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 Table of Contents  
Year : 2019  |  Volume : 6  |  Issue : 2  |  Page : 96-100

Diversity and clinical presentation of Candida species in human immunodeficiency virus patients with oral candidiasis

Department of Oral Medicine and Radiology, KLE Vishwanath Katti Institute of Dental Sciences, Belagavi, Karnataka, India

Date of Web Publication19-Aug-2019

Correspondence Address:
Dr. Arvind Shetti
Department of Oral Medicine and Radiology, KLE Vishwanath Katti Institute of Dental Sciences, Belagavi - 590 003, Karnataka
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/sjos.SJOralSci_74_18

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Background: Change in the distribution profile of nonalbicans Candida species (spp.) can be an indication of immunosuppression or drug resistance to oral candidiasis in patients with human immunodeficiency virus (HIV). Thus, it is essential to analyze the association of the profile of varied Candida spp.
Objective: The study aimed to collect the baseline data of diversity in the Candida spp. in HIV patients with oral candidiasis and correlate it with clinical presentations.
Materials and Methods: A total of 200 HIV patients with CD4 count<200 cells/μL were included in the study. A presumptive diagnosis of oral candidiasis was made, and different clinical forms of candidiasis were recorded. The oral swab samples collected from the patients were sent to the microbiological laboratory for culture. Different Candida spp. were isolated, and an association was analyzed with various variables, including clinical presentation, CD4 count, and duration of antiretroviral therapy (ART). A correlation between CD4 count and ART duration was also assessed.
Results: Pseudomembranous candidiasis was the most (46.50%) prevalent type identified in HIV patients. Candida albicans was the most prevalent (68%) spp. in HIV patients. Clinical form of candidiasis was significantly associated with isolated spp. (P < 0.00001). CD4 counts (P < 0.001) and ART (P = 0.03) duration significantly differed among clinical forms of candidiasis. ART duration was significantly correlated with CD4 count (r = 0.18; P = 0.01).
Conclusion: The study suggests the significance of various Candida spp. in the prediction of disease progression and immune suppression levels in HIV-infected oral candidiasis patients. Intensifying the concentration of nonalbicans spp. isolated in these studies predicts the change in immune status.

Keywords: Antiretroviral therapy, candidiasis, CD4 count, human immunodeficiency virus, pseudomembranous candidiasis

How to cite this article:
Nair V, Shetti A. Diversity and clinical presentation of Candida species in human immunodeficiency virus patients with oral candidiasis. Saudi J Oral Sci 2019;6:96-100

How to cite this URL:
Nair V, Shetti A. Diversity and clinical presentation of Candida species in human immunodeficiency virus patients with oral candidiasis. Saudi J Oral Sci [serial online] 2019 [cited 2023 Mar 27];6:96-100. Available from: https://www.saudijos.org/text.asp?2019/6/2/96/264770

  Introduction Top

Oral candidiasis is considered as one of the most common opportunistic fungal infections in patients infected with human immunodeficiency virus (HIV). The spectrum of candidiasis ranges from asymptomatic colonization to oropharyngeal candidiasis (OPC), onychomycosis, esophagitis, vulvovaginitis, cutaneous candidiasis, and invasive candidiasis or systemic candidiasis, including candidemia.[1] Among these, OPC is often considered as the first clinical sign of HIV-infected patients.[2] The low levels of absolute CD4 count are generally considered the baseline predictor of disease progression, which has been attributed as the greatest risk factor in the development of OPC.[3]

The global prevalence of OPC among HIV patients is 80%–95%, in which Candida albicans is the most common causative agent.[1] Candidiasis is generally attributed to a decline in the host immune system. An alteration in the distribution profile of Candida species (spp.) could be indicative of drug resistance or immunosuppression in a selected population.[4] It could be a sensitive and specific marker for decrease in the number of CD4 cells and might indicate the onset of substantial immune deficiency in patients with HIV. Other Candida spp., such as Candida glabrata, Candida krusei, and Candida Dubliniensis, are also associated with oral candidiasis in HIV patients.[4] Emergence of these resistant strains points toward a reduced antifungal susceptibility in the oral cavity. This can be attributed to the prolonged use of antifungal agents, which could predispose to a shift in nonalbicans spp. associated with refractory and recurrent infections.[5],[6] OPC increases morbidity and mortality and further diminishes the quality of life in HIV patients.[7] Therefore, unrecognized and inappropriately managed HIV patients are susceptible to drug resistance and further impede the care of patients.[8]

Oral infection with Candida can result in several clinical forms, including pseudomembranous candidiasis, erythematous candidiasis, hyperplastic candidiasis, and angular cheilitis.[9] A thorough clinical examination and exfoliative cytology is required to diagnose these forms of candidiasis. Although there are several studies on the diversity of Candida spp., there is a dearth in studies regarding the association of varied Candida spp. profile with clinical forms of candidiasis.[10] Hence, the objective of the present study was to collect a baseline data of Candida spp. diversity in HIV patients with oral candidiasis and associate it with the clinical forms.

  Materials and Methods Top

Study design

The present cross sectional study was conducted between January 2014 to July 2015 in the Department of Oral Medicine and Radiology, KLE Vishwanath Katti Institute of Dental Sciences Belagavi, Karnataka, INDIA. After obtaining the Institutional ethical clearance and written consent from the patient, a total of 200 confirmed cases of oral candidiasis of either gender were recruited for the present study in the following manner: Oral medicine and radiology (OPD), HIV treatment center run by local NGO and Anti retro viral therapy (ART) center at Government hospital, Belagavi.

Selection criteria

Patients previously diagnosed with HIV with CD4 count<200 cells/μL were included in the study. Patients suffering from systemic illness (e.g., diabetes mellitus) and immunocompromised conditions (e.g., diabetes mellitus and transplant recipients) other than HIV-infected patients were excluded from the study. Patients who received corticosteroid and antifungal therapy were also exempted.

Data collection

Demographic data, detailed case history, including habits, and extra- and intraoral examination of all the patients were recorded. Candidiasis was grouped into four clinical types: pseudomembranous candidiasis (thrush), atrophic/erythematous candidiasis, angular cheilitis candidiasis, and hyperplastic candidiasis. Intraoral photographs of the lesions for all the participants were also obtained.

Sample collection

Oral swabs were collected from the patients under aseptic conditions, cultured onto Sabouraud dextrose agar, and incubated at 35°C–37°C for 48 h in the microbiological laboratory and processed to ascertain Candida infection. The Candida isolates, thus, obtained were identified and characterized based on colony characteristics, morphology on corn meal agar, and the color of the colony on HiCrome agar.[11]

Statistical analysis

Data were pooled and coded into a Microsoft Excel spreadsheet. SPSS 21 (IBM corp, Chicago, Illinois, United states) was used to analyze the data. The categorical data were represented in the form of frequencies and compared using Chi-square test. Continuous data were represented in the form of mean ± standard deviation. Pearson's correlation was performed to assess the correlation of duration of ART with CD4 cell count. P < 0.05 was considered statistically significant.

  Results Top

The mean age of the study patients was 32.09 ± 8.44 years. The demographic and clinical profile of the study patients is given in [Table 1]. Most of the patients in our study were aged between 31 and 40 years (40%) with a slight male preponderance (52%). Of all HIV patients assessed, 152 patients showed Candida-associated lesions inside the oral cavity. The most prevalent type of candidiasis identified in HIV patients was the pseudomembranous type [46.50%; [Figure 1].
Table 1: Demographic and clinical profile of the study patients

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Figure 1: Patients showing (a) atrophic candidiasis, (b) hyperplastic candidiasis, (c) pseudomembranous candidiasis

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A total of 164 Candida isolates were obtained from 152 patients. Seven different Candida spp. were identified, wherein C. albicans (136) was the most prevalent form in HIV patients [Figure 2].
Figure 2: Prevalence of isolated Candida species

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The association between clinical diagnosis and isolated species is given in [Table 2]. C. albicans and Candida tropicalis were the most commonly isolated species from all the four clinical types of candidiasis. A significant association was observed between the clinical forms of candidiasis and the species isolated (P < 0.00001).
Table 2: Association of clinical diagnosis with species isolated

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CD4 count (P < 0.001) and ART duration (P = 0.03) significantly differed among different clinical forms of candidiasis. CD4 count (174.18 ± 20.53 cells/μL) and ART duration (0.43 ± 0.70 years) were significantly higher in HIV patients with angular cheilitis candidiasis and atrophic candidiasis, respectively [Table 3]. Further, ART duration was significantly correlated with CD4 count (r = 0.18; P = 0.01).
Table 3: Comparison of clinical diagnosis with CD4 count and antiretroviral therapy duration

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  Discussion Top

Studies evaluating changes in the distribution of Candida spp. in relation to the progression of HIV disease are of great importance and should be carried out in many regions across India. Hence, the present study was conducted to evaluate a comprehensive prevalence of these clinical forms of oral candidiasis in a large sample. The current study revealed exhaustive data regarding the prevalence of candidiasis along with species diversity and common clinical presentation of candidiasis in HIV-infected patients in the Belagavi district.

Oral candidiasis is the first clinical sign of progression toward acquired immune deficiency syndrome in HIV patients. Literature has reported that HIV-infected oral candidiasis patients have 2.5 times more progressive risk toward acquired immune deficiency syndrome than HIV patients without oral candidiasis.[12] Hence, the profile of candidiasis aids in the better prognosis of patients with HIV.

Most of the patients in our study were aged between 31 and 40 years with a slight male preponderance. These demographic variables correlate well with the similar studies conducted on HIV patients across India.[3],[13] The prevalence of oral candidiasis in the present study was consistent with other similar studies conducted worldwide.[3],[14],[15] The CD4 count<200 cells/μL was used as a predictor for OPC; therefore, patients in this range of CD4 count were included in the study. A study by Annapurna et al.[16] revealed that 80% of HIV-infected patients had oral manifestations, of which 88% of the patients had CD4 count<200 cells/μL.

In our study, four different forms of candidiasis were studied to isolate different species/strains of Candida causing oral candidiasis. Of four different clinical forms of candidiasis, pseudomonous type (46.50%) being the most prevalent form. A study conducted by Berberi et al.[13] also reported that pseudomembranous (52.6%) was the prevalent clinical form followed by atrophic erythematous (13.15%) and angular cheilitis (13.15%) candidiasis.

C. albicans (68%) was the most prevalent Candida spp. isolated in our study followed by other nonalbicans, which included C. tropicalis (7.5%) and C. glabrata (2.5%). Some of the recent studies [13],[17],[18] depicted similar species, whereas a study conducted by Castro et al.[19] reported C. dubliniensis as the prevalent species in HIV patients with oral candidiasis.

A study conducted by Kwamin et al.[15] reported a distribution of 20 different species in their sample. The change in the distribution profile of Candida spp. was attributed to the disease progression and immunological status of the population. Although C. albicans is the prevalent strain in oral candidiasis patients, identification of other Candida spp. is important as well. The strains of Candida spp. differ widely, both in their ability to cause infection and susceptibility pattern to different antifungal agents.[20] Therefore, in our study, various Candida spp. causing oral candidiasis were studied. A study conducted by Spalanzani et al.[21] in 60 seropositive HIV patients reported no significant correlation between Candida spp. isolated and clinical presentation of oral lesions. Whereas, our study reported a significant association between clinical forms of candidiasis and candida spp. isolated.

In our study, all the isolated species had inherent antifungal resistance, which is a point of concern. Therefore, in future, studies should focus on isolating each of these species and testing their antifungal sensitivity. In addition, more in vitro studies should be performed to understand the intricate pathogenesis of these nonalbicans species. Antifungal sensitivity testing was beyond the scope of this study due to larger sample size and shorter duration of the study. Further, studies eliciting antifungal sensitivity in a larger sample size should be conducted to acquire a wider array of distribution of species and antifungal susceptibility in a population.

  Conclusion Top

Overall, the present study suggests the significance of various Candida spp. in the prediction of disease progression and immune suppression levels in HIV-infected oral candidiasis patients. Greater amount of isolated nonalbicans species points toward a change in the immune status of the patients. Moreover, future studies should develop positive clinical predictive parameters to monitor the long-term effectiveness of ART and establish guideline protocols to help maintain its long-term effectiveness. A shift in Candida spp. distribution profile would point toward the immune status of the population and in turn the effectiveness of ART therapy. Outcomes may be difficult to generalize due to a variety of confounding factors. Future follow-ups are necessary to assess significant shifts in the distribution of Candida spp., which can aid in evaluating HIV treatment regimens.

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Conflicts of interest

There are no conflicts of interest.

  References Top

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Anwar KP, Malik A, Subhan KH. Profile of candidiasis in HIV infected patients. Iran J Microbiol 2012;4:204-9.  Back to cited text no. 3
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World Helath Organization. AIDS Epidemic Update. December 2009. Switzerland: World Helath Organization Regional Office Europe; 2009 Available from: http://data.unaids.org/pub/Report/2009/JC1700_Epi_Update_2009_en.pdf. [Last accessed on 2017 Feb 23].  Back to cited text no. 6
Shyamala R, Parandekar PK. Identification and in vitro azole resistance of Candida species isolated from Oropharyngeal candidiasis in human immunodeficiency virus infected patients. Int J Curr Microbiol App Sci 2014;3:816-22.  Back to cited text no. 7
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Devi LS, Maheshwari M. Speciation of Candida species isolated from clinical specimens by using Chrom agar and conventional methods. Int J Sci Res Pub 2014;4:1-5.  Back to cited text no. 11
Putranti A, Asmarawati T, Rachman B, Hadi U, editors. Oral Candidiasis as Clinical Manifestation of HIV/AIDS Infection in Airlangga University Hospital Patients. IOP Conference Series. Earth and Environmental Science. IOP Publishing; 2018.  Back to cited text no. 12
Berberi A, Noujeim Z, Aoun G. Epidemiology of oropharyngeal candidiasis in human immunodeficiency virus/Acquired immune deficiency syndrome patients and CD4+counts. J Int Oral Health 2015;7:20-3.  Back to cited text no. 13
Pruthvi B, Vikram S, Suman S, Jayaprakash B, Rau N. Spectrum of clinical presentation and opportunistic infections in HIV: An Indian scenario. Int J Infect Dis 2008;12:e484.  Back to cited text no. 14
Kwamin F, Nartey NO, Codjoe FS, Newman MJ. Distribution of Candida species among HIV-positive patients with oropharyngeal candidiasis in Accra, Ghana. J Infect Dev Ctries 2013;7:41-5.  Back to cited text no. 15
Annapurna CS, Prince CN, Sivaraj S, Ali IM. Oral manifestations of HIV patients in South Indian population. J Pharm Bioallied Sci 2012;4:S364-8.  Back to cited text no. 16
Thompson GR 3rd, Patel PK, Kirkpatrick WR, Westbrook SD, Berg D, Erlandsen J, et al. Oropharyngeal candidiasis in the era of antiretroviral therapy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;109:488-95.  Back to cited text no. 17
Sharifzadeh A, Khosravi AR, Shokri H, Asadi Jamnani F, Hajiabdolbaghi M, Ashrafi Tamami I. Oral microflora and their relation to risk factors in HIV+patients with oropharyngeal candidiasis. J Mycol Med 2013;23:105-12.  Back to cited text no. 18
Castro LÁ, Álvarez MI, Martínez E. Pseudomembranous candidiasis in HIV/AIDS patients in Cali, Colombia. Mycopathologia 2013;175:91-8.  Back to cited text no. 19
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Spalanzani RN, Mattos K, Marques LI, Barros PF, Pereira PI, Paniago AM, et al. Clinical and laboratorial features of oral candidiasis in HIV-positive patients. Rev Soc Bras Med Trop 2018;51:352-6.  Back to cited text no. 21


  [Figure 1], [Figure 2]

  [Table 1], [Table 2], [Table 3]


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