Toward the Standardization of Mycological Examination of Sputum Samples in Cystic Fibrosis: Results from a French Multicenter Prospective Study

Noémie Coron1, Marc Pihet1, Émilie Fréalle2, Yolande Lemeille3, Claudine Pinel3, Hervé Pelloux3, Gilles Gargala4, Loïc Favennec4, Isabelle Accoceberry5, Isabelle Durand-Joly6, Frédéric Dalle7, Frédéric Huet8, Annlyse Fanton8, Amale Boldron9, Guy-André Loeuille9, Philippe Domblides10, Bérengère Coltey11, Isabelle Pin12, C. Llerena12, F. Troussier13, Christine Person13, Christophe Marguet14, N. Wizla15, C. Thumerelle15, Dominique Turck15, Stéphanie Bui16, Michaël Fayon16, Alain Duhamel17, Anne Prévötat18, B. Wallaert18, Sylvie Leroy18, Jean-Philippe Bouchara1, Laurence Delhaès2
1Laboratoire de Parasitologie-Mycologie, Centre Hospitalier Universitaire, Angers, France
2Laboratoire de Parasitologie-Mycologie, Centre Hospitalier Universitaire de Lille, Université de Lille 2, Lille, France
3Service de Parasitologie-Mycologie, Pôle de Biologie et Pathologie, CHU Grenoble-Alpes, Université Grenoble Alpes, Grenoble, France
4Laboratoire de Parasitologie-Mycologie, Centre Hospitalier Universitaire Charles Nicolle, Rouen, France
5Laboratoire de Parasitologie-Mycologie, Centre Hospitalier Universitaire, Université de Bordeaux, Bordeaux, France
6Hygiène hospitalière, Centre Hospitalier de Dunkerque, Dunkerque, France
7Laboratoire de Parasitologie-Mycologie, Service Microbiologie Agents Transmissibles, Centre Hospitalier Universitaire, Dijon, France
8CRCM mixte, Hôpital d’Enfants, Centre Hospitalier Universitaire, Dijon, France
9CRCM, Centre Hospitalier de Dunkerque, Dunkerque, France
10CRCM Adulte, Centre Hospitalier Universitaire, Bordeaux, France
11CRCM Adulte, Centre Hospitalier Universitaire, Grenoble, France
12Pédiatrie, Centre Hospitalier Universitaire de Grenoble Alpes, Grenoble, France
13CRCM mixte, Centre Hospitalier Universitaire, Angers, France
14CRCM mixte, Normandie Univ, UNIROUEN, EA2656/Inserm U1404, département de Pediatrie, Centre Hospitalier Universitaire de Rouen, 76000, Rouen, France
15CRCM de pédiatrie, Centre Hospitalier Universitaire de Lille, Université de Lille 2, Lille, France
16CRCM de pédiatrie, CIC 1401, Centre Hospitalier Universitaire de Bordeaux, Université de Bordeaux, Bordeaux, France
17CERIM, EA2694, Faculté de Médecine, Lille, France
18CRCM adulte, Centre Hospitalier Universitaire de Lille, Université de Lille 2, Lille, France

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Cystic Fibrosis Foundation Patient Registry Annual Report 2015. [cited 2016 Nov 18]. https://www.cff.org/Our-Research/CF-Patient-Registry/2015-Patient-Registry-Annual-Data-Report.pdf .

European Cystic Fibrosis Society Patient Registry Annual Report 2014. [cited 2017 Jan 22]. https://www.ecfs.eu/sites/default/files/images/ECFSPR_Annual%20Report%202014_Nov2016.pdf .

Touati K, Nguyen DNL, Delhaes L. The airway colonization by opportunistic filamentous fungi in patients with cystic fibrosis: recent updates. Curr Fungal Infect Rep. 2014;8:302–11.

Rowe SM, Miller S, Sorscher EJ. Cystic fibrosis. N Engl J Med. 2005;352:1992–2001.

Pihet M, Carrère J, Cimon B, et al. Occurrence and relevance of filamentous fungi in respiratory secretions of patients with cystic fibrosis—a review. Med Mycol. 2009;47:387–97.

Sudfeld CR, Dasenbrook EC, Merz WG, Carroll KC, Boyle MP. Prevalence and risk factors for recovery of filamentous fungi in individuals with cystic fibrosis. J Cyst Fibros. 2010;9:110–6.

Luong ML, Chaparro C, Stephenson A, et al. Pretransplant Aspergillus colonization of cystic fibrosis patients and the incidence of post-lung transplant invasive aspergillosis. Transplantation. 2014;97:351–7.

Symoens F, Knoop C, Schrooyen M, et al. Disseminated Scedosporium apiospermum infection in a cystic fibrosis patient after double-lung transplantation. J Heart Lung Transplant. 2006;25:603–7.

Chotirmall SH, O’Donoghue E, Bennett K, et al. Sputum Candida albicans presages FEV1 decline and hospital-treated exacerbations in cystic fibrosis. Chest. 2010;138:1186–95.

Amin R, Dupuis A, Aaron SD, Ratjen F. The effect of chronic infection with Aspergillus fumigatus on lung function and hospitalization in patients with cystic fibrosis. Chest. 2010;137:171–6.

de Vrankrijker AMM, van der Ent CK, van Berkhout FT, et al. Aspergillus fumigatus colonization in cystic fibrosis: implications for lung function? Clin Microbiol Infect. 2011;17:1381–6.

Kondori N, Gilljam M, Lindblad A, et al. High rate of Exophiala dermatitidis recovery in the airways of patients with cystic fibrosis is associated with pancreatic insufficiency. J Clin Microbiol. 2011;49:1004–9.

Aaron SD, Vandemheen KL, Freitag A, et al. Treatment of Aspergillus fumigatus in patients with cystic fibrosis: a randomized, placebo-controlled pilot study. PLoS ONE. 2012;7:e36077.

Saunders RV, Modha DE, Claydon A, Gaillard EA. Chronic Aspergillus fumigatus colonization of the pediatric cystic fibrosis airway is common and may be associated with a more rapid decline in lung function. Med Mycol. 2016;54:537–43.

Fillaux J, Brémont F, Murris M, et al. Assessment of Aspergillus sensitization or persistent carriage as a factor in lung function impairment in cystic fibrosis patients. Scand J Infect Dis. 2012;44:842–7.

Borman AM, Palmer MD, Delhaes L, et al. Lack of standardization in the procedures for mycological examination of sputum samples from CF patients: a possible cause for variations in the prevalence of filamentous fungi. Med Mycol. 2010;48(Suppl 1):S88–97.

Liu JC, Modha DE, Gaillard EA. What is the clinical significance of filamentous fungi positive sputum cultures in patients with cystic fibrosis? J Cyst Fibros. 2013;12:187–93.

Blyth CC, Harun A, Middleton PG, et al. Detection of occult Scedosporium species in respiratory tract specimens from patients with cystic fibrosis by use of selective media. J Clin Microbiol. 2010;48:314–6.

Delhaes L, Monchy S, Fréalle E, et al. The airway microbiota in cystic fibrosis: a complex fungal and bacterial community—implications for therapeutic management. PLoS ONE. 2012;7:e36313.

Rosenstein BJ, Cutting GR. The diagnosis of cystic fibrosis: a consensus statement. Cystic Fibrosis Foundation Consensus Panel. J Pediatr. 1998;132:589–95.

Pashley CH, Fairs A, Morley JP, et al. Routine processing procedures for isolating filamentous fungi from respiratory sputum samples may underestimate fungal prevalence. Med Mycol. 2012;50:433–8.

Rainer J, Kaltseis J, de Hoog SG, Summerbell RC. Efficacy of a selective isolation procedure for members of the Pseudallescheria boydii complex. Antonie Van Leeuwenhoek. 2007;93:315–22.

Moles DR, Bedi R. A simple technique for data management in general dental practice audit. Prim Dent Care. 1997;4:61–5.

Song Y, Lu Y. Decision tree methods: applications for classification and prediction. Shanghai Arch Psychiatry. 2015;27:130–5.

Nagano Y, Elborn JS, Millar BC, et al. Comparison of techniques to examine the diversity of fungi in adult patients with cystic fibrosis. Med Mycol. 2010;48:166–76.

Güngör O, Tamay Z, Güler N, Erturan Z. Frequency of fungi in respiratory samples from Turkish cystic fibrosis patients. Mycoses. 2013;56:123–9.

Mortensen KL, Jensen RH, Johansen HK, et al. Aspergillus species and other molds in respiratory samples from patients with cystic fibrosis: a laboratory-based study with focus on Aspergillus fumigatus azole resistance. J Clin Microbiol. 2011;49:2243–51.

Paugam A, Baixench MT, Demazes-Dufeu N, et al. Characteristics and consequences of airway colonization by filamentous fungi in 201 adult patients with cystic fibrosis in France. Med Mycol. 2010;48(Suppl 1):S32–6.

Valenza G, Tappe D, Turnwald D, et al. Prevalence and antimicrobial susceptibility of microorganisms isolated from sputa of patients with cystic fibrosis. J Cyst Fibros. 2008;7:123–7.

Masoud-Landgraf L, Badura A, Eber E, et al. Modified culture method detects a high diversity of fungal species in cystic fibrosis patients. Med Mycol. 2014;52:179–86.

Nielsen SM, Kristensen L, Søndergaard A, et al. Increased prevalence and altered species composition of filamentous fungi in respiratory specimens from cystic fibrosis patients. APMIS. 2014;122:1007–12.

Ren CL, Pasta DJ, Rasouliyan L, et al. Relationship between inhaled corticosteroid therapy and rate of lung function decline in children with cystic fibrosis. J Pediatr. 2008;153:746–51.

Burgel PR, Paugam A, Hubert D, Martin C. Aspergillus fumigatus in the cystic fibrosis lung: pros and cons of azole therapy. Infect Drug Resist. 2016;9:229–38.

Chotirmall SH, McElvaney NG. Fungi in the cystic fibrosis lung: bystanders or pathogens? Int J Biochem Cell Biol. 2014;52:161–73.

Whiteson KL, Bailey B, Bergkessel M, et al. The upper respiratory tract as a microbial source for pulmonary infections in cystic fibrosis. Parallels from island biogeography. Am J Respir Crit Care Med. 2014;189:1309–15.

Nagano Y, Millar BC, Goldsmith CE, et al. Development of selective media for the isolation of yeasts and filamentous fungi from the sputum of adult patients with cystic fibrosis (CF). J Cyst Fibros. 2008;7:566–72.

Kerr J. Inhibition of fungal growth by Pseudomonas aeruginosa and Pseudomonas cepacia isolated from patients with cystic fibrosis. J Infect. 1994;28:305–10.

Horré R, Marklein G, Siekmeier R, Nidermajer S, Reiffert SM. Selective isolation of Pseudallescheria and Scedosporium species from respiratory tract specimens of cystic fibrosis patients. Respiration. 2009;77:320–4.

Cortez KJ, Roilides E, Quiroz-Telles F, et al. Infections caused by Scedosporium spp. Clin Microbiol Rev. 2008;21:157–97.

Horré R, Marklein G, Siekmeier R, Reiffert S-M. Detection of hyphomycetes in the upper respiratory tract of patients with cystic fibrosis. Mycoses. 2011;54:514–22.

Lebecque P, Leonard A, Huang D, et al. Exophiala (Wangiella) dermatitidis and cystic fibrosis—prevalence and risk factors. Med Mycol. 2010;48(Suppl 1):S4–9.

Cimon B, Carrère J, Chazalette JP, et al. Fungal colonization and immune response to fungi in cystic fibrosis. J Mycol Méd. 1995;5:211–6.

Bakare N, Rickerts V, Bargon J, Just-Nübling G. Prevalence of Aspergillus fumigatus and other fungal species in the sputum of adult patients with cystic fibrosis. Mycoses. 2003;46:19–23.

Fischer J, van Koningsbruggen-Rietschel S, Rietschel E, et al. Prevalence and molecular characterization of azole resistance in Aspergillus spp. isolates from German cystic fibrosis patients. J Antimicrob Chemother. 2014;69:1533–6.

Baxter CG, Dunn G, Jones AM, et al. Novel immunologic classification of aspergillosis in adult cystic fibrosis. J Allergy Clin Immunol. 2013;132(560–566):e10.

Rougeron A, Giraud S, Razafimandimby B, et al. Different colonization patterns of Aspergillus terreus in patients with cystic fibrosis. Clin Microbiol Infect. 2014;20:327–33.

Cimon B, Carrère J, Vinatier JF, et al. Clinical significance of Scedosporium apiospermum in patients with cystic fibrosis. Eur J Clin Microbiol Infect Dis. 2000;19:53–6.

Russell GK, Gadhok R, Simmonds NJ. The destructive combination of Scedosporium apiospermum lung disease and exuberant inflammation in cystic fibrosis. Paediatr Respir Rev. 2013;14(Suppl 1):22–5.

Guarro J, Kantarcioglu AS, Horré R, et al. Scedosporium apiospermum: changing clinical spectrum of a therapy-refractory opportunist. Med Mycol. 2006;44:295–327.

Rodriguez-Tudela JL, Berenguer J, Guarro J, et al. Epidemiology and outcome of Scedosporium prolificans infection, a review of 162 cases. Med Mycol. 2009;47:359–70.

Muthig M, Hebestreit A, Ziegler U, Seidler M. Müller F-MC. Persistence of Candida species in the respiratory tract of cystic fibrosis patients. Med Mycol. 2010;48:56–63.

LiPuma JJ. The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev. 2010;23:299–323.

Chotirmall SH, Greene CM, McElvaney NG. Candida species in cystic fibrosis: a road less travelled. Med Mycol. 2010;48(Suppl 1):S114–24.

Packeu A, Lebecque P, Rodriguez-Villalobos H, et al. Molecular typing and antifungal susceptibility of Exophiala isolates from patients with cystic fibrosis. J Med Microbiol. 2012;61:1226–33.

Kondori N, Lindblad A, Welinder-Olsson C, Wennerås C, Gilljam M. Development of IgG antibodies to Exophiala dermatitidis is associated with inflammatory responses in patients with cystic fibrosis. J Cyst Fibros. 2014;13:391–9.