Distribution and antifungal susceptibility pattern of Candida species from mainland China: A systematic analysis

Figures & data

Figure 1. Studies identification and selection based on PRISMA guidelines.

Table 1 Characteristics of articles include in current systematic analysis (n = 89)

Characteristics	Frequency (%)	References
Species
C. albicans	65 (73.03%)	(14, 26, 27, 37-42, 44, 47-54, 56-60, 67-108)
C. tropicalis	47 (52.81%)	(14, 37-43, 47-49, 51, 52, 54, 57-60, 67-76, 93, 94, 97-102, 104, 107-117)
C. glabrata	43 (48.31%)	(14, 17, 37-40, 42-44, 47-52, 56-59, 67-76, 96-102, 104-106, 108, 118-120)
C. parapsilosis	37 (41.57%)	(5, 14, 37-41, 43, 48, 49, 51-58, 60, 71-76, 93-95, 97-102, 108, 118, 121)
C. krusei	16 (17.98%)	(14, 38, 43, 44, 56, 59, 97, 99-101, 104-106, 108, 122, 123)
C. guilliermondii	6 (6.74%)	(14, 97, 98, 108, 124, 125)
C. pelliculosa	3 (3.37%)	(98, 102, 108)
C. lusitaniae	3 (3.37%)	(14, 97, 108)
C. auris	2 (2.25%)	(16, 24)
C. haemulonii	1 (1.12%)	(126)
C. africana	1 (1.12%)	(103)
Patient type
Inpatients	35 (39.32%)	(16, 24, 26, 37-41, 47-54, 57-60, 68, 71, 72, 76, 89, 93, 102, 104, 105, 107, 111, 113, 115, 116, 118, 121)
Outpatients	3 (3.37%)	(70, 80, 96)
Both	12 (13.48%)	(14, 41, 55, 69, 94, 97, 98, 108, 110, 119, 120, 124)
NM	39 (43.82%)	NA
Age group
Adult	42 (47.19%)	(5, 24, 26, 37, 39, 40, 42, 44, 49, 51-54, 56, 57, 59, 60, 67, 69-72, 75, 78-80, 84, 85, 90, 91, 93, 95, 96, 100, 103, 106, 107, 115, 118-120, 124)
Adult/ Pediatrics	18 (20.22%)	(14, 17, 38, 47, 48, 50, 55, 58, 76, 94, 97-99, 101, 102, 108, 110, 121)
Age group NM	29 (32.58%)	NA
Gender
Female	19 (21.34%)	(26, 44, 69, 70, 75, 77-80, 85, 89-91, 95, 96, 100, 103, 106)
Male/Female	46 (51.68%)	(5, 14, 17, 24, 37-40, 42, 47-60, 67, 71, 72, 76, 87, 88, 93, 94, 97, 99, 102, 104, 107, 108, 110, 113, 115, 116, 118-121, 124)
NM	24 (26.97%)	NA
Infection types
Invasive Candidiasis	27 (30.33%)	(5, 14, 37, 41, 43, 47, 49, 50, 59, 60, 68, 73, 74, 94, 97-99, 102, 105, 108, 114, 115, 117, 120, 123-125)
Bloodstream infection	15 (16.85%)	(17, 39, 40, 48, 51-55, 57, 58, 71, 72, 76, 93)
Vulvovaginal candidiasis	20 (22.47%)	(26, 44, 69, 70, 75, 77-80, 83-85, 89-91, 95, 96, 100, 103, 106)
Oral candidiasis	5 (5.61%)	(42, 56, 67, 104, 107)
Multiple infections	8 (8.99%)	(16, 86, 87, 109-111, 116, 121)
UTI	1 (1.12%)	(113)
Not Mentioned.	13 (14.61%)	NA
Phenotypic identification methods
CHROMagar media	41 (46.06%)	(26, 37, 42, 44, 47, 50, 55, 56, 59, 67-70, 72, 75-83, 85-88, 91, 95, 96, 98, 99, 101-103, 105, 106, 109, 111, 112, 123)
MALDI-TOF MS	29 (32.58%)	(5, 16, 24, 38, 40, 43, 47, 48, 50, 57, 59, 67, 68, 80, 94, 97, 99, 102, 108, 110, 111, 113, 114, 116, 120, 121, 123, 124, 126)
API 20C AUX	21 (23.59%)	(26, 37, 41, 42, 55, 56, 70, 75, 77, 78, 83, 85, 87, 88, 95, 98-101, 105, 122)
VITEK 2 COMPACT	17 (19.10%)	(39, 41, 51-54, 58, 60, 67, 69, 72, 73, 76, 82, 96, 99, 106)
BD BACTEC™ FX	5 (5.61%)	(39, 40, 52, 53, 93)
VITEK MS system	2 (2.24%)	(14, 16)
Microscopy	2 (2.25%)	(85, 103)
DL-96A ID/AST	2 (2.25%)	(71, 118)
yeast identification kit	1 (1.12%)	(109)
ATB ID32C strips	1 (1.12%)	(27)
Brilliance Candida agar	1 (1.12%)	(41)
NM	4 (4.49%)	NA
Molecular identification methods
ITS sequencings	32 (35.95%)	(5, 14, 16, 24, 38, 41-43, 55, 67, 72-74, 79, 84, 85, 90, 92, 94, 97, 99, 102, 104, 107, 108, 110, 115, 120, 123-126)
D1/D2 analysis	6 (6.74%)	(24, 37, 41, 73, 84, 110)
Molecular beacon assay	1 (1.12%)	(96)
Susceptibility testing method
Broth microdilution	35 (39.32%)	(14, 17, 26, 56, 60, 67, 72-74, 77, 79-83, 85, 86, 89-92, 97, 99-101, 106, 109, 112-116, 120, 122, 123)
ATB FUNGUS 3 kit	24 (26.97%)	(27, 37, 39, 40, 47, 49-54, 57-59, 68-70, 78, 87, 88, 93, 96, 105, 119)
Sensititre Yeast-1 kit	16 (17.98%)	(5, 16, 24, 38, 42, 43, 48, 94, 102, 110, 111, 117, 120, 121, 124, 126)
Agar Diffusion method	12 (13.48%)	(41, 44, 75, 76, 95, 98, 103, 104, 107, 108, 110, 118)
ETEST method	2 (2.25%)	(37, 55)
kit of Autobio	1 (1.12%)	(71)
Neo-Sensitabs	1 (1.12%)	(84)
Breakpoint reference guidelines
CLSI	82 (92.13%)	(5, 14, 16, 17, 24, 26, 27, 37-43, 47-52, 55-57, 59, 60, 67-70, 72-75, 77-83, 85-126)
EUCAST	3 (3.37%)	(40, 52, 93)
NM	7 (7.86%)	NA

Footnote: The sum of percentages is not equal to 100 because some studies stated more than one variable, and we counted each study separately with each variable.

NM= Not mentioned, NA= Not applicable, UTI= urinary tract infection, ITS=internal transcribed spacer, CLSI= clinical laboratory and standard institutes, EUCAST= European committee of antimicrobial sensitivity testing

Table 2 The molecular typing of Candida species mentioned in the included studies

Species/ Method	Outcomes/Detail	References
C. albicans
MLST	DSTs: 79, 435, 1867, 365, 1395, 254, 443, 365, and CC 69	(26, 27)
Microsatellite markers	CAI and CP6	(37, 72)
RAPD analysis	Primer: 5’-ACGGCCGACC-3’ and 5’-CCAGATGCAC-3’	(78, 87)
C. tropicalis
MLST	DSTs; 225, 639, 329, 615, 506, 508, 519, 169, 345, 399, 300, 546, 376, 321, 322, 323, 324, 325, 114, 169, 326, 327, 328, 331, 332, 333, 334, 335, 336, 337, 338, 339, 340, 341, 164, 341, 342, 343, 344, 346, 347, 348, 349, 99, 350, 351, 352, 353, 354, 355, 356, 181, 615, 852, 984, 996, 991,482. 901, 330, 980, 337, 522, 990, 982, 998, 723, 983, 997, 977, 730, 489, 993, 403, 184, 139, 833, 889, 999, 995, 992, 986, 434, 981, 994, 394, 994, 437, 978, 525, 985, 923, 979, 986, 987, 988, 1000, 1001, 1002,	(72, 111, 113, 115, 116)
Microsatellite markers	ctm1, ctm3, ctm24	(117)
C. glabrata
MLST	STs: ST7, ST10, ST22, ST45, ST55, ST3,	(17, 72, 120)
Microsatellite markers	GLM5, RPM2, GLM4, ERG3, MTI, GLM6,	(17, 120)
C. parapsilosis
Microsatellite markers	CAI, CP6, B5, CP1, CP4,	(72, 121)
C. krusei
Microsatellite markers	33 markers were selected; Cakr001–Cakr033	(123)
C. guilliermondii
Microsatellite markers	sc15, sc32, sc72	(125)

Footnote: DSTs; Diploid sequence types, ST; Sequence types, MLST; multilocus sequence type. RAPD; Randomly amplified polymorphic DNA.

Figure 2. Prevalence of Candida species, (a) the total occurrence of Candida species, the numerical on the top of the bar is the number of specific Candida species, (b) the occurrence of Candida species in different regions of China, each region is represented by specific colour as shown in the box, Multiple locations mean the that studies mentioned more than one region of China, (c) Prevalence of Candida species in association with various infection type, OC; oral candidiasis, UTI; urinary tract infection, NM; not mentioned the infection type, MI; multiple infections, involved in more than one infections, VVC; vulvovaginal candidiasis, BSI; bloodstream infection, IC; invasive candidiasis.

Figure 3. Antifungal susceptibility patterns of Candida albicans in the form of median susceptibility/wild type with 95% confidence interval.

Figure 4. Antifungal susceptibility patterns of Candida tropicalis in the form of median susceptibility/wild type with 95% confidence interval.

Figure 5. Antifungal susceptibility patterns of Candida parapsilosis in the form of median susceptibility/wild type with 95% confidence interval.

Figure 6. Antifungal susceptibility patterns of Candida glabrata in the form of median susceptibility/wild type with 95% confidence interval.

Figure 7. Antifungal susceptibility patterns of Candida krusei in the form of median susceptibility/wild type with 95% confidence interval.

Figure 8. Antifungal susceptibility patterns of C. auris, C. pelliculosa, C. guilliermondii and C. lusitaniae in the form of median susceptibility/wild type with 95% confidence interval.

Table 3 Molecular mechanisms of antifungal drug resistance stated in the included studies

Mechanism	Detail	Outcome	Reference
C. albicans
ERG11 mutation	Amino acid substitution: A114S*, Y132H*, F449Y*, Q474K*, T123I*, Y257H*, G448E*, G464S*, F72S*, G450E*, Y132F*, K143Q*, K143R*, Y257H*, D116E, P56S, V88I, V437I, E266D, V488I, D116E/D, R523G, N440S, A114V, T285A, S457P, I333T, S24G, K90R, N168S, V234G, N237D, E260G, T285A, A317T, K344E, E517V, V332L, K128T, G448R, V488I, G448R/G, G465S, D225H, S199N, F104V, L935S, E260V, N435V, G472R and D502E, D117E, E165K, E174A, V234F, G346A, A434V, and L480F	Azole resistance	(26, 27, 70, 74, 80, 82, 83, 86, 88, 125)
Mrr2 mutation	Amino acid substitution: L144V*, T145A*, V451A*, S466L*, A468G*, S480P*, H31Y, T83A, H149Y, S165N, T386I and D404N	Azole resistance	(85)
ERG4 mutation	Silent mutation: CA133 and C435T	Azole resistance	(86)
ERG3 mutation	Amino acid substitution: A18P/A, R365G/R, W219C and R352H Silent mutations: T342G, T435C, C441T, T1047C	Azole resistance	(26, 89)
Efg1 mutation	Amino acid substitution: V86I Silent mutation: A150T, A165C, G210A, G267A, G279A, A285T, A744C, A786G, T954A, C1071T, A1055C, A1317G	Azole resistance	(89)
Cap1 mutation	Amino acid substitution: A390T, S381N, P311S, G481E	Azole resistance	(90)
Mrr1 mutation	Amino acid substitution: R557K*, K844E*, F1032L*, S1037L*, N937K, E1020Q, T917M and T923I	Azole resistance	(90)
Overexpression	ADH1, CDR1, CDR2, MDR1, FLU1, ERG11, TAC1, Cap1, MDR1, Mrr1	Azole resistance	(26, 27, 77, 81, 85, 90, 106)
C. glabrata
ERG 11 mutation	Mutations: T1328C, T1394C, G1487A, A1583G Amino acid substitution= no	Fluconazole resistance	(119)
MSH2 mutation	Polymorphism: V239L, E456D, R636 M	Azole resistance	(17)
PDR1 mutation	Amino acid substitution: G348C*, N764D*, E259G, E555D, N764D, D876N, S98L, R250K, G389V, R293G, S942F, L139I, E818G, Y336H, I378T, L669F, A848V, P76S, P143T, D243N, I91V, L732S, P927S	Azole resistance	(17, 119)
FKS2 mutation	S663F and S663P mutation in FKS2 HS1	Echinocandins resistance	(17)
Overexpression	CDR1, CDR2,	Azole resistance	(119)
C. tropicalis
ERG 11 mutation	Amino acid substitution: Y132F*, S154C*, A114S*, Y132H*, V125A, Y257H, and G464S	Azole resistance	(68, 94, 111, 112, 114)
Overexpression	Erg11, CDR1, MDR1	Azole resistance	(114)
C. krusei
ERG 11 mutation	Codon substitution: T939C, T642C, A756T	Azole resistance	(122)
Overexpression	Erg11	Azole resistance	(122)
C. auris
ERG 11 mutation	VF125AL and I74L mutation	Azole resistance	(16)
FKS1 mutation	S639F mutation	Echinocandins resistance	(16)
C. guilliermondii
ERG 11 mutation	Non-synonymous mutations: W37C, P518R, P430Q, D492N, Y41F, L328T, S346T, V410M, S420T, F39L, N485K, Y132F, S346T, G16S, M332I, R247K, G459S, G459K, K143R, Q469K	Azole resistance	(125)
C. haemulonii
ERG 11 mutation	Amino acid substitution: Y132H*	Azole resistance	(94)

*= Validated: mean all the amino acids found only in resistant strains and not in the susceptible isolates, and the authors discussed their azole resistance validity.

Xiao M, Chen SC, Kong F, et al. Distribution and antifungal susceptibility of candida species causing Candidemia in China: an update from the CHIF-NET study. J Infect Dis. 2020;221(Suppl 2):S139–s47. DOI:10.1093/infdis/jiz573

 PubMedGoogle Scholar

Yang ZH, Song YG, Li RY. A ten-year retrospective study of invasive Candidiasis in a tertiary hospital in Beijing. Biomed Environ Sci. 2021;34(10):773–788.

 PubMed Web of Science ®Google Scholar

Pu S, Niu S, Zhang C, et al. Epidemiology, antifungal susceptibilities, and risk factors for invasive candidiasis from 2011 to 2013 in a teaching hospital in southwest China. J Microbiol Immunol Infect. 2017;50(1):97–103. DOI:10.1016/j.jmii.2015.01.005

 PubMedGoogle Scholar

Pfaller MA, Castanheira M, Messer SA, et al. In vitro antifungal susceptibilities of isolates of Candida spp. And Aspergillus spp. From China to nine systemically active antifungal agents: data from the SENTRY antifungal surveillance program, 2010 through 2012. Mycoses. 2015;58(4):209–214.

 PubMed Web of Science ®Google Scholar

Wang B, Huang L, Zhao J, et al. ERG11 mutations associated with azole resistance in Candida albicans isolates from vulvovaginal candidosis patients. Asian Pac J Tropical Biomedicine. 2015;5:909–914.

 Google Scholar

Shi C, Liu J, Li W, et al. Expression of fluconazole resistance-associated genes in biofilm from 23 clinical isolates of Candida albicans. Braz J Microbiol. 2019;50(1):157–163.

 PubMed Web of Science ®Google Scholar

Liu JY, Shi C, Wang Y, et al. Mechanisms of azole resistance in Candida albicans clinical isolates from Shanghai, China. Res Microbiol. 2015;166(3):153–161.

 PubMed Web of Science ®Google Scholar

Hou X, Xiao M, Chen SC, et al. Molecular epidemiology and antifungal susceptibility of Candida glabrata in China (August 2009 to July 2014): a multi-center study. Front Microbiol. 2017;8:880.

 PubMed Web of Science ®Google Scholar

Liu Y, Kang M, Ye H, et al. Analysis on clinical characteristics and drug resistance of Candida parapsilosis bloodstream infections in West China Hospital, China, from 2012 to 2015. Journal de Mycologie Medicale. 2018;28(1):222–226.

 PubMed Web of Science ®Google Scholar

Sardi JCO, Scorzoni L, Bernardi T, et al. Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. J Med Microbiol. 2013;62(Pt 1):10–24.

 PubMed Web of Science ®Google Scholar

Hu L, Du X, Li T, et al. Genetic and phenotypic characterization of Candida albicans strains isolated from infectious disease patients in Shanghai. J Med Microbiol. 2015;64(Pt 1):74–83. DOI:10.1099/jmm.0.080200-0

 PubMedGoogle Scholar

Tsai MH, Hsu JF, Yang LY, et al. Candidemia due to uncommon Candida species in children: new threat and impacts on outcomes. Sci Rep. 2018;8(1):15239. DOI:10.1038/s41598-018-33662-x

 PubMed Web of Science ®Google Scholar

Dong D, Li Z, Zhang L, et al. Clinical and microbiological investigation of fungemia from four hospitals in China. Mycopathologia. 2015;179(5–6):407–414. DOI:10.1007/s11046-014-9855-0

 PubMed Web of Science ®Google Scholar

Guo H, Zhang XL, Gao LQ, et al. Alcohol dehydrogenase I expression correlates with CDR1, CDR2 and FLU1 expression in Candida albicans from patients with vulvovaginal candidiasis. Chin Med J (Engl). 2013;126(11):2098–2102.

 PubMed Web of Science ®Google Scholar

Ying C, Zhang H, Tang Z, et al. Antifungal susceptibility and molecular typing of 115 Candida albicans isolates obtained from vulvovaginal candidiasis patients in 3 Shanghai maternity hospitals. Med Mycol. 2016;54(4):394–399.

 PubMed Web of Science ®Google Scholar

Feng W, Yang J, Xi Z, et al. Regulatory role of ERG3 and Efg1 in Azoles-Resistant strains of Candida albicans isolated from patients diagnosed with Vulvovaginal Candidiasis. Indian J Microbiol. 2019;59(4):514–524. DOI:10.1007/s12088-019-00833-x

 PubMed Web of Science ®Google Scholar

Forsberg K, Woodworth K, Walters M, et al. Candida auris: the recent emergence of a multidrug-resistant fungal pathogen. Med Mycol. 2019;57(1):1–12. DOI:10.1093/mmy/myy054

 PubMed Web of Science ®Google Scholar

Briano F, Magnasco L, Sepulcri C, et al. Candida auris Candidemia in critically Ill, colonized patients: cumulative incidence and risk factors. Infect Dis Ther. 2022;11(3):1149–1160. DOI:10.1007/s40121-022-00625-9

 PubMed Web of Science ®Google Scholar

Yu SY, Zhang L, Chen S, et al. Candida isolates causing refractory or recurrent oropharyngeal candidiasis in 11 hospitals in China. Infect Drug Resist. 2019;12:865–875.

 PubMed Web of Science ®Google Scholar

Feng W, Yang J, Ji Y, et al. Mrr2 mutations and upregulation are associated with increased fluconazole resistance in Candida albicans isolates from patients with vulvovaginal candidiasis. Lett Appl Microbiol. 2020;70(2):95–101. DOI:10.1111/lam.13248

 PubMed Web of Science ®Google Scholar

Zhang L, Yang HF, Liu YY, et al. Reduced susceptibility of Candida albicans clinical isolates to azoles and detection of mutations in the ERG11 gene. Diagn Microbiol Infect Dis. 2013;77(4):327–329.

 PubMed Web of Science ®Google Scholar

Gong J, Xiao M, Wang H, et al. Genetic differentiation, diversity, and drug susceptibility of Candida krusei. Front Microbiol. 2018;9:2717.

 PubMed Web of Science ®Google Scholar

Lau AF, Kabir M, Chen SC, et al. Candida colonization as a risk marker for invasive candidiasis in mixed medical-surgical intensive care units: development and evaluation of a simple, standard protocol. J Clin Microbiol. 2015;53(4):1324–1330. DOI:10.1128/JCM.03239-14

 PubMed Web of Science ®Google Scholar

Munita JM, Arias CA. Mechanisms of antibiotic resistance. Microbiol Spectr. 2016;4(2). DOI:10.1128/microbiolspec.VMBF-0016-2015

 PubMed Web of Science ®Google Scholar

Cheng JW, Yu SY, Xiao M, et al. Identification and antifungal susceptibility profile of Candida guilliermondii and Candida fermentati from a multicenter study in China. J Clin Microbiol. 2016;54(8):2187–2189. DOI:10.1128/JCM.00938-16

 PubMed Web of Science ®Google Scholar

Sjölund M, Bonnedahl J, Hernandez J, et al. Dissemination of multidrug-resistant bacteria into the Arctic. Emerg Infect Dis. 2008;14(1):70–72. DOI:10.3201/eid1401.070704

 PubMed Web of Science ®Google Scholar

Dynowska M, Ejdys E, Biedunkiewicz A, et al. Yeasts isolated from frequently in-patients and out-patients. Ann Parasitol. 2014;60(3):199–206.

 PubMedGoogle Scholar

Hou X, Xiao M, Chen SC, et al. Identification and antifungal susceptibility profiles of Candida haemulonii species complex clinical isolates from a multicenter study in China. J Clin Microbiol. 2016;54(11):2676–2680. DOI:10.1128/JCM.01492-16

 PubMed Web of Science ®Google Scholar

Wu Y, Li C, Wang Z, et al. Clonal spread and azole-resistant mechanisms of non-susceptible Candida albicans isolates from vulvovaginal candidiasis patients in three Shanghai maternity hospitals. Med Mycol. 2018;56(6):687–694. DOI:10.1093/mmy/myx099

 PubMed Web of Science ®Google Scholar

Wang FJ, Zhang D, Liu ZH, et al. Species distribution and in vitro antifungal susceptibility of Vulvovaginal Candida isolates in China. Chin Med J (Engl). 2016;129(10):1161–1165.

 PubMed Web of Science ®Google Scholar

Diallo OO, Baron SA, Abat C, et al. Antibiotic resistance surveillance systems: a review. J Glob Antimicrob Resist. 2020;23:430–438.

 PubMed Web of Science ®Google Scholar

Mixão V, Gabaldón T. Genomic evidence for a hybrid origin of the yeast opportunistic pathogen Candida albicans. BMC Biol. 2020;18(1):48.

 PubMed Web of Science ®Google Scholar

Guo LN, Yu SY, Xiao M, et al. Species distribution and antifungal susceptibility of invasive Candidiasis: a 2016-2017 multicenter surveillance study in Beijing, China. Infect Drug Resist. 2020;13:2443–2452.

 PubMed Web of Science ®Google Scholar

Shi Y, Zhu Y, Fan S, et al. Molecular identification and antifungal susceptibility profile of yeast from vulvovaginal candidiasis. BMC Infect Dis. 2020;20(1):287.

 PubMed Web of Science ®Google Scholar

Zhang L, Zhou S, Pan A, et al. Surveillance of antifungal susceptibilities in clinical isolates of Candida species at 36 hospitals in China from 2009 to 2013. Int J Infect Dis. 2015;33:1–4.

 PubMed Web of Science ®Google Scholar

Zeng X, Peng M, Liu G, et al. Strain distribution and drug susceptibility of invasive fungal infection in clinical patients with systemic internal diseases. Front Bioeng Biotechnol. 2020;8:625024.

 PubMed Web of Science ®Google Scholar

Fan X, Xiao M, Liao K, et al. Notable increasing trend in Azole non-susceptible Candida tropicalis causing invasive Candidiasis in China (August 2009 to July 2014): molecular epidemiology and clinical Azole consumption. Front Microbiol. 2017;8:464.

 PubMed Web of Science ®Google Scholar

Verma R, Pradhan D, Hasan Z, et al. A systematic review on distribution and antifungal resistance pattern of Candida species in the Indian population. Med Mycol. 2021;59(12):1145–1165.

 PubMed Web of Science ®Google Scholar

Pappas PG, Lionakis MS, Arendrup MC, et al. Invasive candidiasis. Nat Rev Dis Primers. 2018;4:18026.

 PubMed Web of Science ®Google Scholar

Chapman B, Slavin M, Marriott D, et al. Changing epidemiology of candidaemia in Australia. J Antimicrob Chemother. 2017;72(4):1103–1108. DOI:10.1093/jac/dkx047

 PubMed Web of Science ®Google Scholar

Hachem R, Hanna H, Kontoyiannis D, et al. The changing epidemiology of invasive candidiasis: candida glabrata and Candida krusei as the leading causes of candidemia in hematologic malignancy. Cancer. 2008;112(11):2493–2499.

 PubMed Web of Science ®Google Scholar

Pristov KE, Ghannoum MA. Resistance of Candida to azoles and echinocandins worldwide. Clin Microbiol Infect. 2019;25(7):792–798.

 PubMed Web of Science ®Google Scholar

Whaley SG, Berkow EL, Rybak JM, et al. Azole antifungal resistance in Candida albicans and emerging non-albicans Candida species. Front Microbiol. 2016;7:2173.

 PubMed Web of Science ®Google Scholar

Guo LN, Xiao M, Cao B, et al. Epidemiology and antifungal susceptibilities of yeast isolates causing invasive infections across urban Beijing, China. Future Microbiol. 2017;12:1075–1086.

 PubMed Web of Science ®Google Scholar

Xiao M, Fan X, Chen SC, et al. Antifungal susceptibilities of Candida glabrata species complex, Candida krusei, Candida parapsilosis species complex and Candida tropicalis causing invasive candidiasis in China: 3 year national surveillance. J Antimicrob Chemother. 2015;70(3):802–810. DOI:10.1093/jac/dku460

 PubMed Web of Science ®Google Scholar

Feng W, Yang J, Wang Y, et al. ERG11 mutations and upregulation in clinical itraconazole-resistant isolates of Candida krusei. Can J Microbiol. 2016;62(11):938–943.

 PubMed Web of Science ®Google Scholar

Yang L, Su MQ, Ma YY, et al. Epidemiology, species distribution, antifungal susceptibility, and ERG11 mutations of Candida species isolated from pregnant Chinese Han women. Genet Mol Res. 2016;15(2):1–8.

 Web of Science ®Google Scholar

Shi XY, Yang YP, Zhang Y, et al. Molecular identification and antifungal susceptibility of 186 Candida isolates from vulvovaginal candidiasis in southern China. J Med Microbiol. 2015;64(Pt 4):390–393. DOI:10.1099/jmm.0.000024

 PubMedGoogle Scholar

Li W, Hu YA, Li FQ, et al. Distribution of yeast isolates from invasive infections and their in vitro susceptibility to antifungal agents: evidence from 299 cases in a 3-year (2010 to 2012) surveillance study. Mycopathologia. 2015;179(5–6):397–405. DOI:10.1007/s11046-015-9858-5

 PubMed Web of Science ®Google Scholar

Afsarian MH, Badali H, Boekhout T, et al. Multilocus sequence typing of Candida albicans isolates from a burn intensive care unit in Iran. J Med Microbiol. 2015;64(Pt 3):248–253.

 PubMedGoogle Scholar

Alastruey-Izquierdo A, Melhem MS, Bonfietti LX, et al. Susceptibility test for fungi: clinical and laboratorial correlations in medical mycology. Rev Inst Med Trop Sao Paulo. 2015;57 Suppl 19(Suppl 19):57–64.

 PubMedGoogle Scholar

Badiee P, Badali H, Boekhout T, et al. Antifungal susceptibility testing of Candida species isolated from the immunocompromised patients admitted to ten university hospitals in Iran: comparison of colonizing and infecting isolates. BMC Infect Dis. 2017;17(1):727. DOI:10.1186/s12879-017-2825-7

 PubMedGoogle Scholar

Wang H, Liu N, Yin M, et al. The epidemiology, antifungal use and risk factors of death in elderly patients with candidemia: a multicentre retrospective study. BMC Infect Dis. 2014;14:609.

 PubMed Web of Science ®Google Scholar

Wang B, He X, Lu F, et al. Candida isolates from blood and other normally sterile Foci from ICU patients: determination of epidemiology, antifungal susceptibility profile and evaluation of associated risk factors. Front Public Health. 2021;9:779590.

 PubMed Web of Science ®Google Scholar

Luo X, Dong X, Pen Z. Distribution and drug susceptibility of Candida spp. Associated with female genital tract infection, Chongqing, China. Jundishapur J Microbiol. 2016;9(10):e19386.

 PubMed Web of Science ®Google Scholar

Lin S, Chen R, Zhu S, et al. Candidemia in adults at a tertiary hospital in China: clinical characteristics, species distribution, resistance, and outcomes. Mycopathologia. 2018;183(4):679–689. DOI:10.1007/s11046-018-0258-5

 PubMed Web of Science ®Google Scholar

Feng W, Yang J, Xi Z, et al. Mutations and/or Overexpressions of ERG4 and ERG11 genes in clinical Azoles-Resistant isolates of Candida albicans. Microbial Drug Resist (Larchmont, NY). 2017;23(5):563–570. DOI:10.1089/mdr.2016.0095

 PubMed Web of Science ®Google Scholar

Zhai Y, Liu J, Zhou L, et al. Detection of Candida species in pregnant Chinese women with a molecular beacon method. J Med Microbiol. 2018;67(6):783–789. DOI:10.1099/jmm.0.000740

 PubMed Web of Science ®Google Scholar

Wu J, Guo H, Yi G, et al. Prevalent drug resistance among oral yeasts from asymptomatic patients in Hainan, China. Mycopathologia. 2014;177(5–6):299–307. DOI:10.1007/s11046-014-9747-3

 PubMed Web of Science ®Google Scholar

Jiang C, Dong D, Yu B, et al. Mechanisms of azole resistance in 52 clinical isolates of Candida tropicalis in China. J Antimicrob Chemother. 2013;68(4):778–785. DOI:10.1093/jac/dks481

 PubMed Web of Science ®Google Scholar

Wang Q, Li C, Tang D, et al. Molecular epidemiology of Candida tropicalis isolated from urogenital tract infections. Microbiologyopen. 2020;9(11):e1121.

 PubMed Web of Science ®Google Scholar

Hou X, Xiao M, Wang H, et al. Profiling of PDR1 and MSH2 in Candida glabrata bloodstream isolates from a multicenter study in China. Antimicrob Agents Chemother. 2018;62(6): DOI:10.1128/AAC.00153-18

 Web of Science ®Google Scholar

Yang W, Ji X. Analysis of the microbial species, antimicrobial sensitivity and drug resistance in 2652 patients of nursing hospital. Heliyon. 2020;6(5):e03965.

 PubMed Web of Science ®Google Scholar

Zhang L, Yu SY, Chen SC, et al. Molecular Characterization of Candida parapsilosis by microsatellite typing and emergence of clonal antifungal drug resistant strains in a multicenter surveillance in China. Front Microbiol. 2020;11:1320.

 PubMed Web of Science ®Google Scholar

Tian S, Bing J, Chu Y, et al. Genomic epidemiology of Candida auris in a general hospital in Shenyang, China: a three-year surveillance study. Emerging Microbes Infect. 2021;10(1):1088–1096. DOI:10.1080/22221751.2021.1934557

 PubMed Web of Science ®Google Scholar

Zhang Z, Bai HH, Wang FJ, et al. Analysis of homology and drug sensitivity of vaginal isolates of 10 patients with recurrent vulvovaginal candidiasis in recurrent episodes. Zhonghua Fu Chan Ke Za Zhi. 2020;55(3):177–182. DOI:10.3760/cma.j.cn112141-20191210-00665

 PubMedGoogle Scholar

Ma CF, Li FQ, Shi LN, et al. Surveillance study of species distribution, antifungal susceptibility and mortality of nosocomial candidemia in a tertiary care hospital in China. BMC Infect Dis. 2013;13:337.

 PubMed Web of Science ®Google Scholar

Yan L, Wang XD, Seyedmousavi S, et al. Antifungal susceptibility profile of Candida Albicans isolated from Vulvovaginal Candidiasis in Xinjiang Province of China. Mycopathologia. 2019;184(3):413–422. DOI:10.1007/s11046-018-0305-2

 PubMed Web of Science ®Google Scholar

Xu H, Liu M, Chen Y, et al. Randomly amplified polymorphic deoxyribonucleic acid (DNA) analysis of Candida albicans isolates from clinical sources of hospital in south China. Afr J Microbiol Res. 2012;6(10): 2552–2558.

 Google Scholar

Tian S, Rong C, Nian H, et al. First cases and risk factors of super yeast Candida auris infection or colonization from Shenyang, China. Emerging Microbes Infect. 2018;7(1):128. DOI:10.1038/s41426-018-0131-0

 PubMed Web of Science ®Google Scholar

Fan X, Xiao M, Wang H, et al. Multilocus sequence typing indicates diverse origins of invasive Candida tropicalis isolates in China. Chin Med J (Engl). 2014;127(24):4226–4234.

 PubMed Web of Science ®Google Scholar

Wang Q, Tang D, Tang K, et al. Multilocus sequence typing reveals clonality of Fluconazole-Nonsusceptible Candida tropicalis: a Study from Wuhan to the Global. Front Microbiol. 2020;11:554249.

 PubMed Web of Science ®Google Scholar

Cheng JW, Liao K, Kudinha T, et al. Molecular epidemiology and azole resistance mechanism study of Candida guilliermondii from a Chinese surveillance system. Sci Rep. 2017;7(1):907. DOI:10.1038/s41598-017-01106-7

 PubMedGoogle Scholar

Xu H, Yu SY, Zhou ML, et al. Epidemiology and antifungal susceptibility patterns of invasive fungal infections from 2012 to 2014 in a teaching hospital in central China. Infect Drug Resist. 2019;12:3641–3651.

 PubMed Web of Science ®Google Scholar

Shan Y, Fan S, Liu X, et al. Prevalence of Candida albicans-closely related yeasts, Candida africana and Candida dubliniensis, in vulvovaginal candidiasis. Med Mycol. 2014;52(6):636–640.

 PubMed Web of Science ®Google Scholar

Gupta AK, Venkataraman M. Antifungal resistance in Superficial mycoses. J Dermatolog Treat. 2021;32:1–25.

 PubMedGoogle Scholar

Corcione S, D’Avolio A, Pasero D, et al. Acquisition of FKS2 mutation after echinocandin treatment of infective endocarditis by Candida glabrata. Le Infezioni in Medicina. 2019;27(3):328–331.

 PubMedGoogle Scholar

Fan X, Xiao M, Zhang D, et al. Molecular mechanisms of azole resistance in Candida tropicalis isolates causing invasive candidiasis in China. Clin Microbiol Infect. 2019;25(7):885–891. DOI:10.1016/j.cmi.2018.11.007

 PubMed Web of Science ®Google Scholar

Chow NA, Gade L, Tsay SV, et al. Multiple introductions and subsequent transmission of multidrug-resistant Candida auris in the USA: a molecular epidemiological survey. Lancet Infect Dis. 2018;18(12):1377–1384. DOI:10.1016/S1473-3099(18)30597-8

 PubMed Web of Science ®Google Scholar

Lamoth F, Lockhart SR, Berkow EL, et al. Changes in the epidemiological landscape of invasive candidiasis. J Antimicrob Chemother. 2018;73(suppl_1):i4–i13.

 PubMed Web of Science ®Google Scholar

Zhang JY, Liu JH, Liu FD, et al. Vulvovaginal candidiasis: species distribution, fluconazole resistance and drug efflux pump gene overexpression. Mycoses. 2014;57(10):584–591. DOI:10.1111/myc.12204

 PubMed Web of Science ®Google Scholar

Wu J, Gan C, Li J, et al. Species diversity and antifungal susceptibilities of oral yeasts from patients with head and neck cancer. Infect Drug Resist. 2021;14:2279–2288.

 PubMed Web of Science ®Google Scholar

Jin L, Cao Z, Wang Q, et al. MDR1 overexpression combined with ERG11 mutations induce high-level fluconazole resistance in Candida tropicalis clinical isolates. BMC Infect Dis. 2018;18(1):162. DOI:10.1186/s12879-018-3082-0

 PubMedGoogle Scholar

Wang Y, Fan X, Wang H, et al. Continual decline in Azole susceptibility rates in Candida tropicalis over a 9-year period in China. Front Microbiol. 2021;12:702839.

 PubMed Web of Science ®Google Scholar

Ying Y, Zhao Y, Hu X, et al. In vitro fluconazole susceptibility of 1,903 clinical isolates of Candida albicans and the identification of ERG11 mutations. Microbial Drug Resist (Larchmont, NY). 2013;19(4):266–273. DOI:10.1089/mdr.2012.0204

 PubMed Web of Science ®Google Scholar

Xiao M, Sun ZY, Kang M, et al. Five-Year national surveillance of invasive Candidiasis: species distribution and Azole susceptibility from the China Hospital Invasive Fungal Surveillance Net (CHIF-NET) Study. J Clin Microbiol. 2018;56(7): DOI:10.1128/JCM.00577-18

 Web of Science ®Google Scholar

Yao D, Chen J, Chen W, et al. Mechanisms of azole resistance in clinical isolates of Candida glabrata from two hospitals in China. Infect Drug Resist. 2019;12:771–781.

 PubMed Web of Science ®Google Scholar

Wickes BL, Wiederhold NP. Molecular diagnostics in medical mycology. Nat Commun. 2018;9(1):5135.

 PubMedGoogle Scholar

Wang D, An N, Yang Y, et al. Candida tropicalis distribution and drug resistance is correlated with ERG11 and UPC2 expression. Antimicrob Resist Infect Control. 2021;10(1):54.

 PubMed Web of Science ®Google Scholar

Data availability statement

Data supporting our study can be provided by demand from the corresponding author (email: [email protected]) or the first author (email: [email protected]).