Skip to main content
Top
Published in: European Journal of Clinical Microbiology & Infectious Diseases 4/2015

01-04-2015 | Article

Molecular epidemiology of Cryptococcus neoformans and Cryptococcus gattii in China between 2007 and 2013 using multilocus sequence typing and the DiversiLab system

Authors: H.-T. Dou, Y.-C. Xu, H.-Z. Wang, T.-S. Li

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 4/2015

Login to get access

Abstract

The purpose of this study was to investigate the molecular characteristics of 83 clinical Cryptococcus neoformans/C. gattii species complex isolated in Beijing, China, between 2007 and 2013. Restriction fragment length polymorphism of the gene URA5 (URA5-RFLP), multilocus sequence typing (MLST), and automated repetitive polymerase chain reaction (rep-PCR; DiversiLab system) were performed to genotype these cryptococcal isolates. There was an excellent correlation amongst the three methods; however, PU157 was assigned as VNII according to URA5-RFLP, while it was classified as VNI by the DiversiLab system analysis. PU157 was finally identified as VNB by seven-locus MLST analysis. Moreover, though AD hybrids could not be processed by MLST, ideal results could be obtained by the DiversiLab system. The genotype VNI accounted for 95.2 % (79/83) of isolates. Besides one strain of VNB, VNIII, and VGI each, a strain of VGII was detected in our study, which was isolated from a patient from the temperate region in North China. In addition, the most common MLST sequence type (ST) was ST5, accounting for 91.6 % (76/83), followed by ST31, ST63, ST182, ST295, ST296, and ST332. ST295, ST296, and ST332 were new STs. Except for isolate PU157 (VNB), identical results were obtained quickly and accurately through the DiversiLab system compared to MLST and URA5-RFLP. The discovery of VNB and VGII in the temperate climate regions of China suggested that the population structure of C. neoformans and C. gattii should be explored more extensively. Our results also showed that the DiversiLab system can be used in the genotyping of C. neoformans and C. gattii.
Literature
2.
go back to reference Liao Y, Chen M, Hartmann T, Yang RY, Liao WQ (2013) Epidemiology of opportunistic invasive fungal infections in China: review of literature. Chin Med J (Engl) 126:361–368 Liao Y, Chen M, Hartmann T, Yang RY, Liao WQ (2013) Epidemiology of opportunistic invasive fungal infections in China: review of literature. Chin Med J (Engl) 126:361–368
4.
go back to reference Ellis DH, Pfeiffer TJ (1990) Ecology, life cycle, and infectious propagule of Cryptococcus neoformans. Lancet 336:923–925CrossRefPubMed Ellis DH, Pfeiffer TJ (1990) Ecology, life cycle, and infectious propagule of Cryptococcus neoformans. Lancet 336:923–925CrossRefPubMed
5.
go back to reference Kidd SE, Hagen F, Tscharke RL, Huynh M, Bartlett KH, Fyfe M, Macdougall L, Boekhout T, Kwon-Chung KJ, Meyer W (2004) A rare genotype of Cryptococcus gattii caused the cryptococcosis outbreak on Vancouver Island (British Columbia, Canada). Proc Natl Acad Sci U S A 101:17258–17263. doi:10.1073/pnas.0402981101 CrossRefPubMedCentralPubMed Kidd SE, Hagen F, Tscharke RL, Huynh M, Bartlett KH, Fyfe M, Macdougall L, Boekhout T, Kwon-Chung KJ, Meyer W (2004) A rare genotype of Cryptococcus gattii caused the cryptococcosis outbreak on Vancouver Island (British Columbia, Canada). Proc Natl Acad Sci U S A 101:17258–17263. doi:10.​1073/​pnas.​0402981101 CrossRefPubMedCentralPubMed
7.
go back to reference Byrnes EJ 3rd, Bildfell RJ, Frank SA, Mitchell TG, Marr KA, Heitman J (2009) Molecular evidence that the range of the Vancouver Island outbreak of Cryptococcus gattii infection has expanded into the Pacific Northwest in the United States. J Infect Dis 199:1081–1086. doi:10.1086/597306 CrossRefPubMedCentralPubMed Byrnes EJ 3rd, Bildfell RJ, Frank SA, Mitchell TG, Marr KA, Heitman J (2009) Molecular evidence that the range of the Vancouver Island outbreak of Cryptococcus gattii infection has expanded into the Pacific Northwest in the United States. J Infect Dis 199:1081–1086. doi:10.​1086/​597306 CrossRefPubMedCentralPubMed
8.
go back to reference Hagen F, Ceresini PC, Polacheck I, Ma H, van Nieuwerburgh F, Gabaldón T, Kagan S, Pursall ER, Hoogveld HL, van Iersel LJ, Klau GW, Kelk SM, Stougie L, Bartlett KH, Voelz K, Pryszcz LP, Castañeda E, Lazera M, Meyer W, Deforce D, Meis JF, May RC, Klaassen CH, Boekhout T (2013) Ancient dispersal of the human fungal pathogen Cryptococcus gattii from the Amazon rainforest. PLoS One 8:e71148. doi:10.1371/journal.pone.0071148 CrossRefPubMedCentralPubMed Hagen F, Ceresini PC, Polacheck I, Ma H, van Nieuwerburgh F, Gabaldón T, Kagan S, Pursall ER, Hoogveld HL, van Iersel LJ, Klau GW, Kelk SM, Stougie L, Bartlett KH, Voelz K, Pryszcz LP, Castañeda E, Lazera M, Meyer W, Deforce D, Meis JF, May RC, Klaassen CH, Boekhout T (2013) Ancient dispersal of the human fungal pathogen Cryptococcus gattii from the Amazon rainforest. PLoS One 8:e71148. doi:10.​1371/​journal.​pone.​0071148 CrossRefPubMedCentralPubMed
9.
go back to reference Meyer W, Aanensen DM, Boekhout T, Cogliati M, Diaz MR, Esposto MC, Fisher M, Gilgado F, Hagen F, Kaocharoen S, Litvintseva AP, Mitchell TG, Simwami SP, Trilles L, Viviani MA, Kwon-Chung J (2009) Consensus multi-locus sequence typing scheme for Cryptococcus neoformans and Cryptococcus gattii. Med Mycol 47:561–570. doi:10.1080/13693780902953886 CrossRefPubMedCentralPubMed Meyer W, Aanensen DM, Boekhout T, Cogliati M, Diaz MR, Esposto MC, Fisher M, Gilgado F, Hagen F, Kaocharoen S, Litvintseva AP, Mitchell TG, Simwami SP, Trilles L, Viviani MA, Kwon-Chung J (2009) Consensus multi-locus sequence typing scheme for Cryptococcus neoformans and Cryptococcus gattii. Med Mycol 47:561–570. doi:10.​1080/​1369378090295388​6 CrossRefPubMedCentralPubMed
15.
go back to reference Perfect JR, Ketabchi N, Cox GM, Ingram CW, Beiser CL (1993) Karyotyping of Cryptococcus neoformans as an epidemiological tool. J Clin Microbiol 31:3305–3309PubMedCentralPubMed Perfect JR, Ketabchi N, Cox GM, Ingram CW, Beiser CL (1993) Karyotyping of Cryptococcus neoformans as an epidemiological tool. J Clin Microbiol 31:3305–3309PubMedCentralPubMed
16.
go back to reference Meyer W, Marszewska K, Amirmostofian M, Igreja RP, Hardtke C, Methling K, Viviani MA, Chindamporn A, Sukroongreung S, John MA, Ellis DH, Sorrell TC (1999) Molecular typing of global isolates of Cryptococcus neoformans var. neoformans by polymerase chain reaction fingerprinting and randomly amplified polymorphic DNA—a pilot study to standardize techniques on which to base a detailed epidemiological survey. Electrophoresis 20:1790–1799. doi:10.1002/(SICI)1522-2683(19990101)20:8<1790::AID-ELPS1790>3.0.CO;2-2 CrossRefPubMed Meyer W, Marszewska K, Amirmostofian M, Igreja RP, Hardtke C, Methling K, Viviani MA, Chindamporn A, Sukroongreung S, John MA, Ellis DH, Sorrell TC (1999) Molecular typing of global isolates of Cryptococcus neoformans var. neoformans by polymerase chain reaction fingerprinting and randomly amplified polymorphic DNA—a pilot study to standardize techniques on which to base a detailed epidemiological survey. Electrophoresis 20:1790–1799. doi:10.​1002/​(SICI)1522-2683(19990101)20:​8<1790:​:​AID-ELPS1790>3.​0.​CO;2-2 CrossRefPubMed
19.
go back to reference Mihara T, Izumikawa K, Kakeya H, Ngamskulrungroj P, Umeyama T, Takazono T, Tashiro M, Nakamura S, Imamura Y, Miyazaki T, Ohno H, Yamamoto Y, Yanagihara K, Miyzaki Y, Kohno S (2013) Multilocus sequence typing of Cryptococcus neoformans in non-HIV associated cryptococcosis in Nagasaki, Japan. Med Mycol 51:252–260. doi:10.3109/13693786.2012.708883 CrossRefPubMed Mihara T, Izumikawa K, Kakeya H, Ngamskulrungroj P, Umeyama T, Takazono T, Tashiro M, Nakamura S, Imamura Y, Miyazaki T, Ohno H, Yamamoto Y, Yanagihara K, Miyzaki Y, Kohno S (2013) Multilocus sequence typing of Cryptococcus neoformans in non-HIV associated cryptococcosis in Nagasaki, Japan. Med Mycol 51:252–260. doi:10.​3109/​13693786.​2012.​708883 CrossRefPubMed
20.
go back to reference Boekhout T, Theelen B, Diaz M, Fell JW, Hop WC, Abeln EC, Dromer F, Meyer W (2001) Hybrid genotypes in the pathogenic yeast Cryptococcus neoformans. Microbiology 147:891–907PubMed Boekhout T, Theelen B, Diaz M, Fell JW, Hop WC, Abeln EC, Dromer F, Meyer W (2001) Hybrid genotypes in the pathogenic yeast Cryptococcus neoformans. Microbiology 147:891–907PubMed
21.
go back to reference Hagen F, Chowdhary A, Prakash A, Yntema JB, Meis JF (2014) Molecular characterization of Cryptococcus gattii genotype AFLP6/VGII isolated from woody debris of divi-divi (Caesalpinia coriaria), Bonaire, Dutch Caribbean. Rev Iberoam Micol 31:193–196. doi:10.1016/j.riam.2013.10.007 CrossRefPubMed Hagen F, Chowdhary A, Prakash A, Yntema JB, Meis JF (2014) Molecular characterization of Cryptococcus gattii genotype AFLP6/VGII isolated from woody debris of divi-divi (Caesalpinia coriaria), Bonaire, Dutch Caribbean. Rev Iberoam Micol 31:193–196. doi:10.​1016/​j.​riam.​2013.​10.​007 CrossRefPubMed
22.
go back to reference Fraser JA, Giles SS, Wenink EC, Geunes-Boyer SG, Wright JR, Diezmann S, Allen A, Stajich JE, Dietrich FS, Perfect JR, Heitman J (2005) Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 437:1360–1364. doi:10.1038/nature04220 CrossRefPubMed Fraser JA, Giles SS, Wenink EC, Geunes-Boyer SG, Wright JR, Diezmann S, Allen A, Stajich JE, Dietrich FS, Perfect JR, Heitman J (2005) Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 437:1360–1364. doi:10.​1038/​nature04220 CrossRefPubMed
23.
go back to reference Pan W, Khayhan K, Hagen F, Wahyuningsih R, Chakrabarti A, Chowdhary A, Ikeda R, Taj-Aldeen SJ, Khan Z, Imran D, Sjam R, Sriburee P, Liao W, Chaicumpar K, Ingviya N, Mouton JW, Curfs-Breuker I, Boekhout T, Meis JF, Klaassen CH (2012) Resistance of Asian Cryptococcus neoformans serotype A is confined to few microsatellite genotypes. PLoS One 7:e32868. doi:10.1371/journal.pone.0032868 CrossRefPubMedCentralPubMed Pan W, Khayhan K, Hagen F, Wahyuningsih R, Chakrabarti A, Chowdhary A, Ikeda R, Taj-Aldeen SJ, Khan Z, Imran D, Sjam R, Sriburee P, Liao W, Chaicumpar K, Ingviya N, Mouton JW, Curfs-Breuker I, Boekhout T, Meis JF, Klaassen CH (2012) Resistance of Asian Cryptococcus neoformans serotype A is confined to few microsatellite genotypes. PLoS One 7:e32868. doi:10.​1371/​journal.​pone.​0032868 CrossRefPubMedCentralPubMed
25.
go back to reference Wise MG, Healy M, Reece K, Smith R, Walton D, Dutch W, Renwick A, Huong J, Young S, Tarrand J, Kontoyiannis DP (2007) Species identification and strain differentiation of clinical Candida isolates using the DiversiLab system of automated repetitive sequence-based PCR. J Med Microbiol 56:778–787. doi:10.1099/jmm.0.47106-0 CrossRefPubMed Wise MG, Healy M, Reece K, Smith R, Walton D, Dutch W, Renwick A, Huong J, Young S, Tarrand J, Kontoyiannis DP (2007) Species identification and strain differentiation of clinical Candida isolates using the DiversiLab system of automated repetitive sequence-based PCR. J Med Microbiol 56:778–787. doi:10.​1099/​jmm.​0.​47106-0 CrossRefPubMed
26.
go back to reference Treviño M, García-Riestra C, Areses P, García X, Navarro D, Suárez FJ, López-Dequidt IA, Zaragoza O, Cuenca-Estrella M (2014) Emerging Trichosporon asahii in elderly patients: epidemiological and molecular analysis by the DiversiLab system. Eur J Clin Microbiol Infect Dis 33:1497–1503. doi:10.1007/s10096-014-2099-6 CrossRefPubMed Treviño M, García-Riestra C, Areses P, García X, Navarro D, Suárez FJ, López-Dequidt IA, Zaragoza O, Cuenca-Estrella M (2014) Emerging Trichosporon asahii in elderly patients: epidemiological and molecular analysis by the DiversiLab system. Eur J Clin Microbiol Infect Dis 33:1497–1503. doi:10.​1007/​s10096-014-2099-6 CrossRefPubMed
31.
go back to reference Kwon-Chung KJ, Polacheck I, Bennett JE (1982) Improved diagnostic medium for separation of Cryptococcus neoformans var. neoformans (serotypes A and D) and Cryptococcus neoformans var. gattii (serotypes B and C). J Clin Microbiol 15:535–537PubMedCentralPubMed Kwon-Chung KJ, Polacheck I, Bennett JE (1982) Improved diagnostic medium for separation of Cryptococcus neoformans var. neoformans (serotypes A and D) and Cryptococcus neoformans var. gattii (serotypes B and C). J Clin Microbiol 15:535–537PubMedCentralPubMed
34.
go back to reference Choi YH, Ngamskulrungroj P, Varma A, Sionov E, Hwang SM, Carriconde F, Meyer W, Litvintseva AP, Lee WG, Shin JH, Kim EC, Lee KW, Choi TY, Lee YS, Kwon-Chung KJ (2010) Prevalence of the VNIc genotype of Cryptococcus neoformans in non-HIV-associated cryptococcosis in the Republic of Korea. FEMS Yeast Res 10:769–778. doi:10.1111/j.1567-1364.2010.00648.x CrossRefPubMedCentralPubMed Choi YH, Ngamskulrungroj P, Varma A, Sionov E, Hwang SM, Carriconde F, Meyer W, Litvintseva AP, Lee WG, Shin JH, Kim EC, Lee KW, Choi TY, Lee YS, Kwon-Chung KJ (2010) Prevalence of the VNIc genotype of Cryptococcus neoformans in non-HIV-associated cryptococcosis in the Republic of Korea. FEMS Yeast Res 10:769–778. doi:10.​1111/​j.​1567-1364.​2010.​00648.​x CrossRefPubMedCentralPubMed
36.
go back to reference Khayhan K, Hagen F, Pan W, Simwami S, Fisher MC, Wahyuningsih R, Chakrabarti A, Chowdhary A, Ikeda R, Taj-Aldeen SJ, Khan Z, Ip M, Imran D, Sjam R, Sriburee P, Liao W, Chaicumpar K, Vuddhakul V, Meyer W, Trilles L, van Iersel LJ, Meis JF, Klaassen CH, Boekhout T (2013) Geographically structured populations of Cryptococcus neoformans variety grubii in Asia correlate with HIV status and show a clonal population structure. PLoS One 8:e72222. doi:10.1371/journal.pone.0072222 CrossRefPubMedCentralPubMed Khayhan K, Hagen F, Pan W, Simwami S, Fisher MC, Wahyuningsih R, Chakrabarti A, Chowdhary A, Ikeda R, Taj-Aldeen SJ, Khan Z, Ip M, Imran D, Sjam R, Sriburee P, Liao W, Chaicumpar K, Vuddhakul V, Meyer W, Trilles L, van Iersel LJ, Meis JF, Klaassen CH, Boekhout T (2013) Geographically structured populations of Cryptococcus neoformans variety grubii in Asia correlate with HIV status and show a clonal population structure. PLoS One 8:e72222. doi:10.​1371/​journal.​pone.​0072222 CrossRefPubMedCentralPubMed
37.
go back to reference Simwami SP, Khayhan K, Henk DA, Aanensen DM, Boekhout T, Hagen F, Brouwer AE, Harrison TS, Donnelly CA, Fisher MC (2011) Low diversity Cryptococcus neoformans variety grubii multilocus sequence types from Thailand are consistent with an ancestral African origin. PLoS Pathog 7:e1001343. doi:10.1371/journal.ppat.1001343 CrossRefPubMedCentralPubMed Simwami SP, Khayhan K, Henk DA, Aanensen DM, Boekhout T, Hagen F, Brouwer AE, Harrison TS, Donnelly CA, Fisher MC (2011) Low diversity Cryptococcus neoformans variety grubii multilocus sequence types from Thailand are consistent with an ancestral African origin. PLoS Pathog 7:e1001343. doi:10.​1371/​journal.​ppat.​1001343 CrossRefPubMedCentralPubMed
38.
go back to reference Tseng HK, Liu CP, Ho MW, Lu PL, Lo HJ, Lin YH, Cho WL, Chen YC; Taiwan Infectious Diseases Study Network for Cryptococcosis (2013) Microbiological, epidemiological, and clinical characteristics and outcomes of patients with cryptococcosis in Taiwan, 1997–2010. PLoS One 8:e61921. doi:10.1371/journal.pone.0061921 CrossRefPubMedCentralPubMed Tseng HK, Liu CP, Ho MW, Lu PL, Lo HJ, Lin YH, Cho WL, Chen YC; Taiwan Infectious Diseases Study Network for Cryptococcosis (2013) Microbiological, epidemiological, and clinical characteristics and outcomes of patients with cryptococcosis in Taiwan, 1997–2010. PLoS One 8:e61921. doi:10.​1371/​journal.​pone.​0061921 CrossRefPubMedCentralPubMed
Metadata
Title
Molecular epidemiology of Cryptococcus neoformans and Cryptococcus gattii in China between 2007 and 2013 using multilocus sequence typing and the DiversiLab system
Authors
H.-T. Dou
Y.-C. Xu
H.-Z. Wang
T.-S. Li
Publication date
01-04-2015
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 4/2015
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-014-2289-2

Other articles of this Issue 4/2015

European Journal of Clinical Microbiology & Infectious Diseases 4/2015 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine