Managing Fungal Infections in Cystic Fibrosis Patients: Challenges in Clinical Practice

References

• Davies JC, Alton E, Bush A. Cystic fibrosis. BMJ. 2007;335(7632):1255–1259. doi:10.1136/bmj.39391.713229.AD18079549
   PubMed Web of Science ®Google Scholar
• Sanders DB, Bittner RCL, Rosenfeld M, Hoffman LR, Redding GJ, Goss CH. Failure to recover to baseline pulmonary function after cystic fibrosis pulmonary exacerbation. Am J Respir Crit Care Med. 2010;182(5):627–632. doi:10.1164/rccm.200909-1421OC20463179
   PubMed Web of Science ®Google Scholar
• Yankaskas JR, Marshall BC, Sufian B, Simon RH, Rodman D. Cystic fibrosis adult care: consensus conference report. Chest. 2004;125(1 Suppl):1S–39S.14734689
   PubMed Web of Science ®Google Scholar
• Tracy MC, Moss RB. The myriad challenges of respiratory fungal infection in cystic fibrosis. Pediatr Pulmonol. 2018;53(S3):S75–S85. doi:10.1002/ppul.2412629992775
   PubMed Web of Science ®Google Scholar
• Kraemer R, Delosea N, Ballinari P, Gallati S, Creameri R. Effect of allergic bronchopulmonary aspergillosis on lung function in children with cystic fibrosis. Am J Respir Crit Care Med. 2006;174(11):1211–1220. doi:10.1164/rccm.200603-423OC16959918
   PubMed Web of Science ®Google Scholar
• Harun SN, Wainwright CE, Grimwood K, Hennig S. Aspergillus and progression of lung disease in children with cystic fibrosis. Thorax. 2019;74(2):125–131. doi:10.1136/thoraxjnl-2018-21155030275132
   PubMed Web of Science ®Google Scholar
• 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(1):171–176. doi:10.1378/chest.09-110319567494
   PubMed Web of Science ®Google Scholar
• Schwarz C, Hartl D, Eickmeirir O, et al. Progress in definition, prevention and treatment of fungal infections in cystic fibrosis. Mycopathologia. 2018;183:21–32. doi:10.1007/s11046-017-0182-028762125
   PubMed Web of Science ®Google Scholar
• Hong G, Psoter KJ, Jennings MT, et al. Risk factors for persistent Aspergillus respiratory isolation in cystic fibrosis. J Cyst Fibros. 2018;17(5):624–630. doi:10.1016/j.jcf.2018.01.00829444760
   PubMed Web of Science ®Google Scholar
• Mueller C, Braag SA, Keeler A, Hodges C, Drumm M, Flotte TR. Lack of cystic fibrosis transmembrane conductance regulator in CD3+ lymphocytes leads to aberrant cytokine secretion and hyperinflammatory adaptive immune responses. Am J Respir Cell Mol Biol. 2011;44(6):922–929. doi:10.1165/rcmb.2010-0224OC20724552
   PubMed Web of Science ®Google Scholar
• Chaudhary N, Datta K, Askin FB, Staab JF, Marr KA. Cystic fibrosis transmembrane conductance regulator regulates epithelial cell response to Aspergillus and resultant pulmonary inflammation. Am J Respir Crit Care Med. 2012;185(3):301–310. doi:10.1164/rccm.201106-1027OC22135344
   PubMed Web of Science ®Google Scholar
• Knutsen AP, Bellone C, Kauffman H. Immunopathogenesis of allergic bronchopulmonary aspergillosis in cystic fibrosis. J Cyst Fibros. 2002;l1(2):76–89. doi:10.1016/S1569-1993(02)00033-4
   Google Scholar
• Burns JL, Emerson J, Stapp JR, et al. Microbiology of sputum from patients at cystic fibrosis centers in the United States. Clin Infect Dis. 1998;27(1):158–163. doi:10.1086/5146319675470
   PubMed Web of Science ®Google Scholar
• Muthig M, Hebestreit A, Ziegler U, Seidler M, Müller FC. Persistence of Candida species in the respiratory tract of cystic fibrosis patients. Med Mycol. 2010;48(1):56–63. doi:10.3109/1369378080271653219184771
   PubMed Web of Science ®Google Scholar
• Chen AI, Dolben EF, Okegbe C, et al. Candida albicans ethanol stimulates Pseudomonas aeruginosa WspR-controlled biofilm formation as part of a cyclic relationship involving phenazines. PLoS Pathog. 2014;10(10):e1004480. doi:10.1371/journal.ppat.100448025340349
   PubMed Web of Science ®Google Scholar
• Kim SH, Clark ST, Surendra A. Global analysis of the fungal microbiome in cystic fibrosis patients reveals loss of function of the transcriptional repressor Nrg1 as a mechanism of pathogen adaptation. PloS Pathog. 2015;11(11):e1005308. doi:10.1371/journal.ppat.100530826588216
   PubMed Web of Science ®Google Scholar
• 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(2):110–116. doi:10.1016/j.jcf.2009.11.01020045384
   PubMed Web of Science ®Google Scholar
• Jubin V, Ranque S, Le Bel NS, Sarles J, Dubus J. Risk factors for Aspergillus colonization and allergic bronchopulmonary aspergillosis in children with cystic fibrosis. Pediatr Pulmonol. 2010;45(8):764–771. doi:10.1002/ppul.2124020597074
   PubMed Web of Science ®Google Scholar
• Bargon J, Dauletbaev N, Köhler B, Wolf M, Posselt HG, Wagner TO. Prophylactic antibiotic therapy is associated with an increased prevalence of Aspergillus colonization in adult cystic fibrosis patients. Respir Med. 1999;93(11):835–838. doi:10.1016/S0954-6111(99)90270-610603634
   PubMed Web of Science ®Google Scholar
• Mowat E, Rajendran R, Williams C, et al. Pseudomonas aeruginosa and their small diffusible extracellular molecules inhibit Aspergillus fumigatus biofilm formation. FEMS Microbiol Lett. 2010;313(2):96–102. doi:10.1111/j.1574-6968.2010.02130.x20964704
   PubMed Web of Science ®Google Scholar
• Lee TWR, Brownlee KG, Conway SP, Denton M, Littlewood JM. Evaluation of a new definition for chronic Pseudomonas aeruginosa infection in cystic fibrosis patients. J Cyst Fibros. 2003;2(1):29–34. doi:10.1016/S1569-1993(02)00141-815463843
   PubMedGoogle Scholar
• Ziesing S, Suerbaum S, Sedlacek L. Fungal epidemiology and diversity in cystic fibrosis patients over a 5-year period in a national reference center. Med Mycol. 2016;54:781–786. doi:10.1093/mmy/myw03527364649
   PubMed Web of Science ®Google Scholar
• Lackner M, de Hoog GS, Yang L, et al. Proposed nomenclature for Pseudallescheria, Scedosporium and related genera. Fungal Divers. 2014;67:1–10. doi:10.1007/s13225-014-0295-4
   Web of Science ®Google Scholar
• Williams C, Ranjendran R, Ramage G. Pathogenesis of fungal infections in cystic fibrosis. Curr Fungal Infect Rep. 2016;10(4):163–169. doi:10.1007/s12281-016-0268-z28035247
   PubMedGoogle Scholar
• Schwarz C, Bouchara JP, Buzina W, et al. Organization of patient management and fungal epidemiology in cystic fibrosis. Mycopathologia. 2018;183:7–19. doi:10.1007/s11046-017-0205-x29098487
   PubMed Web of Science ®Google Scholar
• Chotirmall SH, O’Donoghue E, Bennett K, et al. Sputum Candida albicans presages FEV1 decline and hospital-treated exacerbations in cystic fibrosis. Chest. 2010;138:1186–1195. doi:10.1378/chest.09-299620472859
   PubMed Web of Science ®Google Scholar
• Gileles-Hillel A, Shoseyov D, Polacheck I, Korem M, Kerem E, Cohen-Cymberknoh M. Association of chronic Candida albicans respiratory infection with a more severe lung disease in patients with cystic fibrosis. Pediatr Pulmonol. 2015;50(11):1082–1089. doi:10.1002/ppul.2330226383963
   PubMed Web of Science ®Google Scholar
• Al Shakirchi M, Klingspor L, Bergman P, Hjelte L, de Monestrol I. A 16-year retrospective study on fungal prevalence and diversity in patients with cystic fibrosis: candida dubliniensis was associated with a decline in lung function. Int J Infect Dis. 2020;96:663–670. doi:10.1016/j.ijid.2020.05.06332450290
   PubMed Web of Science ®Google Scholar
• AbdulWahab A, Salah H, Chandra P, Taj‑Aldeen SJ. Persistence of Candida dubliniensis and lung function in patients with cystic fibrosis. BMC Res Notes. 2017;10:326. doi:10.1186/s13104-017-2656-z28747217
   PubMedGoogle Scholar
• Hector A, Kirn T, Ralhan A, et al. Microbial colonization and lung function in adolescents with cystic fibrosis. J Cystic Fibros. 2016;15(3):340–349. doi:10.1016/j.jcf.2016.01.004
   Web of Science ®Google Scholar
• Chotirmall SH, McElvaney NG. Fungi in the cystic fibrosis lung: bystanders or pathogens? Int J Biochem Cell Biol. 2014;52:161–173. doi:10.1016/j.biocel.2014.03.00124625547
   PubMed Web of Science ®Google Scholar
• Latgé JP. Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev. 1999;12(2):310–350.10194462
   PubMed Web of Science ®Google Scholar
• King J, Brunel SF, Warris A. Aspergillus infections in cystic fibrosis. J Infect. 2016;72:S50–S55. doi:10.1016/j.jinf.2016.04.02227177733
   PubMed Web of Science ®Google Scholar
• Delfino E, Del Puente F, Briano F, Sepulcri C, Roberto Giacobbe D. Respiratory fungal diseases in adult patients with cystic fibrosis. Clin Med Insights Circ Respir Pulm Med. 2019;13:1–6.
   Web of Science ®Google Scholar
• 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. doi:10.1016/j.jaci.2013.04.00723726262
   PubMed Web of Science ®Google Scholar
• Noni M, Katelari A, Dimopoulos G, Doudounakis S-E, Tzoumaka-Bakoula C, Spoulou V. Aspergillus fumigatus chronic colonization and lung function decline in cystic fibrosis may have a two-way relationship. Eur J Clin Microbiol Infect Dis. 2015;34(11):2235–2241. doi:10.1007/s10096-015-2474-y26319147
   PubMed Web of Science ®Google Scholar
• Fillaux J, Bremont 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(11):842–847. doi:10.3109/00365548.2012.69545422831545
   PubMed Web of Science ®Google Scholar
• de Vrankrijker AM, van der Ent CK, van Berkhout FT, et al. Aspergillus fumigatus colonization in cystic fibrosis: implications for lung function? Clin Microbiol Infect. 2011;17(9):1381–1386. doi:10.1111/j.1469-0691.2010.03429.x21087348
   PubMed Web of Science ®Google Scholar
• McMahon MA, Chotirmall SH, McCullagh B, Branagan P, McElvaney NG, Logan PM. Radiological abnormalities associated with Aspergillus colonization in a cystic fibrosis population. Eur J Radiol. 2012;81(3):e197–e202. doi:10.1016/j.ejrad.2011.01.11421349668
   PubMed Web of Science ®Google Scholar
• Royce FH, Blumberg DA. Pneumocystis carinii isolated from lung lavage fluid in an infant with cystic fibrosis. Pediatr Pulmonol. 2007;335(7632):235–238. doi:10.1002/(SICI)1099-0496(200003)29:3<235::AID-PPUL12>3.0.CO;2-9
   Web of Science ®Google Scholar
• Calderón EJ, Friaza V, Dapena FJ, de La Horra C. Pneumocystis jirovecii and cystic fibrosis. Med Mycol. 2010;48(Suppl 1):S17–S21. doi:10.3109/13693786.2010.50520521067325
   PubMed Web of Science ®Google Scholar
• Kondori N, Gilljam M, Lindblad A, Jönsson B, Moore ER, Wennerås C. High rate of exophiala dermatitidis recovery in the airways of patients with cystic fibrosis is associated with pancreatic insufficiency. J Clin Microbiol. 2011;49(3):1004–1009. doi:10.1128/JCM.01899-1021209163
   PubMed Web of Science ®Google Scholar
• Stevens DA, Moss RB, Kurup VP, et al. Allergic bronchopulmonary aspergillosis in cystic fibrosis–state of the art: cystic Fibrosis foundation consensus conference. Clin Infect Dis. 2003;37(Suppl 3):S225–S264. doi:10.1086/37652512975753
   PubMed Web of Science ®Google Scholar
• Agarwal R, Chakrabarti A, Shah A, et al. Allergic bronchopulmonary aspergillosis: review of literature and proposal of new diagnostic and classification criteria. Clin Exp Allergy. 2013;43(8):850–873.23889240
   PubMed Web of Science ®Google Scholar
• 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:S88–S97. doi:10.3109/13693786.2010.51128721067335
   PubMed Web of Science ®Google Scholar
• 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;50:433–438. doi:10.3109/13693786.2011.61576221961802
   PubMed Web of Science ®Google Scholar
• Saunders R, Modha D, Claydon A, Gaillard E. 146 chronic Aspergillus fumigatus colonisation of the cystic fibrosis airway is common and may be associated with a more rapid decline in lung function. J Cyst Fibros. 2011;10:S37. doi:10.1016/S1569-1993(11)60162-821658640
   PubMed Web of Science ®Google Scholar
• Fraczek MG, Kirwan MB, Moore CB, Morris J, Denning DW, Richardson MD. Volume dependency for culture of fungi from respiratory secretions and increased sensitivity of Aspergillus quantitative PCR. Mycoses. 2014;57(2):69–78. doi:10.1111/myc.1210323786547
   PubMed Web of Science ®Google Scholar
• Pihet M, Carrere 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(4):387–397. doi:10.1080/1369378080260960419107638
   PubMed Web of Science ®Google Scholar
• Masoud-Landgraf L, Badura A, Eber E, Feierl G, Marth E, Buzina W. Modified culture method detects a high diversity of fungal species in cystic fibrosis patients. Med Mycol. 2014;52:179–186. doi:10.3109/13693786.2013.79243823651180
   PubMed Web of Science ®Google Scholar
• Baxter CG, Jones AM, Webb K, Denning DW. Homogenisation of cystic fibrosis sputum by sonication-an essential step for Aspergillus PCR. J Microbiol Methods. 2011;85:75–81. doi:10.1016/j.mimet.2011.01.02421277342
   PubMed Web of Science ®Google Scholar
• 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(1):166–176;e161. doi:10.3109/13693780903127506
   Web of Science ®Google Scholar
• Hong G, Miller HB, Allgood S, Lee R, Lechtzin N, Zhang S. Use of selective fungal culture media increases rates of detection of fungi in the respiratory tract of cystic fibrosis patients. J Clin Microbiol. 2017;55(4):1122–1130. doi:10.1128/JCM.02182-1628100601
   PubMed Web of Science ®Google Scholar
• Coron N, Pihet M, Fréalle E, et al. Toward the standardization of mycological examination of sputum samples in cystic fibrosis: results from a French multicenter prospective study. Mycopathologia. 2018;183(1):101–117. doi:10.1007/s11046-017-0173-128748285
   PubMed Web of Science ®Google Scholar
• Delhaes L, Touati K, Faure-Cognet O, et al. Prevalence, geographic risk factor, and development of a standardized protocol for fungal isolation in cystic fibrosis: results from the international prospective study “MFIP”. J Cyst Fibros. 2019;18(2):212–220. doi:10.1016/j.jcf.2018.10.00130348610
   PubMed Web of Science ®Google Scholar
• Nosotti M, Tarsia P, Corinna Morlacchi L. Infections after lung transplantation. J Thorac Dis. 2018;10(6):3849–3868. doi:10.21037/jtd.2018.05.20430069386
   PubMed Web of Science ®Google Scholar
• Chen SC-A, Meyer W, Pashley CH. Challenges in laboratory detection of fungal pathogens in the airways of cystic fibrosis patients. Mycopathologia. 2018;183(1):89–100. doi:10.1007/s11046-017-0150-828589247
   PubMed Web of Science ®Google Scholar
• Mina S, Staerck C, Marot A, et al. Scedosporium boydii CatA1 and SODC recombinant proteins, new tools for serodiagnosis of Scedosporium infection of patients with cystic fibrosis. Diagn Microbiol Infect Dis. 2017;89:282–287. doi:10.1016/j.diagmicrobio.2017.08.01328974395
   PubMed Web of Science ®Google Scholar
• Pappas PG, Kauffman CA, Andes DR. Clinical practice guideline for the management of candidiasis: 2016 update by the infectious diseases society of America. Clin Infect Dis. 2016;62(4):e1–e50.26679628
   PubMed Web of Science ®Google Scholar
• Nett JE, Andes DR. Antifungal agents: spectrum of activity, pharmacology, and clinical indications. Infect Dis Clin North Am. 2016;30(1):51–83.26739608
   PubMed Web of Science ®Google Scholar
• Shah A, Panjabi C. Allergic bronchopulmonary aspergillosis: a perplexing clinical entity. Allergy Asthma Immunol Res. 2016;8(4):282–297. doi:10.4168/aair.2016.8.4.28227126721
   PubMed Web of Science ®Google Scholar
• Moreira AS, Silva D, Ferreira AR, Delgado L. Antifungal treatment in allergic bronchopulmonary aspergillosis with and without cystic fibrosis: a systematic review. Clin Exp Allergy. 2014;44(10):1210–1227. doi:10.1111/cea.1233324809846
   PubMed Web of Science ®Google Scholar
• Rivosecchi RM, Samanta P, Demehin M, et al. Pharmacokinetics of azole antifungals in cystic fibrosis. Mycopathologia. 2018;183(1):139–150. doi:10.1007/s11046-017-0189-628795298
   PubMed Web of Science ®Google Scholar
• Fluconazole, Itraconazole, Voriconazole, Posaconazole, and Isavuconazole. Lexi-drugs. Lexicomp. Wolters Kluwer Health, Inc. Riverwoods, IL. Available from: http://online.lexi.com. Accessed 1215, 2020.
   Google Scholar
• 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(4):e36077. doi:10.1371/journal.pone.003607722563440
   PubMed Web of Science ®Google Scholar
• 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;97:351–357. doi:10.1097/01.TP.0000437434.42851.d424305637
   PubMed Web of Science ®Google Scholar
• Hosseini-Moghaddam SM, Chaparro C, Luong ML, et al. The effectiveness of culture-directed preemptive anti-Aspergillus treatment in lung transplant recipients at one year after transplant. Transplantation. 2015;99:2387–2393. doi:10.1097/TP.000000000000074325961491
   PubMed Web of Science ®Google Scholar
• Patterson TF, Thompson GR, Denning DW, et al. Practice guidelines for the diagnosis and management of Aspergillosis: 2016 update by the infectious diseases society of America. Clin Infect Dis. 2016;63(4):e1–e60.27365388
   PubMed Web of Science ®Google Scholar
• Schwarz C, Vandeputte P, Rougeron A, et al. Developing collaborative works for faster progress on fungal respiratory infections in cystic fibrosis. Med Mycol. 2009;47(4):42–59. doi:10.1093/mmy/myx106
   Web of Science ®Google Scholar
• Heijerman HGM, McKone EF, Downey DG, et al. Efficacy and safety of the elexacaftor plus tezacaftor plus ivacaftor combination regimen in people with cystic fibrosis homozygous for the F508del mutation: a double-blind, randomised, Phase 3 trial. Lancet. 2019;394:1940–1948.31679946
   PubMed Web of Science ®Google Scholar
• Trikafta [Package Insert]. Boston, MA: Vertex Pharmaceutical Inc.; 2019.
   Google Scholar
• Symdeko [Package Insert]. Boston, MA: Vertex Pharmaceutical Inc.; 2018.
   Google Scholar
• Orkambi [Package Insert]. Boston, MA: Vertex Pharmaceutical Inc.; 2015.
   Google Scholar
• Hamprecht A, Morio F, Bader O, Le Pape P, Steinmann J, Dannaoui E. Azole resistance in Aspergillus fumigatus in patients with cystic fibrosis: a matter of concern? Mycopathologia. 2018;183(1):151–160. doi:10.1007/s11046-017-0162-428653258
   PubMed Web of Science ®Google Scholar
• Schwarz C, Brandt C, Whitaker P, et al. Invasive pulmonary fungal infections in cystic fibrosis. Mycopathologia. 2018;183(1):33–43. doi:10.1007/s11046-017-0199-428864921
   PubMed Web of Science ®Google Scholar
• Dodds Ashley ES, Lewis R, Lewis JS, Martin C, Andes D. Pharmacology of systemic antifungal agents. Clin Infect Dis. 2006;43:S28–S39. doi:10.1086/504492
   Web of Science ®Google Scholar