This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Pfaller, M. A.
Right arrow Articles by Hollis, R. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Pfaller, M. A.
Right arrow Articles by Hollis, R. J.

 Previous Article  |  Next Article 

Journal of Clinical Microbiology, March 2002, p. 852-856, Vol. 40, No. 3
0095-1137/02/$04.00+0     DOI: 10.1128/JCM.40.3.852-856.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Trends in Antifungal Susceptibility of Candida spp. Isolated from Pediatric and Adult Patients with Bloodstream Infections: SENTRY Antimicrobial Surveillance Program, 1997 to 2000

M. A. Pfaller,1,2* D. J. Diekema,1,3 R. N. Jones,4 S. A. Messer,1 R. J. Hollis,1 and the SENTRY Participants Group

Departments of Pathology,1 Medicine,3 Epidemiology, University of Iowa College of Medicine and College of Public Health, Iowa City, Iowa,2 The JONES Group/JMI Laboratories, North Liberty, Iowa4

Received 24 September 2001/ Returned for modification 2 December 2001/ Accepted 12 December 2001


arrow
ABSTRACT
 
From 1 January 1997 through 31 December 2000, 2,047 bloodstream infections (BSIs) due to Candida spp. were reported from hospitals in the United States, Canada, Latin America, and Europe participating in the SENTRY Antifungal Surveillance Program. Among individuals in four age groups (<=1, 2 to 15, 16 to 64, and >=65 years) Candida albicans was the most common species, causing 60, 55, 55, and 50% of infections, respectively. C. glabrata caused 17 to 23% of BSIs in those ages 16 to 64 and >=65 years, whereas it caused only 3% of BSIs in the individuals in the two younger age groups (P < 0.001). C. parapsilosis (which caused 21 to 24% of BSIs) and C. tropicalis (which caused 7 to 10% of BSIs) were more common than C. glabrata in individuals ages <=1 year and 2 to 15 years. Isolates of Candida spp. showed a trend of decreasing susceptibility to fluconazole, itraconazole, and amphotericin B with increasing patient age (P <= 0.01). None of the C. glabrata isolates from individuals <=1 year old were resistant to fluconazole, whereas they made up 5 to 9% of isolates from individuals ages 16 to 64 and >=65 years. Isolates of C. tropicalis from patients <=1 year old were more susceptible to flucytosine (MIC at which 90% of isolates are inhibited [MIC90], 0.5 µg/ml; 0% resistant isolates) than those from patients >=65 years old (MIC90, 32 µg/ml; 11% resistant isolates). The investigational triazoles posaconazole, ravuconazole, and voriconazole were all highly active against all species of Candida from individuals in all age groups. These data demonstrate differences in the species distributions of pathogens and differences in antifungal resistance among isolates from individuals in the pediatric and adult age groups. Ongoing surveillance will enhance efforts to limit the extent of antifungal resistance in individuals in various age groups.


arrow
INTRODUCTION
 
The proliferation of antimicrobial resistance surveillance programs has provided useful information regarding resistance trends, the distribution of pathogens among various countries, and among types of infections (7). Although most surveillance programs have focused on bacterial pathogens, several have provided information on invasive candidiasis as well. A population-based surveillance study conducted by the Centers for Disease Control and Prevention (5), the NEMIS study (2, 9, 16, 19), the SCOPE study (4), and the SENTRY Program (3, 11, 13-15) have all contributed information regarding the species distributions and antifungal susceptibilities of isolates of Candida spp. isolated from patients with bloodstream infection (BSIs) over the decade from 1990 to 2000. Although the Centers for Disease Control and Prevention and NEMIS studies provided some information on Candida BSIs in both adult and neonatal populations, none of the Candida surveillance studies have provided information on the distributions of species or the antifungal susceptibility profiles of pathogens isolated from patients with BSIs stratified according to the age of the patient.

The SENTRY Antifungal Surveillance Program has been active continuously since January 1997 and has reported the specific types of pathogens isolated from more than 2,000 episodes of Candida BSIs in 72 medical centers internationally and antifungal susceptibility data for those pathogens (3, 11, 13-15). In the study described in this report, we examined the frequency of pathogen occurrence and the susceptibilities of the various species isolated to both licensed and investigational antifungal agents for individuals in four different age groups: <=1, 2 to 15, 16 to 64, and >=65 years.


arrow
MATERIALS AND METHODS
 
Study design. The SENTRY Antifungal Surveillance Program was established in 1997 and has been described in detail in previous publications (3, 11, 13-15). The present report focuses on BSIs due to Candida spp. from U.S., Canadian, Latin American, and European sites. BSIs due to Candida spp. were reported from 32 medical centers in the United States, 23 medical centers in Europe, 9 medical centers in Latin America, and 7 medical centers in Canada over the 4-year period from January 1997 through December 2000. The institutions that contributed data or isolates to the study are listed in the Appendix.

Organism identification. All fungal isolates from blood cultures were identified at the participating institutions by the routine method in use at each laboratory. Upon receipt at the monitoring site, the isolates were subcultured onto potato dextrose agar (Remel, Lenexa, Kans.) and CHROMagar Candida medium (Hardy Laboratories, Santa Maria, Calif.) to ensure viability and purity. Confirmation of species identification was performed with Vitek and API products (bioMerieux, St. Louis, Mo.), as recommended by the manufacturer, or by conventional methods, as required (22). Isolates were stored as suspensions in water or on agar slants at ambient temperature until needed.

Susceptibility testing. Antifungal susceptibility testing of isolates of Candida spp. was performed by the reference broth microdilution method described by the National Committee for Clinical Laboratory Standards (NCCLS) (8). The susceptibilities of the isolates to amphotericin B were determined by use of the Etest (AB BIODISK, Solna, Sweden) and RPMI 1640 agar with 2% glucose (Remel), as described previously (12). Standard powders of fluconazole (Pfizer, Inc., New York, N.Y.), voriconazole (Pfizer), ravuconazole (Bristol-Myers Squibb, Wallingford, Conn.), posaconazole (Schering-Plough, Kenilworth, N.J.), itraconazole (Janssen, Beerse, Belgium), and amphotericin B and flucytosine (Sigma, St. Louis, Mo.) were obtained from the respective manufacturers. The MICs of fluconazole, voriconazole, ravuconazole, posaconazole, itraconazole, and flucytosine were the lowest concentrations at which a prominent decrease (approximately 50%) in turbidity relative to that in the growth control well was observed (8). Amphotericin B MICs determined by the Etest were read after 48 h of incubation at 35°C and were determined to be the concentration at which 100% inhibition of growth occurred, which on the Etest strip was the location where the border of the elliptical inhibition zone intercepted the scale on the strip edge (12). Quality control was ensured by testing the strains recommended by NCCLS (8): Candida krusei ATCC 6258 and C. parapsilosis ATCC 22019.

Interpretive criteria for susceptibility to fluconazole (MIC, <=8 µg/ml), itraconazole (MIC, <=0.12 µg/ml), and flucytosine (MIC, <=4 µg/ml) were those published by Rex et al. (17) and NCCLS (8). The investigational triazoles posaconazole, voriconazole and ravuconazole have not been assigned interpretive breakpoints. For purposes of comparison and because preliminary pharmacokinetic data indicate that the levels of these agents achievable in serum may range from 2 to 6 µg/ml, depending on the dosing regimen (20), we have used a breakpoint for susceptibility of <=1 µg/ml for all three agents. Interpretive criteria have not yet been defined for amphotericin B; however for comparison purposes in this surveillance study we have determined isolates that were inhibited by <=1 µg/ml to be susceptible.

Statistical methods. Comparison of the species distributions or MIC distributions in terms of other factors were made by the chi-square test for categorical variables and the Wilcoxon rank sum text for ordinal variables (MICs). All reported P values are two-tailed.


arrow
RESULTS AND DISCUSSION
 
Frequency of occurrence of bloodstream pathogens. During the 4-year study period (January 1997 to December 2000), a total of 2,047 BSIs due to Candida spp. were reported by SENTRY participants. Table 1 compares the frequencies of occurrence of the seven most commonly isolated pathogens during the time period of the study. These seven species accounted for 99% of all Candida BSIs reported from SENTRY study sites. Overall, the rank order of the top five species was unchanged from year to year. These five species (C. albicans, C. glabrata, C. parapsilosis, C. tropicalis, and C. krusei) accounted for 97% of all Candida BSIs. As described previously (15), the only notable geographic difference in the species distribution among the three continents was a higher frequency of C. glabrata as a cause of BSIs in the United States.


View this table:
[in this window]
[in a new window]
  		TABLE 1. Species distributions of Candida Bloodstream Isolates by age group, SENTRY Program, 1997 to 2000abc

Comparing the frequency of isolation of different species by age group, we found identical rank orders for the groups 16 to 64 and >=65 years of age: C. albicans > C. glabrata > C. parapsilosis > C. tropicalis > C. krusei. The rank order of the frequency of isolation of different species for the groups <=1 and 2 to 15 years of age was considerably different from that for the two older age groups. The dominant causes of infections in individuals in the infant and pediatric age groups were C. albicans and C. parapsilosis, and very few infections were due to C. glabrata and C. krusei. Although C. albicans was the most common species in all age groups, the proportions of BSIs due to this species decreased from 60% in the group <=1 year of age to 50% in the group >=65 years of age (P = 0.007). C. glabrata was the second most common species overall, causing 17 to 23% of BSIs in the groups ages 16 to 64 and >=65 years. In contrast, C. glabrata accounted for only 3% of BSIs in the groups <=1 year and 2 to 15 years of age (P < 0.001 compared to the groups 16 to 64 and >=65 years of age) and was surpassed by both C. parapsilosis (which was the cause of 21 to 24% of BSIs) and C. tropicalis (which was the cause of 7 to 10% of BSIs) as causes of infection.

Differences in susceptibilities among isolates from individuals in different age groups to both licensed and investigational antifungal agents. Among the licensed antifungal agents fluconazole, itraconazole, amphotericin B, and flucytosine, the susceptibilities of isolates of Candida spp. with increasing patient age (P <= 0.01 for trend). Although flucytosine was active overall against isolates from individuals in all age groups (with 95 to 98% of isolates being susceptible), isolates of C. tropicalis from patients <=1 year of age were more susceptible to this agent (MIC at which 90% of isolates are inhibited [MIC90], 0.5 µg/ml; 0% resistant isolates) than those isolates from patients >=65 years of age (MIC90, 32 µg/ml; 11% resistant isolates) (data not shown).

Among the licensed and investigational azoles, fluconazole, posaconazole, ravuconazole, and voriconazole were all highly active (96 to 100% of isolates were susceptible) against C. albicans, C. tropicalis, C. guilliermondii, and C. lusitaniae, regardless of the age group (Table 2). Although fluconazole appeared to be less active against isolates of C. glabrata in those <=1 year of age (63% of isolates were susceptible) than against isolates from those 16 to 64 years of age (70% of isolates were susceptible) and >=65 years of age (73% of isolates were susceptible), there were no highly resistant (MIC, >=64 µg/ml) isolates in those <=1 year of age, whereas 5 to 9% of isolates from the two older groups were highly resistant. Itraconazole was less active than all of the other azoles tested against all species with the exception of C. albicans. Consistent with previous reports (3, 10, 13, 15), all three investigational triazoles were highly active against all species from all age groups with the exception of C. glabrata isolates from those in the group 16 to 64 years of age, with 88 to 90% of C. glabrata isolates from individuals in that group being susceptible to the three investigational triazoles at <=1 µg/ml but with 95 to 100% of C. glabrata isolates from all other age groups being susceptible to the three agents.


View this table:
[in this window]
[in a new window]
  		TABLE 2. Antifungal activities of fluconazole, itraconazole, and investigational azole antifungal agents against 2,029 invasive isolates of Candida spp. by patient age group, SENTRY Program, 1997 to 2000

The activities of amphotericin B, as determined by the Etest, against the five species that were the most common causes of BSIs are shown in Table 3. As expected, amphotericin B was the most active agent against C. albicans (MIC90, 1 µg/ml). The activities of amphotericin B against the other species were significantly less (P < 0.001) than that observed against C. albicans: MIC90 for C. glabrata, 4 µg/ml; MIC90 for C. parapsilosis, 4 µg/ml; MIC90 for C. krusei, 8 µg/ml. Although in our hands the Etest tended to give higher amphotericin B MICs for the non-C. albicans species than for C. albicans, the same tendency was seen with the NCCLS microdilution method when it was applied to a subset of 1,077 isolates (data not shown). Notably, 17.4% of C. glabrata isolates and 27.8% of C. krusei isolates appeared to be resistant (MICs, >=2 µg/ml) when they were tested by the NCCLS method. As reported previously (12), the level of agreement between the results of the Etest and those of the broth microdilution method was excellent (98.7% within 2 log2 dilutions).


View this table:
[in this window]
[in a new window]
  		TABLE 3. Antifungal activities of amphotericin B against 1,997 invasive isolates of Candida spp., SENTRY, Program, 1997 to 2000

It appears that the differences in susceptibility to amphotericin B and the azoles among the isolates from individuals in four age groups may be largely due to differences in the species distributions among individuals in the younger age groups compared to those among individuals in the older age groups. The groups <=1 year and 2 to 15 years of age were predominantly infected with C. albicans and C. parapsilosis, both of which were considerably more susceptible than C. glabrata to the antifungal agents tested. Individuals in the older age groups, and particularly those >=65 years old, had relatively fewer infections due to C. albicans and significantly more infections due to C. glabrata than individuals in the younger age groups. The decreased susceptibilities of C. glabrata to both the azoles and amphotericin B are evident in Tables 2 and 3 and accounted for the differences in susceptibilities among the isolates from individuals in the different age groups.

The predominance of C. albicans and C. parapsilosis as the etiologic agents of fungemia in neonates has previously been noted by Kao et al. (5) and Saiman et al. (19), among others; however, the lack of infections with C. glabrata and C. krusei in this age group is less well appreciated. The increasing importance of C. glabrata in the adult population is well known, and the proportion of BSIs due to C. glabrata has been noted to be considerably higher in individuals >60 years of age in some institutions (6, 15). The reasons for these differences are speculative but may relate to the tendency for neonatologists and pediatricians to use amphotericin B preferentially over fluconazole in the treatment of documented or suspected candidemia (18) and the pervasive use of fluconazole in the adult hospital population (1). Furthermore, vertical transmission of C. albicans from mother to infant and horizontal transmission of C. parapsilosis from patient to patient in the neonatal intensive care unit environment are well documented and may also account for the predominance of these two species in infants and children (9, 21).

Summary and conclusions. Antifungal resistance surveillance programs provide important information both for the development of recommendations for empirical antifungal therapy and for the design of programs for the control of antifungal resistance. The present study demonstrates differences in the spectrum of pathogens and in antifungal susceptibilities among isolates from individuals in the pediatric and adult age groups in the SENTRY Program. The most notable trends were those of a decreasing frequency of occurrence of C. albicans and an increasing frequency of occurrence of C. glabrata with increasing patient age.

Decreased susceptibilities to fluconazole, itraconazole, and amphotericin B were most prominent among C. glabrata and C. krusei isolates from individuals in all age groups. Ongoing surveillance is essential and will enhance efforts to limit the extent of resistance among isolates from individuals in the various age groups.

APPENDIX Participating institutions contributing data or isolates to the study included The Medical Center of Delaware, Wilmington (L. Steele-Moore); Clarion Health Methodist Hospital, Indianapolis, Ind. (G. Denys); Henry Ford Hospital, Detroit, Mich. (C. Staley); Summa Health System, Akron, Ohio (J. R. Dipersio); Good Samaritan Regional Medical Center, Phoenix, Ariz. (M. Saubolle); Denver General Hospital, Denver, Colo. (M. L. Wilson); University of New Mexico Hospital, Albuquerque (G. D. Overturf); University of Illinois at Chicago (P. C. Schreckenberger); University of Iowa Hospitals and Clinics, Iowa City (R. N. Jones); Creighton University, Omaha, Nebr. (S. Cavalieri); Froedtert Memorial Lutheran Hospital-East, Milwaukee, Wis. (S. Kehl); Boston Veterans Affairs Medical Center, Boston, Mass. (S. Brecher); Columbia Presbyterian Medical Center, New York, N.Y. (P. Della-Latta); Long Island Jewish Medical Center, New Hyde Park, N.Y. (H. Isenberg); Strong Memorial Hospital, Rochester, N.Y. (D. Hardy); Kaiser Regional Laboratory, Berkeley, Calif. (J. Fusco); Sacred Heart Medical Center, Spokane, Wash. (M. Hoffmann); University of Washington Medical Center, Seattle (S. Swanzy); Barnes-Jewish Hospital, St. Louis, Mo. (P. R. Murray); Parkland Health & Hospital System, Dallas, Tex. (P. Southern); The University of Texas Medical School, Houston (A. Wanger); University of Texas Medical Branch at Galveston, Galveston, Tex. (B. Reisner); University of Louisville Hospital, Louisville, Ky. (J. Snyder); University of Mississippi Medical Center, Jackson (J. Humphries); Carolinas Medical Center, Charlotte, N.C. (S. Jenkins); University of Virginia Medical Center, Charlottesville (K. Hazen); University of Alberta Hospital, Edmonton, Alberta, Canada (R. Rennie); Health Sciences Centre, Winnipeg, Manitoba, Canada (D. Hoban); Queen Elizabeth II Health Sciences Centre, Halifax, Nova Scotia, Canada (K. Forward); Ottawa General Hospital, Ottawa, Ontario, Canada (B. Toye); Royal Victoria Hospital, Montreal, Quebec, Canada (H. Robson); Microbiology Laboratory, C.E.M.I.C., Buenos Aires, Argentina (J. Smayvsky); Hospital San Lucas and Olivos Community Hospital, Buenos Aires, Argentina (J. M. Casellas and G. Tome); Lamina LTDA, Rio De Janeiro, Brazil (J. L. M. Sampaio); Unidad De Microbiologia Oriente, Santiago, Chile (V. Prado); Hospital Clinico Universidad Catolica, Santiago, Chile (E. Palavecino); Corp. Para Investigaciones Biologicas, Medellin, Colombia (J. A. Robledo); Instituto Nacional de la Nutricion, Mexico City, Mexico (J. S. Osornio); Laboratorio Medico Santa Luzia, Florianopolis, Brazil; Instituto DE Doencas Infecciosas-IDIPA, Sao Paulo, Brazil (H. S. Sader); Centro Medico De Caracas, San Bernadino, Caracas, Venezuela (M. Guzman); Chru De Lille Hopital Calmette, Lille, France (M. Roussel-Delvallez); National University of Athens Medical School, Athens, Greece (N. Legakis); Sheba Medical Center, Tel-Hashomer, Israel (N. Keller); University Hospital V. de Macarena, Seville, Spain (E. J. Perea); Hospital de Bellvitge, Barcelona, Spain (J. Linares); Hospital Ramon y Cajal, Madrid, Spain (R. Canton); Unite de Bacteriologie, Luasanne, Switzerland (F. Praplan); Hacettepe Universitaesi Tip Fakultesi, Ankara, Turkey (D. Gur); Universita degli Studi di Genova, Genoa, Italy (E. Debbia); Azienda Policlinico University Catania, Catania, Italy (G. Nicoletti); Policlinico Agostino Germelli, Rome, Italy (G. Fadda); Universitat Bonn, Bonn, Germany (K. P. Schaalb); J.-W.-Goethe Universitat, Frankfurt, Germany (P. Shah); University Hospital, Linkoping, Sweden (H. Hanberger); Sera & Vaccines Central Research Laboratory, Warsaw, Poland (W. Hryniewicz); St. Thomas Hospital, London, United Kingdom (G. French); Universite Libre de Bruxelles-Hopital Erasme, Brussels, Belgium (M. J. Struelens); and Marmara Universitesi Tip Fakultesi, Istanbul, Turkey (V. Korten).


arrow
ACKNOWLEDGMENTS
 
This study was supported in part by research grants from Bristol-Myers Squibb (SENTRY), Pfizer Pharmaceuticals, and Schering-Plough Research Institute.

Linda Elliott provided excellent support in the preparation of the manuscript. We express our appreciation to all SENTRY site participants.


arrow
FOOTNOTES
 
* Corresponding author. Mailing address: Medical Microbiology Division, C606 GH, Department of Pathology, University of Iowa College of Medicine, Iowa City, IA 52242. Phone: (319) 384-9566. Fax: (319) 356-4916. E-mail: michael-pfaller{at}uiowa.edu. Back


arrow
REFERENCES
 
    1
  1. Berrouane, Y. F., L. A. Herwaldt, and M. A. Pfaller. 1999. Trends in antifungal use and epidemiology of noscocomial yeast infections in a university hospital. J. Clin. Microbiol. 37:531-537.[Abstract/Free Full Text]
    2. 2
  2. Blumberg, H. M., W. R. Jarvis, J. M. Soucie, J. E. Edwards, J. E. Patterson, M. A. Pfaller, M. S. Rangel-Frausto, M. G. Rinaldi, L. Saiman, R. T. Wiblin, R. P. Wenzel, and the NEMIS Study Group. 2001. Risk factors for candidal blood stream infections in surgical intensive care unit patients: The NEMIS Prospective Multicenter Study. Clin. Infect. Dis. 33:177-186.[CrossRef][Medline]
    3. 3
  3. Diekema, D. J., M. A. Pfaller, S. A. Messer, A. Houston, R. J. Hollis, G. V. Doern, R. N. Jones, and The SENTRY Participants Group. 1999. In vitro activities of BMS-207-147 against over 600 contemporary clinical blood stream isolates of Candida species from the SENTRY Antimicrobial Surveillance Program in North America and Latin America. Antimicrob. Agents Chemother. 43:2236-2239.[Abstract/Free Full Text]
    4. 4
  4. Edmond, M. B., S. E. Wallace, D. K. McClish, M. A. Pfaller, R. N. Jones, and R. P. Wenzel. 1999. Nosocomial blood stream infections in United States hospitals: a three-year analysis. Clin. Infect. Dis. 29:239-244.[Medline]
    5. 5
  5. Kao, A. S., M. E. Brandt, W. R. Pruitt, L. A. Conn, B. A. Perkins, D. S. Stevens, W. S. Baughman, A. L. Reingold, G. A. Rothrock, M. A. Pfaller, R. W. Pinner, and R. A. Hajjeh. 1999. The epidemiology of candidemia in two United States cities: results of a population-based active surveillance. Clin. Infect. Dis. 29:1164-1170.[CrossRef][Medline]
    6. 6
  6. Kauffman, C. A. 2001. Fungal infections in older adults. Clin. Infect. Dis. 33:550-555.[CrossRef][Medline]
    7. 7
  7. Masterton, R. G. 2000. Surveillance studies: how can they help the management of infection? J. Antimicrob. Chemother. 46:53-58.[Abstract/Free Full Text]
    8. 8
  8. National Committee for Clinical Laboratory Standards. 1997. Reference method for broth dilution antifungal susceptibility testing of yeasts. Approved standard M27-A. National Committee for Clinical Laboratory Standards, Wayne, Pa.
    9. 9
  9. Pfaller, M. A., S. A. Messer, A. Houston, M. S. Rangel-Frausto, T. Wiblin, H. M. Blumberg, J. E. Edwards, W. Jarvis, M. A. Martin, H. C. Neu, L. Saiman, J. E. Patterson, J. C. Dibb, C. M. Roldan, M. G. Rinaldi, and R. P. Wenzel. 1998. National Epidemiology of Mycoses Survey: a multicenter study of strain variation and antifungal susceptibility among isolates of Candida species. Diagn. Microbiol. Infect. Dis. 31:289-296.[CrossRef][Medline]
    10. 10
  10. Pfaller, M. A., S. A. Messer, R. J. Hollis, R. N. Jones, G. V. Doern, M. E. Brandt, and R. A. Hajjeh. 1998. In vitro susceptibilities of Candida bloodstream isolates to the new triazole antifungal agents BMS-207147, Sch 56592, and voriconazole. Antimicrob. Agents Chemother. 42:3242-3244.[Abstract/Free Full Text]
    11. 11
  11. Pfaller, M. A., R. N. Jones, G. V. Doern, H. S. Sader, R. J. Hollis, and S. A. Messer for the SENTRY Participant Group. 1998. International surveillance of blood stream infections due to Candida species: frequency of occurrence and antifungal susceptibilities of isolates collected in1997 in the United States, Canada, and South America for the SENTRY Program. J. Clin. Microbiol. 36:1886-1889.[Abstract/Free Full Text]
    12. 12
  12. Pfaller, M. A., S. A. Messer, and A. Bolmstrom. 1998. Evaluation of Etest for determining in vitro susceptibility of yeast isolates to amphotericin B. Diagn. Microbiol Infect. Dis. 32:223-227.[CrossRef][Medline]
    13. 13
  13. Pfaller, M. A., R. N. Jones, G. V. Doern, A. C. Fluit, J. Verhoef, H. S. Sader, S. A. Messer, A. Houston, S. Coffman, and, R. J. Hollis for the SENTRY Participant Group (Europe). 1999. International surveillance of blood stream infections due to Candida species in the European SENTRY Program: species distribution and antifungal susceptibility including the investigational triazole and echinocandin agents. Diagn. Microbiol. Infect. Dis. 35:19-25.[CrossRef][Medline]
    14. 14
  14. Pfaller, M. A., R. N. Jones, G. V. Doern, H. S. Sader, S. A. Messer, A. Houston, S. Coffman, R. J. Hollis, and the SENTRY Participant Group. 2000. Bloodstream infections due to Candida species: SENTRY Antimicrobial Surveillance Program in North America and Latin America, 1997-1998. Antimicrob. Agents Chemother. 44:747-751.[Abstract/Free Full Text]
    15. 15
  15. Pfaller, M. A., D. J. Diekema, R. N. Jones, H. S. Sader, A. C. Fluit, R. J. Hollis, and S. A. Messer. 2001. International surveillance of bloodstream infections due to Candida species: frequency of occurrence and in vitro susceptibility to fluconazole, ravuconazole, and voriconazole among isolates collected from 1997 through 1999 in the SENTRY Antimicrobial Surveillance Program. J. Clin. Microbiol. 39:3254-3259.[Abstract/Free Full Text]
    16. 16
  16. Rangel-Frasuto, M. S., T. Wiblin, H. M. Blumberg, L. Saiman, J. Patterson, M. Rinaldi, M. Pfaller, J. E. Edwards, Jr., W. Jarvis, J. Dawson, and R. P. Wenzel. 1999. National Epidemiology of Mycoses Survey (NEMIS): variations in rates of blood stream infections due to Candida species in seven surgical intensive care units and six neonatal intensive care units. Clin. Infect. Dis. 29:253-258.[Medline]
    17. 17
  17. Rex, J. H., M. A. Pfaller, J. N. Galgiani, M. S. Bartlett, A. Espinel-Ingroff, M. A. Ghannoum, M. Lancaster, F. C. Odds, M. G. Rinaldi, T. J. Walsh, and A. L. Barry for the Subcommittee on Antifungal Susceptibility Testing of the National Committee for Clinical Laboratory Standards. 1997. Development of interpretive breakpoints for antifungal susceptibility testing: conceptual framework and analysis of in vitro-in vivo correlation data for fluconazole, itraconazole, and Candida infections. Clin. Infect. Dis. 24:235-247.[Medline]
    18. 18
  18. Rowen, J. L., and J. M. Tate. 1998. Management of neonatal candidiasis. Neonatal Candidiasis Study Group. Pediatr. Infect. Dis. J. 17:1007-1011.[CrossRef][Medline]
    19. 19
  19. Saiman, L., E. Ludington, M. Pfaller, S. Rangel-Frausto, R. T. Wiblin, J. Dawson, H. M. Blumberg, J. E. Patterson, M. Rinaldi, J. E. Edwards, R. P. Wenzel, W. Jarvis, et al. 2000. Risk factors for candidemia in neonatal intensive care unit patients. Pediatr. Infect. Dis. J. 19:319-324.[CrossRef][Medline]
    20. 20
  20. Sheehan, D. J., C. A. Hitchcock, and C. M. Sibley. 1999. Current and emerging azole antifungal agents. Clin. Microbiol. Rev. 12:40-79.[Abstract/Free Full Text]
    21. 21
  21. Waggoner-Fountain, L. A., M. W. Walker, R. J. Hollis, M. A. Pfaller, J. E. Ferguson II, R. P. Wenzel, and L. G. Donowitz. 1996. Vertical and horizontal transmission of unique Candida species to premature newborns. Clin. Infect. Dis. 22:803-808.[Medline]
    22. 22
  22. Warren, N. G., and K. C. Hazen. 1999. Candida, Cryptococcus, and other yeasts of medical importance, p. 1184-1199. In P. R. Murray, E. J. Baron, M. A. Pfaller, F. C. Tenover, and R. H. Yolken (ed.), Manual of clinical microbiology, 7th ed. ASM Press, Washington, D.C.

Journal of Clinical Microbiology, March 2002, p. 852-856, Vol. 40, No. 3
0095-1137/02/$04.00+0     DOI: 10.1128/JCM.40.3.852-856.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Arana, D. M., Nombela, C., Pla, J. (2009). Fluconazole at subinhibitory concentrations induces the oxidative- and nitrosative-responsive genes TRR1, GRE2 and YHB1, and enhances the resistance of Candida albicans to phagocytes. J Antimicrob Chemother 0: dkp407v1-dkp407 [Abstract] [Full Text]  
  • Silva, A. P., Miranda, I. M., Lisboa, C., Pina-Vaz, C., Rodrigues, A. G. (2009). Prevalence, Distribution, and Antifungal Susceptibility Profiles of Candida parapsilosis, C. orthopsilosis, and C. metapsilosis in a Tertiary Care Hospital. J. Clin. Microbiol. 47: 2392-2397 [Abstract] [Full Text]  
  • Sheppard, D. C., Locas, M.-C., Restieri, C., Laverdiere, M. (2008). Utility of the Germ Tube Test for Direct Identification of Candida albicans from Positive Blood Culture Bottles. J. Clin. Microbiol. 46: 3508-3509 [Abstract] [Full Text]  
  • Dalle, F., Lafon, I., L'Ollivier, C., Ferrant, E., Sicard, P., Labruere, C., Jebrane, A., Laubriet, A., Vagner, O., Caillot, D., Bonnin, A. (2008). A prospective analysis of the genotypic diversity and dynamics of the Candida albicans colonizing flora in neutropenic patients with de novo acute leukemia. haematol 93: 581-587 [Abstract] [Full Text]  
  • Pfaller, M. A., Messer, S. A., Boyken, L., Tendolkar, S., Hollis, R. J., Diekema, D. J. (2008). Selection of a Surrogate Agent (Fluconazole or Voriconazole) for Initial Susceptibility Testing of Posaconazole against Candida spp.: Results from a Global Antifungal Surveillance Program. J. Clin. Microbiol. 46: 551-559 [Abstract] [Full Text]  
  • Shepard, J. R., Addison, R. M., Alexander, B. D., Della-Latta, P., Gherna, M., Haase, G., Hall, G., Johnson, J. K., Merz, W. G., Peltroche-Llacsahuanga, H., Stender, H., Venezia, R. A., Wilson, D., Procop, G. W., Wu, F., Fiandaca, M. J. (2008). Multicenter Evaluation of the Candida albicans/Candida glabrata Peptide Nucleic Acid Fluorescent In Situ Hybridization Method for Simultaneous Dual-Color Identification of C. albicans and C. glabrata Directly from Blood Culture Bottles. J. Clin. Microbiol. 46: 50-55 [Abstract] [Full Text]  
  • Chauhan, N., Kruppa, M., Calderone, R. (2007). The Ssk1p Response Regulator and Chk1p Histidine Kinase Mutants of Candida albicans Are Hypersensitive to Fluconazole and Voriconazole. Antimicrob. Agents Chemother. 51: 3747-3751 [Abstract] [Full Text]  
  • Zepelin, M. B.-v., Kunz, L., Ruchel, R., Reichard, U., Weig, M., Gross, U. (2007). Epidemiology and antifungal susceptibilities of Candida spp. to six antifungal agents: results from a surveillance study on fungaemia in Germany from July 2004 to August 2005. J Antimicrob Chemother 60: 424-428 [Abstract] [Full Text]  
  • Odds, F. C., Hanson, M. F., Davidson, A. D., Jacobsen, M. D., Wright, P., Whyte, J. A., Gow, N. A. R., Jones, B. L. (2007). One year prospective survey of Candida bloodstream infections in Scotland. J Med Microbiol 56: 1066-1075 [Abstract] [Full Text]  
  • Reboli, A. C., Rotstein, C., Pappas, P. G., Chapman, S. W., Kett, D. H., Kumar, D., Betts, R., Wible, M., Goldstein, B. P., Schranz, J., Krause, D. S., Walsh, T. J., the Anidulafungin Study Group, (2007). Anidulafungin versus Fluconazole for Invasive Candidiasis. NEJM 356: 2472-2482 [Abstract] [Full Text]  
  • Wise, M. G., Healy, M., Reece, K., Smith, R., Walton, D., Dutch, W., Renwick, A., Huong, J., Young, S., Tarrand, J., Kontoyiannis, D. P. (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 [Abstract] [Full Text]  
  • Seifert, H., Aurbach, U., Stefanik, D., Cornely, O. (2007). In Vitro Activities of Isavuconazole and Other Antifungal Agents against Candida Bloodstream Isolates. Antimicrob. Agents Chemother. 51: 1818-1821 [Abstract] [Full Text]  
  • Davis, S. L, Vazquez, J. A, McKinnon, P. S (2007). Epidemiology, Risk Factors, and Outcomes of Candida albicans Versus Non-albicans Candidemia in Nonneutropenic Patients. The Annals of Pharmacotherapy 41: 568-573 [Abstract] [Full Text]  
  • Li, L., Redding, S., Dongari-Bagtzoglou, A. (2007). Candida glabrata, an Emerging Oral Opportunistic Pathogen. JDR 86: 204-215 [Abstract] [Full Text]  
  • Barchiesi, F., Spreghini, E., Tomassetti, S., Giannini, D., Scalise, G. (2007). Caspofungin in Combination with Amphotericin B against Candida parapsilosis. Antimicrob. Agents Chemother. 51: 941-945 [Abstract] [Full Text]  
  • Pfaller, M. A., Diekema, D. J. (2007). Epidemiology of Invasive Candidiasis: a Persistent Public Health Problem. Clin. Microbiol. Rev. 20: 133-163 [Abstract] [Full Text]  
  • Girmenia, C., Pizzarelli, G., Cristini, F., Barchiesi, F., Spreghini, E., Scalise, G., Martino, P. (2006). Candida guilliermondii Fungemia in Patients with Hematologic Malignancies.. J. Clin. Microbiol. 44: 2458-2464 [Abstract] [Full Text]  
  • Bopp, L. H., Baltch, A. L., Ritz, W. J., Michelsen, P. B., Smith, R. P. (2006). Antifungal effect of voriconazole on intracellular Candida glabrata, Candida krusei and Candida parapsilosis in human monocyte-derived macrophages.. J Med Microbiol 55: 865-870 [Abstract] [Full Text]  
  • Sandven, P., Bevanger, L., Digranes, A., Haukland, H. H., Mannsaker, T., Gaustad, P., the Norwegian Yeast Study Group, (2006). Candidemia in norway (1991 to 2003): results from a nationwide study.. J. Clin. Microbiol. 44: 1977-1981 [Abstract] [Full Text]  
  • Pfaller, M. A., Diekema, D. J., Sheehan, D. J. (2006). Interpretive Breakpoints for Fluconazole and Candida Revisited: a Blueprint for the Future of Antifungal Susceptibility Testing. Clin. Microbiol. Rev. 19: 435-447 [Abstract] [Full Text]  
  • Zaoutis, T. E., Heydon, K., Chu, J. H., Walsh, T. J., Steinbach, W. J. (2006). Epidemiology, Outcomes, and Costs of Invasive Aspergillosis in Immunocompromised Children in the United States, 2000. Pediatrics 117: e711-e716 [Abstract] [Full Text]  
  • Chamilos, G., Lewis, R. E., Kontoyiannis, D. P. (2006). Inhibition of Candida parapsilosis Mitochondrial Respiratory Pathways Enhances Susceptibility to Caspofungin. Antimicrob. Agents Chemother. 50: 744-747 [Abstract] [Full Text]  
  • Golan, Y., Wolf, M. P., Pauker, S. G., Wong, J. B., Hadley, S. (2005). Empirical Anti-Candida Therapy among Selected Patients in the Intensive Care Unit: A Cost-Effectiveness Analysis. ANN INTERN MED 143: 857-869 [Abstract] [Full Text]  
  • Lin, M. Y., Carmeli, Y., Zumsteg, J., Flores, E. L., Tolentino, J., Sreeramoju, P., Weber, S. G. (2005). Prior Antimicrobial Therapy and Risk for Hospital-Acquired Candida glabrata and Candida krusei Fungemia: a Case-Case-Control Study. Antimicrob. Agents Chemother. 49: 4555-4560 [Abstract] [Full Text]  
  • Arendrup, M. C., Fuursted, K., Gahrn-Hansen, B., Jensen, I. M., Knudsen, J. D., Lundgren, B., Schonheyder, H. C., Tvede, M. (2005). Seminational Surveillance of Fungemia in Denmark: Notably High Rates of Fungemia and Numbers of Isolates with Reduced Azole Susceptibility. J. Clin. Microbiol. 43: 4434-4440 [Abstract] [Full Text]  
  • Foulet, F., Nicolas, N., Eloy, O., Botterel, F., Gantier, J.-C., Costa, J.-M., Bretagne, S. (2005). Microsatellite Marker Analysis as a Typing System for Candida glabrata. J. Clin. Microbiol. 43: 4574-4579 [Abstract] [Full Text]  
  • Oliveira, E. R., Fothergill, A. W., Kirkpatrick, W. R., Coco, B. J., Patterson, T. F., Redding, S. W. (2005). In Vitro Interaction of Posaconazole and Caspofungin against Clinical Isolates of Candida glabrata. Antimicrob. Agents Chemother. 49: 3544-3545 [Abstract] [Full Text]  
  • Brun, S., Dalle, F., Saulnier, P., Renier, G., Bonnin, A., Chabasse, D., Bouchara, J.-P. (2005). Biological consequences of petite mutations in Candida glabrata. J Antimicrob Chemother 56: 307-314 [Abstract] [Full Text]  
  • Klevay, M., Ebinger, A., Diekema, D., Messer, S., Hollis, R., Pfaller, M. (2005). Disk Diffusion Testing Using Candida sp. Colonies Taken Directly from CHROMagar Candida Medium May Decrease Time Required To Obtain Results. J. Clin. Microbiol. 43: 3497-3499 [Abstract] [Full Text]  
  • Logue, M. E., Wong, S., Wolfe, K. H., Butler, G. (2005). A Genome Sequence Survey Shows that the Pathogenic Yeast Candida parapsilosis Has a Defective MTLa1 Allele at Its Mating Type Locus. Eukaryot Cell 4: 1009-1017 [Abstract] [Full Text]  
  • Sanguinetti, M., Posteraro, B., Fiori, B., Ranno, S., Torelli, R., Fadda, G. (2005). Mechanisms of Azole Resistance in Clinical Isolates of Candida glabrata Collected during a Hospital Survey of Antifungal Resistance. Antimicrob. Agents Chemother. 49: 668-679 [Abstract] [Full Text]  
  • Moudgal, V., Little, T., Boikov, D., Vazquez, J. A. (2005). Multiechinocandin- and Multiazole-Resistant Candida parapsilosis Isolates Serially Obtained during Therapy for Prosthetic Valve Endocarditis. Antimicrob. Agents Chemother. 49: 767-769 [Abstract] [Full Text]  
  • Cuenca-Estrella, M., Rodriguez, D., Almirante, B., Morgan, J., Planes, A. M., Almela, M., Mensa, J., Sanchez, F., Ayats, J., Gimenez, M., Salvado, M., Warnock, D. W., Pahissa, A., Rodriguez-Tudela, J. L., on behalf of the Barcelona Candidemia Project Stud, (2005). In vitro susceptibilities of bloodstream isolates of Candida species to six antifungal agents: results from a population-based active surveillance programme, Barcelona, Spain, 2002-2003. J Antimicrob Chemother 55: 194-199 [Abstract] [Full Text]  
  • Kaufman, D., Fairchild, K. D. (2004). Clinical Microbiology of Bacterial and Fungal Sepsis in Very-Low-Birth-Weight Infants. Clin. Microbiol. Rev. 17: 638-680 [Abstract] [Full Text]  
  • Canton, E., Peman, J., Gobernado, M., Viudes, A., Espinel-Ingroff, A. (2004). Patterns of Amphotericin B Killing Kinetics against Seven Candida Species. Antimicrob. Agents Chemother. 48: 2477-2482 [Abstract] [Full Text]  
  • Kaur, R., Castano, I., Cormack, B. P. (2004). Functional Genomic Analysis of Fluconazole Susceptibility in the Pathogenic Yeast Candida glabrata: Roles of Calcium Signaling and Mitochondria. Antimicrob. Agents Chemother. 48: 1600-1613 [Abstract] [Full Text]  
  • Hajjeh, R. A., Sofair, A. N., Harrison, L. H., Lyon, G. M., Arthington-Skaggs, B. A., Mirza, S. A., Phelan, M., Morgan, J., Lee-Yang, W., Ciblak, M. A., Benjamin, L. E., Thomson Sanza, L., Huie, S., Yeo, S. F., Brandt, M. E., Warnock, D. W. (2004). Incidence of Bloodstream Infections Due to Candida Species and In Vitro Susceptibilities of Isolates Collected from 1998 to 2000 in a Population-Based Active Surveillance Program. J. Clin. Microbiol. 42: 1519-1527 [Abstract] [Full Text]  
  • Espinel-Ingroff, A., Pfaller, M., Messer, S. A., Knapp, C. C., Holliday, N., Killian, S. B. (2004). Multicenter Comparison of the Sensititre YeastOne Colorimetric Antifungal Panel with the NCCLS M27-A2 Reference Method for Testing New Antifungal Agents against Clinical Isolates of Candida spp.. J. Clin. Microbiol. 42: 718-721 [Abstract] [Full Text]  
  • Takakura, S., Fujihara, N., Saito, T., Kudo, T., Iinuma, Y., Ichiyama, S., the Japan Invasive Mycosis Surveillance Study Grou, (2004). National surveillance of species distribution in blood isolates of Candida species in Japan and their susceptibility to six antifungal agents including voriconazole and micafungin. J Antimicrob Chemother 53: 283-289 [Abstract] [Full Text]  
  • Hirasawa, M., Takada, K. (2004). Multiple effects of green tea catechin on the antifungal activity of antimycotics against Candida albicans. J Antimicrob Chemother 53: 225-229 [Abstract] [Full Text]  
  • Selvarangan, R., Bui, U., Limaye, A. P., Cookson, B. T. (2003). Rapid Identification of Commonly Encountered Candida Species Directly from Blood Culture Bottles. J. Clin. Microbiol. 41: 5660-5664 [Abstract] [Full Text]  
  • Michalopoulos, A. S., Geroulanos, S., Mentzelopoulos, S. D. (2003). Determinants of Candidemia and Candidemia-Related Death in Cardiothoracic ICU Patients. Chest 124: 2244-2255 [Abstract] [Full Text]  
  • Himmelreich, U., Somorjai, R. L., Dolenko, B., Lee, O. C., Daniel, H.-M., Murray, R., Mountford, C. E., Sorrell, T. C. (2003). Rapid Identification of Candida Species by Using Nuclear Magnetic Resonance Spectroscopy and a Statistical Classification Strategy. Appl. Environ. Microbiol. 69: 4566-4574 [Abstract] [Full Text]  
  • Holland, J, Young, M L, Lee, O, C-A Chen, S (2003). Vulvovaginal carriage of yeasts other than Candida albicans. Sex. Transm. Infect. 79: 249-250 [Abstract] [Full Text]  
  • Pfaller, M. A., Messer, S. A., Boyken, L., Tendolkar, S., Hollis, R. J., Diekema, D. J. (2003). Variation in Susceptibility of Bloodstream Isolates of Candida glabrata to Fluconazole According to Patient Age and Geographic Location. J. Clin. Microbiol. 41: 2176-2179 [Abstract] [Full Text]  
  • Pujol, C., Messer, S. A., Pfaller, M., Soll, D. R. (2003). Drug Resistance Is Not Directly Affected by Mating Type Locus Zygosity in Candida albicans. Antimicrob. Agents Chemother. 47: 1207-1212 [Abstract] [Full Text]  
  • Brown, A. L., Greig, J. R., Kartsonis, N. A., Perfect, J., Walsh, T. J. (2003). Caspofungin versus Amphotericin B for Invasive Candidiasis. NEJM 348: 1287-1288 [Full Text]  
  • Lott, T. J., Fundyga, R. E., Brandt, M. E., Harrison, L. H., Sofair, A. N., Hajjeh, R. A., Warnock, D. W. (2003). Stability of Allelic Frequencies and Distributions of Candida albicans Microsatellite Loci from U.S. Population-Based Surveillance Isolates. J. Clin. Microbiol. 41: 1316-1321 [Abstract] [Full Text]  
  • Kicklighter, S. D. (2002). Antifungal Agents and Fungal Prophylaxis in the Neonate. NeoReviews 3: e249-255 [Full Text]  
  • Pfaller, M. A., Diekema, D. J. (2002). Role of Sentinel Surveillance of Candidemia: Trends in Species Distribution and Antifungal Susceptibility. J. Clin. Microbiol. 40: 3551-3557 [Full Text]  
  • Arthington-Skaggs, B. A., Lee-Yang, W., Ciblak, M. A., Frade, J. P., Brandt, M. E., Hajjeh, R. A., Harrison, L. H., Sofair, A. N., Warnock, a. D. W. (2002). Comparison of Visual and Spectrophotometric Methods of Broth Microdilution MIC End Point Determination and Evaluation of a Sterol Quantitation Method for In Vitro Susceptibility Testing of Fluconazole and Itraconazole against Trailing and Nontrailing Candida Isolates. Antimicrob. Agents Chemother. 46: 2477-2481 [Abstract] [Full Text]  

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Pfaller, M. A.
Right arrow Articles by Hollis, R. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Pfaller, M. A.
Right arrow Articles by Hollis, R. J.

Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»