Correlation between response of Kawasaki disease after initial standard dose of intravenous immunoglobulin therapy and routine laboratory indexes: a meta-analysis_Chinese Journal of Evidence-Based Medicine

Authors：

LIU Zhuoxun , WEN Xiaoying , ZHENG Yanxia , XU Youjia ,  YANG Jinghua

Department of Pediatrics, the Second Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, 510000, P.R.China;

Corresponding author：

YANG Jinghua, Email: doumiaomama@126.com

Keywords：

IVIG; Kawasaki disease; Non-response; Case-control study; Systematic review; Meta-analysis

DOI：

10.7507/1672-2531.201703037

Video：

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ObjectiveTo systematically review the response of Kawasaki disease (KD) after an initial standard dose of intravenous immunoglobulin (IVIG) therapy and routine laboratory indexes.MethodsWe searched PubMed, EMbase, The Cochrane Library, CBM, CNKI, VIP and WanFang Data databases to collect case-control studies about the correlation between response of KD after an initial standard dose of IVIG therapy and routine laboratory indexes till 31^st December 2017. Two reviewers independently screened literature, extracted data and assessed the risk of bias of included studies. A meta-analysis was performed by using RevMan 5.3 software.ResultsThirty studies were included. The results of meta-analysis demonstrated that the levels of hemoglobin (Hb) (SMD=–0.21, 95%CI –0.32 to –0.09, P<0.001), serum albumin (ALB) (SMD=–0.68, 95%CI –0.90 to –0.47,P<0.001) and serum sodium (SMD=–0.64, 95%CI –1.01 to –0.27,P<0.001) in IVIG non-responsiveness group were significantly lower than those in IVIG responsiveness group. The levels of alanine aminotransferase (ALT) (SMD=0.74, 95%CI 0.36 to 1.13,P<0.001), aspartate aminotransferase (AST) (SMD=0.61, 95%CI 0.24 to 0.99,P=0.001) and C-reactive protein (CRP) (SMD=0.63, 95%CI 0.38 to 0.87, P<0.001) in IVIG non-responsiveness group were higher than those in the IVIG responsiveness group.ConclusionThe current evidence shows that low levels of Hb, ALB and serum sodium and high levels of CRP, ALT, and AST are risk factors of IVIG non- responsiveness in KD. Due to limited quality and quantity of included studies, more high-quality studies are needed to verify the conclusion.

Citation： LIU Zhuoxun, WEN Xiaoying, ZHENG Yanxia, XU Youjia, YANG Jinghua. Correlation between response of Kawasaki disease after initial standard dose of intravenous immunoglobulin therapy and routine laboratory indexes: a meta-analysis. Chinese Journal of Evidence-Based Medicine, 2018, 18(4): 347-353. doi: 10.7507/1672-2531.201703037 Copy

1.	Newburger JW, Takahashi M, Gerber MA, et al. 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. Circulation, 2004, 110(17): 2747-2771.
2.	Oates-Whitehead RM, Baumer JH, Haines L, et al. Intravenous immunoglobulin for the treatment of Kawasaki disease in children. Cochrane Database Syst Rev, 2003, (4): CD004000.
3.	Tacke CE, Burgner D, Kuipers IM, et al. Management of acute and refractory Kawasaki disease. Expert Rev Anti Infect Ther, 2012, 10(10): 1203-1215.
4.	Baek JY, Song MS. Meta-analysis of factors predicting resistance to intravenous immunoglobulin treatment in patients with Kawasaki disease. Korean J Pediatr, 2016, 59(2): 80-90.
5.	Wells GA, Shea B, O’Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa, Ontario: The Ottawa Hospital, 2012, Available at: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.
6.	Park HM, Lee DW, Hyun MC, et al. Predictors of nonresponse to intravenous immunoglobulin therapy in Kawasaki disease. Korean J Pediatr, 2013, 56(2): 75-79.
7.	Cho KH, Kang SJ. Clinically useful predictors of resistance to intravenous immunoglobulin and prognosis of coronary artery lesions in patients with incomplete Kawasaki disease. Korean Circ J, 2014, 44(5): 328-335.
8.	Do YS, Kim KW, Chun JK, et al. Predicting factors for refractory Kawasaki disease. Korean Circ J, 2010, 40(5): 239-242.
9.	Cha S, Yoon M, Ahn Y, et al. Risk factors for failure of initial intravenous immunoglobulin treatment in Kawasaki disease. J Korean Med Sci, 2008, 23(4): 718-722.
10.	Song D, Yeo Y, Ha K, et al. Risk factors for Kawasaki disease-associated coronary abnormalities differ depending on age. Eur J Pediatr, 2009, 168(11): 1315-1321.
11.	Lee SM, Lee JB, Go YB, et al. Prediction of resistance to standard intravenous immunoglobulin therapy in kawasaki disease. Korean Circ J, 2014, 44(6): 415-422.
12.	Kim HK, Oh J, Hong YM, et al. Parameters to guide retreatment after initial intravenous immunoglobulin therapy in kawasaki disease. Korean Circ J, 2011, 41(7): 379-384.
13.	Yi DY, Kim JY, Choi EY, et al. Hepatobiliary risk factors for clinical outcome of Kawasaki disease in children. BMC Pediatr, 2014, 14: 51.
14.	Kim BY, Kim D, Kim YH, et al. Non-responders to intravenous immunoglobulin and coronary artery dilatation in Kawasaki disease: predictive parameters in Korean children. Korean Circ J, 2016, 46(4): 542-549.
15.	Lee HY, Song MS. Predictive factors of resistance to intravenous immunoglobulin and coronary artery lesions in Kawasaki disease. Korean J Pediatr, 2016, 59(12): 477-482.
16.	Downie ML, Manlhiot C, Latino GA, et al. Variability in response to intravenous immunoglobulin in the treatment of Kawasaki disease. J Pediatr, 2016, 179: 124-130.
17.	Loomba RS, Raskin A, Gudausky TM, et al. Role of the Egami score in predicting intravenous immunoglobulin resistance in Kawasaki disease among different Ethnicities. Am J Ther, 2016, 23(6): e1293-e1299.
18.	Tremoulet AH, Best BM, Song S, et al. Resistance to intravenous immunoglobulin in children with Kawasaki disease. J Pediatr, 2008, 153(1): 117-121.
19.	Egami K, Muta H, Ishii M, et al. Prediction of resistance to intravenous immunoglobulin treatment in patients with Kawasaki disease. J Pediatr, 2006, 149(2): 237-240.
20.	Tajima M, Shiozawa Y, Kagawa J. Early appearance of principal symptoms of Kawasaki disease is a risk factor for intravenous immunoglobulin resistance. Pediatr Cardiol, 2015, 36(6): 1159-1165.
21.	Yamamoto N, Sato K, Hoshina T, et al. Utility of ferritin as a predictor of the patients with Kawasaki disease refractory to intravenous immunoglobulin therapy. Mod Rheumatol, 2015, 25(6): 898-902.
22.	Hirabayashi Y, Takahashi Y, Xu Y, et al. Lack of CD4⁺CD25⁺FOXP3⁺ regulatory T cells is associated with resistance to intravenous immunoglobulin therapy in patients with Kawasaki disease. Eur J Pediatr, 2013, 172(6): 833-837.
23.	Sato S, Kawashima H, Kashiwagi Y, et al. Inflammatory cytokines as predictors of resistance to intravenous immunoglobulin therapy in Kawasaki disease patients. Int J Rheum Dis, 2013, 16(2): 168-172.
24.	Yoshimura K, Kimata T, Mine K, et al. N-terminal pro-brain natriuretic peptide and risk of coronary artery lesions and resistance to intravenous immunoglobulin in Kawasaki disease. J Pediatr, 2013, 162(6): 1205-1209.
25.	Wakiguchi H, Hasegawa S, Suzuki Y, et al. Relationship between t-cell HLA-DR expression and intravenous immunoglobulin treatment response in Kawasaki disease. Pediatr Res, 2015, 77(4): 536-540.
26.	刘凡, 丁艳, 尹薇. 对静脉注射丙种球蛋白无反应型川崎病临床分析. 实用儿科临床杂志, 2012, 27(21): 1670-1671.
27.	汪芸, 石琳, 马官福, 等. 丙种球蛋白无反应型川崎病患儿肿瘤坏死因子-α、可溶性肿瘤坏死因子受体-1 检测的意义. 中华实用儿科临床杂志, 2014, 29(21): 1635-1639.
28.	Weng KP, Hsieh KS, Ho TY, et al. IL-1B polymorphism in association with initial intravenous immunoglobulin treatment failure in Taiwanese children with Kawasaki disease. Circ J, 2010, 74(3): 544-551.
29.	Kuo HC, Liang CD, Wang CL, et al. Serum albumin level predicts initial intravenous immunoglobulin treatment failure in Kawasaki disease. Acta Paediatr, 2010, 99(10): 1578-1583.
30.	Kuo HC, Yang KD, Liang CD, et al. The relationship of eosinophilia to intravenous immunoglobulin treatment failure in Kawasaki disease. Pediatr Allergy Immunol, 2007, 18(4): 354-359.
31.	Ou-Yang MC, Kuo HC, Lin IC, et al. Plasma clusterin concentrations may predict resistance to intravenous immunoglobulin in patients with Kawasaki disease. Scientific World Journal, 2013, 7(15): 1-5.
32.	Song R, Yao W, Li X. Efficacy of four scoring systems in predicting intravenous immunoglobulin resistance in children with kawasaki disease in a children's hospital in Beijing, north China. J Pediatr, 2016, 184: 120-124.
33.	陈妙月, 吴素玲, 薛功寿. 丙种球蛋白无反应型川崎病的临床特点和治疗. 中华全科医学, 2017, 15(5): 814-816.
34.	Sittiwangkul R, Pongprot Y, Silvilairat S, et al. Management and outcome of intravenous gammaglobulin-resistant Kawasaki disease. Singapore Med J, 2006, 47(9): 780-784.
35.	Durongpisitkul K, Soongswang J, Laohaprasitiporn D, et al. Immunoglobulin failure and retreatment in Kawasaki disease. Pediatr Cardiol, 2003, 24(2): 145-148.
36.	张永兰, 杜忠东, 付培培. 不同剂量静脉丙种球蛋白或加甲泼尼龙治疗无反应川崎病患儿疗效观察. 中国循证儿科杂志, 2013, 8(3): 220-223.
37.	蒋勇, 赵梦, 李维禧, 等. 初始剂量静脉用丙种球蛋白治疗无反应川崎病的临床特征和预测指标. 中华实用儿科临床杂志, 2015, 30(9): 676-680.
38.	Honkanen VE, McCrindle BW, Laxer RM, et al. Clinical relevance of the risk factors for coronary artery inflammation in Kawasaki disease. Pediatr Cardiol. 2003, 24(2):122-126.
39.	Nakagama Y, Inuzuka R, Hayashi T, et al. Fever pattern and C-reactive protein predict response to rescue therapy in Kawasaki disease. Pediatr Int, 2016, 58(3): 180-184.
40.	Eladawy M, Dominguez SR, Anderson MS, et al. Abnormal liver panel in acute Kawasaki disease. Pediatr Infect Dis J. 2011, 30(2): 141-144.
41.	Yasukawa K, Terai M, Shulman ST, et al. Systemic production of vascular endothelial growth factor and fms-like tyrosine kinase-1 receptor in acute Kawasaki disease. Circulation, 2002, 105(6): 766-769.
42.	Kim JJ, Hong YM, Yun SW, et al. Assessment of risk factors for Korean children with Kawasaki disease. Pediatr Cardiol, 2012, 33(4): 513-520.
43.	Liu L, Yin W, Wang R, et al. The prognostic role of abnormal liver function in IVIG unresponsiveness in Kawasaki disease: a meta-analysis. Inflamm Res, 2016, 65(2): 161-168.
44.	Nakamura Y, Yashiro M, Uehara R, et al. Use of laboratory data to identify risk factors of giant coronary aneurysms due to Kawasaki disease. Pediatr Int, 2004, 46(1): 33-38.

1. Newburger JW, Takahashi M, Gerber MA, et al. 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. Circulation, 2004, 110(17): 2747-2771.
2. Oates-Whitehead RM, Baumer JH, Haines L, et al. Intravenous immunoglobulin for the treatment of Kawasaki disease in children. Cochrane Database Syst Rev, 2003, (4): CD004000.
3. Tacke CE, Burgner D, Kuipers IM, et al. Management of acute and refractory Kawasaki disease. Expert Rev Anti Infect Ther, 2012, 10(10): 1203-1215.
4. Baek JY, Song MS. Meta-analysis of factors predicting resistance to intravenous immunoglobulin treatment in patients with Kawasaki disease. Korean J Pediatr, 2016, 59(2): 80-90.
5. Wells GA, Shea B, O’Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa, Ontario: The Ottawa Hospital, 2012, Available at: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.
6. Park HM, Lee DW, Hyun MC, et al. Predictors of nonresponse to intravenous immunoglobulin therapy in Kawasaki disease. Korean J Pediatr, 2013, 56(2): 75-79.
7. Cho KH, Kang SJ. Clinically useful predictors of resistance to intravenous immunoglobulin and prognosis of coronary artery lesions in patients with incomplete Kawasaki disease. Korean Circ J, 2014, 44(5): 328-335.
8. Do YS, Kim KW, Chun JK, et al. Predicting factors for refractory Kawasaki disease. Korean Circ J, 2010, 40(5): 239-242.
9. Cha S, Yoon M, Ahn Y, et al. Risk factors for failure of initial intravenous immunoglobulin treatment in Kawasaki disease. J Korean Med Sci, 2008, 23(4): 718-722.
10. Song D, Yeo Y, Ha K, et al. Risk factors for Kawasaki disease-associated coronary abnormalities differ depending on age. Eur J Pediatr, 2009, 168(11): 1315-1321.
11. Lee SM, Lee JB, Go YB, et al. Prediction of resistance to standard intravenous immunoglobulin therapy in kawasaki disease. Korean Circ J, 2014, 44(6): 415-422.
12. Kim HK, Oh J, Hong YM, et al. Parameters to guide retreatment after initial intravenous immunoglobulin therapy in kawasaki disease. Korean Circ J, 2011, 41(7): 379-384.
13. Yi DY, Kim JY, Choi EY, et al. Hepatobiliary risk factors for clinical outcome of Kawasaki disease in children. BMC Pediatr, 2014, 14: 51.
14. Kim BY, Kim D, Kim YH, et al. Non-responders to intravenous immunoglobulin and coronary artery dilatation in Kawasaki disease: predictive parameters in Korean children. Korean Circ J, 2016, 46(4): 542-549.
15. Lee HY, Song MS. Predictive factors of resistance to intravenous immunoglobulin and coronary artery lesions in Kawasaki disease. Korean J Pediatr, 2016, 59(12): 477-482.
16. Downie ML, Manlhiot C, Latino GA, et al. Variability in response to intravenous immunoglobulin in the treatment of Kawasaki disease. J Pediatr, 2016, 179: 124-130.
17. Loomba RS, Raskin A, Gudausky TM, et al. Role of the Egami score in predicting intravenous immunoglobulin resistance in Kawasaki disease among different Ethnicities. Am J Ther, 2016, 23(6): e1293-e1299.
18. Tremoulet AH, Best BM, Song S, et al. Resistance to intravenous immunoglobulin in children with Kawasaki disease. J Pediatr, 2008, 153(1): 117-121.
19. Egami K, Muta H, Ishii M, et al. Prediction of resistance to intravenous immunoglobulin treatment in patients with Kawasaki disease. J Pediatr, 2006, 149(2): 237-240.
20. Tajima M, Shiozawa Y, Kagawa J. Early appearance of principal symptoms of Kawasaki disease is a risk factor for intravenous immunoglobulin resistance. Pediatr Cardiol, 2015, 36(6): 1159-1165.
21. Yamamoto N, Sato K, Hoshina T, et al. Utility of ferritin as a predictor of the patients with Kawasaki disease refractory to intravenous immunoglobulin therapy. Mod Rheumatol, 2015, 25(6): 898-902.
22. Hirabayashi Y, Takahashi Y, Xu Y, et al. Lack of CD4⁺CD25⁺FOXP3⁺ regulatory T cells is associated with resistance to intravenous immunoglobulin therapy in patients with Kawasaki disease. Eur J Pediatr, 2013, 172(6): 833-837.
23. Sato S, Kawashima H, Kashiwagi Y, et al. Inflammatory cytokines as predictors of resistance to intravenous immunoglobulin therapy in Kawasaki disease patients. Int J Rheum Dis, 2013, 16(2): 168-172.
24. Yoshimura K, Kimata T, Mine K, et al. N-terminal pro-brain natriuretic peptide and risk of coronary artery lesions and resistance to intravenous immunoglobulin in Kawasaki disease. J Pediatr, 2013, 162(6): 1205-1209.
25. Wakiguchi H, Hasegawa S, Suzuki Y, et al. Relationship between t-cell HLA-DR expression and intravenous immunoglobulin treatment response in Kawasaki disease. Pediatr Res, 2015, 77(4): 536-540.
26. 刘凡, 丁艳, 尹薇. 对静脉注射丙种球蛋白无反应型川崎病临床分析. 实用儿科临床杂志, 2012, 27(21): 1670-1671.
27. 汪芸, 石琳, 马官福, 等. 丙种球蛋白无反应型川崎病患儿肿瘤坏死因子-α、可溶性肿瘤坏死因子受体-1 检测的意义. 中华实用儿科临床杂志, 2014, 29(21): 1635-1639.
28. Weng KP, Hsieh KS, Ho TY, et al. IL-1B polymorphism in association with initial intravenous immunoglobulin treatment failure in Taiwanese children with Kawasaki disease. Circ J, 2010, 74(3): 544-551.
29. Kuo HC, Liang CD, Wang CL, et al. Serum albumin level predicts initial intravenous immunoglobulin treatment failure in Kawasaki disease. Acta Paediatr, 2010, 99(10): 1578-1583.
30. Kuo HC, Yang KD, Liang CD, et al. The relationship of eosinophilia to intravenous immunoglobulin treatment failure in Kawasaki disease. Pediatr Allergy Immunol, 2007, 18(4): 354-359.
31. Ou-Yang MC, Kuo HC, Lin IC, et al. Plasma clusterin concentrations may predict resistance to intravenous immunoglobulin in patients with Kawasaki disease. Scientific World Journal, 2013, 7(15): 1-5.
32. Song R, Yao W, Li X. Efficacy of four scoring systems in predicting intravenous immunoglobulin resistance in children with kawasaki disease in a children's hospital in Beijing, north China. J Pediatr, 2016, 184: 120-124.
33. 陈妙月, 吴素玲, 薛功寿. 丙种球蛋白无反应型川崎病的临床特点和治疗. 中华全科医学, 2017, 15(5): 814-816.
34. Sittiwangkul R, Pongprot Y, Silvilairat S, et al. Management and outcome of intravenous gammaglobulin-resistant Kawasaki disease. Singapore Med J, 2006, 47(9): 780-784.
35. Durongpisitkul K, Soongswang J, Laohaprasitiporn D, et al. Immunoglobulin failure and retreatment in Kawasaki disease. Pediatr Cardiol, 2003, 24(2): 145-148.
36. 张永兰, 杜忠东, 付培培. 不同剂量静脉丙种球蛋白或加甲泼尼龙治疗无反应川崎病患儿疗效观察. 中国循证儿科杂志, 2013, 8(3): 220-223.
37. 蒋勇, 赵梦, 李维禧, 等. 初始剂量静脉用丙种球蛋白治疗无反应川崎病的临床特征和预测指标. 中华实用儿科临床杂志, 2015, 30(9): 676-680.
38. Honkanen VE, McCrindle BW, Laxer RM, et al. Clinical relevance of the risk factors for coronary artery inflammation in Kawasaki disease. Pediatr Cardiol. 2003, 24(2):122-126.
39. Nakagama Y, Inuzuka R, Hayashi T, et al. Fever pattern and C-reactive protein predict response to rescue therapy in Kawasaki disease. Pediatr Int, 2016, 58(3): 180-184.
40. Eladawy M, Dominguez SR, Anderson MS, et al. Abnormal liver panel in acute Kawasaki disease. Pediatr Infect Dis J. 2011, 30(2): 141-144.
41. Yasukawa K, Terai M, Shulman ST, et al. Systemic production of vascular endothelial growth factor and fms-like tyrosine kinase-1 receptor in acute Kawasaki disease. Circulation, 2002, 105(6): 766-769.
42. Kim JJ, Hong YM, Yun SW, et al. Assessment of risk factors for Korean children with Kawasaki disease. Pediatr Cardiol, 2012, 33(4): 513-520.
43. Liu L, Yin W, Wang R, et al. The prognostic role of abnormal liver function in IVIG unresponsiveness in Kawasaki disease: a meta-analysis. Inflamm Res, 2016, 65(2): 161-168.
44. Nakamura Y, Yashiro M, Uehara R, et al. Use of laboratory data to identify risk factors of giant coronary aneurysms due to Kawasaki disease. Pediatr Int, 2004, 46(1): 33-38.

Chinese Journal of Evidence-Based Medicine

Correlation between response of Kawasaki disease after initial standard dose of intravenous immunoglobulin therapy and routine laboratory indexes: a meta-analysis

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