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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 33  |  Issue : 3  |  Page : 301-305

Candida prevalence in the saliva of controlled and uncontrolled diabetic patients – A clinical study


1 Department of Oral Medicine and Radiology, Himachal Institute of Dental Sciences, Paonta Sahib, Himachal Pradesh, India
2 Department of Oral Medicine and Radiology, Dasmesh Institute of Research and Dental Sciences, Faridkot, Punjab, India
3 Department of Periodontology and Implantology, Dasmesh Institute of Research and Dental Sciences, Faridkot, Punjab, India
4 Department of Oral Medicine and Radiology, Sri Sukhmani Dental College and Hospital, Dera Bassi, Mohali, Punjab, India
5 Department of Oral Medicine and Radiology, BRS Dental College and Hospital, Barwala, Panchkula, Haryana, India
6 Department of Prosthodontics, Sri Sukhmani Dental College and Hospital, Dera Bassi, Mohali, Punjab, India

Date of Submission04-Aug-2020
Date of Decision25-Feb-2021
Date of Acceptance06-Aug-2021
Date of Web Publication28-Sep-2021

Correspondence Address:
Dr. Mehta Ruchi
Department of Oral Medicine and Radiology, Himachal Institute of Dental Sciences, Paonta Sahib, Himachal Pradesh - 173 025
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jiaomr.jiaomr_167_20

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   Abstract 


Context: Diabetes mellitus is a major cause of mortality and morbidity worldwide. The health of oral tissue is related to saliva and both the composition and flow of saliva are altered in diabetic patients. Aim: This study aims to assess the prevalence of Candida in diabetic patients and non-diabetic controls and to assess the relationship between the candidal carriage and glycemic control, the relationship between the oral prevalence of Candida species, and clinical candidal infection, and the effect of antidiabetic therapy and smoking on candidal infection. Settings and Design: This cross-sectional population-based study was conducted on 100 diabetic and 50 non-diabetic (control) patients. Methods and Material: Saliva samples were collected and the concentrated oral rinse technique was used for quantitative oral candidal isolation. A digital colony counter enumerated several candidal colonies on each plate. Statistical Analysis Used: Chi-square test and Mann–Whitney test are used. Results: Colony-forming units (CFU/ml) in diabetics were 3131.14 and in control was 986.8. Out of 55 diet control patients, 30 had a candidal carrier; out of 44 patients on oral hypoglycemic, 30 had candidal carrier; and out of 1 patient on insulin, 1 had a candidal carrier. Out of 19 diabetics (good control), 8 had candidal carrier; out of 28 (moderate control), 12 had candidal carrier; and out of 53 (poor control), 41 had a candidal carrier. Out of 14 smokers, 8 had candidal carriers, and out of 36 nonsmokers, 11 had candidal carriers. Conclusions: Diabetic patients carry a higher number of candida in their oral cavity.

Keywords: Candida, diabetes, smokers


How to cite this article:
Ruchi M, Sandeep K B, Archana B, Nisha D, Sukriti M, Deepika. Candida prevalence in the saliva of controlled and uncontrolled diabetic patients – A clinical study. J Indian Acad Oral Med Radiol 2021;33:301-5

How to cite this URL:
Ruchi M, Sandeep K B, Archana B, Nisha D, Sukriti M, Deepika. Candida prevalence in the saliva of controlled and uncontrolled diabetic patients – A clinical study. J Indian Acad Oral Med Radiol [serial online] 2021 [cited 2021 Nov 29];33:301-5. Available from: https://www.jiaomr.in/text.asp?2021/33/3/301/326895




   Introduction Top


Diabetes mellitus is a significant global public health problem and is a major source of morbidity and mortality.[1],[2]

The health of oral tissue is related to saliva and both the composition and flow of saliva may be altered in diabetic patients.[3],[4] Uncontrolled diabetes mellitus is a predisposing factor to fungal infections, especially those caused by Candida species.[5],[6] The present study was carried to assess the prevalence of Candida in diabetic patients and nondiabetics, the relationship between the candidal carriage and glycemic control, the relationship of Candida species and clinical candidal infection, and the effect of antidiabetic therapy and smoking on candidal prevalence.

Study design and settings

This study was conducted on randomly selected 100 diabetic patients of both genders.

Sample size estimation

The sample size for the study was calculated considering 80% power at 5% α error (i.e. the false positive rate, as large as we can tolerate, almost always, α=5%) to be as N=100 based on the studies conducted previously by Abu Elteen KH et al.[4]

Inclusion and exclusion criteria

Inclusion criteria selected in the study were diabetic patients irrespective of their glycemic control in the age range of 30–70 years and 50 non-diabetic patients in the same age range as controls. Patients were classified into diabetics and non-diabetics (control) based on glycated hemoglobin values (HbA1c).

Patients presently on antibiotic therapy, steroid therapy, chemotherapy, antiseptic mouthwashes, radiation therapy, hormonal supplements, and pregnant patients were excluded from the study.

Ethical clearance, informed consent

The approval for the study was obtained before starting the study from the Institutional ethical committee (vide reference letter no. – 446 A, Dated 6-2-20). The ethical standard of study was as per the guidelines provided by The Committee for the Purpose of Control and Supervision of Experiments on Animals (CPCSEA) and “World Medical Association Declaration of Helsinki on Ethical Principles for Medical Research involving Human.” All patients were informed regarding the study and their consent was obtained.

General details of patients, such as name, age, and gender were recorded.

Collection of blood sample

Five millimeters of venous blood was taken from median cubital vein under sterilized conditions and blood investigations such as fasting blood sugar and glycosylated hemoglobin level were measured. The serum sample was analyzed using the standard glucose oxidase method. Glycosylated hemoglobin was estimated by an ion-exchange method using a commercial kit—Lifechem GHb.

For diabetics. the HbA1c value >6.5% and for control HbA1c value <5.7% were considered. Based on HbA1c value, good control: 6.0–8.0%; moderate control: 8.0–10.0%; and poor control: >10%.

A thorough intraoral examination was carried out for various conditions like median rhomboid glossitis, atrophic glossitis, fissured tongue, pseudomembranous candidiasis, and angular cheilitis.

Collection of saliva samples

Unstimulated mixed saliva was analyzed in this study. Saliva samples were collected in the morning hours between 9 am and 11 am. Before the collection of the saliva samples, patients were refrain from eating and drinking anything for at least 90 minutes before the procedure. The concentrated oral rinse technique was used for quantitative oral candidal isolation. The sample thus obtained was then centrifuged at 3000 rpm for 15 min. The supernatant was discarded and the rest was diluted with 1 ml phosphate-buffered saline for optimal microbial disaggregation.

Candida estimation

A spiral platter was used to inoculate 50 μl of the rinse onto Sabouraud's dextrose agar using the pour-plate technique [Figure 1] under sterile conditions in an ultraviolet inoculation chamber. The plates were then incubated aerobically at 37°C for 48 h. After incubation, the growth of Candida was identified by smooth, white, or creamy-colored buttery colonies [Figure 2].
Figure 1: Pour plate technique

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Figure 2: Candida colonies

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Several candidal colonies on each plate were enumerated by a digital colony counter [Figure 3] and several CFU/ml of oral rinse were derived by the formula: CFU/ml = 1000 × number of colonies/4.
Figure 3: Digital colony counter

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Statistical analysis

The data thus obtained were tabulated and statistically analyzed using mean, standard deviation, Chi-square test, and Mann–Whitney test.


   Results Top


There were 61 (61%) candidal carriers in diabetic and 19 (38%) in control. The difference was significant (P < 0.05) [Table 1]. There were 31 (57.4%) candidal carrier males and 30 (65.2%) females in diabetics. The difference was nonsignificant (P > 0.05) [Table 2]. There were 11 (35.4%) candidal carrier males and 8 (42.1%) females in controls. The difference was nonsignificant (P > 0.05) [Table 3].
Table 1: Candidal carriage among diabetics and controls

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Table 2: Candidal carriage among males and females in diabetics

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Table 3: Candidal carriage among males and females in controls

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Colony-forming units (CFU/ml) in diabetics were 3131.14 and in control were 986.8. Mann–Whitney test revealed significant differences in both groups (P < 0.05) [Table 4], [Graph 1].
Table 4: CFU/ml among diabetics and controls

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Out of 55 diet control patients, 30 (54.5%) had candidal carrier; out of 44 patients on oral hypoglycemic, 30 (68.1%) had candidal carrier; and out of 1 patient on insulin, 1 (100%) had a candidal carrier. Chi-square test showed nonsignificant difference (P > 0.05) [Graph 2].



Out of 19 diabetics (good control), 8 (42.1%) had candidal carrier; out of 28 (moderate control), 12 (42.8%) had a candidal carrier; and out of 53 (poor control), 41 (77.3%) had candidal carrier [Table 5]. Intergroup comparison between good and moderate control diabetics was nonsignificant (P: 0.95), moderate and poor was significant (P: 0.005); and good and poor had a significant (P: 0.002) difference.
Table 5: Candidal carriage in diabetics in relation to glycemic control

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Out of 14 smokers, 8 (57.1%) had candidal carriers and out of 36 nonsmokers, 11 (30.5%) had candidal carriers. The difference was nonsignificant (P > 0.05) [Graph 3]. [Graph 4] shows that out of 61 diabetic carriers, 18 (29.5%) had clinical candidal infection and out of 19 control carriers, 3 (15.7%) had a clinical candidal infection. The difference was nonsignificant (P > 0.05).




   Discussion Top


It is well established that uncontrolled diabetes mellitus is a predisposing factor to fungal infections, especially those caused by Candida species. The course of infection is also more complicated in these patients.[7] Several factors are associated with the oral carriage of Candida in diabetic patients such as type of diabetes, degree of glycemic control, mode of treatment, and various other local predisposing factors like oral hygiene, smoking, and presence of dentures in the mouth.[8] The present study was carried to assess the prevalence of Candida in the saliva of diabetic patients and controls, to find out the relationship between the candidal carriage and glycemic control, to investigate the relationship between the oral prevalence of Candida species and clinical candidal infection; and the effect of antidiabetic therapy and smoking on candidal prevalence.

In the present study, we observed Candida was more prevalent in the oral cavity of diabetics (61%) than controls (38%). This is following the observations by Taper Jones et al.[9]

CFU is usually recorded to obtain the clinical data, essentially to establish a clinical diagnosis of oral candidiasis. The total number of Candida present in the oral cavity is thought to be important in the development of infection. There were 31 (57.4%) candidal carrier males and 30 (65.2%) females in diabetics. There were 11 (35.4%) candidal carrier males and 8 (42.1%) females in controls. Epstein et al.[7] have demonstrated that carriers and patients with oral candidiasis can be reliably distinguished based on quantitative cultures. In the present study, the mean candidal load for diabetic patients was 3131.14 CFU/ml, and for non-diabetic controls, the mean value was 986.84 CFU/ml, thus showing that CFU of Candida was significantly higher in diabetic patients than in controls.

It is established that diabetes predisposes to the high oral candidal carriage. If so, the question arises whether control of diabetes mellitus with antidiabetic therapy could prevent the carriage of Candida. We found that out of 55 diet control patients, 30 (54.5%) had candidal carrier; out of 44 patients on oral hypoglycemic, 30 (68.1%) had candidal carrier; and out of 1 patient on insulin, 1 (100%) had a candidal carrier. We have established that there was no relationship between the oral candidal carriage and the antidiabetic therapy. Kumar et al.[10] classified patients according to antidiabetic therapy used. It was found that in four diabetic patients, only one (25%) male had an oral candidal carriage. It was observed that in patients on diet alone, only four males and three females showed oral candidal carriage. In diabetic patients having controlled on diet with oral antidiabetic drugs, the oral candidal carriage was observed in 14 (73.68%) male cases out of 19 cases and in 15 (71.43%) female cases out of 21 cases. They did not find any relationship between antidiabetic therapy and oral candidal carriage. Bhuyan et al.[11] also observed that the method of diabetic treatment appeared to have no relationship with oral candidal carriage.

Being diabetic may not place a person at increased risk of fungal infections, unless diabetic control is very poor. In the present study, out of 19 diabetics (good control), 8 (42.1%) had candidal carrier; out of 28 (moderate control), 12 (42.8%) had candidal carrier; and out of 53 (poor control), 41 (77.3%) had a candidal carrier. We observed that although the number of patients having clinical candidal infections was more in the diabetic group as compared to the control group and most of them belonged to poorly controlled glycemic group, the difference in results between the two groups was not statistically significant. This is following Tapper Jones[9] and Willis.[12] Many aspects of oral manifestations of diabetes are related to local factors which are not associated with the disease, if well controlled. Thus, a high frequency of clinical candidiasis was not observed in the whole of the poorly controlled group. The development of oral candidiasis is not the result of a single entity, but a combination of risk factors.

We found that out of 14 smokers, 8 (57.1%) and out of 36 nonsmokers, 11 (30.5%) had candidal carriers. Out of 61 diabetic carriers, 18 (29.5%) had clinical candidal infection and out of 19 control carriers, 3 (15.7%) had a clinical candidal infection. The difference was nonsignificant (P > 0.05).

Darwazeh et al.[13] found that 42 (84%) of the smokers and 37 (74%) of the nonsmokers had candidal species. The mean CFU/ml was 333 in smokers and 268 in nonsmokers. The author suggested that tobacco smoking did not appear to increase oral colonization with Candida species in nonsmokers. In the present study also, we found a nonsignificant difference of Candida species in smokers and nonsmokers which was following Rasool et al.[14] and Conley et al.[15]

Limitations and Future Prospects

Information on the candidal carriage in diabetic patients is often contradictory, possibly because of a variety of sampling techniques that have been employed and also to the different patient and control populations chosen by various investigators.

The shortcoming of the present study is a small sample size. The variation in the results may be because of the specific technique used.

Both local and systemic factors play a role in establishing clinical candidiasis and so the diabetic patients carrying a higher number of Candida in their oral cavity were encouraged to control local factors by maintaining adequate oral hygiene. However, more studies are necessary to determine the relations between other important combinations of risk factors and oral Candida.


   Conclusion Top


Oral candidal prevalence was higher in diabetic patients than in control patients. The carriage rate in the oral cavity increased as the glycemic control becomes worse. No significant association was found between the candidal carriage and antidiabetic therapy and smoking and clinical candidal infections.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/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

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
Soysa NS, Samarnayake LP, Ellepola ANB. Diabetes mellitus as a contributory factor in oral candididasis. Diabet Med 2005;23:455-9.  Back to cited text no. 1
    
2.
Zaremba ML, Daniluk T, Rozkiewiez D, Cylwik-Rokicka D, Kierklo A, Tokajuk G, et al. Incidence rate of candida species in the oral cavity of middle aged and elderly subjects. Adv Med Sci 2006;51:233-6.  Back to cited text no. 2
    
3.
Willis AM, Coulter WA, Hayes JR, Bell P, Lamey PJ. Factors affecting the adhesion of Candida albicans to epithelial cells of insulin using Diabetes mellitus patients. J Med Microbiol 2000;49:291-3.  Back to cited text no. 3
    
4.
Abu-Elteen KH, Hamad MA, Salah SA. Prevalence of oral Candida infections in diabetic patients. Bahrain Med Bull 2006;28:1.  Back to cited text no. 4
    
5.
Young G, Resca HG, Sullivan MT. The yeasts of normal mouth and their relation to salivary acidity. J Dent Res 1951;30:426-30.  Back to cited text no. 5
    
6.
Tang HJ, Liu WL, Lin HL, Lai CC. Epidemiology and prognostic factors of candidemia in elderly patients. Geriatr Gerontol Int 2015;15:688–93.  Back to cited text no. 6
    
7.
Epstein JB, Pearsall NN, Truelove EL. Quantitative relationship between Candida albicans in saliva and the clinical status of human subjects. J Clin Microbiol 1980;12:475-6.  Back to cited text no. 7
    
8.
Lamey PJ, Darwaza A, Fisher BM, Samaranayake LP, Macfarlane TW, Frier BM. Secretor status, candidal carriage and candidal infection in patients with diabetes mellitus. J Oral Pathol 1988;17:354–7.  Back to cited text no. 8
    
9.
Tapper Jones LM, Aldred MJ, Walher DM, Hayes TM. Candidal infections and populations of Candida albicans in mouths of diabetics. J Clin Pathol 1981;34:706-11.  Back to cited text no. 9
    
10.
Kumar BV, Padshetty NS, Bai KY, Rao MS. Prevalence of Candida in the oral cavity of diabetic subjects. J Assoc Physicians India 2005;53:599-602.  Back to cited text no. 10
    
11.
Bhuyan L, Hassan S, Dash KC, Panda A, Behura SS, Ramachandra S. Candida species diversity in oral cavity of type 2 diabetic patients and their in vitro antifungal susceptibility. Contemp Clin Dent 2018;1:83-8.  Back to cited text no. 11
    
12.
Willis AM, Coulter WA, Fulton CR, Hayes JR, Bell PM, Lamey PJ. Oral candidal carriage and infection in insulin treated diabetic patients. Diabet Med 1999;16:675-9.  Back to cited text no. 12
    
13.
Darwazeh AM, Al-Dwairi ZN, Al-Zwairi AA. The relationship between tobacco smoking and oral colonization with Candida species. J Contemp Dent Pract 2010;11:017-24.  Back to cited text no. 13
    
14.
Rasool S, Siar CH, Ng KP. Oral candidal species among smokers and non-smokers. J Coll Physicians Surg Pak 2005;15:679-82.  Back to cited text no. 14
    
15.
Conley LJ, Bush TJ, Buchbinder SP, Penley KA, Judson FN, Holmberg SD. The association between cigarette smoking and selected HIV-related medical conditions. AIDS 1996;10:1121-6.  Back to cited text no. 15
    


    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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