The purpose of this study is to determine whether the lower intakes of yogurt, milk, and calcium are associated with periodontitis in a nationally representative sample of Korean adults. This study comprised 6,150 adults 19 or more years old who took both periodontal examination and nutrition survey. The frequency of yogurt and milk intake was examined with a food frequency questionnaire. The amount of calcium intake was calculated with dietary intakes data gained from complete one-day 24-hour recall interviews. Periodontitis was assessed using the Community Periodontal Index (CPI). Multivariate logistic regression analyses were performed for the whole sample and subgroups with the strata of age, gender, or smoking, in a complex sampling design. Less intake of yogurt was significantly associated with periodontitis (odds ratio [OR] 0.82, 95% confidential interval [CI] 0.70–0.97), but neither less intake of milk (OR 1.04, 95% CI 0.89–1.20) nor lower intake of calcium (OR 1.04, 95% CI 0.89–1.21) was significantly associated with periodontitis. In the subgroup analysis, no difference in the association of yogurt intake with periodontitis was found according to the strata of age, gender, and smoking. In conclusion, periodonitis was significantly associated with the less intake of yogurt among the Korean adults, but the calcium contained in yogurt is not likely to cause it.
Citation: Kim H-S, Kim Y-Y, Oh J-K, Bae K-H (2017) Is yogurt intake associated with periodontitis due to calcium? PLoS ONE 12(10): e0187258. https://doi.org/10.1371/journal.pone.0187258
Editor: Alberto G. Passi, University of Insubria, ITALY
Received: March 29, 2017; Accepted: October 17, 2017; Published: October 30, 2017
Copyright: © 2017 Kim et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: Data are available from the KNHANES database. Interested researchers can sign up and apply for data usage in the same manner as the authors from (http://www.cdc.go.kr/CDC/eng/main.jsp).
Funding: The authors received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Periodontitis is a chronic inflammatory disease that leads to destruction of the connective tissue and alveolar bone around teeth . Due to its high prevalence in adults, it is a major cause of teeth extraction in adults and represents one of the important public health problems that increase the burden of chronic diseases in many countries [2, 3]. In Korea, the prevalence of periodontitis is about 30% among adults in recent years .
Several factors were suggested as risk factors of periodontitis such as smoking and diabetes [5,6]. Diet and lower intake of various nutrients were also suggested as potential risk factors for periodontitis [7, 8].
Dairy foods have various kinds of nutrients including calcium, branched chain amino acids, conjugated linoleic acids, protein, vitamin D, and medium-chain fatty acids . In 2006, Al-Zahrani  proposed a novel hypothesis that dairy food intake might be inversely associated with periodontitis. The fact that dairy foods have a lot of calcium has been suggested as the reason. This suggestion seems reasonable because lower intake of calcium has been found to be significantly associated with increased prevalence of periodontitis . But, Shimazaki  reported a result refuting Al-Zahrani’s hypothesis and also provided potential explanation for it. In Hisayama study, the association of periodontitis with each type of dairy foods was examined. Among various types of dairy foods, only intake of lactic acid foods such as yogurt was associated with periodontitis. Although the amount of calcium in milk is the same as that in yogurt, the intake of milk does not have a significant effect on periodontitis. Yogurt has similar nutrients to milk, but it is characterized by a lot of lactic acid bacteria as a fermented food. Hence, the suggested reason is that lactic acid foods contain many live probiotics that have good effects on periodontitis .
A recent longitudinal study in older Danish adults proposed another hypothesis suggesting that dairy calcium from milk and fermented products may protect against periodontis . Calcium has emerged as an important cause for the association between intake of dairy foods and periodontitis again. But, given some recent studies on the association between probiotics and periodontitis [15,16], probiotics in fermented dairy foods could not be overlooked.
In order to test these conflicting hypotheses, it is necessary to directly investigate the association of yogurt, milk and calcium intake with the prevalence of periodontitis. We hypothesized that if intake of dairy foods is related to periodontitis due to probiotics but not to calcium, only yogurt intake would be associated with periodontitis, and milk or calcium intake would not. Therefore, we aimed to determine whether the lower intake of yogurt, milk, and calcium are associated with periodontitis from a nationally representative sample of Korean adults.
Materials and methods
Study design and subject selection
The data used in this study are a subset of the fourth Korea National Health and Nutrition Examination Survey (KNHANES) conducted in 2009 by Korea Centers for Disease Control and Prevention (KCDC) . The sampling protocol for the KNHANES was designed to involve a complex, stratified, multistage, probability-cluster survey of a representative sample of the non-institutionalized civilian population in Korea. The survey was performed by the Korean Ministry of Health. The target population of the survey was all non-institutionalized civilian Korean individuals aged 1 year or older. The survey employed stratified multistage probability sampling units based on geographic area, gender, and age, which were determined based on the household registries of the 2005 National Census Registry, the most recent 5-year national census in Korea. Using the 2005 census data, 200 primary sampling units (PSU) were selected annually across Korea. The details for sampling are described in the previous study for the association between manganese and periodontal status using this data and the fourth KNHANES reports [18, 19].
The sample set for 2009 KNHANES included 4,600 households and 10,533 participants. Of these participants, 7,095 individuals aged 19 years and older had a periodontal examination. Among them, 6,150 individuals who took a one-day 24-hour recall interview and responded to food frequency questionnaire were included in the final sample for this study.
The World Health Organization (WHO) community periodontal index (CPI) was used to assess periodontitis . Periodontitis was defined as a CPI greater than or equal to ‘code 3’, which indicates that at least one site had a probing pocket depth > 3.5 mm (code 4 > 5.5 mm). Index tooth numbers were 11, 16, 17, 26, 27, 31, 36, 37, 46 and 47.
A CPI probe (Osung MND CO. Ltd., Seoul, Korea) that met the WHO guidelines was used . The mouth was divided into sextants, and approximately 20 g force was used when probing. In the 2009 KNHANES, 27 trained dentists examined the periodontal status of the participants. The inter-examiner mean of Kappa value was 0.77 (0.53 to 0.94) .
Calcium intake levels and the frequency of yogurt & milk intake.
Nutrition surveys for gathering the data of calcium intake levels and the frequency of yogurt & milk intake were conducted by trained nutritionists at participant’s home. Each survey team was composed of two trained nutritionists. The quality control on the nutritional survey was conducted by the Center for Nutrition Policy and Promotion at Korea Health Industry Development Institute [18,22].
The daily calcium intake was converted from food intake data gained using a complete individual one-day 24-hour recall interview. Calcium intake was calculated by multiplying the weight for each food item which a participant reported to take in by calcium concentration data for the corresponding food code in Korean food composition table . The frequency of yogurt and milk intake was divided into two groups by once a week. The calcium intake levels of participants were also divided into two groups by a median value.
Socio-demographic variables comprised gender, age, household income and education level. Household income was the family income adjusted for the number of family members and converted quartiles. Education level was defined as the highest diploma the participant had received.
Oral health behaviors included daily frequency of toothbrushing and usage of dental floss or an interdental brush. For smoking status, participants were divided into three groups depending on the status: non-smokers (those who had never smoked or had smoked fewer than 100 cigarettes in their lifetime); current smokers (those who currently smoked and had smoked 100 cigarettes or more in their lifetime); and past smokers (those who had smoked in the past but were not current smokers). Systemic conditions included diabetes and obesity.
The complex sampling design of the survey was considered, and individual weighted factors were used when obtaining variances. Multivariate logistic regression analyses were applied to examine the associations of the frequency of yogurt & milk intake and calcium intake level with periodontitis. The odds ratios (ORs) of yogurt, milk, and calcium intake for periodontitis were adjusted for the above mentioned covariates in the multivariate logistic regression models. In order to find out effect modifiers, subgroup analyses were performed to gain stratified estimates according to gender, age, and current smoking status. Statistical analyses were performed using SPSS statistical software version 19.0 (SPSS, Chicago, IL).
The prevalence of periodontitis defined as a CPI code ≥ 3 was 30.8% in adults over the age 19 years (n = 6,150). In total participants, mean age (standard deviation) was 48.68 (16.20), female-to-male ratio was 1.44. The total participants consisted of 33% of the 19–39 age group, 54.7% of the 40–69 age group, and 12.3% of the 70 and over age group. Table 1 lists characteristics of participants categorized by periodontitis, including socio-demographic characteristics, oral and systemic health status, and oral and general health behaviors.
In Table 2, the association between the less yogurt intake and periodontitis was shown in the multivariate logistic regression model, but less milk intake and lower calcium intake were not associated with periodontitis. Less intake of yogurt (under once a week) was significantly associated with periodontitis (Odds ratio 0.82; 95% confidential interval 0.70–0.97).
Table 3 shows the results of subgroup analyses. No difference in the association of yogurt intake with periodontitis was found according to the strata of age, gender, and smoking.
This study investigates whether lower level of calcium intake and less intake of yogurt or milk were associated with poor periodontal health in Korean adults 19 or more years old after adjusting for socio-demographic variables, oral and general health behaviors, and oral and systemic health statuses.
In this study, less intake of yogurt was significantly associated with periodontitis, but neither less intake of milk nor lower intake of calcium is significantly associated with periodontitis. This finding is consistent with Hisayama study’s result  suggesting that the intake of lactic acid foods with probiotics was associated significantly with periodontitis, but that milk intake was not. Several studies reported that probiotics application was likely to have beneficial effects on periodontal disease [16,17,24], and it is suggested that probiotics produce metabolic substance such as reuterin which has the activity inhibiting the growth of periodontopathic bacteria . However, there are few studies on the effect of probiotics of yogurt on periodontitis.
The authors of Hisayama study inferred that calcium intake from dairy products might not have had a major impact on periodontitis, but they did not prove it directly. In this study, it is directly proved that calcium intake may not be associated with periodontitis. Contra the results of this study, a Danish study  reported that milk as well as yogurt was associated with periodontitis. But, it did not provide any reasonable explanation for the result that not cheese or non-dairy calcium but milk was associated with periodontitis.
In the subgroup analysis, the association of yogurt intake with periodontitis was not different according to the strata of age, gender, and smoking. Neither milk nor calcium intake was associated with periodontitis in all subgroups, either. We could not find any effect modifications in this analysis.
There are several limitations in this study. First of all, in KNHANES data, the intake level of calcium can be only supposed by the Korean dietary reference intakes (KDRIs) . Therefore, the criteria assessing the internal calcium status included the amounts of intake calculated from dietary survey data but not from biochemical indicators. Even though several countries adopt a 24-hour recall to yield the amount of nutrition intakes , it could not perfectly represent habitual calcium intake of individuals due to the shortness of survey days (a one-day 24-hour recall in Korea) and the dependence of the memory of individuals. Thus, using biochemical values would reflect the calcium status more accurately. However, the KDRIs were established as based on biochemical markers, which is one of the biochemical indicators for the calcium level .
Another limitation of this study in terms of dental examination is that periodontitis was assessed using the CPI. Although the CPI is an easy way to assess the prevalence of periodontitis in population surveys and epidemiological studies, it may overestimate or underestimate periodontal status due to the use of representative teeth and pseudo-pockets . Also, the type of periodontitis such as chronic or aggressive could not be divided.
The third limitation of this study is that we could not consider the systemic conditions such as gastrointestinal disease and malabsorption, which may affect the intake of dairy foods.
Finally, it is not possible to determine the direction of causal-relationship between yogurt intake and periodontitis since this study is cross-sectional.
Nevertheless, we directly investigated the association of yogurt, milk and calcium intake with the prevalence of periodontitis after adjusting for various potential confounders including sociodemographic variables, oral and general health behavioural factors and systemic health statuses. In addition, this study was carried out comprehensively with a representative Korean population sample.
In conclusion, periodontitis was significantly associated with less intake of yogurt among the Korean adults, but the calcium contained in yogurt is not likely to cause it. Further clinical studies are needed to elucidate the effect of yogurt intake on periodontitis.
The authors declare no conflicts of interest related to this study. The study was self-supported, but the Korea Center for Disease Control and Prevention (Cheongwongun, Korea) provided data from the Fourth Korea National Health and Nutrition Examination Survey to be used in the study.
- 1. Williams RC. Periodontal disease. N Engl J Med. 1990;323:373–82.
- 2. Albander JM, Bunelle JA, Kingman A. Destructive periodontal disease in adults 30 years of age and older in the United States, 1988–1994. J Periodontol. 1999;70:13–29. pmid:10052767
- 3. Petersen PE, Ogawa H. The global burden of periodontal disease: towards integration with chronic disease prevention and control. Periodontol 2000. 2012;60:15–39. pmid:22909104
- 4. Korea Centers for Disease Control and Prevention. Korea National Health and Nutrition Examination Survey. 2010. c2016 [cited 2016 Nov 15]. https://knhanes.cdc.go.kr/knhanes/index.do.
- 5. Genco RJ. Current view of risk factors for periodontal diseases. J Periodontol. 1996;67(Suppl.):1041–9.
- 6. Albandar JM. Global risk factors and risk indicators for periodontal diseases. Periodontol 2000. 2002;29: 177–206. pmid:12102708
- 7. Al-Zahrani MS, Bissada NF, Borawski EA. Diet and periodontitis. J Int Acad Periodontol. 2005;7:21–6. pmid:15736892
- 8. Nishida M, Grossi SG, Dunford RG, Ho AW, Trevisan M, Genco RJ. Dietary vitamin C and the risk for periodontal disease. J Periodontol. 2000;71:1215–23. pmid:10972636
- 9. Van Loan M. The role of dairy foods and dietary calcium in weight management. J Am Coll Nutr. 2009;28 Suppl 1:120S–9S.
- 10. Al-Zahrani MS. Increased intake of dairy products is related to lower periodontitis prevalence. J Periodontol. 2006;77:289–94. pmid:16460256
- 11. Nishida M, Grossi SG, Dunford RG, Ho AW, Trevisan M, Genco RJ. Calcium and the risk for periodontal disease. J Periodontol. 2000;71:1057–66. pmid:10960010
- 12. Shimazaki Y, Shirota T, Uchida K, Yonemoto K, Kiyohara Y, Iida M, et al. Intake of dairy products and periodontal disease: the Hisayama Study. J Periodontol. 2008;79:131–7. pmid:18166102
- 13. Sookkhee S, Chulasiri M, Prachyabrued W. Lactic acid bacteria from healthy oral cavity of Thai volunteers: Inhibition of oral pathogens. J Appl Microbiol. 2001;90:172–9. pmid:11168719
- 14. Adegboye AR, Christensen LB, Holm-Pedersen P, Avlund K, Boucher BJ, Heitmann BL. Intake of dairy products in relation to periodontitis in older Danish adults. Nutrients. 2012;4:1219–29. pmid:23112910
- 15. Teughels W, Durukan A, Ozcelik O, Pauwels M, Quirynen M, Haytac MC. Clinical and microbiological effects of Lactobacillus reuteri probiotics in the treatment of chronic periodontitis: a randomized placebo-controlled study. J Clin Periodontol. 2013;40:1025–35. pmid:24164569
- 16. Tekce M, Ince G, Gursoy H, Dirikan Ipci S, Cakar G, Kadir T, et al. Clinical and microbiological effects of probiotic lozenges in the treatment of chronic periodontitis: a 1-year follow-up study. J Clin Periodontol. 2015;42:363–72. pmid:25728888
- 17. Korea Centers for Disease Control and Prevention. The Forth Korea National Health and Nutrition Examination Survey (KNHANES IV-3). Cheongwongun: Korea Center for Disease Control and Prevention; 2010.
- 18. Korea Centers for Disease Control and Prevention. The sample design for the Forth Korea National Health and Nutrition Examination Survey (2007–2009). Cheongwongun: Korea Center for Disease Control and Prevention; 2010.
- 19. Korea Center for Disease Control and Prevention. Guidelines for raw materials of the Forth Korea National Health and Nutrition Examination Survey (2007–2009). Cheongwongun: Korea Center for Disease Control and Prevention; 2010.
- 20. World Health Organization. Oral Health Surveys: Basic Methods. 4th ed. Geneva: World Health Organization; 1997.
- 21. Korea Center for Disease Control and Prevention. Standardization for Oral Health Survey in KNHANES (2009). Cheongwongun: Korea Center for Disease Control and Prevention; 2010.
- 22. Lee HJ, Cho JI, Lee HS, Kim CI, Cho E. Intakes of dairy products and calcium and obesity in Korean adults: Korean National Health and Nutrition Examination Surveys (KNHANES) 2007–2009. PLoS One. 2014;9:e99085. pmid:24915202
- 23. Twetman S, Derawi B, Keller M, Ekstrand K, Yucel-Lindberg T, Stecksen-Blicks C. Short-term effect of chewing gums containing probiotic Lactobacillus reuteri on the levels of inflammatory mediators in gingival crevicular fluid. Acta Odontol Scand. 2009;67:19–24. pmid:18985460
- 24. Hur IY, Jang MJ, Oh KW. Food and Nutrient Intakes According to Income in Korean Men and Women. Osong Public Health Res Perspect 2011;2:192–7. pmid:24159472
- 25. The Korean Nutrition Society. Dietary reference intakes for Koreans 2010. Seoul: The Korean Nutrition Society; 2010.
- 26. Korea Center for Disease Control and Prevention. Guidelines for raw materials of the Forth Korea National Health and Nutrition Examination Survey (2007–2009). Cheongwongun: Korea Center for Disease Control and Prevention; 2010.
- 27. Kingman A, Albandar JM. Methodological aspects of epidemiological studies of periodontal diseases. Periodontol 2000 2002;29:11–30. pmid:12102701