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Inicio Revista Iberoamericana de Micología Epidemiology of candidaemia and invasive candidiasis. A changing face
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Vol. 31. Núm. 1.
Páginas 42-48 (enero - marzo 2014)
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11833
Vol. 31. Núm. 1.
Páginas 42-48 (enero - marzo 2014)
Mycologic Forum
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Epidemiology of candidaemia and invasive candidiasis. A changing face
Epidemiología de la candidemia y la candidiasis invasiva. Un rostro en continuo cambio
Visitas
11833
Guillermo Quindós
Departamento de Inmunología, Microbiología y Parasitología, UFI11/25 (Microbios y Salud), Facultad de Medicina y Odontología, Universidad del País Vasco/Euskal Herriko Unibertsitatea, Bilbao, Spain
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Table 1. Selected population-based epidemiological studies on candidaemia and invasive candidiasis.
Table 2. Selected epidemiological studies on candidaemia and invasive candidiasis.
Table 3. Distribution of the five most frequent species of Candida on selected epidemiological studies on candidaemia and invasive candidiasis.
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Abstract

Invasive candidiasis is a leading cause of mortality. Candidaemia is the most common clinical presentation of invasive candidiasis but more that 30% of these infections do not yield positive blood cultures. Candida albicans remains the predominant aetiology, accounting for 50% of all cases. However, there has been an epidemiological shift in the last decades. Some species of Candida different to C. albicans have emerged as an important cause of severe candidaemia as they can exhibit resistance to fluconazole and other antifungal agents. Moreover, there is a different distribution of non C. albicans Candida species in relationship to patients’ and hospital characteristics. Thus, Candida parapsilosis has been associated to candidaemia in neonates and young adults. This species usually has an exogenously origin and contaminates medical devices, causing central venous catheter-associated candidaemias. Candida glabrata, Candida tropicalis and Candida krusei are isolated in blood cultures from older patients (>65 years) with important risk factors, such as major abdominal surgery, solid tumours and haematologic malignancies, transplants, and/or prolonged treatment with corticoids. Moreover, important geographical differences in the distribution of the Candida species different to C. albicans causing invasive candidiasis have been reported: C. parapsilosis predominates in Australia, Latin America and Mediterranean countries of Africa, Asia and Europe. In contrast, C. glabrata has an important aetiological role in USA and Central and Northern Europe. Finally, an important and worrying issue is that mortality due to invasive candidiasis remains unacceptably high.

This manuscript is part of the series of works presented at the “V International Workshop: Molecular genetic approaches to the study of human pathogenic fungi” (Oaxaca, Mexico, 2012).

Keywords:
Candidaemia
Invasive candidiasis
Epidemiology
Candida albicans
Candida parapsilosis
Candida tropicalis
Candida krusei
Resumen

La candidiasis invasiva es una causa destacada de mortalidad. Su presentación más habitual es la candidemia peroen más de un 30% de las candidiasis invasivas, los hemocultivos son negativos. Candida albicans continúa siendo el patógeno etiológico más frecuente de las candidiasis invasivas y alrededor del 50% de todos los aislamientos de hemocultivos corresponden a esta especie. Sin embargo, en las últimas décadas, se está observando un cambio epidemiológico, con un incremento notable de especies de Candida diferentes de C. albicans. Además, las candidemias causadas por esta última especie pueden ser más graves porque muchas de ellas son resistentes a fluconazol y otros fármacos antimicóticos. La distribución de las candidemias causadas por especies de Candida diferentes de C. albicans difiere según la población de pacientes estudiados y las características del hospital. Así, Candida parapsilosis causa candidemias en recién nacidos y adultos jóvenes. Esta especie suele tener un origen exógeno y contamina instrumental y diferentes dispositivos médicos, por lo que induce candidemia asociada a catéteres. Candida glabrata, Candida tropicalis y Candida krusei se aíslan de hemocultivos de pacientes de mayor edad (>65 años) con importantes factores de riesgo subyacentes, como cirugía abdominal, tumores sólidos y neoplasias hematológicas, trasplantes o tratamientos prolongados con corticoesteroides. También se han descrito diferencias geográficas importantes en la distribución de las especies de Candida diferentes de C. albicans causantes de candidiasis invasiva: C. parapsilosis predomina en Australia, América Latina y los países de la cuenca mediterránea de África, Asia y Europa. Por el contrario, C. glabrata desempeña un sustancial papel etiológico en los Estados Unidos y en los países nórdicos y de Europa central. Por último, un aspecto muy importante y preocupante es que la mortalidad atribuida a la candidiasis invasiva sigue siendo inaceptablemente alta.

Este manuscrito forma parte de la serie de artículos presentados en el «V International Workshop: Molecular genetic approaches to the study of human pathogenic fungi» (Oaxaca, México, 2012).

Palabras clave:
Candidemia
Candidiasis invasive
Epidemiología
Candida albicans
Candida parapsilosis
Candida tropicalis
Candida krusei
Texto completo

Invasive candidiasis is a severe infection that causes high morbidity and mortality. Candidaemia is the commonest presentation of invasive candidiasis, but it represents less than 75% of all invasive candidiasis. These invasive mycoses are mainly hospital-acquired infections and approximately two-thirds of them have their origin in different hospital wards. In recent years, community invasive candidiasis is raising in association to an increase of at home healthcare.21,66 Hajjeh et al.29 observed in a population-based study that 36% of candidaemia occurred in the Intensive Care Unit (ICU), and a third of them were of community onset. Wenzel and Edmond65 estimated that 5% of the patients admitted to tertiary hospitals will be affected by a nosocomial infection; a 10% of them will suffer from bloodstream infections (BSI), being 8–10% of these BSI caused by Candida. Since the 1980s, Candida is the fourth most common cause of BSI in USA and Europe, accounting for >85% of all fungaemias.56,61

Most studies have reported a steady increase in the rate of invasive candidiasis until 1990 that was remarkably consistent until 2003 (from 8 to 10 cases per 100,000 inhabitants). The current incidence of invasive candidiasis has remained similar in the last years or even has decreased slightly in Australia, Canada, Europe and USA. However, incidence is continuously growing in Latin America and the rest of the world (Tables 1 and 2). The incidence of candidaemia in Australia, Canada, Europe, and Latin America is significantly lower than in the USA. Incidences of 6–10 per 100,000 inhabitants have been reported in most population-based studies in the USA.21,22,30 In contrast, most European surveys show incidences of 1.4–5.7 per 100,000 inhabitants.3,7,8,46,63 However, there are two notable exceptions: Denmark and, most recently, Spain, where the incidence of invasive candidiasis is higher than in other European countries.1,4–6 Most Nordic countries have reported candidaemia in the range of 1.4–5.7 per 100,000 inhabitants, with more than 70% of them caused by Candida albicans.7,8,53,54,59 Candidaemia rates in Australia (1.8 invasive candidiasis per 100,000) and Canada (2.9 per 100,000) are similar to European ones.13,33

Table 1.

Selected population-based epidemiological studies on candidaemia and invasive candidiasis.

Location  Year  Incidence (no. of cases/100,000 inhabitants/year)References 
    Total  Children <1 year old  Patients ≥65 years old   
America
Canada  1999–2004  2.9  20  21.3  33 
USA  1992–1993  70 (Black: 165 vs. white 41)  26 (Black: 40 vs. white 10)  30 
USA  1998–2001      22 
USA  1998–2000  10 (7–24)  Black: 157 vs. white: 33  Black (92) vs. white (30)  29 
Europe
Denmark  2004–2006  10.4  16.3  36.9  6 
Denmark  2004–2009  8.6  11.3  27.7  4 
Finland  1995–1999  1.9  9.4  5.2  54 
Finland  2004–2007  2.86  6.9  12.2  53 
Iceland  1980–1989  1.4    12.7  7 
Iceland  1990–1999  4.9  11.3  19.3  7 
Iceland  2000–2011  5.7  20.7  18.1  8 
Norway  1991–2003  2.4  10.3  59 
Spain  2002–2003  4.3  38.8  12  3 
Spain  2010–2011  8.14  96.4  25  1 
Scotland (UK)  2005–2006  4.8    55.9  46 
Oceania
Australia  2001–2004  1.8  24.8  13.7  13 
Table 2.

Selected epidemiological studies on candidaemia and invasive candidiasis.

Location  Year  Incidence (no. of cases/1000 admissions/year)  References 
America
Argentina  2005–2008  1.15 (0.35–2.65)  38 
Brazil  1997–2007  0.74 (0.41–1.21)  58 
Brazil  2006–2010  0.54 (0.41–0.71)  16 
International  2010  1.18 (0.33–1.96)  44 
USA  1998–2000  0.15  29 
Asia
China  1998–2007  0.026  67 
Taiwan  2000–2010  0.351  32 
Europe
Austria  2001–2006  0.27–0.77  55 
Denmark  2004–2006  0.51  6 
Denmark  2004–2009  0.41  4 
England (UK)  2005–2008  0.11  20 
Germany  1998–2008  0.47  64 
Iceland  1980–1989  0.15  7 
Iceland  1990–1999  0.55  7 
International  1997–1999  0.20–0.38  62 
Scotland (UK)  2005–2008  0.59  46 
Spain  2002–2003  0.53  3 
Spain  2008–2009  1.09  14 
Spain  2010  0.92  47 
Spain  2010–2011  0.90  1 
Oceania
Australia  2001–2004  0.21  13 
Australia  1999–2008  0.45  52 

Although the epidemiology of candidaemia in Latin America has not been studied so deeply, a recent prospective laboratory-based survey in 22 hospitals from 8 Latin American countries showed an incidence of 0.98 episodes per 1000 hospital admissions. In spite of being broad variations among countries (0.33 in Chile versus 1.96 episodes per 1000 hospital admissions in Argentina and Colombia), the mean incidence was higher than those reported in USA (0.28–0.96 episodes per 1000 hospital admissions) or Europe (0.2–0.38 episodes per 1000 hospital admissions).44,45 There is not a clear reason of these higher rates of invasive candidiasis in Latin America, USA, Denmark or Spain, but the different rates of sampling, distribution of risk factors in the populations studied, the age distribution, or in the study methodologies, can contribute.1,6,33

Of interest, the highest incidences of invasive candidiasis occur in males (60%), at age extremes (infants <1 year and adults >65 years’ old: circa 16 episodes and circa 36 episodes per 100,000 inhabitants, respectively), in cancer (71 episodes per 100,000), and diabetic patients (28 episodes per 100,000).1–3,29,30 Cancer is a very frequent underlying disease in patients suffering from candidaemia but there are differences among cancer patients. In those patients with haematological malignancies, chemotherapy and the consequent neutropaenia, digestive tract mucositis and treatment with corticoids are added risk factors for invasive candidiasis. By comparison, in patients with solid tumours, candidaemia is associated to complications of surgery, ICU admission, mechanical ventilation, hyperalimentation and presence of central venous catheters.10 These rates are particularly high in surgical, trauma and burn units, and neonatal ICUs. A recent SENTRY study reported a total of 1752 Candida isolates distributed nearly equal from invasive ICU and non-ICU settings. The frequency of ICU-associated candidaemia was also higher in Latin America (56.5%) compared with Europe (44.4%) and USA (39.6%).50,56,66

Role of different species of Candida in the aetiology of candidaemia

During the past decades, most hospitals have reported an important and progressive shift in the aetiology of invasive candidiasis in different groups of patients and distinct hospital settings. Nevertheless, C. albicans remains the predominant species in most studies, with incidences ranging from 11.5% in Turkey or 32% in Mexico and Taiwan to more than 60% in Austria and Sweden (Table 3). The reasons of this shift are not completely understood but several factors have been associated with candidaemia depending on the implicated species. In the 2008–2009 SENTRY study including Candida isolates from 79 medical centres, approximately 90–95% of isolates belonged to five species: C. albicans, Candida glabrata, Candida parapsilosis, Candida tropicalis and Candida krusei.50 However, the distribution of C. albicans and non-C. albicans Candida species causing candidaemia vary enormously between hospitals and patients with a significant increase in those invasive candidiasis caused by Candida different to C. albicans.15,16,28,36,37,63 An interesting feature of the latter is a patient-specificity and a particular geographical distribution (Fig. 1 and Table 3). Moreover, other important feature of some Candida different to C. albicans, such as C. glabrata and C. krusei, is their lower susceptibility to fluconazole and other antifungal agents.3,4,36,41,42,49–52 These characteristics can complicate the therapeutic approach of candidaemia caused by these Candida species. The attributable mortality rate of candidaemia is estimated to be >30%, with a crude mortality rate of >50%. This mortality exceeds widely the one reported for most bacterial infections. Since 1989, a 50% reduction in mortality rates for invasive candidiasis has been reported, following a steady increase in mortality in the previous decades reaching 0.62 deaths per 100,000 persons. A similar decline in rates of death from invasive candidiasis associated with HIV infection occurred (0.04 per 100,000). The explanation for decreased mortality in both HIV infected and non-infected patients could be related to the increased awareness, earlier diagnosis, and the enhanced therapy of candidaemias. Furthermore, candidaemia not only increases patient mortality, but also extends the length of stay and increases the total cost of medical care. Patient outcomes appear to be worst for candidaemia due to Candida different to C. albicans, mainly caused by C. glabrata and C. tropicalis, and to a lesser extent C. krusei. However, infections due to C. parapsilosis tend to be associated with reduced lethality (23%).1,41,42

Table 3.

Distribution of the five most frequent species of Candida on selected epidemiological studies on candidaemia and invasive candidiasis.

Location  Year  No. of isolates  Species (%)References 
      CA  CP  CT  CG  CK   
Africa
South Africa  1990  –  62  –  23  –  0.6  31 
South Africa  2005–2007  –  46  25  –  23  0.6  31 
America
Argentina  2005–2008  683  41.3  24.3  19.9  6.3  0.6  38 
Argentina  2007–2008  461  38.4  26  15.4  4.3  0.4  17 
Brazil  1997–2007  151  44  22  15  58 
Brazil  2006–2007  300  34  26  24  16 
Brazil  2006–2010  313  44  14.4  21.7  11.2  3.5  43 
Brazila  2006–2010  117  31  23  23  10 
Brazil2  2006–2010  248  41  15  20  12  10 
Canada  1999–2004  209  51.1  6.2  5.7  21.5  4.8  33 
Colombia  2001–2007  921  44.7  13.6  13.6  1.7  2.1  19 
Mexico  2004–2007  398  31.9  37.9  14.8  2.7  26 
Internationalc  2010  303  37.6  26.1  14.2  3.3  60 
International  2010  672  37.6  22.5  17.6  6.3  2.7  44 
USA  1998–2000  1143  45  13  12  24  29 
USA  2004–2007  108  47  12  29  21 
USA  2001–2009  453  50  13  11  22  27 
Asia
China  1998–2007  102  57.8  10.8  12.8  10.8  67 
Israel  2006–2007  444  44.4  16.6  17.1  15.3  3.1  9 
Taiwan  2000–2010  2856  50  13.2  19.3  16.1  1.4  32 
Taiwan  2001–2010  154  32  12  46  13 
Thailand  2006–2009  147  39  28  22  –  11 
Turkey  2010–2011  39  11.5  22.2  5.9  1.78  2.1  23 
Europe
Austria  2001–2006  283  70  8.1  4.9  13.8  55 
Denmark  2004–2006  1133  59.8  4.6  20.5  4.1  6 
Denmark  2004–2009  2820  57.1  3.7  4.8  21.1  4.1  4 
England (UK)  2005–2008  106  43  20  31  2.5  20 
Finland  1995–1999  479  70  54 
Germany  1998–2008  35  45.7  17.1  5.7  14.3  64 
Iceland  1980–1999  172  64.4  9.6  5.6  12.4  7 
Iceland  2000–2011  222  56  13  16  8 
Scotland (UK)  2005–2006  300  52  11.7  22.7  46 
Spain  2002–2003  345  51  23  10  3 
Spain  1990–2003  555  42.3  36.3  4.4  9.7  40 
Spain  2008–2009  984  49.1  20.7  10.7  13.6  2.1  14 
Spain  2009  1377  43  29  10  8.5  47 
Spain  2009  752  46  26  11  1 
Sweden  2005–2006  403  60.8  8.9  20.1  1.2  24 
Oceania
Australia  2001–2004  1068  47.3  19.9  5.1  15.4  4.3  13 
Australia  1999–2008  1137  45.4  26.9  5.2  13.4  2.8  52 

Candidaemia in patients with haematological malignancies1 or solid tumours2. 3Candidaemia in children from 8 Latin American countries. CA=Candida albicans, CP=Candida parapsilosis, CT=Candida tropicalis, CG=Candida glabrata, and CK=Candida krusei.

Fig. 1.

Distribution of most frequently species of Candida other than Candida albicans (in the case of Candida dubliniensis the areas represent those places reporting more than 2% of blood isolates corresponding to this species).

(0,26MB).

C. parapsilosis is acquired from an exogenous source and is primarily isolated from cancer patients, and young adults and neonates in ICUs, usually in association to colonisation of central venous catheters and parenteral nutrition. This species predominates in candidaemias reported from Australia, Latin America and the Mediterranean countries of Africa, Asia and Europe. C. parapsilosis is usually susceptible to most antifungal agents, but there are reports of clinical isolates with decreased susceptibility to azoles and echinocandins.1–3,10–16,23–26,38,40,43–48,52,60

C. glabrata and C. krusei are associated with recent major abdominal surgery, solid tumours, old patients (>65 years), neutropaenic neonates, transplant recipients, and patients treated with corticoids.1,10,45,48,60C. glabrata predominates as second cause of candidaemia in USA and the countries of the North and Centre of Europe.4–8,20,55 The proportion of C. glabrata has remained constant worldwide at 9–12% but C. glabrata is more common in USA (21.1%) than in the rest of the world (7.6–12.6%).15,47–49 Some authors have linked institutional or individual fluconazole use to the selection of C. glabrata, especially in cancer centres.28,35,51,56,57 In a recent SENTRY study, including 79 medical centres and a total of 1752 Candida isolates, C. glabrata was the only species in which resistance to azoles and echinocandins was reported.50 Of interest, candidaemia due to C. glabrata and C. krusei is relatively low in Latin America, and the fluconazole resistance rates of clinical isolates of C. glabrata are lower (10–13%) than in USA (18–20%).44,45 However, in Brazil a significant increase of C. glabrata blood isolates from the 1995–2003 period to the 2005–2007 period was observed, mainly in hospitals with higher use of fluconazole in the treatment of invasive candidiasis.15 In Northern European countries, C. dubliniensis, a species close-related to C. albicans, can exceed 2–3% of blood isolates.4,8,46 Finally, C. tropicalis has been isolated from patients with solid tumours or haematologic diseases and it has been reported as the second etiological agent of invasive candidiasis in Asia and some parts of Latin America (Colombia and Brazil). The overrepresentation of C. tropicalis candidaemia in patients aged >70 years can be related to the increased frequency of solid tumours and haematologic malignancies in the elderly population.32,34,43,67 Multi-fungal infections do not exceed 5% of candidaemias, being C. albicans the species most frequently isolated in combination with other yeasts, with C. glabrata and C. tropicalis accounting for the majority of episodes.6

Two of these emerging species, C. parapsilosis and C. glabrata are in fact complexes of species with special clinical and demographic characteristics.12,18,40C. parapsilosis includes 3 different species: Candida parapsilosis sensu stricto, Candida metapsilosis and Candida orthopsilosis, but the real importance of C. orthopsilosis and C. metapsilosis as human pathogens remains unknown. In a recent Spanish nationwide study, the incidence of episodes of candidaemia due to C. parapsilosis and C. orthopsilosis were 0.22 and 0.02 per 1000 admissions, respectively. C. orthopsilosis was the fifth most frequently isolated species, preceding C. krusei (0.018 episodes per 1000 admissions).47,48 The prevalence of C. orthopsilosis is apparently higher in warmer Mediterranean countries than in the cooler countries of the Atlantic, Central and North Europe. A higher prevalence of C. orthopsilosis has also been reported in countries with hot and humid climates, such as Taiwan (8.5%), Brazil (9.1%) and Malaysia (24.4%). However, other factors could be responsible for local specificities, such as differences in hospital services (presence or absence of ICU or surgical wards) and the patient population (transplant recipients and other immunodeficient patients).40C. glabrata complex includes C. glabrata sensu stricto and two newly described species, Candida bracarensis and Candida nivariensis.18,39 Lockhart et al.37, in their analysis of 1598 C. glabrata isolates from 29 countries, observed that C. bracarensis and C. nivariensis isolates constituted a very small percentage (0.2%) of the C. glabrata clinical isolates. However, these cryptic species could be more prevalent in specific regions. Most reports have underlined the lower susceptibility of C. bracarensis and C. nivariensis to the most commonly used azoles.

Conclusions

Invasive candidiasis is a leading cause of mortality worldwide. C. albicans remains the predominant cause of candidaemia and invasive candidiasis, accounting for 50% of all cases. However, an evident shift has been reported in the epidemiology, as some Candida species different to C. albicans have emerged as cause of candidaemia and can exhibit resistance to fluconazole and other triazoles, echinocandins and/or amphotericin B. C. parapsilosis is associated to infections in neonates and young adults, usually related to the presence of central venous catheter and hyperalimentation. C. glabrata, C. tropicalis and C. krusei cause infections in older patients in association to recent major abdominal surgery, solid tumours, transplants, and/or prolonged treatment with corticoids. Moreover, there are some important geographical differences in the distribution of those Candida species different to C. albicans causing invasive candidiasis. C. parapsilosis is the first or second aetiology of candidaemia in Australia, Latin America and Mediterranean countries of Africa, Asia and Europe. Conversely, C. glabrata has an important aetiological role in USA and Central and Northern Europe. Finally, an important and worrying issue is that mortality due to invasive candidiasis remains unacceptably high.

Conflict of interest

In the past 5 years, GQA has received grant support from Astellas Pharma, Gilead Sciences, Pfizer, Schering Plough and Merck Sharp and Dohme. He has been an advisor/consultant to Merck Sharp and Dohme, and has been paid for talks on behalf of Astellas Pharma, Esteve Hospital, Gilead Sciences, Merck Sharp and Dohme, Pfizer, and Schering Plough.

Acknowledgements

GQA has received grant support from Consejería de Educación, Universidades e Investigación (GIC12 210-IT-696-13) and Departamento de Industria, Comercio y Turismo (S-PR12UN002, S-PR11UN003) of Gobierno Vasco-Eusko Jaurlaritza, Fondo de Investigación Sanitaria (FIS PI11/00203), and Universidad del País Vasco-Euskal Herriko Unibertsitatea (UFI 11/25, UPV/EHU).

References
[1]
B. Almirante, Proyecto CandiPop.
Estudio multicéntrico nacional sobre candidemia: presentación de estudios clínicos.
IV Jornada científica del Grupo de Estudio de Micología Médica de la SEIMC,
[2]
B. Almirante, D. Rodríguez, M. Cuenca-Estrella, M. Almela, F. Sanchez, J. Ayats, et al.
Epidemiology, risk factors, and prognosis of Candida parapsilosis bloodstream infections: case-control population-based surveillance study of patients in Barcelona, Spain, from 2002 to 2003.
J Clin Microbiol, 44 (2006), pp. 1681-1685
[3]
B. Almirante, D. Rodríguez, B.J. Park, M. Cuenca-Estrella, A.M. Planes, M. Almela, et al.
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, 43 (2005), pp. 1829-1835
[4]
M.C. Arendrup, B. Bruun, J.J. Christensen, K. Fuursted, H.K. Johansen, P. Kjaeldgaard, et al.
National surveillance of fungemia in Denmark (2004 to 2009).
J Clin Microbiol, 49 (2011), pp. 325-334
[5]
M.C. Arendrup, K. Fuursted, B. Gahrn-Hansen, I.M. Jensen, J.D. Knudsen, B. Lundgren, et al.
Seminational surveillance of fungemia in Denmark: notably high rates of fungemia and numbers of isolates with reduced azole susceptibility.
J Clin Microbiol, 43 (2005), pp. 4434-4440
[6]
M.C. Arendrup, K. Fuursted, B. Gahrn-Hansen, H.C. Schønheyder, J.D. Knudsen, I.M. Jensen, et al.
Semi-national surveillance of fungaemia in Denmark 2004-2006: increasing incidence of fungaemia and numbers of isolates with reduced azole susceptibility.
Clin Microbiol Infect, 14 (2008), pp. 487-494
[7]
L.R. Asmundsdóttir, H. Erlendsdóttir, M. Gottfredsson.
Increasing incidence of candidemia: results from a 20-year nationwide study in Iceland.
J Clin Microbiol, 40 (2002), pp. 3489-3492
[8]
L.R. Asmundsdottir, H. Erlendsdottir, M. Gottfredsson.
Nationwide study of candidemia, antifungal use and antifungal drug resistance in Iceland, 2000–2011.
J Clin Microbiol, 51 (2013), pp. 841-848
[9]
R. Ben-Ami, G. Rahav, H. Elinav, I. Kassis, I. Shalit, T. Gottesman, et al.
Distribution of fluconazole-resistant Candida bloodstream isolates among hospitals and in patient services in Israel.
Clin Microbiol Infect, 19 (2013), pp. 752-756
[10]
M.D. Bergamasco, M. Garnica, A.L. Colombo, M. Nucci.
Epidemiology of candidemia in patients with hematologic malignancies and solid tumours in Brazil.
Mycoses, 56 (2013), pp. 256-263
[11]
A. Boonyasiri, J. Jearanaisilavong, S. Assanasen.
Candidemia in Siriraj Hospital: epidemiology and factors associated with mortality.
J Med Assoc Thai, 96 (2013), pp. S91-S97
[12]
E. Cantón, J. Pemán, G. Quindós, E. Eraso, I. Miranda-Zapico, M. Álvarez, et al.
Prospective multicenter study of the epidemiology, molecular identification, and antifungal susceptibility of Candida parapsilosis, Candida orthopsilosis, and Candida metapsilosis isolated from patients with candidemia.
Antimicrob Agents Chemother, 55 (2011), pp. 5590-5596
[13]
S. Chen, M. Slavin, Q. Nguyen, D. Marriott, E.G. Playford, D. Ellis, et al.
Active surveillance for candidemia.
Australia Emerg Infect Dis, 12 (2006), pp. 1508-1516
[14]
R. Cisterna, G. Ezpeleta, O. Telleria, Spanish Candidemia Surveillance Group.
Nationwide sentinel surveillance of bloodstream Candida infections in 40 tertiary care hospitals in Spain.
J Clin Microbiol, 48 (2010), pp. 4200-4206
[15]
A.L. Colombo, M. Garnica, L.F. Aranha Camargo, C.A. Da Cunha, A.C. Bandeira, D. Borghi, et al.
Candida glabrata: an emerging pathogen in Brazilian tertiary care hospitals.
[16]
A.L. Colombo, M. Nucci, B.J. Park, S.A. Nouér, B. Arthington-Skaggs, D.A. da Matta, et al.
Epidemiology of candidemia in Brazil: a nationwide sentinel surveillance of candidemia in eleven medical centers.
J Clin Microbiol, 44 (2006), pp. 2816-2823
[17]
S. Córdoba, W. Vivot, M.E. Bosco-Borgeat, C. Taverna, W. Szusz, O. Murisengo, et al.
Species distribution and susceptibility profile of yeasts isolated from blood cultures: results of a multicenter active laboratory-based surveillance study in Argentina.
Rev Argent Microbiol, 43 (2011), pp. 176-185
[18]
A. Correia, P. Sampaio, S. James, C. Pais.
Candida bracarensis sp. nov., a novel anamorphic yeast species phenotypically similar to Candida glabrata.
Int J Syst Evol Microbiol, 56 (2006), pp. 313-317
[19]
J.A. Cortés, P. Reyes, C. Gómez, G. Buitrago, A.L. Leal, GREBO.
Fungal bloodstream infections in tertiary care hospitals in Colombia.
Rev Iberoam Micol, 28 (2011), pp. 74-78
[20]
I. Das, P. Nightingale, M. Patel, P. Jumaa.
Epidemiology, clinical characteristics, and outcome of candidemia: experience in a tertiary referral center in the UK.
Int J Infect Dis, 15 (2011), pp. e759-e763
[21]
D. Diekema, S. Arbefeville, L. Boyken, J. Kroeger, M. Pfaller.
The changing epidemiology of healthcare-associated candidemia over three decades.
Diagn Microbiol Infect Dis, 73 (2012), pp. 45-48
[22]
D.J. Diekema, S.A. Messer, A.B. Brueggemann, S.L. Coffman, G.V. Doern, L.A. Herwaldt, et al.
Epidemiology of candidemia: 3-year results from the emerging infections and the epidemiology of Iowa organisms study.
J Clin Microbiol, 40 (2002), pp. 1298-1302
[23]
G. Ece, P. Samlioglu, G. Akkoclu, S. Atalay, S. Kose.
The evaluation of the distribution of yeast like fungi ‘Candida Species’ at a tertiary care center in western Turkey.
Int J Med Sci, 9 (2012), pp. 617-620
[24]
J. Ericsson, E. Chryssanthou, L. Klingspor, A.G. Johansson, P. Ljungman, E. Svensson, et al.
Candidaemia in Sweden: a nationwide prospective observational survey.
Clin Microbiol Infect, 19 (2013), pp. E218-E221
[25]
G.N. Forrest, E. Weekes, J.K. Johnson.
Increasing incidence of Candida parapsilosis candidemia with caspofungin usage.
J Infect, 56 (2008), pp. 126-129
[26]
G.M. González, M. Elizondo, J. Ayala.
Trends in species distribution and susceptibility of bloodstream isolates of Candida collected in Monterrey Mexico, to seven antifungal agents: results of a 3-year (2004 to 2007) surveillance study.
J Clin Microbiol, 46 (2008), pp. 2902-2905
[27]
S.A. Grim, K. Berger, C. Teng, S. Gupta, J.E. Layden, W.M. Janda, et al.
Timing of susceptibility-based antifungal drug administration in patients with Candida bloodstream infection: correlation with outcomes.
J Antimicrob Chemother, 67 (2012), pp. 707-714
[28]
R. Hachem, H. Hanna, D. Kontoyiannis, Y. Jiang, I. Raad.
The changing epidemiology of invasive candidiasis: Candida glabrata and Candida krusei as the leading causes of candidemia in hematologic malignancy.
Cancer, 112 (2008), pp. 2493-2499
[29]
R.A. Hajjeh, A.N. Sofair, L.H. Harrison, G.M. Lyon, B.A. Arthington-Skaggs, S.A. Mirza, et al.
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 (2004), pp. 1519-1527
[30]
A.S. Kao, M.E. Brandt, W.R. Pruitt, L.A. Conn, B.A. Perkins, D.S. Stephens, et al.
The epidemiology of candidemia in two United States cities: results of a population-based active surveillance.
Clin Infect Dis, 29 (1999), pp. 1164-1170
[31]
A. Kreusch, A.S. Karstaedt.
Candidemia among adults in Soweto South Africa, 1990–2007.
Int J Infect Dis, 17 (2013), pp. e621-e623
[32]
C.C. Lai, C.C. Chu, C.Y. Wang, H.Y. Tsai, A. Cheng, Y.C. Lee, et al.
Association between incidence of candidaemia and consumption of antifungal agents at a medical centre in Taiwan.
Int J Antimicrob Agents, 40 (2012), pp. 349-353
[33]
K.B. Laupland, D.B. Gregson, D.L. Church, T. Ross, S. Elsayed.
Invasive Candida species infections: a 5 year population-based assessment.
J Antimicrob Chemother, 56 (2005), pp. 532-537
[34]
A.Y. Leung, C.S. Chim, P.L. Ho, V.C. Cheng, K.Y. Yuen, A.K. Lie, et al.
Candida tropicalis fungaemia in adult patients with haematological malignancies: clinical features and risk factors.
J Hosp Infect, 50 (2002), pp. 316-319
[35]
M.Y. Lin, Y. Carmeli, J. Zumsteg, E.L. Flores, J. Tolentino, P. Sreeramoju, et al.
Prior antimicrobial therapy and risk for hospital-acquired Candida glabrata and Candida krusei fungemia: a case-case control study.
Antimicrob Agents Chemother, 49 (2005), pp. 4555-4560
[36]
S.R. Lockhart, N. Iqbal, A.A. Cleveland, M.M. Farley, L.H. Harrison, C.B. Bolden, et al.
Species identification and antifungal susceptibility testing of Candida bloodstream isolates from population-based surveillance studies in two U.S. cities from 2008 to 2011.
J Clin Microbiol, 50 (2012), pp. 3435-3442
[37]
S.R. Lockhart, S.A. Messer, M. Gherna, J.A. Bishop, W.G. Merz, M.A. Pfaller, et al.
Identification of Candida nivariensis and Candida bracarensis in a large global collection of Candida glabrata isolates: comparison to the literature.
J Clin Microbiol, 47 (2009), pp. 1216-1217
[38]
L. López Moral, I.N. Tiraboschi, M. Schijman, M. Bianchi, L. Guelfand, S. Cataldi, et al.
Fungemias en hospitales de la Ciudad de Buenos Aires.
Rev Iberoam Micol, 29 (2012), pp. 144-149
[39]
L.M. López-Soria, E. Bereciartua, M. Santamaría, L.M. Soria, J.L. Hernández-Almaraz, A. Mularoni, et al.
First case report of catheter-related fungemia by Candida nivariensis in the Iberian Peninsula.
Rev Iberoam Micol, 30 (2013), pp. 69-71
[40]
I. Miranda-Zapico, E. Eraso, J.L. Hernández-Almaraz, L.M. López-Soria, A.J. Carrillo-Muñoz, J.M. Hernández-Molina, et al.
Prevalence and antifungal susceptibility patterns of new cryptic species inside the species complexes Candida parapsilosis and Candida glabrata among blood isolates from a Spanish tertiary hospital.
J Antimicrob Chemother, 66 (2011), pp. 2315-2322
[41]
C. Moran, C.A. Grussemeyer, J.R. Spalding, D.K. Benjamin Jr., S.D. Reed.
Candida albicans and non-albicans bloodstream infections in adult and pediatric patients: comparison of mortality and costs.
Pediatr Infect Dis J, 28 (2009), pp. 433-435
[42]
C. Moran, C.A. Grussemeyer, J.R. Spalding, D.K. Benjamin Jr., S.D. Reed.
Comparison of costs, length of stay, and mortality associated with Candida glabrata and Candida albicans bloodstream infections.
Am J Infect Control, 38 (2010), pp. 78-80
[43]
M.L. Moretti, P. Trabasso, L. Lyra, R. Fagnani, M.R. Resende, L.G. de Oliveira Cardoso, et al.
Is the incidence of candidemia caused by Candida glabrata increasing in Brazil? Five-year surveillance of Candida bloodstream infection in a university reference hospital in southeast Brazil.
Med Mycol, 51 (2013), pp. 225-230
[44]
M. Nucci, F. Queiroz-Telles, T. Alvarado-Matute, I.N. Tiraboschi, J. Cortes, J. Zurita, et al.
Epidemiology of candidemia in Latin America: a laboratory-based survey.
[45]
M. Nucci, L. Thompson-Moya, M. Guzmán-Blanco, N. Tiraboschi, J.A. Cortés, J. Echevarria, et al.
Recommendations for the management of candidemia in adults in Latin America.
Rev Iberoam Micol, 30 (2013), pp. 179-188
[46]
F.C. Odds, M.F. Hanson, A.D. Davidson, M.D. Jacobsen, P. Wright, J.A. Whyte, et al.
One year prospective survey of Candida bloodstream infections in Scotland.
J Med Microbiol, 56 (2007), pp. 1066-1075
[47]
J. Pemán, E. Cantón, J.J. Miñana, J.A. Florez, J. Echeverria, D.N. Ortega, et al.
Changes in the epidemiology of fungaemia and fluconazole susceptibility of blood isolates during the last 10 years in Spain: results from the FUNGEMYCA study.
Rev Iberoam Micol, 28 (2011), pp. 91-99
[48]
J. Pemán, E. Cantón, G. Quindós, E. Eraso, J. Alcoba, J. Guinea, et al.
Epidemiology, species distribution and in vitro antifungal susceptibility of fungaemia in a Spanish multicentre prospective survey.
J Antimicrob Chemother, 67 (2012), pp. 1181-1187
[49]
M.A. Pfaller, D.J. Diekema, D.L. Gibbs, V.A. Newell, R. Barton, H. Bijie, et al.
Geographic variation in the frequency of isolation and fluconazole and voriconazole susceptibilities of Candida glabrata: an assessment from the ARTEMIS DISK Global Antifungal Surveillance Program.
Diagn Microbiol Infect Dis, 67 (2010), pp. 162-171
[50]
M.A. Pfaller, G.J. Moet, S.A. Messer, R.N. Jones, M. Castanheira.
Candida bloodstream infections: comparison of species distributions and antifungal resistance patterns in community-onset and nosocomial isolates in the SENTRY Antimicrobial Surveillance Program, 2008–2009.
Antimicrob Agents Chemother, 55 (2011), pp. 561-566
[51]
E.G. Playford, D. Marriott, Q. Nguyen, S. Chen, D. Ellis, M. Slavin, et al.
Candidemia in nonneutropenic critically ill patients: risk factors for non-albicans Candida spp..
Crit Care Med, 36 (2008), pp. 2034-2039
[52]
E.G. Playford, G.R. Nimmo, M. Tilse, T.C. Sorrell.
Increasing incidence of candidaemia: long-term epidemiological trends, Queensland Australia, 1999–2008.
J Hosp Infect, 76 (2010), pp. 46-51
[53]
E. Poikonen, O. Lyytikäinen, V.J. Anttila, I. Koivula, J. Lumio, P. Kotilainen, et al.
Secular trend in candidemia and the use of fluconazole in Finland, 2004–2007.
BMC Infect Dis, 10 (2010), pp. 312
[54]
E. Poikonen, O. Lyytikäinen, V.J. Anttila, P. Ruutu.
Candidemia in Finland, 1995–1999.
Emerg Infect Dis, 9 (2003), pp. 985-990
[55]
E. Presterl, F. Daxböck, W. Graninger, B. Willinger.
Changing pattern of candidaemia 2001–2006 and use of antifungal therapy at the University Hospital of Vienna, Austria.
Clin Microbiol Infect, 13 (2007), pp. 1072-1076
[56]
G. Quindós.
Candidemias y candidiasis invasivas nosocomiales.
Med Clin (Barc), 134 (2010), pp. 17-19
[57]
G. Quindós, L.O. Sánchez-Vargas, M. Villar-Vidal, E. Eraso, M. Alkorta, J.L. Hernández-Almaraz.
Activities of fluconazole and voriconazole against bloodstream isolates of Candida glabrata and Candida krusei: a 14-year study in a Spanish tertiary medical centre.
Int J Antimicrob Agents, 31 (2008), pp. 266-271
[58]
T.Z. Sampaio-Camargo, A.R. Marra, C.V. Silva, M.F. Cardoso, M.D. Martino, L.F. Camargo, et al.
Secular trends of candidemia in a tertiary care hospital.
Am J Infect Control, 38 (2010), pp. 546-551
[59]
P. Sandven, L. Bevanger, A. Digranes, H.H. Haukland, T. Mannsåker, P. Gaustad, et al.
Candidemia in Norway (1991 to 2003): results from a nationwide study.
J Clin Microbiol, 44 (2006), pp. 1977-1981
[60]
M.E. Santolaya, F. de Queiroz Telles, T. Alvarado Matute, A.L. Colombo, J. Zurita, N. Tiraboschi, et al.
Recommendations for the management of candidemia in neonates in Latin America.
Rev Iberoam Micol, 30 (2013), pp. 158-170
[61]
A.M. Tortorano, C. Kibbler, J. Peman, H. Bernhardt, L. Klingspor, R. Grillot.
Candidaemia in Europe: epidemiology and resistance.
Int J Antimicrob Agents, 27 (2006), pp. 359-366
[62]
A.M. Tortorano, J. Peman, H. Bernhardt, L. Klingspor, C.C. Kibbler, O. Faure, et al.
Epidemiology of candidaemia in Europe: results of 28-month European Confederation of Medical Mycology (ECMM) hospital-based surveillance study.
Eur J Clin Microbiol Infect Dis, 23 (2004), pp. 317-322
[63]
A.M. Tortorano, A. Prigitano, E. Biraghi, M.A. Viviani, FIMUA-ECMM Candidaemia Study Group.
The European Confederation of Medical Mycology (ECMM) survey of candidaemia in Italy: in vitro susceptibility of 375 Candida albicans isolates and biofilm production.
J Antimicrob Chemother, 56 (2005), pp. 777-779
[64]
A. Tragiannidis, W. Fegeler, G. Rellensmann, V. Debus, V. Müller, I. Hoernig-Franz, et al.
Candidaemia in a European Paediatric University Hospital: a 10-year observational study.
Clin Microbiol Infect, 18 (2012), pp. E27-E30
[65]
R.P. Wenzel, M.B. Edmond.
The impact of hospital-acquired bloodstream infections.
Emerg Infect Dis, 7 (2001), pp. 174-177
[66]
R.P. Wenzel, C. Gennings.
Bloodstream infections due to Candida species in the intensive care unit: identifying especially high-risk patients to determine prevention strategies.
Clin Infect Dis, 41 (2005), pp. S389-S393
[67]
J.Q. Wu, L.P. Zhu, X.T. Ou, B. Xu, X.P. Hu, X. Wang, et al.
Epidemiology and risk factors for non-Candida albicans candidemia in non-neutropenic patients at a Chinese teaching hospital.
Med Mycol, 49 (2011), pp. 552-555
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