264
Views
2
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Epidemiology of Clinically Significant Aspergillus Species from a Large Tertiary Hospital in Shanghai, China, for the Period of Two Years

, , , , , , , & ORCID Icon show all
Pages 4645-4657 | Received 19 Apr 2023, Accepted 12 Jul 2023, Published online: 17 Jul 2023

References

  • Mullins J, Harvey R, Seaton A. Sources and incidence of airborne Aspergillus fumigatus (Fres). Clin Exp Allergy. 1976;6(3):209–217. doi:10.1111/j.1365-2222.1976.tb01899.x
  • Species Fungorum [homepage on the Internet]. Aspergillus – search Page. Available from: www.speciesfungorum.org. Accessed June 16, 2023.
  • Latgé JP, Chamilos G. Aspergillus fumigatus and Aspergillosis in 2019. Clin Microbiol Rev. 2019;33(1):e00140–18.
  • Bongomin F, Gago S, Oladele RO, Denning DW. Global and Multi-National Prevalence of Fungal Diseases-Estimate Precision. J Fungi. 2017;3(4):57.
  • Hammond EE, McDonald CS, Vestbo J, Denning DW. The global impact of Aspergillus infection on COPD. BMC Pulm Med. 2020;20(1):241.
  • González-García P, Alonso-Sardón M, Rodríguez-Alonso B, et al. How Has the Aspergillosis Case Fatality Rate Changed over the Last Two Decades in Spain? J Fungi. 2022;8(6):576.
  • WHO. Fungal priority pathogens list to guide research, development and public health action [Online]. Geneva: World Health Organization; 2022. Available from: https://www.who.int/publications-detail-redirect/9789240060241. Accessed March 13, 2023.
  • Zhang J, Li L, Lv Q, Yan L, Wang Y, Jiang Y. The Fungal CYP51s: their Functions, Structures, Related Drug Resistance, and Inhibitors. Front Microbiol. 2019;10:691.
  • Verweij PE, Lucas JA, Arendrup MC, et al. The one health problem of azole resistance in Aspergillus fumigatus: current insights and future research agenda. Fungal Biol Rev. 2020;34(4):203–214.
  • Rivero-Menendez O, Alastruey-Izquierdo A, Mellado E, Cuenca-Estrella M. Triazole Resistance in Aspergillus spp.: a Worldwide Problem? J Fungi. 2016;2:21.
  • van der Linden JW, Arendrup MC, Warris A, et al. Prospective multicenter international surveillance of azole resistance in Aspergillus fumigatus. Emerg Infect Dis. 2015;21(6):1041–1044.
  • Rotjanapan P, Chen YC, Chakrabarti A, et al. Epidemiology and clinical characteristics of invasive mould infections: a multicenter, retrospective analysis in five Asian countries. Med Mycol. 2018;56:186–196.
  • Lestrade PPA, Bentvelsen R, Schauwvlieghe AFAD, et al. Voriconazole resistance and mortality in invasive aspergillosis: a multicentre retrospective cohort study. Clin Infect Dis. 2019;68:1463–1471.
  • Ragozzino S, Goldenberger D, Wright PR, et al. Distribution of Aspergillus Species and Prevalence of Azole Resistance in Respiratory Samples From Swiss Tertiary Care Hospitals. Open Forum Infect Dis. 2021;9(2):ofab638.
  • Bueid A, Howard SJ, Moore CB, et al. Azole antifungal resistance in Aspergillus fumigatus: 2008 and 2009. J Antimicrob Chemother. 2010;65:2116–2118.
  • Baddley JW, Marr KA, Andes DR, et al. Patterns of susceptibility of Aspergillus isolates recovered from patients enrolled in the Transplant-Associated Infection Surveillance Network. J Clin Microbiol. 2009;47(10):3271–3275.
  • Chowdhary A, Sharma C, van den Boom M, et al. Multi-azole-resistant Aspergillus fumigatus in the environment in Tanzania. J Antimicrob Chemother. 2014;69(11):2979–2983.
  • Xu Y, Chen M, Zhu J, et al. Aspergillus Species in Lower Respiratory Tract of Hospitalized Patients from Shanghai, China: species Diversity and Emerging Azole Resistance. Infect Drug Resist. 2020;13:4663–4672.
  • Xiao C, Qiao D, Xiong L, et al. Clinical and Microbiological Characteristics of Aspergillosis at a Chinese Tertiary Teaching Hospital. Infect Drug Resist. 2022;15:7249–7257.
  • Yang X, Chen W, Liang T, et al. A 20-Year Antifungal Susceptibility Surveillance (From 1999 to 2019) for Aspergillus spp. and Proposed Epidemiological Cutoff Values for Aspergillus fumigatus and Aspergillus flavus: a Study in a Tertiary Hospital in China. Front Microbiol. 2021;12:680884.
  • Wang Y, Zhang L, Zhou L, Zhang M, Epidemiology XY. Drug Susceptibility, and Clinical Risk Factors in Patients With Invasive Aspergillosis. Front Public Health. 2022;10:835092.
  • Deng S, Zhang L, Ji Y, et al. Triazole phenotypes and genotypic characterization of clinical Aspergillus fumigatus isolates in China. Emerg Microbes Infect. 2017;6(12):e109.
  • Ullmann AJ, Aguado JM, Arikan-Akdagli S, et al. Diagnosis and management of Aspergillus diseases: executive summary of the 2017 ESCMID-ECMM-ERS guideline. Clin Microbiol Infect. 2018;24(Suppl 1):e1–e38.
  • Donnelly JP, Chen SC, Kauffman CA, et al. Revision and Update of the Consensus Definitions of Invasive Fungal Disease From the European Organization for Research and Treatment of Cancer and the Mycoses Study Group Education and Research Consortium. Clin Infect Dis. 2020;71(6):1367–1376.
  • Asano K, Hebisawa A, Ishiguro T, et al. New clinical diagnostic criteria for allergic bronchopulmonary aspergillosis/mycosis and its validation. J Allergy Clin Immunol. 2021;147(4):1261–1268.e5.
  • Carroll KC, Pfaller MA, Landry ML, McAdam AJ, Patel R, Richter SS. Manual of Clinical Microbiology. 12th ed. Washington, DC: American Society for Microbiology; 2019.
  • Samson RA, Visagie CM, Houbraken J, et al. Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol. 2008;78:141–173.
  • CLSI. 2017 Reference Method for Broth Dilution Antifungal Susceptibility Testing of fIlamentous Fungi. CLSI Standard M38. 3rd ed. Wayne, PA: Clinical and Laboratory Standards Institute; 2017.
  • CLSI. 2020 Performance Standards for Antifungal Susceptibility Testing of Filamentous Fungi. CLSI Standard M61. 2nd ed. Wayne, PA: Clinical and Laboratory Standard Institute; 2020.
  • CLSI. 2020. Epidemiological Cutoff Values for Antifungal Susceptibility Testing. CLSI Standard M59. 3rd ed. Wayne, PA: Clinical and Laboratory Standard Institute; 2020.
  • Sewell TR, Zhang Y, Brackin AP, Shelton JMG, Rhodes J, Fisher MC. Elevated prevalence of azole-resistant Aspergillus fumigatus in urban versus rural environments in the United Kingdom. Antimicrob Agents Chemother. 2019;63:e00548–19.
  • Ozmerdiven GE, Ak S, Ener B, et al. First determination of azole resistance in Aspergillus fumigatus strains carrying the TR34/L98H mutations in Turkey. J Infect Chemother. 2015;21(8):581–586.
  • Klaassen CH, de Valk HA, Balajee SA, Meis JF. Utility of CSP typing to sub-type clinical Aspergillus fumigatus isolates and proposal for a new CSP type nomenclature. J Microbiol Methods. 2009;77:292–296.
  • Gao LJ, Sun Y, Wan Z, Li RY, Yu J. CSP typing of Chinese Aspergillus fumigatus isolates: identification of additional CSP types. Med Mycol. 2013;51:683–687.
  • Krishnan S, Manavathu EK, Chandrasekar PH. Aspergillus flavus: an emerging non- fumigatus Aspergillus species of significance. Mycoses. 2009;52:206–222.
  • Rudramurthy SM, Paul RA, Chakrabarti A, Mouton JW, Meis JF. Invasive Aspergillosis by Aspergillus flavus: epidemiology, Diagnosis, Antifungal Resistance, and Management. J Fungi. 2019;5(3):55.
  • Heo MS, Shin JH, Choi MJ, et al. Molecular identification and amphotericin B susceptibility testing of clinical isolates of Aspergillus from 11 hospitals in Korea. Ann Lab Med. 2015;35:602–610.
  • Zanganeh E, Zarrinfar H, Rezaeetalab F, et al. Predominance of non-fumigatus Aspergillus species among patients suspected to pulmonary aspergillosis in a tropical and subtropical region of the Middle East. Microb Pathog. 2018;116:296–300.
  • Al-Wathiqi F, Ahmad S, Khan Z. Molecular identification and antifungal susceptibility profile of Aspergillus flavus isolates recovered from clinical specimens in Kuwait. BMC Infect Dis. 2013;13:126.
  • Zarrinfar H, Saber S, Kordbacheh P, et al. Mycological microscopic and culture examination of 400 bronchoalveolar lavage (BAL) samples. Iran J Public Health. 2012;41:70–76.
  • Risum M, Hare RK, Gertsen JB, et al. Azole-Resistant Aspergillus fumigatus Among Danish Cystic Fibrosis Patients: increasing Prevalence and Dominance of TR34/L98H. Front Microbiol. 2020;11:1850.
  • Al-Bader N, Sheppard DC. Aspergillosis and stem cell transplantation: an overview of experimental pathogenesis studies. Virulence. 2016;7(8):950–966.
  • Takeda K, Suzuki J, Watanabe A, et al. High detection rate of azole-resistant Aspergillus fumigatus after treatment with azole antifungal drugs among patients with chronic pulmonary aspergillosis in a single hospital setting with low azole resistance. Med Mycol. 2021;59(4):327–334.
  • Cho SY, Lee DG, Kim WB, et al. Epidemiology and Antifungal Susceptibility Profile of Aspergillus Species: comparison between Environmental and Clinical Isolates from Patients with Hematologic Malignancies. J Clin Microbiol. 2019;57(7):e02023–18.
  • Moin S, Farooqi J, Jabeen K, Laiq S, Zafar A. Screening for triazole resistance in clinically significant Aspergillus species; report from Pakistan. Antimicrob Resist Infect Control. 2020;9(1):62.
  • Hsu TH, Huang PY, Fan YC, Sun PL. Azole Resistance and cyp51A Mutation of Aspergillus fumigatus in a Tertiary Referral Hospital in Taiwan. J Fungi. 2022;8(9):908.
  • Lv Q, Elders BBLJ, Warris A, Caudri D, Ciet P. Aspergillus-related lung disease in people with cystic fibrosis: can imaging help us to diagnose disease? Eur Respir Rev. 2021;30(162):210103.
  • Burks C, Darby A, Gómez Londoño L, Momany M, Brewer MT. Azole-resistant Aspergillus fumigatus in the environment: identifying key reservoirs and hotspots of antifungal resistance. PLoS Pathog. 2021;17(7):e1009711.
  • Cao D, Wang F, Yu S, et al. Prevalence of Azole-Resistant Aspergillus Fumigatus Is Highly Associated With Azole Fungicide Residues in the Fields. Environ Sci Technol. 2021;55(5):3041–3049.
  • Rhodes J, Abdolrasouli A, Dunne K, et al. Population genomics confirms acquisition of drug-resistant Aspergillus fumigatus infection by humans from the environment. Nat Microbiol. 2022;7(5):663–674.
  • Fuhren J, Voskuil WS, Boel CH, et al. High prevalence of azole resistance in Aspergillus fumigatus isolates from high-risk patients. J Antimicrob Chemother. 2015;70(10):2894–2898.
  • Steinmann J, Hamprecht A, Vehreschild MJGT, et al. Emergence of azole-resistant invasive aspergillosis in HSCT recipients in Germany. J Antimicrob Chemother. 2015;70:1522–1526.
  • van Paassen J, Russcher A, In ‘t Veld-van Wingerden AW, Verweij PE, Kuijper EJ. Emerging aspergillosis by azole-resistant Aspergillus fumigatus at an intensive care unit in the Netherlands, 2010 to 2013. Euro Surveill. 2016;21(30):3456.
  • Montesinos I, Argudín MA, Hites M, et al. Culture-Based Methods and Molecular Tools for Azole-Resistant Aspergillus fumigatus Detection in a Belgian University Hospital. J Clin Microbiol. 2017;55(8):2391–2399.
  • Duong TN, Le TV, Tran KH, et al. Azole-resistant Aspergillus fumigatus is highly prevalent in the environment of Vietnam, with marked variability by land use type. Environ Microbiol. 2021;23(12):7632–7642.
  • Majima H, Arai T, Kusuya Y, et al. Genetic differences between Japan and other countries in cyp51A polymorphisms of Aspergillus fumigatus. Mycoses. 2021;64(11):1354–1365.
  • L R, Ninan MM, Kurien R, F NA, Sahni RD, Michael JS. Cryptic aspergillosis: a rare entity and a diagnostic challenge. Access Microbiol. 2022;4(4):000344.
  • Nematollahi S, Permpalung N, Zhang SX, Morales M, Marr KA. Aspergillus lentulus: an Under-recognized Cause of Antifungal Drug-Resistant Aspergillosis. Open Forum Infect Dis. 2021;8(8):ofab392.
  • Pérez-Cantero A, López-Fernández L, Guarro J, Capilla J. New Insights into the Cyp51 Contribution to Azole Resistance in Aspergillus Section Nigri. Antimicrob Agents Chemother. 2019;63(7):e00543–19.
  • Bader O. Phylogenetic Distribution of csp1 Types in Aspergillus fumigatus and Their Correlates to Azole Antifungal Drug Resistance. Microbiol Spectr. 2021;9(3):e0121421.
  • de Groot T, Meis JF. Microsatellite stability in STR analysis Aspergillus fumigatus depends on number of repeat units. Front Cell Infect Microbiol. 2019;9:82.
  • Chen Y, Lu Z, Zhao J, et al. Epidemiology and molecular characterizations of azole resistance in clinical and environmental Aspergillus fumigatus isolates from China. Antimicrob Agents Chemother. 2016;60:5878–5884.
  • Falahatinejad M, Vaezi A, Fakhim H, et al. Use of cell surface protein typing for genotyping of azole-resistant and -susceptible Aspergillus fumigatus isolates in Iran. Mycoses. 2018;61:143–147.
  • Duarte-Escalante E, Frías-De-León MG, Martínez-Herrera E, et al. Identification of CSP Types and Genotypic Variability of Clinical and Environmental Isolates of Aspergillus fumigatus from Different Geographic Origins. Microorganisms. 2020;8(5):688.
  • Kidd SE, Nik Zulkepeli NA, Slavin MA, Morrissey CO. Utility of a proposed CSP typing nomenclature for Australian Aspergillus fumigatus isolates: identification of additional CSP types and suggested modifications. J Microbiol Methods. 2009;78:223–226.
  • Garcia-Rubio R, Gil H, Monteiro MC, Pelaez T, Mellado E. A New Aspergillus fumigatus Typing Method Based on Hypervariable Tandem Repeats Located within Exons of Surface Protein Coding Genes (TRESP). PLoS One. 2016;11(10):e0163869.
  • Camps SM, Rijs AJ, Klaassen CH, et al. Molecular epidemiology of Aspergillus fumigatus isolates harboring the TR34/L98H azole resistance mechanism. J Clin Microbiol. 2012;50(8):2674–2680.
  • Ashu EE, Korfanty GA, Xu J. Evidence of unique genetic diversity in Aspergillus fumigatus isolates from Cameroon. Mycoses. 2017;60:739–748.
  • Ballard E, Melchers WJG, Zoll J, Brown AJP, Verweij PE, Warris A. In-host microevolution of Aspergillus fumigatus: a phenotypic and genotypic analysis. Fungal Genet Biol. 2018;113:1–13.
  • Balajee SA, Tay ST, Lasker BA, Hurst SF, Rooney AP. Characterization of a novel gene for strain typing reveals substructuring of Aspergillus fumigatus across North America. Eukaryot Cell. 2007;6:1392–1399.