EDUSJ, Vol, 34, No: 4, 2025 (1-13)

Journal of Education and Science (ISSN 1812-125X)

Determination of Factors Affecting the Isolation of Candida Species Among Diabetic

Patients with Oral Candidiasis in Duhok Governorate, Iraq

N. H. B. Sultan(1*) , A. A. M. Saadullah(2)

(1)
Medical Laboratory Department, College of Health Sciences, University of Duhok, Iraq
(2)
Biology Department, College of Sciences, University of Duhok, Iraq

Article information Abstract

Article history: Oral candidiasis, a fungal infection primarily caused by Candida albicans, poses a
Received: May 11, 2025
significant health risk for diabetics due to their weakened immune systems and altered oral
Revised: July 17, 2025
Accepted: July 21, 2025 environments. The prevalence and risk factors for oral candidiasis were evaluated in this
Available online: October 01.2025 cross-sectional study of 367 diabetic patients at Azadi Teaching Hospital in Duhok City
Keywords: from August 2024 to April 2025. Sterile swabs were used to collect clinical samples, which
Diabetic were then cultured on various selective media to identify the species of Candida. According
Oral Candidiasis
Candida Species
to the results, 34.1% of patients tested positive for Candida species, with the most common
Duhok species being Candida albicans (13.9%), followed by Candida tropicalis (9.8%) and
Normal Flora Candida glabrata (3.0%). A noteworthy correlation was observed between comorbid
conditions such as dental problems, high blood pressure, and high cholesterol with oral
Correspondence:
Narmin Hassan Biso Sultan
candidiasis. Additionally, type 2 diabetes and advanced age were prevalent among those
[email protected] affected. The study emphasises the importance of preventive measures and regular oral
health examinations to reduce the risk of fungal infections in diabetic patients.

DOI:10.33899/jes.v34i4.49244, ©Authors, 2025, College of Education for Pure Science, University of Mosul.
This is an open access article under the CC BY 4.0 license (http://creativecommons.org/licenses/by/4.0/).

1. Introduction
Candida is a genus of opportunistic fungi that are frequently present in the oral cavity, vaginal mucosa, and
gastrointestinal tract as a natural component of the human microbiota. Certain species, such as Candida albicans, are
generally harmless in healthy individuals, but they can cause infections when the host's immune system is weakened or when
the microbiome is disrupted [1]. These infections, referred to as candidiasis, can range from minor mucosal infections to
potentially fatal systemic candidemia, especially in immunocompromised individuals [2].
Oral candidiasis, often referred to as oral thrush, is a fungal infection caused by Candida species, primarily Candida
albicans. This condition arises when immunosuppression, antibiotic use, diabetes, or poor oral hygiene disrupt the normal
balance of the oral microbiota [3]. Oral candidiasis manifests as white, curd-like plaques on the tongue, inner cheeks, and
other parts of the oral cavity, which can be uncomfortable or unpleasant [4].
The Candida genus comprises various species, some of which can develop into opportunistic infections, while
others are commensal microbes in the human microbiome. The most frequent cause of candidiasis in humans is Candida
albicans, which can lead to both superficial infections, such as vaginal candidiasis and oral thrush, and systemic infections,
including candidemia. Candida glabrata is commonly associated with bloodstream infections (candidemia) [5]. Patients with
impaired immune systems, especially those suffering from neutropenia, are frequently infected with Candida tropicalis.
Candida parapsilosis is often linked to catheter-associated bloodstream infections, while Candida krusei is commonly
associated with infections in immunocompromised individuals, such as cancer patients undergoing chemotherapy. A new
multidrug-resistant strain, Candida auris, is responsible for hospital outbreaks worldwide [6]. Numerous studies suggest that
individuals with diabetes are at an increased risk of candidiasis. Factors such as decreased immunity, angiopathy,
neuropathy, and increased medicinal interventions contribute to the high prevalence of infections among diabetic patients
[7]. High glucose levels in diabetic individuals may promote the growth of yeast in the oral cavity, further increasing the
risk of fungal infections [8].

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The diagnosis of oral candidiasis may be based on the clinical recognition of a specific Candida species. Clinical
forms of oral candidiasis include pseudomembranous candidiasis, hyperplastic candidiasis (candidal leukoplakia), atrophic
candidiasis (both acute and chronic erythematous forms), and angular cheilitis [9]. In some cases, diagnosing candidiasis
can be challenging, as individuals exhibit varying signs and symptoms depending on their age, gender, host immunity, and
environmental exposures. However, diagnostic tools such as questionnaires, complete digestive stool analysis (CDSA), and
laboratory methods can be used to screen for and confirm yeast infections [10].
Oral candidiasis can now be treated with a variety of topical and systemic medications. Systemic antifungal
medications, such as triazoles (fluconazole, itraconazole), are suitable for individuals at high risk of acquiring systemic
infections or those who do not respond to or are intolerant to topical therapies. Topical antifungal medications, including
clotrimazole, miconazole, amphotericin B, and nystatin, are typically recommended as the first line of treatment for mild
cases of oral candidiasis [11]. The purpose of this study is to isolate and identify Candida species from oral candidiasis in
diabetic patients from Duhok Province using HI Chrome Agar and to investigate some associated features.

2. Materials and Methods

2.1 Specimen collection
A total of 367 oral samples must be written in the past tense collected from diabetic patients in the morning period
at the Azadi Teaching Hospital in Duhok City, between August 2024 to April 2025. After obtaining permission from the
patients to participate in this study. The control sample was taken from healthy individuals without oral candidiasis to
compare the presence or absence of Candida species, colony, morphology, virulence factors, or immuneresponse.
Samples will be collected from patients using sterile cotton swabs (Sterile Cotton Swabs) containing physiological
salt solution NaCl for the clinical evaluation of individuals who were diagnosed, after which they will be reviewed by trained
medical professionals. Then, to monitor fungal species, they were cultivated on three basic agars: Sabouraud dextrose agar,
Sabouraud Dextrose Broth, Nutrient agar, Sabouraud Chloramphenicol agar, HiCrome Candida Differential Agar, and Corn-
Meal Agar (CMA). The tongue, buccal mucosa, and labial sulcus were all touched with a sterile transport swab. Patients
who visited hospitals in Iraq's Kurdistan region's Duhok province.

2.2 Number of Samples

A total of 367 swab samples were included in this study.

2.3 Sample collection

Swabs were cleaned with saline and then rubbed over the lesion to collect samples from the base of the ulcer. They
can be extracted straight from the purulent exudate as well. After being collected for 24 hours, the samples were brought to
the lab and cultivated on potato dextrose agar and Sabouraud dextrose agar. The plates were kept at 37°C for 48 hours

2.4 Preparation of Media

The preparation of all used media was done according to the manufacturer's instructions.

2.4.1 Sabouraud dextrose agar

One litre of distilled water should be used to suspend 65 g of the medium.
To fully dissolve the medium, heat for one minute while stirring often.
Autoclave for 15 minutes at 121° C.
Pour into petri dishes or tubes for slants after cooling to 45 to 50°C.

Figure 1. This is a result

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2.4.2 Sabouraud Dextrose Broth

30 g of dehydrated medium (BK026) should be dissolved in 1 litre of demineralised or distilled water.
Slowly stir until the mixture dissolves completely. •
Pour into 100 mL vials or 10 mL tubes. •
Autoclave for 15 minutes at 121 °C to sterilise.
The medium should be cooled to room temperature.

2.4.3 Sabouraud Chloramphenicol agar

42.5 g of powder should be dissolved in 1 L of distilled water.
It should then be heated, swirling constantly, until it dissolves completely.
It should then be autoclaved for 20 minutes at 121 ± 3°C.
Gentamicin or chloramphenicol can be added as needed.
Finally, it should be mixed and poured into sterile Petri plates.

2.4.4 HiCrome™ Candida Differential Agar

1. In 1000 millilitres of distilled water, suspend 42.72 grams.
2. Bring to a boil in order to fully dissolve the medium.
3. AVOID AUTOCLAVING.
4. Lower the temperature to 45–50°C.
5. Pour onto sterilized Petri dishes after thoroughly mixin .

Figure 2. This is a result

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2.4.5 Corn Meal Agar (CMA)

This test is a quick way to distinguish between Candida dubliniensis and Candida albicans because it produces
fragile, small, tube-like structures called germ tubes after two hours of incubation in human blood serum at 37 oC. In contrast
to pseudo-hyphae, germ tubes are elongations of daughter cells from the mother cell without origin shrinking [12].
Virulence factor testing should be performed, ex, proteinase, esterase, hemolysin
The three main enzymes produced by C.albicans are secreted aspartyl protease, phospholipase, and hemolysin [13].

Figure 3. This is a result

2.5 Gram stain

The Gram stain is a differential stain that involves a process called decolourisation, which is the most crucial stage.
The data indicate that the cell wall components of Gram-positive (thick peptidoglycan) and Gram-negative (thin
peptidoglycan) bacteria determine their ability to withstand decolourisation. Because alcohol or acetone extracts the lipid,
the Gram-negative cell wall becomes porous and loses its ability to retain the crystal violet–iodine complex. As a result, the
safranin dye can stain it, giving the Gram-negative bacteria a reddish-pink appearance. In contrast, the thick peptidoglycan
in Gram-positive bacteria efficiently traps the crystal violet–iodine complex, giving the Gram-positive bacteria a purple
appearance and increasing their resistance to decolourisation [14].

Figure 4. Structure of Candida in Gram staining

2.5.1 Germ tube formation test

Candida albicans and Candida dubliniensis may be quickly identified with this test because, when cultured in human
blood serum at 37 ˊ C for two to three hours, they develop short, slender, tube-like structures termed germ tubes. Because
they are elongated daughter cells from the mother cell without constriction at the origin, they are different from pseudo
hyphae [15].

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Figure 5. germ tube of Candida albicans

2.5.2 Antifungal susceptibility test
The antifungal sensitivity test includes several in vitro techniques, such as the minimum inhibitory concentration
(MIC), which can be used to assess the activity against certain fungal isolates. The MIC, defined as the lowest
concentration of an antifungal agent that will prevent visible growth of a fungus after incubation, is the most widely used
laboratory test to determine an antimicrobial's efficacy against fungal species [16]. Antifungal agents that are used in the
current study are: Itraconazole, Clotrimazole, Amphotericin B, and Fluconazole.

Figure 6. Resulty

3. The Results
Among 367 diabetic patients (n=125; 34.1%) were positive for Candida species (oral candidiasis), and (n=242;
65.9%) were negative, as shown in Graph 1. Of all 367 patients (n=255; 69.5%) were female, and (n=112; 30.5%) were
male. Among 367 diabetic patients (n=350; 95.4%) were type 2 diabetic patients, and (16; 4.4%) were type 1 diabetic
patients. Most frequent diabetic patients were in the age group 52 – 72 (n=216; 58.9%), and the least wan was the group <=9
years, as shown in Graph 2. The most common Candida species isolated from infected patients was Candida albicans
(13.9%) followed by Candida tropicalis (9.8%) and Candida glabrata (3.0%), in addition to many other species Candida
utilis (1.1%), Candida krusei (2.7%), in addition to others shown in Table 1. On sabaroud dextrose agar, shown growth of
Candida species is shown without selecting the type of Candida, as shown in Figure 1. Neither on Hichrom Candida agar,
most Candida species can the identified as the type of Candida. Most frequent diabetic patients have High blood pressure,
which 339 of 367, and among patients with High blood pressure, 111 were positive for oral candidiasis Table 3. Also, 357
of diabetic patients have high cholesterol levels, 117 of them have positive oral candidiasis Table 4. Also, from diabetic
patients, 212 have teeth problems, and 93 of them were positive for oral candidiasis Table 5. Some patients have shortness
of breath, and some of them have heart disease, eye problems, surgery, obesity, kidney disease, thyroid disease, and skin
problems.

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4. Statistical Analysis
SPSS (IBM, version 25) was used to analyse the data. The mean, standard deviation, median, and range were used to express
quantitative data. Numbers and percentages were used to present qualitative data.

Graph 1: Presence of oral candidiasis in diabetic patients

Graph 2 : group of age of diabetic patients

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Table 1: Frequency percentage of isolated Candida species.

Frequency Percent
Valid Negative 245 66.8
C. albicans 51 13.9
C. tropicaliss 36 9.8
C. glabrata 11 3.0
C. utilis 4 1.1
C. krusei 10 2.7
C. kefyr 3 .8
C. mixed 1 .3
C. dubliensis 3 .8
C. glabrataCh 1 .3
C. parapsilosis 1 .3
C. membranifaciens 1 .3
Total 367 100.0

Table 2: Relationship between variables

Type_of_ Years_
Gender Enus_species Age (Binned)
Diabetes Diagnosed

Correlation Coefficient 0.078 -0.019 0.017 0.954** 0.057

Oral_candidiasis

Sig. 0.134 0.719 0.750 0.000 0.278

Table 3: High blood pressure

Oral_candidiasis Crosstabulation
Count
Oral_candidiasis
Negative Positive Total
High blood pressure 228 111 339
Total 228 111 339

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Table 4: High cholesterol level

Oral_candidiasis Crosstabulation
Count
Oral_candidiasis
Negative Positive Total
High cholesterol 240 117 357
Total 240 117 357

-Although high blood pressure and hyperlipidemia are not considered direct risk factors for oral candidiasis, their frequent
presence in diabetic patients may indicate poor glycemic control. This poor metabolic regulation can compromise immune
function and create a favorable environment for fungal overgrowth. Therefore, the association between these comorbidities
and oral candidiasis is likely circumstantial rather than causal. This interpretation is supported by several studies that have
highlighted the indirect influence of systemic conditions, particularly uncontrolled diabetes, on the risk of oral Candida
infections.
Table 5: teeth problems
Oral_candidiasis Crosstabulation
Count
Oral_candidiasis
Negative Positive Total
Teeth problems 119 93 212
Total 119 93 212

Table 6: Shortness of breath

Oral_candidiasis Crosstabulation
Count
Oral_candidiasis
Negative Positive Total
Shortness of breath 245 119 364
Total 245 119 364

Table 7: Heart disease

Oral_candidiasis Crosstabulation
Count
Oral_candidiasis
Negative Positive Total
Heart disease 36 25 61
Total 36 25 61
Table 8: Eye problems

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Oral_candidiasis Crosstabulation
Count
Oral_candidiasis
Negative Positive Total
Eye problems 11 23 34
Total 11 23 34

Table 9: surgery in last 5 years

Oral_candidiasis Crosstabulation
Count
Oral_candidiasis
Negative Positive Total
surgery in last 5 years 2 3 5
Total 2 3 5

Table 10: Obesity

Oral_candidiasis Crosstabulation
Count
Oral_candidiasis
Negative Positive Total
Obesity 2 5 7
Total 2 5 7

Table 11: Kidney disease

Oral_candidiasis Crosstabulation
Count
Oral_candidiasis
Negative Total
Kidney disease 1 1
Total 1 1

Table 12: Thyroid disease

Oral_candidiasis Crosstabulation
Count
Oral_candidiasis
Negative Positive Total
Thyroid disease 7 7 14
Total 7 7 14

Table 13: Skin problems

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Oral_candidiasis Crosstabulation
Count
Oral_candidiasis
Negative Positive Total
Skin problems 1 4 5
Total 1 4 5

5. The Discussion
The results of this research show a notable occurrence of oral candidiasis in patients with diabetes, with 34. 1%
testing positive for Candida species. This finding corresponds with earlier investigations that indicate people with diabetes
have a higher likelihood of experiencing fungal infections, including oral candidiasis [17]. Multiple factors contribute to this
situation, such as weakened immune responses, poor control of blood sugar levels, and conditions in the mouth that support
the growth and colonisation of fungi [8].
Among the Candida species identified, Candida albicans was the most commonly found at 13. 9%, followed by
Candida tropicalis at 9. 8% and Candida glabrata at 3. 0%. This pattern agrees with earlier research that has identified C.
albicans as the leading cause of oral candidiasis, thanks to its ability to adhere strongly and
create biofilms [18] [19] The presence of non-albicans Candida species like C. glabrata and C. krusei raises clinical concerns
because of their greater resistance to standard antifungal treatments, especially azoles.
The information also reveals that issues like high blood pressure and high cholesterol were common within the
group studied and linked to a greater occurrence of oral candidiasis. Among 339 diabetic subjects with high blood pressure,
111 were found to have candidiasis, whereas 117 out of 357 patients with high cholesterol were also positive for it. These
results indicate that systemic health issues typically associated with diabetes may weaken the body’s defences and promote
fungal overgrowth.
Oral hygiene seems to be another important factor; of the 212 patients who reported dental problems, 93 (43. 9%)
had oral candidiasis. Poor dental care and oral health issues can disturb the balance of microorganisms in the mouth and
harm the mucous membranes, leading to increased vulnerability to fungal growth [20] Moreover, the link between older age,
especially in the 52 to 72 age bracket, and higher rates of candidiasis might represent both age-related immune decline and
the extended duration of diabetes, which together raise the risk of infections [2] .
The high occurrence of type 2 diabetes (95. 4%) among the participants aligns with global trends, where type 2
diabetes accounts for most cases. The elevated rates of infections in these individuals further emphasise the importance of
regular oral health screenings and strategies for preventing candidiasis, especially. For those with additional risk factors such
as high blood pressure, abnormal lipid levels, or dental problems.

6. Conclusion
Patients with diabetes have a significantly higher prevalence of oral candidiasis, with Candida albicans being the
most prevalent causal species, according to this study. The results emphasise the role that diabetes-related factors, such as
poor glycemic control, comorbid conditions (e.g., high blood pressure and high cholesterol), and dental health issues, play
in increasing susceptibility to fungal infections. The correlation between higher infection rates and advanced age further
highlights the risk for elderly diabetics. These findings underscore the need for heightened clinical awareness of fungal
infections in this group, as well as the importance of proactive oral hygiene management and regular oral examinations as
part of diabetes care. With early detection and coordinated healthcare measures, patients with diabetes can improve their
quality of life and significantly reduce the burden of oral candidiasis.

7. Acknowledgement
I would like to express my sincere gratitude to the college of health sciences and to Dr. Asia A.M. saadullah for
their valuable support. my heartfelt thanks also go to my family for their continuous in encouragement.

8. Conflict of Interest
The authors declare that there are no conflicts of interest regarding the publication.

9. Funding
The authors declare that they have no known competing financial interests or personal relationships that could have
appeared to influence the work reported in this paper

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‫تحديد العوامل المؤثرة على عزل أنواع الكانديدا بين مرضى السكري الذين يعانون من داء المبيضات الفموي في‬
‫محافظة دهوك‪ ،‬العراق‬
‫(‪)2‬‬ ‫(‪)*1‬‬
‫أسيا عبدالحميد محمد سعدهللا‬ ‫‪،‬‬ ‫نرمين حسن بيسو سلطان‬

‫(‪)1‬كلية العلوم الصحية ‪ ،‬قسم المختبرات الطبية جامعة دهوك‪ ،‬العراق‬

‫(‪ )2‬قسم األحياء‪ ،‬كلية العلوم‪ ،‬جامعة دهوك‪ ،‬العراق‪.‬‬

‫المستخلص‬
‫نظرا لضعف‬
‫كبيرا على مرضى السكري ً‬ ‫خطرا صحيًا ً‬ ‫ً‬ ‫داء المبيضات الفموي هو عدوى فطرية غالبًا ما تسببها فطريات المبيضات البيضاء‪ ،‬ويشكل‬
‫أجهزتهم المناعية وتغير بيئة الفم‪ .‬تم تقييم انتشار داء المبيضات الفموي وعوامل الخطر المرتبطة به في هذه الدراسة المقطعية التي شملت ‪ 367‬مريضًا بالسكري‬
‫في مستشفى آزادي التعليمي بمدينة دهوك‪ ،‬في الفترة من أغسطس ‪ 2024‬إلى أبريل ‪ .2025‬استُخدمت مسحات معقمة لجمع العينات السريرية‪ ،‬ثم ُزرعت على‬
‫أوساط انتقائية متنوعة لتحديد أنواع المبيضات‪ .‬ووفقًا للنتائج‪ ،‬أظهرت االختبارات أن ‪ %34.1‬من المرضى كانوا إيجابيين ألنواع المبيضات‪ ،‬وكانت األنواع‬
‫األكثر شيوعًا هي المبيضات البيضاء (‪ ،)%13.9‬تليها المبيضات االستوائية (‪ )%9.8‬والمبيضات الجالبراتا (‪ .)% 3.0‬كما لوحظ وجود عالقة ذات داللة إحصائية‬
‫بين األمراض المصاحبة مثل مشاكل األسنان وارتفاع ضغط الدم وارتفاع الكوليس ترول وبين داء المبيضات الفموي لدى المرضى‪ .‬كان داء السكري من النوع‬
‫الثاني والتقدم في العمر شائعين أيضًا‪ .‬تؤكد الدراسة على أهمية اتخاذ التدابير الوقائية وإجراء فحوصات دورية لصحة الفم للحد من خطر اإلصابة بالعدوى الفطرية‬
‫لدى مرضى السكري‪.‬‬

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