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 Table of Contents  
ORIGINAL ARTICLE
Year : 2012  |  Volume : 1  |  Issue : 3  |  Page : 132-138

Antibiogram of candida species isolated from mono and multi-species oral candidal carriage using disk diffusion method


1 Department of Microbiology, Modern Dental College and Research Centre, Indore (M.P.), India
2 Department of Pathology, Modern Dental College and Research Centre, Indore (M.P.), India

Date of Web Publication15-Jan-2013

Correspondence Address:
Apurva K Pathak
Department of Microbiology, Modern Dental College and Research Centre, Indore (M.P.)
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2278-0521.106082

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  Abstract 

Context: Oral candidiasis is the most common oral opportunistic infection has seen in the immunocompromised patients. Apart from C. albicans the non-Candida albicans Candida species, which are less susceptible to the commonly used antifungal drugs are major etiological agent for candidiasis. Thus, the treatment strategy for candidiasis should be different in case of multiple species infection. Aims: The aim of this present study is to compare the antifungal susceptibility patterns of Candida species isolated from mono species and multiple species oral Candidal carriage. Materials and Methods: The species of Candida, isolated from mono and multiple species oral Candidal carriage of the healthy and immunocompromised patients were used for the experiment. Antifungal susceptibility test was performed by using disk diffusion susceptibility method on Methylene blue Glucose- Mueller-Hinton agar. Statistical Analysis Used: Paired student's t-test. Results: In this, present study, variability in antibiogram of Candida species isolated from mono species and the corresponding species isolated from multiple species combinations were reported. The susceptibility ranking for antifungal drugs for the strain isolated from mono species OPC (C. albicans > C.tropicalis > C. glabrata > C.krusei) and for the strains isolated from multiple species combination (C. albicans > C. glabrata > C.krusei > C.tropicalis) for mean of the five antifungal drugs combined were reported. Species of C. albicans and C. tropicalis were reported more resistant towards anti fungal agents when these present in mono-species condition, whereas; C. krusei and C. glabrata were more susceptible when these present in mono-species condition. Polyenes (amphotericin-B and nystatin) compounds were found to be most effective than azoles against Candida spp. isolated from multi-species lesions as none of the strain were shown resistant towards these drugs, conversely; a significant fraction of C. tropicalis and C. albicans isolated from mono-species lesion were shown resistant toward polyenes compound tested. Conclusions: The findings of this study shows statistically insignificant diverse antifungal susceptibility pattern of Candida species isolated from mono and multiple species Oropharyngeal Candidiasis combinations.

Keywords: Antifungal drug, candidiasis, disk diffusion test, multiple species, resistance


How to cite this article:
Pathak AK, Jain NR, Joshi R. Antibiogram of candida species isolated from mono and multi-species oral candidal carriage using disk diffusion method. Saudi J Health Sci 2012;1:132-8

How to cite this URL:
Pathak AK, Jain NR, Joshi R. Antibiogram of candida species isolated from mono and multi-species oral candidal carriage using disk diffusion method. Saudi J Health Sci [serial online] 2012 [cited 2019 Apr 25];1:132-8. Available from: http://www.saudijhealthsci.org/text.asp?2012/1/3/132/106082


  Introduction Top


Candida spp. lives commensally in the human oral cavity with high carriage rate (>70%); responsible for candidiasis, the most common opportunistic infection has seen in the immunocompromised patients. Although, C. albicans is the predominant etiologic agent of candidiasis, numerous records indicated that epidemiology of candidemia has changed with increased incidence of non-Candida albicans Candida species among immunocompromised patients. The cause of changes in these causative agents of candidiasis is probably due to environmental selection pressure, which arises in due course of inappropriate antifungal therapy or some other reasons. [1],[2],[3],[4] All the species of genera Candida are closely related; but differ with one another in pharmacology, prevalence and virulence characteristics. Non-Candida albicans Candida species that have a tendency to be less susceptible to the frequently used antifungal drugs in clinical practices, such as C. krusei, C. glabrata, C. parapsilosis, C. lusitaniae and C. tropicalis, have emerged as substantial opportunistic pathogens in immunocompromised patients. [5]

One of the major factors contributing to the virulence of Candida is its adaptability to a variety of environment or its ability to create its own micro-environment by the formation of sessile, but physiologically active surface attached communities known as 'biofilms'. Biofilms are defined as co-aggregation of microbial communities, which are encased in slime, and exhibiting phenotypic features that differ with their planktonic unicellular forms. [6],[7] Previous workers have suggested that more than one species or even strain of Candida can cohabitate the same site of infection. [8],[9],[10],[11] Multispecies Candida biofilms could serve as a safe reservoir for the release of infecting cells i.e., persisters into the oral or other environment; biofilm formation by the antifungal drug resistant Candida species represents a key factor in the survival of non-resistant Candida, with important clinical repercussions. [7],[12],[13] Moreover; biofilm-associated Candida show uniform resistance to a wide spectrum of antifungal drugs, and irrespective to their pathogenic state and under multi-species condition the biofilms forming ability of Candida species varied with varying combination. [12] Since, the environmental factors influence the expression of genes in Candida species; [14] the presence of one or more intrinsically resistance organism in multi-species Candida biofilms may influence the antifungal susceptible patterns of other species. Thus, the antifungal susceptibility test must be performed before starting medication.

The disk diffusion method of sensitivity testing used for testing both antibiotics and drugs is relatively simple, reliable, reproducible and commonly used, can be useful to initiation preventive antifungal therapy, [15] nevertheless; antifungal disk diffusion tests are generally not used for the selection and monitoring of antifungal therapy. [16],[17] The National Committee for Clinical Laboratory Standards (NCCLS) M27-A, recommend microtiter method for antifungal susceptibility testing used planktonic unicellular forms of yeasts. [18],[19] However, minimum inhibitory concentration, which involves growth inhibition, is not suitable to determine the drug susceptibility of biofilms, as the species of Candida found in biofilms are reportedly more resistant to antifungal drugs compared to its planktonic unicellular forms. [20],[21],[22],[23],[24] Resistance towards most of the common antifungal drugs were emerging, thus, rapid in vitro antifungal susceptibility test is required to guide the selection of antifungal chemotherapy for successful clinical management particularly in the case of mixed Candida infection. [17],[19]

The objective of this study was to evaluate the in-vitro antifungal susceptibility patterns of Candida species isolated from the oral cavity of the patients with mono-species and multi-species (Mixed Candida infection) Candida carriage by using disk diffusion susceptibility method and compare the antifungal susceptibility patterns of Candida species isolated from mono-species and multi-species infection by using the paired Student's t-test.


  Materials and Methods Top


Organisms

The test organisms include randomly selected 80 Candida spp. of four different species of Candida i.e., C. albicans, C. krusei, C. glabrata and C. tropicalis (n = 10 each) from mono-species and multi-species carriage, isolated from the oral cavity of neutropenic patients (absolute neutrophil count <1.5 × 10 9 cells/L) (20 from mono-species carriage and 32 from multi-species carriage out of 146 sample received) and from denture wearer healthy patients (20 from mono-species carriage and 8 from multi-species carriage out of 63 sample received) by using previously described oral rinsing techniques. [25] The identification of Candida species was conducted by culture characteristics on HiChrome Candida agar medium (HiMedia, Mumbai, India), growth at 45°C, assessing germ tube, chlamydospore formation and sugar assimilation patterns. Quality control was performed as stated by the manufacturer using, C. albicans (ATCC 10231) and C. krusei (ATCC 6258), obtain from KWIK-STIK, HiMedia, Mumbai, India, with a recommended acceptable performance range for selected antifungal drugs. The patients from whom the specimens were collected have not been exposed prior to antifungal drugs.

Antifungal susceptibility testing

We used a previously described disk diffusion assay to test all yeast isolates. [17],[26],[27],[28] Classes of agents used in the treatment of Oropharyngeal Candidiasis include the polyenes, pyrimidine synthesis inhibitors, azoles and echinocandins. [29] Candida species were shown limited resistance to the polyenes and it is considered a "gold" standard for the treatment of mucosal candidiasis; whereas, triazoles which are less toxic than polyenes and can be administered orally are the drug of choice and considered a reasonable alternative. However, intrinsically resistance to imidazoles and triazoles is common in some of the Candida species.

In this study, the most preferred class of antifungal agents like polyenes and azoles were included; the test disks contained amphotericin-B (100 Units), nystatin (100 units), clotrimazole (10 μg/mL.), fluconazole (25 μg/mL.), and itraconazole (10 μg/mL.) (HiMedia, Mumbai, India) were used, stored in desiccators at 4°C. Inoculums were prepared by picking five distinct colonies of approximately one mm from each 24 hours old culture grew on Sabouraud Dextrose Agar (HiMedia, Mumbai, India) and incubated at 35 ± 2°C. Colonies were suspended in 5 mL of sterile 0.85% Saline. Vortexes the resulting suspension and adjusted the turbidity to yield 1 × 10 6 - 5 × 10 6 cells/mL (i.e., 0.5 McFarland standard). A sterile cotton swab moistened with the inoculums suspension was used to apply to a 90 mm diameter plate containing Mueller-Hinton agar (HiMedia, Mumbai, India) supplemented with 2% glucose and 0.5 μg/mL methylene blue (GM-MH agar medium). The plates were allowed to dry for 5-15 minutes before disks were placed in the center of the agar. The plates were incubated for 18-24 hours at 37 ± 2°C and the slowly growing isolates were again read after 48 hours incubation. Zone sizes were measured in millimeters with Zone Scale (HiMedia, Mumbai, India), the zone diameter to the nearest whole millimeter the point at which there is prominent reduction in growth were taken into consideration. Pinpoint micro-colonies at the zone edge or large colonies within the zones were ignored when testing the azoles. [30],[31],[32] The result was further verified with minimum inhibitory concentration (MIC) test by using HiComb disk (HiMedia, Mumbai, India) of amphotericin-B (0.002-32 μg), fluconazole (0.016-256 μg) and itraconazole (0.002-32 μg) according to manufacturer instruction (HiMedia, Mumbai, India).

All the disk diffusion experiments were repeated twice and mean with standard deviation were taken. In order to interprets the result we used the NCCLS zone interpretative criteria for susceptible (diameter, ≥19 mm), resistant (diameter, ≤14 mm), or susceptible-dose dependant (diameter between 15 and 18 mm) for fluconazole. During present study, for other drug-organism combinations a zone size ≤12 mm or the zone of less than 2 mm ( <2 mm) radius were considered as a resistance against the zone size of sensitive control culture of the standard strains, lowest zone size was taken into account (HiMedia, Mumbai, India). All the tested species of Candida grew well on the GM-MH agar medium at 18-24 h. with a well-demarcated layer of growth with clear zone of inhibition. If, the zone size varied in its 24 h. and 48 h. measurements, maximum size of zone was taken into account. [33]

Statistical analysis

Zone sizes obtained by using disk diffusion experiments for Candida species, were compared by the paired Student's t-test by using the SPSS Win 12.0 program (SPSS Inc, Chicago, U.S.A.). Differences in the zone size between isolated strain from mono-species and its multi-species combinations were considered significant for P of 0.05. The null hypothesis (HO) rejected in favor of the alternative hypothesis (H1) at significance level α (0.05) if; T > t n-1, α/2 (value of the Student table with n -1 degrees of freedom). The null hypothesis is H0: δ = 0 (there is a difference in zone of inhibition of antifungal disk among the tested species) and the alternative hypothesis is H1: δ = 0 (there is no difference in zone of inhibition of tested antifungal disk among the tested species). All the data were presented in the form of tables.


  Results Top


Eighty Candida species isolated from clinical samples and were used for this study. Amongst the 80 isolates, 10 each of C. albicans, C. glabrata, C . krusei, and C. tropicalis were used to test the antifungal susceptible patterns of the species of Candida isolated from mono-species and multi-species lesion. The range, mean and standard deviation of zone of inhibition of antifungal disk obtain by diffusion tests for different species of Candida is shown in [Table 1].
Table 1: Antibiogram of species isolated from mono species and multiple species lesion#


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Disk diffusion tests performed on mono-species lesion isolates of C. glabrata and C. krusei generated smaller inhibition zones than in the assays of C.albicans , and C. tropicalis strains. C . krusei from mono species lesion and C. tropicalis from multi-species lesion generated smallest inhibition zone. C. krusei shows highest standard deviation in zone size (S.D. ± 5.5) when it present in mono-species condition and lowest when it presents in multi-species combination (S.D. ± 1.2), when mean of the five antifungal drugs combined were taken.

Polyenes (amphotericin-B and nystatin) compounds were found to be most effective against Candida spp. isolated from multi-species lesions as none of the strain were shown resistant towards these drugs, conversely; 25% of C. tropicalis (n = 10) and 20% of C. albicans (n = 10) isolated from mono-species lesion were shown resistant toward polyenes compound tested. Maximum resistance toward azoles (clotrimazole, fluconazole, and itraconazole) were reported in the species of C. krusei (53%) and C. glabrata (47%) of multi-species lesions, however; C. krusei and C. glabrata (83% each) were found more susceptible than C. albicans (60%) and C. tropicalis (66%), when these were recovered from mono-species carriage, moreover; C. tropicalis (90%) isolated from multi-species carriage was displaying highest degree of susceptibility to azoles [Table 2].
Table 2: Susceptibility patterns to antifungal agents (values in percentage)


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The susceptibility ranking (from resistant to susceptible) for antifungal drugs for the strain isolated from mono-species (S) and multi-species (M) carriage combinations for mean of the polyenes drugs combined was C.tropicalis (S) > C.krusei (S) > C. krusei (M) > C. albicans (S) > C. albicans (M) > C. glabrata (M) > C.tropicalis (M) > C. glabrata (S); and for mean of the azoles drugs combined was C. krusei (M) > C. glabrata (M) > C. tropicalis (s) > C. glabrata (S) > C. tropicalis (M) > C. albicans (S) > C. krusei (S) > C. albicans (M) reported during the present study [Figure 1]. Species of C. albicans and C. tropicalis were reported more resistant towards anti fungal agents when these present in mono-species condition, whereas; C. krusei and C. glabrata were more susceptible when these present in mono-species condition.
Figure 1: Susceptibility ranking of Candida, species for azoles and polyenes compounds, (s): Species isolated from mono-species lesion, (m): Species isolated from multi-species lesion

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To test the hypothesis of no difference or no relationship between the size of zone of inhibition amongst isolated strain from mono species lesion and its multiple species lesion combinations paired t-test was performed [Table 3]. For all the four pairs of Candida spp. and a pair of mean of the polyenes and azole compounds, 100% of pairs rejected null hypothesis in favour of alternate hypothesis; it means that there is no significant difference between the mean values of the size of zone of inhibition of isolated strains from mono species lesion and its multispecies lesion combinations. The level of significance is low for C.tropicalis, C. glabrata and C.krusei and high for C. albicans proven that non Candida albicans Candida strains isolated from multiple species combinations show variable resistance towards antifungal drugs tested.
Table 3: Paired samples student's t-test test$


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  Discussion Top


Candida species are ubiquitous colonizers of human mucosal surfaces; they are the part of the normal microbial flora of human oral cavity. [34] These, normal microbial floras adapt a pathogenic role under compromised conditions and manifested in number of distinct clinical forms collectively known as candidiasis or moniliasis. In Human, species of Candida producing broad range of infection ranging from most common superficial infection of the oral cavity or vagina, that involves the formation of whitish mucoid plaques known as biofilm on the mucous membranes; to acute or chronic invasive infection affecting single organ or disseminated resulted into candidaemia. Carriage of multiple species is a common phenomenon encountered in oropharyngeal candidiasis with a prevalence rate of 2-36%. [35],[36] In a study made by Coco et al., suggested that co-existence of mixed species in biofilms could aggravate the clinical condition, that further complicate the treatment modalities. [36],[37]

Instead of prevalence study, the primary aim of the present study was to evaluate the difference in susceptibility pattern in the clinical isolates of different strains of Candida species against various antifungal drugs by using rapid test like disk diffusion method. According to Espinel-Ingroff, the zone interpretive criteria (breakpoints) are only available for fluconazole and voriconazole, therefore, the clinical relevance for any other drug-organism combinations are uncertain. [38] However considering that, disk-diffusion assays are simple to perform and inexpensive, it may be an useful tool in large-scale surveys of clinical isolates to identify population distribution patterns of susceptibility to antifungal substances, and even more some reports has been suggested that it is reproducible and rapid. [15],[39],[40]

Higher prevalence of fungal infection corresponds with marked increase in the use of antifungal agents. Amphotericin-B, nystatin and clotrimazole were applied topically for oral fungal infection, whereas; triazole can be administered orally that include fluconazole and more efficacious itraconazole. Fluconazole, which has the widest therapeutic index of the azoles, was the drug of choice for the treatment of mucosal candidiasis since 1980s. For the first time in 1992, resistance towards fluconazole treatment in AIDS patients with oral or oesophageal candidiasis were reported from European countries. [41] Subsequently, Candida albicans and the species of non Candida albicans Candida with unusual antifungal susceptibility profiles have been reported world-wide.

In this study, disk diffusion analysis results showed that, 14% of Candida isolates were resistant to antifungal drugs; 19% of Candida isolates were resistant to azole and of which C. krusei account 47% and C. glabrata account 31%, isolated from both types of carriage, whereas; only 6% of strains isolated from both the carriage were resistant to polyenes compounds belongs to C. albicans and C. tropicalis (3% each). Both the C. kruzei and C. glabrata was intrinsically and cross-resistant to azole compounds. [5],[42] Previous study have been reported resistance in C. glabrata to azole compounds was ranging from 3.6% to 64% among the species isolated from mucosal candidiasis, and no species were reported resistant to polyenes compound, is similar to present findings and difference in results of azoles (0% mono-species condition), may attributed to methods of test applied. [43],[44] Sαnchez-Vargas et al., reported the prevalence of Candida spp. resistant to azole antifungal of 18.7%, in Human Immunodeficiency Virus-infected and healthy Maxicans with oral candidiasis or carriage; they have also reported that, there is no correlation established between resistant patterns of antifungal agents with its virulence, is similar to the present findings. [45]

During present study, there was a non-significant correlation established between antifungal susceptibility patterns of Candida species isolated from mono species with the type of multiple species carriage; the student t-test also reported variability in antibiogram of Candida species isolated from mono species and the corresponding species isolated from multiple species carriage. This variability was observed higher in non-Candida albicans Candida species than the strains of Candida albicans that was probably due to the fact that the disk diffusion method, endorsed by NCCLS, for fluconazole, showed poor correlation for non-Candida albicans Candida isolates. [17]

It has previously been demonstrated that more than one strain can colonize the same individual and different switch phenotypes of the same strain can cohabit the same site of infection. [13],[40],[46] Pfaller et al., were also reported diversity in the species distributions of Candida spp. and variation in antifungal resistance patterns while studying isolates from individuals in the paediatric and adult age groups. [47] In this study, there is marked variation between antifungal resistances among the species isolated from different individuals both from mono and from multiple species carriage were reported, which are similar to previous findings. [40]

Based on the results of this study, a diverse antifungal susceptibility pattern of Candida species isolated from mono and multiple species carriage were reported, however; it is statistically insignificant (Sig. 0.3063; [Table 2] and [Table 3]). One of the most significant features of Candida sp. is that it form biofilms in vivo, biofilms provides resistance to a variety of antimicrobial agents, and these organisms could become the source of systemic infection. [48] Presence of two or more species in a biofilms could aggregate virulence factors. Synergistic affects of these factors can pose major problems to the clinicians. [12] Thus, the management strategy for candidiasis should be different in case of multi-species infection, and it must be supported by mycological investigation.

 
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    Figures

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    Tables

  [Table 1], [Table 2], [Table 3]


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