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Background and Aim: Controversy exists regarding the correlation of saliva secretion with obesity. Considering the significant role of saliva in oral and dental health and the increasing prevalence of obesity in Iran in the past three decades, this study aimed to assess the independent association of anthropometric indices including body mass index (BMI), weight gain after the age of 20 years and waist circumference (WC) with unstimulated whole saliva flow rate. Materials and Methods: This comparative cross-sectional study was conducted on 313 systematically healthy subjects who referred to Guilan Dental School. Age, gender, the level of education, BMI, WC and weight gain after the age of 20 was recorded. Unstimulated whole saliva flow rate was measured and the independent association of anthropometric indices with saliva flow rate was statistically analyzed. Statistical significance was set at P < 0.05. Results: 331 subjects (186 females and 145 males) were evaluated. Among them, 107 were obese (BMI≥30kg/m2), 114 were overweight (BMI=25-29.9kg/m2), and 110 had normal weight (BMI=18.5-24.9kg/m2). The mean saliva flow rate was 0.33ml/minute. The odds ratio of reduction in saliva flow below the mean value (0.33mL/minute) in obese compared to normal weight individuals was 1.84. The cut-off point of saliva flow reduction was 10.20 kg weight gain after the age of 20 with 62.3% sensitivity and 61.2% specificity. Weight gain after the age of 20 (odds ratio=1.06, 95% CI: 1.03-1.08) and gender (odds ratio: 1.87, 95% CI: 1.18-2.97) were found to be predictors of saliva flow reduction. Conclusion: This study showed that weight gain in adults was significantly correlated with the saliva flow rate, and weight gain after the age of 20 years was the main anthropometric index related to saliva flow reduction. The mean saliva flow rate in overweight and obese females was higher than counterpart males. Key Words: Weight Gain, Saliva, Body Mass Index, Obesity
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Autumn 2016; Vol. 28, No. 4
134
Original Article
Correlation Assessment of unstimulated whole saliva flow rate with
anthropometric indices
M. Rabiei 1, M. Maddah 2, M. Ghamgosar 3.
1 Professor, Department of Oral & Maxillofacial Medicine, School of Dentistry, Guilan University of Medical Sciences, Rasht,
Iran
2 Department of Human Nutrition, School of Public Health, Guilan University of Medical Sciences AND Health Services, Rasht,
Iran
3 Dentist, School of Dentistry, Guilan University of Medical Sciences, Rasht, Iran
Corresponding author:
M. Rabiei, Professor,
Department of Oral &
Maxillofacial Medicine, School
of Dentistry, Guilan University
of Medical Sciences, Rasht, Iran
rabiei@gums.ac.ir
Received: 2 July 2016
Accepted: 5 Sep 2016
Abstract
Background and Aim: Controversy exists regarding the correlation of saliva secretion
with obesity. Considering the significant role of saliva in oral and dental health and the
increasing prevalence of obesity in Iran in the past three decades, this study aimed to
assess the independent association of anthropometric indices including body mass index
(BMI), weight gain after the age of 20 years and waist circumference (WC) with
unstimulated whole saliva flow rate.
Materials and Methods: This comparative cross-sectional study was conducted on 313
systematically healthy subjects who referred to Guilan Dental School. Age, gender, the
level of education, BMI, WC and weight gain after the age of 20 was recorded.
Unstimulated whole saliva flow rate was measured and the independent association of
anthropometric indices with saliva flow rate was statistically analyzed. Statistical
significance was set at P < 0.05.
Results: 331 subjects (186 females and 145 males) were evaluated. Among them, 107
were obese (BMI≥30kg/m2), 114 were overweight (BMI=25-29.9kg/m2), and 110 had
normal weight (BMI=18.5-24.9kg/m2). The mean saliva flow rate was 0.33ml/minute.
The odds ratio of reduction in saliva flow below the mean value (0.33mL/minute) in
obese compared to normal weight individuals was 1.84. The cut-off point of saliva flow
reduction was 10.20 kg weight gain after the age of 20 with 62.3% sensitivity and 61.2%
specificity. Weight gain after the age of 20 (odds ratio=1.06, 95% CI: 1.03-1.08) and
gender (odds ratio: 1.87, 95% CI: 1.18-2.97) were found to be predictors of saliva flow
reduction.
Conclusion: This study showed that weight gain in adults was significantly correlated
with the saliva flow rate, and weight gain after the age of 20 years was the main
anthropometric index related to saliva flow reduction. The mean saliva flow rate in
overweight and obese females was higher than counterpart males.
Key Words: Weight Gain, Saliva, Body Mass Index, Obesity
Journal of Islamic Dental Association of IRAN (JIDAI) Autumn 2016 ;28, (4)
Introduction
Saliva is secreted by the salivary glands and plays
an important role in health, function, and
homeostasis of the oral environment; it also
regulates the intraoral ecosystem [1-3].
Quantitative and qualitative shortage of saliva
adversely affects the physical and social health,
self-confidence and consequently the quality of life
of individuals [3]. Evidence shows that childhood
obesity is correlated with a reduction in stimulated
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Rabiei et. al Correlation Assessment of unstimulated whole saliva
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saliva flow rate and subsequent development of
dental caries and adversely affects the oral health
of children [4-8]. In adulthood, obesity is
correlated with tooth loss due to increased rate of
caries and periodontal disease, mediated by the
inflammatory factors such as the C-reactive
protein, fibrinogen, adipokines and other
inflammatory cytokines secreted by adipose tissue
[9,10]. Evidence shows that salivary bacteria may
be related to overweight and obesity [11]. Adipose
tissue and its secretory products have been isolated
from the salivary glands and their secretions. In
many cadaver studies, increased fat accumulation
in salivary glands has been noted due to advanced
age [12-17].
Dental caries and obesity are both related to
nutritional habits, socioeconomic status, and
lifestyle. They both impose a high burden on the
health system. Prevalence of caries has been
reported between 17.9 to 90% [9]. However,
epidemiologic studies have reported this rate to be
42-67% [18]. The prevalence of obesity varies
from 9 to 35% in different parts of the world. Iran,
as a fast developing country, is not an exception to
this rule and obesity follows an ascending trend in
different parts of Iran as well [19-22]. In Guilan,
the prevalence of overweight and obesity in
individuals over 25 years was reported 24.6%
[23,24]. Several studies with different
methodologies have been carried out to elucidate
the correlation between dental caries and obesity
and have reported various results. One of the
important factors involving the development of
caries is the reduction of saliva flow by decreasing
the food debris and cariogenic microorganisms’
washout, and reducing the cariostatic enzymes
production, and changing the buffering capacity of
the saliva which results in decreasing its ability to
neutralize the critical pH. All these factors are
contributed to increased rate of dental caries
[25,26].
It has been postulated that there is a correlation
between decreased saliva secretion and the
occurrence of dental caries and periodontal
diseases [8,9]. Although there might be an
association between decreased saliva flow and
increasing prevalence of obesity, because of
insufficient evidence regarding the presence of a
correlation between obesity and saliva secretion
rate in adults, this study aimed to assess the
independent correlation of anthropometric indices
with saliva flow in overweight and obese adults in
city of Rasht, Guilan Province.
Materials and Methods
This study was approved by the ethics committee
of Guilan University of Medical Sciences
(IR.GUMS.REC.1395.119) and was conducted in
accordance with the Declaration of Helsinki. A
total of 331 subjects were evaluated in this
comparative cross-sectional study after signing
written informed consent forms.
The inclusion criteria were as follows: healthy
adults, males and/or females, with no history of
weight loss in the past six months, no auto-immune
or any systemic diseases such as diabetes mellitus,
hyperlipidemia, hypertension (metabolic
syndrome), Sjogren’s syndrome, Parkinson’s
disease or Alzheimer. Subjects with hormonal
disorders (hyper- or hypothyroidism, adrenal
insufficiency, acromegaly), cirrhosis, renal disease,
cancer, AIDS, pregnant women, professional
athletes, those on a specific diet in the past six
months or subjects experiencing either weight loss
or gain, and patients who take neurological and/or
any other drugs which may have an impact on
saliva secretion were not included. Drug addicts,
subjects with xerostomia and patients taking
antihistaminic drugs (e.g. diphenhydramine),
acetyl choline, pilocarpine, phenothiazine, and
iodine or histamine containing drugs were not
included either [1,2,3].
Data collection tools:
Sociodemographic characteristics:
Sociodemographic information of subjects
including age, gender, occupation, and weight at
20 years of age were recorded using a self-report
questionnaire. The level of education was divided
into two groups of high school diploma and
college/university degree.
Anthropometric characteristics:
In order to calculate body mass index (BMI),
patients were asked to take off their shoes and
thick clothing and weight were measured using a
digital scale with 0.1kg accuracy and height was
measured using a stadiometer. The waist
circumference (WC) was measured above the iliac
crest and below the umbilicus without applying
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Journal of Islamic Dental Association of IRAN (JIDAI) Autumn 2016 ;28, (4) Rabiei et. al
Autumn 2016; Vol. 28, No. 4
136
pressure using a tape measure in centimeters.
Patients were asked about their weight at age 20
and by subtracting this value from the current
weight, weight gain of each subject was calculated.
The WC reference was considered 102cm in
males and 88cm in females [27]. According to the
World Health Organization, patients with BMI
between 18.5-24.9 kg/m2 were considered normal,
25-29.9 kg/m2 were considered overweight and
>30kg/m2 were considered obese.
Saliva collection: Unstimulated whole saliva was
collected by the spitting method during 10 minutes
between 9 a.m. to 12 p.m. [28]. Participants were
asked to refrain from eating, drinking, and chewing
gum or smoking for one hour prior to saliva
collection. The saliva flow rate was calculated in
g/minute [3,28].
Statistical analysis:
Kolmogorov-Smirnov test was used in order to
examine the normal distribution of the data
regarding unstimulated saliva and the P-value was
set at <0.05. The Partial correlation was used to
assess the presence of correlations. Multiple
logistic regression was applied to assess the odds
ratios and ANCOVA was used to evaluate the
effect of confounders.
Results
In the present study, a total of 331 healthy
individuals were evaluated among whom were 86
(56.2%) females and 145 (43.8%) males. The mean
age of participants was 31.056.5 years (ranged
20-48 years). The BMI results showed that 110
(33.2%) of contributors had normal weight, 114
(34.4%) were overweight and 107 (32.3%) were
obese. The mean increase in weight after the age of
20 was 10.229.6 kg. The mean unstimulated
saliva flow rate was 0.330.10ml/min (ranged
between 0.04-0.67ml/min). Table 1 shows
demographic information of subjects and
anthropometric indices including weight gain after
the age of 20 years, BMI and WC.
Weight gain after the age of 20 years showed a
significant inverse correlation with saliva flow rate
(P<0.0001, r=-0.232). In other words, per each 1kg
weight gain after the age of 20 years, the odds of
the reduction in saliva flow to a value less than the
mean value of 0.33ml/min increased by 1.05 times.
BMI also showed a significant inverse correlation
with saliva flow rate (P=0.004, r=-0.159). The odd
ratio of saliva flow reduction to less than the mean
value of 0.33ml/min in the obese individuals
compared to normal weight subjects was 1.84
(95% CI: 1.08-3.16). In females, the saliva flow
decreased significantly (P=0.02) by increasing the
BMI (Fig. 1).
Subjects with a higher WC had 2.04 times higher
odds of saliva flow reduction (95% CI: 1.3-3.2)
compared to contributors with normal WC (Fig. 2).
The mean unstimulated saliva flow rate was
significantly different among different age groups
(P=0.041) and males had significantly higher flow
rate than females (P=0.003). Aging showed a
significant correlation with reduction in saliva flow
rate (P=0.0444, r=-0.111) (Fig 3). Gender and
weight gain after the age of 20 were the predictors
of reduction in saliva flow rate in the final logistic
model (P<0.0001).
Women were1.9 times more likely to experience a
reduction in saliva flow rate compared to men
(odds ratio: 1.87, 95% CI: 1.18-2.97). In other
words, by every 1kg weight gain after the age of
20, the odds ratio of reduction in saliva flow
increased by 1.06 times. This rate was 1.33 per 5kg
weight gain in males (odds ratio: 1.06, 95% CI:
1.03-1.08). The mean saliva flow rate was
0.350.11 ml/min in subjects with a weight gain
less than the median and 0.30.09ml/min in
subjects with a weight gain more than the median
(10kg)(P=0.001).
ANCOVA was used to control for the potential
effect of confounders and showed that weight gain
over 10kg significantly influenced the saliva flow
rate (P<0.0001). Weight gain by 10.20kg after the
age of 20 years was the cutoff point for decreasing
the saliva flow rate below the mean value of
0.33ml/min with 62.3% sensitivity 61.2%
specificity and area under the curve of 0.6440.32,
95% AUC:0.581-0.708, P<0.0001).
Discussion
Saliva is an important factor in maintaining oral
health, and change in its flow and contents affects
all components of the oral cavity. Several studies
have pointed to the adverse effects of obesity on
dental and periodontal health [4-10].
The current study provides evidence of the
correlation between saliva flow rate and
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Rabiei et. al Correlation Assessment of unstimulated whole saliva
Autumn 2016; Vol. 28, No. 4
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-
-
weight gain after
the age of 20
BMI
WC
unstimulated
saliva flow rate
Gender
Males (n=145)
11.62±9.7
27.78±3.8
96.04±8.96
0.35±0.08
Females (n=186)
9.13±9.35
27.48±4.61
88.72±10.42
0.32±0.13
P value
0.019*
0.539
<0.0001*
0.005*
Age group
20-30 years (n=162)
6.51±7.24
26.45±4.44
88.20±10.26
0.34±0.11
30-40 years (n=143)
14.07±9.85
29±3.82
95.37±9.48
0.32±0.11
40-50 years (n=26)
12.21±12.21
27.24±3.78
96.23±8.66
0.32±0.08
P value
<0.0001*
<0.0001*
<0.0001*
0.219
BMI
Normal weight (n=110)
2.57±5.85
22.81±1.68
82.89±6.85
0.35±0.12
Overweight (n=114)
11.10±8.05
27.64±1.38
91.46±7.34
0.34±0.10
Obese (n=107)
17.15±8.52
32.52±2.10
101.71±7.23
0.31±0.10
P value
<0.0001*
<0.0001*
<0.0001*
0.034*
Table 1. The frequency distribution of demographic information and anthropometric indices as well as
the unstimulated saliva flow rate in subjects (values are presented as Mean± Standard deviation)
*= significant differences
Figure 1. Comparison of unstimulated saliva flow (ml/min) in males and regarding the BMI
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Journal of Islamic Dental Association of IRAN (JIDAI) Autumn 2016 ;28, (4) Rabiei et. al
Autumn 2016; Vol. 28, No. 4
138
anthropometric indices. The results showed that
10kg weight gain after the age of 20 years
significantly decreased the saliva flow rate,
irrespective of the gender. This finding also
supports the theory of adverse effects of fat
accumulation in the body, on salivary glands and
their function [12-14]. Fat accumulation can
adversely affect saliva secretion and consequently,
compromise oral and dental health. It is also a risk
factor for chronic oral diseases such as
periodontitis and dental caries. On the other hand,
reduction in saliva flow rate decreases the saliva
pH (to the critical threshold) and adversely affects
dental health [25,26]. Moreover, reduction in
saliva flow because of sympathetic innervations
results in a decrease in the concentration of
salivary compounds such as enzymes and
protective agents, which increase the risk of caries
and damages to oral tissues [29]. According to
Dawes [26], reduction in saliva flow, increase the
adhesion of microorganisms to epithelial cells and
due to higher availability of substrates and
decreased washout, bacteria proliferate at a faster
rate (up to three times); therefore, tissue
destruction occurs faster and to a greater extent
[26].
Figure 2. Comparison of unstimulated saliva flow in males and females regarding their WC
Figure 3. Difference in saliva flow rate among different age groups
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Rabiei et. al Correlation Assessment of unstimulated whole saliva
Autumn 2016; Vol. 28, No. 4
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The results of current study detected an association
between BMI and secretion of unstimulated saliva,
which was that obese individuals had a lower
saliva flow rate compared to overweight and
normal weight subjects and they are more prone to
the reduction of the saliva flow rate to the less than
the mean value.
Yamamoto et al. [30] stated that unstimulated
saliva flow rate in both males and females was
significantly correlated with BMI while
unstimulated saliva in each of the two groups of
males and females was not independently
correlated with anthropometric indices [30].
However, in our study, the interaction effect of
gender and BMI was significant [12,13,16,
31,32,33].
The results from current study indicated that in
addition to BMI, gender had also a significant
effect on salivary flow rate; female individuals had
lower salivary flow rate (P=0.005). Inoue et al.
[13] measured the size of salivary glands using
magnetic resonance imaging (MRI) and found a
significant association between unstimulated saliva
flow rate and the size of salivary glands with BMI
and weight [13]. However, Fenoll-Palomare et al.
[34] found no significant correlation between
obesity and secretion of unstimulated saliva. It
seems that lack of correlation in the Fenoll’s study
[34] might be due to small sample size and
younger age of obese subjects compared to normal
weight individuals in their study.
The association of WC and weight gain after 20
years and unstimulated saliva flow rate was also
evaluated in the current study, however, no
significant association was found in this respect
between WC and unstimulated saliva flow rate
(P=0.219). This association has not been
previously evaluated in any study.
In the current study, the unstimulated saliva flow
rate decreased with an increase in age, which was
in line with the findings of some previous studies
[35,36]. Pedersen et al. [31] stated that the effect of
drug intake on the reduction of unstimulated saliva
flow rate was greater than that of age while
Percival et al. [32] reported that decreased function
of salivary glands was mainly due to advanced age.
Waterhouse et al [14] and Scott [17] have
suggested the theory of replacement of the acinar
salivary gland tissue with adipose tissue. Our
findings support this theory since weight gain after
the age of 20 years in our study decreased the
saliva flow rate. In other words, reduction in saliva
flow rate may occur following weight gain after
the age of 20 years.
In addition to age, gender also had an association
with unstimulated saliva flow rate in the current
study; unstimulated saliva flow rate in women was
significantly lower than that in men (P=0.003).
This finding was similar to the results of some
previous studies [31,24,19,7]. Inoue et al. [13]
have measured the size of salivary glands by
means of MRI. They revealed that the size of
salivary glands was smaller in females. They have
also observed that BMI and weight were correlated
with size of salivary glands and consequently
unstimulated saliva flow rate [13]. Dawes [12]
explained that smaller size of the oral cavity and a
smaller mucosal surface area in females were
probably responsible for this difference. In other
words, smaller salivary glands are more affected
by fat accumulation and subsequent reduction in
saliva flow. Percival et al. [32] and Heintze et al.
[33] stated that hormones in females are
responsible for these differences. However,
Tylendaet al. [37] declared that the mean saliva
flow rate in males and females was almost the
same (0.16 versus 0.18ml/min). Flink et al. [9]
discussed that the difference in saliva flow rate
occurs between males and females in ages over 40
years. Despite all the above, Foglio-Bonda et al.
[38] reported that no significant difference exists in
unstimulated saliva flow rate between males and
females. However, it should be noted that the study
by Foglio-Bonda et al. [38] was conducted on a
smaller sample size at a lower age range. However,
the current study showed that saliva flow rate
decreased with the age in both males and females
as reported by Flink et al. [9] and demonstrated
that the difference in saliva flow rate was more
evident after the age of 30 years.
Conclusion
The present study was a cross-sectional study
therefore, it could not establish a cause and effect
relationship between obesity and saliva flow. In
general, this study showed that gender and weight
gain in adulthood were independently correlated
with saliva flow rate. The effect of aging on the
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Journal of Islamic Dental Association of IRAN (JIDAI) Autumn 2016 ;28, (4) Rabiei et. al
Autumn 2016; Vol. 28, No. 4
140
reduction of saliva flow after controlling for
weight gain was not significant. Since the present
study revealed an independent inverse correlation
between weight gain in adulthood and saliva flow
rate, the use of some anthropometric indices (other
than BMI) may be required to describe the
association of weight gain with the oral and dental
diseases related to saliva secretion.
Future studies are recommended to assess the
effect of weight loss on saliva flow rate in obese
patients in different age groups. Also, in order to
find evidence on whether a correlation between
body weight and oral and dental diseases exist,
further studies are required to evaluate and
measure the frequency of dental caries and
saliva-related oral diseases in obese and normal
weight individuals. The health system authorities
and dentists must be aware of the adverse effects
of obesity on the reduction of saliva flow and its
consequences.
Acknowledgement
This study was conducted with the cooperation of
Guilan Dental School and the Reference
Laboratory of Guialn Province. The authors would
like to thank Professor Ehsan Kazemnejad Leyli
for his statistical Analysis and participation in this
study.
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The prevalence of overweight and obesity in most developed and developing countries have been increasing markedly over the past two decades. This increase includes all ages, genders, racial and ethnic groups, income, and educational levels. A variety of genetic, environmental, physiological, psychological and sociocultural factors influence the development of obesity. Iran like many other developing countries is now experiencing the global epidemic of obesity and its consequences. Recent epidemiological studies have revealed that the prevalence of obesity, overweight, and metabolic syndrome in Iran is equal to or higher than Europe and the United States and it is the primary cause of the rising prevalence of type 2 diabetes and the important comorbid states such as hypertension, cardiovascular, renal, and gastrointestinal diseases along with increasing the burden of cancers. This is also in line with the present etiologies of death in Iran with cardiovascular disease and cancer accounting for nearly 60% of causes of nontraumatic death. The prevalence of obesity in Iran has reached epidemic proportions and is specifically affecting women and younger age groups also. The increased consumption of calorie-dense regular and fast foods and sucrose-enriched drinks, together with an increasingly sedentary lifestyle, appear to be major factors contributing to this epidemic. The per capita consumption of carbonated beverages in Iran is 42 liters per year and 40% of Iranians consume more food than they need, and the average Iranian consumes 40% more carbohydrate and 30% more fat than needed. To deal with this epidemic, prevention should receive high priority and social measures such as taxing fast foods, subsidizing fresh food and vegetables, and spending more public money on projects to promote physical activity are necessary. There is also emerging evidence that treating obese subjects, particularly those with metabolic syndrome or type 2 diabetes, has short-term effects on the prevention of diabetes; improves glucose, lipid, and blood pressure parameters; and is likely to have beneficial effects on long-term health outcomes.
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SUMMARY Saliva is a noninvasive and accessible biofluid that permits early detection of oral and systemic diseases. Recent scientific and technologic advances have uncovered specific salivary biomarkers for a number of clinical conditions, including cancers, autoimmune diseases, and cardiovascular disorders. The availability of highly sensitive and high-throughput assays such as microarray, mass spectrometry, reverse transcriptase quantitative polymerase chain reaction (RT-qPCR) and nano-scale sensors that can measure proteins and nucleic acids are poising saliva as an emerging biofluid for translational and clinical applications. This paper will discuss development of salivary biomarkers for the detection of oral and systemic diseases and the translational application of these markers for clinical applications.
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