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  Table of Contents  
Year : 2020  |  Volume : 38  |  Issue : 1  |  Page : 110-116

Candidaemia in a tertiary care centre of developing country: Monitoring possible change in spectrum of agents and antifungal susceptibility

1 Department of Medical Microbiology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
2 Department of Paediatric Medicine, Postgraduate Institute of Medical Education and Research, Chandigarh, India
3 Department of Anaesthesiology and Intensive Care, Postgraduate Institute of Medical Education and Research, Chandigarh, India

Date of Submission18-Mar-2020
Date of Decision17-Jun-2020
Date of Acceptance24-Jun-2020
Date of Web Publication25-Jul-2020

Correspondence Address:
Prof. Shivaprakash M Rudramurthy
Department of Medical Microbiology, Postgraduate Institute of Medical Education and Research, Chandigarh - 160 012
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijmm.IJMM_20_112

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 ~ Abstract 

Purpose: Candidaemia is a major cause of morbidity and mortality of hospitalised patients, especially in developing countries. This study was conducted to monitor any change in species distribution and antifungal susceptibility pattern of Candida species causing candidaemia over the last 20 years. Materials and Methods: The candidaemia cases reported during January 1999 and December 2018 at our centre were reviewed. The yeasts were identified by phenotypic characters (during 1999–2014) and matrix-assisted laser desorption ionisation-time of flight mass spectrometry (MALDI-TOF MS) (during 2014–2018). Antifungal susceptibility testing (AFST) was performed in accordance with the Clinical and Laboratory Standards Institute guidelines. Results: A total of 602,963 blood samples from patients with suspected sepsis were processed. Candidaemia was diagnosed in 7927 (1.31%) cases. The frequency of cases rose significantly (P = 0.000) in the last quarter of the study. Candida tropicalis (40.1%) was the most common species, followed by Candida albicans (15.2%), Wickerhamomyces anomalus (13.1%), Candida krusei (6.6%), Candida parapsilosis (4.7%) and others. Rare species such as Candida auris, Candida lambica, Candida orthopsilosis, Candida vishwanathii were identified after the introduction of MALDI-TOF. The minimum inhibitory concentrations of amphotericin B rose significantly from the first to last quarter (0.5%–4.9%). Fluconazole resistance was fairly constant at 7.4%–8.8%. Conclusion: Local epidemiology of candidaemia at our centre was distinct regarding prevalence and change of spectrum of species. The identification of rare species was possible after the introduction of MALDI-TOF. With the emergence of multidrug-resistant C. auris and resistance in other species, routine AFST has become imperative.

Keywords: Antifungal resistance, candidaemia, epidemiology, India, matrix-assisted laser desorption ionisation-time of flight

How to cite this article:
Kaur H, Singh S, Rudramurthy SM, Ghosh AK, Jayashree M, Narayana Y, Ray P, Chakrabarti A. Candidaemia in a tertiary care centre of developing country: Monitoring possible change in spectrum of agents and antifungal susceptibility. Indian J Med Microbiol 2020;38:110-6

How to cite this URL:
Kaur H, Singh S, Rudramurthy SM, Ghosh AK, Jayashree M, Narayana Y, Ray P, Chakrabarti A. Candidaemia in a tertiary care centre of developing country: Monitoring possible change in spectrum of agents and antifungal susceptibility. Indian J Med Microbiol [serial online] 2020 [cited 2020 Aug 7];38:110-6. Available from:

 ~ Introduction Top

Candidaemia ranks top in the list of invasive fungal infections worldwide. The incidence of candidaemia has increased over the years due to advancements in medical interventions, expanding pool of elderly and susceptible population including transplant recipients and haematological malignancies; though a decline has also been observed in few centres with improved infection control and stewardship practices.[1],[2],[3] A noticeable shift of species causing candidaemia from Candida albicans to non-albicans Candida (NAC) (Candida glabrata in developed countries and Candida tropicalis and Candida parapsilosis in developing nations) with the recent emergence of Candida auris has also been reported.[4],[5] The incidence of candidaemia in developing countries is difficult to predict due to the limited number of studies. The estimate from limited studies indicates 4–15 times higher rate of candidaemia in developing countries than developed nations.[6] A multi-centre study on candidaemia of Indian ICUs reported distinct epidemiology and high antifungal resistance.[4] However, such multi-centre studies are rare and can not be compared without baseline data to denote any change in epidemiology over the years. Previous studies from our centre have shown the increasing frequency of NAC species causing candidaemia with a rise in fluconazole resistance.[7],[8],[9],[10] The aim of the present study was to monitor the trend of candidaemia in 20 years (from 1999 to 2018) to determine any change in the distribution of species and patterns of antifungal drug resistance.

 ~ Materials and Methods Top

The retrospective study was conducted at a tertiary care public sector hospital in North India. The total bed strength of our hospital is 1740, with 1497 beds dedicated for adults and separate 243 bedded advanced paediatric centre for children. The intensive care units (ICUs) for adults include critical coronary unit (25 beds), cardiothoracic vascular surgery ICU (25 beds), medicine ICU (13 beds), renal transplant ICU (12 beds), trauma ICU (12 beds), liver ICU (10 beds), burns ICU (10 beds), respiratory ICU(8 beds), gastroenterology ICU (8 beds), neurosurgery ICU (6 beds), while paediatric centre harbours separate neonatal ICU (16 beds), paediatric medicine ICU (12 beds), and paediatric surgery ICU (12 beds). All blood culture results of suspected sepsis cases from January 1999 to December 2018 at our centre were screened for candidaemia cases. Candidaemia was defined as the isolation of Candida species from blood at least once in the presence of clinical features of sepsis. The blood was cultured conventionally by biphasic brain heart infusion agar and broth (HiMedia, India) till 2008 and by automated BACTEC system (BD BACTEC™ 9240, New Jersey, USA) since 2009.

Yeast identification

The yeast species isolated were identified by conventional methods (germ tube, corn meal agar, sugar assimilation, sugar fermentation, urease tests) till 2013 and since 2014 by matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) (Bruker Daltonics, Billerica, MA, USA) using flex control software (Bruker Daltonics) and auto mode. The database of Bruker MALDI-TOF MS was expanded for locally prevalent Candida species by developing novel main spectrum projections.[11] The species identification was confirmed with a score of ≥2 and to the genus level with a log score of 1.7–2. Those yeasts that could not be identified by auto mode (score ≤1.7) were identified by manual mode. In manual mode, the peaks were acquired by flex control software and matched with the database of MALDI biotyper. The yeasts that still had the score <2 by manual mode were further identified by sequencing the internal transcriber spacer or D1/D2 of 26S region of ribosomal DNA as described previously.[11],[12],[13]

Antifungal susceptibility testing

Candida isolates were subjected to antifungal susceptibility against amphotericin B (Sigma Aldrich, India), fluconazole (FDC, India; Sigma Aldrich, India), itraconazole (Janssen Laboratories, Belgium; Sigma Aldrich, India). Voriconazole (Pfizer Central Research, Tadworth, UK; Sigma Aldrich, India), posaconazole (Sigma Aldrich, India; Merck Sharp and Dohme, Gurgaon, India) and echinocandins [caspofungin (Merck Sharp and Dohme, India), micafungin (Astellas Pharma, US) and anidulafungin (Pfizer Central Research, Tadworth, UK)] were added to antifungals panel since 2012. The minimum inhibitory concentrations (MICs) were determined by micro broth dilution method as per the recommendations of the National Committee for Clinical Laboratory Standards (NCCLS) M27-A from 1999 to 2001 and Clinical Laboratory Standards Institute (CLSI, formerly NCCLS) recommendations in M27-A2, M-27A-A3, M27 documents.[14],[15],[16],[17]C. parapsilosis (ATCC 22019) and Candida krusei (ATCC 6258) were included in the study as quality control strains for antifungal susceptibility testing (AFST).

Statistical analysis

The analysis was carried out using the Statistical Package for the Social Sciences (SPSS Inc., Chicago, IL, USA version 22.0 for Windows). Data were represented as mean (standard deviation) and median (range) for quantitative variables and number (frequency/proportions) for qualitative variables. The proportions were compared using the Chi-square test or Fisher's exact test when applicable, and a P ≤ 0.05 was considered statistically significant.

 ~ Results Top

A total of 602,963 blood samples from suspected sepsis cases were received at our tertiary care centre during the study period and Candida species were isolated in 7927 (1.31%) samples. A rising trend of Candida species isolation was noted over the years [Figure 1]. The rate of candidaemia among suspected sepsis cases rose from 0.9% in 1999 to 2.29% in 2018; with the frequency at 1.42%, 0.95%, 1.00% and 1.68% during 1999–2003, 2004–2008, 2009–2013 and 2014–2018 respectively. A significant rise (P = 0.000) in candidaemia rate was noted in the last quarter of the study. The majority of the candidaemia cases were reported in children (n = 5035; 63.5%) compared to adults (n = 2892; 36.5%). The candidaemia was reported in 2660 (33.6%) patients in ICUs, of which 2,109 (79.3%) were from paediatric ICUs and 551 (20.7%) from adult ICUs.
Figure 1: Trend of candidaemia over the 20-year study period (1999–2018)

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Distribution of Candida species

C. tropicalis (n = 3182; 40.1%) was the most common species isolated, followed by C. albicans (n = 1201; 15.2%), Wickerhamomyces anomalus (previously known as Candida pelliculosa, Pichia anomala) (n = 1036; 13.1%), C. krusei (n = 527, 6.6%), C. parapsilosis (n = 372, 4.7%), Candida guilliermondii (n = 362, 4.6%), C. glabrata (n = 250; 3.2%) and others. The spectrum of yeast species isolated in four quarters of the study period is shown in [Figure 2], and the distribution in adults and paediatrics over the four quarters is depicted in [Supplementary Figure 1] and [Supplementary Figure 2]. A significant change of spectrum of yeast species was noted in fourth quarter with the rise of C. glabrata (2%–4.3%; P = 0.000), C. krusei (4.6%–9.3%; P = 0.000), C. parapsilosis (1.5%–6.6%; P = 0.000) and W. anomalus (6.4%–17%; P = 0.000); and a noticeable fall in isolation of C. tropicalis (56.4%–28.7%; P = 0.000), C. albicans (19%–13.6%; P = 0.000) and C. guilliermondii (7.8%–1.1%; P = 0.000). Amongst adults, a significantly higher isolation of C. tropicalis in surgical units and C. krusei and C. guilliermondii in medical units was seen [Table 1]. In children, a predominance of W. anomalus and C. krusei was observed in medical units.[Table 1] The identification of rare species was possible after the introduction of MALDI-TOF in 2014 [Figure 3]. Those rare yeasts included C. auris (41/3389; 1.2%), Candida orthopsilosis (37/3889; 1.09%), Candida lambica (23/3389; 0.67%), Candida fabianii (17/3389; 0.5%), Candida intermedia (4/3389; 0.11%), Candida metapsilosis (4/3389; 0.11%), Candida vishwanathii (3/3389; 0.08%), Candida sake (2/3389; 0.05%), Candida carpophila (1/3389; 0.02%), Candida catenulata (1/3389; 0.02%), Candida duobushaemulonii, (1/3389; 0.02%), Candida inconspicua (1/3389; 0.02%), Candida pseudohaemulonii (1/3389; 0.02%) and Candida sorbosa (1/3389; 0.02%) [Figure 3].
Figure 2: Percentage of yeast species isolated from blood in each study quarter (1st: 1999–2003, 2nd: 2004–2008, 3rd: 2009-2013, 4th: 2014–2018). *All statistically significant comparisons between the four study quarters

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Table 1: The distribution of common yeast species across medical and surgical specialties in pediatric and adult population

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Figure 3: Doughnut chart depicting rare yeast species before (outer circle) and after (inner circle) the introduction of matrix assisted laser desorption ionization-time of flight MS in 2014

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Antifungal susceptibility

The trend of antifungal resistance of the common yeast isolates is shown in [Table 2]. The higher MIC was noted to amphotericin B in the last quarter of the study (0.5%, 0.1%, 1.1%, 4.9% in successive four quarters; P = 0.000). Fluconazole resistance was fairly constant (7.4%, 8.6%, 6.3%, 8.8% in successive quarters; P = 0.601). A significant decline was noticed in itraconazole resistance (22.2%, 8%, 14.3%, 3.8%; P = 0.000) over the quarters. Voriconazole, posaconazole, caspofungin, anidulafungin and micafungin resistance of the last quarter of the study was at 2.4%, 0.4%, 6.2%, 2.4% and 3.0% respectively. A significant decline in resistance rate to fluconazole was seen in C. albicans and C. glabrata, while increase was noticed in C. guilliermondii and C. krusei.
Table 2: Percentage antifungal resistance in common yeast species tested in the four study quarters from 1999 to 2018 (1: 1999-2003, 2: 2004-2008, 3: 2009-2013, 4: 2014-2018)

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 ~ Discussion Top

We report a 1.31% prevalence of candidaemia with an overall rise in isolation rate across the 20-year study duration [Figure 1]. The majority of the cases were from paediatric units. Among the Candida species, C. tropicalis was the commonest isolate followed by W. anomalus and C. albicans. A significant rise in isolation rate was noted in C. parapsilosis and C. glabrata in adults, while C. krusei and W. anomalus in children. Other species prevalent in paediatric units were Candida utilis and Kodamaea ohmeri. The identification of multidrug-resistant C. auris and other rare species, including C. vishwanathii was possible after the introduction of MALDI-TOF. During those 20 years, we recorded multiple outbreaks due to K. ohmeri, C. krusei and C. auris in our hospital, and due to P. anomala before the study period.[18],[19],[20] In addition, a cluster of fluconazole-resistant C. vishwanathii candidaemia cases was noted during the present study.[13]

The overall high rate of candidaemia cases at our centre is a matter of concern. The over-capacity patient load, compromise in healthcare, rise in susceptible population in our hospital may explain the rise in incidence. Our hospital data may represent the scenario in other hospitals of developing countries, as patient care is similar.[21] A multicentric study from our country hypothesised early colonisation by Candida species in Indian ICUs and compromise in healthcare which are possible causes of early acquisition of candidaemia following ICU admission.[4] In a neonatal ICU study from our centre, >70% of neonates were colonized by Candida within a week of delivery, contrary to 50% in developed countries.[21] The higher colonisation may lead to a higher incidence of candidaemia in paediatric ICUs of developing countries (42.7/1000 admissions) when compared to developed countries (0.043–0.47/1000 admissions).[21]

A temporal change in Candida species distribution with C. tropicalis being most common isolate had been highlighted in many studies from India, as shown in [Figure 4].[8],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39],[40],[41],[42] In the present study, though C. tropicalis was the most common isolate, a further shift with the rise in the isolation of C. glabrata and C. parapsilosis in adults, and C. krusei and W. anomalus in children was observed. The rise in C. glabrata isolation had been linked to increased use of fluconazole.[43] We also observed a rise in antifungal use in recent years at our centre. C. parapsilosis exhibits a unique capacity to form biofilms and is increasingly associated with device-related candidaemia.[44]C. krusei and W. anomalus are usually exogenous in origin. Both these species have been reported as cause of outbreaks in paediatric wards at our centre.[20],[45] During W. anomalus outbreak, 28% of neonates were colonised by this fungus on the day of delivery and 20% of them developed W. anomalus candidaemia subsequently.[20] We observed the overall decline of C. guilliermondii isolation rate during the study period, though the reason is not clear. The high isolation rate of C. utilis and K. ohmeri (previously called Pichia ohmeri, Yamadazyma ohmeri) in paediatric units requires further investigation. C. utilis is extensively used in the food industry and has been reported to cause nosocomial candidaemia in neonates.[46]K. ohmeri is persisting in our hospital for a long time and has been linked with nosocomial candidaemia. We reported a large cluster of candidaemia due to K. ohmeri in an earlier study.[19] Other resistant species such as C. auris and C. vishwanathii could be identified after the introduction of MALDI-TOF. These species are usually misidentified by phenotypic methods and require either MALDI or molecular technique for accurate recognition. The necessity of accurate identification of C. auris has been highlighted by many studies during the global outbreak.[13],[47]
Figure 4: Candida species isolated from blood stream infections as reported in Indian studies from 1999 to 2018

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We reported outbreaks of fungemia due to P. anomala (n = 379), K. ohmeri (n = 38) and C. krusei (n = 82) in children during 1996–1998, 2008–2009 and 2014. All those outbreaks were controlled with the improvement of infection control practices. C. auris outbreak in 2017 was controlled by the expeditious implementation of multiple interventions like chlorhexidine body wash of the colonizers, improvement in handwashing and disinfectant use practices.[18] We also reported twice the clusters of C. vishwanathii candidaemia cases during 2013–2015 across our hospital. Interestingly, all C. vishwanathii isolates turned fluconazole resistant in the second year.[13]

The overall low fluconazole resistance among C. tropicalis, C. albicans and W. anomalus, which constitute more than 70% of our isolates, is good news, as fluconazole may be empirically used in stable patients. We also noticed decline in fluconazole resistance among C. glabrata isolates similar to previous Indian reports indicating the possibility of genetic strain variations in Indian C. glabrata isolates compared to other countries.[48] The overall fall in itraconazole resistance may be due to less use of the drug over the years in our paediatric units. The voriconazole resistance in C. krusei (1.9%), and echinocandins resistance (6.2%) in C. glabrata, C. guilliermondii, C. tropicalis and C. krusei were noted in the later quarter of our study when those antifungals were tested. However, those antifungal drugs are not so commonly used due to the high cost.[4],[49] A rise in amphotericin B MICs (0.%–4.9%) in C. tropicalis, C. albicans, C. glabrata and C. krusei warrants close monitoring.[4],[50] The antifungal resistance of the isolates may vary in between the centres of the same country due to different management protocols practiced. A similar variation was noted in different reports from India [Table 3]. The emergence of multidrug-resistant species like C. auris demands implementation of routine AFST.
Table 3: Details of antifungal resistance reported in Indian studies from 1999 to 2018

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Our centre has reported local epidemiology of candidaemia time to time and on comparing the earlier studies, though C. tropicalis remained the first rank of isolation, many relatively rare Candida species were isolated in the present study.[7],[8],[10],[42] It is not clear whether the phenomenon was due to the introduction MALDI-TOF in the identification or new entry of those species in our hospital. W. anomalus (P. anomala) fungemia outbreak was reported in our hospital before the present study period. Although the outbreak was controlled, the isolation of 13.1% W. anomalus in the present study indicates the fungus has become endemic in our hospital. C. guilliermondii showed a marked decline from 16.7% in previous studies to 4.6% in the present study. An upward or downward swing had been noted with C. parapsilosis and C. krusei isolation, which warrants detailed investigation. The fluconazole resistance rate in the present study was higher compared to the earlier studies from our centre. On the contrary, antifungal resistance against amphotericin B showed a decline from 9% in the previous study to 3.2% in the present study.[8] All these findings emphasize the need of publication of local epidemiology time to time and routine AFST of blood isolates.

The strength of our study is that it is the largest collection of candidaemia cases over 20 years period from a single centre with the denominator of all suspected sepsis cases of our hospital, which provides the exact prevalence of candidaemia cases in a tertiary care centre in a developing country and highlights the change of species distribution and antifungal resistance over the years. As our centre reported epidemiology of candidaemia cases time to time, the study could provide change of the face of candidaemia. The study possibly reflects the scenario of candidaemia cases in tertiary care centres of developing countries. It also emphasizes the need of improvement of species identification by MALDI-TOF for rapid and accurate identification of the fungus. The limitation of the study is that it is a retrospective study and could not analyse the risk factors, attributable mortality of candidaemia without control cases and limitation of data.[51]

 ~ Conclusion Top

C. tropicalis continues to be the common cause of candidaemia at our centre with increased recognition of rare yeasts such as C. auris, C. utilis, C. vishwanathii. There was a significant rise in isolation of C. parapsilosis and C. glabrata in adults while C. krusei and W. anomalus in children. The rise in resistance against amphotericin B (C. parapsilosis), voriconazole (C. krusei) and echinocandins (C. guilliermondii, C. glabrata) is a matter of concern. The study highlights the need of accurate identification of Candida species and AFST in the routine laboratory.

Financial support and sponsorship

We would like to acknowledge the Indian Council of Medical Research for financial support (Grant No. AMR/TF/51/13ECDII).

Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1], [Table 2], [Table 3]


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2004 - Indian Journal of Medical Microbiology
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