The Triangle of Nonalcoholic Fatty Liver Disease, Metabolic Dysfunction, and Periodontitis: Analysis of the Dental, Oral, Medical and Epidemiological (DOME) Records-Based Nationwide Research
Abstract
:1. Introduction
- A.
- Measure the prevalence of NAFLD and study the associations of NAFLD, with the prevalence of the following planned and delivered dental procedures: (1) fillings, (2) endodontic treatments, (3) post-treatment, (4) crowns, (5) extractions, (6) periodontal disease, and (7) missing teeth, as well as with the medical and dental attendance patterns. This specific goal will enable us to address the “dental cluster”.
- B.
- To address possible confounders, we aim to further explore the associations of NAFLD with dental status in a multivariate model controlling for (1) socio-demographic parameters, (2) health-related risk habits, and (3) each of the MetS components and consequences and related conditions, including diabetes type 2, hypertension, hyperlipidemia, impaired glucose tolerance (IGT), obesity, cardiovascular disease, S/P stroke, S/P transient ischemic attack (TIA), obstructive sleep apnea (OSA), and (5) auxiliary test results, including the blood tests used in the assessment of MetS related conditions. This specific goal will enable us to address the “MetS cluster”.
2. Methods
2.1. Data Source
2.2. Data Collection
2.3. Study Variables
- 1.
- The dependent variable—nonalcoholic fatty liver disease (NAFLD), equivalent to 2015 ICD-9-CM Diagnosis Code 571.8: other chronic nonalcoholic liver disease.
- 2.
- Other systemic conditions related to MetS were included as independent variables and were also based on ICD-9-CM diagnoses, including diabetes mellitus, impaired glucose tolerance (IGT), hyperlipidemia, hypertension, cardiovascular disease, obesity (BMI > 30 kg/m2), obstructive sleep apnea (OSA), S/P (status post) transient ischemic attack (TIA), and S/P stroke [14,15,30].
2.4. Statistical Methods
3. Results
3.1. The Associations between NAFLD and Socio-Demographic Parameters
- (1)
- Male sex (OR (95% CI) men vs. women: 6.29 (4.69–8.47)).
- (2)
- Education: technical vs. high school education (OR = 26.73 (22.44–31.83)) and academic vs. high school education (OR = 17.17 (14.48–20.36)).
- (3)
- SES: low vs. high SES (OR= 1.19 (0.86–1.65)) and medium vs. high SES (OR = 1.25 (1.09–1.43)).
- (4)
- Birth country: being an immigrant from the following birth countries, compared to native Israelis: Africa (OR = 4.77 (2.60–8.73)), Asia (3.79 (2.18–6.61)), western Europe (OR = 1.49 (1.22–1.83)), eastern Europe (OR = 1.19 (0.70–2.02)).
- (5)
- Older age (OR = 1.19 (1.18–1.20)).
- (6)
- More time in service (OR = 1.14 (1.13–1.15)).
- (1)
- The locality of residence: urban Jewish vs. rural locality (OR = 0.26 (0.16–0.43)) and urban non-Jewish vs. rural locality (OR = 0.16 (0.09–0.28)).
- (2)
- Birth country: being an immigrant from the following birth countries compared to native Israelis: Ethiopia (OR = 0.33 (0.13–0.80)), North America (OR = 0.25 (0.10–0.61)), and South America (OR = 0.76 (0.31–1.83)).
3.2. The Associations between NAFLD and MetS Components, Consequences, and Related Conditions
3.3. The Associations of NAFLD with Auxiliary Test Results
3.4. The Associations of NAFLD with Health-Related Habits and Medical and Dental Attendance Patterns
3.5. The Associations of NAFLD with Dental and Oral Status
3.6. Receiver Operating Characteristic (ROC) Analyses of Planned and Delivered Standard Dental Units (SDU-P and SDU-D) as Predictors of NAFLD
3.7. Multivariate Analysis of NAFLD Diagnosis as a Dependent Variable
4. Discussion
4.1. Socio-Demographic Parameters and NAFLD
4.2. Health-Related Habits and NAFLD
4.3. MetS Components, Consequences, and Related Conditions and NAFLD
4.4. Dental Status and NAFLD
5. Strength and Limitations
6. Conclusions
- The results confirmed the hypothesis of this research, i.e., that NAFLD is associated with dental morbidity, particularly with periodontitis.
- The multivariate analysis established a profile of the “patient vulnerable to NAFLD”, including older age, male sex, and other MetS components, including diabetes type 2, hypertension, hyperlipidemia, BMI, and periodontitis.
- This profile aligns with the current new definition of metabolic dysfunction-associated fatty liver disease (MAFLD).
- A collaborative effort is needed from the dental and general medical authorities by sharing information regarding dental and systemic morbidities.
- The study also highlights the need to adopt a holistic risk management approach that considers both dental and systemic conditions.
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
BMI | Body mass index |
MPR | Medical patient record |
CRP | C-reactive protein |
CVD | Cardiovascular disease |
DPR | Dental patient record |
HbA1c | Glycated hemoglobin |
HDL | High-density lipoprotein |
IDF | Israeli Defense Force |
LDL | Low-density lipoprotein |
MetS NAFLD | Metabolic syndrome Non-alcoholic fatty liver disease |
OSA | Obstructive sleep apnea |
SES | Socio-economic status |
TIA | Transient ischemic attack |
VLDL | Very low-density lipoprotein |
References
- Younossi, Z.; Anstee, Q.M.; Marietti, M.; Hardy, T.; Henry, L.; Eslam, M.; George, J.; Bugianesi, E. Global burden of NAFLD and NASH: Trends, predictions, risk factors and prevention. Nat. Rev. Gastroenterol. Hepatol. 2018, 15, 11–20. [Google Scholar] [CrossRef] [PubMed]
- Eslam, M.; Newsome, P.N.; Sarin, S.K.; Anstee, Q.M.; Targher, G.; Romero-Gomez, M.; Zelber-Sagi, S.; Wai-Sun Wong, V.; Dufour, J.F.; Schattenberg, J.M.; et al. A new definition for metabolic dysfunction-associated fatty liver disease: An international expert consensus statement. J. Hepatol. 2020, 73, 202–209. [Google Scholar] [CrossRef] [PubMed]
- Williams, C.D.; Stengel, J.; Asike, M.I.; Torres, D.M.; Shaw, J.; Contreras, M.; Landt, C.L.; Harrison, S.A. Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: A prospective study. Gastroenterology 2011, 140, 124–131. [Google Scholar] [CrossRef] [PubMed]
- Alberti, K.G.; Eckel, R.H.; Grundy, S.M.; Zimmet, P.Z.; Cleeman, J.I.; Donato, K.A.; Fruchart, J.C.; James, W.P.; Loria, C.M.; Smith, S.C., Jr. Harmonizing the metabolic syndrome: A joint interim statement of the international diabetes federation task force on epidemiology and prevention; national heart, lung, and blood institute; american heart association; world heart federation; international atherosclerosis society; and international association for the study of obesity. Circulation 2009, 120, 1640–1645. [Google Scholar] [PubMed] [Green Version]
- Weintraub, J.A.; Lopez Mitnik, G.; Dye, B.A. Oral diseases associated with nonalcoholic fatty liver disease in the united states. J. Dent. Res. 2019, 98, 1219–1226. [Google Scholar] [CrossRef] [PubMed]
- Kassebaum, N.J.; Bernabe, E.; Dahiya, M.; Bhandari, B.; Murray, C.J.; Marcenes, W. Global burden of severe periodontitis in 1990-2010: A systematic review and meta-regression. J. Dent. Res. 2014, 93, 1045–1053. [Google Scholar] [CrossRef]
- Bernabe, E.; Marcenes, W.; Hernandez, C.R.; Bailey, J.; Abreu, L.G.; Alipour, V.; Amini, S.; Arabloo, J.; Arefi, Z.; Arora, A.; et al. Global, regional, and national levels and trends in burden of oral conditions from 1990 to 2017: A systematic analysis for the global burden of disease 2017 Study. J. Dent. Res. 2020, 99, 362–373. [Google Scholar]
- Tonetti, M.S.; Jepsen, S.; Jin, L.; Otomo-Corgel, J. Impact of the global burden of periodontal diseases on health, nutrition and wellbeing of mankind: A call for global action. J. Clin. Periodontol. 2017, 44, 456–462. [Google Scholar] [CrossRef] [Green Version]
- Marcenes, W.; Kassebaum, N.J.; Bernabe, E.; Flaxman, A.; Naghavi, M.; Lopez, A.; Murray, C.J. Global burden of oral conditions in 1990–2010: A systematic analysis. J. Dent. Res. 2013, 92, 592–597. [Google Scholar] [CrossRef] [Green Version]
- Cappelli, D.P.; Mobley, C.C. Prevention in Clinical Oral Health Care; Mosby Elsevier St.: Louis, MO, USA, 2007. [Google Scholar]
- Marthaler, T.M. Changes in dental caries 1953–2003. Caries Res. 2004, 38, 173–181. [Google Scholar] [CrossRef]
- Abdalla-Aslan, R.; Findler, M.; Levin, L.; Zini, A.; Shay, B.; Twig, G.; Almoznino, G. Where periodontitis meets metabolic syndrome-The role of common health-related risk factors. J. Oral. Rehabil. 2019, 46, 647–656. [Google Scholar] [CrossRef] [PubMed]
- Abdalla-Aslan, R.; Findler, M.; Zini, A.; Almoznino, G. Caries experience, periodontal status, and metabolic morbidity in patients with psychiatric disorders. Quintessence Int. 2021, 52, 516–526. [Google Scholar]
- Almoznino, G.; Kessler Baruch, O.; Kedem, R.; Protter, N.E.; Shay, B.; Yavnai, N.; Zur, D.; Mijiritsky, E.; Abramovitz, I. SOS Teeth: First priority teeth with advanced caries and its associations with metabolic syndrome among a national representative sample of young and middle-aged adults. J. Clin. Med. 2020, 9, 3170. [Google Scholar] [CrossRef] [PubMed]
- Abramovitz, I.; Zini, A.; Pribluda, P.; Kedem, R.; Zur, D.; Protter, N.E.; Almoznino, G. “Dental Cluster” versus “metabolic cluster”: Analyzing the Associations of planned and delivered dental procedures with metabolic syndrome, utilizing data from the dental, oral, medical epidemiological (DOME) cross-sectional record-based nationwide study. Biology 2021, 10, 608. [Google Scholar] [CrossRef]
- Almoznino, G.; Gal, N.; Levin, L.; Mijiritsky, E.; Weinberg, G.; Lev, R.; Zini, A.; Touger-Decker, R.; Chebath-Taub, D.; Shay, B. Diet practices, body mass index, and oral health-related quality of life in adults with periodontitis- A case-control study. Int. J. Environ. Res. Public Healthy 2020, 17, 2340. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Almoznino, G.; Zini, A.; Kedem, R.; Protter, N.E.; Zur, D.; Abramovitz, I. Hypertension and its associations with dental status: Data from the dental, oral, medical epidemiological (DOME) nationwide records-based study. J. Clin. Med. 2021, 10, 176. [Google Scholar] [CrossRef] [PubMed]
- Baima, G.; Romandini, M.; Citterio, F.; Romano, F.; Aimetti, M. Periodontitis and accelerated biological aging: A geroscience approach. J. Dent. Res. 2021, 101, 125–132. [Google Scholar] [CrossRef]
- Sanz, M.; Marco Del Castillo, A.; Jepsen, S.; Gonzalez-Juanatey, J.R.; D’Aiuto, F.; Bouchard, P.; Chapple, I.; Dietrich, T.; Gotsman, I.; Graziani, F.; et al. Periodontitis and cardiovascular diseases: Consensus report. J. Clin. Periodontol. 2020, 47, 268–288. [Google Scholar] [CrossRef] [PubMed]
- Loe, H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 1993, 16, 329–334. [Google Scholar] [CrossRef]
- Kim, J.Y.; Lee, G.N.; Song, H.C.; Park, Y.M.; Ahn, Y.B.; Han, K.; Ko, S.H. Association between fatty liver index and periodontitis: The Korea national health and nutrition examination survey. Sci. Rep. 2020, 10, 3805. [Google Scholar] [CrossRef] [Green Version]
- Yao, C.; Lan, D.; Li, X.; Wang, Y.; Qi, S.; Liu, Y. Porphyromonas gingivalis is a risk factor for the development of nonalcoholic fatty liver disease via ferroptosis. Microbes Infect. 2022, 105040. [Google Scholar] [CrossRef] [PubMed]
- Ahmad, A.; Furuta, M.; Shinagawa, T.; Takeuchi, K.; Takeshita, T.; Shimazaki, Y.; Yamashita, Y. Association of periodontal status with liver abnormalities and metabolic syndrome. J. Oral. Sci. 2015, 57, 335–343. [Google Scholar] [CrossRef] [PubMed]
- Kuraji, R.; Sekino, S.; Kapila, Y.; Numabe, Y. Periodontal disease-related nonalcoholic fatty liver disease and nonalcoholic steatohepatitis: An emerging concept of oral-liver axis. Periodontol. 2000 2021, 87, 204–240. [Google Scholar] [CrossRef]
- Akinkugbe, A.A.; Barritt, A.S.; Cai, J.; Offenbacher, S.; Thyagarajan, B.; Khambaty, T.; Singer, R.; Kallwitz, E.; Heiss, G.; Slade, G.D. Periodontitis and prevalence of elevated aminotransferases in the Hispanic Community Health Study/Study of Latinos. J. Periodontol. 2018, 89, 949–958. [Google Scholar] [CrossRef] [PubMed]
- Wijarnpreecha, K.; Panjawatanan, P.; Cheungpasitporn, W.; Lukens, F.J.; Harnois, D.M.; Pungpapong, S.; Ungprasert, P. The association between periodontitis and nonalcoholic fatty liver disease: A systematic review and meta-analysis. J. Gastrointestin. Liver Dis. 2020, 29, 211–217. [Google Scholar] [CrossRef]
- Sheiham, A.; Watt, R.G. The common risk factor approach: A rational basis for promoting oral health. Community Dent. Oral. Epidemiol. 2000, 28, 399–406. [Google Scholar] [CrossRef]
- Abramovitz, I.; Zini, A.; Atzmoni, M.; Kedem, R.; Zur, D.; Protter, N.E.; Almoznino, G. Cognitive performance and its associations with dental caries: Results from the dental, oral, medical epidemiological (DOME) records-based nationwide study. Biology 2021, 10, 178. [Google Scholar] [CrossRef]
- Almoznino, G.; Abramovitz, I.; Kessler Baruch, O.; Kedem, R.; Protter, N.E.; Levine, J.; Bader, T.; Yavnai, N.; Zur, D.; Mijiritsky, E.; et al. SOS Teeth: Age and sex differences in the prevalence of first priority teeth among a national representative sample of young and middle-aged adults. Int. J Environ. Res. Public. Healthy 2020, 17, 4847. [Google Scholar] [CrossRef]
- Almoznino, G.; Kedem, R.; Turgeman, R.; Bader, T.; Yavnai, N.; Zur, D.; Shay, B. The Dental, Oral, Medical Epidemiological (DOME) Study: Protocol and study methods. Methods Inf. Med. 2020, 59, 119–130. [Google Scholar] [CrossRef]
- Abramovitz, I.; Zini, A.; Kessler Baruch, O.; Kedem, R.; Protter, N.E.; Shay, B.; Yavnai, N.; Zur, D.; Mijiritsky, E.; Almoznino, G. SOS teeth with advanced caries and sociodemographic indicators, health-related habits and dental attendance patterns: Data from the Dental, Oral, Medical Epidemiological (DOME) nationwide records-based study. BMC Oral. Healthy 2021, 21, 389. [Google Scholar] [CrossRef]
- Twig, G.; Yaniv, G.; Levine, H.; Leiba, A.; Goldberger, N.; Derazne, E.; Ben-Ami Shor, D.; Tzur, D.; Afek, A.; Shamiss, A.; et al. Body-Mass index in 2.3 million adolescents and cardiovascular death in adulthood. N. Engl. J. Med. 2016, 374, 2430–2440. [Google Scholar] [CrossRef] [PubMed]
- IDF (Israel Defense Forces). Personal Data- The Medical Profile. Available online: https://www.mitgaisim.idf.il/%D7%9B%D7%AA%D7%91%D7%95%D7%AA/english/tzav-rishon/the-medical-profile/#/ (accessed on 1 November 2022).
- IDF. Volunteering in the IDF for Military Exemption Recipients. Available online: https://www.kolzchut.org.il/en/Volunteering_in_the_IDF_for_Military_Exemption_Recipients (accessed on 1 November 2022).
- Engelchin-Nissan, E.; Catan, G.; Oz, N.; Arieli, E.; Brief, I.; Ben Moshe, R.; Shmueli, A. Utilization of Health Services by IDF Soldiers and Civilian Population at an Israeli HMO. Healthy Econ. Outcome Res. Open Access S1 2017, 103, 2–6. [Google Scholar]
- ADA (American Dental Association). ADA Guide to Dental Procedures Reported with Area of the Oral Cavity or Tooth Anatomy (or Both). Version 1. Available online: https://www.ada.org/-/media/project/ada-organization/ada/ada-org/files/publications/cdt/appendix-3_areaoftheoralcavityandtoothanatomybycdtcode_2023jan.pdf (accessed on 30 October 2022).
- Yang, S.; Berdine, G. The receiver operating characteristic (ROC) curve. Southwest Respir. Crit. Care Chron. 2017, 5, 34–36. [Google Scholar] [CrossRef]
- Dietrich, P.; Hellerbrand, C. Non-alcoholic fatty liver disease, obesity and the metabolic syndrome. Best Pract. Res. Clin. Gastroenterol. 2014, 28, 637–653. [Google Scholar] [CrossRef]
- Gutierrez-Grobe, Y.; Ponciano-Rodriguez, G.; Ramos, M.H.; Uribe, M.; Mendez-Sanchez, N. Prevalence of non alcoholic fatty liver disease in premenopausal, posmenopausal and polycystic ovary syndrome women. The role of estrogens. Ann. Hepatol. 2010, 9, 402–409. [Google Scholar] [CrossRef]
- Vilar-Gomez, E.; Nephew, L.D.; Vuppalanchi, R.; Gawrieh, S.; Mladenovic, A.; Pike, F.; Samala, N.; Chalasani, N. High-quality diet, physical activity, and college education are associated with low risk of NAFLD among the US population. Hepatology 2022, 75, 1491–1506. [Google Scholar] [CrossRef]
- Liu, Y.; Dai, M.; Bi, Y.; Xu, M.; Xu, Y.; Li, M.; Wang, T.; Huang, F.; Xu, B.; Zhang, J.; et al. Active smoking, passive smoking, and risk of nonalcoholic fatty liver disease (NAFLD): A population-based study in China. J. Epidemiol. 2013, 23, 115–121. [Google Scholar] [CrossRef] [Green Version]
- Yki-Jarvinen, H. Non-alcoholic fatty liver disease as a cause and a consequence of metabolic syndrome. Lancet Diabetes Endocrinol. 2014, 2, 901–910. [Google Scholar] [CrossRef]
- Munoz-Garach, A.; Cornejo-Pareja, I.; Tinahones, F.J. Does Metabolically Healthy Obesity Exist? Nutrients 2016, 8, 320. [Google Scholar] [CrossRef] [Green Version]
- Qiao, F.; Fu, K.; Zhang, Q.; Liu, L.; Meng, G.; Wu, H.; Xia, Y.; Bao, X.; Gu, Y.; Shi, H.; et al. The association between missing teeth and non-alcoholic fatty liver disease in adults. J. Clin. Periodontol. 2018, 45, 941–951. [Google Scholar] [CrossRef]
- Fu, K.Y.; Qiao, F.; Meng, G.; Zhang, Q.; Liu, L.; Song, K.; Niu, K.J. Association between tooth missing and non-alcoholic fatty liver disease. Zhonghua Liu Xing Bing Xue Za Zhi 2020, 41, 716–721. [Google Scholar] [PubMed]
- Akinkugbe, A.A.; Slade, G.D.; Barritt, A.S.; Cole, S.R.; Offenbacher, S.; Petersmann, A.; Kocher, T.; Lerch, M.M.; Mayerle, J.; Volzke, H.; et al. Periodontitis and non-alcoholic fatty liver disease, a population-based cohort investigation in the study of health in pomerania. J. Clin. Periodontol. 2017, 44, 1077–1087. [Google Scholar] [CrossRef] [PubMed]
- Yoneda, M.; Naka, S.; Nakano, K.; Wada, K.; Endo, H.; Mawatari, H.; Imajo, K.; Nomura, R.; Hokamura, K.; Ono, M.; et al. Involvement of a periodontal pathogen, Porphyromonas gingivalis on the pathogenesis of non-alcoholic fatty liver disease. BMC Gastroenterol. 2012, 12, 16. [Google Scholar] [CrossRef] [PubMed]
- Duseja, A.; Chahal, G.S.; Jain, A.; Mehta, M.; Ranjan, A.; Grover, V. Association between nonalcoholic fatty liver disease and inflammatory periodontal disease: A casecontrol study. J. Indian Soc. Periodontol. 2021, 25, 47–54. [Google Scholar]
- Han, P.; Sun, D.; Yang, J. Interaction between periodontitis and liver diseases. Biomed. Rep. 2016, 5, 267–276. [Google Scholar] [CrossRef] [Green Version]
- Alakhali, M.S.; Al-Maweri, S.A.; Al-Shamiri, H.M.; Al-Haddad, K.; Halboub, E. The potential association between periodontitis and non-alcoholic fatty liver disease: A systematic review. Clin. Oral. Investig. 2018, 22, 2965–2974. [Google Scholar] [CrossRef]
- Albuquerque-Souza, E.; Sahingur, S.E. Periodontitis, chronic liver diseases, and the emerging oral-gut-liver axis. Periodontol. 2000 2022, 89, 125–141. [Google Scholar] [CrossRef]
- Ishikawa, M.; Yoshida, K.; Okamura, H.; Ochiai, K.; Takamura, H.; Fujiwara, N.; Ozaki, K. Oral porphyromonas gingivalis translocates to the liver and regulates hepatic glycogen synthesis through the Akt/GSK-3beta signaling pathway. Biochim. Biophys Acta 2013, 1832, 2035–2043. [Google Scholar] [CrossRef]
Parameter | Variable | Without NAFLD (N, %) | NAFLD (N, %) | p Value | OR and 95% CI # |
---|---|---|---|---|---|
NAFLD diagnosis (No/Yes) | 131,591 (99.3) | 938 (0.7) | |||
Sex | Men | 98,575 (99.1) | 891 (0.9) | <0.001 ^ | 6.29 (4.69–8.47) |
Women | 33,016 (99.9) | 47 (0.1) | 1 | ||
Education (Y) | High school | 111,908 (99.8) | 204 (0.2) | <0.001 * | 1 |
Technicians | 7081 (95.4) | 345 (4.6) | 26.73 (22.44–31.83) | ||
Academic | 12,427 (97.0) | 389 (3.0) | 17.17 (14.48–20.36) | ||
Locality of residence | Urban Jewish | 112,635 (99.3) | 833 (0.7) | <0.001 * | 0.26 (0.16–0.43) |
Urban Non-Jewish | 17,835 (99.5) | 83 (0.5) | 0.16 (0.09–0.28) | ||
Rural | 567 (97.3) | 16 (2.7) | 1 | ||
Socio-economic status (SES) | Low | 5677 (99.3) | 42 (0.7) | 0.005 * | 1.19 (0.86–1.65) |
Medium | 68,093 (99.2) | 526 (0.8) | 1.25 (1.09–1.43) | ||
High | 56,359 (99.4) | 348 (0.6) | 1 | ||
Birth country | Western Europe | 10,463 (99.0) | 108 (1.0) | <0.001 * | 1.49 (1.22–1.83) |
Eastern Europe | 1701 (99.2) | 14 (0.8) | 1.19 (0.70–2.02) | ||
Asia | 496 (97.4) | 13 (2.6) | 3.79 (2.18–6.61) | ||
Ethiopia | 2180 (99.8) | 5 (0.2) | 0.33 (0.13–0.80) | ||
Africa | 334 (96.8) | 11 (3.2) | 4.77 (2.60–8.73) | ||
North America | 2854 (99.8) | 5 (0.2) | 0.25 (0.10–0.61) | ||
South America | 952 (99.5) | 5 (0.5) | 0.76 (0.31–1.83) | ||
Israel | 112,582 (99.3) | 777 (0.7) | 1 | ||
Parameter | NAFLD | Mean ± SD | p value ** | OR (95% CI) ## | |
Age | No | 21.78 ± 5.88 | <0.001 | 1.19 (1.18–1.20) | |
Yes | 36.81 ± 7.67 | ||||
Time in service | No | 3.02 ± 6.13 | <0.001 | 1.14 (1.13–1.15) | |
Yes | 18.46 ± 9.17 |
Parameter | Variable | No NAFLD | NAFLD | p Value ^ | OR and 95% CI # |
---|---|---|---|---|---|
Hypertension | No | 128,473 (99.5) | 693 (0.5) | <0.001 | 1 |
Yes | 3118 (92.7) | 245 (7.3) | 13.51 (11.76–15.62) | ||
Hyperlipidemia | No | 124,527 (99.8) | 276 (0.2) | <0.001 | 1 |
Yes | 7064 (91.4) | 662 (8.6) | 38.46 (33.33–45.45) | ||
Impaired glucosetolerance (IGT) | No | 131,488 (99.3) | 913 (0.7) | <0.001 | 1 |
Yes | 103 (80.5) | 25 (19.5) | 34.95 (22.47–54.37) | ||
Diabetes type 2 | No | 131,321 (99.3) | 863 (0.7) | <0.001 | 1 |
Yes | 270 (78.3) | 75 (21.7) | 33.33 (27.02–41.66) | ||
Obesity | No | 124,826 (99.8) | 255 (0.2) | <0.001 | 1 |
Yes | 6765 (90.8) | 683 (9.2) | 45.45 (38.46–52.63) | ||
Cardiovascular disease | No | 128,161 (99.4) | 770 (0.6) | <0.001 | 1 |
Yes | 3430 (95.3) | 168 (4.7) | 7.81 (6.62–9.17) | ||
Obstructive sleep apnea (OSA) | No | 131,308 (99.3) | 903 (0.7) | <0.001 | 1 |
Yes | 283 (89.0) | 35 (11.0) | 16.13 (11.76–22.22) | ||
Stroke | No | 131,509 (99.3) | 928 (0.7) | <0.001 | 1 |
Yes | 82 (89.1) | 10 (10.9) | 15.63 (8.62–27.78) | ||
Transient ischemic attack (TIA) | No | 131,500 (99.3) | 930 (0.7) | <0.001 | 1 |
Yes | 91 (91.9) | 8 (8.1) | 11.49 (5.92–22.22) |
Parameter | Without NAFLD | NAFLD | p Value * | OR and 95% CI ## | ||
---|---|---|---|---|---|---|
N | Mean ± SD | N | Mean ± SD | |||
Weight (kilograms) | 65,810 | 73.04 ± 32.44 | 807 | 93.95 ± 17.22 | <0.001 | 1.005 (1.004–1.005) |
Body mass index (BMI) | 65,589 | 24.20 ± 4.24 | 805 | 30.28 ± 4.64 | <0.001 | 1.231 (1.217–1.245) |
C reactive protein (CRP) (mg/L) | 29,878 | 3.74 ± 10.12 | 540 | 5.54 ± 12.83 | <0.001 | 1.010 (1.005–1.015) |
Glycated hemoglobin (HbA1c) (%) | 1727 | 5.35 ± 0.92 | 216 | 5.78 ± 1.18 | <0.001 | 1.277 (1.143–1.427) |
Fasting glucose (mg/dL) | 2421 | 86.95 ± 11.65 | 106 | 91.00 ± 16.79 | 0.016 | 1.020 (1.008–1.032) |
Cholesterol (mg/dL) | 27,280 | 175.43 ± 35.48 | 900 | 187.79 ± 37.96 | <0.001 | 1.009 (1.007–1.011) |
High-density lipoprotein (HDL) (mg/dL) | 27,273 | 48.49 ± 11.79 | 900 | 41.81 ± 8.83 | <0.001 | 0.938 (0.931–0.945) |
Low-density lipoprotein (LDL) (mg/dL) | 19,359 | 108.05 ± 29.92 | 854 | 114.95 ± 31.85 | <0.001 | 1.007 (1.005–1.009) |
LDL cholesterol calculated (mg/dL) | 16,788 | 108.10 ± 30.26 | 670 | 115.18 ± 33.10 | <0.001 | 1.007 (1.005–1.009) |
Triglycerides (mg/dL) | 27,283 | 102.75 ± 62.00 | 900 | 156.49 ± 95.03 | <0.001 | 1.007 (1.006–1.008) |
Very low-density lipoprotein (VLDL) (mg/dL) | 27,234 | 20.30 ± 10.93 | 897 | 29.90 ± 14.67 | <0.001 | 1.051 (1.047–1.055) |
Non-HDL cholesterol (mg/dL) | 16,035 | 128.76 ± 34.82 | 787 | 144.69 ± 35.39 | <0.001 | 1.012 (1.010–1.014) |
Parameter | Variable | Without NAFLD | NAFLD | p Value ^ | OR and 95% CI # |
---|---|---|---|---|---|
Smoking | No | 125,060 (99.5) | 585 (0.5) | <0.001 | 1 |
Yes | 6531 (94.9) | 353 (5.1) | 11.55 (10.10–13.2) | ||
Teeth brushing once a day or more | No | 17,557 (98.5) | 263 (1.5) | <0.001 | 1 |
Yes | 39,381 (99.3) | 295 (0.7) | 0.50 (0.42–0.59) | ||
Consumption of a cariogenic diet | No | 34,106 (98.8) | 415 (1.2) | <0.001 | 1 |
Yes | 22,832 (99.4) | 143 (0.6) | 0.52 (0.43–0.62) | ||
Consumption of sweetened beverages | No | 32,601 (98.8) | 408 (1.2) | <0.001 | 1 |
Yes | 24,337 (99.4) | 150 (0.6) | 0.49 (0.41–0.59) | ||
Parameter | Variable | Without NAFLD | NAFLD | p Value ** | OR and 95% CI ## |
Total number of appointments with a general physician | 14.19 ± 11.96 | 17.85 ± 15.01 | <0.001 | 1.016 (1.016–1.024) | |
The number of times where scaling was performed | 0.63 ± 0.86 | 1.07 ± 1.22 | <0.001 | 1.41 (1.35–1.47) | |
The number of times where root planning was performed | 0.06 ± 0.57 | 0.47 ± 1.56 | <0.001 | 1.35 (1.30–1.40) | |
The number of examinations by an oral medicine specialist | 0.01 ± 0.17 | 0.07 ± 0.43 | <0.001 | 1.59 (1.38–1.82) | |
The number of examinations by a periodontal specialist | 0.03 ± 0.27 | 0.21 ± 0.68 | <0.001 | 1.84 (1.70–1.99) | |
Total number of dental appointments | 5.81 ± 10.14 | 15.26 ± 18.16 | <0.001 | 1.03 (1.02–1.03) | |
Non-attendance to scheduled dental appointments | 0.98 ± 2.646 | 2.17 ± 4.218 | <0.001 | 1.06 (1.05–1.08) |
Parameter | Variable | Without NAFLD | NAFLD | p Value ^ | OR and 95% CI # |
---|---|---|---|---|---|
Periodontitis | No | 51,424 (99.1) | 442 (0.9) | <0.001 | 1 |
Yes | 5514 (97.9) | 116 (2.1) | 2.41 (1.97–2.96) | ||
Presence of an oral soft tissue lesion in an oral examination | No | 130,013 (99.3) | 859 (0.7) | <0.001 | 1 |
Yes | 1578 (95.2) | 79 (4.8) | 7.25 (5.81–9.09) | ||
Parameter | Without NAFLD | NAFLD | p Value ** | OR and 95% CI ## | |
Mean ± SD | Mean ± SD | ||||
The number of teeth that required one surface amalgam filling | 0.61 ± 1.21 | 0.39 ± 0.88 | <0.001 | 0.82 (0.76–0.88) | |
The number of teeth where one surface amalgam filling was performed | 0.29 ± 0.78 | 0.26 ± 0.70 | <0.009 | 0.94 (0.87–1.03) | |
The number of teeth that required two amalgam fillings on two surfaces | 2.03 ± 1.46 | 1.67 ± 1.12 | <0.001 | 0.79 (0.71–0.88) | |
The number of teeth where two surface amalgam fillings were performed | 0.32 ± 0.84 | 0.47 ± 0.86 | <0.001 | 1.17 (1.10–1.24) | |
The number of teeth that required three and more amalgam fillings on surfaces | 0.11 ± 0.45 | 0.14 ± 0.47 | <0.035 | 1.14 (1.01–1.28) | |
The number of teeth where three and more surface amalgam fillings were performed | 0.07 ± 0.32 | 0.13 ± 0.40 | <0.001 | 1.44 (1.27–1.64) | |
The number of teeth that required four or more surfaces amalgam fillings | 0.01 ± 0.11 | 0.02 ± 0.15 | <0.025 | 1.72 (1.22–2.43) | |
The number of teeth where four or more surfaces amalgam fillings were performed | 0.03 ± 0.18 | 0.07 ± 0.31 | <0.001 | 1.91 (1.58–2.31) | |
The number of teeth that required resin-based composite fillings on one to four surfaces, anterior | 0.24 ± 0.79 | 0.30 ± 0.93 | <0.057 | 1.08 (1.01–1.15) | |
The number of teeth where resin-based composite fillings were performed on one to four surfaces, anterior | 0.25 ± 0.86 | 0.45 ± 2.14 | <0.005 | 1.11 (1.07–1.15) | |
Total number of teeth that required fillings | 1.55 ± 2.41 | 1.42 ± 2.13 | <0.048 | 0.97 (0.94–1.00) | |
Total number of teeth where fillings were performed | 1.00 ± 1.96 | 1.49 ± 2.81 | <0.001 | 1.08 (1.06–1.10) | |
Total number of teeth that required endodontic treatment | 0.08 ± 0.38 | 0.13 ± 0.41 | 0.001 | 1.21 (1.09–1.34) | |
Total number of teeth where endodontic treatment was performed | 0.07 ± 0.33 | 0.18 ± 0.48 | <0.001 | 1.53 (1.39–1.69) | |
The number of teeth that required prefabricated (direct, post and core) | 0.10 ± 0.42 | 0.15 ± 0.43 | 0.002 | 1.20 (1.08–1.34) | |
The number of teeth on which prefabricated (direct, post and core) was performed | 0.10 ± 0.39 | 0.25 ± 0.61 | <0.001 | 1.44 (1.341. 55) | |
The number of teeth that required crowns | 0.15 ± 0.57 | 0.26 ± 0.70 | <0.001 | 1.22 (1.14–1.30) | |
The number of teeth where a crown was performed | 0.05 ± 0.53 | 0.34 ± 1.40 | <0.001 | 1.21 (1.16–1.25) | |
The number of teeth that required extractions | 0.14 ± 0.51 | 0.22 ± 0.71 | 0.001 | 1.23 (1.13–1.34) | |
Total number of teeth where extractions were performed | 0.10 ± 0.42 | 0.23 ± 0.79 | <0.001 | 1.27 (1.19–1.36) | |
Missing teeth | 0.57 ± 1.28 | 1.30 ± 1.67 | <0.001 | 1.15 (1.12–1.18) |
Parameter | Multivariate Logistic Regression Analysis | Linear Regression Analysis Collinearity Statistics | |||||
---|---|---|---|---|---|---|---|
B | Std. Error | p Value | OR (95% CI) | ||||
Tolerance | VIF | ||||||
(Intercept) | 7.19 | 0.98 | <0.001 | 0.001 (0.000–0.005) | |||
Age | 0.07 | 0.008 | <0.001 | 1.08 (1.06–1.09) | 0.448 | 2.234 | |
Sex: men vs. women | 1.36 | 0.27 | <0.001 | 3.91 (2.29–6.66) | 0.934 | 1.071 | |
Locality of residence (reference: rural) | urban Jewish | −0.24 | 0.56 | 0.667 | 0.78 (0.26–2.35) | 0.998 | 1.012 |
Urban non-Jewish | −0.69 | 0.58 | 0.233 | 0.49 (0.16–1.56) | 0.979 | 1.021 | |
Socioeconomic status (SES) (reference: low SES) | High | 0.12 | 0.25 | 0.619 | 1.13 (0.68–1.87) | 0.948 | 1.055 |
Medium | 0.32 | 0.24 | 0.183 | 1.39 (0.85–2.25) | 0.944 | 1.059 | |
Birth country (reference native Israelis) | Western Europe | 0.19 | 0.16 | 0.254 | 1.21 (0.87–1.671 | 0.983 | 1.017 |
Eastern Europe | −0.11 | 0.60 | 0.856 | 0.89 (0.27–2.93) | 0.979 | 1.022 | |
Asia | −0.45 | 0.56 | 0.417 | 0.63 (0.21–1.90) | 0.995 | 1.005 | |
Ethiopia | 0.07 | 0.60 | 0.897 | 1.08 (0.33–3.54) | 0.984 | 1.017 | |
Africa | 0.42 | 0.48 | 0.382 | 1.52 (0.59–3.94) | 0.995 | 1.005 | |
North America | 0.08 | 0.60 | 0.883 | 1.09 (0.33–3.55) | 0.987 | 1.013 | |
South America | 0.02 | 0.61 | 0.969 | 1.02 (0.31–3.39) | 0.997 | 1.003 | |
Smoking | 0.15 | 0.11 | 0.183 | 1.16 (0.93–1.45) | 0.749 | 1.334 | |
Teeth brushing once a day or more | 0.05 | 0.13 | 0.696 | 1.05 (0.81–1.36) | 0.694 | 1.441 | |
Consumption of a cariogenic diet | 0.03 | 0.16 | 0.830 | 1.03 (0.75–1.43) | 0.587 | 1.702 | |
Sweetened beverages | −0.23 | 0.16 | 0.145 | 0.79 (0.57–1.08) | 0.576 | 1.736 | |
Diabetes type 2 | 1.14 | 0.18 | <0.001 | 3.14 (2.21–4.46) | 0.917 | 1.090 | |
Impaired glucose tolerance (IGT) | 0.51 | 0.42 | 0.224 | 1.67 (0.73–3.85) | 0.963 | 1.038 | |
Hypertension | 0.51 | 0.12 | <0.001 | 1.67 (1.30–2.14) | 0.901 | 1.109 | |
Hyperlipidemia | 1.31 | 0.15 | <0.001 | 3.69 (2.75–4.95) | 0.546 | 1.832 | |
BMI | 0.14 | 0.01 | <0.001 | 1.15 (1.13–1.18) | 0.840 | 1.190 | |
Cardiovascular disease | 0.02 | 0.14 | 0.901 | 1.02 (0.76–1.36) | 0.920 | 1.086 | |
Obstructive sleep apnea (OSA) | −0.39 | 0.30 | 0.185 | 0.67 (0.37–1.21) | 0.972 | 1.029 | |
Periodontitis | 0.35 | 0.14 | 0.017 | 1.42 (1.06–1.89) | 0.959 | 1.043 | |
Missing teeth | −0.02 | 0.03 | 0.513 | 0.97 (0.91–1.04) | 0.768 | 1.302 | |
Total number of teeth that required endodontic treatment | −0.04 | 0.11 | 0.740 | 0.96 (0.76–1.21) | 0.810 | 1.235 | |
The number of teeth that required regular extraction | −0.11 | 0.07 | 0.149 | 0.89 (0.77–1.04) | 0.949 | 1.053 | |
The number of teeth that required a crown | −0.006 | 0.05 | 0.924 | 0.99 (0.88–1.11) | 0.822 | 1.216 | |
Presence of oral soft tissue disease | 0.03 | 0.19 | 0.873 | 1.03 (0.71–1.50) | 0.854 | 1.123 |
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Ram, D.; Wilensky, A.; Zur, D.; Almoznino, G. The Triangle of Nonalcoholic Fatty Liver Disease, Metabolic Dysfunction, and Periodontitis: Analysis of the Dental, Oral, Medical and Epidemiological (DOME) Records-Based Nationwide Research. Metabolites 2022, 12, 1212. https://doi.org/10.3390/metabo12121212
Ram D, Wilensky A, Zur D, Almoznino G. The Triangle of Nonalcoholic Fatty Liver Disease, Metabolic Dysfunction, and Periodontitis: Analysis of the Dental, Oral, Medical and Epidemiological (DOME) Records-Based Nationwide Research. Metabolites. 2022; 12(12):1212. https://doi.org/10.3390/metabo12121212
Chicago/Turabian StyleRam, Doron, Asaf Wilensky, Dorit Zur, and Galit Almoznino. 2022. "The Triangle of Nonalcoholic Fatty Liver Disease, Metabolic Dysfunction, and Periodontitis: Analysis of the Dental, Oral, Medical and Epidemiological (DOME) Records-Based Nationwide Research" Metabolites 12, no. 12: 1212. https://doi.org/10.3390/metabo12121212