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The use of neutrophil–lymphocyte ratio for the prediction of refractory disease and coronary artery lesions in patients with Kawasaki disease

Published online by Cambridge University Press:  04 April 2023

Juan S. Farias*
Affiliation:
Tecnologico de Monterrey, Escuela de Medicina y Ciencias de la Salud, Monterrey, Nuevo Leon, Mexico
Enrique G. Villarreal
Affiliation:
Tecnologico de Monterrey, Escuela de Medicina y Ciencias de la Salud, Monterrey, Nuevo Leon, Mexico
Fabio Savorgnan
Affiliation:
Section of Critical Care Medicine and Cardiology, Texas Children’s Hospital, Houston, TX, USA Department of Pediatrics, Baylor College of Medicine, Houston, TX, USA
Sebastian Acosta
Affiliation:
Section of Critical Care Medicine and Cardiology, Texas Children’s Hospital, Houston, TX, USA Department of Pediatrics, Baylor College of Medicine, Houston, TX, USA
Saul Flores
Affiliation:
Section of Critical Care Medicine and Cardiology, Texas Children’s Hospital, Houston, TX, USA Department of Pediatrics, Baylor College of Medicine, Houston, TX, USA
Rohit S. Loomba
Affiliation:
Division of Pediatric Cardiac Critical Care, Advocate Children’s Hospital, Oak Lawn, IL, USA Department of Pediatrics, Chicago Medical School/Rosalind Franklin University of Medicine and Science, Chicago, IL, USA
*
Author for correspondence: Juan S. Farias, MD, Tecnologico de Monterrey, Escuela de Medicina y Ciencias de la Salud, Av. Morones Prieto 3000, Colonia Los Doctores, 64710, Monterrey, Nuevo Leon, Mexico. Tel: +52 81 1588 8197. E-mail: jsfariast@gmail.com

Abstract

Background:

Kawasaki disease is a vasculitis that can lead to cardiac complications, including coronary artery disease and cardiogenic shock. Various scoring systems have been developed to determine those that will be refractory to routine intravenous immunoglobulin therapy or develop coronary artery disease. The objective of this study was to determine if the neutrophil–lymphocyte ratio could predict refractory disease and coronary artery lesions in patients with Kawasaki disease.

Methods:

A systematic review of the literature was performed to identify manuscripts describing comparisons of neutrophil–lymphocyte ratio between those who had refractory disease and those who did not, and between those who developed coronary artery lesions and those who did not. Mean difference was compared between groups. Areas under the curve were utilised to determine the pooled area under the curve.

Results:

12 studies with 5593 patients were included in the final analyses of neutrophil–lymphocyte ratio for the prediction of refractory disease. Neutrophil–lymphocyte ratio before therapy was higher in refractory disease with a mean difference of 2.55 (p < 0.01) and pooled area under the curve of 0.724. Neutrophil–lymphocyte ratio after therapy was higher in refractory disease with a mean difference of 1.42 (p < 0.01) and pooled area under the curve for of 0.803. Five studies with 1690 patients were included in the final analyses of neutrophil–lymphocyte ratio for the prediction of coronary artery lesions. Neutrophil–lymphocyte ratio before therapy was higher in coronary artery lesions with a mean difference of 0.65 (p < 0.01).

Conclusion:

The use of neutrophil–lymphocyte ratio may help physicians in the identification of patients at risk of refractory disease and coronary artery lesions in patients with Kawasaki disease.

Type
Review
Copyright
© The Author(s), 2023. Published by Cambridge University Press

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References

Son, MBF, Newburger, JW. Kawasaki disease. Pediatr Rev. 2018; 39: 7890. DOI 10.1542/pir.2016-0182.CrossRefGoogle ScholarPubMed
Kawasaki, T. [Acute febrile mucocutaneous syndrome with lymphoid involvement with specific desquamation of the fingers and toes in children]. Arerugi. 1967; 16: 178222.Google ScholarPubMed
Younger, DS. Epidemiology of the vasculitides. Neurol Clin 2019; 37: 201217. DOI 10.1016/j.ncl.2019.01.016.CrossRefGoogle ScholarPubMed
Uehara, R, Belay, ED. Epidemiology of Kawasaki disease in Asia, Europe, and the United States. J Epidemiol. 2012; 22: 7985. DOI 10.2188/jea.je20110131.CrossRefGoogle ScholarPubMed
Rife, E, Gedalia, A. Kawasaki disease: an update. Curr Rheumatol Rep 2020; 22: –. DOI 10.1007/s11926-020-00941-4.CrossRefGoogle ScholarPubMed
Suzuki, A, Kamiya, T, Kuwahara, N, et al. Coronary arterial lesions of Kawasaki disease: cardiac catheterization findings of 1100 cases. Pediatr Cardiol. 1986; 7: 39. DOI 10.1007/bf02315475.CrossRefGoogle ScholarPubMed
Newburger, JW, Takahashi, M, Burns, JC, et al. The treatment of Kawasaki syndrome with intravenous gamma globulin. N Engl J Med. 1986; 315: 341347. DOI 10.1056/nejm198608073150601.CrossRefGoogle ScholarPubMed
Furusho, K, Kamiya, T, Nakano, H, et al. High-dose intravenous gammaglobulin for Kawasaki disease. Lancet. 1984; 10: 10551058. DOI 10.1016/s0140-6736(84)91504-6.CrossRefGoogle Scholar
Durongpisitkul, K, Soongswang, J, Laohaprasitiporn, D, Nana, A, Prachuabmoh, C, Kangkagate, C. Immunoglobulin failure and retreatment in Kawasaki disease. Pediatr Cardiol. 2003; 24: 145148. DOI 10.1007/s00246-002-0216-2.CrossRefGoogle ScholarPubMed
Burns, JC, Capparelli, EV, Brown, JA, Newburger, JW, Glode, MP. Intravenous gamma-globulin treatment and retreatment in Kawasaki disease. US/Canadian Kawasaki syndrome study group. Pediatr Infect Dis J 1998; 17: 11441148. DOI 10.1097/00006454-199812000-00009.CrossRefGoogle ScholarPubMed
Wallace, CA, French, JW, Kahn, SJ, Sherry, DD. Initial intravenous gammaglobulin treatment failure in Kawasaki disease. Pediatrics. 2000; 105: E78e78. DOI 10.1542/peds.105.6.e78.CrossRefGoogle ScholarPubMed
Sano, T, Kurotobi, S, Matsuzaki, K, et al. Prediction of non-responsiveness to standard high-dose gamma-globulin therapy in patients with acute Kawasaki disease before starting initial treatment. Eur J Pediatr. 2006; 166: 131137. DOI 10.1007/s00431-006-0223-z.CrossRefGoogle ScholarPubMed
Mori, M, Imagawa, T, Yasui, K, Kanaya, A, Yokota, S. Predictors of coronary artery lesions after intravenous gamma-globulin treatment in Kawasaki disease. J Pediatr 2000; 137: 177180. DOI 10.1067/mpd.2000.107890.CrossRefGoogle ScholarPubMed
Fukunishi, M, Kikkawa, M, Hamana, K, et al. Prediction of non-responsiveness to intravenous high-dose gamma-globulin therapy in patients with Kawasaki disease at onset. J Pediatr 2000; 137: 172176. DOI 10.1067/mpd.2000.104815.CrossRefGoogle ScholarPubMed
Kobayashi, T, Inoue, Y, Takeuchi, K, et al. Prediction of intravenous immunoglobulin unresponsiveness in patients with Kawasaki disease. Circulation. 2006; 113: 26062612. DOI 10.1161/circulationaha.105.592865.CrossRefGoogle ScholarPubMed
Liu, HH, Chen, WX, Niu, MM, et al. A new scoring system for coronary artery abnormalities in Kawasaki disease. Pediatr Res 2021; 92: 275283. DOI 10.1038/s41390-021-01752-8.CrossRefGoogle ScholarPubMed
Egami, K, Muta, H, Ishii, M, et al. Prediction of resistance to intravenous immunoglobulin treatment in patients with Kawasaki disease. J Pediatr 2006; 149: 237240. DOI 10.1016/j.jpeds.2006.03.050.CrossRefGoogle ScholarPubMed
Sato, S, Kawashima, H, Kashiwagi, Y, Hoshika, A. Inflammatory cytokines as predictors of resistance to intravenous immunoglobulin therapy in Kawasaki disease patients. Int J Rheum Dis 2013; 16: 168172. DOI 10.1111/1756-185x.12082.CrossRefGoogle ScholarPubMed
Tremoulet, AH, Best, BM, Song, S, et al. Resistance to intravenous immunoglobulin in children with Kawasaki disease. J Pediatr. 2008; 153: 117121.e3. DOI 10.1016/j.jpeds.2007.12.021.CrossRefGoogle ScholarPubMed
Arane, K, Mendelsohn, K, Mimouni, M, et al. Japanese scoring systems to predict resistance to intravenous immunoglobulin in Kawasaki disease were unreliable for Caucasian Israeli children. Acta Paediatr 2018; 107: 21792184. DOI 10.1111/apa.14418.CrossRefGoogle ScholarPubMed
Davies, S, Sutton, N, Blackstock, S, et al. Predicting IVIG resistance in UK Kawasaki disease. Arch Dis Child 2015; 100: 366368. DOI 10.1136/archdischild-2014-307397.CrossRefGoogle ScholarPubMed
Zahorec, R. Ratio of neutrophil to lymphocyte counts--rapid and simple parameter of systemic inflammation and stress in critically ill. Bratisl Lek Listy. 2001; 102: 514.Google ScholarPubMed
Azab, B, Zaher, M, Weiserbs, KF, et al. Usefulness of neutrophil to lymphocyte ratio in predicting short- and long-term mortality after non-ST-elevation myocardial infarction. Am J Cardiol 2010; 106: 470476. DOI 10.1016/j.amjcard.2010.03.062.CrossRefGoogle Scholar
Park, JJ, Jang, HJ, Oh, IY, et al. Prognostic value of neutrophil to lymphocyte ratio in patients presenting with ST-elevation myocardial infarction undergoing primary percutaneous coronary intervention. Am J Cardiol 2013; 1: 636642. DOI 10.1016/j.amjcard.2012.11.012.CrossRefGoogle Scholar
Tang, H, Lu, W, Li, B, Li, C, Xu, Y, Dong, J. Prognostic significance of neutrophil-to-lymphocyte ratio in biliary tract cancers: a systematic review and meta-analysis. Oncotarget 2017; 8: 3685736868. DOI 10.18632/oncotarget.16143.CrossRefGoogle ScholarPubMed
Cummings, M, Merone, L, Keeble, C, et al. Preoperative neutrophil: lymphocyte and platelet: lymphocyte ratios predict endometrial cancer survival. Br J Cancer 2015; 113: 311320. DOI 10.1038/bjc.2015.200.CrossRefGoogle ScholarPubMed
Widjaja, H, Rusmawatiningtyas, D, Makrufardi, F, Arguni, E. Neutrophil lymphocyte ratio as predictor of mortality in pediatric patients with bacterial meningitis: a retrospective cohort study. Ann Med Surg (Lond). 2022; 73: 103191. DOI 10.1016/j.amsu.2021.103191.Google ScholarPubMed
Kawamura, Y, Takeshita, S, Kanai, T, Yoshida, Y, Nonoyama, S. The combined usefulness of the neutrophil-to-lymphocyte and platelet-to-lymphocyte ratios in predicting intravenous immunoglobulin resistance with Kawasaki disease. J Pediatr. 2016; 178: 281284 e1. DOI 10.1016/j.jpeds.2016.07.035.CrossRefGoogle ScholarPubMed
Ha, KS, Lee, J, Jang, GY, et al. Value of neutrophil-lymphocyte ratio in predicting outcomes in Kawasaki disease. Am J Cardiol 2015; 116: 301306. DOI 10.1016/j.amjcard.2015.04.021.CrossRefGoogle ScholarPubMed
Page, MJ, McKenzie, JE, Bossuyt, PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021, n71. DOI 10.1136/bmj.n71.CrossRefGoogle ScholarPubMed
Wells G.A., SB, O.'Connell, D, Peterson, J, Welch, V, Losos, M, Tugwell, P. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses 2020, http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.Google Scholar
Wan, X, Wang, W, Liu, J, Tong, T. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol 2014; 14: 135. DOI 10.1186/1471-2288-14-135.CrossRefGoogle ScholarPubMed
Do, Y-S, Kim, K-W, Chun, J-K, Cha, BH, Namgoong, MK, Lee, HY. Predicting factors for refractory Kawasaki disease. Korean Circ J 2010; 5: 239242.CrossRefGoogle Scholar
Lee, SM, Lee, JB, Go, YB, Song, HY, Lee, BJ, Kwak, JH. Prediction of resistance to standard intravenous immunoglobulin therapy in kawasaki disease. Korean Circ J 2014; 44: 415422. DOI 10.4070/kcj.2014.44.6.415.CrossRefGoogle ScholarPubMed
Cho, HJ, Bak, SY, Kim, SY, et al. High neutrophil : lymphocyte ratio is associated with refractory Kawasaki disease. Pediatr Int. 2017; 59: 669674. DOI 10.1111/ped.13240.CrossRefGoogle ScholarPubMed
Hua, W, Sun, Y, Wang, Y, et al. A new model to predict intravenous immunoglobin-resistant Kawasaki disease. Oncotarget. 2017; 8: 8072280729. DOI 10.18632/oncotarget.21083.CrossRefGoogle ScholarPubMed
Takeshita, S, Kanai, T, Kawamura, Y, Yoshida, Y, Nonoyama, S. A comparison of the predictive validity of the combination of the neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio and other risk scoring systems for intravenous immunoglobulin (ivig)-resistance in Kawasaki disease. PLoS One 2017; 12: e0176957. DOI 10.1371/journal.pone.0176957.CrossRefGoogle ScholarPubMed
Yuan, YD, Sun, J, Li, PF, Wei, CL, Yu, YH. Values of neutrophil-lymphocyte ratio and platelet-lymphocyte ratio in predicting sensitivity to intravenous immunoglobulin in Kawasaki disease. Zhongguo Dang Dai Er Ke Za Zhi. 2017; 19: 410413.Google ScholarPubMed
Chantasiriwan, N, Silvilairat, S, Makonkawkeyoon, K, Pongprot, Y, Sittiwangkul, R. Predictors of intravenous immunoglobulin resistance and coronary artery aneurysm in patients with Kawasaki disease. Paediatr Int Child Health 2018; 38: 209212. DOI 10.1080/20469047.2018.1471381.Google ScholarPubMed
Wu, S, Long, Y, Chen, S, et al. A new scoring system for prediction of intravenous immunoglobulin resistance of Kawasaki disease in infants under 1-year old. Front Pediatr 2019; 7: 514. DOI 10.3389/fped.2019.00514.CrossRefGoogle ScholarPubMed
Turkucar, S, Yildiz, K, Acari, C, Dundar, HA, Kir, M, Unsal, E. Risk factors of intravenous immunoglobulin resistance and coronary arterial lesions in Turkish children with Kawasaki disease. Turk J Pediatr. 2020; 62: 19. DOI 10.24953/turkjped.2020.01.001.CrossRefGoogle ScholarPubMed
Liu, X, Shao, S, Wang, L, et al. Predictive value of the systemic immune-inflammation index for intravenous immunoglobulin resistance and cardiovascular complications in Kawasaki disease. Front Cardiovasc Med 2021; 8: 711007. DOI 10.3389/fcvm.2021.711007.CrossRefGoogle ScholarPubMed
Demir, F, Karadeniz, C, Ozdemir, R, et al. Usefulness of neutrophil to lymphocyte ratio in prediction of coronary artery lesions in patients with Kawasaki disease. Balkan Med J 2015; 32: 371376. DOI 10.5152/balkanmedj.2015.151108.CrossRefGoogle ScholarPubMed
Seo, YM, Kang, HM, Lee, SC, et al. Clinical implications in laboratory parameter values in acute Kawasaki disease for early diagnosis and proper treatment. Korean J Pediatr 2018; 61: 160166. DOI 10.3345/kjp.2018.61.5.160.CrossRefGoogle ScholarPubMed
Hua, W, Ma, F, Wang, Y, et al. A new scoring system to predict Kawasaki disease with coronary artery lesions. Clin Rheumatol. 2019; 38: 10991107. DOI 10.1007/s10067-018-4393-7.CrossRefGoogle ScholarPubMed
Harada, K. Intravenous gamma-globulin treatment in Kawasaki disease. Acta Paediatr Jpn 1991; 33: 805810. DOI 10.1111/j.1442-200x.1991.tb02612.x.CrossRefGoogle ScholarPubMed
Lin, MT, Chang, CH, Sun, LC, et al. Risk factors and derived formosa score for intravenous immunoglobulin unresponsiveness in Taiwanese children with Kawasaki disease. J Formos Med Assoc 2016; 115: 350355. DOI 10.1016/j.jfma.2015.03.012.CrossRefGoogle ScholarPubMed
Tang, Y, Yan, W, Sun, L, et al. Prediction of intravenous immunoglobulin resistance in Kawasaki disease in an East China population. Clin Rheumatol 2016; 35: 27712776. DOI 10.1007/s10067-016-3370-2.CrossRefGoogle Scholar
Davies, S, Sutton, N, Blackstock, S, et al. Predicting IVIG resistance in UK Kawasaki disease. Arch Dis Childhood. 2015; 100: 366368.CrossRefGoogle ScholarPubMed
Danesh, J, Collins, R, Appleby, P, Peto, R. Association of fibrinogen, C-reactive protein, albumin, or leukocyte count with coronary heart disease: meta-analyses of prospective studies. JAMA 1998; 279: 14771482. DOI 10.1001/jama.279.18.1477.CrossRefGoogle ScholarPubMed
Ates, AH, Canpolat, U, Yorgun, H, et al. Total white blood cell count is associated with the presence, severity and extent of coronary atherosclerosis detected by dual-source multislice computed tomographic coronary angiography. Cardiol J. 2011; 18: 371377.Google ScholarPubMed
Whittaker, E, Bamford, A, Kenny, J, et al. Clinical characteristics of 58 children with a pediatric inflammatory multisystem syndrome temporally associated with SARS-CoV-2. JAMA. 2020; 324: 259269. DOI 10.1001/jama.2020.10369.CrossRefGoogle ScholarPubMed
Abrams, JY, Oster, ME, Godfred-Cato, SE, et al. Factors linked to severe outcomes in multisystem inflammatory syndrome in children (MIS-C) in the USA: a retrospective surveillance study. Lancet Child Adolesc Health 2021; 5: 323331. DOI 10.1016/s2352-4642(21)00050-x.CrossRefGoogle Scholar
Matsubara, T, Ichiyama, T, Furukawa, S. Immunological profile of peripheral blood lymphocytes and monocytes/macrophages in Kawasaki disease. Clin Exp Immunol 2005; 141: 381387. DOI 10.1111/j.1365-2249.2005.02821.x.CrossRefGoogle ScholarPubMed
Rowley, AH. Multisystem inflammatory syndrome in children and Kawasaki disease: two different illnesses with overlapping clinical features. J Pediatr. 2020; 224: 129132. DOI 10.1016/j.jpeds.2020.06.057.CrossRefGoogle ScholarPubMed
Cem, E, Böncüoğlu, E, Kıymet, E, et al. Which findings make multisystem inflammatory syndrome in children different from the pre-pandemic Kawasaki disease? Pediatr Cardiol. 2023; 44: 424432. DOI 10.1007/s00246-022-02961-6.CrossRefGoogle ScholarPubMed
Bar-Meir, M, Guri, A, Godfrey, ME, et al. Characterizing the differences between multisystem inflammatory syndrome in children and Kawasaki disease. Sci Rep UK 2021; 11: 10.1038/s41598–021-93389-0.CrossRefGoogle Scholar
Godfred-Cato, S, Abrams, JY, Balachandran, N, et al. Distinguishing multisystem inflammatory syndrome in children from COVID-19, Kawasaki disease and toxic shock syndrome. Pediatr Infect Dis J. 2022; 41: 315323. DOI 10.1097/inf.0000000000003449.CrossRefGoogle ScholarPubMed
Tremoulet, AH, Jain, S, Chandrasekar, D, Sun, X, Sato, Y, Burns, JC. Evolution of laboratory values in patients with Kawasaki disease. Pediatr Infect Dis J. 2011; 30: 10221026. DOI 10.1097/inf.0b013e31822d4f56.CrossRefGoogle ScholarPubMed
Noval Rivas, M, Arditi, M. Kawasaki disease: pathophysiology and insights from mouse models. Nat Rev Rheumatol. 2020; 16: 391405. DOI 10.1038/s41584-020-0426-0.CrossRefGoogle ScholarPubMed
Orenstein, JM, Shulman, ST, Fox, LM, et al. Three linked vasculopathic processes characterize Kawasaki disease: a light and transmission electron microscopic study. PLoS ONE 2012; 7: e38998. DOI 10.1371/journal.pone.0038998.CrossRefGoogle ScholarPubMed
Kim, T, Choi, W, Woo, C-W, et al. Predictive risk factors for coronary artery abnormalities in Kawasaki disease. Eur J Pediatr. 2007; 166: 421425. DOI 10.1007/s00431-006-0251-8.CrossRefGoogle ScholarPubMed
Wu, G, Yue, P, Ma, F, Zhang, Y, Zheng, X, Li, Y. Neutrophil-to-lymphocyte ratio as a biomarker for predicting the intravenous immunoglobulin-resistant Kawasaki disease. Medicine (Baltimore) 2020; 99: e18535. DOI 10.1097/md.0000000000018535.CrossRefGoogle ScholarPubMed