Oral Manifestations of Diabetes Mellitus in Controlled and Uncontrolled Patients

 
Maria Rozeli S. QUIRINO[1]
Esther G. BIRMAN[2]
Claudete R. PAULA[3]
 
[1]University of Taubaté.
[2]Department of Stomatology, School of Dentistry, University of S. Paulo.
[3]Department of Microbiology, Biomedical Science Institute, University of São Paulo. São Paulo, SP, Brasil

Braz Dent J (1995) 6(2): 131-136 ISSN 0103-6440

| Introduction | Material/Methods | Results | Discussion | Conclusions | References |


The authors studied the oral manifestations of a sample of 70 diabetic patients, divided in controlled and uncontrolled patients. Medical history and stomatological data were analyzed and diabetic controlled patients were matched to uncontrolled patients. The main symptoms observed were hyposalivation, taste alterations and burning mouth, with the main sign being parotid enlargement. The lesions observed were candidosis of the erythematous type and proliferative lesions both associated to the use of total prosthesis. No pathognomonic lesions or alterations could be observed in relation to the disease. The frequency of carriers of Candida albicans and also the lesions observed could be compared to normal patients also using total dentures.


Key words:diabetes mellitus, oral manifestations, diabetes.


Introduction

Oral manifestations of diabetes mellitus have been discussed in the literature for a long time but many controversial aspects of signs and symptoms are being reviewed today. Symptoms such as hyposalivation or xerostomia associated to burning mouth, loss of taste, enlargement of salivary glands, mycotic infections represented by candidosis and other less frequent lesions such as lichen planus are reported (Russoto, 1981; Murrah et al., 1985; Gibson et al., 1990; Albrecht et al., 1992). Thus, we studied a group of controlled and uncontrolled diabetic patients in order to observe their main symptoms, signs or lesions presented and correlate them, or not, to their systemic disease.

Patients and Methods

From a group of 120 diabetic patients diagnosed with diabetes type II from the Endocrinology Department of the Hospital of the University of Taubaté in São Paulo, Brazil, 70 with no other severe health problem were randomly selected and divided into two groups. The first group was composed of 35 controlled diabetic patients who used insulin, oral hypoglycemics or an adequate diet. The second group was composed of 35 uncontrolled diabetic patients without dietary control. A special record was designed to obtain a good medical history, with special reference to symptoms and habits, as well as the clinical data obtained by the physician or endocrinologist and stomatologist.

There was a predominance of women in the group, totalizing 52 female patients, 44 of them white, and most from 50-60 years of age.

An accurate examination of the mouth, analysis of the salivary and dental conditions and of the prosthesis used were performed. Cultures for fungi were submitted to the mycology laboratory in order to characterize carriers and non-carriers of Candida, as well as to identify and determine the prevalence of Candida species.

The sample material was collected from the normal oral mucosae neighboring all areas clinically diagnosed as candidosis, either erythematous or pseudomembranous. Sterilized cotton swabs were used to obtain the material which was plated onto a Petri dish with Sabouraud dextrose agar medium (DIFCO), plus chloramphenicol (100 mg/ml) maintained at 25ºC, at least until 15 days. The different morphological colonies were selected and were sub-cultured on the same fresh medium in tubes. Yeast identification was performed using the Kreger-van Rij (1984) and Lodder (1970) criteria.


Results

The analysis of the medical data indicated a prevalence of high blood pressure predominantly in the uncontrolled group (68.6%).

Hyposalivation was the main oral symptom observed in both groups, although more frequent in the uncontrolled diabetics (82.8%) when compared to controlled diabetics (68.6%). Other symptoms such as alterations of taste, burning mouth sensation and signs of glandular enlargement are presented in Table 1. More than 60% of the patients from both groups were edentulous, with 81.8% using total dentures for 20 to 30 years (Table 2).
 
 


 
 


 
 


 
 

On oral examination, erythematous lesions on the palate of both groups, related to the prosthesis, and diagnosed as denture stomatitis associated to candidosis were observed. Only one case of candidosis, which was the pseudo-membranous type, was not related to the use of a prosthesis. Cultures were positive for Candida species in 35.7% and only 14.2% were related to clinical manifestations while the percent of carriers corresponded to 21.4% (Tables 3 and 4).

A unique case of herpetic infection was detected on the upper lip, without any recent history of this infection by other patients of both groups.

Proliferative lesions were observed in ten cases represented by fibrous hyperplasia in both groups, associated to the use of total prosthesis. Only two benign neoplasias, one papilloma and one fibroma, could be detected in these patients. Traumatic ulcerations were observed in relation to the poor conditions of the total dentures. A unique case of actinic cheilites was diagnosed (Table 4).
 
 


 
 

In older patients of both groups, Fordyce granules (18.6%) and varicosities of the tongue (27.1%) could be observed. Pigmentation of racial origin was detected in only one controlled diabetic patient.


Discussion

Pathognomonic lesions associated to diabetes do not seem to be very common, but some complaints are frequently present and similar in these patients even when they aren't associated to old age (Murrah et al., 1985; Gibson et al., 1990).

Hyposalivation, a very common symptom seems to be related to polyuria and the involvement of the parenchyma of major salivary glands. It is suggested that the substitution of the functioning tissue by adipose tissue modifies qualitatively and quantitatively saliva production, facilitates hyposalivation and burning mouth symptoms (Russoto, 1981; Murrah et al., 1985; Gibson et al., 1990; Zachariasen, 1992). On the other hand, the use of some medications, mainly diuretics, also seems to be directly associated to this symptom. The important role of saliva for the maintenance of microbiota equilibrium is well known. When saliva is decreased fungi such as Candida albicans or even the associated development of other species can increase. In our sample, the predominant clinical type of candidosis was erythematous, associated with total dentures with only one case of pseudo-membranous type. Our results are different from the clinical approaches reported in the literature, with the exception of Peters et al. (1966). Budtz-Jorgensen and Bertran (1970) and Oslen (1974) observed that healthy patients presented almost the same frequency or even more candidosis (denture sore mouth). Complete dentures can induce the proliferation of fungi, since with dentures the palatine mucosa does not self-clean. The association of decreased local vascular circulation due to the compression of the prosthesis with deficient higienic habits must also be considered (Oslen, 1974; Odds, 1988).

Atrophic lesions of the tongue have been described associated to Candida albicans by Farman and Nutt (1976), Lamey et al. (1988). It is suggested that diabetic patients have predisposed local factors related to possible damage of the microvascularization, concluding that decreased blood supply can predispose to infections like candidosis, due to a reduction of the local resistence of the tissues, which is not yet well explained.

In our opinion many aspects of the oral manifestations of diabetics are related to local problems which are not associated to the disease, whether controlled or not. A major frequency of candidosis was not observed in our patients, even uncontrolled, showing a large number of negative results (more than 60%), while carriers represented only 20%. About 14% of the patients presented positive cultures of Candida albicans associated to other species and related to lesions as also observed by Odds et al. (1978), Fisher et al. (1987) and Quirino et al. (1994). The association of oral candidosis and diabetes is still controversial, needing better evaluation.

Lamey et al. (1988) did not observe significant differences in relation to the number of microorganisms in treated diabetics, duration of disease or even age of the patient, considering as important local factors the wearing of a total prosthesis, hyposalivation and smoking. In previous experience with healthy patients, smoking did not interfere with the colonization of Candida in patients without total prothesis; this is also another aspect to be considered (Silveira et al., 1993).

It is necessary to point out the factors associated with a greater frequency of these microorganisms, since the increase of glucose in saliva promotes greater adherence of fungi to epithelial cells. Thus, blood glucose levels could also interfere with the defense mechanism of neutrophils, which in these patients present some altered functions, facilitating possible candidosis in the presence of local predisposing factors (Lamey et al., 1988; Odds, 1988; Darwazeh et al., 1991).

Proliferative lesions associated with dentures were related to the poor conditions of the prosthesis, and to the long time of usage associated with modifications of the hard supporting tissues.

Gibson et al. (1990) associated the finding of oral lichen planus to diabetes. More recent studies on the epidemiology of lichen planus in diabetic patients reported these lesions to be mainly of the erosive or ulcerative type (Brown et al., 1993). There is a possibility that immunological changes could be related as in non-diabetic patients, although these lesions were not observed in our study. Albrecht et al. (1992) believe that some antidiabetic drugs can produce lesions clinically similar to lichen planus, the so-called lichenoid reactions. The same authors also observed a prevalence of leukoplakia when comparing diabetic to healthy patients, correlating an atrophy of the oral mucosa to hyposalivation and deficient hygiene.

The bilateral enlargement of parotid glands has been unquestionably associated with diabetic patients and diagnosed as sialosis, although its real prevalence is not known. In our study, this aspect was observed in 48.7% of uncontrolled diabetics and in 28.5% of the controlled diabetics, very different from the results of Russoto (1981).

Birman et al. (1991), evaluating oral manifestations of geriatric patients, observed the main lesions to be varicosities of the tongue and Fordyce granules. These alterations were not associated to other systemic problems, as also observed in our study.


Conclusions

I -Hyposalivation was the main complaint of diabetic patients, especially in uncontrolled ones.

II -Symptoms such as alteration of taste, burning mouth and signs of salivary gland enlargement, mainly parotid, could be associated to the disease.

III -Erythematous candidosis was the prevalent type observed, associated to the use of upper total denture or prosthesis (denture stomatitis).

IV -Other lesions observed such as varicosities of the tongue and the presence of Fordyce granules was related to age and not to the disease.

V -Hyperplastic lesions were correlated to poor conditions of the total prosthesis, long time of usage and local modifications of the hard support tissues.

VI -No pathognomonic lesions of the oral mucosa could be associated to diabetes mellitus.


References

Albrecht M, Banoczy J, Dinya E, Tamas JRG: Occurrence of oral leukoplakia and lichen planus in diabetes mellitus. J Oral Pathol Med 21: 364-366, 1992

Birman EG, Silveira FRX, Sampaio MCC: Study of oral mucosal lesions in geriatric patients. Rev Fac Odontol FZL 3: 17-25, 1991

Brown RS, Bottomley WK, Puent E, Lavigne GJ: A retrospective evaluation of 193 patients with oral lichen planus. J Oral Pathol Med 22: 69-72, 1993

Budtz-Jorgensen E, Bertran V: Denture stomatitis. I. The etiology in trauma and infection. Acta Odont Scand 28: 71-90, 1970

Darwazeh AMG, MacFarlane TW, McCuish A, Lamey PJ: Mixed salivary glucose levels and candidal carriage in patients with diabetes mellitus. J Oral Pathol Med 20: 280-283, 1991

Farman AG, Nutt G: Oral candida, debilitating disease and atrophic lesion of the tongue. J Biol Buc 4: 203-226, 1976

Fisher BM, Lamey PJ, Samaranayake LP, MacFarlane TW, Frier BM: Carriage of candida species in the oral cavity in diabetic patients: relationship to glycaemic control. J Oral Path 16: 282-284, 1987

Gibson J, Lamey PJ, Lewis M, Frier B: Oral manifestations of previously undiagnosed non-insulin dependent diabetes mellitus. J Oral Pathol Med 19: 284-287, 1990

Kreger-van Rij Njw (Editor): The yeast: a taxonomic study. 3rd ed. Elsevier, Amsterdam, 1984

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 Path 17: 354-357, 1988

Lodder J (Editor): The yeast: a taxonomic study. 2nd ed. Elsevier North Holland, Amsterdam 1970

Murrah VA, Crosson JT, Sauk JJ: Parotid gland basement membrane variation in diabetes mellitus. J Oral Path 14: 236-246, 1985

Odds FC: Candida and Candidosis. 2nd ed. Bailliére Tindall, London, Philadelphia, 1988

Odds FC, Evans EGV, Taylor MAR, Wales JL: Prevalence of pathogenic yeasts and humoral antibodies to candida in diabetic patients. J Clin Path 31: 840-844, 1978

Oslen I: Denture stomatitis. Occurrence and distribuition of fungi. Acta Odont Scand 32: 329-333, 1974

Peters RB, Bahn AR, Barens G: Candida albicans in the oral cavities of diabetics. J Dent. Res 45: 771-777, 1966

Quirino MRS, Birman EG, Paula CR, Gambale W, Corrêa B, Souza VM: Distribution of oral yeasts in controlled and uncontrolled diabetic patients. Rev Microbiol 25: 37-41, 1994

Russoto SB: A symptomatic parotid gland enlargement in diabetes mellitus. Oral Surg Oral Med Oral Pathol 52: 594-598, 1981

Silveira FRX, Paula CR, Birman EG, Batista JM: Proteinase and phospholipase activity of Candida albicans isolated from oral mucosa of healthy carriers (smokers and non-smokers). Rev Iberoam Micol 10: 26-29, 1993

Zachariasen R: Diabetes mellitus and xerostomia. Compendium, XIII: 314-324, 1992


Correspondence:Esther G. Birman, Rua Gabriel dos Santos 168 / apt 51-A, São Paulo, SP, Brasil. FAX : 55-011-818-7883. E-mail: egbirman @ siso.fo.usp br.


Accepted August 14, 1995
Electronic publication: March, 1996


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