Keywords
intraoral conditions - saliva - pH - flow rate - phosphate level - phosphorus intake
- menopause
Introduction
Menopause, a natural physiological process that typically occurs between the ages
of 49 to 52, marks the permanent cessation of the menstrual cycle for 12 consecutive
months.[1] Menopause involves hormonal fluctuations, particularly a decline in estrogen levels,
which affect diverse bodily systems, including the oral cavity.[2] Despite numerous investigations into the implications of menopause on oral health
parameters, findings remain inconsistent. While some studies assert an increased vulnerability
to periodontal diseases among postmenopausal women,[2]
[3]
[4] others report no significant difference in periodontal disease severity between
premenopausal and postmenopausal cohorts, suggesting influences beyond menopause play
a pivotal role.[5] Xerostomia and burning mouth syndrome emerge as common menopausal symptoms in certain
studies,[2]
[6]
[7]
[8] contrasting with findings that report no such symptoms in postmenopausal women.[9] Additionally, conflicting results surround salivary flow rates, with some studies
indicating lower rates in postmenopausal women compared with their premenopausal counterparts,[8]
[10]
[11] while others find no significant distinctions.[12] Salivary pH levels in postmenopausal women also elicit divergent findings, with
some studies reporting a statistically significant decrease,[10]
[13] others indicating no change,[14] and some revealing a statistically significant increase.[15]
The impact of menopause on salivary flow rate can potentially lead to changes in salivary
components, including phosphate. Salivary phosphate, in conjunction with other elements
such as calcium, bicarbonate, and proteins, plays a crucial role in regulating saliva's
buffering capacity and influencing the processes of dental demineralization and remineralization.[16] The intake of phosphorus further contributes to intraoral conditions. Previous studies
have identified that an excessive intake of phosphorus is associated with the development
of gingivitis and caries.[17]
[18] In postmenopausal women, research indicates higher salivary phosphate levels compared
with premenopausal women.[19]
[20] Furthermore, postmenopausal women with diabetes mellitus exhibit higher levels of
both stimulated and unstimulated salivary phosphate compared with their nondiabetic
counterparts.[21] However, to our knowledge, no studies have comprehensively compared salivary phosphate
levels and phosphorus intake, nor have examined their correlation between postmenopausal
and premenopausal women.
This study aimed to investigate salivary parameters, pH, flow rate, and phosphate
levels, along with phosphorus intake, to identify potential variations between postmenopausal
and premenopausal women. Furthermore, it seeks to explore the correlation between
salivary phosphate levels and phosphorus intake in both groups. Such insights are
essential for comprehending the unique oral health challenges associated with menopause,
contributing to a broader understanding of women's health and well-being.
Material and Methods
Employing purposive sampling, this cross-sectional study included 68 postmenopausal
and 94 premenopausal women, conducted in Bandung, West Java, Indonesia, from January
to April 2022. Inclusion criteria comprised women aged 45 to 65 years with a minimum
menopausal duration of 2 years and women aged 21 to 40 years for premenopausal participants.
All subjects were asked to sign the informed consent prior to data collection. All
subjects provided informed consent, and only those who completed all the research
procedures were included. Exclusion criteria involved systemic diseases (diabetes
mellitus, kidney disease, or hyperparathyroidism) and any dental treatments (scaling,
orthodontic treatment, denture, or dental restoration) received in the last 6 months.
The assessed variables included physical status (weight, height, and blood pressure),
intraoral conditions (inflammation signs, lesions, and disorders), salivary parameters,
and phosphorus intake. Intraoral inflammation, such as gingival bleeding, discoloration,
swelling, and recession, along with ulcers, plaque, calculus, tooth mobility, and
caries, was detected through direct observation using a dental mirror. The examination
results only recorded the presence or absence of these intraoral conditions. A questionnaire
covering demographic data, dental pain, xerostomia, burning sensation, ulcer etiology
and duration, and gingival bleeding etiology was administered. Phosphorus intake was
assessed using a semiquantitative food frequency questionnaire consisting of 37 food
items with pictures and portion sizes. The questionnaire's validity and reliability
were tested on 20 subjects from each postmenopausal and premenopausal group.
Unstimulated whole saliva was collected using the spitting method. The salivary flow
rate was calculated by measuring the total volume of saliva collected over the 5-minute
period. Salivary pH was determined using a universal indicator pH paper (pH 0–14 Universal
Indicator pH Paper, Merck, Darmstadt, Germany). The Atomic Absorption Spectrophotometer
AAnalyst 400 (PerkinElmer, Waltham, MA, USA) was used to determine subjects' salivary
phosphate level.
Statistical Analysis
The analysis of the significance difference in intraoral conditions between groups
utilized the chi-square test. However, in cases where expected counts in cells were
less than five, the Fisher's exact test was employed. For the comparison of salivary
parameters and phosphorus intake between study groups, adjusted by age, body mass
index (BMI), and blood pressure, the ANOVA univariate general linear model was utilized.
The correlation between salivary phosphate levels and age, BMI, blood pressure, and
phosphorus intake was examined using Spearman's rank correlation. Statistical significance
was defined as p < 0.05. All analyses were conducted using SPSS (IBM Corp, Version 26.0, Armonk, NY).
Results
As illustrated in [Table 1], the mean age of postmenopausal group was 53.4 (standard deviation: 6.6). The majority
of subjects in this group (76.5%) had been menopausal for more than 12 months. The
postmenopausal group also exhibited higher BMI and blood pressure (both systolic and
diastolic) compared with the premenopausal group. [Table 2] reveals a statistically significant difference in the proportion of subjects experiencing
10 out of the 14 assessed intraoral conditions between the two groups. The postmenopausal
group demonstrated a significantly higher prevalence (p < 0.005) of gingival swelling, gingival discoloration, gingival recession, plaque,
calculus, caries, tooth mobility, xerostomia, and burning sensation.
Table 1
Characteristics of study subjects
|
Characteristic
|
Postmenopausal group
|
Premenopausal group
|
|
(n = 68)
|
(n = 94)
|
|
Mean (SD)
|
Median (range)
|
Mean (SD)
|
Median (range)
|
|
Age (y)
|
53.4 (6.6)
|
54 (21–75)
|
26.7 (8.5)
|
21 (19–49)
|
|
BMI (kg/m2)
|
26.9 (4.4)
|
27.3 (17.1–38.0)
|
23.2 (5.4)
|
21.9 (16.0–38.0)
|
|
Systolic blood pressure (mmHg)
|
139.4 (24.0)
|
132 (97–201)
|
115.7 (15.4)
|
115 (90–156)
|
|
Diastolic blood pressure (mmHg)
|
86.3 (11.6)
|
83 (63–116)
|
81.5 (10.7)
|
80 (64–111)
|
Abbreviation: SD, standard deviation.
Table 2
Intraoral conditions of study subjects
|
Variables
|
Postmenopausal group (n = 68)
|
Premenopausal group (n = 94)
|
p-Value
|
|
Count
|
Percentage (%)
|
Count
|
Percentage (%)
|
|
|
Gingival swelling
|
18
|
26.5
|
12
|
12.8
|
0.027[a]
|
|
Gingival bleeding (nonspontaneous)
|
13
|
19.1
|
33
|
35.1
|
0.026[a]
|
|
Gingival bleeding (spontaneous)
|
5
|
7.4
|
5
|
5.3
|
0.743
|
|
Gingival discoloration
|
21
|
30.9
|
16
|
17.0
|
0.038[a]
|
|
Gingival recession
|
44
|
64.7
|
20
|
21.3
|
<0.001[a]
|
|
Ulcers (nontraumatic)
|
10
|
14.7
|
16
|
17.0
|
0.692
|
|
Ulcers (traumatic)
|
14
|
20.6
|
12
|
12.8
|
0.181
|
|
Plaque
|
52
|
76.5
|
58
|
61.7
|
0.047[a]
|
|
Calculus
|
49
|
72.1
|
41
|
43.6
|
<0.001[a]
|
|
Caries
|
63
|
92.6
|
64
|
68.1
|
<0.001[a]
|
|
Tooth mobility
|
27
|
39.7
|
10
|
10.6
|
<0.001[a]
|
|
Dental pain
|
30
|
44.1
|
41
|
43.6
|
0.949
|
|
Xerostomia
|
21
|
30.9
|
16
|
17.0
|
0.038[a]
|
|
Burning sensation
|
9
|
13.2
|
4
|
4.3
|
0.038[a]
|
a Statistically significant (p-value < 0.05) according to chi-square test or Fisher's exact test.
In [Table 3], following adjustments for age, BMI, and blood pressure, a statistically significant
difference in salivary flow rate between groups was observed (p = 0.008), with the postmenopausal group exhibiting lower mean and median salivary
flow rate. However, no significant differences were found in salivary pH (p = 0.764), salivary phosphate level (p = 0.142), or phosphorus intake (p = 0.323) between the two groups. As indicated in [Table 4], there was no significant correlation between salivary phosphate levels and subject
characteristics, including age (p = 0.747), BMI (p = 0.308), systolic blood pressure (p = 0.747), diastolic blood pressure (p = 0.622), and phosphorus intake (0.829) in both groups.
Table 3
Comparison of salivary parameters and phosphorus intake between study groups adjusted
for age, BMI, and blood pressure
|
Variables
|
Postmenopausal group (n = 68)
|
Premenopausal group (n = 94)
|
p-Value
|
|
Mean (SD)
|
Median (range)
|
Mean (SD)
|
Median (range)
|
|
Salivary pH
|
6.07 (0.47)
|
6 (5–7)
|
6.21 (0.48)
|
6 (5–7)
|
0.764
|
|
Salivary flow rate (mL/5 minutes)
|
1.90 (0.66)
|
2 (1–4)
|
3.05 (1.40)
|
3 (1–8.5)
|
0.008[a]
|
|
Salivary phosphate level (mmol/L)
|
23.17 (11.14)
|
21.63 (2.58–52.31)
|
14.53 (5.79)
|
13.56 (4.49–28.81)
|
0.142
|
|
Phosphorus intake (mg/d)
|
1103.8 (766.6)
|
956.7 (398.0–5424.3)
|
1179.5 (905.0)
|
939.6 (387.3–5693.4)
|
0.323
|
Abbreviation: SD, standard deviation.
a Statistically significant (p-value < 0.05) according to ANOVA: univariate general linear model.
Table 4
Correlation between salivary phosphate levels with subject characteristics and phosphorus
intake
|
The correlation of salivary phosphate level with
|
Postmenopausal group (n = 68)
|
Premenopausal group (n = 94)
|
|
r
|
p-Value
|
r
|
p-Value
|
|
Age (y)
|
0.147
|
0.337
|
0.057
|
0.747
|
|
BMI (kg/m2)
|
0.194
|
0.202
|
0.177
|
0.308
|
|
Systolic blood pressure (mmHg)
|
0.069
|
0.650
|
0.057
|
0.747
|
|
Diastolic blood pressure (mmHg)
|
−0.009
|
0.953
|
0.086
|
0.622
|
|
Phosphorus intake (mg/daily)
|
0.006
|
0.968
|
–0.038
|
0.829
|
Note: r is Spearman's rank coefficient correlation.
Discussion
Subject Characteristics
The observed higher BMI in the postmenopausal group compared with the premenopausal
group in this study aligns with findings from previous studies.[22]
[23] The changes in fat distribution, loss of lean body mass, and the overall increase
in body weight and composition that occur with menopause are associated with an elevated
risk of obesity in postmenopausal women.[24] Furthermore, Chen et al reported that postmenopausal women experiencing moderate/high
levels of stress, inadequate sleep (<6 h/d), and not breastfeeding their infants were
at an increased risk of obesity.[22]
[25] This should draw more attention, as obesity is linked to a wide range of comorbidities
and an increased risk of cardiovascular-associated and cancer-associated mortality.[26] Additionally, obese postmenopausal women are more likely to experience hot flushes,
sweating, and feeling bloated in the perimenopausal period and increased vasomotor
syndrome in the postmenopausal period compared with normal-weight women.[27] The higher BMI observed in postmenopausal women in this study may also be attributed
to higher blood pressure, in addition to the decrease in estrogen levels.[28]
[29]
Intraoral Conditions
This study reveals a significantly higher proportion of postmenopausal women who experienced
gingivitis symptoms (gingival swelling, bleeding, and discoloration) and periodontitis
indicators (gingival recession and tooth mobility) compared with premenopausal counterparts.
Consistent with previous research, women exhibit an increased susceptibility to periodontal
diseases during the postmenopausal period.[2]
[3]
[4] The alterations in periodontal tissue due to estrogen deficiency and advancing age
in postmenopausal women contribute to these findings.[2]
[3]
[30] Menopause induces changes in the gingival epithelium, including atrophy, thinning,
and heightened susceptibility to inflammatory changes.[5] Moreover, the significant higher proportion of postmenopausal women with plaque
and calculus accumulation suggest an elevated risk of periodontal disease, where subgingival
and supragingival calculus may result in gingival recession.[31]
Additionally, postmenopausal women in this study reported a higher prevalence of xerostomia
and burning sensation, aligning with previous research indicating these symptoms as
common among postmenopausal women.[2]
[6]
[7]
[8] However, contradictory findings exist, as some studies report no symptoms of xerostomia
in postmenopausal women despite a decrease in salivary flow rate.[9] The emergence of these symptoms may be influenced by psychological conditions, stress
levels, and other local and systemic factors such as anemia, drug side effects, diabetes
mellitus, and abnormal oral habits.[32]
[33] Xerostomia can lead to difficulties in chewing, swallowing, and speaking among the
elderly, significantly reducing their oral health-related quality of life.[34]
Salivary pH and Flow Rate
Among the salivary parameters assessed in this study, only salivary flow rate demonstrated
a significant difference between groups, with postmenopausal women exhibiting a significantly
lower salivary flow rate. This aligns with findings from previous studies.[8]
[10]
[11] However, one study reported no significant difference in salivary flow rate between
premenopausal and postmenopausal women.[12]
Furthermore, despite a noticeable decrease in salivary pH among postmenopausal women,
no significant difference was observed between groups. The literature presents varied
results on changes in salivary pH during menopause. For instance, Mahesh et al[10] reported a statistically significant decrease in stimulated salivary pH in postmenopausal
women, while Foglio-Bonda et al[13] found a statistically significant decrease in unstimulated salivary pH. Conversely,
Yalçin et al[14] found no changes in salivary pH among postmenopausal women, and Prasad et al[15] reported a statistically significant higher salivary pH in this group.
The simultaneous occurrence of lower salivary pH and reduced salivary flow rate in
postmenopausal women may result from salivary gland hypofunction and qualitative changes
in saliva composition related to estrogen decrease during menopause.[35] This decrease in salivary pH and flow rate could also contribute to the symptoms
of xerostomia observed in the postmenopausal sample in this study.[10]
Salivary Phosphate Level and Phosphorus Intake
This study found no significant difference in salivary phosphate levels between groups,
contradicting some previous research indicating lower salivary phosphorus concentrations
in postmenopausal women.[36] Additionally, there was no significant difference in phosphorus intake between groups,
with both groups exhibiting daily phosphorus intake higher than the recommended dietary
allowance (700 mg).[37] High phosphorus intakes (1,000 mg/d or higher) may increase the risk of disturbance
in bone and mineral metabolism, cardiovascular disease, kidney disease, and mortality.[38]
[39] Regarding the oral conditions, high intake of phosphorus is associated with the
increase of various inflammatory markers such interleukin-1β and C-reactive protein,
potentially explaining the relatively high proportion of subjects in both groups experiencing
gingivitis and dental caries.[17]
[18]
Previous studies have indicated that serum phosphate levels correlate with age, BMI,
and blood pressure.[20]
[40]
[41] However, the current study did not find any correlation between these variables
and salivary phosphate levels. Additionally, salivary phosphate levels did not show
a significant correlation with the daily phosphorus intake. Further investigation
is recommended, taking into account additional factors that may influence salivary
phosphate in oral physiological functions. These factors include other dietary components
(such as calcium and protein) and salivary compositions (including sodium, potassium,
calcium, magnesium, and bicarbonate), aiming to provide a comprehensive understanding
of these findings.
Conclusion
Postmenopausal women exhibited a lower salivary flow rate compared with premenopausal
women, potentially contributing to a higher prevalence of gingivitis symptoms, periodontitis
symptoms, caries, plaque and calculus accumulation, xerostomia, and burning sensation.
However, no differences were observed in salivary pH, phosphate level, and phosphorus
intake between the two groups. Additionally, salivary phosphate levels did not show
a correlation with daily phosphorus intake in either group.
