82

Dental Journal
(Majalah Kedokteran Gigi)

2021 June; 54(2): 82–86

Original article

The antifungal susceptibility of Candida albicans isolated from 
HIV/AIDS patients

Sri Rezeki1, Siti Aliyah Pradono2, Gus Permana Subita2, Yeva Rosana3, Sunnati4 and Basri A. Gani5
1 Department of Oral Medicine, Faculty of Dentistry, Universitas Syiah Kuala, Banda Aceh, Indonesia
2 Department of Oral Medicine, Faculty of Dentistry, Universitas Indonesia, Jakarta, Indonesia
3 Department of Microbiology, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia
4 Department of Periodontics, Faculty of Dentistry, Universitas Syiah Kuala, Banda Aceh, Indonesia
5 Department of Oral Biology, Faculty of Dentistry, Universitas Syiah Kuala, Banda Aceh, Indonesia

ABSTRACT
Background: Candida albicans was found to be dominant in patients with human immunodeficiency virus / acquired immunodeficiency 
syndrome (HIV/AIDS). The antifungals fluconazole, ketoconazole, and nystatin were used as oral candidiasis therapy for HIV/AIDS, 
each of which has differing susceptibility in oral candidiasis therapy. Purpose: The present study aimed to evaluate the susceptibility 
and antifungal resistance to oral C. albicans in HIV/AIDS patients. Methods: The subjects followed the universal precaution principles. 
Oral Candida species were isolated from the saliva of 98 HIV/AIDS subjects. Identification of Candida species was carried out by 
the mycobiotic agar of API 20 C Aux system. Susceptibility and resistance antifungal tests on the Candida species were performed 
using a Fungus ATB Kit. Results: Candida albicans was the most dominant species found from 98 subjects (95%). The rest were 
other Candida species. There are 41 subjects (42%) with a history of oral candidiasis, and 57 subjects (58%) without. The history of 
those who used antifungals were: nystatin = 60 subjects (61%), fluconazole = 39 subjects (40%), and ketoconazole = two subjects 
(2%). These antifungals have a susceptibility above 80% against C. albicans, except the nystatin group (79%) (p>0.05; 0.628), but 
fluconazole has a strong correlation (r=0.820) to susceptibility, susceptibility-dependent dose, and resistance. Conclusion: Candida 
albicans was dominant in the saliva of HIV/AIDS patients. This fungus was effectively treated by fluconazole, ketoconazole and nystatin. 
These antifungals had a high susceptibility at ≤ 8 μg/mL to C. albicans.

Keywords: antifungal; Candida albicans; HIV/AIDS; susceptibility and resistance

Correspondence: Sri Rezeki, Department of Oral Medicine, Faculty of Dentistry, Universitas Syiah Kuala. Jl. Teuku Nyak Arief 
Darussalam, Banda Aceh, 23111 Indonesia Email: iy_99fkg@unsyiah.ac.id

INTRODUCTION

In Indonesia (data 2005–2019), the number of people 
living with human immunodeficiency virus (HIV) was  
338,363. Meanwhile, an acquired immunodeficiency 
syndrome (AIDS) was reported in 115,601 cases.1 One 
of the conditions experienced by people with HIV/AIDS 
is mucosal candidiasis in the oral, esophageal, or vaginal 
regions. The circumstances of oral candidiasis in HIV 
infections vary from 7% to 93%, depending on the patient 
mix, diagnostic criteria, and research methods.2 It is 
considered an important marker of immune decline as an 
early manifestation of HIV infection. In addition, there is 
a decrease in CD4 lymphocyte cells <200.3

Oropharyngeal and esophageal candidiasis are 
common manifestation in HIV patients. The disease 
is caused by C. albicans and other oral Candida 
species. Antiretroviral therapy (ART) can reduce the 
prevalence of oropharyngeal and esophageal candidiasis 
in refractory disease.4 The resistance of fluconazole 
or azole is influenced by repeated long-term exposure.                                                                                                   
In this permutation, the majority of cases relate to the 
acquisition of resistance to C. albicans.5 Both local 
and systemic predisposing factors lead to Candida’s                      
commensal changes, developing into oral candidiasis. 
These infections of esophageal candidiasis, as well as 
morbidity, and even mortality, were reported as secondary 
complications.6

Dental Journal (Majalah Kedokteran Gigi) p-ISSN: 1978-3728; e-ISSN: 2442-9740. Accredited No. 32a/E/KPT/2017. 
Open access under CC-BY-SA license. Available at https://e-journal.unair.ac.id/MKG/index
DOI: 10.20473/j.djmkg.v54.i2.p82–86

mailto:iy_99fkg@unsyiah.ac.id
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83Rezeki et al./Dent. J. (Majalah Kedokteran Gigi) 2021 June; 54(2): 82–86

The antifungal drugs fluconazole, ketoconazole, 
and nystatin effectively treat HIV oropharyngeal and 
esophageal candidiasis. Therefore, their widespread 
use has the potential to increase C. albicans resistance. 
These antifungals, when observed in different groups of 
HIV patients, were resistant to C. albicans. One-third                          
of C. albicans HIV isolates were resistant to several 
antifungals.7 Mohamadi et al.8 revealed that C. albicans 
remains the most common species that rapidly developed 
into fluconazole, ketoconazole, and nystatin resistant. 
The resistance of these antifungals has an impact on 
dehydration, malnutrition, and increased HIV infection. It 
is often reported in cases of esophageal and oropharyngeal 
candidiasis. Monroy-Pérez et al.9 reported that fluconazole, 
ketoconazole, and nystatin have varying susceptibility to 
C. albicans. However, these three antifungals have the 
same principle action for inhibiting the development of 
C. albicans by damaging the cell walls and inhibiting 
synthesis protein.10

Susceptibility of fluconazole, ketoconazole, and 
nystatin to C. albicans in HIV/AIDS patients can be used 
as a reference for determining relevant and appropriate 
doses for HIV/AIDS oral candidiasis, which can reduce 
the prevalence of resistance. This study evaluated the 
susceptibility of antifungals to oral C. albicans isolates 
from HIV/AIDS patients.

MATERIALS AND METHODS

The research was approved ethical clearance by the Faculty 
of Dentistry, Universitas Syiah Kuala, Banda Aceh, 
Indonesia, No.187/KE/FKG/2020. Saliva was collected 
from 98 people with HIV/AIDS at the AIDS center of Cipto 
Mangunkusumo Hospital (RSCM), Jakarta, Indonesia. 
The isolation and characterization of Candida species 
from the samples were carried out at the Microbiology 
Laboratory, Faculty of Medicine, University of Indonesia. 
Criteria for inclusion were patients with HIV/AIDS who 
had not used antifungal drugs for the previous week, were 
communicative and were cooperative. The patients included 
male and female patients. Meanwhile, the exclusion criteria 
included people living with HIV/AIDS who have refused 
to be research subjects, who have used antifungal drugs 
for the past week, were non-communicative and were 
non-cooperative.

The subjects were asked to sign an informed consent, 
and questionnaire sheets were filled in with the subjects’ 
demographic data obtained from interviews. Interviews 
were conducted before sampling, and the medical records 
of subjects were obtained from the RSCM’s AIDS clinic, 
Jakarta, Indonesia. The researcher applied the sampling 
procedure to people with HIV/AIDS using personal 
protective equipment and precautions, such as gloves and 
masks, hand hygiene and sterility, disposing of medical 
waste contaminated with the saliva of research subjects, 
and applying laboratory work safety procedures.

The following oral rinse technique was used to collect 
the saliva: the subjects were instructed to rinse their 
mouths in 10 mL of phosphate buffer saline (PBS) (Sigma-
Aldrich, Darmstadt, Germany) for 15 sec. The saliva was 
then expectorated into sterile containers and stored at 
-25°C.11 Next, the oral saliva specimen was cultured on 
Mycobiotic® agar at 35°C for 48 h for identified a Candida 
species. 12  The suspensions of C. albicans cultured on 
the Mycobiotic® agar medium using 0.85% NaCl and 
adjusted to McFarland 2 (6 x 108 CFU/mL).13 Then, 100 
μL of Candida suspension in 0.85% NaCl was mixed to 
API 20 liquid medium. Then homogenization was carried 
out. Subsequently, 200 μl was taken and placed into a 
test vial. A fermentation assay was conducted on several 
carbohydrates in parallel. After 48 h of incubating at 30oC, 
a well-observed growth was taken randomly. A positive 
reaction was characterised by turbidity in each well 
observed after incubation at 30oC for 48 h.9

The Fungus ATB® commercial kit was used to evaluate 
the susceptibility test, with the maximal assay in 128 μg/mL. 
A 20 μL suspension of C. albicans in 0.85% NaCl was added 
to the Fungus ATB® media. After homogenisation, each 
well was inoculated with 135 μl of homogeneous inoculums 
and incubated at 37°C for 24 h. The growth of C. albicans 
on the strip was read visually, according to the instructions 
kit, with baseline turbidity as the indicator of the growth 
of C. albicans in fluconazole, ketoconazole and nystatin in 
concentrations of <1, 2, 4, 64, and >128 μg/mL, which was 
an indicator of susceptibility (≤8 μg/ml), susceptibility-dose 
dependent (S-DD) (16–64 μg/mL) and resistance (>128 μg/
mL). The growth of C. albicans characterised by turbidity 
relates to the ATB® kit: 0 (no growth), 1 (weak growth), 
2 (reduction in growth), 3 (growth reduced slightly), and 
4 (no reduction in growth).14

The Kruskal–Wallis test analysed the data of 
susceptibility, S-DD, and fluconazole-resistant against 
C. albicans. The significance limit of p<0.05 and the 
correlation coefficient (r = 1) was strongly correlated.

RESULTS 

Data from study subjects included in this study are 
shown in Table 1, representing age group, sex, history of                              
HIV/AIDS transmission, history of antifungal agents and 
oral candidiasis. These indicators could be the reference 
for this study, which also correlated with Candida species 
susceptibility.

C. albicans were found predominantly in HIV/AIDS 
subjects without a history of candidiasis (Table 2). Its 
antifungals were reported susceptible to C. albicans and 
other Candida species. The data from Table 2 refer to 
an in vitro assay related to antifungal susceptibility to                    
C. albicans, which were selected to represent the dominant 
population of Candida species from HIV/AIDS subjects.

Table 3 shows that the three antifungal drugs have 
a high susceptibility above 80%, but not significantly 

Dental Journal (Majalah Kedokteran Gigi) p-ISSN: 1978-3728; e-ISSN: 2442-9740. Accredited No. 32a/E/KPT/2017. 
Open access under CC-BY-SA license. Available at https://e-journal.unair.ac.id/MKG/index
DOI: 10.20473/j.djmkg.v54.i2.p82–86

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84 Rezeki et al./Dent. J. (Majalah Kedokteran Gigi) 2021 June; 54(2): 82–86

(p> 0.05; 0.628), which means that all drugs have a 
potential antifungal effect on C. albicans. Three antifungal 
drug concentrations showed significant differences in 
fluconazole’s susceptibility against C. albicans (p<0.05; 
0.024). It means that the concentration of the three drugs has 
a strong influence on fungicidal or fungistatic properties. 
The subject status was related to susceptibility, S-DD, and 

resistance of the three antifungal drugs against C. albicans 
(p> 0.05; 0.175). Based on Spearman’s rho correlation, drug 
status (susceptibility, S-DD, and resistance) has a strong 
relationship with the concentration of the three groups of 
antifungal drugs (r = 0.820). The standard susceptibility            
≤ 8 μg/mL, S-DD 16-64 μg/mL, and resistant ≥ 128 μg/mL 
is based on the ATB® Fungus kit.

Table 1. Distribution and frequency characteristics of HIV/AIDS subjects

Characteristics N %
Gender
   Female 10 10
   Male 88 90
Age (Year)
   20–29 47 48
   30–39 40 41
   40–49 10 10
   50–59 1 1
Risk factors for HIV transmission
   Intravenous drug users (IVDU) 61 69
   Homosexual intercourse 1 1
   Heterosexual intercourse 22 22
   IVDU and homosexual intercourse 1 1
   IVDU and heterosexual intercourse 5 5
   IVDU and tattoo/piercing 2 2
History of antifungal agents
Fluconazole
   No 59 60
   Yes 39 40
Nystatin
   No 38 39
   Yes 60 61
Ketoconazole
   No 96 98
   Yes 2 2
Oral candidiasis
   No 57 58
   Yes 41 42

Table 2. Susceptibility and resistance antifungal on the Candida species and oral candidiasis history in HIV/AIDS patients

Candida species N %
Fluconazole Ketoconazole Nystatin

Oral candidiasis 
history

Susceptible Resistant Susceptible Resistant Susceptible Resistant Yes No

C. albicans 93 95 80 13 81 12 80 13 39 50
C. dubliniensis 2 2 2 0 1 1 2 0 1 2

C. guillermondii 1 1 1 0 1 0 1 0 1 2

C. famata 1 1 1 0 1 0 1 0 0 2
C. tropicalis 1 1 1 0 1 0 1 0 0 1

Table 3. Antifungal Susceptibility on C. albicans in HIV/AIDS patients

Antifungals
(μg/mL)

Fluconazole Ketoconazole Nystatin
p-value

N % Status Turbidity N % Status Turbidity N % Status Turbidity

1 74 80 Susceptible 0 75 81 Susceptible 0 73 79 Susceptible 0

*p>0.05 
(0.628)

2 3 3 Susceptible 1 1 1 Susceptible 1 1 1 Susceptible 1

4 3 3 Susceptible 1 1 1 Susceptible 1 1 1 Susceptible 1

64 1 1 S-DD 2 1 1 S-DD 2 1 1 S-DD 2

128 12 13 Resistant 3 15 16 Resistant 3 17 18 Resistant 3

*  Kruskal–Wallis  test  and  Spearman’s  rho  correlation;  S-DD  (Susceptibility-Dose  Dependent);  Susceptible ≤ 8  μg/mL,  S-DD  16-64  μg/mL, 
Resistant ≥ 128 μg/mL, and 250 μg/mL not recommended: Turbidity indicator, 0 (no growth), 1 (weak growth), 2 (reduction in growth), 3 (growth 
reduced slightly), 4 (No reduction in growth).

Dental Journal (Majalah Kedokteran Gigi) p-ISSN: 1978-3728; e-ISSN: 2442-9740. Accredited No. 32a/E/KPT/2017.
Open access under CC-BY-SA license. Available at https://e-journal.unair.ac.id/MKG/index
DOI: 10.20473/j.djmkg.v54.i2.p82–86

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85Rezeki et al./Dent. J. (Majalah Kedokteran Gigi) 2021 June; 54(2): 82–86

DISCUSSION

This research reported that subjects without candidiasis 
are more dominant than with oral candidiasis. These 
subjects have susceptibility and resistance to fluconazole, 
ketoconazole, and nystatin in low. Generally, these 
antifungals have a vulnerability to the oral Candida 
species, mainly C. albicans. The presence of C. albicans 
in the oral candidiasis of HIV patients is confirmed                                                  
by Patil et al.15 who found 95.2% of C. albicans cases 
leading to oropharyngeal candidiasis in HIV/AIDS.

This study indicates that the male population is 
higher than the female population with an average age 
of 20–29 years and ages 30–39 (Table 1). The most 
dominant transmission is through intravenous and 
heterosexual injections. Glick et al.16 reports that men 
who have sex with men (MSM) have higher rates of HIV 
and sexually transmitted infections (STIs) than women 
and other heterosexual men. This increased risk persists 
across all age groups and reflects various biological and 
behavioural factors, but there are some direct comparisons 
of sexual behaviour patterns between populations.16 In this 
research, we found the different effects of three antifungal 
types to treat oral candidiasis on HIV/AIDS subjects                              
(Table 3). They have a susceptibility to preventing the 
oral candidiasis treatment of subjects with HIV/AIDS. 
The oral candidiasis prophylaxis used fluconazole (200 
mg/day) with a CD4 count <100 cells/μL also in patients 
with CD4 100–200 cells/μL. Additionally, long-term oral 
candidiasis prophylaxis with fluconazole is likely to lead 
to resistance.17

Based on the characteristics analyses of HIV/AIDS, 
42% of the subjects had a history of candidiasis, 58% had 
no history of candidiasis. The Candida species cultures 
from the 98 subjects showed 95% C. albicans, while the 
rest were other Candida species. It is, therefore, explained 
that in HIV, oral candidiasis is related to the history of 
antifungal use (Table 1). The subjects had a history of 
antifungal use with different percentages of antifungals. 
Garcia-Cuesta et al.18 explain that the oral antifungal of 
candidiasis of a patient with HIV status is often given 
several antifungal types to prevent oral Candida species 
symptoms and infection. The use of an antifungal mixture to 
maintain the fungal population’s balance in the oral cavity 
can also help increase the mucosal oral defence system to 
prevent Candida species’ adhesion.19 

The development of oral candidiasis in HIV/AIDS 
patients is highly dependent on the history of antifungal 
treatment. It is reasonable to suspect that some subjects 
in this study have had proper oral candidiasis treatment. 
Nevertheless, the prevalence of C. albicans in HIV 
is always associated with resistance to fluconazole.20                              
In general, the injection of narcotic drugs and heterosexual 
relationships tend to be experienced by other people living 
with HIV. These trends indicate that the susceptibility 
population is strongly related to the level of resistance to 
fluconazole or other antifungal drugs such as nystatin and 

ketoconazole. Maheshwari et al.21 reported that in general 
HIV-positive patients with CD4+ cell counts between 
200 and 400/μL had more colonisation of C. albicans and         
C. dubliniensis.

Table 3 shows that the lowest concentration of 
fluconazole has susceptibility to oral C. albicans. 
In contrast, the highest concentration of fluconazole 
is resistant to the antifungal of C. albicans essence                                                        
of HIV/AIDS. Thus, fluconazole toxicity to Candida 
species at the lowest concentration is becoming higher. 
This antifungal has the ability to prevent Candida  
infections by inhibiting DNA synthesis and ergosterol 
biosynthesis in fungal cell membranes, changing cell 
surface hydrophobicity, and influencing the synthesis of 
triglycerides and phospholipids.22

Based on this study, resistance occurs due to intense 
administration with varying doses. This finding concurs 
with previous research showing that resistance occurred, 
on average, in minimal inhibition concentration (MIC) of 
fluconazole concentrations of up to three times due to long-
term treatment.23 Patil et al.24 reported that the subject’s 
decreased resistance could support oral candidiasis 
development. As many as 95% of C. albicans cases were 
reported as a trigger factor for oral candidiasis. The oral 
Candida species’ resistance was reported to be less than 
sensitive, but it can threaten oral candidiasis if HIV/AIDS 
infection persists.24 This study found that susceptibility 
frequency is higher than that of resistance, so these 
antifungals are recommended to prevent oral candidiasis 
in HIV/AIDS.

The antifungal drugs used in this research have different 
susceptibility and resistance properties. However, they have 
the same tendency to suppress the growth of C. albicans, 
as shown in Tables 2 and 3. It is indicated that fluconazole, 
ketoconazole, and nystatin have a high susceptibility, 
with an average above 80%. These antifungals have a 
substantial effect on C. albicans, both fungicidal and 
fungistatic. Other findings from this study are that the 
three drugs’ susceptibility and resistance.  Whaley et al.25 
reported that in the treatment of HIV, the administration 
of azole groups could cause C. albicans resistance or 
trigger the development of non-C. albicans species, such as                                                                                                                      
C. glabrata and C. krusei, which intrinsically cause 
resistance. The opposition to one of the azole antifungal 
drugs is often associated with other azole resistance.25 

Period exposure is a risk factor in fluconazole resistance. 
Refractory oropharyngeal candidiasis of treatment by 
fluconazole is most frequently used in HIV.8

The tracing of the possible history of antifungal 
drug administration was obtained through periods of 
HIV infection and diagnosed HIV patients. The higher 
possibility of opportunistic infections impacts oral 
candidiasis with treatment by antifungals, which then 
affects susceptibility. However, these allegations still need 
further analysis regarding the relationship between the 
length of HIV infection with a history of antifungal use and 
susceptibility based on more accurate data. In this study, 

Dental Journal (Majalah Kedokteran Gigi) p-ISSN: 1978-3728; e-ISSN: 2442-9740. Accredited No. 32a/E/KPT/2017. 
Open access under CC-BY-SA license. Available at https://e-journal.unair.ac.id/MKG/index
DOI: 10.20473/j.djmkg.v54.i2.p82–86

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86 Rezeki et al./Dent. J. (Majalah Kedokteran Gigi) 2021 June; 54(2): 82–86

the susceptibility test was not carried out on other Candida 
species because the population was too small. There was 
also no antifungal combination to test the susceptibility to 
C. albicans. It can be concluded that Candida albicans was 
dominant in the saliva of HIV/AIDS patients. This fungus 
was effectively treated by fluconazole, ketoconazole, 
and nystatin. These antifungals had high susceptibility at                                                  
≤ 8 μg/mL to C. albicans.

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Dental Journal (Majalah Kedokteran Gigi) p-ISSN: 1978-3728; e-ISSN: 2442-9740. Accredited No. 32a/E/KPT/2017. 
Open access under CC-BY-SA license. Available at https://e-journal.unair.ac.id/MKG/index
DOI: 10.20473/j.djmkg.v54.i2.p82–86

https://e-journal.unair.ac.id/MKG/index
http://dx.doi.org/10.20473/j.djmkg.v54.i2.p82-86