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Impact of clinical status and salivary conditions on xerostomia and oral healthrelated quality of life of adolescents with type 1 diabetes mellitus
cio SA, Brancher JA, Moyse s ST, Azevedo-Alanis LR. Impact of Busato IMS, Igna clinical status and salivary conditions on xerostomia and oral health-related quality of life of adolescents with type 1 diabetes mellitus. Community Dent Oral Epidemiol 2012; 40: 6269. 2011 John Wiley & Sons A S Abstract Objectives: To investigate the inuence of clinical status and salivary conditions on the presence of xerostomia on adolescents with and without type 1 diabetes mellitus (DM1), and further to investigate the inuence of clinical status, salivary conditions and xerostomia on oral health-related quality of life (OHQoL) of those with DM1. Methods: A cross-sectional study was performed on 102 adolescents, 51 with DM1 and 51 nondiabetics. Xerostomia was detected by asking a question about the sensation of having dry mouth, and Oral Health Impact Prole-14 was used to measure the impact of xerostomia on OHQoL. The clinical status was assessed by using decayed, missing or lled and Community Periodontal indices, and by evaluating oral manifestations; and the following salivary conditions were evaluated: stimulated salivary ow, pH, buffer capacity, total protein, amylase, urea, calcium, and glucose salivary concentrations. Multiple logistic regression analysis was used to evaluate the inuence of clinical status and salivary conditions on xerostomia and the impact of xerostomia on the OHQoL of adolescents with DM1. Results: Clinical status and salivary conditions was shown to have no inuence on the presence of xerostomia. Bivariate (P = 0.00) and logistic regression (P = 0.01) analysis showed a signicant association between DM1 and xerostomia. Logistic regression analysis showed association between xerostomia (P = 0.00) and OHQoL, and caries experience (P = 0.03) and OHQoL. Conclusions: DM1 showed to be predictive of a high prevalence of xerostomia in adolescents. Caries experience and xerostomia showed to have a negative impact on the OHQoL of adolescents with DM1.
rgio ApaIvana Maria Saes Busato1, Se cio2, Joa recido Igna o Armando Bran s2 and cher2, Simone Tetu Moyse 2 Luciana Reis Azevedo-Alanis
1
Department of Stomatology, 2School of Dentistry, Pontical Catholic University of , Curitiba, Brazil Parana
Key words: oral health; quality of life; saliva sIvana Maria Saes Busato, Programa de Po cia o em Odontologia, Pontif Graduac a lica do Parana PUCPR, Universidade Cato o, 1155 Curitiba, PR Rua Imaculada Conceic a 80215-901, Brazil Tel.: +55 41 3271 2592 Fax: +55 41 3271 1405 e-mail: ivanabusato@brturbo.com.br Submitted 14 February 2011; accepted 22 July 2011
Xerostomia is dened as a subjective sensation of having a dry mouth (1) and is reported by the patient (26). Xerostomia can result from a reduction in saliva secretion, although it may occur in spite of the presence of normal saliva ow rate (2). It is considered that both alterations in saliva
composition and in the quantity of saliva may play a role in the induction of xerostomia (7). Type 1 diabetes mellitus (DM1) is a metabolic dysfunction characterized by hyperglycemia resulting from denitive deciency in insulin secretion, caused by autoimmune illness and
doi: 10.1111/j.1600-0528.2011.00635.x
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genetic factors (8). The American Diabetes Association (ADA) reports that 75% of DM1 cases are diagnosed in persons below 18 years of age (9). Adolescence is a period of biological alterations and increased psychological, emotional, and cognitive maturity. This stage of life is marked by increased independence from family members and the quest for social involvement with friends. For these reasons, patients with DM1 can lose adherence to treatment and monitoring of the disease (10). Xerostomia (dry mouth) is one of the oral manifestations of DM (11, 12), and its prevalence varies from 24.1% in elderly patients with DM1 (3) to 76.4% in elderly patients with DM2 (13). In a recent study, xerostomia prevalence was demonstrated in 52.9% of adolescents with DM1 (14). The relationship between DM1 and clinical status (3, 11, 1522) has been widely investigated. Some studies have demonstrated differences in caries experience among adolescents with and without DM1 (3, 1517, 23), while others have not observed these differences (11, 18, 19). Periodontal conditions may be worsened in the presence of DM1 (15, 17, 18, 20, 23). Even when the prevalence of oral lesions is low in adolescence (23), it is higher in subjects with DM1 compared with nondiabetics, according to Belazi et al. (21). Similarly, the relationship between DM1 and salivary conditions (15, 16, 1821) has also been investigated. The presence of DM1 was either associated with a signicant reduction of salivary ow rate (SFR) in adolescents (16, 18) or it did not inuence the SFR in teenagers with DM1 (19, 20). The presence of DM1 was associated with changes in pH (20) and in the buffering capacity (BC) of saliva (20, 21) in adolescents. In contrast, Swanljung et al. (19) found no differences in salivary pH or in BC between patients with and without DM1. Some studies have shown differences in salivary concentrations of total proteins, glucose and calcium in patients with DM1 compared with nonDM1 subjects (15, 18), contrasting to studies that showed no differences between subjects with and without DM1 in relation to glucose (19), calcium (15), and total protein (21) salivary concentrations. Oral health clinical conditions may have an important impact on oral health-related quality of life (OHQoL). Locker (24) proposed a multidimensional model of oral health that is sensitive in investigating clinical conditions and their impact on OHQoL. In 1997, Slade (25) studied the possibility of evaluating this impact through the Oral Health Impact Prole OHIP-14 (14 questions), a
smaller version than the OHIP (49 questions), maintaining condence, validity, and accuracy. The relationship between OHQoL and xerostomia has been studied in recent research (14, 2631). Furthermore, xerostomia was shown to have a negative impact on the OHQoL of adolescents with DM1, although it did not present a relationship with hyposalivation (14). Both social incapacity and social disadvantages dimensions of OHIP-14 questionnaires of these adolescents showed to be signicantly affected by the presence of xerostomia (14). Others conditions rather than the SFR could be implicated in the sensation of dry mouth and even could inuence the OHQoL. In this study, caries experience, periodontal conditions, and mucosal lesions were assumed to inuence xerostomia (Fig. 1, dashed line) because caries experience (3, 1517, 23) and prevalence of oral lesions (21) were shown to be high in the presence of DM1, as periodontal conditions (15, 17, 18, 20, 23) were shown to be altered in the presence of DM1. Because the previous conditions and xerostomia represent oral manifestations of DM1, and, until now, it is known that any effect of diabetes on OHQoL is mediated through the effect of xerostomia, a theoretical model was proposed to explain the interactions among them (Fig. 1). Because previous studies with xerostomia either investigated diabetic subjects with variable ages or comprised subjects with type 1 and type 2 DM in the same study, which did not exclude others factors that could be involved with xerostomia, we decided to evaluate a selective group of adolescents with DM1. The aim of this study was to investigate the inuence of clinical status and salivary conditions
Type 1 diabetes mellitus
Clinical status
Salivary conditions
Xerostomia
Fig. 1. Theoretical model for explaining the impacts of type 1 diabetes mellitus on oral health-related quality of life.
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on the presence of xerostomia on adolescents with DM1. We hypothesized that adolescents with DM1 would have poorer OHQoL compared with a similar sample of nondiabetics; we further hypothesized that the presence of xerostomia, clinical status and salivary conditions could explain this difference.
OHQoL evaluation
Evaluation of the impact of xerostomia on OHQoL was performed using a Portuguese version of OHIP14 questionnaire (25, 32). This questionnaire has good psychometric properties and appears to be a useful measure of OHQoL in xerostomia (5). Patients were asked to answer the questionnaire considering the previous 6-month period. The answers were assessed using a Likert-type evaluation scale with ve points: never-0, rarely-1, sometimes-2, repeatedly-3, always-4. Replies stating sometimes, repeatedly, and always were considered as answers indicating a negative impact on OHQoL. Replies stating never and rarely were considered as not having an impact on OHQoL. To calculate the impact on OHQoL, the standardized weighted method was used. A weight was attributed to each question (25, 32, 33). The weight of each question was multiplied by the corresponding answer score (04). The nal scoring enabled values between 0 and 28 to be obtained. The higher the score, the greater the negative impact of xerostomia on OHQoL (32). The nal OHIP-14 scores were categorized as follows: 0 no impact; 13 low impact; 46 medium impact; 710 negative impact; 1116 high negative impact (33).
Population
A cross-sectional study was performed on adolescents, allocated between two groups: DM1 group comprised 51 adolescents with DM1, who received follow-up at the Diabetes Outpatients Department Federal University Teaching Hospiof the Parana tal, and non-DM1 group comprised 51 nondiabetic participants who were recruited from public high schools. DM1 diagnosis using the ADA (8) classication was established as a criterion for inclusion in DM1 group. The criterion for inclusion in nonDM1 group was that of nondiabetic adolescents who had not used any medication for at least 1 month. The exclusion criteria used for both groups were the following: presence of systemic conditions that could inuence the salivary gland physiology; psychotropic drugs users, smokers or illicit drugs users and alcohol users (14). Sex and age (1419 years) were matched between the groups (DM1 and non-DM1).
Clinical status
Clinical status assessment was performed by an appraiser and consisted of three examinations: physical intraoral examination, periodontal evaluation and dental caries experience (34). Any alteration to oral mucosa was recorded. The Community Periodontal Index (CPI) was used for periodontal evaluation. The examination was performed using a periodontal probe with a spherical tip. The CPI was evaluated by adding together the values of the six index teeth (rst molars in each quadrant, right upper central, and left mandibular central), whereby the total value could vary between 0 and 24. Dental caries experience was rated using the decayed, missing or lled (DMF) index for teeth. The examination was performed using a at clinical mirror. The criteria for diagnosis followed those proposed by WHO (34).
Xerostomia
Xerostomia was dened as a dry-mouth sensation, reported by the participant (1). Xerostomia was detected by asking: have you had a dry-mouth sensation every day for the last 6 months? If the answer was yes, xerostomia was considered to be present (6, 13, 14). Groups DM1 and non-DM1 were separated into four subgroups according to the presence of xerostomia: DM1 group with xerostomia (n = 27), DM1 group without xerostomia (n = 24), non-DM1 group with xerostomia (n = 8) and non-DM1 group without xerostomia (n = 43).
Salivary conditions
Salivary ow was evaluated by means of stimulated saliva collection. The method used was that of mechanical masticatory stimulation, using a piece of sterile rubber tourniquet of a standardized size (1.5 cm), masticated continuously by the patient for
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6 min. Saliva produced during the rst minute of stimulation was discarded. During the following 5 min, the patient expelled saliva into a sterilized universal collecting recipient that had been previously weighed using Marte analytical scales, o Paulo, SP, Brazil). The saliva model AL 500 (Sa was collected between 8 am and 10 am (14). Stimulated salivary ow rate (SSFR) was evaluated by means of the gravimetric method and expressed in millilitre per minute (35). Immediately following saliva collection, the salivary pH was assessed using a QUIMIS Q400BD pocket pH meter (direct electrode) (QUIMIS, Diadema, SP, Brazil). BC was determined by titration with 3 ml of HCl 5 mmol l added to 1 ml of saliva. After 10 min, the nal pH value was measured using a pocket pH meter (direct electrode) (36). The saliva samples were centrifuged (3000 g for 10 min) before being submitted to the biochemical tests. Total protein and calcium salivary concentrations were determined using the colorimetric method (LABTEST kits; Vista Alegre, MG, Brazil). Amylase concentration was determined using the kinetic colorimetric method (LABTEST kits). Urea concentration was determinedusingtheenzymaticcolorimetricmethod (LABTEST kits). Glucose was determined by the enzymic colorimetric method (BIOCLIN kits; Belo Horizonte, MG, Brazil). The biochemical salivary tests were performed three times.
Absence of xerostomia was coded as 0 and presence of xerostomia was coded as 1. Independent variables were the presence of DM1, clinical status, and salivary conditions. The fourth stage involved the use of a multiple logistic regression statistical model to investigate the probability of the occurrence of negative impact on OHQoL in the presence of xerostomia and according to clinical status and salivary conditions (Fig. 1). Two sets of analyses were undertaken; one included all participants (n = 102) and the other only adolescents with DM1 (n = 51). In the former, the independent variables were presence of DM1, presence of xerostomia, clinical status, and salivary conditions. In the latter, the independent variables were the presence of xerostomia, clinical status, and salivary conditions. In the analyses, OHIP-14 scores were used as a dependent variable, were reduced to two categories using median splits and were coded as 0 (not having negative impact) and 1 (having negative impact). The level of signicance applied to all the multiple logistic regression analysis was 5% (P < 0.05).
Results
Average age was 17 1.4 (1419), with the presence of 27 female participants and 24 male participants in both groups (DM1 and non-DM1). The presence of DM1 was associated with a high prevalence of xerostomia, worsening of clinical status and alterations to the salivary conditions (Table 1). Caries experience and the glucose, amylase, and urea salivary concentrations were not shown to be associated with xerostomia in the bivariate analysis (Table 1). The logistic regression analysis applied to the data of the 102 adolescents showed signicant association between DM1 and xerostomia (P = 0.01) (Table 2). The logistic regression analysis applied to the data of the 51 DM1 adolescents showed association between xerostomia and OHQoL (P = 0.00), and caries experience and OHQoL (P = 0.03) (Table 3). The bivariate analysis considering the presence of DM1 as a dependent variable indicated that there was a signicant difference between DM1 group and non-DM1 group in relation to xerostomia (P = 0.00), and that average OHIP-14 scores did not show a signicant difference between DM1 group and non-DM1 group (P > 0.05). Table 1 shows the bivariate analysis considering xerostomia as a dependent variable and n (%) or
Statistical analysis
Data analysis was performed in four stages using SPSS version 15.0 for Windows. Normality analysis was performed using the KolmogorovSmirnov test, and Levene test was used to analyse variance homogeneity. The rst stage consisted of performing the bivariate analyses considering the presence of DM1 as a dependent variable, using the Mann Whitney U-test and Fishers exact test. The level of signicance was set at P 0.05 and CI 95%. In the second stage, bivariate analysis was performed considering the presence of xerostomia in DM1 and non-DM1 groups as a dependent variable, using the KruskalWallis test, whereby statistical signicance was considered to be P 0.05 and CI 95%. The third stage was performed using a multiple logistic regression statistical model to investigate the probability of the occurrence of xerostomia in the presence of DM1, and according to clinical status and salivary conditions (Fig. 1). The xerostomia variable was used as a dependent variable.
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Busato et al. Table 1. Bivariate analysis of studied population, considering xerostomia as dependent variable DM1 group with xerostomia n = 27 2.81 (2.98) 2.04 (1.99) 4 (15) 1.037 7.9 4.99 164 780 4.967 0.600 0.181 (0.561) (0.44) (0.81) (99) (27) (2.235) (0.431) (0.226) DM1 group without xerostomia n = 24 4.58 (4.80) 1.63 (1.66) 7 (29) 0.885 7.73 4.63 139 750 5.407 0.796 0.144 (0.508) (0.61) (0.78) (82) (39) (1.738) (0.493) (0.126) Non-DM1 group with xerostomia n=8 3.13 (3.72) 0.88 (1.81) 0 (0) 1.345 7.19 4.20 201 781 4.036 0.313 0.100 (0.528) (0.09) (1.00) (206) (4) (1.565) (0.210) (0.128) Non-DM1 group without xerostomia n = 43 1.42 (1.74) 0.07 (0.33) 2 (5) 1.161 7.45 3.63 239 777 5.085 0.424 0.098 (0.599) (0.40) (1.09) (130) (10) (2.065) (0.361) (0.113)
Variables n (%) or mean (SD) Clinical status DMF index CPI Oral lesions, n (%) Salivary conditions SSFR pH BC Total protein (mg dl) Amylase (U dl) Urea (mmol l) Calcium (mmol l) Glucose (mmol l) OHQoL OHIP-14
7.0 (4.8)
2.8 (2.3)
3.4 (1.7)
4.3 (3.5)
DM1, type 1 diabetes mellitus; SSFR, stimulated salivary ow rate; DMF index, decayed, missing and lled; CPI, community periodontal index; BC, buffer capacity; OHQoL, oral health-related quality of life; OHIP, Oral Health Impact Prole. NS P > 0.05, *KruskalWallis Test. Table 2. Multiple logistic regression analysis of the studied population of adolescents (n = 102), considering xerostomia as dependent variable Independent variable DM1 B )1.581 SE 0.613 P-value 0.01 95% CI 0.062; 0.684
Variables P > 0.05. Stimulated salivary ow rate, decayed, missing and lled, community periodontal index, pH, buffer capacity, oral lesions, total protein, calcium, and glucose salivary concentrations. CI, condence interval; DM1, type 1 diabetes mellitus. Table 3. Multiple logistic regression analysis of the studied population of adolescents (n = 51) with type 1 diabetes mellitus, considering OHIP-14 scores as dependent variable Independent variables DMF ndex Xerostomia B 0.259 )2.367 SE 0.122 0.841 P-value 0.03 0.00 95% CI 1.021; 1.644 0.018; 0.487
Variables P > 0.05. Stimulated salivary ow rate, community periodontal index, pH, buffer capacity, oral lesions, total protein, calcium, and glucose salivary concentrations. CI, condence interval; DMF ndex, decayed, missing and lled; OHIP, Oral Health Impact Prole.
DM1 group (7.0) represents a negative impact of xerostomia on OHQoL (33). Tables 2 and 3 show the results of the logistic regression analyses performed. Amylase and urea salivary concentrations were not included in the regression analysis because there were no signicant differences among groups in the bivariate analyses (Table 1). In the third stage of the statistical analysis, the Model Chi-square of the logistic model was 35.345 (10 d.f.; P > 0.05) and the adjusted Nagelkerk R2 test reached 39%. Only the presence of DM1 was predictive of the presence of xerostomia, whereby P = 0.01 (Table 2). In the fourth stage of the statistical analysis, the logistic regression model with all participants (n = 102) with negative impact on OHQoL (OHIP-14 scores) did not indicate signicant results (P > 0.05). The results of the logistic regression analysis with the group of adolescents with DM1 (n = 51) with negative impact on OHQoL (OHIP-14 scores) indicated that the Model Chisquare of the logistic model was 17.608 (12 d.f.; P > 0.05), and the adjusted Nagelkerk R2 test showed 38.9%. The independent variables xerostomia (P = 0.00) and DMF index (P = 0.03) were predictive of the negative impact on OHQoL (Table 3).
mean (SD) of the independent variables in the four subgroups analyzed. There was a signicant difference among the groups in relation to the OHIP14 scores (P = 0.00). The average OHIP-14 score in
Discussion
In the present study, DM1 was shown to be associated with higher prevalence of xerostomia and
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appeared not to have a negative impact on the OHQoL of adolescents when compared with adolescents without diabetes. DM1 presence was signicant for the worsening of clinical status and alterations in salivary conditions. Caries experience and salivary concentrations of amylase, urea, and glucose were not shown to be associated with xerostomia. Conversely, xerostomia and caries experience showed to be predictive of a poor OHQoL. Xerostomia is an important condition in subjects with diabetes (11, 12, 14) and, when present, causes clinical and social problems (7), with negative impact on the OHQoL (14). In this study, xerostomia prevalence was 53% (n = 27) in adolescents with DM1, which is in accordance with a study that obtained 54% (27) in adults with type 2 diabetes. The signicant difference between the prevalence of xerostomia in adolescents with and without DM1 demonstrated the importance of this condition in adolescents with DM1 (Table 1). Adolescents with DM1 valued social involvement with friends (10), and the negative impact of xerostomia on OHQoL could be seen to hinder this social involvement. Thus, addressing and preventing xerostomia could improve adherence to DM1 treatment and monitoring as well as combating its consequences on the daily lives of adolescents with DM1. We highlight the limitations of the studies in the literature on xerostomia prevalence in adolescents with DM1 to compare with the ndings of this study. Caries experience was not shown to be related to xerostomia, which was also indicated by Moore et al. (3). OHQoL, measured according to the average OHIP-14 scores, showed itself to be related to xerostomia in the bivariate analysis among the groups (Table 1), which is in consonance with previous studies (46, 14, 2631). In the present study, alterations in the quantity (SSFR) and in the biochemical composition of the saliva (total proteins and calcium) were associated with the presence of xerostomia (Table 1). We have chosen to study only stimulated whole saliva because unstimulated SFRs have been shown to be variable and more dependent on the time of day. In addition, it takes longer to collect the saliva because of lower ow rates. This instability and the time needed are signicant disadvantages, especially in a survey of a large population outside of a laboratory (i.e. adolescents in hospitals and schools) (6). Type 1 diabetes mellitus was predictive of the presence of xerostomia in adolescents (Table 2). In the theoretical model used for explaining the
impacts of DM1 on OHQoL in this study (Fig. 1), the absence of DM1 would appear to contribute to reducing the probability of the occurrence of xerostomia. The logistic regression analysis did not demonstrate that clinical status and salivary conditions, even SFR, inuenced xerostomia, which contradicts the proposed theoretical model (Fig. 1). However, other studies with predictive variables different from those evaluated in this study, such as glycoproteins, cetonic compounds, and other salivary components, should be performed. This result is in contrast to results found in elderly subjects in whom clinical status and xerostomia were related (26). Atkison et al. (37) indicated that xerostomia may present a relationship with the lack of hydration or systemic conditions. Other studies have related xerostomia to the poor control of DM1 (38), psychological factors (39, 40), and to DM1 (14). In the present study, while the subjective feeling of dry mouth was consistent with a systemic condition (DM1), there was no relationship with the most commonly used clinical indicator SFR. Such weak association is in accordance with previous ndings in relation to xerostomia (1, 5, 29). According to Baker et al. (29), a full understanding of the impact of a chronic condition on an individual cannot be captured by clinical assessment alone. Interventions aimed solely at the biological level, which do not take into account the patients experience of their symptoms, may not be fully effective. Although poor control of DM1 was related to xerostomia (38), metabolic control levels (capillary glucose and glycosylated hemoglobin levels) did not differ between adolescents with and without xerostomia (P > 0.05) (14). In the study by Busato et al. (14), the results of glycosylated hemoglobin tests performed <3 months prior to saliva collection, and the results of capillary glucose tests performed at the time of saliva collection were recorded; patients with good metabolic control were considered to be those with glycosylated hemoglobin values 8.0%, whereas poorly controlled patients were considered to be those with values >8.0%. Capillary glucose values between 90 and 130 mg dl characterized good glycemic control (9). Seven patients of 13 with good metabolic control complained of xerostomia in contrast to 18 of 34 poorly controlled ones who complained of xerostomia (P > 0.05) (14). In fact, there is not a consensus in the literature regarding the relationship between metabolic control and xerostomia and or salivary function. Some studies assumed that levels of glycemic control were important for
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xerostomia and or salivary function (41, 42) while others did not show this relationship (16, 43). Our study is in accordance with the latter. The logistic regression analysis with adolescents with DM1 (n = 51) demonstrated that xerostomia was predictive of a poor OHQoL. Other studies that evaluated adults (5, 27, 29) and elderly subjects (4, 6, 26, 31) have also demonstrated this relationship. The absence of xerostomia would appear to collaborate toward reducing the negative impact on the OHQoL of adolescents. In this study, the presence of DM1 was not shown to negatively impact on OHQoL of adolescents, in contrast to the results found by Sandberg & Wikblad (27), who studied adults with type 2 diabetes. Caries experience (DMF index) showed itself to be predictive of poor OHQoL of adolescents with DM1, and this is in agreement with the results obtained in young adults with DM1 (28). This should be taken into consideration when evaluating the impacts of DM1 on OHQoL, because, until now, it is known that any effect of diabetes on OHQoL is mediated through the effect of xerostomia. Decrease in caries experience (DMF index) would appear to contribute to decreasing the probability of the occurrence of negative impact on the OHQoL of adolescents with DM1. In the present study, DM1 in adolescents was shown to be associated with a high prevalence of xerostomia. The presence of xerostomia was predictive of a poor OHQoL. However, these ndings in this cross-sectional study make direct comparisons between our results and other studies in adults difcult. Multi-center follow-up studies with an increased subject number, control groups, and clinical measures repeated over multiple visits should be performed to evaluate the progression of DM1 in adolescents and the impact of xerostomia on OHQoL of these subjects. Furthermore, when xerostomia occurs, the need exists for continuous investigation into the complex relationship between clinical conditions and negative impact on behavior (24). The theoretical model used for explaining the impacts of DM1 on OHQoL in the present study should be explored, with the inclusion of other clinical, socio-economic and psychological variables, and general health factors.
References
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Acknowledgements
Authors would like to thank the Director and the nicas, Universidade employees of the Hospital de Cl . This study was supported by Federal do Parana MCT CNPq grant no 477932 2007-0.
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