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 Table of Contents  
Year : 2020  |  Volume : 7  |  Issue : 3  |  Page : 167-172

Candidemia – Changing trends from Candida albicans to non-albicans Candida from a tertiary care center in western UP, India

1 Department of Microbiology, Jawaharlal Nehru Medical College, Aligarh Muslim University, Aligarh, Uttar Pradesh, India
2 Department of Microbiology, Immunology and Infectious Disease, College of Medicine and Medical Science, Arabian Gulf University, Manama, Kingdom of Bahrain

Date of Submission17-Feb-2020
Date of Decision13-Jul-2020
Date of Acceptance27-Jul-2020
Date of Web Publication25-Jan-2021

Correspondence Address:
Shariq Ahmed
Department of Microbiology, Jawaharlal Nehru Medical College, Aligarh Muslim University, Aligarh - 202 001, Uttar Pradesh
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/cjhr.cjhr_12_20

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Introduction: Candidemia is a major cause of morbidity and mortality in hospitalized patients, especially pediatric population, justifying the importance of adequate antifungal therapy. Immunocompromised patients, preterm neonates, elderly patients and patients admitted to intensive care units are at higher risk of invasive candidiasis infections. A shift has been observed in the relative frequency of non-albicans Candida (NAC) and Candida albicans in blood stream infections. Studies on the prevalence of infections and antifungal susceptibility testing can help with deciding on clinical strategies to manage this problem. Aims and Objectives: The following study was performed to find the prevalence of various Candida species causing candidemia and their resistant pattern in Aligarh region of western Uttar Pradesh. Materials and Methods: Two thousand and eighty-four samples for blood culture were received in the microbiology laboratory over a period of 5 months. Seventy-one positive samples for Candida were identified and tested for antifungal susceptibility testing by Vitek-2 (21) and conventional methods (50). Results: 3.41% of the blood culture were positive for Candida species. Candida tropicalis (35.21%) was the most common species isolated followed by Candida glabrata (21.13%), C. albicans (14.08%), Candida krusei (9.86%), Candida pelliculosa (9.86%), Candida parapsilosis (4.23%), Candida guilliermondii (4.23%), and Candida utilis (1.41%). Maximum percentage of isolates were from neonates (47.89%) followed by infants (25.35%). Resistance to fluconazole and amphotericin B was seen in 11.27% and 1.41% of isolates. Conclusion: NAC species outnumbering C. albicans even as single most common species in candidemia patient isolates is alarming. Fluconazole is generally used as empirical therapy. NAC being more resistant and some being intrinsically resistant (C. krusei) to fluconazole strengthens the need of antifungal susceptibility testing on priority basis.

Keywords: Candida tropicalis, candidemia, non-albicans Candida

How to cite this article:
Ahmed S, Shahid M, Fatima N, Khan F, Tayyaba U. Candidemia – Changing trends from Candida albicans to non-albicans Candida from a tertiary care center in western UP, India. CHRISMED J Health Res 2020;7:167-72

How to cite this URL:
Ahmed S, Shahid M, Fatima N, Khan F, Tayyaba U. Candidemia – Changing trends from Candida albicans to non-albicans Candida from a tertiary care center in western UP, India. CHRISMED J Health Res [serial online] 2020 [cited 2022 Jul 7];7:167-72. Available from: https://www.cjhr.org/text.asp?2020/7/3/167/307815

  Introduction Top

The incidence and prevalence of candidemia are on a rise in many countries.[1] Bloodstream infection by Candida species is a major cause of morbidity and mortality in hospitalized pediatric and adult patients especially those in intensive care units (ICUs).[2],[3],[4],[5] Candida species are the fourth leading cause of nosocomial blood stream infection (BSI) in the United States and ranks 7th in Europe.[1] Although more than 17 different species of Candida have been reported to be etiologic agents of invasive candidiasis in humans, only five species (Candida albicans, Candida glabrata, Candida tropicalis, Candida parapsilosis, and Candida krusei) accounted for 92% of cases of candidemia.[6] An increase in the isolation of non-albicans Candida (NAC) species can be seen worldwide; however, C. albicans still remains the most common cause of candidemia.[1]

Region-wise distribution of NAC species has shown quite a variability. The USA and northern Europe have reported a high number of cases by C. glabrata whereas in Brazil and Spain C. parapsilosis is the predominant species isolated from candidemia patients among the NAC species. Furthermore, globally, it is seen that the frequency of C. albicans is decreasing, while that of C. glabrata and C. krusei is stable, and C. parapsilosis and C. tropicalis are increasing.[7] Nationwide data are lacking from India, but from individual studies, 6%–8% of candidemia rates have been reported with increasing isolation of NAC species. Among them, C. tropicalis is found to be the most common species.[8],[9],[10]

Polyenes, allylamines, azoles, and echinocandins are the antifungal drugs available for the treatment of systemic and invasive candidiasis. Azoles is the most common group of antifungal used worldwide with fluconazole topping the list.[11],[12] Epidemiological shift from C. albicans to NAC may be attributed to the increasing use of azoles giving rise to increased isolation of resistant species from candidemia patients such as C. glabrata and C. krusei (intrinsically resistant to fluconazole). They may also show cross resistance to newer triazoles.[13]

Hospitalized, ICU patients, neonates, patients receiving organ transplant, suffering from malignant diseases, on immunosuppressive drugs or other conditions leading to decreased immunity are subjected to abundant use of antibiotics and antifungals. The isolation of antifungal resistant Candida is on a rise from such group of patients. As morbidity and mortality are very high in such patients, selection of an effective empirical therapy for invasive candidiasis requires a critical knowledge of local epidemiology and regional variability of the concerned area. Therefore, following study was conducted to know the occurrence of candidemia in our region, among suspected septicemic patients and determine the antifungal susceptibility profile of the candida species isolated from them.

  Materials and Methods Top

This retrospective, observational study was performed in the microbiology laboratory of a tertiary care hospital in Aligarh region of western Uttar Pradesh, India, during May 2019–October 2019 for 5 months. During this period, a total of 2084 blood samples were received in the microbiology laboratory from suspected cases of septicemia, out of which 71 samples yielded a growth of Candida isolates.

Specimen collection

Specimens were collected under aseptic precautions after taking informed consent from patients for routine diagnosis. Blood culture was carried out by BacTAlert3D (Biomerieux, France) automated blood culture system or conventional blood culture bottles as per request of the physician (the hospital caters a very poor population, Bactec and Vitek were not possible on all samples due to monetary restraints). Once a blood culture bottle showed a positive growth, initially, a Gram-stain was done from the broth in the bottle to look for yeast cells. Then, it was subcultured for isolation and speciation. Each positive blood sample was inoculated onto two plates of Sabouraud dextrose agar and blood agar and incubated at 25°C and 37°C. The colonies appeared within 24 h in all the cases. Then, several phenotypic tests were performed for speciation of the Candida isolates. These included Gram's staining, germ tube test, colony morphology on cornmeal agar (HiMedia, India), CHROMagar Candida (CHROMagar, Paris, France). Antifungal susceptibility testing was also performed by disk diffusion method according to Clinical and Laboratory Standards Institute (CLSI) guidelines.[14]

Twenty-one samples were identified with VITEK 2 Compact (Biomerieux, France) using VITEK 2 cards for the identification of yeast and yeast-like organisms (ID-YST cards). Antifungal susceptibility testing was performed with AST YS07 Kits on VITEK 2 Compact system.

  Observations and Results Top

A total of 2084 blood cultures were received in the microbiology laboratory during the period of 5 months from May 2019 to October 2019 from the patients suspected of septicemia. Of these, 71 blood cultures showed the growth of Candida species. The rate of Candida infection was 3.41% (71/2084). From these 71 Candida isolates, 21 isolates were subjected to identification and antifungal susceptibility by Vitek 2 compact and other 50 isolates were identified by conventional methods and antifungal susceptibility by disc diffusion method.

It was seen that out of the total 71 patients that were suffering from candidemia. Maximum (34 [47.89%]) belonged to the age group below 1 month followed by infants, i.e., up to 1 year of age (18 [25.35%]) and children up to 5-year (10 [14.08%]). The detailed result is shown in [Table 1].
Table 1: Age-wise distribution of patients showing candidemia (n=71)

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Isolates from NAC species dominated over Candida albicans 61 (85.91%) vs. 10 (14.08%) with C. tropicalis (35.21%) being the most common species followed by C. glabrata (21.13%). C. albicans (14.08%) was the third most common species isolated. 9.86% of isolates were identified as C. krusei and C. pelliculosa while 4.23% isolates were of C. parapsilosis and C. gulliermondii. Only 1 isolate was identified as C. utilis [Table 2].
Table 2: Distribution of Candida species among various age groups (n=71)

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C. albicans infection in infants was slightly more than that in neonates (5.63% vs. 4.23%). However, all NAC species except C. pelliculosa (4.23% vs. 4.23%) had higher isolation rate in neonates than in infants; C. tropicalis (14.08% vs. 9.86%), C. glabrata (12.68% vs. 4.23%), C. krusei (5.63% vs. 1.41%), C. gulliermondii (2.82% vs. 0%), C. parapsilosis (2.82% vs. 0%), and C. utilis (1.41% vs. 0%) [Table 2].

Among the 50 Candida isolates that were tested for antifungal susceptibility by disc diffusion method (n = 50) according to CLSI guidelines; resistance to fluconazole, amphotericin B, clotrimazole, itraconazole, nystatin, and ketoconazole was 14%, 0%, 4%, 6%, 4%, and 2% respectively. All of the C. albicans and C. parapsilosis isolates were sensitive to fluconazole, amphotericin B, clotrimazole, itraconazole, nystatin, and ketoconazole. No resistance was seen in C. tropicalis isolates to fluconazole and amphotericin B; however, 1 (5.89%) isolate was resistant to clotrimazole, itraconazole, and ketoconazole, each. Similarly, out of 14 C. glabrata isolates tested, no resistance was seen with fluconazole, amphotericin B, nystatin, and ketoconazole; but 1 (7.14%) isolate was resistant to clotrimazole and itraconazole.

All the 7 isolates of C. krusei was resistant to fluconazole, 1 (14.2%) isolate was resistant to itraconazole and nystatin. No resistance was seen with amphotericin B, clotrimazole, and ketoconazole [Table 3].
Table 3: Antifungal susceptibility profile of Candida isolates by disc diffusion method (n=50)

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Among the 21 candida isolates that were tested for antifungal susceptibility by Vitek 2, all the isolates of C. gulliermondii,[3] C. parapsilosis.[2] C. utilis[1] were sensitive to fluconazole, amphotericin B, voriconazole, flucytocine, capsofungin, and micafungin. Only 1 (14.28%) isolates of C. pelliculosa was resistant to amphotericin B, while 1 (12.5%) isolates of C. tropicalis was resistant to fluconazole [Table 4].
Table 4: Antifungal susceptibility profile of Candida isolates by Vitek 2 (n=21)

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Overall (by disc diffusion + Vitek 2) resistance to fluconazole (including resistant isolates of C. krusei) and amphotericin B was 11.27% and 1.41% in all the 71 Candida isolates.

  Discussion and Conclusion Top

Blood stream Candida infections are on a rise in the recent past. The contribution of NAC species in causing candidemia has increased significantly, some studies showed them surpassing BSIs caused by Candida albicans. Pfaller and Diekema 2007 noted a decreasing trend in the isolation of C. albicans over time.[1] They also depicted rate of isolation increased by 2.9% of Candida tropicalis and 3.1% of C. parapsilosis between 1997 and 2003.[1] Furthermore, the isolation rates of rare species such as C. guilliermondii, C. kefyr, C. rugosa, and C. famata increased between 2 and 10-fold over the course of the study done by Pfaller 2007.[1]

In our study, 3.41% (71/2084) of the blood culture received from suspected septicemic cases were positive for candida species. Studies from across India have shown a varied rate of Candida isolation from BSIs. Isolation rate reported were; 32.5% from Jammu and Kashmir in clinically diagnosed septicemia neonates,[15] 4.03% from Kolkata,[16] 1.74%,[17] 6%,[8] and 6.9%[10] from New Delhi, 5.7% from Chennai among children with hematological malignancy,[18] 9.4% from Cuttack,[19] 1.61% from Lucknow.[20] However, from across the globe a low incidence (per thousand admissions) candidemia is reported like 0.47 from Chile,[21] 0.21 from Australia,[22] 0.44 from Belgium,[23] 0.58 from Spain,[24] 1.09 from Northern Ireland,[25] 1.73 from Italy[26] 2.04 from Peru,[27] 2.49% from Brazil.[5]

In the present study, Candida was isolated maximum 34 (47.89%) from neonates (below 1 month) followed by Infants 18 (25.35%) (up to 1 year) and children 10 (14.08%) (up to 5 years of age). However, blood stream Candida infection was seen in only 12.68% in patients above 5 years of age. One reason for such low percentage of Candida infection detected from adults in our study is that most of the blood culture received in our setup are from the pediatric age group. Similarly, Chakrabarti et al. from Chandigarh showed 72.9% and 27.2% of candidemia in pediatric and adult age group.[28] However, Santolaya ME et al.(2019) from Chile reported that 35% of candidemia occurred in in pediatric patients (25 cases in neonates, 45 in infants, and 64 in children) and 250 (65%) occurred in the adult population (102 in adults and 148 in the elderly).

The study showed NAC species predominated over C. albicans (61 [85.91%] vs. 10 [14.08%]). Similar findings were reported from various studies done in India (85.3%,[15] 82.85%,[19] 86.4%[8]). C. albicans is reported as the most common Candida species causing BSI worldwide.[1],[29],[30] However, our study showed that C. tropicalis (35.21%) was the most common species isolated followed by C. glabrata (21.13%). C. albicans (14.08%) was the third most common species isolated. 9.86% of isolates were identified as C. krusei and C. pelliculosa while 4.23% isolates were of C. parapsilosis and C. gulleirmondii. Only 1 isolate was identified as C. utilis. From various part of India such as Jammu and Kashmir 13.08%;[15] Kolkata 24.28%;[16] Delhi 39%,[19] 29.2%,[17] 35.3%;[8] and 45%[31] C. tropicalis has been reported as the most common NAC species isolated. However, Gupta et al.[32] reported C. glabrata (42%) as the most common species isolated followed by C. tropicalis (31.6%), C. albicans (21.1%), and C. parapsilosis (5.2%). While trends from recent studies across the world show C. parapsilosis 30% (Chile),[21] 22.6% (Brazil),[33] 34.67% (Kuwait)[34] as the predominant NAC species isolated from BSIs. Xess et al. also reported C. parapsilosis dominating C. tropicalis in the last year of their study.[8] It can be seen from the above observations that C. tropicalis is the most common C. glabrata NAC species causing BSIs in our region of India sometimes even surpassing C. albicans isolation rates. From the same institution 5 years back Jahan et al. reported, C. albicans (59.2%) as the most common species while NAC species were 40.8% (C. tropicalis 14.3%, C. parapsilosis 12.2%, C. gulliermondii 6.2%, 4%, C. krusei 2%, and C. dubliniensis 2%, respectively)[35] which indicates the shift toward NAC species.

C. albicans infection in infants was slightly more than that in neonates (5.63% vs. 4.23%). However, all NAC species except C. pelliculosa (4.23% vs. 4.23%) had higher isolation rate in neonates than in infants; C. tropicalis (14.08% vs. 9.86%), C. glabrata (12.68% vs. 4.23%), C. krusei (5.63% vs. 1.41%), C. gulleirmondii (2.82% vs. 0%), C. parapsilosis (2.82% vs. 0%), and C. utilis (1.41% vs. 0%). In our study, infection of all Candida species was more common in neonates than adults (C. albicans 4.23% vs. 0, C. tropicalis 14.08% vs. 2.82%, C. glabrata 12.68% vs. 0, C. krusei 5.63% vs. 1.41%, C. gulliermondii 2.82% vs. 0%, C. parapsilosis 2.82% vs. 1.41%, C. pelliculosa 4.23% vs. 0%, C. utilis 1.41% vs. 0% respectively]. However, Pfaller et al. reported that C. albicans and C. parapsilosis are more frequent in neonates (60% vs. 50% and 24% vs. 12%, respectively). In contrast, the frequency of cases caused by azole-resistant species such as C. glabrata and C. krusei is much lower in neonates (3% vs. 23% and 0% vs. 2%), probably reflecting scant use of azoles in neonatology.[36]

In our study, fluconazole resistance among all isolates of Candida species (n = 71) was 11.27%, which was quite similar to 11.7% reported by Xess et al.,[8] 12.2% by Sarver Jahan et al.[35] and was higher than 5.9% reported by Pahwa et al.[37] However, most of the other Indian studies have shown a high percentage 31.2%,[17] 64%,[31] 37.5%,[38] 35%[19] of fluconazole resistance. Fluconazole resistance is on a rise as it is the most commonly used antifungal drug giving rise to frequent isolation of resistant antifungal strains C. glabrata and intrinsically fluconazole-resistant strains of C. krusei. 1.41% of the Candida isolates were resistant to amphotericin b in our study which were quite similar to 2% reported by Jahan et al.[35] but lower than 2.9%,[37] 8%[31] as depicted by other studies. None of the C. albicans isolate was resistant to fluconazole and amphotericin B in the present study. However, Bhattacharjee showed similar fluconazole resistance but a very high resistance to amphotericin B (53.6%) among C. albicans isolates.[16] Furthermore, Nazir and Masoodi showed a very high resistance to fluconazole 42% and amphotericin B 14% in C. albicans.[15] In our study, NAC species were 13.11% resistant to fluconazole and 1.64% resistant to amphotericin B which was much lower than that depicted by Bhattacharjee (61.11%, 30.56%)[16] and Jahan et al. (15%, 10%).[35]

Resistance to fluconazole (4%), clotrimazole (5.89%), itraconazole (5.89%), nystatin (5.89%), and ketoconazole (5.89%) was seen among C. tropicalis isolates; none of them was resistant to amphotericin B, voriconazole, flucytosine, caspofungin, and micafungin. Similar resistance to fluconazole (3.7%) were depicted by Santolaya et al.[21] but a higher (14.2%),[35] (9.5%),[17] and (49%)[15] by other authors. No resistance to voriconazole, flucytosine, caspofungin, and micafungin was seen in any of the NAC species isolates from our study. Nazir and Masoodi showed no resistance to voriconazole and caspofungin while resistance to flucytosine was 12%.[15] While, Santolaya et al. detected resistance to voriconazole (2.2%) in C. parapsilosis and (3.7%) in C. tropicalis.[21]

In conclusion, it was seen that NAC species predominated C. albicans in causing BSIs however resistance rates to antifungals in our setup were quite low especially to newer azoles such as voriconazole and echinocandins group of drugs even in NAC species as compared to fluconazole. However, high rates of isolation of NAC species which are notorious of being multidrug resistance suggests the need to know the regional epidemiology of Candida in BSIs and of performing a prospective azole and echinocandins resistance surveillance in our country and formulating a prudent antifungal drug policy. Prior knowledge of species distribution in clinical isolates and drug sensitivity pattern among species help the clinician to choose early empirical therapy. Delay in the initiation of antifungal drug may contribute to elevated mortality rate, in spite of low antifungal resistance. There should be strengthening of antifungal stewardship policies to minimize acquisition of acquired resistance. Limitation of our study was that it was a retrospective single-center study done for a short duration of time. However, a nationwide study is the need of the hour to formulate policies and strategies for risk identification and management (i.e., prophylaxis, preemptive therapy, or empirical therapy) for invasive candidiasis.

The authors declare that there is no conflict of interest.

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Conflicts of interest

There are no conflicts of interest.

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  [Table 1], [Table 2], [Table 3], [Table 4]

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