Indian Journal of Dental Research

ORIGINAL RESEARCH
Year
: 2021  |  Volume : 32  |  Issue : 3  |  Page : 292--298

Prevalence of species-specific candidiasis and status of oral hygiene and dentition among diabetic patients: A hospital-based study


Ritu Duggal1, Ravinder Goswami2, Immaculata Xess3, Isha Duggal1, Aditya Talwar1, Vijay Prakash Mathur4,  
1 Division of Orthodontics & Dentofacial Deformities, CDER, All India Institute of Medical Sciences, New Delhi, India
2 Department of Endocrinology & Metabolism, CDER, All India Institute of Medical Sciences, New Delhi, India
3 Department of Microbiology, CDER, All India Institute of Medical Sciences, New Delhi, India
4 Division of Pedodontics & Preventive Dentistry, CDER, All India Institute of Medical Sciences, New Delhi, India

Correspondence Address:
Prof. Vijay Prakash Mathur
Room No 602, 6th Floor, Centre for Dental Education and Research, All India Institute of Medical Sciences, New Delhi - 110 029
India

Abstract

Objective: The study was undertaken to estimate the species-specific prevalence of oral candidiasis in diabetic individuals in India, and further find the relationship of oral carriage of Candida in diabetes with degree of diabetic control, duration of disease, type of diabetes and its effect on the status of oral hygiene status and decayed, missing and filled teeth (DMFT) score. Methodology: The prospective cross-sectional study involved 900 individuals (470 diabetic and 430 non-diabetic) visiting a tertiary care hospital. Informed consent was obtained from all the individuals participating in the study. The demographic details, medical history and oral cavity examination were recorded in a specially designed proforma. Swabs were taken for microbiological evaluation for specific prevalence of Candida. Results: The overall prevalence of Candida in diabetics was 22.1% as compared to 9.7% in non-diabetic individuals. However, among the type 1 and type 2 diabetics, the prevalence of Candida was equally distributed as 22.6% and 20.8%, respectively. C. albicans was the most common species (97.1%), while isolated cases of other species like C. rugosa, C. tropicalis, C. glabrata were also observed. The individuals with higher glycaemic score (HbA1c >7) showed higher prevalence of oral candidiasis. Oral hygiene status was observed to be lower among diabetics as compared to non-diabetic individuals. Conclusion: Oral candidiasis was more prevalent in diabetic patients, and C. albicans was the most common species. The diabetics also showed higher mean DMFT with lower oral hygiene status as compared to non-diabetic individuals.



How to cite this article:
Duggal R, Goswami R, Xess I, Duggal I, Talwar A, Mathur VP. Prevalence of species-specific candidiasis and status of oral hygiene and dentition among diabetic patients: A hospital-based study.Indian J Dent Res 2021;32:292-298


How to cite this URL:
Duggal R, Goswami R, Xess I, Duggal I, Talwar A, Mathur VP. Prevalence of species-specific candidiasis and status of oral hygiene and dentition among diabetic patients: A hospital-based study. Indian J Dent Res [serial online] 2021 [cited 2022 Aug 17 ];32:292-298
Available from: https://www.ijdr.in/text.asp?2021/32/3/292/338134


Full Text



 Introduction



Diabetes mellitus (DM) is a group of diseases characterised by abnormal carbohydrate, fat and protein metabolism, resulting in complications due to lack of insulin, which may be absolute or relative. As per 2019 estimates, India has approximately 7.3 crore people living with diabetes, and another 3.7 crore people are likely to have prediabetes.[1]

Patients with DM are at greater risk of having infections like gingival and periodontal diseases, salivary dysfunction, oral and vaginal candidiasis.[2] The occurrence of Candida infections in the oral cavity of patients with diabetes mellitus has been well documented in the past.[3],[4],[5],[6] This may be due to compromised immunity and nutrition, decreased salivary function and pH, and high level of salivary glucose that aid the growth of commensals in the oral cavity.[7]

The carriage of Candida species in oral environment is claimed to be increased in patients with diabetes mellitus. Candida albicans is by far the most predominant fungal species found in the oral mycobiome.[8],[9] However, the presence of other species, such as C. glabrata, C. tropicalis, C. krusei, C. dubliniensis and C. parapsilosis have also been reported.[10] The prevalence of the microorganism in these patients has been reported varies from 18%–80% in different studies.[8] This variation may be due to differences in sampling technique, type and duration of the disease, the degree of glycaemic control and presence of denture.

In one of the previous studies, the investigators found out differences in species of Candida in the vulvovaginal region among diabetic and non-diabetic individuals.[11] This difference had implications on treatment planning and medication for the infection. A similar characterisation seems essential to determine strategies for prevention, control and treatment of oral fungal infections, and also for developing effective therapeutic interventions.

Despite a high diabetic population in India, there is a lacuna in literature on species-specific prevalence of oral candidiasis in diabetics. Thus, the present study was undertaken to primarily estimate the prevalence of oral candidiasis in diabetic patients. An attempt was made to find the relationship of oral carriage of Candida species in diabetics with their degree of diabetic control, duration of disease and type of diabetes. Secondarily, it was also aimed to examine the relationship between diabetics and their oral health status. The information obtained from this study would throw light on the prevalence of Candida in diabetic patients as compared to the healthy ones, and help identify high-risk individuals where regular screening should be implemented for early detection of oral candidiasis. This would also guide the specific prophylactic antifungal therapy, to be followed after susceptibility testing which might prevent systemic dissemination of opportunistic Candida in these patients.

 Materials and Methods



The present prospective cross-sectional observational study was undertaken by the Centre for Dental Education and Research in collaboration with the Department of Endocrinology, AIIMS, New Delhi, after approval by the Institute Ethics Committee.

Sample size calculation: Due to the unavailability of similar studies on the prevalence of oral candidiasis for the Indian population, the sample size was calculated based on rough estimates of prevalence in diabetics as 60%. As the study was planned to be in a hospital-based setting and the subjects reporting to the hospital may not be a true representative of the population, the design effect was kept as 2. The required precision was kept at 5%, and the value of certainty was kept at 95%. Thus, the formula used for calculating sample size calculation for this study design was as follows:

[INLINE:1]

Study tool and observer calibration: A specially designed case sheet was developed for recording the demographic details, medical history, oral examination and laboratory findings. The observers were trained and calibrated by examining 10 subjects from the out-patient department (OPD). It is pertinent to mention that these patients were not included in the study sample. The recording sheets were checked by another independent expert, and if there were any differences, they were explained. The same calibration process was repeated after examination of about 50% subjects to ensure uniformity and minimise fatigue bias.

Study population: The patients were recruited from the Endocrine Clinic of All India Institute of Medical Sciences, New Delhi, India, during their routine follow-up appointments. The subjects who had received any antibiotic/steroid therapy or had been using antiseptic mouthwashes were excluded from the study. The healthy controls (non-diabetics) were recruited from the Out-Patient Department of Centre for Dental Education and Research, All India Institute of Medical Sciences, New Delhi, India. All the participants were provided with a detailed description of the study and written informed consent prepared according to the Declaration of Helsinki was obtained prior to their induction in the study.

Blood sugar levels (fasting and 2-hour post prandial) were recorded for all the participants, with additional total glycated haemoglobin levels for all diabetic subjects. Patients were further stratified based on the degree of the glycaemic control (HbA1c below or above 7), duration of disease (below and above 10 years) and type of diabetes (type 1 and 2). In order to have a sufficient number of patients with type 1 and type 2 diabetes in the study cohort, an enrichment policy was followed by recruiting patients from the weekly carried out 'Diabetes of young' clinic.

Oral cavity examination: Before starting the examination, the participants were made to sit comfortably on a chair, so that the oral cavity was clearly visible to the examiner, preferably under light.

The oral health examination was carried out according to the WHO Oral Health assessment form (2004) for oral mucosal conditions, dentition and periodontal health status.[12] Oral Hygiene Index-Simplified (OHI-S) and presence of clinical lesions of candidiasis, if any, were also recorded in pictorial performa. Following the oral cavity examination, oral swabs for microbiological evaluation were taken on the same visit as a means to prevent the accumulation of partial data.

Microbiological Evaluation: Swabs in duplicate were taken for all participants by gently rubbing a sterile cotton swab over the buccal mucosa and dorsum of the tongue. Subsequently, gram-stained exfoliative cytology was performed to demonstrate the presence of yeast and filamentous structures. These swabs were sealed and coded to achieve blinding and avoid any analytical or reporting bias. These coded samples were sent for microbiological examination without disclosing any clinical details or identity of the subjects.

Oral swab samples were cultured in Sabouraud dextrose agar (with or without gentamicin 40 μg/ml) for the growth of fungi. Cultures were incubated for a maximum of 7 days before giving a negative report. They were monitored routinely for the presence of any visible growth at 37°C and 25°C. Culture positive yeast isolates were subjected to Gram's staining. Presumptive identification was made based on gram-positive 2–4 μm, oval-shaped budding yeast cells on oil immersion (100×). Further identification of yeast was done by standard laboratory methods. Also, identification of species level and the characterisation was done with the help of germ tube test (Reynold–Braude phenomenon), urea hydrolysis, corn meal agar test, CHROM agar test, tetrazolium reduction medium, sugar assimilation test and sugar fermentation tests.

If any case or control was found positive for Candida by direct microscopy and culture, they were advised to apply standard dosage of clotrimazole mouth paint and reviewed after 2 weeks, and the swab was repeated. In case Candida was present on follow-up, they were asked to continue the medication for 2 more weeks and reviewed.

Statistical analysis

The data was entered on a Microsoft Excel Spreadsheet and imported into Statistical Package for Social Sciences (SPSS) version 20 (SPSS Inc, Chicago, IL, USA) for statistical analysis. Data was presented in mean ± (S.D.) and median (minimum–maximum) as applicable. Data was compared in two groups by Wilcoxon rank-sum (following non-normal distribution) and a P value less than 0.05 was considered statistically significant.

 Results



The mean age of subjects with diabetes (study) was 32.89 years (age range 5–76 years), whereas the mean age for non-diabetic subjects (controls) was 30.3 years (age range 3–74 years). The mean age of type 1 diabetes subjects was 26.2 years, and for type 2 diabetes was 49.6 years.

The study comprised of total 900 subjects of which 470 were diabetic and 430 were non-diabetic subjects [Table 1]. Among the 470 diabetic patients, only 164 had a family history of diabetes. Out of the 336 type 1 diabetes individuals (n = 336), only 120 had a positive family history of diabetes. Forty-four subjects with type 2 diabetes (n = 134) had a family history of the disease. The mean duration of disease (diabetics) in type 1 subjects (n = 336) was 11.7 ± 7.8 years. The mean duration of disease (diabetics) in type 2 subjects (n = 134) was 6.9 ± 5.9 years.{Table 1}

Overall prevalence of candidiasis

The overall prevalence of Candida in diabetics was 22.1%, as compared to 9.7% in non-diabetics [Table 2]. Among the diabetics, the prevalence of Candida was equally distributed between the type 1 (22.6%) and type 2 (20.8%). Fifty-six males out of 247 and 48 females out of 223 showed the presence of Candida in the oral cavity [Table 3] (P value = 0.322).{Table 2}{Table 3}

Among the species-specific prevalence, C. albicans was the most common species (97.1%), and isolated cases of other species like C. rugosa, C. tropicalis and C. glabrata were also observed. However, non-albicans Candida, i.e. C. haemolunii was also reported in one of the controls.

The prevalence of Candida in individuals with the duration of type 1 diabetics less than ten years (n = 149) was observed to be 23.4%, whereas in individuals with disease duration more than 10 years (n = 187), it was 21.9% [Table 4] which was statistically non-significant.{Table 4}

The prevalence of C. albicans was 24.7% (n = 231) among the type 1 diabetics with glycaemic control above 7 and 17.5% (n = 40) in patients with glycaemic control below 7. Among the type 2 diabetic individuals, the prevalence of C. albicans was 27.4% (n = 84) in patients with glycaemic control above 7 and 7.7% (n = 13) in patients with glycaemic control below 7, with the difference being statistically significant [Table 5].{Table 5}

Oral health status among diabetic and non-diabetic individuals

The mean number of decayed, missing and filled teeth (DMFT) was higher in type 2 than type 1 diabetics. In disease duration of more than 10 years in type 2 diabetic population, the mean number of missing and filled teeth was higher than the other group, but this difference was not significant. When comparing type 1 diabetic population based on HbA1c level (below and above 7), there was no statistically significant difference seen in patients with controlled or uncontrolled diabetes. On comparing type 2 diabetic population based on HbA1c level, the mean number of DMFT score was higher in patients with uncontrolled diabetes (HbA1c above 7) than controlled diabetes, but this difference was not statistically significant [Table 6] and [Table 7].{Table 6}{Table 7}

Oral hygiene status of 12.3% of diabetic patients was poor, in contrast to 9% non-diabetic subjects, with the difference being statistically significant (P value < 0.04). Pattern of distribution of OHI between type 1 and type 2 diabetics was comparable [Table 8].{Table 8}

 Discussion



In the present study, investigators attempted to primarily estimate the prevalence of oral candidiasis in diabetic patients through a hospital-based cross-sectional study. It was also aimed to evaluate various factors that have been associated with the oral presence of Candida in diabetic patients, such as the type and duration of the disease and the degree of glycaemic control.

The large sample used in this study overcame the limitation of previous studies having similar methodology.[13],[14],[15],[16],[17] The sample of diabetics included patients visiting the endocrine clinic of a tertiary care hospital, undergoing treatment or making follow-up visits after long-term therapy.

In view of the comfort of the patient, ease and less time consumption, the oral swab technique was used in the present study for isolation of Candida within the oral cavity. Also, the Sabouraud Dextrose Agar (SBA) culture technique followed by the germ tube test used in the study is considered a significantly better method for identifying oral Candida.[18]

The overall prevalence of oral Candida among diabetics in our study sample was 22.1%, and with 22.6% type 1 and 20.8% type 2 diabetics. Mohammadi et al.[7] (2016) reported a higher prevalence of 55% in the diabetic group age range of 40-50 years in a diabetic clinic in Iran. Whereas Shenoy et al.[14] (2014) found oral Candida in 31% in a small sample of diabetics (type 1 and type 2) in a South Indian state, using a simpler oral rinse technique to isolate Candida from the cavity. The prevalence in the present study was lower than other regions, probably due to the socio-demographic factors of the study population which was primarily an urban and educated population with relatively better oral hygiene. The difference in sampling techniques could also attribute to the disparity in prevalence reported by different investigators.

The prevalence of Candida species in the oral cavity of non-diabetic individuals was observed to be 9.7%, which is within the range of 3% to 47%, as reported by Soysa et al.[8] Many of the previous studies have also reported similar prevalence of Candida in non-diabetics, like Al-Attas and Amro 2010 (14.3%),[15] Shenoy et al. 2014 (7%)[14] and Mohammadi et al. 2016 (27%).[7] However, one of the recent studies by Bremenkamp et al.[19] in 2011 shows no significant difference in the prevalence of Candida species between diabetics and healthy controls.

Candida albicans was the commonest species isolated from the oral cavity of diabetics in the present study (97.1%). It could be attributed to the fact that C. albicans is the most communal of the Candida species, and it grows as a biofilm consisting of a complex community of cells embedded in extracellular polysaccharide matrix. Other Candida species isolated apart from Candida albicans included Candida rugosa, Candida tropicalis and Candida glabrata. The Candida haemolunii was recovered from the oral cavity of one non-diabetic individual. This finding is in concordance with the previous studies by Abu-Elteen et al., 2006 (81.8%)[20] and Anil Kumar et al., 2014 (51%),[21] irrespective of their methodology.

In the present study, individuals with type 1 diabetes showed higher colonisation of Candida in the oral cavity. Candida albicans was the most frequent species to be isolated. There are also reports of few other species, like Candida rugosa, Candida tropicalis and Candida glabrata being found in some type 1 diabetic patients, but Candida albicans was the only species recovered from the oral cavities of type 2 diabetics. Thus, the present study is in concordance with the previous reports that oral yeast colonisation is higher in type 1 than in type 2 diabetics.[15],[17],[22] However, Sharma et al.[23] in 2017, using CHROM agar for speciation of Candida isolates, found a statistically significant increased colonisation of Candida in type 2 diabetics, compared to controls.

High glycosylated haemoglobin concentration is considered to be an important factor that affects the rate of Candida carriage and subsequent development of candidiasis in diabetics. It is due to the increased salivary glucose levels that may promote the overgrowth of Candida.[6],[24],[25] In the present study, we observed a higher prevalence of Candida (irrespective of the type of diabetes) in patients having HbA1c level more than 7. This was in concordance with studies by Khosravi et al. (2008)[26] and Al Mubarak et al. (2013)[27] that stated that the degree of Candida prevalence in the oral cavity may be altered by levels of blood glucose. In contrary to the findings of the present study, Manfredi et al. (2002)[28] and Fisher et al. (1987)[29] found the frequency and the carrier state of Candida to be independent of the HbA1c level.

There was no statistically significant difference seen in the prevalence of Candida with the duration of the disease in this study. The prevalence of Candida in individuals with less than 10 years and more than 10 years was not found to be significantly different in both type 1 and type 2 diabetes. We did not find any other study in literature for the effect of duration of diabetes on the prevalence of Candida.

Individuals with diabetes endure numerous problems during the course of their lives, including dental and oral health problems. Thus, the secondary objective of this cross-sectional study was to evaluate the effects of diabetes on dentition and oral health status. It was found that the mean DMFT score was numerically higher in diabetic individuals as compared to non-diabetics, but this difference was not significant. Albrecht et al. (1988)[30] and Tanwir et al. (2009)[31] also found similar observations in their studies. However, Bacić et al. (1989)[32] and Tenovuo et al. (1986)[33] reported almost equal DMFT score in both the groups.

It was also noted that diabetics are more prone to accumulation of debris and calculus, in spite of similar oral hygiene habits as non-diabetics. This could be due to the fact that excess glucose reaches the oral cavity through saliva and gingival crevicular fluid in patients with poor metabolic control, and contributes to a sugar-rich bio-film, which enhances plaque and calculus growth. This finding was in accordance with Radhika and Ranganathan (2014),[34] Orbak et al. (2008)[35] and Arrieta-Blanco et al. (2003)[36] who also concluded that oral hygiene index was significantly increased in diabetics compared to non-diabetics. However, a few other studies[37],[38],[39] were not in concordance with the present study and concluded that there is no significant difference in oral hygiene status among diabetic and non-diabetic patients.

The number of decayed teeth in the patients with type 2 diabetes with a history of disease less than 10 years is considerably higher than in patients with type 1 diabetes, thus suggestive of more decay activity in these patients. This pattern is however reversed in patients with history of disease for more than 10 years, and corresponding considerable increase in the number of missing teeth in patients with type 2 diabetes. The continued pattern of relatively low numbers of filled teeth in both groups is also suggestive of the neglect towards the dentition and potential loss of salvageable teeth.

Limitations

The number of subjects with clinical signs and symptoms of oral candidiasis were very low as compared to the previous studies. Therefore, the findings of this study may be seen with caution.

A more advanced speciation method like RT-PCR or whole genome sequencing could have added more value to the study.

 Conclusions



Within the constraints, the following conclusions may be drawn from the present observational cross-sectional study:

There was a two-fold increase in the prevalence of oral candidiasis in diabetic patients (22.1%) as compared to non-diabetics (9.7%).Candida albicans was the most common species isolated from the oral cavity of diabetics (97.1%).The prevalence of oral candidiasis was not dependent upon the type of diabetes. However, a higher prevalence of candidiasis was observed in subjects with poor glycaemic control, i.e., HbA1c more than 7, irrespective of the type of diabetes.The mean DMFT and poor oral hygiene status were higher in diabetics. Thus, patients suffering from diabetes had a higher burden of care for dental therapy.

As the number of people suffering from diabetes is increasing in our country over the last decade, the education and management of patients are both justified and appropriate. Thus, the dental professionals who are in a position to have a considerable, positive effect on the oral and overall health of patients with diabetes mellitus must make constant efforts in this direction. Regular dental check-ups and advice on meticulous oral hygiene practices must be imparted to all patients.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patients have given their consent for their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

The project was funded by the Indian Council for Medical Research as a part of an extramural funding project. The authors RD, RG, IX and VM were the investigators of the project sanctioned by ICMR. The authors ID and AT did significant contribution in data filteration, preparation, analysis, helped in manuscript writing and final approval of the manuscript along with other authors.

Conflicts of interest

There are no conflicts of interest.

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