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 Table of Contents  
ORIGINAL ARTICLE
Year : 2017  |  Volume : 4  |  Issue : 2  |  Page : 78-83

Increased role of nonalbicans Candida, potential risk factors, and attributable mortality in hospitalized patients


Department of Microbiology, BPS GMC for Women, Khanpur Kalan, Sonepat, Haryana, India

Date of Submission12-Nov-2016
Date of Acceptance02-Jan-2017
Date of Web Publication15-Jun-2017

Correspondence Address:
Raminder Sandhu
Department of Microbiology, BPS GMC for Women, Khanpur Kalan, Sonepat, Haryana
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2394-2010.208115

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  Abstract 

Aim: The aim of this study was to evaluate the distribution of nonalbicans Candida (NAC) along with their associated risk factors, clinical outcome, and antifungal susceptibility pattern among inpatients. Materials and Methods: Retrospective descriptive study comprising 94 isolates of Candida species obtained from various clinical specimens of hospitalized patients. The clinical charts of patients were reviewed retrospectively who stayed in the hospital for more than 7 days irrespective of their diagnosis. Statistical Analysis: Descriptive statistics was used which involves the use of simple percentage and bar chart to analyze the data. In addition, Chi-square test was performed and P value was calculated. Results: NAC was identified in 72 (77%) patients and Candida albicans in 22 (23%). Factors associated with Candida krusei were stay in hospital ≥15 days (78%), broad-spectrum antimicrobial therapy (72%), prophylactic fluconazole therapy (67%), preterm newborn with low birth weight (LBW) (67%), stay in the Intensive Care Unit (ICU) ≥10 days (67%), indwelling devices (67%), and mechanical ventilation (67%); Candida glabrata infection as broad-spectrum antimicrobial therapy (69%), preterm newborn with LBW (62%), stay in ICU ≥10 days (62%), and indwelling devices (62%); Candida tropicalis as indwelling devices (86%), broad-spectrum antimicrobial therapy (71%), stay in ICU ≥10 days (71%), stay in hospital ≥15 days (71%), pulmonary tuberculosis (71%), neutropenia (71%). Amphotericin B was effective against both C. albicans as well as NAC with susceptibility of 91% and 89%, respectively. Mortality was similar in patients infected with C. albicans and nonalbicans species (27.27% vs. 27.77%). Conclusion: The study concludes higher prevalence of NAC with majority of patients having multiple underlying illnesses and other associated risk factors. Continued surveillance of Candida infections will be required to document changes in epidemiology and antifungal susceptibilities.

Keywords: Antifungal susceptibility pattern, inpatients, Nonalbicans Candida


How to cite this article:
Sandhu R, Dahiya S, Sayal P, Budhani D. Increased role of nonalbicans Candida, potential risk factors, and attributable mortality in hospitalized patients. J Health Res Rev 2017;4:78-83

How to cite this URL:
Sandhu R, Dahiya S, Sayal P, Budhani D. Increased role of nonalbicans Candida, potential risk factors, and attributable mortality in hospitalized patients. J Health Res Rev [serial online] 2017 [cited 2019 Dec 11];4:78-83. Available from: http://www.jhrr.org/text.asp?2017/4/2/78/208115




  Introduction Top


Candida spp. is among the most common fungal pathogens which are capable of initiating infections in both immunocompetent individuals as well as immunocompromised hosts; however, the incidence of infections is more in immunocompromised individuals; candidiasis, hence, is rightly called the “disease of diseased.”[1] Since 1995, Candida species have become the fourth most common cause of nosocomial bloodstream infection that are associated with a crude mortality rate of 39%. In the Intensive Care Units (ICUs), infection with Candida species is rated as the third most frequent cause of nosocomial bloodstream infection which is associated with a crude mortality rate of 47%.[2] The term candidiasis covers a wide range of diseases that vary from more superficial and milder clinical manifestations such as esophageal or oropharyngeal candidiasis to serious infections including BSIs and disseminated candidiasis, whereas the description of invasive candidiasis (IC) encompasses severe diseases such as candidemia, endocarditis, disseminated infections, central nervous system infections, endophthalmitis, and osteomyelitis. A wide range of risk factors including underlying malignancies, immunosuppressive diseases, hematopoietic stem cell or solid organ transplantation, the use of wide-spectrum antibiotics or corticosteroids, invasive interventions, aggressive chemotherapy, parenteral alimentation, and internal prosthetic devices can increase the risk of candidiasis.[3] Recent epidemiological data also reveal a mycological shift from Candida albicans to the nonalbicans Candida (NAC) species such as Candida glabrata, Candida tropicalis, Candida parapsilosis, and Candida krusei. It is considered that frequent use of fluconazole as antifungal prophylaxis has played a major role in the emergence of NAC species. Some of these species have been correlated with increased virulence and sometimes with increased mortality.[4] Due to varied forms of clinical presentations resulting out of Candida species infections, the identification of this pathogen from all the clinical specimens received at laboratory irrespective of clinician's suspicion becomes utmost important. Thus, identification of Candida up to species level along with antifungal susceptibility becomes very essential, as C. krusei and C. glabrata are known for their innate resistance to fluconazole which can limit their clinical usage.[5] The transition of Candida spp. from commensal to potent pathogen is facilitated by a number of virulence factors such as adherence to host tissues and medical devices, biofilm formation, and secretion of extracellular hydrolytic enzymes. Although the research has been extensive to identify these virulence attributable factors in C. albicans, relatively less is known about NAC species.[6] The present study shall address the distribution of C. albicans and nonalbicans species along with their related risk factors, mortality rate and antifungal susceptibility pattern in hospitalized patients. The knowledge of local epidemiological trends among Candida species is important as a guide in making the choice of empiric therapy.

Aims of the study

  1. To determine the prevalence and in vitro antifungal susceptibility pattern of C. albicans and NAC among inpatients of a tertiary care institute
  2. To evaluate different risk factors and comorbid conditions associated with the inpatients infected by C. albicans and NAC
  3. To know about the mortality rate as a clinical outcome of infection with Candida species.



  Materials And Methods Top


A retrospective descriptive study was conducted in the Microbiology Department of a tertiary care institute from February 2014 to December 2014. The material comprised 94 isolates of Candida species obtained from various clinical specimens including blood, urine, sputum, and body fluids of hospitalized patients during the study period. All patients infected with these Candida species (C. albicans, C. tropicalis, C. glabrata, and C. krusei) who stayed in the hospital for more than 7 days irrespective of their diagnosis were included in the study. No informed consent was obtained because of the retrospective nature of this study. Death was defined as death before hospital discharge. The clinical charts of these patients were reviewed retrospectively with the permission of Head of Department of Medical Records to access the patient's documents.

As per the standard operating procedures, all the clinical specimens were inoculated on blood agar and MacConkey agar except blood samples which were inoculated in biphasic brain heart infusion agar plus broth. The culture plates were incubated aerobically at 37°C for 24–48 h. The visual growth was stained, and the one which revealed Gram-positive budding yeast cells was further subcultured on sabrauads dextrose agar (SDA) and CHROMagar. The colony color and morphology on the chromogenic media were interpreted by separate individuals to remove the observer bias for completion of the study in a blinded manner. The growth on SDA was further speciated by standard methods using germ tube test and sugar fermentation and assimilation test. The isolates that remained doubtful in their appearance on CHROMagar and those which did not confirm to the accepted morphological characteristics were considered as unidentified and excluded from the study. The antifungal susceptibility testing of yeast isolates was carried out using the disk diffusion method as per the Clinical and Laboratory Standards Institute (CLSI) document M44-A.[7] The discs tested were amphotericin B (100 units), fluconazole (25 μg), and voriconazole (1 μg), with their zone diameters measured as per the instruction manual of manufacturer (HiMedia Labs Pvt. Ltd., Mumbai, India). The interpretive criteria for the fluconazole and voriconazole DD tests were those of the CLSI: Susceptible (S), zone diameters of ≥19 mm (fluconazole) and ≥17 mm (voriconazole); susceptible dose dependent, zone diameters of 15–18 mm (fluconazole) and 14–16 mm (voriconazole); and resistant (R), zone diameters of ≤14 mm (fluconazole) and ≤13 mm (voriconazole).[8] All the media and discs were procured from HiMedia Labs, Mumbai.

Clinical data of all the patients infected with Candida species (C. albicans, C. tropicalis, C. glabrata, and C. krusei) were recorded from clinical case sheets. The data included age and gender of the patient, duration of stay in hospital and ICUs, and other risk factors, namely, current or prior use of antimicrobials, underlying morbid illness, diabetes mellitus, neutropenia, hematologic malignancies, presence or absence of sepsis, immunosuppressive therapy, presence of indwelling central venous catheters (CVCs) and urinary catheters, invasive procedures, surgical intervention, requirement of vasopressor support, and total parenteral nutrition.

Statistical analysis

Descriptive statistics was used which involves the use of simple percentage and bar chart to analyze the data. In addition, Chi-square test SPSS v 20 programme (SPSS Inc., Chicago, IL, USA) was performed, and P value was calculated. P < 0.05 was considered statistically significant to show an association between potential risk factors and the dependent variables.


  Results Top


A total of 94 Candida species isolates were included in the study (59 from blood, 25 from urine, 8 from sputum, and 4 from body fluid cultures). Of these, NAC was identified in 72 (77%) patients and C. albicans in 22 (23%). Among NAC, the predominant species was C. tropicalis (39%), followed by C. glabrata (36%) and C. krusei (25%). Nonalbicans species, as well as C. albicans, remained important pathogens in patients admitted in various ICUs, with C. glabrata (92%), C. krusei (78%) as predominant pathogen in neonatal ICU, C. tropicalis (64%) and C. albicans (50%) in medical ICU. The majority of patients had multiple underlying illnesses and other risk factors associated with the episodes of candidal infections. The predisposing factors for C. albicans infection remained administration of broad-spectrum antimicrobial therapy (82%), duration of stay in hospital ≥15 days (68%), respiratory tract infection (64%), anemia (64%), intake of corticosteroids (64%), presence of indwelling devices (64%), neutropenia (36%), and pulmonary tuberculosis (32%). The factors responsible for acquisition of C. krusei in present study were stay in hospital ≥15 days (78%), administration of broad-spectrum antimicrobial therapy (72%), prophylactic fluconazole therapy (67%), preterm newborn with low birth weight (LBW) (67%), stay in ICU ≥10 days (67%), presence of indwelling devices (67%), and mechanical ventilation (67%), whereas in C. glabrata infection, administration of broad-spectrum antimicrobial therapy (69%), preterm newborn with LBW (62%), stay in ICU ≥10 days (62%), and presence of indwelling devices (62%) remained major risk factors. In C. tropicalis infection, the important risk factors in decreasing order were presence of indwelling devices (86%), administration of broad-spectrum antimicrobial therapy (71%), stay in ICU ≥10 days (71%), duration of stay in hospital ≥15 days (71%), pulmonary tuberculosis (71%), neutropenia (71%), anemia (57%), diabetes mellitus (57%), and abdominal surgery (57%) [Table 1]. The comparative analysis of risk factors associated with C. albicans and NAC depicted P < 0.0001 (significant P < 0.05) for four variables, i.e., stay in ICU ≥10 days, respiratory tract infections, intake of steroids, and preterm newborn with LBW [Table 2].
Table 1: Risk factors associated with Candida albicans and Non albicans Candida

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Table 2: Comparative analysis of risk factors associated with Candida albicans and Non albicans Candida (n=94)

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Disk diffusion analysis revealed the sensitivity of fluconazole and voriconazole as 73% and 77%, respectively, against C. albicans. The NAC, on the other hand, showed high resistance to fluconazole (86%) and voriconazole (74%). Polyene compound, amphotericin B, was found to be effective against both C. albicans as well as NAC with susceptibility of 91% and 89%, respectively [Table 3]. The overall mortality rate due to infection with Candida species was 27.6%. Mortality was similar in patients infected with C. albicans and nonalbicans species (27.27% vs. 27.77%) [Figure 1]. The highest mortality among nonalbicans species was related to C. krusei infection (50%), followed by C. glabrata (30.76%) and C. tropicalis (10.71%) [Figure 2].
Table 3: Antifungal susceptibility pattern of 94 Candida isolates

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Figure 1: Overall mortality rate associated with various Candia Spp.

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Figure 2: Mortality rate associated with Non-albicans species (n=72)

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  Discussion Top


All the species of genera Candida are closely related, but differ with one another in pharmacology, prevalence, and virulence characteristics. NAC species, such as C. krusei, C. glabrata, C. parapsilosis, Candida Lusitaniae, and C. tropicalis which have a poor susceptibility to the frequently used antifungal drugs in clinical practices, have led to their emergence as substantial opportunistic pathogens in immune-compromised hosts.[9] Invasive Candida infections account for 70%–90% of all invasive mycoses. Unfortunately, early diagnosis of IC remains a challenge, and criteria for starting empirical antifungal therapy in ICU patients are poorly defined. Recent Infectious Diseases Society of America guidelines suggest that “empirical antifungal therapy should be considered in critically ill patients with risk factors for IC and no other known cause of fever.”[10] In the present study, we observed that nonalbicans species (77%) was encountered with greater frequency in comparison to C. albicans (23%). The results have been concordant with a study done by Deorukhkar et al. that showed a higher frequency of NAC (63.3%) in comparison to C. albicans (36.7%).[6] Bajwa and Kulshrestha have quoted that the isolation rate of NAC documented in India ranges from 52% to 96%, with C. tropicalis being the predominant species instead of C. glabrata or C. parapsilosis in all age groups. This increased incidence of NAC may be because of increased use of fluconazole prophylaxis in immunocompromised patients, central venous cannulations, and prior gastrointestinal surgery, and the resulting mortality due to IC can range from 40% to 60%.[11] Among nonalbicans species, C. tropicalis (39%) was isolated from majority of patients, which remained consistent with findings of Deorukhkar et al. and Kaur et al., who reported 35.1% and 41.1% of C. tropicalis among the NAC, respectively.[6],[12]C. tropicalis remains the most virulent among NAC species and this may be due to its ability to adhere to epithelial cells in vitro and its ability to secrete moderate levels of enzyme proteinase.[13]

The antifungal susceptibility testing revealed that amphotericin B exhibited a sensitivity of 91% and 89% against C. albicans and nonalbicans species, respectively, which points out that this drug can serve as a good candidate in empirical therapy of Candida infections. These findings remained in concordance with a study done by Kaur et al., who quoted that resistance rate was lower for amphotericin B (7.8%) with Candida isolates studied, and Mondal et al. reported that all the Candida isolates remained sensitive to amphotericin B.[12],[14] In the context of fluconazole, high resistance (86%) was observed for nonalbicans species whereas the efficacy remained fair for C. albicans with a sensitivity rate of 73%. Similar observations were noted for voriconazole which showed 77% sensitivity for C. albicans whereas 74% resistance in nonalbicans species. A number of factors may be responsible for the development of drug resistance observed in various clinical conditions. It is possible that higher minimum inhibitory concentrations in strains from patients who have received antifungal regimes in the past in either a consistent or inconsistent manner or widespread use of fluconazole within community care facilities might have facilitated the resistance to fluconazole. The epidemiology appears complex and varies among the different patient care units.[15]

The emergence of azole-resistant strains and advent of new antifungal drugs (new azoles and echinocandins) have made the use of fluconazole questionable as a first-line drug. Hence, identification of risk factors that facilitate distinction between C. albicans and NAC species infections shall be of great help to clinicians in choosing an empiric therapy against these candidal infections.[16] The risk factors identified in patients with C. albicans infection were administration of broad-spectrum antimicrobial therapy (82%), duration of stay in hospital ≥15 days (68%), respiratory tract infection (64%), anemia (64%), corticosteroids intake (64%), presence of indwelling devices (64%), neutropenia (36%), and pulmonary tuberculosis (32%). The results obtained were similar to those of Rodríguez et al., who reported prior antibiotics, hospitalization, length of stay in hospital, CVC placement, total parenteral nutrition, prior immunosuppressive drugs, surgery in previous 3 months as important risk factors associated with C. albicans.[17] Several risk factors related to Candida species infection have been identified among hospitalized patients, but there is a paucity of data pertaining to their differences between C. albicans and NAC. Hence, the present study shall provide additional information with further analysis of risk factors for NAC species and their final clinical outcome. The comparative analysis of risk factors associated with C. albicans and NAC depicted statistical significance (P < 0.05) for stay in ICU ≥10 days, respiratory tract infections, intake of steroids, and preterm newborn with LBW.

The factors responsible for acquisition of C. krusei in present study were stay in hospital ≥15 days (78%), administration of broad-spectrum antimicrobial therapy (72%), prophylactic fluconazole therapy (67%), stay in ICU ≥10 days (67%), presence of indwelling devices (67%), and mechanical ventilation (67%). The study done by Choi et al. has highlighted similar risk factors for C. krusei/C. glabrata as prolonged hospital stay 67 ± 50 (mean ± standard deviation [SD]) days, stay in ICU for 15 ± 31 days (mean ± SD), CVCs, parenteral nutrition, mechanical ventilation, use of prophylactic fluconazole.[18] In our study group, the most common risk factors for C. glabrata were administration of broad-spectrum antimicrobial therapy (69%), stay in ICU ≥10 days (62%), and presence of indwelling devices (62%). The current findings remained in concordance with observations of other researchers.[4],[5],[19] Preterm newborn with LBW (62%) had important episodes of C. glabrata. Newborns admitted to ICUs are at a greater risk of acquiring infections because of prematurity and further requirement of invasive medical equipment needed for their survival.[20] The patients infected with C. tropicalis revealed higher likelihood of the following risk factors in decreasing order, presence of indwelling devices (86%), and administration of broad-spectrum antimicrobial therapy (71%), whereas Hii et al. quoted broad-spectrum antibiotic exposure (88.6%) and placement of CVC (81.8%) as important predisposing factors associated with C. tropicalis infection.[21] Neutropenia (71%) as a risk factor was similar to Jordán et al., who mentioned that neutropenia (42.1%) was found to be more frequent among patients infected by C. tropicalis as compared to other species.[22] Hii et al. observed that neutropenia (27.3%) remained a less likely related risk factor in case of infection due to C. tropicalis in hospitalized patients.[21] Stay in ICU ≥10 days (71%), duration of stay in hospital ≥15 days (71%), diabetes mellitus (57%), and abdominal surgery (57%) were other risk factors that contributed to C. tropicalis infection. All these risk factors have been discussed in studies conducted by previous health-care researchers,[5],[23] except for pulmonary tuberculosis (71%), and anemia (57%) that remained in contrast to other studies. Non-Candida species are emerging as an important cause of infections in hospitalized patients throughout the globe; hence, their isolation from clinical specimens should not be overlooked as a contaminant rather their complete identification up to the species level, isolation, and evaluating therapies should become an integral part of clinical microbiology services.

Mortality was seen mainly in patients having multiple risk factors. The crude mortality rate due to infection with Candida species was 27.6%. Overall mortality was similar in patients infected with C. albicans and nonalbicans species (27.27% vs. 27.77%). The highest mortality among nonalbicans species was related to C. krusei infection (50%), followed by C. glabrata (30.76%) and C. tropicalis (10.71%). This is consistent with the findings of Klevay et al., and Bassetti et al., who observed that mortality did not differ by infecting species.[24],[25] There are several limitations pertaining to the current study. First, the study included retrospective analysis of clinical records which may be susceptible to reviewer bias. Second, the data were collected from an individual tertiary care institute resulting in limited sample size that could be further influenced by prevailing infection control practices, local outbreaks and varying drug susceptibility pattern in this specific region.


  Conclusion Top


Multiple risk factors were found to be associated with Candida species infection. Hospitalization, especially prolonged stay in ICUs, usage of broad spectrum antibiotics, placement of intravascular invasive lines and catheters were identified as important predisposing factors. With an ever-expanding array of non-Candida species-related infections in highly compromised and terminally ill patients, understanding the activity of the antifungal agents used against both C. albicans and nonalbicans species becomes mandatory. It is comforting to know that amphotericin B remains efficacious against both albicans and nonalbicans species. However, fluconazole has exhibited reduced activity, especially among NAC species, and resistance to voriconazole has also been encountered among those with acquired resistance to fluconazole. Continued surveillance of IC, both locally and on a regional as well as national level, is clearly warranted.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

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    Tables

  [Table 1], [Table 2], [Table 3]


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