeloperoxidase (MPO) heavy chain and that sera from systemic lupus erythematosus (SLE) and rheumatoid arthritis (RA) patients reacted to all epitopes of the MPO heavy chain. Sera from KD patients reacted mainly to the Hf epitope. The epitopic specificity of MPO-ANCA may show predilection to some vasculitic disorders, such as CSS, SLE, RA and KD. Therefore, reaction of patient sera with MPO heavy chain Hf epitopes may be considered a potential aid for diagnosis of KD. However, there is only 50% positive rate of p-anca in this study, which suggests that the value of such a diagnostic would be limited. Pathologic findings that are strikingly similar to those seen in KD have been described for infantile polyarteritis nodosa (PAN) ; ANCA testing currently plays a critical role in the diagnosis and monitoring of PAN This connection helped propel us to investigate the role of ANCA in patients with KD because the 2 patterns of ANCA staining, c-anca staining p-anca staining 13, are differentially linked to other vasculitic disorders. For example, c-ancas are often linked to Wegener s granulomatosis patients, whereas p-ancas are related to patients with microscopic polyangiitis and CSS. Additionally, c-anca-positive vasculitis is more frequently present in patients with renal, lung, and sinus diseases 28, whereas p-anca-positive vasculitis is associated with isolated renal damage or involvement other target organs, particularly the lungs. 29 Reports have shown that 28-73% of patients with KD were ANCA-positive in the acute phase and 0-89% of patients with KD were ANCApositive in the convalescent phase. 30,32 Different results may be related to population stratification and sample numbers. In the present study, there was a 50% positive rate for p-anca and a 0% positive rate for c-anca in the acute phase of KD. There was no renal or lung involvement in these p-anca-positive KD patients. Analyzing medical records, we found a tendency that the age of patients attesting positive for p-anca trended towards being older than those with a negative p-anca result, but this difference was not significant. However, white cell counts and clinical presentations also did not show significant differences between the two groups divided according to their p-anca status, but CRP levels were significantly higher in the group with a positive p-anca. Consequently, based on our limited data, we think that p-anca may possibly be related to patient age and inflammation status. Discrepancies among p-anca positive rates in studies may be due to the different detection techniques, the time point for blood sampling, and genetic backgrounds. 33 In this study, all patients received IVIG (2 g kg -1 day -1 ) and aspirin ( mg/ kg -1 day -1 ). 15 To investigate the effects of IVIG on ANCA levels, blood samples were taken before and after IVIG administration to measure c-anca and p-anca during the acute and convalescent phases. Results showed p-anca was positive and c-anca was negative at the time of sampling in both the acute and convalescent phases. Although neutralization of autoantibodies is part of the underlying rationale for IVIG administration for the treatment of KD 15, our results suggest that circulating p-ancas are not effectively neutralized by IVIG. Alternately, they may not be the main target of IVIG or may be a by-product of an aberrant cascade activated during acute inflammation. Interestingly, Jayne et al., were unable to demonstrate a 132
5 Fang-Yih Liaw, et al. difference in ANCA levels between KD patients receiving IVIG or placebo treatment. 34 Combined, these results suggest that the role of p-anca in the pathogenesis of KD may be minor. CONCLUSION KD is an acute systemic inflammatory illness of childhood and is the leading cause of pediatric acquired heart disease in developed countries. KD is potentially lethal if left untreated. The diagnosis of KD is based on the exclusion of other diseases as well as on the recognition of a typical cadre of clinical features. Adding to the diagnostic challenge, a specific laboratory test to confirm the disease is not available. In this study, the clinical presentations of KD patients with or without positive p-anca were similar. The presence of p-ancas may only be related to patients ages and inflammatory status as they appear to play a minor role, if any, in the pathogenesis of KD. The results of this study add further evidence that ANCAs cannot be used for diagnostic purposes in patients with KD. DISCLOSURE The authors declare that they have no conflict of interest. REFERENCES 1. Rowley AH, Shulman ST. Kawasaki syndrome. Pediatr Clin North Am 1999;46: Taubert KA, Shulman ST. Kawasaki disease. Am Fam Physician 1999;59: , Nakamura Y, Yashiro M, Uehara R. Sadakane A, Chihara I, Aoyama Y, Kotani K, Yanagawa H. Epidemiologic features of Kawasaki disease in Japan: Results of the nationwide survey. J Epidemiol 2010;20: Dajani AS, Taubert KA, Gerber MA. Shulman ST, Ferrieri P, Freed M, Takahashi M, Bierman FZ, Karchmer AW, Wilson W, Rahimtoola SH, Durak DT, Peter G. Diagnosis and therapy of Kawasaki disease in children. Circulation 1993;87: Dhillon R, Newton L, Rudd PT, Hall SM. Management of Kawasaki disease in the British Isles. Arch Dis Child.1993;69: Royle JA, Williams K, Elliott E, Sholler G, Nolan T, Allen R, Isaacs D. Kawasaki disease in Australia, Arch Dis Child 1998;78: Huang WC, Huang LM, Chang IS, Chang LY, Chiang BL, Chen PJ, Wu MH, Lue HC, Lee CY, Kawasaki Disease Research Group. Epidemiologic features of Kawasaki disease in Taiwan, Pediatrics. 2009;123:e Lie JT. Systemic and isolated vasculitis: A rational approach to classification and pathologic diagnosis. Pathol Annu.1989;24: Amano S, Hazama F, Hamashima Y. Pathology of Kawasaki disease: II. Distribution and incidence of the vascular lesions. Jpn Circ J 1979;43: Bosch X, Guilabert A, Font J. Antineutrophil cytoplasmic antibodies. Lancet 2006;368: Jennette JC, Falk RJ. New insight into the pathogenesis of vasculitis associated with antineutrophil cytoplasmic autoantibodies. Curr Opin Rheumatol 2008;20: Schmitt WH, van der Woude FJ. Clinical applications of antineutrophil cytoplasmic antibody testing. Curr Opin Rheumatol 2004;16: Glanz S, Bittner SJ, Berman MA, Dolan TF Jr, Talner NS. Regression of coronary-artery aneurysms in infantile polyarteritis nodosa. N Engl J Med 1976;294: Yanagisawa M, Kobayashi N, Matsuya S. Myocardial infarction due to coronary thromboarteritis, following acute febrile mucocutaneous lymph node syndrome (MLNS) in an infant. Pediatrics 1974;54: Newburger JW, Takahashi M, Gerber MA, Gewitz MH, Tani LY, Burns JC, Shulman ST, Bolger AF, Ferrieri P, Baltimore RS, Wilson WR, Baddour LM, Levison ME, Pallasch TJ, Falace DA, Taubert KA. Diagnosis, treatment, and long-term management of Kawasaki disease: a statement for health professionals from the Committee on Rheumatic Fever, Endocarditis, and Kawasaki Disease, Council on Cardiovascular Disease in the Young, American Heart Association. Pediatrics 2004;114: Research Committee on Kawasaki Disease. Report of subcommittee on standardization of diagnostic criteria and reporting of coronary artery lesions in Kawasaki disease Tokyo, Japan, Ministry of Health and Welfare. Ref Type: Report. 17. Yanagawa H, Nakamura Y, Yashiro M, Uehara R, Oki I, Kayaba K. Incidence of Kawasaki disease in Japan: the nationwide surveys of Pediatr Int 2006;48: Holman RC, Curns AT, Belay ED, Steiner CA, Schonberger LB. Kawasaki syndrome hospitalizations in the United States, 1997 and Pediatrics 133
6 ANCA in Kawasaki disease 2003;112: Yanagawa H, Yashiro M, Nakamura Y, Kawasaki T, Kato H. Results of 12 nationwide epidemiological incidence surveys of Kawasaki disease in Japan. Arch Pediatr Adolesc Med 1995;149: Brogan PA, Bose A, Burgner D, Shingadia D, Tulloh R, Michie C, Klein N, Booy R, Levin M, Dillon MJ. Kawasaki disease: an evidence based approach to diagnosis, treatment, and proposals for future research. Arch Dis Child 2002;86: Antony D, Jessy PL. Involvement of BCG scar in Kawasaki disease. Indian Pediatr 2005;42: Maury CP, Salo E, Pelkonen P. Circulating interleukin-1 beta in patients with Kawasaki disease. N Engl J Med.1988;319: Matsubara T, Furukawa S, Yabuta K. Serum levels of tumor necrosis factor, interleukin 2 receptor, and interferon-gamma in Kawasaki disease involved coronary-artery lesions. Clin Immunol Immunopathol. 1990;56: Lin CY, Lin CC, Hwang B, Chiang B. Serial changes of serum interleukin-6, interleukin-8, and tumor necrosis factor alpha among patients with Kawasaki disease. J Pediatr. 1992;121: Hirao J, Hibi S, Andoh T, Ichimura T. High levels of circulating interleukin-4 and interleukin- 10 in Kawasaki disease. Int Arch Allergy Immunol 1997;112: Weng KP, Ho TY, Chiao YH, Cheng JT, Hsieh KS, Huang SH, Ou SF, Liu KH, Hsu CJ, Lu PJ, Hsiao M, Ger LP. Cytokine genetic polymorphisms and susceptibility to Kawasaki disease in Taiwanese children. Circ J 2010;74: Suzuki K, Kobayashi S, Yamazaki K, Gondo M, Tomizawa K, Arimura Y, Nakabayashi K, Ozaki S, Yoshida M, Yoshida T, Tsusaka N, Muso E, Okazaki T, Hashimoto H. Analysis of risk epitopes of antineutrophil antibody MPO-ANCA in vasculitis in Japanese population. Microbiol Immunol 2007;51: Ellis EN, Wood EG, Berry P. Spectrum of disease associated with anti-neutrophil cytoplasmic autoantibodies in pediatric patients. J Pediatr. 1995;126: Lesavre P. The diagnostic and prognostic significance of ANCA. Ren Fail 1996;18: Soppi E, Salo E, Pelkonen P. Antibodies against neutrophil cytoplasmic components in Kawasaki disease. APMIS 1992;100: Rider LG, Wener MH, French J, Sherry DD, Mendelman PM. Autoantibody production in Kawasaki syndrome. Clin Exp Rheumatol 1993;11: Savage CO, Tizard J, Jayne D, Lockwood CM, Dillon MJ. Antineutrophil cytoplasm antibodies in Kawasaki disease. Arch Dis Child 1989;64: Venkatraman R, Singh S, Minz RW. Study of the autoantibody profile after the acute phase of Kawasaki disease in a cohort of children from North India. Rheumatol Int 2006;26: Jayne DR, Chapel H, Adu D, Misbah S, O Donoghue D, Scott D, Lockwood CM. Intravenous immunoglobulin for ANCA-associated systemic vasculitis with persistent disease activity. QJM 2000;93:
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