Association of Urine (pH < 5.5) with Community Periodontal Index (CPI) and the Number of Remaining Teeth in Korean Adults: A Cross-Sectional Study Using Data from Korea National Health and Nutrition Examination Survey 2016–2018

This study aims to determine the association between UpH (<5.5), Community Periodontal Index (CPI), and the number of remaining teeth—cumulative indicators of oral health—using data from the 7th Korea National Health and Nutrition Examination Survey (KNHANES, 2016–2018), which represents the Korean population. Data from 12,689 adults aged 19 years and older who had periodontal examinations were analyzed. Logistic regression analysis was performed after adjusting for demographic, health, and health-related behavioral factors as covariates to determine the association between UpH, CPI, and the number of remaining teeth. This study found that UpH (<5.5) was associated with CPI and the number of remaining teeth. For UpH (<5.5), the odds ratio for CPI (≥4 mm) was 1.19 times (95% CI: 1.06–1.33). The risk of tooth loss was 1.25 times (95% CI: 1.06–1.48) for those with 0–19 remaining teeth and 1.20 times (95% CI: 1.07–1.34) for those with 20–27 teeth. The results revealed an association between UpH, CPI, and the number of remaining teeth. However, further longitudinal research on UpH and oral status is necessary.


Introduction
Urine pH (UpH) refers to urine acidity.On average, UpH is slightly acidic with a pH of 6.0, and acidic urine means a pH of less than 5.5 [1].It is known to be influenced by systemic factors such as an individual's diet, insulin resistance, hydration status, diuretics, and chronic kidney disease medications [2][3][4][5].
Previous studies have reported that UpH (<5.5) is associated with metabolic syndrome (Mets), obesity, diabetes development, and insulin resistance [6][7][8].In addition, a retrospective cohort study of predictors of acidic urine and Mets has found that acidic urine is associated with a higher risk of developing Mets [9].These results suggest that insulin resistance may be involved in the reduction in ammonium excretion in the proximal tubule, which acts as a buffer for urine [6].
Additionally, previous studies with gout patients have suggested that insulin resistance plays an important role in acidic urine [10], and longitudinal analysis has indicated that it is a risk factor for the new onset of Mets within 5 years among participants with acidic urine [9].Therefore, acidic urine seems to be influenced by the participant's systemic condition related to insulin resistance and a healthy lifestyle.Research on metabolic disorders and insulin resistance using UpH has been conducted.However, there is limited research on the oral cavity and other organs using UpH.
Previous studies related to the oral cavity have reported that insulin resistance is associated with an increased risk of inflammation of the gingival and periodontal tissues in the oral cavity.Alternatively, it has been suggested that the presence of periodontal tissue inflammation may reflect undetected insulin resistance [11].
A previous study reported that tooth loss is considered a cumulative indicator of lifelong oral health among the indicators of oral health [12].Among the various bacteria that contribute to periodontitis, virulence factors of Porphyromonas gingivalis have been suggested to be the main cause of tooth loss [13].Through multiple virulence factors, the bacterium interferes with the host's immune system, triggers an inflammatory response, and induces insulin resistance [14].Notably, oral inflammation is correlated with systemic diseases, such as diabetes, non-alcoholic fatty liver disease, and cardiovascular diseases [15].
According to these findings, insulin resistance might lead to acidic urine induction and periodontal tissue inflammation.However, research on the association between UpH (<5.5) and oral disease is scarce.Therefore, understanding the association between Community Periodontal Index (CPI) and tooth loss according to the level of UpH will contribute to the study of oral systemic conditions and biological markers.
This study was conducted based on the research hypothesis that UpH (<5.5) would be associated with CPI and tooth loss, which are indicators of oral health.
Therefore, this study aims to determine the association between UpH (<5.5),CPI, and the number of remaining teeth using data from the 7 th Korea National Health and Nutrition Examination Survey (KNHANES, 2016-2018), which represents the Korean population.

Study Participants
This study utilized the 7 th KNHANES, a nationally representative cross-sectional survey conducted from 2016 to 2018.Year 1 and 2 (2016-2017) data of the 7 th KNHANES were collected without an Institutional Review Board (IRB) review in accordance with the Bioethics and Safety Act, and year 3 (2018) data were collected with approval from the IRB of the Korea Disease Control and Prevention Agency (IRB No. 2018-01-03-P-A).Out of a total of 16,489 individuals, 13,199 individuals who were over the age of 19 were analyzed.Out of a total of 16,489 participants who took part in the health survey and screening examination, 13,199 participants aged 19 years and older were extracted.Among them, 12,689 participants who underwent periodontal tissue examination were selected for the analysis.In the results, the discrepancy in the total frequency is due to missing data.This study utilized data from the 7 th Korea National Health and Nutrition Examination Survey, and the results of oral examinations were analyzed.

Number of Teeth
The measurement of the dependent variable, tooth count, was conducted by highly trained public health dentists using standardized methods.The training was provided through orthodontic lectures, training using tooth models, web-based photo and human oral examination simulations, and on-site training to ensure the reliability of the oral examination.The number of remaining teeth was calculated after excluding the third molars.The number of remaining teeth of the participants was categorized into three groups: ≤19, 20-27, and 28 teeth, according to the classification of previous studies [16].

Community Periodontal Index (CPI)
Periodontal examinations for CPI, a dependent variable, were performed by highly trained public health dentists with ongoing quality control.The examinations were conducted according to the CPI screening criteria set forth by the World Health Organization (WHO) [17].Periodontal pocket depths were measured at six sites (maxillary right posterior, maxillary anterior, maxillary left posterior, mandibular right posterior, mandibular anterior, and mandibular left posterior).Periodontal pocket depth was measured using the WHO probe, with markings at 3.5 mm and 5.5 mm.The CPI criteria were as follows: 0 (healthy and no signs of inflammation), 1 (gingival bleeding), 2 (calculus), 3 (shallow pocket; >3.5 mm and ≤5.5 mm), and 4 (deep pocket; >5.5 mm).For the CPI record, index teeth or teeth remaining in the sextant were evaluated, and the highest score was recorded.In this study, we defined a pocket depth of <4 mm (CPI 0-2) and ≥4 mm (CPI 3, 4).

Covariates
Each variable was reclassified as follows.Demographic factors included gender, age, household income level, and education.Age was categorized into 19-29, 30-39, 40-49, 50-59, and 60+.Household income quartiles were categorized into three groups: high, middle (mid-high and mid-low), and low.Education level was categorized into less than an elementary school diploma, middle school diploma, high school diploma, and college degree or higher.
For health-related behavioral factors, current smoking status was divided into nonsmoking (smoking less than five packs) and smoking (smoking more than five packs) [21,22].Drinking status was divided into non-drinking (lifetime non-drinking or drinking less than one drink per month in the past year) and drinking (drinking more than one drink per month in the past year) [23].Daily toothbrushing frequency was divided into ≤ 1 times/day, and ≥2 times/day.

Statistical Analysis
The KNHANES data were collected using a complex sample design, and a composite sample analysis was conducted after applying weights, stratification variables (kstrata), and primary sampling unit (psu).
A cross-analysis was conducted on UpH, CPI, and the number of remaining teeth according to the general characteristics of the participants.The association between UpH and the number of remaining teeth was assessed using the Multinomial logistic regression models.The association between UpH and CPI was evaluated using logistic regression models.
Model 1 is the unadjusted model, and Model 2 is the adjusted model for gender, age, household income, education, diabetes, BMI, smoking, drinking, and daily toothbrushing frequency.Results are presented as odds ratios for tooth loss and CPI, with 95% confidence intervals (CIs).
All statistical analyses were conducted using the SPSS Windows software version 20.0, and significance was tested at a Type I error level of 0.05.

Urine pH by General Characteristics
Table 1 shows the UpH by the general characteristics of the participants.The frequency of UpH < 5.5 was higher in females than in males (p = 0.126) and increased with age (p < 0.05).It was higher among those with a middle household income and those with a college degree or higher, but this was not statistically significant.It was higher among those without diabetes at 88.6% (p < 0.001), in the obese group at 37.5%, and in the non-smoking group at 80.5% (p < 0.001).It was as high as 90.4% in the group brushing teeth two times or more a day (p < 0.05), 66.1% in the group with CPI (<4 mm), and 44.4% in the group with 20-27 teeth (p < 0.001).

CPI by General Characteristics
Table 2 shows the periodontal tissue condition by the general characteristics of the participants.The CPI (≥4 mm) was higher in men and increased with age (p < 0.001).It was higher among those with a middle household income at 52.3% and high school graduates at 30.4%, but this was not statistically significant (p < 0.001).
It was higher among those without diabetes at 84.5%, in the obese group at 40.5% (p < 0.001), in the non-smoking group at 76.2%, and in the group brushing teeth two times or more a day at 88.1% (p < 0.001).It was 57.5% in the group with UpH ≥ 5.5 and 53.2% in the group with 20-27 remaining teeth (p < 0.001).

Number of Remaining Teeth by General Characteristics
Table 3 shows the number of remaining teeth by the general characteristics of the participants.The group with 0-19 remaining teeth had a higher frequency in women than men, with increasing age, and in a lower household income and education level (p < 0.001).It was higher among those without diabetes at 85.9% (p < 0.001) and in the obese group at 37.0% (p < 0.001).It was higher in the non-smoking and non-drinking groups at 81.2% (p = 0.132) and 60.6% (p < 0.001), respectively.It was as high as 80.2% in the group brushing teeth two times or more a day (p < 0.05), 58.8% in the group with UpH ≥ 5.5, and 53.3% in the group with CPI (<4 mm) (p < 0.001).

Association between Urine pH and the Number of Teeth
Table 5 shows the results of the association between UpH and the number of teeth.Model 1 for 0-19 teeth shows an odds ratio of tooth loss increase of 1.26 times in the UpH ≥ 5.5 group compared to the UpH < 5.5 group.In Model 2, adjusted for all variables, it increased 1.25 times (95% CI 1.06-1.48).Furthermore, in Model 1 for 20-27 teeth, the odds ratio increased 1.21 times.In Model 2, the odds ratio of tooth loss was 1.20 times (95% CI 1.07-1.34) in the UpH < 5.5 group.Data are presented as OR (95% CI).OR: odds ratio; CI: confidence interval, * p < 0.01 and ** p < 0.001.
Model 1 unadjusted model.Model 2 adjusted for socioeconomic variables (sex, age, household income, and education), general health variables (diabetes mellitus and BMI), and health and behavior variables (smoking, alcohol drinking, and toothbrushing).

Discussion
This study analyzed the association between UpH (<5.5), which may indicate systemic health status, CPI, and the number of remaining teeth using raw data from the 7 th KN-HANES, representing the Korean adult population.A total of 12,689 adults aged 19 years and older who underwent periodontal examinations were examined.This is the first study to examine the association of UpH (<5.5) with oral indicators (CPI and the number of remaining teeth).Key findings from the study were as follows.
The results of this study show that there was no significant difference in the CPI by alcohol consumption (Table 2).The covariate of alcohol drinking is defined as the monthly alcohol intake.Non-drinkers were defined as individuals who had consumed less than one drink per month in the past year, while drinkers were those who had consumed one or more drinks per month in the past year.Therefore, it is presumed that such results were retrieved because the degree of alcohol consumption was not categorized in detail.Furthermore, regarding the number of remaining teeth according to alcohol consumption status, among the drinkers group, the percentage of individuals with 0-19 teeth was 39.4%, and the percentage with 28 teeth was 60.1% (Table 3).As mentioned earlier, this could be due to the issue of categorizing alcohol consumption, or alternatively, although not mentioned in the data, it is possible that non-drinkers exhibited similar results due to factors such as their older age and prevalence of systemic diseases.
This study also found that there was no significant difference in the number of remaining teeth by smoking status (Table 3).When considering the percentage distribution by the number of remaining teeth, the proportion of non-smokers was higher at 83.3% in the group with 28 teeth, while the proportion of non-smokers was lower at 81.2% in the group with 0-19 teeth.Looking at the results of CPI (≥4 mm) by the frequency of daily tooth brushing, the number of individuals with CPI (≥4 mm) was found to be higher in the group who brushed their teeth two or more times a day.
If we consider the cross-analysis in terms of the proportion of vertical sums, individuals who brushed their teeth two or more times a day accounted for 93.4% in the CPI (<4 mm) group, while they accounted for a lower proportion of 88.1% in the CPI (≥4 mm) group.Therefore, while theoretically valid when considering the proportions of the CPI (≥4 mm) and CPI (<4 mm) groups, it seems that further analysis is needed for individuals who brush their teeth two or fewer times a day.
In this study, UpH (<5.5) was associated with the Community Periodontal Index and number of remaining teeth.The causal relationship cannot be established at this point due to the inadequate literature on the association between UpH and oral health.
We considered insulin resistance as a major factor contributing to urine acidity [24,25].Insulin resistance is the inability of the body's cells and tissues to respond appropriately to normal levels of insulin.Causes include obesity, lack of exercise, advanced glycosylation end products (AGEs), excess free fatty acids (FFAs), stress, smoking, alcohol, or drugs [24,25].It manifests in various outcomes, including a combination of metabolic disorders, lipotoxicity, glucotoxicity, and inflammation [26].As such, it is associated with the pathophysiologic mechanisms of insulin resistance in the development of Mets, cardiovascular disease, and inflammation [14].
Previous studies reported that periodontitis causes colonization of bacteria such as Aggregatibacter actinomycetemcomitans and Porphyromonas gingivalis within the periodontal pocket, and that bacteria and antigens introduced into the bloodstream via local epithelial ulcers induce the release of inflammatory mediators.This triggers the inflammation cascade [27][28][29].
Furthermore, research suggests a bidirectional relationship between periodontitis and insulin resistance, where chronic systemic inflammation exacerbates periodontitis by inducing the expression of tumor necrosis factor-α in periodontal tissues [30].Such exacerbation can contribute to tooth loss by promoting the resorption of periodontal tissues.
Since this study did not analyze the data based on the measurements of insulin resistance, future research should be conducted for investigation in relation to insulin resistance and type 2 diabetes.
The findings of this study were similar to those of cross-sectional studies on the association between Mets and decreased masticatory capacity.Participants with poor masticatory function, categorized based on the total number of functioning teeth and masticatory capacity, had a more than 2.5-fold increased risk for diseases such as Mets (diabetes, hypertension, abdominal circumference, and hypercholesterolemia) [31].Similarly, metabolic syndrome (MetS) and periodontitis exhibit a bidirectional relationship, arising from factors related to immune and inflammatory responses [32].
The mechanism linking periodontitis and MetS involves the infiltration of proinflammatory cytokines from the gingiva into the bloodstream, leading to increased oxidative stress, triggering insulin resistance and atherosclerotic changes, potentially resulting in the development of MetS [33].
Previous studies have noted that risk factors associated with UpH, such as insulin resistance and MetS, can also be risk factors for oral diseases.This bidirectional relationship partially explains the findings of this study.
This study has several strengths.This is the first study to analyze the association between UpH, a readily measurable urinary parameter, and oral health (CPI and number of remaining teeth).A representative raw dataset from the Korea National Health and Nutrition Examination Survey was used.
This study also has the following limitations.First, as it was a cross-sectional study, causal relationships could not be confirmed.Second, the number of remaining teeth applied in this study may have varying definitions depending on the status of the subjects.For example, the number of remaining teeth in individuals with poor oral health may be inappropriate to reflect a healthy lifestyle.Therefore, in this study, the periodontal status was also considered to complement the limitations of the number of remaining teeth.Subsequently, it would be necessary to consider data that allows for a more specific evaluation of the oral health status.Third, although UpH is associated with specific conditions and medications, this aspect was not considered in this study.Therefore, bias may occur as a result.Hence, future research designs need to consider specific conditions and medication interactions related to UpH.
This study investigated the association between UpH, a readily measurable urinary parameter, and oral health (CPI and number of remaining teeth).The findings of this study suggest that UpH could serve as a valuable tool for predicting and screening for oral diseases in both clinical and community settings following further systematic research.Additionally, this parameter holds the potential to contribute to preventive health promotion programs aimed at addressing non-communicable diseases.In the research domain, UpH could be a useful biomarker in various biomarker research, including clinical, longitudinal, and cohort studies.

Conclusions
Based on the results of this study, UpH (<5.5) was associated with CPI and the number of remaining teeth.Since UpH changes with Mets, insulin resistance, and a healthy lifestyle, comprehensive healthcare is needed for systemic and oral health.

Table 1 .
Characteristics of the study population stratified by urine pH.
* Weighted %; ** p-Value was calculated by complex sample chi-square test.

Table 2 .
Characteristics of the study population stratified by CPI.
* Weighted %; ** p-Value was calculated by complex sample chi-square test.

Table 3 .
Characteristics of the study population stratified by number of teeth.
* Weighted %; ** p-Value was calculated by complex sample chi-square test.

Table 4 .
Multivariable association between UpH and CPI ≥ 4 mm.Model 1 unadjusted model.Model 2 adjusted for socioeconomic variables (sex, age, household income, and education).Model 3 adjusted for the same factors as model 2 plus general health variables (diabetes mellitus and BMI).Model 4 adjusted for the same factors as Model 3 plus health and behavior variables (smoking, alcohol drinking, and toothbrushing).