Epidemiology and molecular characterizations of azole resistance in clinical and environmental aspergillus fumigatus isolates from China

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 10, 2016, Pages 5878-5884

  Chen, Yong ^a   Lu, Zhongyi ^a   Zhao, Jingjun ^b   Zou, Ziying ^c   Gong, Yanwen ^d   Qu, Fen ^e   Bao, Zhiyao ^f   Qiu, Guangbin ^g   Song, Mingsheng ^h   Zhang, Qing ^a   Liu, Lin ^a   Hu, Mandong ^a   Han, Xuelin ^a   Tian, Shuguang ^a   Zhao, Jingya ^a   Chen, Fangyan ^a   Zhang, Changjian ^a   Sun, Yansong ^a   Verweij, Paul E ⁱ   Huang, Liuyu ^a   Hana, Li ^a   more..

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^b TONGJI HOSPITAL OF TONGJI UNIVERSITY   (China)

^c CHENGDU MILITARY GENERAL HOSPITAL   (China)

^d JINAN MILITARY GENERAL HOSPITAL   (China)

^e BEIJING 302 HOSPITAL   (China)

^f SHANGHAI JIAO TONG UNIVERSITY   (China)

^g No 202 Hospital of PLA   (China)

^h THE THIRD XIANGYA HOSPITAL OF CENTRAL SOUTH UNIVERSITY   (China)

ⁱ RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE PROTEIN; PYRROLE; ANTIFUNGAL AGENT; CYTOCHROME P-450 CYP51A, ASPERGILLUS; CYTOCHROME P450; FUNGAL PROTEIN; MICROSATELLITE DNA; PYRROLE DERIVATIVE;

ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; ASPERGILLUS FUMIGATUS; CHINA; CONTROLLED STUDY; FUNGAL GENE; FUNGUS ISOLATION; GENE MUTATION; GENE SEQUENCE; GENETIC BACKGROUND; GENOTYPE; MATING TYPE; MOLECULAR PHYLOGENY; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; ASPERGILLOSIS; DRUG EFFECTS; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYLOGENY;

ANTIFUNGAL AGENTS; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; AZOLES; CHINA; CYTOCHROME P-450 ENZYME SYSTEM; DRUG RESISTANCE, FUNGAL; FUNGAL PROTEINS; HUMANS; MICROSATELLITE REPEATS; PHYLOGENY;

EID: 84992694585     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01005-16     Document Type: Article

References (46)

1. Latge JP. 1999. Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 12:310-350.
2. Verweij PE, Ananda-Rajah M, Andes D, Arendrup MC, Bruggemann RJ, Chowdhary A, Cornely OA, Denning DW, Groll AH, Izumikawa K, Kullberg BJ, Lagrou K, Maertens J, Meis JF, Newton P, Page I, Seyedmousavi S, Sheppard DC, Viscoli C, Warris A, Donnelly JP. 2015. International expert opinion on the management of infection caused by azole-resistant Aspergillus fumigatus. Drug Resist Updat 21-22:30-40. http://dx.doi.org/10.1016/j.drup.2015.08.001.
3. Verweij PE, Chowdhary A, Melchers WJ, Meis JF. 2016. Azole resistance in Aspergillus fumigatus: can we retain the clinical use of mold-active antifungal azoles? Clin Infect Dis 62:362-368. http://dx.doi.org/10.1093/cid /civ885.
4. Snelders E, van der Lee HA, Kuijpers J, Rijs AJ, Varga J, Samson RA, Mellado E, Donders AR, Melchers WJ, Verweij PE. 2008. Emergence of azole resistance in Aspergillus fumigatus and spread of a single resistance mechanism. PLoS Med 5:e219. http://dx.doi.org/10.1371/journal.pmed .0050219.
5. Chowdhary A, Kathuria S, Xu J, Meis JF. 2013. Emergence of azoleresistant Aspergillus fumigatus strains due to agricultural azole use creates an increasing threat to human health. PLoS Pathog 9:e1003633. http://dx .doi.org/10.1371/journal.ppat.1003633.
6. van der Linden JW, Camps SM, Kampinga GA, Arends JP, Debets- Ossenkopp YJ, Haas PJ, Rijnders BJ, Kuijper EJ, van Tiel FH, Varga J, Karawajczyk A, Zoll J, Melchers WJ, Verweij PE. 2013. Aspergillosis due to voriconazole highly resistant Aspergillus fumigatus and recovery of genetically related resistant isolates from domiciles. Clin Infect Dis 57:513-520. http://dx.doi.org/10.1093/cid/cit320.
7. Vermeulen E, Maertens J, Schoemans H, Lagrou K. 2012. Azoleresistant Aspergillus fumigatus due to TR46/Y121F/T289A mutation emerging in Belgium, July 2012. Euro Surveill 17:20326. http://www .eurosurveillance.org/ViewArticle.aspx?ArticleId-20326.
8. Chowdhary A, Sharma C, van den Boom M, Yntema JB, Hagen F, Verweij PE, Meis JF. 2014. Multi-azole-resistant Aspergillus fumigatus in the environment in Tanzania. J Antimicrob Chemother 69:2979-2983. http://dx.doi.org/10.1093/jac/dku259.
9. Lavergne RA, Morio F, Favennec L, Dominique S, Meis JF, Gargala G, Verweij PE, Le Pape P. 2015. First description of azole-resistant Aspergillus fumigatus due to TR46/Y121F/T289A mutation in France. Antimicrob Agents Chemother 59:4331-4335. http://dx.doi.org/10.1128/AAC .00127-15.
10. Chen Y, Wang H, Lu Z, Li P, Zhang Q, Jia T, Zhao J, Tian S, Han X, Chen F, Zhang C, Jia X, Huang L, Qu F, Han L. 2015. Emergence of TR46/Y121F/T289A in an Aspergillus fumigatus isolate from a Chinese patient. Antimicrob Agents Chemother 59:7148-7150. http://dx.doi.org /10.1128/AAC.00887-15.
11. Wiederhold NP, Gil VG, Gutierrez F, Lindner JR, Albataineh MT, McCarthy DI, Sanders C, Fan H, Fothergill AW, Sutton DA. 2016. First detection of TR34 L98H and TR46 Y121F T289A Cyp51 mutations in Aspergillus fumigatus Isolates in the United States. J Clin Microbiol 54: 168-171. http://dx.doi.org/10.1128/JCM.02478-15.
12. Lockhart SR, Frade JP, Etienne KA, Pfaller MA, Diekema DJ, Balajee SA. 2011. Azole resistance in Aspergillus fumigatus isolates from the ARTEMIS global surveillance study is primarily due to the TR/L98H mutation in the cyp51A gene. Antimicrob Agents Chemother 55:4465-4468. http://dx.doi.org/10.1128/AAC.00185-11.
13. Liu M, Zeng R, Zhang L, Li D, Lv G, Shen Y, Zheng H, Zhang Q, Zhao J, Zheng N, Liu W. 2015. Multiple cyp51A-based mechanisms identified in azole-resistant isolates of Aspergillus fumigatus from China. Antimicrob Agents Chemother 59:4321-4325. http://dx.doi.org/10 .1128/AAC.00003-15.
14. Wang DY, Gricourt M, Arne P, Thierry S, Seguin D, Chermette R, Huang WY, Dannaoui E, Botterel F, Guillot J. 2014. Mutations in the cyp51A gene and susceptibility to itraconazole in Aspergillus fumigatus isolated from avian farms in France and China. Poult Sci 93:12-15. http: //dx.doi.org/10.3382/ps.2013-03541.
15. Snelders E, Huis In 't Veld RA, Rijs AJ, Kema GH, Melchers WJ, Verweij PE. 2009. Possible environmental origin of resistance of Aspergillus fumigatus to medical triazoles. Appl Environ Microbiol 75:4053-4057. http://dx.doi.org/10.1128/AEM.00231-09.
16. Morio F, Aubin GG, Danner-Boucher I, Haloun A, Sacchetto E, Garcia- Hermoso D, Bretagne S, Miegeville M, Le Pape P. 2012. High prevalence of triazole resistance in Aspergillus fumigatus, especially mediated by TR/ L98H, in a French cohort of patients with cystic fibrosis. J Antimicrob Chemother 67:1870-1873. http://dx.doi.org/10.1093/jac/dks160.
17. Arendrup MC, Guinea J, Cuenca-Estrella M, Meletiadis J, Mouton JW, Lagrou K, Howard SJ, Subcommittee on Antifungal Susceptibility Testing (AFST) of the ESCMID European Committee for Antimicrobial Susceptibility Testing (EUCAST). 2015. Method for the determination of broth dilution minimum inhibitory concentrations of antifungal agents for conidia forming moulds, EUCAST definitive document EDef 9.3. European Committee for Antimicrobial Sus ceptibility Testing, Basel, Switzerland. http://www.eucast.org/fileadmin /src/media/PDFs/EUCAST-files/AFST/Files/EUCAST-E-Def-9-3 -Mould-testing-definitive.pdf.
18. Balajee SA, Gribskov JL, Hanley E, Nickle D, Marr KA. 2005. Aspergillus lentulus sp. nov., a new sibling species of A. fumigatus. Eukaryot Cell 4:625-632. http://dx.doi.org/10.1128/EC.4.3.625-632.2005.
19. Snelders E, Karawajczyk A, Schaftenaar G, Verweij PE, Melchers WJ. 2010. Azole resistance profile of amino acid changes in Aspergillus fumigatus CYP51A based on protein homology modeling. Antimicrob Agents Chemother 54:2425-2430. http://dx.doi.org/10.1128/AAC.01599-09.
20. Mellado E, Diaz-Guerra TM, Cuenca-Estrella M, Rodriguez-Tudela JL. 2001. Identification of two different 14-alpha sterol demethylase-related genes (cyp51A and cyp51B) in Aspergillus fumigatus and other Aspergillus species. J Clin Microbiol 39:2431-2438. http://dx.doi.org/10.1128/JCM .39.7.2431-2438.2001.
21. Kidd SE, Nik Zulkepeli NA, Slavin MA, Morrissey CO. 2009. Utility of a proposed CSP typing nomenclature for Australian Aspergillus fumigatus isolates: identification of additional CSP types and suggested modifications. J Microbiol Methods 78:223-226. http://dx.doi.org/10 .1016/j.mimet.2009.06.003.
22. Gao LJ, Sun Y, Wan Z, Li RY, Yu J. 2013. CSP typing of Chinese Aspergillus fumigatus isolates: identification of additional CSP types. Med Mycol 51:683-687. http://dx.doi.org/10.3109/13693786.2013.770609.
23. Klaassen CH, de Valk HA, Balajee SA, Meis JF. 2009. Utility of CSP typing to sub-type clinical Aspergillus fumigatus isolates and proposal for a new CSP type nomenclature. J Microbiol Methods 77:292-296. http://dx .doi.org/10.1016/j.mimet.2009.03.004.
24. de Valk HA, Meis JF, Curfs IM, Muehlethaler K, Mouton JW, Klaassen CH. 2005. Use of a novel panel of nine short tandem repeats for exact and high-resolution fingerprinting of Aspergillus fumigatus isolates. J Clin Microbiol 43:4112-4120. http://dx.doi.org/10.1128 /JCM.43.8.4112-4120.2005.
25. Steinmann J, Hamprecht A, Vehreschild MJ, Cornely OA, Buchheidt D, Spiess B, Koldehoff M, Buer J, Meis JF, Rath PM. 2015. Emergence of azole-resistant invasive aspergillosis in HSCT recipients in Germany. J Antimicrob Chemother 70:1522-1526. http://dx.doi.org /10.1093/jac/dku566.
26. Astvad KM, Jensen RH, Hassan TM, Mathiasen EG, Thomsen GM, Pedersen UG, Christensen M, Hilberg O, Arendrup MC. 2014. First detection of TR46/Y121F/T289A and TR34/L98H alterations in Aspergillus fumigatus isolates from azole-naive patients in Denmark despite negative findings in the environment. Antimicrob Agents Chemother 58:5096-5101. http://dx.doi.org/10.1128/AAC.02855-14.
27. Ahmad S, Joseph L, Hagen F, Meis JF, Khan Z. 2014. Concomitant occurrence of itraconazole-resistant and -susceptible strains of Aspergillus fumigatus in routine cultures. J Antimicrob Chemother 70:412-415. http: //dx.doi.org/10.1093/jac/dku410.
28. Al-WathiqiAhmad S, Khan Z, Hagen F, Meis JF. 2014. Occurrence of triazole-resistant Aspergillus fumigatus with TR/L98H mutations in outdoor and hospital environment in Kuwait. Environ Res 133C:20-26. http: //dx.doi.org/10.1016/j.envres.2014.05.009.
29. Tashiro M, Izumikawa K, Hirano K, Ide S, Mihara T, Hosogaya N, Takazono T, Morinaga Y, Nakamura S, Kurihara S, Imamura Y, Miyazaki T, Nishino T, Tsukamoto M, Kakeya H, Yamamoto Y, Yanagihara K, Yasuoka A, Tashiro T, Kohno S. 2012. Correlation between triazole treatment history and susceptibility in clinically isolated Aspergillus fumigatus. Antimicrob Agents Chemother 56:4870-4875. http://dx .doi.org/10.1128/AAC.00514-12.
30. Chowdhary A, Kathuria S, Xu J, Sharma C, Sundar G, Singh PK, Gaur SN, Hagen F, Klaassen CH, Meis JF. 2012. Clonal expansion and emergence of environmental multiple-triazole-resistant Aspergillus fumigatus strains carrying the TR(3)(4)/L98H mutations in the cyp51A gene in India. PLoS One 7:e52871. http://dx.doi.org/10.1371/journal.pone.0052871.
31. Badali H, Vaezi A, Haghani I, Yazdanparast SA, Hedayati MT, Mousavi B, Ansari S, Hagen F, Meis JF, Chowdhary A. 2013. Environmental study of azole-resistant Aspergillus fumigatus with TR34/L98H mutations in the cyp51A gene in Iran. Mycoses 56:659-663. http://dx.doi.org/10 .1111/myc.12089.
32. Mortensen KL, Jensen RH, Johansen HK, Skov M, Pressler T, Howard SJ, Leatherbarrow H, Mellado E, Arendrup MC. 2011. 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 49:2243-2251. http://dx.doi.org/10.1128/JCM .00213-11.
33. Fuhren J, Voskuil WS, Boel CH, Haas PJ, Hagen F, Meis JF, Kusters JG. 2015. High prevalence of azole resistance in Aspergillus fumigatus isolates from high-risk patients. J Antimicrob Chemother 70:2894-2898. http: //dx.doi.org/10.1093/jac/dkv177.
34. Wu CJ, Wang HC, Lee JC, Lo HJ, Dai CT, Chou PH, Ko WC, Chen YC. 2015. Azole-resistant Aspergillus fumigatus isolates carrying TR34/ L98H mutations in Taiwan. Mycoses 58:544-549. http://dx.doi.org/10 .1111/myc.12354.
35. Kidd SE, Goeman E, Meis JF, Slavin MA, Verweij PE. 2015. Multitriazole- resistant Aspergillus fumigatus infections in Australia. Mycoses 58:350-355. http://dx.doi.org/10.1111/myc.12324.
36. Sugui JA, Losada L, Wang W, Varga J, Ngamskulrungroj P, Abu-Asab M, Chang YC, O'Gorman CM, Wickes BL, Nierman WC, Dyer PS, Kwon-Chung KJ. 2011. Identification and characterization of an Aspergillus fumigatus "supermater" pair. mBio 2:e00234-11. http://dx.doi.org /10.1128/mBio.00234-11.
37. Howard SJ, Cerar D, Anderson MJ, Albarrag A, Fisher MC, Pasqualotto AC, Laverdiere M, Arendrup MC, Perlin DS, Denning DW. 2009. Frequency and evolution of Azole resistance in Aspergillus fumigatus associated with treatment failure. Emerg Infect Dis 15:1068-1076. http://dx .doi.org/10.3201/eid1507.090043.
38. Vermeulen E, Lagrou K, Verweij PE. 2013. Azole resistance in Aspergillus fumigatus: a growing public health concern. Curr Opin Infect Dis 26:493-500. http://dx.doi.org/10.1097/QCO.0000000000000005.
39. Lestrade PP, Meis JF, Arends JP, van der Beek MT, de Brauwer E, van Dijk K, de Greeff SC, Haas PJ, Hodiamont CJ, Kuijper EJ, Leenstra T, Muller AE, Oude Lashof AM, Rijnders BJ, Roelofsen E, Rozemeijer W, Tersmette M, Terveer EM, Verduin CM, Wolfhagen MJ, Melchers WJ, Verweij PE. 2016. Diagnosis and management of aspergillosis in the Netherlands: a national survey. Mycoses 59:101-107. http://dx.doi.org/10.1111 /myc.12440.
40. Camps SM, Rijs AJ, Klaassen CH, Meis JF, O'Gorman CM, Dyer PS, Melchers WJ, Verweij PE. 2012. Molecular epidemiology of Aspergillus fumigatus isolates harboring the TR34/L98H azole resistance mechanism. J Clin Microbiol 50:2674-2680. http://dx.doi.org/10.1128/JCM.00335-12.
41. Vanhee LM, Symoens F, Jacobsen MD, Nelis HJ, Coenye T. 2009. Comparison of multiple typing methods for Aspergillus fumigatus. Clin Microbiol Infect 15:643-650. http://dx.doi.org/10.1111/j.1469-0691.2009 .02844.x.
42. de Valk HA, Meis JF, Klaassen CH. 2007. Microsatellite based typing of Aspergillus fumigatus: strengths, pitfalls and solutions. J Microbiol Methods 69:268-272. http://dx.doi.org/10.1016/j.mimet.2007.01.009.
43. Heitman J, Carter DA, Dyer PS, Soll DR. 2014. Sexual reproduction of human fungal pathogens. Cold Spring Harb Perspect Med 4:a019281. http://dx.doi.org/10.1101/cshperspect.a019281.
44. Klaassen CH, Gibbons JG, Fedorova ND, Meis JF, Rokas A. 2012. Evidence for genetic differentiation and variable recombination rates among Dutch populations of the opportunistic human pathogen Aspergillus fumigatus. Mol Ecol 21:57-70. http://dx.doi.org/10.1111/j.1365-294X.2011.05364.x.
45. Wang Z. 2012. The status of fungicide market and its future trends. Market Information for Pesticides 6:22-23. (In Chinese.)
46. European Centre for Disease Prevention and Control. 2013. Technical report: risk assessment on the impact of environmental usage of triazoles on the development and spread of resistance to medical triazoles in Aspergillus species. ECDC, Solna, Sweden. http://ecdc.europa.eu /en/publications/Publications/risk-assessment-impact-environmental -usage-of-triazoles-on-Aspergillus-spp-resistance-to-medical-triazoles .pdf.