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Journal of Clinical Microbiology, September 2001, p. 3254-3259, Vol. 39, No. 9
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.9.3254-3259.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Departments of Pathology1 and Medicine,2 University of Iowa College of Medicine, Iowa City, Iowa; Universidade Federal de Sao Paulo/EPM Sao Paulo, Brazil3; and University Hospital Utrecht, Utrecht, The Netherlands4
Received 20 November 2000/Returned for modification 19 April 2001/Accepted 29 May 2001
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ABSTRACT |
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Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
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A surveillance program (SENTRY) of bloodstream infections (BSI) in
the United States, Canada, Latin America, and Europe from 1997 through
1999 detected 1,184 episodes of candidemia in 71 medical centers (32 in
the United States, 23 in Europe, 9 in Latin America, and 7 in Canada).
Overall, 55% of the yeast BSIs were due to Candida
albicans, followed by Candida glabrata and
Candida parapsilosis (15%), Candida tropicalis
(9%), and miscellaneous Candida spp. (6%). In the United
States, 45% of candidemias were due to non-C. albicans
species. C. glabrata (21%) was the most common
non-C. albicans species in the United States, and the
proportion of non-C. albicans BSIs was highest in
Latin America (55%). C. albicans accounted for 60% of BSI
in Canada and 58% in Europe. C. parapsilosis
was the most common non-C. albicans species in Latin
America (25%), Canada (16%), and Europe (17%). Isolates of
C. albicans, C. parapsilosis, and C. tropicalis
were all highly susceptible to fluconazole (97 to 100% at 
8
µg/ml). Likewise, 97 to 100% of these species were inhibited by 1
µg/ml of ravuconazole (concentration at which 50% were
inhibited [MIC50], 0.007 to 0.03 µg/ml) or
voriconazole (MIC50, 0.007 to 0.06 µg/ml). Both ravuconazole and voriconazole were significantly more
active than fluconazole against C. glabrata
(MIC90s of 0.5 to 1.0 µg/ml versus 16 to 32 µg/ml,
respectively). A trend of increased
susceptibility of C. glabrata to fluconazole was noted
over the three-year period. The percentage of C. glabrata
isolates susceptible to fluconazole increased from 48% in
1997 to 84% in 1999, and MIC50s decreased from 16 to 4 µg/ml. A similar trend was documented in both the Americas (57 to
84% susceptible) and Europe (22 to 80% susceptible). Some
geographic differences in susceptibility to triazole were observed with
Canadian isolates generally more susceptible than isolates from
the United States and Europe. These observations suggest
susceptibility patterns and trends among yeast isolates from BSI and
raise additional questions that can be answered only by
continued surveillance and clinical investigations of the type reported
here (SENTRY Program).
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INTRODUCTION |
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Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
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It is now well accepted that antimicrobial resistance is an important concern with respect to virtually all major groups of pathogenic microorganisms, including viruses, bacteria, parasites, and fungi. Numerous approaches to control this ever-increasing problem have been suggested (2, 10, 27, 30). One critical component in every suggested mode of intervention is the need for continued monitoring or surveillance of resistance on a global scale. Surveillance of antibacterial resistance is now being conducted by several different groups with the common goal of providing accurate data for use in the development of empiric treatment recommendations, for the development of guidelines and policies for appropriate antimicrobial utilization, for assessing the progress and effectiveness of various intervention efforts, and for tailoring or improving antimicrobial susceptibility testing (AST) methods and resistance screening (2, 10, 13).
Although innate or acquired resistance to available antifungal agents is now recognized among pathogenic fungi, particularly the Candida species, the true extent of the resistance problem among fungi causing hematogenously disseminated or bloodstream infections (BSI) is largely unknown. Among the several active antimicrobial resistance surveillance programs now in existence, the SENTRY Antimicrobial Surveillance Program is the only system that monitors BSI due to Candida spp. as well as bacterial species (5, 6, 13, 22). The SENTRY Program is comprehensive, longitudinal, and global in scope and utilizes a central laboratory concept to monitor trends in microbial spectra and resistance in 74 sentinel sites in 22 nations.
Since 1997, one of the important objectives of the SENTRY Program has been the study of the frequency of occurrence and antifungal resistance among species of Candida causing BSI in the United States, Canada, Latin America, and Europe (5, 16, 21, 22). The rank order of occurrence and resistance profiles of the various species of Candida causing BSI is important in establishing empiric treatment protocols and in judging the potential impact of newer antifungal agents. Using this approach, a number of important and unusual resistance phenotypes have been detected over the three-year period from 1997 to 1999 (5, 16, 21, 22). Examples that will be discussed herein include Candida glabrata isolates resistant to amphotericin B, Candida krusei isolates resistant to amphotericin B, fluconazole, and 5-fluorocytosine (5FC), cross-resistance to established and investigational triazoles, and decreased resistance to fluconazole among C. glabrata isolates and to itraconazole among Candida tropicalis isolates. Species differences occurring among different geographic regions have also been noted.
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MATERIALS AND METHODS |
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Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
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Study design. The SENTRY Program was established in 1997 to monitor the predominant pathogens and antimicrobial resistance patterns of nosocomial and community-acquired infections via a broad network of sentinel hospitals categorized by geographic location and size (5, 16, 21, 22). The present report focuses on BSI due to Candida spp. from U.S., Canadian, Latin American, and European sites. BSI due to Candida spp. were reported from 32 monitored medical centers in the United States, 23 in Europe, 9 in Latin America, and 7 in Canada over the three-year period from January 1997 through December 1999.
Each participant hospital contributed results (organism identification, date of isolation, and hospital location) for consecutive blood culture isolates (one isolate per patient) of Candida spp. judged to be clinically significant by local criteria, detected in each calendar month during the study period. All isolates were stored on agar slants and sent on a regular basis to the University of Iowa College of Medicine (Iowa City) for storage and further characterization by reference identification and susceptibility testing (14, 29).Organism identification. All fungal blood culture isolates were identified at the participating institutions by the routine method in use at each laboratory. Upon receipt at the University of Iowa, 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 (29). Isolates were stored as suspensions in water or on agar slants at an 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 NCCLS (14). Susceptibility of isolates to amphotericin B was determined using Etest (AB BIODISK, Sonia, Sweden) and RPMI 1640 agar with 2% glucose (Remel, Lenexa, Kans.) as described previously (17). Standard powders of fluconazole (Pfizer, Inc., New York, N.Y.), voriconazole (Pfizer), ravuconazole (Bristol-Myers Squibb, Wallingford, Conn.), itraconazole (Janssen, Beerse, Belgium), and 5-fluorocytosine (5FC; Sigma, St. Louis, Mo.) were obtained from their respective manufacturers. Following incubation at 35°C for 48 h, the MICs of fluconazole, voriconazole, ravuconazole, itraconazole, and 5FC were read as the lowest concentration at which a prominent decrease in turbidity relative to the growth control well was observed (14). Amphotericin B MICs determined by Etest were read after 48 h of incubation at 35°C and were determined to be at 100% inhibition of growth where the border of the elliptical inhibition zone intercepted the scale on the strip edge (17). Quality control (QC) was ensured by testing the NCCLS (14)-recommended strains, Candida krusei ATCC 6258 and Candida parapsilosis ATCC 22019.
Interpretive criteria for susceptibility to fluconazole (susceptibility breakpoint, MIC of8 µg/ml), itraconazole (susceptible, MIC
of 0.12 µg/ml), and 5FC (susceptible, MIC of 4 µg/ml) were those published by Rex et al. (23) and the NCCLS
(14). These breakpoints apply to all Candida
spp. (including C. glabrata) with the exception of
C. krusei, which is considered inherently resistant to
fluconazole regardless of the MIC obtained (14). Interpretive criteria have not yet been defined for amphotericin B;
however, because the study of Nguyen et al. (15) suggested that amphotericin B MICs of >1 µg/ml may indicate clinically
resistant isolates of Candida spp., we determined the
percentage of isolates inhibited by 1 µg/ml to be susceptible in
this surveillance study. Likewise, the investigational triazoles,
voriconazole and ravuconazole, have not been assigned interpretive
breakpoints. For purposes of comparison and because preliminary
pharmacokinetic data indicate that achievable serum levels for these
agents may range from 2 to 6 µg/ml depending on the dosing regimen
(26), we have employed a susceptibility breakpoint of 1
µg/ml for both voriconazole and ravuconazole.
Statistical analysis. Comparison of species distribution and/or MIC distribution by other factors (e.g., year, geographic region) were made using the chi-square test with Yates' correction for categorical variables and the Wilcoxon rank sum test for ordinal variables (MICs). All reported P values are two-tailed.
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RESULTS AND DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
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During the 36-month study period, a total of 1,184 BSI isolates (episodes) of Candida spp. were submitted by 71 study centers in the United States (32 centers, 589 isolates), Canada (7 centers, 161 isolates), Latin America (9 centers, 132 isolates), and Europe (23 centers, 302 isolates). These isolates accounted for 3% of all BSI isolates (bacterial and fungal) from nosocomial and community-acquired infections and 9% of nosocomial BSI (bacterial and fungal) isolates submitted by SENTRY participants from 1997 to 1999. Candida spp. was the fourth-most-common nosocomial BSI isolate category, preceded only by Staphylococcus aureus, coagulase-negative staphylococci, and enterococci (data not shown). The original identification assigned by the participating center was confirmed for 97% of the isolates submitted. Among the 1,184 BSI, 75% were nosocomial (detected more than 48 h after admission to a hospital), and 50% occurred in patients hospitalized in an intensive care unit (ICU).
The frequencies of BSI due to the various species of Candida
in each country over the three-year period are presented in Table 1. Of the 1,184 yeast BSI whose organisms
were identified, 55% were due to C. albicans,
15% were due to C. glabrata, 15% were due to
C. parapsilosis, 9% were due to C. tropicalis, and 6% were due to miscellaneous Candida
spp. The rank order of the various species differed according to
geographic location. C. albicans was the predominant
species in all four geographic areas, accounting for 45 to 60% of all
BSI. C. glabrata was the second-most-common species in
the United States (21% of BSI; P 0.01 compared to prevalence in other geographic areas) but ranked either third or fourth
in the other areas. In contrast to the case in the United States,
C. glabrata was very uncommon in Latin America (6% of all isolates; P 0.001 compared to U.S. results).
C. parapsilosis was the second-most-common
Candida species, causing BSI in Latin America (25%;
P 0.001 compared to U.S. results), Canada (16%), and Europe (19%; P 0.001 compared to U.S. results).
C. krusei was encountered infrequently (1 to 2%) in
all geographic areas.
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The rank order of species in all four geographic areas was relatively
stable over the three-year period. However, the overall rank order may
not represent the situation in individual medical centers. The
percentages of candidemias due to C. albicans varied considerably among the individual participating study sites (Table 2). C. albicans was
clearly the predominating species in certain medical centers,
accounting for 
70% of candidemias in Turkey-3 (73%), France-3
(73%), Italy-2 (88%), Switzerland (80%), Turkey-2 (74%), New Mexico (82%), New York-3 (70%), Texas-2 (83%),
Nova Scotia (71%), and Ontario (85%) (a numerical suffix
indicates a particular site within a state or country). In contrast,
C. albicans accounted for 40% of BSI in
Germany-1 (21%), Spain-2 (29%), Massachusetts (38%), New York-2
(37%), North Carolina (35%), and Brazil-1 (24%).
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These data demonstrate that although C. albicans may continue to play a dominant role as a cause of fungemia in many centers, it has been supplanted by C. glabrata in certain U.S. centers and by C. parapsilosis or C. tropicalis in some European and Latin American centers. The reasons for such dramatic differences in Candida species causing BSI remains speculative, although the emergence of C. glabrata in certain centers has been linked to utilization of fluconazole prophylaxis (1, 3), and infections attributable to C. parapsilosis are often associated with hyperalimentation and breaches of catheter care and of infection control practice (12, 18, 19, 22).
In vitro susceptibility results for the 1,184 isolates tested with
fluconazole, ravuconazole, and voriconazole are shown in Table
3. Fluconazole was active in all regions,
with 90 to 98% of isolates susceptible (S) to a drug concentration of
8 µg/ml. Isolates from Canada (concentration at which 90% of the
isolates are inhibited [MIC90], 4 µg/ml; 96% S) and
Latin America (MIC90, 4 µg/ml; 98% S) were more
susceptible than those from the United States (MIC90,
16; 90% S) and Europe (MIC90, 8 µg/m; 90% S) due to the presence of resistance (MIC, 64 µg/ml) among
C. glabrata isolates in the latter two regions. Both
ravuconazole (MIC90, 0.12 to 0.5 µg/m; 98 to 99% S) and
voriconazole (MIC90, 0.12 to 0.25 µg/ml; 98 to 99% S)
were considerably more potent than fluconazole against isolates from
all four geographic areas.
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Table 4 summarizes the in vitro
susceptibilities to fluconazole, ravuconazole, and voriconazole for the
individual species of Candida from all areas stratified by
year. Isolates of C. albicans, C. parapsilosis,
and C. tropicalis were all highly susceptible (97 to 100%) to fluconazole and the investigational
triazoles. Interestingly, C. glabrata
demonstrated a trend towards increased susceptibility to
fluconazole from 1997 (MIC50, 16 µg/ml; 48% S) to 1999 (MIC50, 4 µg/ml; 83% S; P = 0.004 for the trend). This trend was apparent in both the Americas
and Europe (data not shown). Reasons for this trend are unclear but may
be related to more appropriate uses and improved dosing of fluconazole
(3). Both ravuconazole and voriconazole were quite active
(MIC50, 0.12 to 0.5 µg/ml; 97 to 100% S) against both
C. glabrata and C. krusei. Notably, no
trend towards increased resistance to any of the agents tested was
observed over the three-year period.
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Although it is not shown in Table 4, C. tropicalis
demonstrated a trend towards increased susceptibility to itraconazole (susceptible MIC, 0.12 µg/ml) from 1997 (MIC50, 0.25 µg/ml; 48% S) to 1999 (MIC50, 0.06 µg/ml; 82% S;
P = 0.005). A similar shift was not observed with
itraconazole and any other species. More than 97% of C. tropicalis isolates were inhibited by 1 µg/ml of itraconazole.
This trend is similar to the shift observed with C. glabrata and fluconazole and bears watching.
Despite excellent activity against the vast majority of
Candida BSI isolates, cross-resistance was observed with
both ravuconazole and voriconazole when they were tested against 12 isolates of C. albicans that were resistant to both
fluconazole (MIC, 64 µg/ml) and itraconazole (MIC, 1 µg/ml)
(data not shown) (20). Such isolates are quite rare among
those organisms causing BSI but are indicative of the potential for
development of complete class resistance against the azoles if
fluconazole or itraconazole are misused.
Fluconazole was equally active against Candida BSI isolates
from patients hospitalized in the ICU (93% S) and the non-ICU (92% S)
setting (Table 5). This finding was in
contrast to that observed with bacterial BSI isolates, where
ICU-related infection isolates were generally less susceptible to
antimicrobial agents than non-ICU strains (5, 7, 9).
Similarly, no difference in susceptibility to six different antifungal
agents was noted between nosocomial and community-acquired BSI isolates
of Candida spp. Again, this observation was distinctly
different from the experience with bacterial BSI isolates, where
nosocomial strains were almost always more resistant to antimicrobial
agents than community-acquired strains (5). Notably, only
70 to 72% of Candida spp. were found to be susceptible to
amphotericin B at concentrations of 1 µg/ml when tested on RPMI
agar using Etest (17). The Etest method has been shown to
be the most sensitive and reliable method for identifying strains of
Candida with clinically significant resistance to
amphotericin B (4, 17, 28).
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Further examination of selected species susceptibility to amphotericin
B revealed striking differences when the isolates were tested on
RPMI agar using Etest (Table 6). As
has been noted previously, approximately 95% of C. albicans isolates were inhibited by 1 µg/ml of amphotericin B
compared to only 41% of C. glabrata isolates and 0%
of C. krusei isolates (P 0.01 for
comparison of susceptibility by species) (8, 11, 15, 17, 24,
25). This in vitro data is consistent with the clinical
experience of breakthrough fungemias with C. glabrata
and C. krusei despite treatment with amphotericin B at
standard doses of 0.5 to 0.6 mg/kg of body weight/day
(25). Current Infectious Diseases Society of America
(IDSA) treatment guidelines recommend higher doses of amphotericin B
(1 mg/kg/day) when treating C. glabrata and C. krusei fungemia (25). Thus, both
C. glabrata and C. krusei may be
relatively resistant to both azoles and polyenes and could pose
significant therapeutic problems in the future if such strains proliferate. C. krusei is also often resistant (70%)
to 5FC as well (20).
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Summary and conclusions. This most recent analysis of data from the SENTRY Antimicrobial Surveillance Program confirms the fact that Candida spp. remain the fourth-most-common cause of nosocomial BSI (7, 18). Although C. albicans continues to account for approximately one-half of candidemias world-wide, its frequency may vary widely from institution to institution, emphasizing the need for yeast species identification of BSI isolates in individual institutions. Different, and as yet unknown, factors may influence the species distribution of Candida spp. causing BSI. The prominence of C. glabrata in the United States as opposed to the other regions in the SENTRY Program may be influenced by extensive utilization of fluconazole at relatively low doses (<400 mg/day), enhancing selection of this species (3). In contrast, the frequent isolation of C. parapsilosis in other regions may reflect issues of suboptimal catheter care and infection control (1, 12).
Importantly, no increase in resistance to azoles was observed in any of the geographic regions over the three-year study period. The trend towards decreased resistance to fluconazole among C. glabrata isolates and to itraconazole among C. tropicalis isolates is interesting and will require further investigation to determine the factors behind these observations. Although there is some evidence in the literature that both C. glabrata and C. krusei may be relatively resistant to amphotericin B (15, 17, 24, 25), the application of the Etest to a large international collection of Candida spp., such as the SENTRY Program collection, provides information suggesting that elevated MICs of drugs for these species may be more common than anticipated. Additional data, not previously available, indicate that in contrast to the experience with antibacterial agents, no difference in susceptibility to the existing antifungal agents was observed among ICU versus non-ICU isolates and nosocomial versus community-acquired strains of Candida spp. This may reflect the fact that to the best of our knowledge Candida spp. lack mobile resistance genes and thus require considerably different circumstances and exposures in order to develop high levels of resistance compared to bacterial pathogens. Finally, although the new triazoles (ravuconazole and voriconazole) display improved potency compared to fluconazole, it is apparent that cross-resistance to these agents may be observed among the rare BSI isolates of Candida that are resistant to both fluconazole and itraconazole. These observations suggest certain susceptibility patterns and trends among yeast isolates from BSI and raise additional questions that can be answered only by continued surveillance and clinical investigations of the type reported here (SENTRY Program).| |
ACKNOWLEDGMENTS |
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Kay Meyer and Linda Elliott provided excellent support in the preparation of the manuscript.
The SENTRY Antimicrobial Surveillance Program was supported in part by a research grant from Bristol-Myers Squibb.
We express our appreciation to all SENTRY site participants. Participants contributing data isolates to the study included: The Medical Center of Delaware, Wilmington, Del. (L. Steele-Moore); Clarion Health Methodist Hospital, Indianapolis, Ind. (G. Denys); Henry Ford Hospital (C. Staley); Summa Health System, Akron, Ohio (J. R. Dipersio); Good Samaritan Regional Medical Center (M. Saubolle); Denver General Hospital, Denver, Colo. (M. L. Wilson); University of New Mexico Hospital, Albuquerque, N.M. (G. D. Overturf); University of Illinois at Chicago, Chicago, Ill. (P. C. Schreckenberger); University of Iowa Hospitals and Clinics, Iowa City, Iowa (R. N. Jones); Creighton University, Omaha, Nebr. (S. Cavalieri); Froedtert Memorial Lutheran Hospital-East, Milwaukee, Wisc. (S. Kehl); Boston VAMC, 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, Wash. (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, Tex. (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, Miss. (J. Humphries); Carolinas Medical Center, Charlotte, N.C. (S. Jenkins); University of Virginia Medical Center, Charlottesville, Va. (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 Investig. Biologicas, Medellin, Columbia (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, Cedex, 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, Sevilla, Spain (E. J. Perea); Hospital de Bellvitge, Barcelona, Spain (J. Linares); Hospital Ramon y Cajal, Madrid, Spain (R. Canton); Unite de Bacteriologie, Lausanne, Switzerland (F. Praplan); Hacettepe Universitaesi Tip Fakultesi, Ankara, Turkey (D. Gur); Universita degli Studi di Genova, Genova, Italy (E. Debbia); Azienda Policlinico Univ. 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 Lab, Warsaw, Poland (W. Hryniewicz); St. Thomas Hospital, London, United Kingdom (G. French); Univ. Libre de Bruxelles-Hopital Erasme, Brussels, Belgium (M. J. Struelens); Marmara Universitesi Tip Fakultesi, Istanbul, Turkey (V. Korten).
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FOOTNOTES |
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* 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.
Present address: Beaver Kreek Centre, Suite A, North Liberty, IA 52317.
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REFERENCES |
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Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
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