Skip to main content
Log in

Epidemiology of fungal infections in China

  • Review
  • Published:
Frontiers of Medicine Aims and scope Submit manuscript

Abstract

With the increasing number of immunocompromised hosts, the epidemiological characteristics of fungal infections have undergone enormous changes worldwide, including in China. In this paper, we reviewed the existing data on mycosis across China to summarize available epidemiological profiles. We found that the general incidence of superficial fungal infections in China has been stable, but the incidence of tinea capitis has decreased and the transmission route has changed. By contrast, the overall incidence of invasive fungal infections has continued to rise. The occurrence of candidemia caused by Candida species other than C. albicans and including some uncommon Candida species has increased recently in China. Infections caused by Aspergillus have also propagated in recent years, particularly with the emergence of azole-resistant Aspergillus fumigatus. An increasing trend of cryptococcosis has been noted in China, with Cryptococcus neoformans var. grubii ST 5 genotype isolates as the predominant pathogen. Retrospective studies have suggested that the epidemiological characteristics of Pneumocystis pneumonia in China may be similar to those in other developing countries. Endemic fungal infections, such as sporotrichosis in Northeastern China, must arouse research, diagnostic, and treatment vigilance. Currently, the epidemiological data on mycosis in China are variable and fragmentary. Thus, a nationwide epidemiological research on fungal infections in China is an important need for improving the country’s health.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Wang DY, Kumar S, Hedges SB. Divergence time estimates for the early history of animal phyla and the origin of plants, animals and fungi. Proc Biol Sci 1999; 266(1415): 163–171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ. Emerging fungal threats to animal, plant and ecosystem health. Nature 2012; 484(7393): 186–194

    Article  CAS  PubMed  Google Scholar 

  3. Garcia-Solache MA, Casadevall A. Global warming will bring new fungal diseases for mammals. MBio 2010; 1(1): e00061–10

    Article  PubMed  PubMed Central  Google Scholar 

  4. Taylor LH, Latham SM, Woolhouse ME. Risk factors for human disease emergence. Philos Trans R Soc Lond B Biol Sci 2001; 356 (1411): 983–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Kaushik N, Pujalte GG, Reese ST. Superficial fungal infections. Prim Care 2015; 42(4): 501–516

    Article  PubMed  Google Scholar 

  6. Ameen M. Epidemiology of superficial fungal infections. Clin Dermatol 2010; 28(2): 197–201

    Article  PubMed  Google Scholar 

  7. Zhan P, Li D, Wang C, Sun J, Geng C, Xiong Z, Seyedmousavi S, Liu W, de Hoog GS. Epidemiological changes in tinea capitis over the sixty years of economic growth in China. Med Mycol 2015; 53 (7): 691–698

    Article  PubMed  Google Scholar 

  8. Miceli MH, Díaz JA, Lee SA. Emerging opportunistic yeast infections. Lancet Infect Dis 2011; 11(2): 142–151

    Article  PubMed  Google Scholar 

  9. Adams P. Cryptococcal meningitis: a blind spot in curbing AIDS. Lancet 2016; 387(10028): 1605–1606

    Article  PubMed  Google Scholar 

  10. Bahr NC, Sarosi GA, Meya DB, Bohjanen PR, Richer SM, Swartzentruber S, Halupnick R, Jarrett D, Wheat LJ, Boulware DR. Seroprevalence of histoplasmosis in Kampala, Uganda. Med Mycol 2016; 54(3): 295–300

    Article  CAS  PubMed  Google Scholar 

  11. Parkes-Ratanshi R, Achan B, Kwizera R, Kambugu A, Meya D, Denning DW. Cryptococcal disease and the burden of other fungal diseases in Uganda; Where are the knowledge gaps and how can we fill them? Mycoses 2015; 58(Suppl 5): 85–93

    Article  PubMed  Google Scholar 

  12. Wu SX, Guo NR, Li XF, Liao WQ, Chen M, Zhang QQ, Li CY, Li RY, Bulmer GS, Li DM, Xi LY, Lu S, Liu B, Zheng YC, Ran YP, Kuan YZ. Human pathogenic fungi in China—emerging trends from ongoing national survey for 1986, 1996, and 2006. Mycopathologia 2011; 171(6): 387–393

    Article  CAS  PubMed  Google Scholar 

  13. Liao Y, Chen M, Hartmann T, Yang RY, Liao WQ. Epidemiology of opportunistic invasive fungal infections in China: review of literature. Chin Med J (Engl) 2013; 126(2): 361–368

    Google Scholar 

  14. Havlickova B, Czaika VA, Friedrich M. Epidemiological trends in skin mycoses worldwide. Mycoses 2008; 51(Suppl 4): 2–15

    Article  PubMed  Google Scholar 

  15. Zhan P, Liu W. The changing face of dermatophytic infections worldwide. Mycopathologia 2017; 182(1-2): 77–86

    Article  PubMed  Google Scholar 

  16. Li GZ, Liu YH, Chen XW. Etiologic analysis of 4000 cases of superficial mycosis in Tianjin region. China J Lepr Skin Dis (Zhongguo Ma Feng Pi Fu Bing Za Zhi) 2010; 26(8): 602 (in Chinese)

    Google Scholar 

  17. Cai W, Lu C, Li X, Zhang J, Zhan P, Xi L, Sun J, Yu X. Epidemiology of superficial fungal infections in Guangdong, Southern China: a retrospective study from 2004 to 2014. Mycopathologia 2016; 181(5-6): 387–395

    Article  PubMed  Google Scholar 

  18. Zhu JH, Han DM, Zhao Y, Li L, Zhang QQ. Etiologic analysis of 9566 cases of superficial mycosis in Shanghai region. Chin J Mycol (Zhongguo Zhen Jun Xue Za Zhi) 2016; 11(3): 178–180 (in Chinese)

    Google Scholar 

  19. LI LN. Zhang SM, Liu HW, Gao L, Lei DC, Li ZL, Yu HQ, Li JG. Analysis of superficial mycoses and pathogenic fungi in 668 cases. Chin J Derm Venereol (Zhongguo Pi Fu Xing Bing Xue Za Zhi) 2016; 30(3): 259–260 (in Chinese)

    Google Scholar 

  20. Ma XN, Zhang H, Han XH, Wang HD, Shi LQ, Ren Y. Clinical analysis of 1422 cases of superficial mycoses in Yan’an Area. Chin J Derm Venereol (Zhongguo Pi Fu Xing Bing Xue Za Zhi) 2016; 30(9): 908–910 (in Chinese)

    Google Scholar 

  21. Xu W, Li Y. Clinical analysis of 818 cases of superficial mycosis. Guide China Med (Zhongguo Yi Yao Zhi Nan) 2010; 8(13): 131–132 (in Chinese)

    Google Scholar 

  22. Xiong Y, Zhou CJ, Li QJ, Huang XY, Huang YH, Zhong BY, Tang SQ, Dai W, Hao F. Etiologic analysis of 2135 cases of superficial mycosis in Chongqing region. J Clin Dermatol (Lin Chuang Pi Fu Ke Za Zhi) 2008; 37(11): 711–713 (in Chinese)

    Google Scholar 

  23. Silva-Rocha WP, de Azevedo MF, Chaves GM. Epidemiology and fungal species distribution of superficial mycoses in Northeast Brazil. J Mycol Med 2017; 27(1): 57–64

    Article  CAS  PubMed  Google Scholar 

  24. Foster KW, Ghannoum MA, Elewski BE. Epidemiologic surveillance of cutaneous fungal infection in the United States from 1999 to 2002. J Am Acad Dermatol 2004; 50(5): 748–752

    Article  PubMed  Google Scholar 

  25. Drakensjö IT, Chryssanthou E. Epidemiology of dermatophyte infections in Stockholm, Sweden: a retrospective study from 2005–2009. Med Mycol 2011; 49(5): 484–488

    PubMed  Google Scholar 

  26. Simonnet C, Berger F, Gantier JC. Epidemiology of superficial fungal diseases in French Guiana: a three-year retrospective analysis. Med Mycol 2011; 49(6): 608–611

    PubMed  Google Scholar 

  27. Tan HH. Superficial fungal infections seen at the National Skin Centre, Singapore. Nihon Ishinkin Gakkai Zasshi 2005; 46(2): 77–80

    Article  PubMed  Google Scholar 

  28. Fuller LC, Barton RC, Mohd Mustapa MF, Proudfoot LE, Punjabi SP, Higgins EM. British Association of Dermatologists’ guidelines for the management of tinea capitis 2014. Br J Dermatol 2014; 171 (3): 454–463

    Article  CAS  PubMed  Google Scholar 

  29. Zhan P, Geng C, Li Z, Jin Y, Jiang Q, Tao L, Luo Y, Xiong Z, Wu S, Li D, Liu W, de Hoog GS. Evolution of tinea capitis in the Nanchang area, Southern China: a 50-year survey (1965–2014). Mycoses 2015; 58(5): 261–266

    Article  PubMed  Google Scholar 

  30. Liu ZS, Fu XQ, Xie SW, Wang Y, Sun JB. Analysis of situation of tinea capitis in Hubei from 1995 to 2000. China J Lepr Skin Dis (Zhongguo Ma Feng Pi Fu Bing Za Zhi) 2003; 14(4): 54–55 (in Chinese)

    Google Scholar 

  31. Yu J, Li R, Bulmer G. Current topics of tinea capitis in China. Nihon Ishinkin Gakkai Zasshi 2005; 46(2): 61–66

    Article  PubMed  Google Scholar 

  32. Zhu M, Li L, Wang J, Zhang C, Kang K, Zhang Q. Tinea capitis in Southeastern China: a 16-year survey. Mycopathologia 2010; 169 (4): 235–239

    Article  PubMed  Google Scholar 

  33. Korstanje MJ, Staats CG. Tinea capitis in Northwestern Europe 1963–1993: etiologic agents and their changing prevalence. Int J Dermatol 1994; 33(8): 548–549

    Article  CAS  PubMed  Google Scholar 

  34. Sigurgeirsson B, Baran R. The prevalence of onychomycosis in the global population: a literature study. J Eur Acad Dermatol Venereol 2014; 28(11): 1480–1491

    Article  CAS  PubMed  Google Scholar 

  35. Wang AP, Yu J, Wan Z, Li FQ, Zeng JS, Liu WD, Zhang QQ, Hao F, Ran YP, Xi LY, Lai W, Li RY. Multi-center epidemiological survey of pathogenic fungi of onychomycosis in China. Chin J Mycol (Zhongguo Zhen Jun Xue Za Zhi) 2015; 10(4): 197–202 (in Chinese)

    Google Scholar 

  36. Gupta AK, Versteeg SG, Shear NH. Onychomycosis in the 21st century: an update on diagnosis, epidemiology, and treatment. J Cutan Med Surg 2017 Jun 1 [Epub ahead of print] https://doi.org/ 10.1177/1203475417716362

    Google Scholar 

  37. Papini M, Piraccini BM, Difonzo E, Brunoro A. Epidemiology of onychomycosis in Italy: prevalence data and risk factor identification. Mycoses 2015; 58(11): 659–664

    Article  PubMed  Google Scholar 

  38. Ribeiro CS, Zaitz C, Framil VM, Ottoboni TS, Tonoli MS, Ribeiro RP. Descriptive study of onychomycosis in a hospital in São Paulo. Braz J Microbiol 2015; 46(2): 485–492

    Article  PubMed  PubMed Central  Google Scholar 

  39. Gupta C, Jongman M, Das S, Snehaa K, Bhattacharya SN, Seyedmousavi S, van Diepeningen AD. Genotyping and in vitro antifungal susceptibility testing of fusarium isolates from onychomycosis in India. Mycopathologia 2016; 181(7-8): 497–504

    Article  CAS  PubMed  Google Scholar 

  40. Segal R, Shemer A, Hochberg M, Keness Y, Shvarzman R, Mandelblat M, Frenkel M, Segal E. Onychomycosis in Israel: epidemiological aspects. Mycoses 2015; 58(3): 133–139

    Article  CAS  PubMed  Google Scholar 

  41. Maraki S, Mavromanolaki VE. Epidemiology of onychomycosis in Crete, Greece: a 12-year study. Mycoses 2016; 59(12): 798–802

    Article  PubMed  Google Scholar 

  42. Hashemi SJ, Gerami M, Zibafar E, Daei M, Moazeni M, Nasrollahi A. Onychomycosis in Tehran: mycological study of 504 patients. Mycoses 2010; 53(3): 251–255

    Article  CAS  PubMed  Google Scholar 

  43. Souza LK, Fernandes OF, Passos XS, Costa CR, Lemos JA, Silva MR. Epidemiological and mycological data of onychomycosis in Goiania, Brazil. Mycoses 2010; 53(1): 68–71

    Article  CAS  PubMed  Google Scholar 

  44. Yin SC, Zhang YQ, Tan YF, Yang JY, Huang HQ, Li H, Lai W. Analysis of pathogenic fungi of 805 cases with onychomycosis. Chin J Mycol (Zhongguo Zhen Jun Xue Za Zhi) 2013; 8(4): 214–216 (in Chinese)

    Google Scholar 

  45. Zhou J, Chen M, Chen H, Pan W, Liao W. Rhodotorula minuta as onychomycosis agent in a Chinese patient: first report and literature review. Mycoses 2014; 57(3): 191–195

    Article  CAS  PubMed  Google Scholar 

  46. Meersseman W, Van Wijngaerden E. Invasive aspergillosis in the ICU: an emerging disease. Intensive Care Med 2007; 33(10): 1679–1681

    Article  PubMed  Google Scholar 

  47. Pappas PG, Alexander BD, Andes DR, Hadley S, Kauffman CA, Freifeld A, Anaissie EJ, Brumble LM, Herwaldt L, Ito J, Kontoyiannis DP, Lyon GM, Marr KA, Morrison VA, Park BJ, Patterson TF, Perl TM, Oster RA, Schuster MG, Walker R, Walsh TJ, Wannemuehler KA, Chiller TM. Invasive fungal infections among organ transplant recipients: results of the Transplant-Associated Infection Surveillance Network (TRANSNET). Clin Infect Dis 2010; 50(8): 1101–1111

    Article  PubMed  Google Scholar 

  48. Gavaldà J, Meije Y, Fortún J, Roilides E, Saliba F, Lortholary O, Muñoz P, Grossi P, Cuenca-Estrella M; ESCMID Study Group for Infections in Compromised Hosts. Invasive fungal infections in solid organ transplant recipients. Clin Microbiol Infect 2014; 20 (Suppl 7): 27–48

    Article  PubMed  Google Scholar 

  49. Brown GD, Denning DW, Gow NA, Levitz SM, Netea MG, White TC. Hidden killers: human fungal infections. Sci Transl Med 2012; 4(165): 165rv13

    Article  CAS  Google Scholar 

  50. Montagna MT, Caggiano G, Lovero G, De Giglio O, Coretti C, Cuna T, Iatta R, Giglio M, Dalfino L, Bruno F, Puntillo F. Epidemiology of invasive fungal infections in the intensive care unit: results of a multicenter Italian survey (AURORA Project). Infection 2013; 41(3): 645–653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Feng WL, Yang J, Xi ZQ, Wang YQ, Zhang RM, Ji Y, Wu Y, Jia XQ. Epidemiologic study on patients with invasive fungal infections. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 2009; 30(10): 1043–1046 (in Chinese)

    Google Scholar 

  52. Liu ZY, Sheng RY, Li XL, Li TS, Wang AX. Nosocomial fungal infections, analysis of 149 cases. Natl Med J China (Zhonghua Yi Xue Za Zhi) 2003; 83(5): 399–402 (in Chinese)

    Google Scholar 

  53. Gao LY, Yu J, Li RY. Epidemiology of aspergillosis in mainland China. Chin J Mycol (Zhongguo Zhen Jun Xue Za Zhi) 2010; 5 (4): 247–251 (in Chinese)

    Google Scholar 

  54. Liu YN, She DY, Sun TY, Tong ZH, He B, Xiao Y, He LX, Qu JM, Liu XQ, Li ER, Chen P, Ma ZS, Shi Y, Feng YL, Jiang SJ, Xiong SD, Hu CP. A multicentre retrospective study of pulmonary mycosis clinically proven from 1998 to 2007. Chin J Tubere Respir Dis (Zhonghua Jie He He Hu Xi Za Zhi) 2011; 34(2): 86–90 (in Chinese)

    Google Scholar 

  55. Seneviratne CJ, Rajan S, Wong SS, Tsang DN, Lai CK, Samaranayake LP, Jin L. Antifungal susceptibility in serum and virulence determinants of Candida bloodstream isolates from Hong Kong. Front Microbiol 2016; 7: 216

    PubMed  PubMed Central  Google Scholar 

  56. Guo F, Yang Y, Kang Y, Zang B, Cui W, Qin B, Qin Y, Fang Q, Qin T, Jiang D, Li W, Gu Q, Zhao H, Liu D, Guan X, Li J, Ma X, Yu K, Chan D, Yan J, Tang Y, Liu W, Li R, Qiu H; China-SCAN Team. Invasive candidiasis in intensive care units in China: a multicentre prospective observational study. J Antimicrob Chemother 2013; 68(7): 1660–1668

    Article  CAS  PubMed  Google Scholar 

  57. Méan M, Marchetti O, Calandra T. Bench-to-bedside review: Candida infections in the intensive care unit. Crit Care 2008; 12 (1): 204

    Article  PubMed  PubMed Central  Google Scholar 

  58. Kett DH, Azoulay E, Echeverria PM, Vincent JL; Extended Prevalence of Infection in ICU Study (EPIC II) Group of Investigators. Candida bloodstream infections in intensive care units: analysis of the extended prevalence of infection in intensive care unit study. Crit Care Med 2011; 39(4): 665–670

    Article  PubMed  Google Scholar 

  59. Falagas ME, Roussos N, Vardakas KZ. Relative frequency of albicans and the various non-albicans Candida spp. among candidemia isolates from inpatients in various parts of the world: a systematic review. Int J Infect Dis 2010; 14(11): e954–e966

    PubMed  Google Scholar 

  60. Horn DL, Neofytos D, Anaissie EJ, Fishman JA, Steinbach WJ, Olyaei AJ, Marr KA, Pfaller MA, Chang CH, Webster KM. Epidemiology and outcomes of candidemia in 2019 patients: data from the prospective antifungal therapy alliance registry. Clin Infect Dis 2009; 48(12): 1695–1703

    Article  CAS  PubMed  Google Scholar 

  61. Gong X, Luan T,Wu X, Li G, Qiu H, Kang Y, Qin B, Fang Q, Cui W, Qin Y, Li J, Zang B. Invasive candidiasis in intensive care units in China: Risk factors and prognoses of Candida albicans and nonalbicans Candida infections. Am J Infect Control 2016; 44(5): e59–e63

    Article  PubMed  Google Scholar 

  62. Ma CF, Li FQ, Shi LN, Hu YA, Wang Y, Huang M, Kong QQ. Surveillance study of species distribution, antifungal susceptibility and mortality of nosocomial candidemia in a tertiary care hospital in China. BMC Infect Dis 2013; 13(1): 337

    Article  PubMed  PubMed Central  Google Scholar 

  63. Li S, An YZ. Retrospective analysis of invasive fungal infection in surgical intensive care unit. Natl Med J China (Zhonghua Yi Xue Za Zhi) 2010; 90(6): 382–385 (in Chinese)

    Google Scholar 

  64. Cao B, Wang H, Wu L, Sun WJ, Li F, Liu YM. Epidemiological study of invasive nosocomial candidiasis in 2 teaching hospitals in Beijing. Natl Med J China (Zhonghua Yi Xue Za Zhi) 2008; 88 (28): 1970–1973 (in Chinese)

    CAS  Google Scholar 

  65. Poikonen E, Lyytikäinen O, Anttila VJ, Koivula I, Lumio J, Kotilainen P, Syrjälä H, Ruutu P. Secular trend in candidemia and the use of fluconazole in Finland, 2004–2007. BMC Infect Dis 2010; 10(1): 312

    Article  PubMed  PubMed Central  Google Scholar 

  66. Almirante B, Rodríguez D, Park BJ, Cuenca-Estrella M, Planes AM, Almela M, Mensa J, Sanchez F, Ayats J, Gimenez M, Saballs P, Fridkin SK, Morgan J, Rodriguez-Tudela JL, Warnock DW, Pahissa A; Barcelona Candidemia Project Study Group. Epidemiology and predictors of mortality in cases of Candida bloodstream infection: results from population-based surveillance, Barcelona, Spain, from 2002 to 2003. J Clin Microbiol 2005; 43 (4): 1829–1835

    Article  PubMed  PubMed Central  Google Scholar 

  67. Paphitou NI, Ostrosky-Zeichner L, Rex JH. Rules for identifying patients at increased risk for Candidal infections in the surgical intensive care unit: approach to developing practical criteria for systematic use in antifungal prophylaxis trials. Med Mycol 2005; 43(3): 235–243

    Article  PubMed  Google Scholar 

  68. Marchetti O, Bille J, Fluckiger U, Eggimann P, Ruef C, Garbino J, Calandra T, Glauser MP, Täuber MG, Pittet D; Fungal Infection Network of Switzerland. Epidemiology of candidemia in Swiss tertiary care hospitals: secular trends, 1991–2000. Clin Infect Dis 2004; 38(3): 311–320

    Article  PubMed  Google Scholar 

  69. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin Infect Dis 2004; 39(3): 309–317

    Article  PubMed  Google Scholar 

  70. González GM, Treviño-Rangel RdeJ, Palma-Nicolás JP, Martínez C, González JG, Ayala J, Caballero A, Morfín-Otero R, Rodríguez-Noriega E, Velarde F, Ascencio EP, Tinoco JC, Vázquez JA, Cano MA, León-Sicairos N, González R, Rincón J, Elías MA, Bonifaz A. Species distribution and antifungal susceptibility of bloodstream fungal isolates in paediatric patients in Mexico: a nationwide surveillance study. J Antimicrob Chemother 2013; 68(12): 2847–2851

    Article  PubMed  CAS  Google Scholar 

  71. Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Ellis D, Tullio V, Rodloff A, Fu W, Ling TA; Global Antifungal Surveillance Group. Results from the ARTEMIS DISK Global Antifungal Surveillance Study, 1997 to 2007: a 10.5-year analysis of susceptibilities of Candida species to fluconazole and voriconazole as determined by CLSI standardized disk diffusion. J Clin Microbiol 2010; 48(4): 1366–1377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Pu S, Niu S, Zhang C, Xu X, Qin M, Huang S, Zhang L. 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

    Article  PubMed  Google Scholar 

  73. Li F, Wu L, Cao B, Zhang Y, Li X, Liu Y. Surveillance of the prevalence, antibiotic susceptibility, and genotypic characterization of invasive candidiasis in a teaching hospital in China between 2006 to 2011. BMC Infect Dis 2013; 13(1): 353

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Zhang Z, Zhao SL, Pang LJ, Wang H, Liu WY, Yan W. The analysis and survey of 475 strains of fungi from clinical samples. Chin J Lab Med (Zhonghua Jian Yan Yi Xue Za Zhi) 1996; 19(5): 267–269 (in Chinese)

    CAS  Google Scholar 

  75. Yu J, Li RY,Wang D, Zhao M, Jiang H, Chen W,Wang AP,Wang DL. Analysis on species distribution and risk factors of nosocomial invasive Candida infection. China J Lepr Skin Dis (Zhongguo Ma Feng Pi Fu Bing Za Zhi) 2000; 16(4): 211–215 (in Chinese)

    Google Scholar 

  76. Wang H, Xu YC, Hsueh PR. Epidemiology of candidemia and antifungal susceptibility in invasive Candida species in the Asia-Pacific region. Future Microbiol 2016; 11(11): 1461–1477

    Article  CAS  PubMed  Google Scholar 

  77. Nucci M, Queiroz-Telles F, Tobón AM, Restrepo A, Colombo AL. Epidemiology of opportunistic fungal infections in Latin America. Clin Infect Dis 2010; 51(5): 561–570

    Article  PubMed  Google Scholar 

  78. Wang H, Xiao M, Chen SC, Kong F, Sun ZY, Liao K, Lu J, Shao HF, Yan Y, Fan H, Hu ZD, Chu YZ, Hu TS, Ni YX, Zou GL, Xu YC. In vitro susceptibilities of yeast species to fluconazole and voriconazole as determined by the 2010 National China Hospital Invasive Fungal Surveillance Net (CHIF-NET) study. J Clin Microbiol 2012; 50(12): 3952–3959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Puig-Asensio M, Pemán J, Zaragoza R, Garnacho-Montero J, Martín-Mazuelos E, Cuenca-Estrella M, Almirante B; Prospective Population Study on Candidemia in Spain (CANDIPOP) Project; Hospital Infection Study Group (GEIH); Medical Mycology Study Group (GEMICOMED) of the Spanish Society of Infectious Diseases and Clinical Microbiology (SEIMC); Spanish Network for Research in Infectious Diseases. Impact of therapeutic strategies on the prognosis of candidemia in the ICU. Crit Care Med 2014; 42(6): 1423–1432

    Article  CAS  PubMed  Google Scholar 

  80. Wu JQ, Zhu LP, Ou XT, Xu B, Hu XP, Wang X, Weng XH. Epidemiology and risk factors for non-Candida albicans candidemia in non-neutropenic patients at a Chinese teaching hospital. Med Mycol 2011; 49(5): 552–555

    PubMed  Google Scholar 

  81. Liu W, Tan J, Sun J, Xu Z, Li M, Yang Q, Shao H, Zhang L, Liu W, Wan Z, Cui W, Zang B, Jiang D, Fang Q, Qin B, Qin T, Li W, Guo F, Liu D, Guan X, Yu K, Qiu H, Li R; China-SCAN team. Invasive candidiasis in intensive care units in China: in vitro antifungal susceptibility in the China-SCAN study. J Antimicrob Chemother 2014; 69(1): 162–167

    Article  CAS  PubMed  Google Scholar 

  82. Chen TC, Chen YH, Tsai JJ, Peng CF, Lu PL, Chang K, Hsieh HC, Chen TP. Epidemiologic analysis and antifungal susceptibility of Candida blood isolates in southern Taiwan. J Microbiol Immunol Infect 2005; 38(3): 200–210

    CAS  PubMed  Google Scholar 

  83. Chen PL, Lo HJ,Wu CJ, Lee HC, Chang CM, Lee NY,Wang AH, Lin WL, Ko NY, Lee CC, Ko WC. Species distribution and antifungal susceptibility of blood Candida isolates at a tertiary hospital in southern Taiwan, 1999–2006. Mycoses 2011; 54(4): e17–e23

    Article  PubMed  Google Scholar 

  84. Li Y, Du M, Chen LA, Liu Y, Liang Z. Nosocomial bloodstream infection due to Candida spp. in China: species distribution, clinical features, and outcomes. Mycopathologia 2016; 181(7-8): 485–495

    Article  CAS  PubMed  Google Scholar 

  85. Yang ZT, Wu L, Liu XY, Zhou M, Li J, Wu JY, Cai Y, Mao EQ, Chen EZ, Lortholary O. Epidemiology, species distribution and outcome of nosocomial Candida spp. bloodstream infection in Shanghai. BMC Infect Dis 2014; 14(1): 241

    Article  PubMed  PubMed Central  Google Scholar 

  86. Wang H, Liu N, Yin M, Han H, Yue J, Zhang F, Shan T, Guo H, Wu D. The epidemiology, antifungal use and risk factors of death in elderly patients with candidemia: a multicentre retrospective study. BMC Infect Dis 2014; 14(1): 609

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Zhang XB, Yu SJ, Yu JX, Gong YL, Feng W, Sun FJ. Retrospective analysis of epidemiology and prognostic factors for candidemia at a hospital in China, 2000–2009. Jpn J Infect Dis 2012; 65(6): 510–515

    Article  PubMed  Google Scholar 

  88. Yap HY, Kwok KM, Gomersall CD, Fung SC, Lam TC, Leung PN, Hui M, Joynt GM. Epidemiology and outcome of Candida bloodstream infection in an intensive care unit in Hong Kong. Hong Kong Med J 2009; 15(4): 255–261

    CAS  PubMed  Google Scholar 

  89. Chen PY, Chuang YC, Wang JT, Sheng WH, Yu CJ, Chu CC, Hsueh PR, Chang SC, Chen YC. Comparison of epidemiology and treatment outcome of patients with candidemia at a teaching hospital in Northern Taiwan, in 2002 and 2010. J Microbiol Immunol Infect 2014; 47(2): 95–103

    Article  PubMed  Google Scholar 

  90. Chen SC, Marriott D, Playford EG, Nguyen Q, Ellis D, Meyer W, Sorrell TC, Slavin M; Australian Candidaemia Study. Candidaemia with uncommon Candida species: predisposing factors, outcome, antifungal susceptibility, and implications for management. Clin Microbiol Infect 2009; 15(7): 662–669

    Article  CAS  PubMed  Google Scholar 

  91. Pfaller MA, Diekema DJ, Colombo AL, Kibbler C, Ng KP, Gibbs DL, Newell VA. Candida rugosa, an emerging fungal pathogen with resistance to azoles: geographic and temporal trends from the ARTEMIS DISK antifungal surveillance program. J Clin Microbiol 2006; 44(10): 3578–3582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Xiao M, Wang H, Lu J, Chen SC, Kong F, Ma XJ, Xu YC. Three clustered cases of candidemia caused by Candida quercitrusa and mycological characteristics of this novel species. J Clin Microbiol 2014; 52(8): 3044–3048

    Article  PubMed  PubMed Central  Google Scholar 

  93. Chowdhary A, Sharma C, Meis JF. Candida auris: a rapidly emerging cause of hospital-acquired multidrug-resistant fungal infections globally. PLoS Pathog 2017; 13(5): e1006290

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Wu Z, Liu Y, Feng X, Liu Y, Wang S, Zhu X, Chen Q, Pan S. Candidemia: incidence rates, type of species, and risk factors at a tertiary care academic hospital in China. Int J Infect Dis 2014; 22: 4–8

    Article  PubMed  Google Scholar 

  95. Huang YT, Liu CY, Liao CH, Chung KP, Sheng WH, Hsueh PR. Antifungal susceptibilities of Candida isolates causing bloodstream infections at a medical center in Taiwan, 2009–2010. Antimicrob Agents Chemother 2014; 58(7): 3814–3819

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Chowdhary A, Sharma C, Duggal S, Agarwal K, Prakash A, Singh PK, Jain S, Kathuria S, Randhawa HS, Hagen F, Meis JF. New clonal strain of Candida auris, Delhi, India. Emerg Infect Dis 2013; 19(10): 1670–1673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Magobo RE, Corcoran C, Seetharam S, Govender NP. Candida auris-associated candidemia, South Africa. Emerg Infect Dis 2014; 20(7): 1250–1251

    Article  PubMed  PubMed Central  Google Scholar 

  98. Vallabhaneni S, Kallen A, Tsay S, Chow N, Welsh R, Kerins J, Kemble SK, Pacilli M, Black SR, Landon E, Ridgway J, Palmore TN, Zelzany A, Adams EH, Quinn M, Chaturvedi S, Greenko J, Fernandez R, Southwick K, Furuya EY, Calfee DP, Hamula C, Patel G, Barrett P; MSD,Lafaro P, Berkow EL, Moulton-Meissner H, Noble-Wang J, Fagan RP, Jackson BR, Lockhart SR, Litvintseva AP, Chiller TM. Investigation of the first seven reported cases of Candida auris, a globally emerging invasive, multidrug-resistant fungus — United States, May 2013–August 2016. MMWR Morb Mortal Wkly Rep 2016; 65(44): 1234–1237

    Article  PubMed  Google Scholar 

  99. Mohsin J, Hagen F, Al-Balushi ZAM, de Hoog GS, Chowdhary A, Meis JF, Al-Hatmi AMS. The first cases of Candida auris Candidaemia in Oman. Mycoses 2017; 60(9): 569–575

    Article  PubMed  Google Scholar 

  100. Chowdhary A, Anil Kumar V, Sharma C, Prakash A, Agarwal K, Babu R, Dinesh KR, Karim S, Singh SK, Hagen F, Meis JF. Multidrug-resistant endemic clonal strain of Candida auris in India. Eur J Clin Microbiol Infect Dis 2014; 33(6): 919–926

    Article  CAS  PubMed  Google Scholar 

  101. Wang FJ, Zhang D, Liu ZH, Wu WX, Bai HH, Dong HY. Species distribution and in vitro antifungal susceptibility of vulvovaginal Candida isolates in China. Chin Med J (Engl) 2016; 129(10): 1161–1165

    Article  Google Scholar 

  102. Ding X, Yan D, Sun W, Zeng Z, Su R, Su J. Epidemiology and risk factors for nosocomial non-Candida albicans candidemia in adult patients at a tertiary care hospital in North China. Med Mycol 2015; 53(7): 684–690

    Article  PubMed  Google Scholar 

  103. Chen J, Jiang Y, Wei B, Ding Y, Xu S, Qin P, Fu J. Epidemiology of and risk factors for neonatal candidemia at a tertiary care hospital in western China. BMC Infect Dis 2016; 16(1): 700

    Article  PubMed  PubMed Central  Google Scholar 

  104. Pfaller MA, Castanheira M, Messer SA, Moet GJ, Jones RN. Echinocandin and triazole antifungal susceptibility profiles for Candida spp., Cryptococcus neoformans, and Aspergillus fumigatus: application of new CLSI clinical breakpoints and epidemiologic cutoff values to characterize resistance in the SENTRY Antimicrobial Surveillance Program (2009). Diagn Microbiol Infect Dis 2011; 69(1): 45–50

    Article  CAS  PubMed  Google Scholar 

  105. Montagna MT, Lovero G, Coretti C, Martinelli D, Delia M, De Giglio O, Caira M, Puntillo F, D’Antonio D, Venditti M, Sambri V, Di Bernardo F, Barbui A, Lo Cascio G, Concia E, Mikulska M, Viscoli C, Maximova N, Candoni A, Oliveri S, Lombardi G, Pitzurra L, Sanguinetti M, Masciari R, Santantonio T, Andreoni S, Barchiesi F, Pecile P, Farina C, Viale P, Specchia G, Caggiano G, Pagano L. SIMIFF study: Italian fungal registry of mold infections in hematological and non-hematological patients. Infection 2014; 42(1): 141–151

    Article  CAS  PubMed  Google Scholar 

  106. Lin SJ, Schranz J, Teutsch SM. Aspergillosis case-fatality rate: systematic review of the literature. Clin Infect Dis 2001; 32(3): 358–366

    Article  CAS  PubMed  Google Scholar 

  107. Zhang S, Wang S, Wan Z, Li R, Yu J. The diagnosis of invasive and noninvasive pulmonary aspergillosis by serum and bronchoalveolar lavage fluid galactomannan assay. Biomed Res Int 2015; 2015: 943691

    PubMed  PubMed Central  Google Scholar 

  108. Chen Y, Lu ZY, Jin Y, Han L, Huang LY. Progress of research on azole resistance in Aspergillus fumigatus. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 2016; 37(12): 1687–1692 (in Chinese)

    CAS  Google Scholar 

  109. He H, Ding L, Li F, Zhan Q. Clinical features of invasive bronchial-pulmonary aspergillosis in critically ill patients with chronic obstructive respiratory diseases: a prospective study. Crit Care 2011; 15(1): R5

    Article  PubMed  PubMed Central  Google Scholar 

  110. Chen J, Yang Q, Huang J, Li L. Clinical findings in 19 cases of invasive pulmonary aspergillosis with liver cirrhosis. Multidiscip Respir Med 2014; 9(1): 1

    Article  PubMed  PubMed Central  Google Scholar 

  111. Chen J, Yang Q, Huang J, Li L. Risk factors for invasive pulmonary aspergillosis and hospital mortality in acute-on-chronic liver failure patients: a retrospective-cohort study. Int J Med Sci 2013; 10(12): 1625–1631

    Article  PubMed  PubMed Central  Google Scholar 

  112. Meersseman W, Vandecasteele SJ, Wilmer A, Verbeken E, Peetermans WE, Van Wijngaerden E. Invasive aspergillosis in critically ill patients without malignancy. Am J Respir Crit Care Med 2004; 170(6): 621–625

    Article  PubMed  Google Scholar 

  113. Yan X, Li M, Jiang M, Zou LQ, Luo F, Jiang Y. Clinical characteristics of 45 patients with invasive pulmonary aspergillosis: retrospective analysis of 1711 lung cancer cases. Cancer 2009; 115(21): 5018–5025

    Article  PubMed  Google Scholar 

  114. Taccone FS, Van den Abeele AM, Bulpa P, Misset B, Meersseman W, Cardoso T, Paiva JA, Blasco-Navalpotro M, De Laere E, Dimopoulos G, Rello J, Vogelaers D, Blot SI; AspICU Study Investigators. Epidemiology of invasive aspergillosis in critically ill patients: clinical presentation, underlying conditions, and outcomes. Crit Care 2015; 19(1): 7

    Article  PubMed  PubMed Central  Google Scholar 

  115. Lockhart SR, Frade JP, Etienne KA, Pfaller MA, Diekema DJ, Balajee SA. 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 2011; 55(9): 4465–4468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Li Y, Wan Z, Liu W, Li R. Identification and susceptibility of Aspergillus section nigri in china: prevalence of species and paradoxical growth in response to echinocandins. J Clin Microbiol 2015; 53(2): 702–705

    Article  PubMed  PubMed Central  Google Scholar 

  117. Wang W, Zhao CY, Zhou JY, Wang YD, Shen C, Zhou DF, Yin HZ. Invasive pulmonary aspergillosis in patients with HBV-related liver failure. Eur J Clin Microbiol Infect Dis 2011; 30(5): 661–667

    Article  CAS  PubMed  Google Scholar 

  118. Liu M, Zeng R, Zhang L, Li D, Lv G, Shen Y, Zheng H, Zhang Q, Zhao J, Zheng N, Liu W. Multiple cyp51A-based mechanisms identified in azole-resistant isolates of Aspergillus fumigatus from China. Antimicrob Agents Chemother 2015; 59(7): 4321–4325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Chen Y, Lu Z, Zhao J, Zou Z, Gong Y, Qu F, Bao Z, Qiu G, Song M, Zhang Q, Liu L, Hu M, Han X, Tian S, Zhao J, Chen F, Zhang C, Sun Y, Verweij PE, Huang L, Han L. Epidemiology and molecular characterizations of azole resistance in clinical and environmental Aspergillus fumigatus isolates from China. Antimicrob Agents Chemother 2016; 60(10): 5878–5884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Chen J, Li H, Li R, Bu D, Wan Z. Mutations in the cyp51A gene and susceptibility to itraconazole in Aspergillus fumigatus serially isolated from a patient with lung aspergilloma. J Antimicrob Chemother 2005; 55(1): 31–37

    Article  CAS  PubMed  Google Scholar 

  121. 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. Emergence of TR46/Y121F/T289A in an Aspergillus fumigatus isolate from a Chinese patient. Antimicrob Agents Chemother 2015; 59(11): 7148–7150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Sloan DJ, Parris V. Cryptococcal meningitis: epidemiology and therapeutic options. Clin Epidemiol 2014; 6: 169–182

    Article  PubMed  PubMed Central  Google Scholar 

  123. Gullo FP, Rossi SA, Sardi JdeC, Teodoro VL, Mendes-Giannini MJ, Fusco-Almeida AM. Cryptococcosis: epidemiology, fungal resistance, and new alternatives for treatment. Eur J Clin Microbiol Infect Dis 2013; 32(11): 1377–1391

    Article  CAS  PubMed  Google Scholar 

  124. Cogliati M. Global molecular epidemiology of Cryptococcus neoformans and Cryptococcus gattii: an atlas of the molecular types. Scientifica (Cairo) 2013; 2013: 675213

    Google Scholar 

  125. 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. Consensus multi-locus sequence typing scheme for Cryptococcus neoformans and Cryptococcus gattii. Med Mycol 2009; 47(6): 561–570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Fan X, Xiao M, Chen S, Kong F, Dou HT, Wang H, Xiao YL, Kang M, Sun ZY, Hu ZD, Wan Z, Chen SL, Liao K, Chu YZ, Hu TS, Zou GL, Hou X, Zhang L, Zhao YP, Xu YC, Liu ZY. Predominance of Cryptococcus neoformans var. grubii multilocus sequence type 5 and emergence of isolates with non-wild-type minimum inhibitory concentrations to fluconazole: a multi-centre study in China. Clin Microbiol Infect 2016; 22(10): 887.e1–887.e9

    Article  CAS  Google Scholar 

  127. Dou HT, Xu YC, Wang HZ, Li TS. Molecular epidemiology of Cryptococcus neoformans and Cryptococcus gattii in China between 2007 and 2013 using multilocus sequence typing and the DiversiLab system. Eur J Clin Microbiol Infect Dis 2015; 34 (4): 753–762

    Article  PubMed  Google Scholar 

  128. 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. Geographically structured populations of Cryptococcus neoformans variety grubii in Asia correlate with HIV status and show a clonal population structure. PLoS One 2013; 8(9): e72222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Park SH, Kim M, Joo SI, Hwang SM. Molecular epidemiology of clinical Cryptococcus neoformans isolates in Seoul, Korea. Mycobiology 2014; 42(1): 73–78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. 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. Multilocus sequence typing of Cryptococcus neoformans in non-HIV associated cryptococcosis in Nagasaki, Japan. Med Mycol 2013; 51(3): 252–260

    Article  CAS  PubMed  Google Scholar 

  131. Simwami SP, Khayhan K, Henk DA, Aanensen DM, Boekhout T, Hagen F, Brouwer AE, Harrison TS, Donnelly CA, Fisher MC. Low diversity Cryptococcus neoformans variety grubii multilocus sequence types from Thailand are consistent with an ancestral African origin. PLoS Pathog 2011; 7(4): e1001343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Xue X, Wu H, Wang K, Cao J, Shen D. Cryptococcosis by Cryptococcus gattii in China. Lancet Infect Dis 2015; 15(10): 1135–1136

    Article  PubMed  Google Scholar 

  133. Kronstad JW, Attarian R, Cadieux B, Choi J, D’Souza CA, Griffiths EJ, Geddes JM, Hu G, Jung WH, Kretschmer M, Saikia S, Wang J. Expanding fungal pathogenesis: Cryptococcus breaks out of the opportunistic box. Nat Rev Microbiol 2011; 9(3): 193–203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Feng X, Yao Z, Ren D, Liao W, Wu J. Genotype and mating type analysis of Cryptococcus neoformans and Cryptococcus gattii isolates from China that mainly originated from non-HIV-infected patients. FEMS Yeast Res 2008; 8(6): 930–938

    Article  CAS  PubMed  Google Scholar 

  135. Okamoto K, Hatakeyama S, Itoyama S, Nukui Y, Yoshino Y, Kitazawa T, Yotsuyanagi H, Ikeda R, Sugita T, Koike K. Cryptococcus gattii genotype VGIIa infection in man, Japan, 2007. Emerg Infect Dis 2010; 16(7): 1155–1157

    Article  PubMed  PubMed Central  Google Scholar 

  136. Yuchong C, Fubin C, Jianghan C, Fenglian W, Nan X, Minghui Y, Yalin S, Zhizhong Z. Cryptococcosis in China (1985–2010): review of cases from Chinese database. Mycopathologia 2012; 173 (5-6): 329–335

    Article  PubMed  Google Scholar 

  137. Lui G, Lee N, Ip M, Choi KW, Tso YK, Lam E, Chau S, Lai R, Cockram CS. Cryptococcosis in apparently immunocompetent patients. QJM 2006; 99(3): 143–151

    Article  CAS  PubMed  Google Scholar 

  138. Tseng HK, Liu CP, Ho MW, Lu PL, Lo HJ, Lin YH, Cho WL, Chen YC; Taiwan Infectious Diseases Study Network for Cryptococcosis. Microbiological, epidemiological, and clinical characteristics and outcomes of patients with cryptococcosis in Taiwan, 1997–2010. PLoS One 2013; 8(4): e61921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Chen J, Varma A, Diaz MR, Litvintseva AP, Wollenberg KK, Kwon-Chung KJ. Cryptococcus neoformans strains and infection in apparently immunocompetent patients, China. Emerg Infect Dis 2008; 14(5): 755–762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Chen YY, Lai CH. Nationwide population-based epidemiologic study of cryptococcal meningitis in Taiwan. Neuroepidemiology 2011; 36(2): 79–84

    Article  PubMed  Google Scholar 

  141. Lu CH, Chang WN, Chang HW, Chuang YC. The prognostic factors of cryptococcal meningitis in HIV-negative patients. J Hosp Infect 1999; 42(4): 313–320

    Article  CAS  PubMed  Google Scholar 

  142. Fang W, Fa Z, Liao W. Epidemiology of Cryptococcus and cryptococcosis in China. Fungal Genet Biol 2015; 78: 7–15

    Article  PubMed  Google Scholar 

  143. Dou H, Wang H, Xie S, Chen X, Xu Z, Xu Y. Molecular characterization of Cryptococcus neoformans isolated from the environment in Beijing, China. Med Mycol 2017; 55(7):737–747

    Article  PubMed  Google Scholar 

  144. Li AS, Pan WH, Wu SX, Hideaki T, Guo NR, Shen YN, Lu GX, Pan RG, Zhu MC, Chen M, Shi WM, Liao WQ. Ecological surveys of the Cryptococcus species complex in China. Chin Med J (Engl) 2012; 125(3): 511–516

    Google Scholar 

  145. Skiada A, Pagano L, Groll A, Zimmerli S, Dupont B, Lagrou K, Lass-Florl C, Bouza E, Klimko N, Gaustad P, Richardson M, Hamal P, Akova M, Meis JF, Rodriguez-Tudela JL, Roilides E, Mitrousia-Ziouva A, Petrikkos G; European Confederation of Medical Mycology Working Group on Zygomycosis. Zygomycosis in Europe: analysis of 230 cases accrued by the registry of the European Confederation of Medical Mycology (ECMM) Working Group on Zygomycosis between 2005 and 2007. Clin Microbiol Infect 2011; 17(12): 1859–1867

    Article  CAS  PubMed  Google Scholar 

  146. Ribes JA, Vanover-Sams CL, Baker DJ. Zygomycetes in human disease. Clin Microbiol Rev 2000; 13(2): 236–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Katragkou A, Walsh TJ, Roilides E. Why is mucormycosis more difficult to cure than more common mycoses? Clin Microbiol Infect 2014; 20(Suppl 6): 74–81

    Article  PubMed  Google Scholar 

  148. Rees JR, Pinner RW, Hajjeh RA, Brandt ME, Reingold AL. The epidemiological features of invasive mycotic infections in the San Francisco Bay area, 1992–1993: results of population-based laboratory active surveillance. Clin Infect Dis 1998; 27(5): 1138–1147

    Article  CAS  PubMed  Google Scholar 

  149. Torres-Narbona M, Guinea J, Martínez-Alarcón J, Muñoz P, Gadea I, Bouza E; MYCOMED Zygomycosis Study Group. Impact of zygomycosis on microbiology workload: a survey study in Spain. J Clin Microbiol 2007; 45(6): 2051–2053

    Article  PubMed  PubMed Central  Google Scholar 

  150. Bitar D, Van Cauteren D, Lanternier F, Dannaoui E, Che D, Dromer F, Desenclos JC, Lortholary O. Increasing incidence of zygomycosis (mucormycosis), France, 1997–2006. Emerg Infect Dis 2009; 15(9): 1395–1401

    Article  PubMed  PubMed Central  Google Scholar 

  151. Zhao JY, Fang W, Yang YL, Pan WH, Liao WQ, Tang YC. Retrospective analysis of diabetes combined with zygomycosis in mainland China: a review of 74 cases. Chin J Mycol (Zhongguo Zhen Jun Xue Za Zhi) 2016; 11(1): 33–36 (in Chinese)

    Google Scholar 

  152. Wang SB, Li RY, Yu J. Epidemiology of zygomycosis in mainland China. Chin J Mycol (Zhongguo Zhen Jun Xue Za Zhi) 2013; 8(3): 163–168 (in Chinese)

    Google Scholar 

  153. Zhao JY, Wang GZ, Zhang JY, Yang YL, Jia HL, Fang W, Pan WH, Liao WQ. Retrospective analysis of pulmonary zygomycosis in mainland China: a review of 102 cases. Chin J Mycol (Zhongguo Zhen Jun Xue Za Zhi) 2014; 9(3): 150–154 (in Chinese)

    Google Scholar 

  154. Roden MM, Zaoutis TE, Buchanan WL, Knudsen TA, Sarkisova TA, Schaufele RL, Sein M, Sein T, Chiou CC, Chu JH, Kontoyiannis DP, Walsh TJ. Epidemiology and outcome of zygomycosis: a review of 929 reported cases. Clin Infect Dis 2005; 41(5): 634–653

    Article  PubMed  Google Scholar 

  155. Cornely OA, Arikan-Akdagli S, Dannaoui E, Groll AH, Lagrou K, Chakrabarti A, Lanternier F, Pagano L, Skiada A, Akova M, Arendrup MC, Boekhout T, Chowdhary A, Cuenca-Estrella M, Freiberger T, Guinea J, Guarro J, de Hoog S, Hope W, Johnson E, Kathuria S, Lackner M, Lass-Flörl C, Lortholary O, Meis JF, Meletiadis J, Muñoz P, Richardson M, Roilides E, Tortorano AM, Ullmann AJ, van Diepeningen A, Verweij P, Petrikkos G; European Society of Clinical Microbiology and Infectious Diseases Fungal Infection Study Group; European Confederation of Medical Mycology. ESCMID and ECMM joint clinical guidelines for the diagnosis and management of mucormycosis 2013. Clin Microbiol Infect 2014; 20(Suppl 3): 5–26

    Article  CAS  PubMed  Google Scholar 

  156. Yang W, Lu J,Weng J, Jia W, Ji L, Xiao J, Shan Z, Liu J, Tian H, Ji Q, Zhu D, Ge J, Lin L, Chen L, Guo X, Zhao Z, Li Q, Zhou Z, Shan G, He J; China National Diabetes and Metabolic Disorders Study Group. Prevalence of diabetes among men and women in China. N Engl J Med 2010; 362(12): 1090–1101

    Article  CAS  PubMed  Google Scholar 

  157. Thomas CF Jr, Limper AH. Pneumocystis pneumonia. N Engl J Med 2004; 350(24): 2487–2498

    Article  CAS  PubMed  Google Scholar 

  158. Thomas CF Jr, Limper AH. Current insights into the biology and pathogenesis of Pneumocystis pneumonia. Nat Rev Microbiol 2007; 5(4): 298–308

    Article  CAS  PubMed  Google Scholar 

  159. Edman JC, Kovacs JA, Masur H, Santi DV, Elwood HJ, Sogin ML. Ribosomal RNA sequence shows Pneumocystis carinii to be a member of the fungi. Nature 1988; 334(6182): 519–522

    Article  CAS  PubMed  Google Scholar 

  160. Stringer SL, Stringer JR, Blase MA, Walzer PD, Cushion MT. Pneumocystis carinii: sequence from ribosomal RNA implies a close relationship with fungi. Exp Parasitol 1989; 68(4): 450–461

    Article  CAS  PubMed  Google Scholar 

  161. Gigliotti F, Limper AH, Wright T. Pneumocystis. Cold Spring Harb Perspect Med 2014; 4(12): a019828

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  162. Lu JJ, Lee CH. Pneumocystis pneumonia. J Formos Med Assoc 2008; 107(11): 830–842

    Article  CAS  PubMed  Google Scholar 

  163. Catherinot E, Lanternier F, Bougnoux ME, Lecuit M, Couderc LJ, Lortholary O. Pneumocystis jirovecii pneumonia. Infect Dis Clin North Am 2010; 24(1): 107–138

    Article  PubMed  Google Scholar 

  164. Kaplan JE, Hanson D, Dworkin MS, Frederick T, Bertolli J, Lindegren ML, Holmberg S, Jones JL. Epidemiology of human immunodeficiency virus-associated opportunistic infections in the United States in the era of highly active antiretroviral therapy. Clin Infect Dis 2000; 30(s1 Suppl 1): S5–S14

    Article  PubMed  Google Scholar 

  165. Ruxrungtham K, Brown T, Phanuphak P. HIV/AIDS in Asia. Lancet 2004; 364(9428): 69–82

    Article  PubMed  Google Scholar 

  166. Beck JM, Cushion MT. Pneumocystis workshop: 10th anniversary summary. Eukaryot Cell 2009; 8(4): 446–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Wang XL, Wang XL, Wei W, An CL. Retrospective study of Pneumocystis pneumonia over half a century in mainland China. J Med Microbiol 2011; 60(Pt 5): 631–638

    Article  PubMed  Google Scholar 

  168. Liu Y, Su L, Jiang SJ, Qu H. Risk factors for mortality from Pneumocystis carinii pneumonia (PCP) in non-HIV patients: a meta-analysis. Oncotarget 2017; 8(35): 59729–59739

    PubMed  PubMed Central  Google Scholar 

  169. Wang DD, Zheng MQ, Zhang N, An CL. Investigation of Pneumocystis jirovecii colonization in patients with chronic pulmonary diseases in the People’s Republic of China. Int J Chron Obstruct Pulmon Dis 2015; 10: 2079–2085

    CAS  PubMed  PubMed Central  Google Scholar 

  170. Huang YS, Yang JJ, Lee NY, Chen GJ, Ko WC, Sun HY, Hung CC. Treatment of Pneumocystis jirovecii pneumonia in HIVinfected patients: a review. Expert Rev Anti Infect Ther 2017; 15 (9): 873–892

    Article  CAS  PubMed  Google Scholar 

  171. Guo F, Chen Y, Yang SL, Xia H, Li XW, Tong ZH. Pneumocystis pneumonia in HIV-infected and immunocompromised non-HIV infected patients: a retrospective study of two centers in China. PLoS One 2014; 9(7): e101943

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  172. Chen M, Tian X, Qin F, Zhou J, Liu J, Wang M, Xu KF. Pneumocystis pneumonia in patients with autoimmune diseases: a retrospective study focused on clinical characteristics and prognostic factors related to death. PLoS One 2015; 10(9): e0139144

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  173. Lemiale V, Debrumetz A, Delannoy A, Alberti C, Azoulay E. Adjunctive steroid in HIV-negative patients with severe Pneumocystis pneumonia. Respir Res 2013; 14(1): 87

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  174. Asai N, Motojima S, Ohkuni Y, Matsunuma R, Nakashima K, Iwasaki T, Nakashita T, Otsuka Y, Kaneko N. Early diagnosis and treatment are crucial for the survival of Pneumocystis pneumonia patients without human immunodeficiency virus infection. J Infect Chemother 2012; 18(6): 898–905

    Article  PubMed  Google Scholar 

  175. Deng X, Zhuo L, Lan Y, Dai Z, Chen WS, Cai W, Kovacs JA, Ma L, Tang X. Mutational analysis of Pneumocystis jirovecii dihydropteroate synthase and dihydrofolate reductase genes in HIV-infected patients in China. J Clin Microbiol 2014; 52(11): 4017–4019

    Article  PubMed  PubMed Central  Google Scholar 

  176. Takahashi T, Endo T, Nakamura T, Sakashitat H, Kimurat K, Ohnishit K, Kitamura Y, Iwamoto A. Dihydrofolate reductase gene polymorphisms in Pneumocystis carinii f. sp. hominis in Japan. J Med Microbiol 2002; 51(6): 510–515

    Article  CAS  PubMed  Google Scholar 

  177. Siripattanapipong S, Leelayoova S, Mungthin M, Worapong J, Tan-Ariya P. Study of DHPS and DHFR genes of Pneumocystis jirovecii in Thai HIV-infected patients. Med Mycol 2008; 46(4): 389–392

    Article  CAS  PubMed  Google Scholar 

  178. Robberts FJ, Chalkley LJ, Weyer K, Goussard P, Liebowitz LD. Dihydropteroate synthase and novel dihydrofolate reductase gene mutations in strains of Pneumocystis jirovecii from South Africa. J Clin Microbiol 2005; 43(3): 1443–1444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Kazanjian PH, Fisk D, Armstrong W, Shulin Q, Liwei H, Ke Z, Meshnick S. Increase in prevalence of Pneumocystis carinii mutations in patients with AIDS and P. carinii pneumonia, in the United States and China. J Infect Dis 2004; 189(9): 1684–1687

    Article  PubMed  Google Scholar 

  180. Zhang Y, Hagen F,Wan Z, Liu Y, Liu Y,Wang Q, de Hoog GS, Li R, Zhang J. Two cases of sporotrichosis of the right upper extremity in right-handed patients with diabetes mellitus. Rev Iberoam Micol 2016; 33(1): 38–42

    Article  CAS  PubMed  Google Scholar 

  181. Zhang Y, Hagen F, Stielow B, Rodrigues AM, Samerpitak K, Zhou X, Feng P, Yang L, Chen M, Deng S, Li S, Liao W, Li R, Li F, Meis JF, Guarro J, Teixeira M, Al-Zahrani HS, Pires de Camargo Z, Zhang L, de Hoog GS. Phylogeography and evolutionary patterns in Sporothrix spanning more than 14 000 human and animal case reports. Persoonia 2015; 35(1): 1–20

    Article  PubMed  PubMed Central  Google Scholar 

  182. Chen YC. Sporotrichosis. Chin J Mycol (Zhongguo Zhen Jun Xue Za Zhi) 2008; 3(4): 233–241 (in Chinese)

    CAS  Google Scholar 

  183. Liu TT, Zhang K, Zhou X. Molecular identification of Sporothrix clinical isolates in China. J Zhejiang Univ Sci B 2014; 15(1): 100–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Yu X, Wan Z, Zhang Z, Li F, Li R, Liu X. Phenotypic and molecular identification of Sporothrix isolates of clinical origin in Northeast China. Mycopathologia 2013; 176(1-2): 67–74

    Article  PubMed  PubMed Central  Google Scholar 

  185. Zhao MD, Zhou X, Liu TT, Yang ZB. Morphological and physiological comparison of taxa comprising the Sporothrix schenckii complex. J Zhejiang Univ Sci B 2015; 16(11): 940–947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Marimon R, Cano J, Gené J, Sutton DA, Kawasaki M, Guarro J. Sporothrix brasiliensis, S. globosa, and S. mexicana, three new Sporothrix species of clinical interest. J Clin Microbiol 2007; 45 (10): 3198–3206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Mahajan VK. Sporotrichosis: an overview and therapeutic options. Dermatol Res Pract 2014; 2014: 272376

    Article  PubMed  PubMed Central  Google Scholar 

  188. Pappas PG, Tellez I, Deep AE, Nolasco D, Holgado W, Bustamante B. Sporotrichosis in Peru: description of an area of hyperendemicity. Clin Infect Dis 2000; 30(1): 65–70

    Article  CAS  PubMed  Google Scholar 

  189. Sirisanthana T, Supparatpinyo K. Epidemiology and management of penicilliosis in human immunodeficiency virus-infected patients. Int J Infect Dis 1998; 3(1): 48–53

    Article  CAS  PubMed  Google Scholar 

  190. Li HR, Cai SX, Chen YS, Yu ME, Xu NL, Xie BS, Lin M, Hu XL. Comparison of Talaromyces marneffei infection in human immunodeficiency virus-positive and human immunodeficiency virus-negative patients from Fujian, China. Chin Med J (Engl) 2016; 129(9): 1059–1065

    Article  Google Scholar 

  191. Zheng J, Gui X, Cao Q, Yang R, Yan Y, Deng L, Lio J. A clinical study of acquired immunodeficiency syndrome associated Penicillium marneffei infection from a non-endemic area in China. PLoS One 2015; 10(6): e0130376

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  192. Capponi M, Segretain G, Sureau P. Penicillosis from Rhizomys sinensis. Bull Soc Pathol Exot 1956; 49(3): 418–421

    CAS  Google Scholar 

  193. DiSalvo AF, Fickling AM, Ajello L. Infection caused by Penicillium marneffei: description of first natural infection in man. Am J Clin Pathol 1973; 60(2): 259–263

    Article  CAS  PubMed  Google Scholar 

  194. Deng ZL. Progressive disseminated penicilliosis caused by Penicillium marneffei. J Guangxi Med Col (Gangxi Yi Xue Yuan Xue Bao) 1984; 1(1): 1–4 (in Chinese)

    CAS  Google Scholar 

  195. Chan JF, Lau SK, Yuen KY, Woo PC. Talaromyces (Penicillium) marneffei infection in non-HIV-infected patients. Emerg Microbes Infect 2016; 5(3): e19

    Article  PubMed  PubMed Central  Google Scholar 

  196. Hu Y, Zhang J, Li X, Yang Y, Zhang Y, Ma J, Xi L. Penicillium marneffei infection: an emerging disease in mainland China. Mycopathologia 2013; 175(1-2): 57–67

    Article  PubMed  Google Scholar 

  197. Cao C, Liang L,Wang W, Luo H, Huang S, Liu D, Xu J, Henk DA, Fisher MC. Common reservoirs for Penicillium marneffei infection in humans and rodents, China. Emerg Infect Dis 2011; 17(2): 209–214

    Article  PubMed  PubMed Central  Google Scholar 

  198. Huang X, He G, Lu S, Liang Y, Xi L. Role of Rhizomys pruinosus as a natural animal host of Penicillium marneffei in Guangdong, China. Microb Biotechnol 2015; 8(4): 659–664

    Article  PubMed  PubMed Central  Google Scholar 

  199. Gugnani H, Fisher MC, Paliwal-Johsi A, Vanittanakom N, Singh I, Yadav PS. Role of Cannomys badius as a natural animal host of Penicillium marneffei in India. J Clin Microbiol 2004; 42(11): 5070–5075

    Article  PubMed  PubMed Central  Google Scholar 

  200. Fisher MC, Hanage WP, de Hoog S, Johnson E, Smith MD, White NJ, Vanittanakom N. Low effective dispersal of asexual genotypes in heterogeneous landscapes by the endemic pathogen Penicillium marneffei. PLoS Pathog 2005; 1(2): e20

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  201. Kauffman CA. Histoplasmosis: a clinical and laboratory update. Clin Microbiol Rev 2007; 20(1): 115–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  202. Wang Y, Pan B, Wu J, Bi X, Liao W, Pan W, Gu J. Detection and phylogenetic characterization of a case of Histoplasma capsulatum infection in mainland China. Am J Trop Med Hyg 2014; 90(6): 1180–1183

    Article  PubMed  PubMed Central  Google Scholar 

  203. Ge L, Zhou C, Song Z, Zhang Y, Wang L, Zhong B, Hao F. Primary localized histoplasmosis with lesions restricted to the mouth in a Chinese HIV-negative patient. Int J Infect Dis 2010; 14 (Suppl 3): e325–e328

    Article  PubMed  Google Scholar 

  204. Pan B, Chen M, Pan W, Liao W. Histoplasmosis: a new endemic fungal infection in China? Review and analysis of cases. Mycoses 2013; 56(3): 212–221

    Article  PubMed  Google Scholar 

  205. Stevens DA. Coccidioidomycosis. N Engl J Med 1995; 332(16): 1077–1082

    Article  CAS  PubMed  Google Scholar 

  206. Wang XL, Wang S, An CL. Mini-review of published reports on coccidioidomycosis in China. Mycopathologia 2015; 180(5-6): 299–303

    Article  CAS  PubMed  Google Scholar 

  207. Xi L, Fukushima K, Lu C, Takizawa K, Liao R, Nishimura K. First case of Arthrographis kalrae ethmoid sinusitis and ophthalmitis in the People’s Republic of China. J Clin Microbiol 2004; 42(10): 4828–4831

    Article  PubMed  PubMed Central  Google Scholar 

  208. Zhang QQ, Zhu LP, Weng XH, Li L, Wang JJ. Meningitis due to Prototheca wickerhamii: rare case in China. Med Mycol 2007; 45 (1): 85–88

    Article  PubMed  Google Scholar 

  209. Li DM, Li RY, de Hoog GS, Sudhadham M, Wang DL. Fatal Exophiala infections in China, with a report of seven cases. Mycoses 2011; 54(4): e136–e142

    Article  PubMed  Google Scholar 

  210. Li DM, Chen XR. A new superficial fungal infection caused by Coniosporium epidermidis. J Am Acad Dermatol 2010; 63(4): 725–727

    Article  PubMed  Google Scholar 

  211. Pan W, Liao W, Hagen F, Theelen B, Shi W, Meis JF, Boekhout T. Meningitis caused by Filobasidium uniguttulatum: case report and overview of the literature. Mycoses 2012; 55(2): 105–109

    CAS  PubMed  Google Scholar 

  212. Wu Y, Wang J, Li W, Jia H, Che J, Lu J, Liu L, Cheng Y. Pichia fabianii blood infection in a premature infant in China: case report. BMC Res Notes 2013; 6(1): 77

    Article  PubMed  PubMed Central  Google Scholar 

  213. Fu M, Ge Y, Chen W, Feng S, She X, Li X, Liu W. Tinea faciei in a newborn due to Trichophyton tonsurans. J Biomed Res 2013; 27 (1): 71–74

    Article  PubMed  Google Scholar 

  214. Chen M, Houbraken J, Pan W, Zhang C, Peng H, Wu L, Xu D, Xiao Y, Wang Z, Liao W. Pulmonary fungus ball caused by Penicillium capsulatum in a patient with type 2 diabetes: a case report. BMC Infect Dis 2013; 13(1): 496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  215. Cai Q, Lv GX, Jiang YQ, Mei H, Hu SQ, Xu HB, Wu XF, Shen YN, Liu WD. The first case of phaeohyphomycosis caused by Rhinocladiella basitona in an immunocompetent child in China. Mycopathologia 2013; 176(1-2): 101–105

    Article  PubMed  Google Scholar 

  216. Zou Y, Bi Y, Bu H, He Y, Guo L, Shi D. Infective meningitis caused by Phialemonium curvatum. J Clin Microbiol 2014; 52(8): 3111–3113

    Article  PubMed  PubMed Central  Google Scholar 

  217. Zhu CY, Yang YP, Sheng P, Li W, Huang WM, Fan YM. Cutaneous chromoblastomycosis caused by Veronaea botryosa in a patient with pemphigus vulgaris and review of published reports. Mycopathologia 2015; 180(1-2): 123–129

    Article  PubMed  Google Scholar 

  218. Wang L, Al-Hatmi AM, Lai X, Peng L, Yang C, Lai H, Li J, Meis JF, de Hoog GS, Zhuo C, Chen M. Bipolaris oryzae, a novel fungal opportunist causing keratitis. Diagn Microbiol Infect Dis 2016; 85 (1): 61–65

    Article  CAS  PubMed  Google Scholar 

  219. Mijiti J, Pan B, de Hoog S, Horie Y, Matsuzawa T, Yilifan Y, Liu Y, Abliz P, Pan W, Deng D, Guo Y, Zhang P, Liao W, Deng S. Severe chromoblastomycosis-like cutaneous infection caused by Chrysosporium keratinophilum. Front Microbiol 2017; 8: 83

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was funded in part by grants from the Severe Infectious Diseases Specific Projects from China’s Ministry of Health (No. 2013ZX10004612-7), the 973 Program (Nos. 2013CB531601 and 2013CB531606), and the National Natural Science Foundation of China (No. 81201269).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Weihua Pan or Wanqing Liao.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, M., Xu, Y., Hong, N. et al. Epidemiology of fungal infections in China. Front. Med. 12, 58–75 (2018). https://doi.org/10.1007/s11684-017-0601-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11684-017-0601-0

Keywords

Navigation