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200779372.Pdf PDF hosted at the Radboud Repository of the Radboud University Nijmegen The following full text is a publisher's version. For additional information about this publication click this link. http://hdl.handle.net/2066/200115 Please be advised that this information was generated on 2019-06-02 and may be subject to change. fmicb-09-02434 October 12, 2018 Time: 16:44 # 1 REVIEW published: 12 October 2018 doi: 10.3389/fmicb.2018.02434 Frequency and Geographic Distribution of CARD9 Mutations in Patients With Severe Fungal Infections Afsane Vaezi1, Hamed Fakhim2,3, Zahra Abtahian4, Sadegh Khodavaisy5, Mohsen Geramishoar5, Ahad Alizadeh6, Jacques F. Meis7,8 and Hamid Badali1,9* 1 Department of Medical Mycology, School of Medicine, Mazandaran University of Medical Sciences, Sari, Iran, 2 Department of Medical Parasitology and Mycology, Faculty of Medicine, Urmia University of Medical Sciences, Urmia, Iran, 3 Cellular and Molecular Research Center, Urmia University of Medical Sciences, Urmia, Iran, 4 Infectious Disease and Tropical Medicine Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran, 5 Department of Medical Parasitology and Mycology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran, 6 Department of Epidemiology and Reproductive Health, Reproductive Epidemiology Research Center, Royan Institute for Reproductive Biomedicine, Academic Center for Education, Culture and Research, Tehran, Iran, 7 Department of Medical Microbiology Edited by: and Infectious Diseases, ECMM Excellence Center for Medical Mycology, Canisius-Wilhelmina Hospital, Nijmegen, Martin Hoenigl, Netherlands, 8 Centre of Expertise in Mycology Radboudumc/CWZ, Nijmegen, Netherlands, 9 Invasive Fungi Research University of California, San Diego, Center, School of Medicine, Mazandaran University of Medical Sciences, Sari, Iran United States Reviewed by: Aleksandra Barac, Autosomal recessive deficiency in the caspase recruitment domain containing protein University of Belgrade, Serbia 9 (CARD9) results in susceptibility to fungal infections. In the last decade, infections Danila Seidel, associated with CARD9 deficiency are more reported due to the advent of genome Uniklinik Köln, Germany sequencing. The aim of this study was to evaluate the frequency, geographic distribution *Correspondence: Hamid Badali and nature of mutations in patients with CARD9 deficiency. We identified 60 patients badalii@yahoo.com with 24 mutations and different fungal infections. The presence of the homozygous Specialty section: (HMZ) p.Q295X (c.883C > T) and HMZ p.Q289X (c.865C > T) mutations were This article was submitted to associated with an elevated risk of candidiasis (OR: 1.6; 95% CI: 1.18–2.15; p = 0.004) Fungi and Their Interactions, and dermatophytosis (OR: 1.85; 95% CI: 1.47–2.37; p < 0.001), respectively. The a section of the journal Frontiers in Microbiology geographical distribution differed, showing that the main mutations in African patients Received: 11 July 2018 were different Asian patients; HMZ p.Q289X (c.865C > T) and HMZ p.Q295X Accepted: 24 September 2018 (c.865C > T) accounted for 75% and 37.9% of the African and Asian cases, respectively. Published: 12 October 2018 The spectrum of CARD9 mutations in Asian patients was higher than in African. Asia Citation: Vaezi A, Fakhim H, Abtahian Z, is the most populous continent in the world and may have a greater genetic burden Khodavaisy S, Geramishoar M resulting in more patients with severe fungal infections. The presence of a high diversity Alizadeh A, Meis JF and Badali H of mutations revealing 24 distinct variations among 60 patients emphasize that the (2018) Frequency and Geographic Distribution of CARD9 Mutations unique genetic alteration in CARD9 gene may be associated with certain geographical in Patients With Severe Fungal areas. Infections. Front. Microbiol. 9:2434. doi: 10.3389/fmicb.2018.02434 Keywords: severe fungal infections, CARD9 deficiency, mutation, candidiasis, dermatophytosis Frontiers in Microbiology| www.frontiersin.org 1 October 2018| Volume 9| Article 2434 fmicb-09-02434 October 12, 2018 Time: 16:44 # 2 Vaezi et al. Frequency and Geographic Distribution of CARD9 Mutations INTRODUCTION A total of 21 relevant articles were found using these key words. The extracted data were analyzed using R software version Susceptibility to fungal infections in otherwise healthy 3.4.1. The chi-square test was utilized to evaluate associations individuals with Mendelian disorders are increasingly being between nominal variables and the p-value was estimated recognized (Vinh, 2011) than before the widespread use of using the Monte Carlo method. To compare the differential genome sequencing. Primary immunodeficiencies consist of prevalence of CARD9 mutations and determine differences various genetic defects that affect the innate and adaptive in causative agents of fungal infections, odds ratios (ORs) immune systems. In addition, evaluation of previously healthy, were used. The significance of all ORs, using a 95% Bayesian fungus infected patients, suspected of having a primary genetic credible interval (CI), was calculated using Bayesian logistic immunodeficiency may give valuable insights on the role of regression. specific proteins in the immune system for protection from these infections (Wang et al., 2014; Corvilain et al., 2018). Caspase recruitment domain containing protein 9 (CARD9) is RESULTS a central regulator of innate immunity that is highly expressed in neutrophils, macrophages, dendritic cells, and during cell The Burden of CARD9 Deficiency Is apoptosis in low-serum conditions (Bertin et al., 2000; Liang Positively Correlated With Fungal et al., 2015). Mutations in several proteins involved in the Infection CARD9 signaling protein have been demonstrated to cause To analyze the role of CARD9 deficiency in fungal infection, primary immunodeficiencies in humans. These mutations cause we reviewed the literature and identified 60 cases until 2018. a decreased production of cytokines from innate immune cells, The total number of patients with severe fungal infection related leading to deficiencies of TH17 and accordingly predispose to CARD9 deficiency has been summarized in Tables 1A,B patients to severe disseminated infections (Conti and Gaffen, (Boudghène-Stambouli and Mérad-Boudia, 1989, 1991, 1998; 2015). Severe fungal infections in healthy patients have recently Pruszkowski et al., 1995; Glocker et al., 2009; Drewniak et al., been reported from a few countries, i.e., Algeria, Brazil, France, 2013; Gavino et al., 2014; Wang et al., 2014; Drummond China, Iran, Morocco and Tunisia (Glocker et al., 2009; et al., 2015; Grumach et al., 2015; Herbst et al., 2015; Jachiet Drewniak et al., 2013; Lanternier et al., 2013; Wang et al., et al., 2015; Lanternier et al., 2015a,b; Alves de Medeiros 2014; Grumach et al., 2015) and linked to autosomal recessive et al., 2016; Gavino et al., 2016; Jones et al., 2016; Rieber CARD9 deficiency. The species involved in these infections et al., 2016; Yan et al., 2016; Boudghene-Stambouli et al., are Trichophyton violaceum, Trichophyton rubrum, Candida 2017; Gavino et al., 2018; Sari et al., 2018; Vaezi et al., 2018; species, Exophiala species, Phialophora verrucosa, Aspergillus Wang et al., 2018a,b). The age at the time of diagnosis ranged fumigatus, Prototheca zopfii, and Mucor irregularis. Some of from 4 to 91 years (mean 34.3 ± 17.9 years). Since 1989, those etiological agents are plant pathogens, which rarely a total of 14 countries reported cases of fungal infections have been associated with human infection. Highly diverse associated with CARD9 deficiency (Figure 1). Although most clinical manifestations from cutaneous to disseminated and cases originate from Algeria (North Africa) [n = 12 (21.1%)], progressive infections are observed (Boudghène-Stambouli the majority of cases were from several countries in the Asian and Mérad-Boudia, 1991; Boudghène-Stambouli et al., 1992; continent (n = 29, 48.3%), with Iran reporting the majority Pruszkowski et al., 1995). Our aim was to evaluate the global (n = 10/29, 34.5%). The main fungal infection associated frequency, geographic distribution and nature of mutations with CARD9 deficiency was candidiasis (40.3%) followed by in patients with CARD9 deficiency associated with fungal deep dermatophytosis (37.3%), phaeohyphomycosis (16.4%) infections. and invasive aspergillosis (3.0%). T. violaceum, T. rubrum, and Trichophyton mentagrophytes were observed as etiological agents of dermatophytosis. Candida infections were caused MATERIALS AND METHODS by C. albicans and non-albicans Candida species in 70.8% and 29.2% of the cases, respectively. P. verrucosa (36.4%) The review process involved study of existing published represented the major species of phaeohyphomycosis and were literature of all reported cases with fungal infection due only reported from China. Neurological infection (40.5%) was to CARD9 deficiency. To search the published literature, the predominant clinical presentation in Candida infected Medline database through PubMed, Embase through patients followed by chronic mucosal and cutaneous candidiasis Scopus, ISI Web of Science, Science Direct and Google (29.7%). The outcome was recorded in 45 cases and 11 (24.4%) Scholar were used to explore the published literature expired. of patients with severe fungal infection and CARD9 deficiency using the key words “caspase recruitment domain Associations Among Mutations of the deficiency,” “CARD9 deficiency,” “autosomal recessive CARD9 deficiency,” “primary
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