Inborn errors of immunity and invasive fungal infections: presentation and management.


Journal

Current opinion in infectious diseases
ISSN: 1473-6527
Titre abrégé: Curr Opin Infect Dis
Pays: United States
ID NLM: 8809878

Informations de publication

Date de publication:
04 Sep 2024
Historique:
medline: 11 9 2024
pubmed: 11 9 2024
entrez: 11 9 2024
Statut: aheadofprint

Résumé

We review the clinical presentations of invasive fungal infections in a selection of inborn errors of immunity. In addition, we review the particularities of their management, including antifungal therapy, prophylaxis, and immunomodulatory treatments. Patients with chronic granulomatous disease and with signal transducer and activator of transcription 3 (STAT3) deficiency are particularly prone to aspergillosis. Mold-active antifungal prophylaxis should be prescribed to all patients with chronic granulomatous disease, and in patients with STAT3 deficiency and underlying parenchymal lung disease. Invasive fungal infections are rare in patients with STAT1 gain-of-function mutations, while the clinical phenotype of caspase-associated recruitment domain-containing protein 9 deficiency encompasses a wide range of superficial and invasive fungal infections. Most patients with inborn errors of immunity and invasive fungal infections require prolonged durations of antifungals. Hematopoietic stem cell transplantation should be considered early for patients with chronic granulomatous disease, but results have been more mixed for other inborn errors of immunity with active invasive fungal infections. Inborn errors of immunity can confer increased susceptibility to a variety of invasive fungal infections, which can present with specific clinical and radiological features. Management of fungal infections in these patients is often challenging, and relies on a combination of antimicrobial prophylaxis, antifungal treatments, and immunomodulation.

Identifiants

pubmed: 39259685
doi: 10.1097/QCO.0000000000001062
pii: 00001432-990000000-00183
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024 Wolters Kluwer Health, Inc. All rights reserved.

Références

Seidel MG, Kindle G, Gathmann B, et al. The European Society for Immunodeficiencies (ESID) registry working definitions for the clinical diagnosis of inborn errors of immunity. J Allergy Clin Immunol Pract 2019; 7:1763–1770.
Lionakis MS, Drummond RA, Hohl TM. Immune responses to human fungal pathogens and therapeutic prospects. Nat Rev Immunol 2023; 23:433–452.
Cifaldi C, Ursu GM, D’Alba I, et al. Main human inborn errors of immunity leading to fungal infections. Clin Microbiol Infect 2022; 28:1435–1440.
Winkelstein JA, Marino MC, Johnston RB, et al. Chronic granulomatous disease. Report on a national registry of 368 patients. Medicine (Baltimore) 2000; 79:155–169.
Chiriaco M, Salfa I, Di Matteo G, et al. Chronic granulomatous disease: Clinical, molecular, and therapeutic aspects. Pediatr Allergy Immunol 2016; 27:242–253.
van den Berg JM, van Koppen E, Ahlin A, et al. Chronic granulomatous disease: the European experience. PLoS One 2009; 4:e5234.
Kuhns DB, Alvord WG, Heller T, et al. Residual NADPH oxidase and survival in chronic granulomatous disease. N Engl J Med 2010; 363:2600–2610.
Beauté J, Obenga G, Le Mignot L, et al. Epidemiology and outcome of invasive fungal diseases in patients with chronic granulomatous disease: a multicenter study in France. Pediatr Infect Dis J 2011; 30:57–62.
Salvator H, Mahlaoui N, Catherinot E, et al. Pulmonary manifestations in adult patients with chronic granulomatous disease. Eur Respir J 2015; 45:1613–1623.
Henriet S, Verweij PE, Holland SM, Warris A. Invasive fungal infections in patients with chronic granulomatous disease. Adv Exp Med Biol 2013; 764:27–55.
King J, Henriet SSV, Warris A. Aspergillosis in chronic granulomatous disease. J Fungi (Basel) 2016; 2:15.
Paccoud O, Guery R, Poirée S, et al. Aspergillus felis in patient with chronic granulomatous disease. Emerg Infect Dis 2019; 25:2319–2321.
Seyedmousavi S, Lionakis MS, Parta M, et al. Emerging Aspergillus species almost exclusively associated with primary immunodeficiencies. Open Forum Infect Dis 2018; 5:ofy213.
Guery R, Pilmis B, Dunogue B, et al. Non-Aspergillus fungal infections in chronic granulomatous disease. Curr Fungal Infect Rep 2019; 13:59–66.
Conrad A, Neven B, Mahlaoui N, et al. Infections in patients with chronic granulomatous disease treated with tumor necrosis factor alpha blockers for inflammatory complications. J Clin Immunol 2021; 41:185–193.
Siddiqui S, Anderson VL, Hilligoss DM, et al. Fulminant mulch pneumonitis: an emergency presentation of chronic granulomatous disease. Clin Infect Dis 2007; 45:673–681.
Margolis DM, Melnick DA, Alling DW, Gallin JI. Trimethoprim-sulfamethoxazole prophylaxis in the management of chronic granulomatous disease. J Infect Dis 1990; 162:723–726.
Mouy R, Veber F, Blanche S, et al. Long-term itraconazole prophylaxis against Aspergillus infections in thirty-two patients with chronic granulomatous disease. J Pediatr 1994; 125:998–1003.
Gallin JI, Alling DW, Malech HL, et al. Itraconazole to prevent fungal infections in chronic granulomatous disease. N Engl J Med 2003; 348:2416–2422.
Slack MA, Thomsen IP. Prevention of infectious complications in patients with chronic granulomatous disease. J Pediatric Infect Dis Soc 2018; 7:S25–S30.
Lugo Reyes SO, González Garay A, González Bobadilla NY, et al. Efficacy and safety of interferon-gamma in chronic granulomatous disease: a systematic review and meta-analysis. J Clin Immunol 2023; 43:578–584.
International Chronic Granulomatous Disease Cooperative Study Group: a controlled trial of interferon gamma to prevent infection in chronic granulomatous disease. N Engl J Med 1991; 324:509–516.
Marciano BE, Wesley R, De Carlo ES, et al. Long-term interferon-gamma therapy for patients with chronic granulomatous disease. Clin Infect Dis 2004; 39:692–699.
Leiding JW, Arnold DE, Parikh S, et al. Genotype, oxidase status, and preceding infection or autoinflammation do not affect allogeneic HCT outcomes for CGD. Blood 2023; 142:2105–2118.
Chiesa R, Wang J, Blok H-J, et al. Hematopoietic cell transplantation in chronic granulomatous disease: a study of 712 children and adults. Blood 2020; 136:1201–1211.
Campos LC, Di Colo G, Dattani V, et al. Long-term outcomes for adults with chronic granulomatous disease in the United Kingdom. J Allergy Clin Immunol 2021; 147:1104–1107.
Cole T, Pearce MS, Cant AJ, et al. Clinical outcome in children with chronic granulomatous disease managed conservatively or with hematopoietic stem cell transplantation. J Allergy Clin Immunol 2013; 132:1150–1155.
Gernez Y, Freeman AF, Holland SM, et al. Autosomal dominant Hyper-IgE syndrome in the USIDNET registry. J Allergy Clin Immunol Pract 2018; 6:996–1001.
Grimbacher B, Holland SM, Gallin JI, et al. Hyper-IgE syndrome with recurrent infections--an autosomal dominant multisystem disorder. N Engl J Med 1999; 340:692–702.
Chandesris M-O, Melki I, Natividad A, et al. Autosomal dominant STAT3 deficiency and hyper-IgE syndrome: molecular, cellular, and clinical features from a French national survey. Medicine (Baltimore) 2012; 91:e1–e19.
Freeman AF, Olivier KN. Hyper IgE syndromes and the lung. Clin Chest Med 2016; 37:557–567.
Vinh DC, Sugui JA, Hsu AP, et al. Invasive fungal disease in autosomal-dominant hyper-IgE syndrome. J Allergy Clin Immunol 2010; 125:1389–1390.
Danion F, Aimanianda V, Bayry J, et al. Aspergillus fumigatus infection in humans with STAT3-deficiency is associated with defective interferon-gamma and Th17 responses. Front Immunol 2020; 11:38.
Duréault A, Tcherakian C, Poiree S, et al. Spectrum of pulmonary aspergillosis in hyper-IgE syndrome with autosomal-dominant STAT3 deficiency. J Allergy Clin Immunol Pract 2019; 7:1986–1995. e3.
Freeman AF, Davis J, Anderson VL, et al. Holland SM: Pneumocystis jiroveci infection in patients with hyper-immunoglobulin E syndrome. Pediatrics 2006; 118:e1271–e1275.
Odio CD, Milligan KL, McGowan K, et al. Endemic mycoses in patients with STAT3-mutated hyper-IgE (Job) syndrome. J Allergy Clin Immunol 2015; 136:1411–1413. e1-2.
Abbara S, Freeman AF, Cohen JF, et al. Primary invasive cutaneous fusariosis in patients with STAT3 hyper-IgE syndrome. J Clin Immunol 2023; 43:647–652.
Gilje EA, Abbott JK. The pulmonary effects of STAT3 deficiency. J Allergy Clin Immunol 2023; 152:368–370.
Aguilar C, Malphettes M, Donadieu J, et al. Prevention of infections during primary immunodeficiency. Clin Infect Dis 2014; 59:1462–1470.
Freeman AF, Kleiner DE, Nadiminti H, et al. Causes of death in hyper-IgE syndrome. J Allergy Clin Immunol 2007; 119:1234–1240.
Muthu V, Sehgal IS, Agarwal R. Aerosolized antifungals for the treatment of pulmonary fungal diseases. Curr Fungal Infect Rep 2024; 18:154–162.
Freeman AF, Renner ED, Henderson C, et al. Lung parenchyma surgery in autosomal dominant hyper-IgE syndrome. J Clin Immunol 2013; 33:896–902.
Gennery AR, Flood TJ, Abinun M, Cant AJ. Bone marrow transplantation does not correct the hyper IgE syndrome. Bone Marrow Transplant 2000; 25:1303–1305.
Nester TA, Wagnon AH, Reilly WF, et al. Effects of allogeneic peripheral stem cell transplantation in a patient with job syndrome of hyperimmunoglobulinemia E and recurrent infections. Am J Med 1998; 105:162–164.
Harrison SC, Tsilifis C, Slatter MA, et al. Hematopoietic stem cell transplantation resolves the immune deficit associated with STAT3-dominant-negative hyper-IgE syndrome. J Clin Immunol 2021; 41:934–943.
Tsilifis C, Freeman AF, Gennery AR. STAT3 hyper-IgE syndrome-an update and unanswered questions. J Clin Immunol 2021; 41:864–880.
Okada S, Asano T, Moriya K, et al. Human STAT1 gain-of-function heterozygous mutations: chronic mucocutaneous candidiasis and type I interferonopathy. J Clin Immunol 2020; 40:1065–1081.
van de Veerdonk FL, Plantinga TS, Hoischen A, et al. STAT1 mutations in autosomal dominant chronic mucocutaneous candidiasis. N Engl J Med 2011; 365:54–61.
Liu L, Okada S, Kong X-F, et al. Gain-of-function human STAT1 mutations impair IL-17 immunity and underlie chronic mucocutaneous candidiasis. J Exp Med 2011; 208:1635–1648.
Toubiana J, Okada S, Hiller J, et al. Heterozygous STAT1 gain-of-function mutations underlie an unexpectedly broad clinical phenotype. Blood 2016; 127:3154–3164.
Sampaio EP, Hsu AP, Pechacek J, et al. Signal transducer and activator of transcription 1 (STAT1) gain-of-function mutations and disseminated coccidioidomycosis and histoplasmosis. J Allergy Clin Immunol 2013; 131:1624–1634.
Ba H, Peng H, Cheng L, et al. Case report: Talaromyces marneffei infection in a Chinese child with a complex heterozygous CARD9 mutation. Front Immunol 2021; 12:685546.
Most ZM, Lieu T, Filkins L, et al. Disseminated Nannizziopsis infection in an adolescent with a STAT1 mutation. Open Forum Infect Dis 2020; 7:ofaa390.
Asano T, Noma K, Mizoguchi Y, et al. Human STAT1 gain of function with chronic mucocutaneous candidiasis: a comprehensive review for strengthening the connection between bedside observations and laboratory research. Immunol Rev 2024; 322:81–97.
Marazzi MG, Bondi E, Giannattasio A, et al. Intracranial aneurysm associated with chronic mucocutaneous candidiasis. Eur J Pediatr 2008; 167:461–463.
McGurk M, Holmes M. Chronic muco-cutaneous candidiasis and oral neoplasia. J Laryngol Otol 1988; 102:643–645.
Hadjadj J, Frémond M-L, Neven B. Emerging place of JAK inhibitors in the treatment of inborn errors of immunity. Front Immunol 2021; 12:717388.
Fischer M, Olbrich P, Hadjadj J, et al. JAK inhibitor treatment for inborn errors of JAK/STAT signaling: an ESID/EBMT-IEWP retrospective study. J Allergy Clin Immunol 2024; 153:275–286. e18.
Zimmerman O, Rösler B, Zerbe CS, et al. Risks of ruxolitinib in STAT1 gain-of-function-associated severe fungal disease. Open Forum Infect Dis 2017; 4:ofx202.
Bazan-Socha S, Gradzikiewicz A, Celińska-Lowenhoff M, et al. Chronic mucocutaneous candidiasis, pancytopenia, and systemic mycosis in a patient with STAT1 gene mutation ineffectively treated with ruxolitinib. Cent Eur J Immunol 2022; 47:92–94.
Leiding JW, Okada S, Hagin D, et al. Hematopoietic stem cell transplantation in patients with gain-of-function signal transducer and activator of transcription 1 mutations. J Allergy Clin Immunol 2018; 141:704–717. e5.
Zhang W, Chen X, Gao G, et al. Clinical relevance of gain- and loss-of-function germline mutations in STAT1: a systematic review. Front Immunol 2021; 12:654406.
Kunvarjee B, Bidgoli A, Madan RP, et al. Emapalumab as bridge to hematopoietic cell transplant for STAT1 gain-of-function mutations. J Allergy Clin Immunol 2023; 152:815–817.
Hsu Y-MS, Zhang Y, You Y, et al. The adaptor protein CARD9 is required for innate immune responses to intracellular pathogens. Nat Immunol 2007; 8:198–205.
Drummond RA, Lionakis MS. Mechanistic insights into the role of C-type lectin receptor/CARD9 signaling in human antifungal immunity. Front Cell Infect Microbiol 2016; 6:39.
Corvilain E, Casanova J-L, Puel A. Inherited CARD9 deficiency: invasive disease caused by ascomycete fungi in previously healthy children and adults. J Clin Immunol 2018; 38:656–693.
Wang X, Zhang R, Wu W, et al. Impaired specific antifungal immunity in CARD9-deficient patients with phaeohyphomycosis. J Invest Dermatol 2018; 138:607–617.
Glocker E-O, Hennigs A, Nabavi M, et al. A homozygous CARD9 mutation in a family with susceptibility to fungal infections. N Engl J Med 2009; 361:1727–1735.
Li J, Vinh DC, Casanova J-L, Puel A. Inborn errors of immunity underlying fungal diseases in otherwise healthy individuals. Curr Opin Microbiol 2017; 40:46–57.
Goel S, Kuehn HS, Chinen J, et al. CARD9 expression pattern, gene dosage, and immunodeficiency phenotype revisited. J Clin Immunol 2021; 42:336–349.
Puel A. Human inborn errors of immunity underlying superficial or invasive candidiasis. Hum Genet 2020; 139:1011–1022.
Tomomasa D, Lee BH, Hirata Y, et al. Inherited CARD9 deficiency due to a founder effect in East Asia. J Clin Immunol 2024; 44:121.
Lanternier F, Mahdaviani SA, Barbati E, et al. Inherited CARD9 deficiency in otherwise healthy children and adults with Candida species-induced meningoencephalitis, colitis, or both. J Allergy Clin Immunol 2015; 135:1558–1568. e2.
Rieber N, Gazendam RP, Freeman AF, et al. Extrapulmonary Aspergillus infection in patients with CARD9 deficiency. JCI Insight 2016; 1:e89890.
Alves de Medeiros AK, Lodewick E, Bogaert DJA, et al. Chronic and invasive fungal infections in a family with CARD9 deficiency. J Clin Immunol 2016; 36:204–209.
Lanternier F, Barbati E, Meinzer U, et al. Inherited CARD9 deficiency in 2 unrelated patients with invasive Exophiala infection. J Infect Dis 2015; 211:1241–1250.
Paccoud O, Vignier N, Boui M, et al. Invasive rhinosinusitis caused by Alternaria infectoria in a patient with autosomal recessive CARD9 deficiency and a review of the literature. J Fungi (Basel) 2022; 8:446.
Lanternier F, Pathan S, Vincent QB, et al. Deep dermatophytosis and inherited CARD9 deficiency. N Engl J Med 2013; 369:1704–1714.
Gavino C, Cotter A, Lichtenstein D, et al. CARD9 deficiency and spontaneous central nervous system candidiasis: complete clinical remission with GM-CSF therapy. Clin Infect Dis 2014; 59:81–84.
Gavino C, Hamel N, Zeng JB, et al. Impaired RASGRF1/ERK-mediated GM-CSF response characterizes CARD9 deficiency in French-Canadians. J Allergy Clin Immunol 2016; 137:1178–1188. e7.
Drummond RA, Zahra FT, Natarajan M, et al. GM-CSF therapy in human caspase recruitment domain–containing protein 9 deficiency. J Allergy Clin Immunol 2018; 142:1334–1338. e5.
Queiroz-Telles F, Mercier T, Maertens J, et al. Successful allogenic stem cell transplantation in patients with inherited CARD9 deficiency. J Clin Immunol 2019; 39:462–469.
Meyts I. Hematopoietic stem cell transplantation in CARD9 deficiency: knight in shining armor? J Clin Immunol 2019; 39:459–461.
Bousfiha A, Moundir A, Tangye SG, et al. The 2022 update of IUIS phenotypical classification for human inborn errors of immunity. J Clin Immunol 2022; 42:1508–1520.
Lisco A, Ortega-Villa Ana M, Mystakelis H, et al. Reappraisal of Idiopathic CD4 Lymphocytopenia at 30 Years. N Engl J Med 2023; 388:1680–1691.
Vinh DC, Patel SY, Uzel G, et al. Autosomal dominant and sporadic monocytopenia with susceptibility to mycobacteria, fungi, papillomaviruses, and myelodysplasia. Blood 2010; 115:1519–1529.
Françoise U, Lafont E, Suarez F, et al. Disseminated cryptococcosis in a patient with CD40 ligand deficiency. J Clin Immunol 2022; 42:1622–1625.
Zerbe CS, Holland SM. Disseminated histoplasmosis in persons with interferon-gamma receptor 1 deficiency. Clin Infect Dis 2005; 41:e38–e41.
Vinh DC, Schwartz B, Hsu AP, et al. Interleukin-12 receptor β1 deficiency predisposing to disseminated Coccidioidomycosis. Clin Infect Dis 2011; 52:e99–e102.

Auteurs

Olivier Paccoud (O)

Université Paris Cité, Department of Infectious Diseases and Tropical Medicine, Necker - Enfants Malades University Hospital, Assistance Publique - Hôpitaux de Paris (AP-HP), IHU Imagine, Paris, France.

Adilia Warris (A)

MRC Centre for Medical Mycology, University of Exeter, Exeter, UK; Department of Paediatric Infectious Diseases, Great Ormond Street Hospital London, London, UK.

Anne Puel (A)

Laboratory of Human Genetics of Infectious Diseases, Necker Branch, UMR 1163, INSERM, Necker - Enfants Malades University Hospital, Paris, France.
St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, New York, USA.
Université Paris Cité, Imagine Institute, Paris.

Fanny Lanternier (F)

Université Paris Cité, Department of Infectious Diseases and Tropical Medicine, Necker - Enfants Malades University Hospital, Assistance Publique - Hôpitaux de Paris (AP-HP), IHU Imagine, Paris, France.
Institut Pasteur, Université Paris Cité, National Reference Center for Invasive Mycoses and Antifungals, Mycology Translational Research Group, Mycology Department, France.

Classifications MeSH