The Influence of Diet and Physical Activity on Periodontal Health: A Narrative Review
Abstract
:1. Introduction
2. Dietary Factors Affecting Periodontal Health
2.1. Micronutrients and the Periodontium
2.1.1. Vitamin C and Collagen Synthesis
Biological Rationale
Scientific Evidence
2.1.2. Vitamin D and Inflammatory Modulation
Biological Rationale
Scientific Evidence
2.1.3. Omega-3 Fatty Acids and Inflammation
Biological Rationale
Scientific Evidence
2.1.4. Minerals and Periodontitis
Biological Rationale
Scientific Evidence
3. Relationship Between Dietary Patterns and Periodontitis
3.1. Western Diet
3.2. Mediterranean Diet
3.3. Plant-Based Diet
3.4. Ketogenic Diet
3.5. Stone-Age Diet
4. The Oral–Gut Microbiota Axis: A Bidirectional Interface Influenced by Diet
4.1. Oral Microbiota as a Determinant of Gut Microbial Composition
4.2. Dietary Modulation of the Oral–Gut Microbiota Axis
- (a)
- Transient Colonization: Delivering viable bacteria (e.g., Lactobacillus, Leuconostoc, Pediococcus, Bifidobacterium) that temporarily interact with the host gut ecosystem.
- (b)
- Substrate Liberation: Enhancing availability of microbiota-accessible carbohydrates (MACs) and producing SCFAs through fermentation.
- (c)
- Immunomodulation: Influencing TLR signaling, NF-κB inhibition, and regulatory T-cell activation via bioactive metabolites such as exopolysaccharides and peptides.
5. Obesity, Physical Activity, and Periodontal Health
5.1. Obesity and Periodontitis
5.2. Relationship Between NSPT and Obesity
5.3. Exercise and Systemic Inflammation: Biological Implications
5.4. Physical Activity and Periodontal Health
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
Abbreviations
PA | Physical activity |
ROS | Reactive oxygen species |
SVCT2 | Sodium-Dependent Vitamin C Transporter 2 |
DHA | Dehydroascorbate |
NF-κB | Nuclear Factor kappa-light-chain-enhancer of activated B cells |
CAL | Clinical attachment loss |
CRP | C-reactive protein |
TOSC | Total oxyradical scavenging capacity |
GCF | Gingival crevicular fluid |
8-OHdG | 8-hydroxy-2’-deoxyguanosine |
MMP | Matrix Metalloproteinase |
ABL | Alveolar bone loss |
TNF-α | Tumor Necrosis Factor-alpha |
25(OH)D | 25-hydroxyvitamin D |
1,25(OH)2D3 | 1,25-dihydroxyvitamin D₃ |
NSPT | Non-surgical periodontal therapy |
SRP | Scaling and Root Planing |
PPD | Probing depth |
BoP | Bleeding on probing |
VDR | Vitamin D receptor |
TLR | Toll-like receptor |
SNP | Single nucleotide polymorphism |
DBP | Vitamin D-binding protein |
MAF | Macrophage activating factor |
PUFAs | Polyunsaturated fatty acids |
EPA | Eicosapentaenoic acid |
DHA | Docosahexaenoic acid |
SPMs | Specialized pro-resolving mediators |
GI | Gingival Index |
BI | Bleeding Index |
MD | Mediterranean diet |
Zn2⁺ | Zinc Ion |
SOD | Superoxide dismutase |
OR | Odds ratio |
CI | Confidence interval |
WD | Western diet |
BW | Body weight |
BMI | Body Mass Index |
WC | Waist circumference |
TMAO | Trimethylamine N-oxide |
TC | Total cholesterol |
HDL | High-Density Lipoprotein |
oxLDL | Oxidized Low-Density Lipoprotein |
LDL | Low-Density Lipoprotein |
SFAs | Saturated fatty acids |
PI | Plaque Index |
PISA | Periodontal Inflamed Surface Area |
PBD | Plant-based diet |
hPDI | Healthful Plant-Based Diet Index |
uPDI | Unhealthful Plant-Based Diet Index |
KD | Ketogenic diet |
SD | Stone-age diet |
LPS | Lipopolysaccharide |
SCFAs | Short-Chain Fatty Acids |
MACs | Microbiota-accessible carbohydrates |
GABA | Gamma-aminobutyric acid |
WHR | Waist-to-hip ratio |
MCP-1 | Monocyte Chemoattractant Protein-1 |
G-CSF | Granulocyte colony-stimulating factor |
IL-1ra | Interleukin-1 Receptor Antagonist |
LPO | Lipid peroxidation |
References
- Trindade, D.; Carvalho, R.; Machado, V.; Chambrone, L.; Mendes, J.J.; Botelho, J. Prevalence of periodontitis in dentate people between 2011 and 2020: A systematic review and meta-analysis of epidemiological studies. J. Clin. Periodontol. 2023, 50, 604–626. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Wang, Y.; Fan, L.; Yu, Y. The Burden of Severe Periodontitis in China from 1990 to 2021, with Projections to 2050: A Comprehensive Analysis from the Global Burden of Disease Study 2021. Int. Dent. J. 2025, 75, 32–44. [Google Scholar] [CrossRef]
- 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]
- Scannapieco, F.A.; Dongari-Bagtzoglou, A. Dysbiosis revisited: Understanding the role of the oral microbiome in the pathogenesis of gingivitis and periodontitis: A critical assessment. J. Periodontol. 2021, 92, 1071–1078. [Google Scholar] [CrossRef] [PubMed]
- El Sayed, N.; Rahim-Wöstefeld, S.; Stocker, F.; Behnisch, R.; Eickholz, P.; Pretzl, B. The 2018 classification of periodontal diseases: Its predictive value for tooth loss. J. Periodontol. 2022, 93, 560–569. [Google Scholar] [CrossRef]
- Bianchi, S.; Mancini, L.; Torge, D.; Cristiano, L.; Mattei, A.; Varvara, G.; Macchiarelli, G.; Marchetti, E.; Bernardi, S. Bio-Morphological Reaction of Human Periodontal Ligament Fibroblasts to Different Types of Dentinal Derivates: In Vitro Study. Int. J. Mol. Sci. 2021, 22, 8681. [Google Scholar] [CrossRef] [PubMed]
- Shi, X.; Zhu, P.; Du, M.; Deng, K.; Li, P.; Sáenz-Ravello, G.; Xu, S.; Li, A. Dietary patterns and periodontitis: A systematic review. J. Periodontal Res. 2024. [Google Scholar] [CrossRef]
- Cao, R.; Qiu, P.; Zhou, Y.; Dong, B.; Han, Y.; Fan, Z. The underlying relationship between exercise and the prevalence of periodontitis: A systematic review and meta-analysis. BMC Sports Sci. Med. Rehabil. 2023, 15, 161. [Google Scholar] [CrossRef]
- Nishikimi, M.; Yagi, K. Molecular basis for the deficiency in humans of gulonolactone oxidase, a key enzyme for ascorbic acid biosynthesis. Am. J. Clin. Nutr. 1991, 54 (Suppl. S6), 1203S–1208S. [Google Scholar] [CrossRef]
- Ohta, Y.; Nishikimi, M. Random nucleotide substitutions in primate nonfunctional gene for L-gulono-γ-lactone oxidase, the missing enzyme in L-ascorbic acid biosynthesis. Biochim. Biophys. Acta Gen. Subj. 1999, 1472, 408–411. [Google Scholar] [CrossRef]
- Nishikimi, M.; Koshizaka, T.; Ozawa, T.; Yagi, K. Occurrence in humans and guinea pigs of the gene related to their missing enzyme l-gulono-γ-lactone oxidase. Arch. Biochem. Biophys. 1988, 267, 842–846. [Google Scholar] [CrossRef] [PubMed]
- Murererehe, J.; Uwitonze, A.M.; Nikuze, P.; Patel, J.; Razzaque, M.S. Beneficial Effects of Vitamin C in Maintaining Optimal Oral Health. Front. Nutr. 2022, 8, 805809. [Google Scholar] [CrossRef] [PubMed]
- Buzatu, R.; Luca, M.M.; Bumbu, B.A. Does Vitamin C Supplementation Provide a Protective Effect in Periodontal Health? A Systematic Review and Meta-Analysis. Int. J. Mol. Sci. 2024, 25, 8598. [Google Scholar] [CrossRef]
- Carr, A.C.; Shaw, G.M.; Fowler, A.A.; Natarajan, R. Ascorbate-dependent vasopressor synthesis: A rationale for vitamin C administration in severe sepsis and septic shock? Crit. Care 2015, 19, 418. [Google Scholar] [CrossRef]
- Kaźmierczak-Barańska, J.; Boguszewska, K.; Adamus-Grabicka, A.; Karwowski, B.T. Two Faces of Vitamin C-Antioxidative and Pro-Oxidative Agent. Nutrients 2020, 12, 1501. [Google Scholar] [CrossRef]
- Carr, A.C.; Maggini, S. Vitamin C and Immune Function. Nutrients 2017, 9, 1211. [Google Scholar] [CrossRef] [PubMed]
- Sharma, P.; Raghavan, S.A.V.; Saini, R.; Dikshit, M. Ascorbate-mediated enhancement of reactive oxygen species generation from polymorphonuclear leukocytes: Modulatory effect of nitric oxide. J. Leukoc. Biol. 2004, 75, 1070–1078. [Google Scholar] [CrossRef] [PubMed]
- Vissers, M.C.M.; Wilkie, R.P. Ascorbate deficiency results in impaired neutrophil apoptosis and clearance and is associated with up-regulation of hypoxia-inducible factor 1α. J. Leukoc. Biol. 2007, 81, 1236–1244. [Google Scholar] [CrossRef]
- Touyz, L.Z. Oral scurvy and periodontal disease. J. Can. Dent. Assoc. 1997, 63, 837–845. [Google Scholar]
- Pflipsen, M.; Zenchenko, Y. Nutrition for oral health and oral manifestations of poor nutrition and unhealthy habits. Gen. Dent. 2017, 65, 36–43. [Google Scholar]
- Alqanatish, J.T.; Alqahtani, F.; Alsewairi, W.M.; Al-kenaizan, S. Childhood scurvy: An unusual cause of refusal to walk in a child. Pediatr. Rheumatol. 2015, 13, 23. [Google Scholar] [CrossRef] [PubMed]
- Weinstein, M.; Babyn, P.; Zlotkin, S. An orange a day keeps the doctor away: Scurvy in the year 2000. Pediatrics 2001, 108, e55. [Google Scholar] [CrossRef]
- Trapani, S.; Rubino, C.; Indolfi, G.; Lionetti, P. A Narrative Review on Pediatric Scurvy: The Last Twenty Years. Nutrients 2022, 14, 684. [Google Scholar] [CrossRef] [PubMed]
- Tada, A.; Miura, H. The Relationship between Vitamin C and Periodontal Diseases: A Systematic Review. Int. J. Environ. Res. Public Health 2019, 16, 2472. [Google Scholar] [CrossRef] [PubMed]
- Ustianowski, Ł.; Ustianowska, K.; Gurazda, K.; Rusiński, M.; Ostrowski, P.; Pawlik, A. The Role of Vitamin C and Vitamin D in the Pathogenesis and Therapy of Periodontitis-Narrative Review. Int. J. Mol. Sci. 2023, 24, 6774. [Google Scholar] [CrossRef]
- Munday, M.R.; Rodricks, R.; Fitzpatrick, M.; Flood, V.M.; Gunton, J.E. A Pilot Study Examining Vitamin C Levels in Periodontal Patients. Nutrients 2020, 12, 225. [Google Scholar] [CrossRef]
- Li, W.; Song, J.; Chen, Z. The association between dietary vitamin C intake and periodontitis: Result from the NHANES (2009-2014). BMC Oral Health 2022, 22, 390. [Google Scholar] [CrossRef]
- Vogel, R.I.; Lamster, I.B.; Wechsler, S.A.; Macedo, B.; Hartley, L.J.; Macedo, J.A. The effects of megadoses of ascorbic acid on PMN chemotaxis and experimental gingivitis. J. Periodontol. 1986, 57, 472–479. [Google Scholar] [CrossRef]
- Schifferle, R.E. Periodontal disease and nutrition: Separating the evidence from current fads. Periodontology 2000 2009, 50, 78–89. [Google Scholar] [CrossRef]
- Eberhardt, M.V.; Lee, C.Y.; Liu, R.H. Antioxidant activity of fresh apples. Nature 2000, 405, 903–904. [Google Scholar] [CrossRef]
- Meyle, J.; Kapitza, K. Assay of ascorbic acid in human crevicular fluid from clinically healthy gingival sites by high-performance liquid chromatography. Arch. Oral Biol. 1990, 35, 319–323. [Google Scholar] [CrossRef] [PubMed]
- Woolfk, S.N.; Kenney, E.B.; Hume, W.R.; Carranza, F.A. Relationship of ascorbic acid levels of blood and gingival tissue with response to periodontal therapy. J. Clin. Periodontol. 1984, 11, 159–165. [Google Scholar] [CrossRef] [PubMed]
- Aytekin, Z.; Toraman, A.; Karaçam, K. Investigation of Effects of Local Vitamin C Application on Inflammatory Response and Periodontal Tissue Destruction in Rat Periodontitis Model. Selcuk. Dent. J. 2023, 10, 371–376. [Google Scholar] [CrossRef]
- Sulaiman, A.E.A.; Shehadeh, R.M.H. Assessment of total antioxidant capacity and the use of vitamin C in the treatment of non-smokers with chronic periodontitis. J. Periodontol. 2010, 81, 1547–1554. [Google Scholar] [CrossRef]
- Yussif, N.M.; Aziz, M.A.A.; Rahman, A.R.A. Evaluation of the Anti-Inflammatory Effect of Locally Delivered Vitamin C in the Treatment of Persistent Gingival Inflammation: Clinical and Histopathological Study. J. Nutr. Metab. 2016, 2016, 2978741. [Google Scholar] [CrossRef]
- Greenstein, G. Local drug delivery in the treatment of periodontal diseases: Assessing the clinical significance of the results. J. Periodontol. 2006, 77, 565–578. [Google Scholar] [CrossRef]
- Sassi, F.; Tamone, C.; D’amelio, P. Vitamin D: Nutrient, Hormone, and Immunomodulator. Nutrients 2018, 10, 1656. [Google Scholar] [CrossRef]
- Garand, M.; Toufiq, M.; Singh, P.; Huang, S.S.Y.; Tomei, S.; Mathew, R.; Mattei, V.; Al Wakeel, M.; Sharif, E.; Al Khodor, S. Immunomodulatory Effects of Vitamin D Supplementation in a Deficient Population. Int. J. Mol. Sci. 2021, 22, 5041. [Google Scholar] [CrossRef]
- Khammissa, R.A.G.; Ballyram, R.; Jadwat, Y.; Fourie, J.; Lemmer, J.; Feller, L. Vitamin D Deficiency as It Relates to Oral Immunity and Chronic Periodontitis. Int. J. Dent. 2018, 2018, 7315797. [Google Scholar] [CrossRef]
- Liang, F.; Zhou, Y.; Zhang, Z.; Zhang, Z.; Shen, J. Association of vitamin D in individuals with periodontitis: An updated systematic review and meta-analysis. BMC Oral Health 2023, 23, 387. [Google Scholar] [CrossRef]
- Pinto, J.P.N.S.; Goergen, J.; Muniz, F.W.M.G.; Haas, A.N. Vitamin D levels and risk for periodontal disease: A systematic review. J. Periodontal Res. 2018, 53, 298–305. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Dai, B.; Chuai, Y.; Hu, M.; Zhang, H. Associations between vitamin D levels and periodontal attachment loss. Clin. Oral Investig. 2023, 27, 4727–4733. [Google Scholar] [CrossRef]
- Machado, V.; Lobo, S.; Proença, L.; Mendes, J.J.; Botelho, J. Vitamin D and Periodontitis: A Systematic Review and Meta-Analysis. Nutrients 2020, 12, 2177. [Google Scholar] [CrossRef]
- Lu, E.M.C. The role of vitamin D in periodontal health and disease. J. Periodontal Res. 2023, 58, 213–224. [Google Scholar] [CrossRef]
- Sone, T.; Marx, S.J.; Liberman, U.A.; Pike, J.W. A unique point mutation in the human vitamin D receptor chromosomal gene confers hereditary resistance to 1,25-dihydroxyvitamin D3. Mol. Endocrinol. 1990, 4, 623–631. [Google Scholar] [CrossRef] [PubMed]
- Meghil, M.M.; Hutchens, L.; Raed, A.; Multani, N.A.; Rajendran, M.; Zhu, H.; Looney, S.; Elashiry, M.; Arce, R.M.; Peacock, M.E.; et al. The influence of vitamin D supplementation on local and systemic inflammatory markers in periodontitis patients: A pilot study. Oral Dis. 2019, 25, 1403–1413. [Google Scholar] [CrossRef]
- Hennig, B.J.W.; Parkhill, J.M.; Chapple, L.L.C.; Heasman, P.A.; Taylor, J.J. Association of a vitamin D receptor gene polymorphism with localized early-onset periodontal diseases. J. Periodontol. 1999, 70, 1032–1038. [Google Scholar] [CrossRef] [PubMed]
- Laine, M.L.; Loos, B.G.; Crielaard, W. Gene polymorphisms in chronic periodontitis. Int. J. Dent. 2010, 2010, 324719. [Google Scholar] [CrossRef]
- Nibali, L.; Parkar, M.; D’Aiuto, F.; Suvan, J.E.; Brett, P.M.; Griffiths, G.S.; Rosin, M.; Schwahn, C.; Tonetti, M.S. Vitamin D receptor polymorphism (-1056 Taq-I) interacts with smoking for the presence and progression of periodontitis. J. Clin. Periodontol. 2008, 35, 561–567. [Google Scholar] [CrossRef]
- Wan, Q.S.; Li, L.; Yang, S.K.; Liu, Z.L.; Song, N. Role of Vitamin D Receptor Gene Polymorphisms on the Susceptibility to Periodontitis: A Meta-Analysis of a Controversial Issue. Genet. Test Mol. Biomark. 2019, 23, 618–633. [Google Scholar] [CrossRef]
- Yu, X.; Zong, X.; Pan, Y. Associations between vitamin D receptor genetic variants and periodontitis: A meta-analysis. Acta Odontol. Scand. 2019, 77, 484–494. [Google Scholar] [CrossRef]
- Yıldırım, Y.A.; Ozturk, A.; Doğruel, F.; Saraçoğlu, H.; Yazıcı, C. Serum vitamin D concentration is inversely associated with matrix metalloproteinase-9 level in periodontal diseases. J. Periodontol. 2024. [Google Scholar] [CrossRef]
- Li, W.; Zhu, W.; Hou, J.; Meng, H. Vitamin D-binding protein expression in healthy tooth and periodontium: An experimental study both in monkeys in vivo and in humans in vitro. J. Periodontal Res. 2017, 52, 755–760. [Google Scholar] [CrossRef] [PubMed]
- Chakravarthy, Y.; Mishra, A.; Krishnan, P.; Pathakota, K.; Vijaya, V.; Kamatham, S. Evaluation of serum and gingival crevicular fluid levels of Vitamin D binding protein in subjects with clinically healthy periodontium and chronic periodontitis: A clinico bio-chemical study. Indian J. Dent. Res. 2022, 33, 301–306. [Google Scholar] [CrossRef]
- Simopoulos, A.P. The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp. Biol. Med. 2008, 233, 674–688. [Google Scholar] [CrossRef] [PubMed]
- Calder, P.C. n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am. J. Clin. Nutr. 2006, 83 (Suppl. S6), 1505S–1519S. [Google Scholar] [CrossRef] [PubMed]
- Serhan, C.N.; Chiang, N.; Van Dyke, T.E. Resolving inflammation: Dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 2008, 8, 349–361. [Google Scholar] [CrossRef]
- Bannenberg, G.; Serhan, C.N. Specialized pro-resolving lipid mediators in the inflammatory response: An update. Biochim. Biophys. Acta 2010, 1801, 1260–1273. [Google Scholar] [CrossRef]
- Kiecolt-Glaser, J.K.; Belury, M.A.; Andridge, R.; Malarkey, W.B.; Glaser, R. Omega-3 supplementation lowers inflammation and anxiety in medical students: A randomized controlled trial. Brain Behav. Immun. 2011, 25, 1725–1734. [Google Scholar] [CrossRef]
- Nälsén, C.; Vessby, B.; Berglund, L.; Uusitupa, M.; Hermansen, K.; Riccardi, G.; Rivellese, A.; Storlien, L.; Erkkilä, A.; Ylä-Herttuala, S.; et al. Dietary (n-3) fatty acids reduce plasma F2-isoprostanes but not prostaglandin F2alpha in healthy humans. J. Nutr. 2006, 136, 1222–1228. [Google Scholar] [CrossRef]
- Mori, T.A.; Bao, D.Q.; Burke, V.; Puddey, I.B.; Beilin, L.J. Docosahexaenoic acid but not eicosapentaenoic acid lowers ambulatory blood pressure and heart rate in humans. Hypertension 1999, 34, 253–260. [Google Scholar] [CrossRef] [PubMed]
- Calder, P.C. Polyunsaturated fatty acids and inflammation. Biochem. Soc. Trans. 2005, 33 Pt 2, 423–427. [Google Scholar] [CrossRef] [PubMed]
- Miroult, C.; Lasserre, J.; Toma, S. Effects of Omega-3 as an adjuvant in the treatment of periodontal disease: A systematic review and meta-analysis. Clin. Exp. Dent. Res. 2023, 9, 545–556. [Google Scholar] [CrossRef] [PubMed]
- Chee, B.; Park, B.; Fitzsimmons, T.; Coates, A.M.; Bartold, P.M. Omega-3 fatty acids as an adjunct for periodontal therapy-a review. Clin. Oral Investig. 2016, 20, 879–894. [Google Scholar] [CrossRef]
- Deore, G.D.; Gurav, A.N.; Patil, R.; Shete, A.R.; NaikTari, R.S.; Inamdar, S.P. Omega 3 fatty acids as a host modulator in chronic periodontitis patients: A randomised, double-blind, palcebo-controlled, clinical trial. J. Periodontal Implant. Sci. 2014, 44, 25–32. [Google Scholar] [CrossRef]
- Bartha, V.; Exner, L.; Basrai, M.; Bischoff, S.C.; Schweikert, D.; Adolph, M.; Bruckner, T.; Grueninger, D.; Klein, D.; Meller, C. Changes in serum omega fatty acids on a Mediterranean diet intervention in patients with gingivitis: An exploratory study. J. Periodontal Res. 2022, 57, 1198–1209. [Google Scholar] [CrossRef]
- Van Ravensteijn, M.M.; Timmerman, M.F.; Brouwer, E.A.G.; Slot, D.E. The effect of omega-3 fatty acids on active periodontal therapy: A systematic review and meta-analysis. J. Clin. Periodontol. 2022, 49, 1024–1037. [Google Scholar] [CrossRef]
- Rosenstein, E.D.; Kushner, L.J.; Kramer, N.; Kazandjian, G. Pilot study of dietary fatty acid supplementation in the treatment of adult periodontitis. Prostaglandins Leukot. Essent. Fat. Acids 2003, 68, 213–218. [Google Scholar] [CrossRef]
- Dommisch, H.; Kuzmanova, D.; Jönsson, D.; Grant, M.; Chapple, I. Effect of micronutrient malnutrition on periodontal disease and periodontal therapy. Periodontology 2000 2018, 78, 129–153. [Google Scholar] [CrossRef]
- Goh, H.J.; Lee, K.S.; Kim, T.H.; Lim, H.J.; Kim, K.S.; Yang, W.J.; Jo, J.K. K. Intravenous Iron Isomaltoside 1000 Reduces Postoperative Anemia in Patients Undergoing Elective Urologic Surgery and Those with Urosepsis. Drug Des. Dev. Ther. 2020, 14, 5679–5687. [Google Scholar] [CrossRef]
- Institute of Medicine (US); Panel on Micronutrients. Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc; The National Academies Press: Washington, DC, USA, 2001. [Google Scholar] [CrossRef]
- Adegboye, A.R.A.; Boucher, B.J.; Kongstad, J.; Fiehn, N.E.; Christensen, L.B.; Heitmann, B.L. Calcium, vitamin D, casein and whey protein intakes and periodontitis among Danish adults. Public Health Nutr. 2016, 19, 503–510. [Google Scholar] [CrossRef] [PubMed]
- Nishida, M.; Grossi, S.G.; Dunford, R.G.; Ho, A.W.; Trevisan, M.; Genco, R.J. Calcium and the risk for periodontal disease. J. Periodontol. 2000, 71, 1057–1066. [Google Scholar] [CrossRef]
- Cao, H.; Wang, M.; Duan, M.; Wang, S.; Zhang, H. Association of serum calcium level with periodontitis: A cross-sectional study from NHANES 2009-2014. Front. Nutr. 2025, 11, 1520639. [Google Scholar] [CrossRef]
- Meisel, P.; Schwahn, C.; Luedemann, J.; John, U.; Kroemer, H.K.; Kocher, T. Magnesium deficiency is associated with periodontal disease. J. Dent. Res. 2005, 84, 937–941. [Google Scholar] [CrossRef] [PubMed]
- Meisel, P.; Pink, C.; Nauck, M.; Jablonowski, L.; Voelzke, H.; Kocher, T. Magnesium/calcium ratio in serum predicts periodontitis and tooth loss in a 5-year follow-up. JDR Clin. Trans. Res. 2016, 1, 266–274. [Google Scholar] [CrossRef]
- Sundaram, G.; Ramakrishnan, T.; Parthasarathy, H.; Moses, J.; Lalitha, T. Evaluation of Micronutrient (Zinc, Magnesium, and Copper) Levels in Serum and Glycemic Status after Nonsurgical Periodontal Therapy in Type 2 Diabetic Patients with Chronic Periodontitis. Contemp. Clin. Dent. 2017, 8, 26–32. [Google Scholar] [CrossRef] [PubMed]
- Yamamoto, T.; Tsuneishi, M.; Furuta, M.; Ekuni, D.; Morita, M.; Hirata, Y. Relationship Between Decrease of Erythrocyte Count and Progression of Periodontal Disease in a Rural Japanese Population. J. Periodontol. 2011, 82, 106–113. [Google Scholar] [CrossRef]
- Łobacz, M.; Mertowska, P.; Mertowski, S.; Kozińska, A.; Kwaśniewski, W.; Kos, M.; Grywalska, E.; Rahnama-Hezavah, M. The Bloody Crossroads: Interactions between Periodontitis and Hematologic Diseases. Int. J. Mol. Sci. 2024, 25, 6115. [Google Scholar] [CrossRef]
- Agarwal, N.; Kumar, V.S.C.; Gujjari, S.A. Effect of periodontal therapy on hemoglobin and erythrocyte levels in chronic generalized periodontitis patients: An interventional study. J. Indian Soc. Periodontol. 2009, 13, 6. [Google Scholar] [CrossRef]
- Chakraborty, S.; Tewari, S.; Sharma, R.K.; Narula, S.C.; Ghalaut, P.S.; Ghalaut, V. Impact of iron deficiency anemia on chronic periodontitis and superoxide dismutase activity: A cross-sectional study. J. Periodontal Implant. Sci. 2014, 44, 57–64. [Google Scholar] [CrossRef]
- Pushparani, D.S.; Nirmala, S. High Level of Serum Calcium and Iron Influences the Risk of Type 2 Diabetes Mellitus with Periodontitis. J. Asian Sci. Res. 2014, 4, 70–82. [Google Scholar]
- Thomas, B.; Gautam, A.; Prasad, B.R.; Kumari, S. Evaluation of micronutrient (zinc, copper and iron) levels in periodontitis patients with and without diabetes mellitus type 2: A biochemical study. Indian J. Dent. Res. 2013, 24, 468–473. [Google Scholar] [CrossRef] [PubMed]
- Enhos, S.; Duran, I.; Erdem, S.; Buyukbas, S. Relationship between iron-deficiency anemia and periodontal status in female patients. J. Periodontol. 2009, 80, 1750–1755. [Google Scholar] [CrossRef]
- Lin, P.H.; Sermersheim, M.; Li, H.; Lee, P.H.U.; Steinberg, S.M.; Ma, J. Zinc in Wound Healing Modulation. Nutrients 2017, 10, 16. [Google Scholar] [CrossRef]
- O’Brien, K.O.; Zavaleta, N.; Caulfield, L.E.; Wen, J.; Abrams, S.A. Prenatal iron supplements impair zinc absorption in pregnant Peruvian women. J. Nutr. 2000, 130, 2251–2255. [Google Scholar] [CrossRef]
- Olivares, M.; Pizarro, F.; Ruz, M.; De Romaña, D.L. Acute inhibition of iron bioavailability by zinc: Studies in humans. Biometals 2012, 25, 657–664. [Google Scholar] [CrossRef]
- Gröber, U. Micronutrients: Metabolic Tuning-Prevention-Therapy; MedPharm Scientific Publisher: Stuttgart, Germany, 2009; p. 478. Available online: https://search.worldcat.org/title/276777395 (accessed on 11 March 2025).
- Gröber, U.; Schmidt, J.; Kisters, K. Magnesium in Prevention and Therapy. Nutrients 2015, 7, 8199–8226. [Google Scholar] [CrossRef] [PubMed]
- Zhou, F.; Yao, S.; Shan, F.; Zhou, Y. Serum zinc and periodontitis in non-diabetic smoking and non-smoking adults: NHANES 2011–2014. Oral Dis. 2024, 30, 2592–2598. [Google Scholar] [CrossRef]
- Jeong, J.; Kim, H.S.; Lee, D.; Kim, K.; Kim, Y.H. Association between Four Dietary Patterns and the Risk of Periodontal Diseases: A Systematic Review and Meta-Analysis. Nutrients 2022, 14, 4362. [Google Scholar] [CrossRef]
- Graff, E.; Vedantam, S.; Parianos, M.; Khakoo, N.; Beiling, M.; Pearlman, M. Dietary Intake and Systemic Inflammation: Can We Use Food as Medicine? Curr. Nutr. Rep. 2023, 12, 247–254. [Google Scholar] [CrossRef]
- Bhupathiraju, S.N.; Tobias, D.K.; Malik, V.S.; Pan, A.; Hruby, A.; Manson, J.E.; Willett, W.C.; Hu, F.B. Glycemic index, glycemic load, and risk of type 2 diabetes: Results from 3 large US cohorts and an updated meta-analysis. Am. J. Clin. Nutr. 2014, 100, 218–232. [Google Scholar] [CrossRef] [PubMed]
- Atkinson, F.S.; Foster-Powell, K.; Brand-Miller, J.C. International tables of glycemic index and glycemic load values: 2008. Diabetes Care 2008, 31, 2281–2283. [Google Scholar] [CrossRef]
- Hosseini, Z.; Whiting, S.J.; Vatanparast, H. Current evidence on the association of the metabolic syndrome and dietary patterns in a global perspective. Nutr. Res. Rev. 2016, 29, 152–162. [Google Scholar] [CrossRef]
- Lopez-Garcia, E.; Schulze, M.B.; Fung, T.T.; Meigs, J.B.; Rifai, N.; Manson, J.E.; Hu, F.B. Major dietary patterns are related to plasma concentrations of markers of inflammation and endothelial dysfunction. Am. J. Clin. Nutr. 2004, 80, 1029–1035. [Google Scholar] [CrossRef] [PubMed]
- Hansson, G.K.; Hermansson, A. The immune system in atherosclerosis. Nat. Immunol. 2011, 12, 204–212. [Google Scholar] [CrossRef]
- Sheedy, F.J.; Grebe, A.; Rayner, K.J.; Kalantari, P.; Ramkhelawon, B.; Carpenter, S.B.; Becker, C.E.; Ediriweera, H.N.; Mullick, A.E.; Golenbock, D.T. CD36 coordinates NLRP3 inflammasome activation by facilitating intracellular nucleation of soluble ligands into particulate ligands in sterile inflammation. Nat. Immunol. 2013, 14, 812–820. [Google Scholar] [CrossRef]
- Lancaster, G.I.; Langley, K.G.; Berglund, N.A.; Kammoun, H.L.; Reibe, S.; Estevez, E.; Weir, J.; Mellett, N.A.; Pernes, G.; Conway, J.R.W. Evidence that TLR4 Is Not a Receptor for Saturated Fatty Acids but Mediates Lipid-Induced Inflammation by Reprogramming Macrophage Metabolism. Cell Metab. 2018, 27, 1096–1110.e5. [Google Scholar] [CrossRef]
- Koeth, R.A.; Lam-Galvez, B.R.; Kirsop, J.; Wang, Z.; Levison, B.S.; Gu, X.; Copeland, M.F.; Bartlett, D.; Cody, D.B.; Dai, H.J.; et al. l-Carnitine in omnivorous diets induces an atherogenic gut microbial pathway in humans. J. Clin. Investig. 2019, 129, 373–387. [Google Scholar] [CrossRef] [PubMed]
- Sansores-España, L.D.; Melgar-Rodríguez, S.; Olivares-Sagredo, K.; Cafferata, E.A.; Martínez-Aguilar, V.M.; Vernal, R.; Paula-Lima, A.C.; Díaz-Zúñiga, J. Oral-Gut-Brain Axis in Experimental Models of Periodontitis: Associating Gut Dysbiosis with Neurodegenerative Diseases. Front. Aging 2021, 2, 781582. [Google Scholar] [CrossRef]
- Willett, W.C.; Sacks, F.; Trichopoulou, A.; Drescher, G.; Ferro-Luzzi, A.; Helsing, E.; Trichopoulos, D. Mediterranean diet pyramid: A cultural model for healthy eating. Am. J. Clin. Nutr. 1995, 61 (Suppl. S6), 1402S–1406S. [Google Scholar] [CrossRef]
- Dinu, M.; Pagliai, G.; Casini, A.; Sofi, F. Mediterranean diet and multiple health outcomes: An umbrella review of meta-analyses of observational studies and randomised trials. Eur. J. Clin. Nutr. 2018, 72, 30–43. [Google Scholar] [CrossRef]
- Bartha, V.; Exner, L.; Schweikert, D.; Woelber, J.P.; Vach, K.; Meyer, A.; Basrai, M.; Bischoff, S.C.; Meller, C.; Wolff, D. Effect of the Mediterranean diet on gingivitis: A randomized controlled trial. J. Clin. Periodontol. 2022, 49, 111–122. [Google Scholar] [CrossRef] [PubMed]
- Laiola, M.; De Filippis, F.; Vitaglione, P.; Ercolini, D. A Mediterranean Diet Intervention Reduces the Levels of Salivary Periodontopathogenic Bacteria in Overweight and Obese Subjects. Appl. Environ. Microbiol. 2020, 86, e00777-20. [Google Scholar] [CrossRef] [PubMed]
- Woelber, J.P.; Gärtner, M.; Breuninger, L.; Anderson, A.; König, D.; Hellwig, E.; Al-Ahmad, A.; Vach, K.; Dötsch, A.; Ratka-Krüger, P.; et al. The influence of an anti-inflammatory diet on gingivitis. A randomized controlled trial. J. Clin. Periodontol. 2019, 46, 481–490. [Google Scholar] [CrossRef] [PubMed]
- Marruganti, C.; Traversi, J.; Gaeta, C.; Cagidiaco, E.F.; Parrini, S.; Discepoli, N.; Grandini, S. Adherence to Mediterranean diet, physical activity level, and severity of periodontitis: Results from a university-based cross-sectional study. J. Periodontol. 2022, 93, 1218–1232. [Google Scholar] [CrossRef]
- Marruganti, C.; Baima, G.; Grandini, S.; Graziani, F.; Aimetti, M.; Sanz, M.; Romandini, M. Leisure-time and occupational physical activity demonstrate divergent associations with periodontitis: A population-based study. J. Clin. Periodontol. 2023, 50, 559–570. [Google Scholar] [CrossRef]
- Iwasaki, M.; Ennibi, O.K.; Bouziane, A.; Erraji, S.; Lakhdar, L.; Rhissassi, M.; Ansai, T.; Yoshida, A.; Miyazaki, H. Association between periodontitis and the Mediterranean diet in young Moroccan individuals. J. Periodontal Res. 2021, 56, 408–414. [Google Scholar] [CrossRef]
- Aalizadeh, Y.; Khamisi, N.; Asghari, P.; Safari, A.; Mottaghi, M.; Taherkhani, M.H.; Alemi, A.; Ghaderi, M.; Rahmanian, M. The Mediterranean diet and periodontitis: A systematic review and meta-analysis. Heliyon 2024, 10, e35633. [Google Scholar] [CrossRef]
- Plant-Based Diets and Their Impact on Health, Sustainability and the Environment: A Review of the Evidence: WHO European Office for the Prevention and Control of Noncommunicable Diseases. Available online: https://iris.who.int/handle/10665/349086 (accessed on 11 March 2025).
- Ruby, M.B. Vegetarianism. A blossoming field of study. Appetite 2012, 58, 141–150. [Google Scholar] [CrossRef]
- Wang, Y.B.; Page, A.J.; Gill, T.K.; Melaku, Y.A. The association between diet quality, plant-based diets, systemic inflammation, and mortality risk: Findings from NHANES. Eur. J. Nutr. 2023, 62, 2723–2737. [Google Scholar] [CrossRef]
- Azzola, L.G.; Fankhauser, N.; Srinivasan, M. Influence of the vegan, vegetarian and omnivore diet on the oral health status in adults: A systematic review and meta-analysis. Evid. Based Dent. 2023, 24, 43–44. [Google Scholar] [CrossRef] [PubMed]
- Li, A.; Qiu, B.; Goettsch, M.; Chen, Y.; Ge, S.; Xu, S.; Tjakkes, G.E. Association between the quality of plant-based diets and periodontitis in the U.S. general population. J. Clin. Periodontol. 2023, 50, 591–603. [Google Scholar] [CrossRef]
- Satija, A.; Bhupathiraju, S.N.; Spiegelman, D.; Chiuve, S.E.; Manson, J.E.; Willett, W.; Rexrode, K.M.; Rimm, E.B.; Hu, F.B. Healthful and Unhealthful Plant-Based Diets and the Risk of Coronary Heart Disease in U.S. Adults. J. Am. Coll. Cardiol. 2017, 70, 411–422. [Google Scholar] [CrossRef]
- Satija, A.; Bhupathiraju, S.N.; Rimm, E.B.; Spiegelman, D.; Chiuve, S.E.; Borgi, L.; Willett, W.C.; Manson, J.E.; Sun, Q.; Hu, F.B. Plant-Based Dietary Patterns and Incidence of Type 2 Diabetes in US Men and Women: Results from Three Prospective Cohort Studies. PLoS Med. 2016, 13, e1002039. [Google Scholar] [CrossRef]
- Woelber, J.P.; Reichenbächer, K.; Groß, T.; Vach, K.; Ratka-Krüger, P.; Bartha, V. Dietary and Nutraceutical Interventions as an Adjunct to Non-Surgical Periodontal Therapy—A Systematic Review. Nutrients 2023, 15, 1538. [Google Scholar] [CrossRef] [PubMed]
- Masood, W.; Annamaraju, P.; Suheb, M.Z.K.; Uppaluri, K.R. Ketogenic Diet. In StatPearls; StatPearls Publishing: Treasure Island, FL, USA, 2023. Available online: https://www.ncbi.nlm.nih.gov/books/NBK499830/ (accessed on 11 March 2025).
- Alarim, R.A.; Alasmre, F.A.; Alotaibi, H.A.; Alshehri, M.A.; Hussain, S.A. Effects of the Ketogenic Diet on Glycemic Control in Diabetic Patients: Meta-Analysis of Clinical Trials. Cureus 2020, 12, e10796. [Google Scholar] [CrossRef]
- Rajaram, S.S.; Nisha, S.; Ali, N.M.; Shashikumar, P.; Karmakar, S.; Pandey, V. Influence of a Low-Carbohydrate and Rich in Omega-3 Fatty Acids, Ascorbic Acid, Antioxidants, and Fiber Diet on Clinical Outcomes in Patients with Chronic Gingivitis: A Randomized Controlled Trial. J. Int. Soc. Prev. Community Dent. 2021, 11, 58–67. [Google Scholar] [CrossRef]
- Woelber, J.P.; Tennert, C.; Ernst, S.F.; Vach, K.; Ratka-Krüger, P.; Bertz, H.; Urbain, P. Effects of a Non-Energy-Restricted Ketogenic Diet on Clinical Oral Parameters. An Exploratory Pilot Trial. Nutrients 2021, 13, 4229. [Google Scholar] [CrossRef] [PubMed]
- Sharma, S.; Lamsal, M.; Sharma, S.K.; Niraula, S.R.; Koirala, B. Association of serum LDL cholesterol level with periodontitis among patients visiting a tertiary-care hospital. JNMA J. Nepal Med. Assoc. 2011, 51, 104–108. [Google Scholar] [CrossRef]
- Saxlin, T.; Suominen-Taipale, L.; Kattainen, A.; Marniemi, J.; Knuuttila, M.; Ylöstalo, P. Association between serum lipid levels and periodontal infection. J. Clin. Periodontol. 2008, 35, 1040–1047. [Google Scholar] [CrossRef]
- Sridhar, R.; Byakod, G.; Pudakalkatti, P.; Patil, R. A study to evaluate the relationship between periodontitis, cardiovascular disease and serum lipid levels. Int. J. Dent. Hyg. 2009, 7, 144–150. [Google Scholar] [CrossRef] [PubMed]
- Al Taher, H.; Salah, A.; Rammal, C.; Varma, S.R. Role of ketogenic diet and its effect on the periodontium. A scoping review. Front. Oral Health 2024, 5, 1364578. [Google Scholar] [CrossRef]
- Jönsson, T.; Granfeldt, Y.; Ahrén, B.; Branell, U.C.; Pålsson, G.; Hansson, A.; Söderström, M. Beneficial effects of a Paleolithic diet on cardiovascular risk factors in type 2 diabetes: A randomized cross-over pilot study. Cardiovasc. Diabetol. 2009, 8, 35. [Google Scholar] [CrossRef] [PubMed]
- Jamka, M.; Kulczyński, B.; Juruć, A.; Gramza-michałowska, A.; Stokes, C.S.; Walkowiak, J. The Effect of the Paleolithic Diet vs. Healthy Diets on Glucose and Insulin Homeostasis: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. J. Clin. Med. 2020, 9, 296. [Google Scholar] [CrossRef]
- Baumgartner, S.; Imfeld, T.; Schicht, O.; Rath, C.; Persson, R.E.; Persson, G.R. The impact of the stone age diet on gingival conditions in the absence of oral hygiene. J. Periodontol. 2009, 80, 759–768. [Google Scholar] [CrossRef]
- Lam, G.A.; Albarrak, H.; McColl, C.J.; Pizarro, A.; Sanaka, H.; Gomez-Nguyen, A.; Cominelli, F.; da Silva, A.P.B. The Oral-Gut Axis: Periodontal Diseases and Gastrointestinal Disorders. Inflamm. Bowel Dis. 2023, 29, 1153–1164. [Google Scholar] [CrossRef] [PubMed]
- Xu, A.A.; Hoffman, K.; Gurwara, S.; White, D.L.; Kanwal, F.; El-Serag, H.B.; Petrosino, J.F.; Jiao, L. Oral Health and the Altered Colonic Mucosa-Associated Gut Microbiota. Dig. Dis. Sci. 2021, 66, 2981–2991. [Google Scholar] [CrossRef]
- Kitamoto, S.; Nagao-Kitamoto, H.; Hein, R.; Schmidt, T.M.; Kamada, N. The Bacterial Connection between the Oral Cavity and the Gut Diseases. J. Dent. Res. 2020, 99, 1021–1029. [Google Scholar] [CrossRef]
- Bao, J.; Li, L.; Zhang, Y.; Wang, M.; Chen, F.; Ge, S.; Chen, B.; Yan, F. Periodontitis may induce gut microbiota dysbiosis via salivary microbiota. Int. J. Oral Sci. 2022, 14, 32. [Google Scholar] [CrossRef]
- Sohn, J.; Li, L.; Zhang, L.; Settem, R.P.; Honma, K.; Sharma, A.; Falkner, K.L.; Novak, J.M.; Sun, Y.; Kirkwood, K.L. Porphyromonas gingivalis indirectly elicits intestinal inflammation by altering the gut microbiota and disrupting epithelial barrier function through IL9-producing CD4+ T cells. Mol. Oral Microbiol. 2022, 37, 42–52. [Google Scholar] [CrossRef]
- Di Stefano, M.; Polizzi, A.; Santonocito, S.; Romano, A.; Lombardi, T.; Isola, G. Impact of Oral Microbiome in Periodontal Health and Periodontitis: A Critical Review on Prevention and Treatment. Int. J. Mol. Sci. 2022, 23, 5142. [Google Scholar] [CrossRef]
- Lu, J.; Zhang, S.; Huang, Y.; Qian, J.; Tan, B.; Qian, X.; Zhuang, J.; Zou, X.; Li, Y.; Yan, F. Periodontitis-related salivary microbiota aggravates Alzheimer’s disease via gut-brain axis crosstalk. Gut Microbes 2022, 14, 2126272. [Google Scholar] [CrossRef] [PubMed]
- Kamer, A.R.; Pushalkar, S.; Hamidi, B.; Janal, M.N.; Tang, V.; Annam, K.R.C.; Palomo, L.; Gulivindala, D.; Glodzik, L.; Saxena, D. Periodontal Inflammation and Dysbiosis Relate to Microbial Changes in the Gut. Microorganisms 2024, 12, 1225. [Google Scholar] [CrossRef] [PubMed]
- Baima, G.; Ferrocino, I.; Del Lupo, V.; Colonna, E.; Thumbigere-Math, V.; Caviglia, G.; Franciosa, I.; Mariani, G.; Romandini, M.; Ribaldone, D. Effect of Periodontitis and Periodontal Therapy on Oral and Gut Microbiota. J. Dent. Res. 2024, 103, 359–368. [Google Scholar] [CrossRef] [PubMed]
- Singh, R.K.; Chang, H.-W.; Yan, D.; Lee, K.M.; Ucmak, D.; Wong, K.; Abrouk, M.; Farahnik, B.; Nakamura, M.; Zhu, T.H.; et al. Influence of diet on the gut microbiome and implications for human health. J. Transl. Med. 2017, 15, 73. [Google Scholar] [CrossRef]
- Beam, A.; Clinger, E.; Hao, L. Effect of Diet and Dietary Components on the Composition of the Gut Microbiota. Nutrients 2021, 13, 2795. [Google Scholar] [CrossRef]
- Barber, T.M.; Kabisch, S.; Pfeiffer, A.F.H.; Weickert, M.O. The Effects of the Mediterranean Diet on Health and Gut Microbiota. Nutrients 2023, 15, 2150. [Google Scholar] [CrossRef]
- Merra, G.; Noce, A.; Marrone, G.; Cintoni, M.; Tarsitano, M.G.; Capacci, A.; De Lorenzo, A. Influence of Mediterranean Diet on Human Gut Microbiota. Nutrients 2021, 13, 7. [Google Scholar] [CrossRef]
- Leeuwendaal, N.K.; Stanton, C.; O’toole, P.W.; Beresford, T.P. Fermented Foods, Health and the Gut Microbiome. Nutrients 2022, 14, 1527. [Google Scholar] [CrossRef]
- Rungsri, P.; Akkarachaneeyakorn, N.; Wongsuwanlert, M.; Piwat, S.; Nantarakchaikul, P.; Teanpaisan, R. Effect of fermented milk containing Lactobacillus rhamnosus SD11 on oral microbiota of healthy volunteers: A randomized clinical trial. J. Dairy Sci. 2017, 100, 7780–7787. [Google Scholar] [CrossRef]
- Lim, J.-M.; Letchumanan, V.; Tan, L.T.-H.; Hong, K.-W.; Wong, S.-H.; Ab Mutalib, N.-S.; Lee, L.-H.; Law, J.W.-F. Ketogenic Diet: A Dietary Intervention via Gut Microbiome Modulation for the Treatment of Neurological and Nutritional Disorders (a Narrative Review). Nutrients 2022, 14, 3566. [Google Scholar] [CrossRef] [PubMed]
- Newell, C.; Bomhof, M.R.; Reimer, R.A.; Hittel, D.S.; Rho, J.M.; Shearer, J. Ketogenic diet modifies the gut microbiota in a murine model of autism spectrum disorder. Mol. Autism 2016, 7, 37. [Google Scholar] [CrossRef] [PubMed]
- Nishida, C.; Ko, G.T.; Kumanyika, S. Body fat distribution and noncommunicable diseases in populations: Overview of the 2008 WHO Expert Consultation on Waist Circumference and Waist-Hip Ratio. Eur. J. Clin. Nutr. 2010, 64, 2–5. [Google Scholar] [CrossRef]
- Suvan, J.; D’Aiuto, F.; Moles, D.R.; Petrie, A.; Donos, N. Association between overweight/obesity and periodontitis in adults. A systematic review. Obes. Rev. 2011, 12, e381–e404. [Google Scholar] [CrossRef]
- Brum, R.; Duarte, P.; Canto, G.L.; Flores-Mir, C.; Benfatti, C.M.; Porporatti, A.; Zimmermann, G. Biomarkers in biological fluids in adults with periodontitis and/or obesity: A meta-analysis. J. Indian Soc. Periodontol. 2020, 24, 191–215. [Google Scholar] [CrossRef] [PubMed]
- Fantuzzi, G. Adipose tissue, adipokines, and inflammation. J. Allergy Clin. Immunol. 2005, 115, 911–919. [Google Scholar] [CrossRef]
- Falagas, M.E.; Kompoti, M. Obesity and infection. Lancet Infect. Dis. 2006, 6, 438–446. [Google Scholar] [CrossRef]
- Virto, L.; Cano, P.; Jiménez-Ortega, V.; Fernández-Mateos, P.; González, J.; Esquifino, A.I.; Sanz, M. Obesity and periodontitis: An experimental study to evaluate periodontal and systemic effects of comorbidity. J. Periodontol. 2018, 89, 176–185. [Google Scholar] [CrossRef]
- Khan, S.; Barrington, G.; Bettiol, S.; Barnett, T.; Crocombe, L. Is overweight/obesity a risk factor for periodontitis in young adults and adolescents?: A systematic review. Obes. Rev. 2018, 19, 852–883. [Google Scholar] [CrossRef]
- Iwashita, M.; Hayashi, M.; Nishimura, Y.; Yamashita, A. The Link Between Periodontal Inflammation and Obesity. Curr. Oral Health Rep. 2021, 8, 76–83. [Google Scholar] [CrossRef]
- da Silva, F.G.; Pola, N.M.; Casarin, M.; Silva, C.F.E.; Muniz, F.W.M.G. Association between clinical measures of gingival inflammation and obesity in adults: Systematic review and meta-analyses. Clin. Oral Investig. 2021, 25, 4281–4298. [Google Scholar] [CrossRef] [PubMed]
- Linden, G.; Patterson, C.; Evans, A.; Kee, F. Obesity and periodontitis in 60-70-year-old men. J. Clin. Periodontol. 2007, 34, 461–466. [Google Scholar] [CrossRef]
- Ylöstalo, P.; Suominen-Taipale, L.; Reunanen, A.; Knuuttila, M. Association between body weight and periodontal infection. J. Clin. Periodontol. 2008, 35, 297–304. [Google Scholar] [CrossRef] [PubMed]
- Kongstad, J.; Hvidtfeldt, U.A.; Grønbæk, M.; Stoltze, K.; Holmstrup, P. The relationship between body mass index and periodontitis in the Copenhagen City Heart Study. J. Periodontol. 2009, 80, 1246–1253. [Google Scholar] [CrossRef] [PubMed]
- Pamuk, F.; Kantarci, A. Inflammation as a link between periodontal disease and obesity. Periodontology 2000 2022, 90, 186–196. [Google Scholar] [CrossRef]
- Pischon, N.; Heng, N.; Bernimoulin, J.P.; Kleber, B.M.; Willich, S.N.; Pischon, T. Obesity, inflammation, and periodontal disease. J. Dent. Res. 2007, 86, 400–409. [Google Scholar] [CrossRef]
- Azuma, T.; Tomofuji, T.; Endo, Y.; Tamaki, N.; Ekuni, D.; Irie, K.; Kasuyama, K.; Kato, T.; Morita, M. Effects of exercise training on gingival oxidative stress in obese rats. Arch. Oral Biol. 2011, 56, 768–774. [Google Scholar] [CrossRef] [PubMed]
- Park, H.S.; Nam, H.S.; Seo, H.S.; Hwang, S.J. Change of periodontal inflammatory indicators through a 4-week weight control intervention including caloric restriction and exercise training in young Koreans: A pilot study. BMC Oral Health 2015, 15, 109. [Google Scholar] [CrossRef]
- Pereira, K.K.Y.; Jara, C.M.; Antunes, G.L.; Gomes, M.S.; Rösing, C.K.; Cavagni, J.; Haas, A.N. Effects of periodontitis and periodontal treatment on systemic inflammatory markers and metabolic profile in obese and non-obese rats. J. Periodontol. 2022, 93, 1411–1420. [Google Scholar] [CrossRef]
- Papageorgiou, S.N.; Reichert, C.; Jäger, A.; Deschner, J. Effect of overweight/obesity on response to periodontal treatment: Systematic review and a meta-analysis. J. Clin. Periodontol. 2015, 42, 247–261. [Google Scholar] [CrossRef]
- Zhang, Y.; Jia, R.; Zhang, Y.; Sun, X.; Mei, Y.; Zou, R.; Niu, L.; Dong, S. Effect of non-surgical periodontal treatment on cytokines/adipocytokines levels among periodontitis patients with or without obesity: A systematic review and meta-analysis. BMC Oral Health 2023, 23, 717. [Google Scholar] [CrossRef] [PubMed]
- Tzanavari, T.; Giannogonas, P.; Karalis, K.P. TNF-alpha and obesity. Curr. Dir. Autoimmun. 2010, 11, 145–156. [Google Scholar] [CrossRef]
- Gonçalves, T.E.D.; Feres, M.; Zimmermann, G.S.; Faveri, M.; Figueiredo, L.C.; Braga, P.G.; Duarte, P.M. Effects of scaling and root planing on clinical response and serum levels of adipocytokines in patients with obesity and chronic periodontitis. J. Periodontol. 2015, 86, 53–61. [Google Scholar] [CrossRef] [PubMed]
- Zuza, E.C.; Pires, J.R.; de Almeida, A.A.; Toledo, B.E.C.; Guimaraes-Stabili, M.R.; Junior, C.R.; Barroso, E.M. Evaluation of recurrence of periodontal disease after treatment in obese and normal weight patients: Two-year follow-up. J. Periodontol. 2020, 91, 1123–1131. [Google Scholar] [CrossRef] [PubMed]
- Kaye, E.; McDonough, R.; Singhal, A.; Garcia, R.I.; Jurasic, M. Effect of Overweight and Obesity on Periodontal Treatment Intensity. JDR Clin. Trans. Res. 2023, 8, 158–167. [Google Scholar] [CrossRef]
- Martinez-Herrera, M.; López-Domènech, S.; Silvestre, F.J.; Silvestre-Rangil, J.; Bañuls, C.; Hernández-Mijares, A.; Rocha, M. Dietary therapy and non-surgical periodontal treatment in obese patients with chronic periodontitis. J. Clin. Periodontol. 2018, 45, 1448–1457. [Google Scholar] [CrossRef]
- Lakkis, D.; Bissada, N.F.; Saber, A.; Khaitan, L.; Palomo, L.; Narendran, S.; Al-Zahrani, M.S. Response to Periodontal Therapy in Patients Who Had Weight Loss After Bariatric Surgery and Obese Counterparts: A Pilot Study. J. Periodontol. 2012, 83, 684–689. [Google Scholar] [CrossRef]
- Driscoll, K.E.; Carter, J.M.; Hassenbein, D.G.; Howard, B. Cytokines and particle-induced inflammatory cell recruitment. Environ. Health Perspect. 1997, 105 (Suppl. S5), 1159–1164. [Google Scholar] [CrossRef]
- Van Der Meide, P.H.; Schellekens, H. Cytokines and the immune response. Biotherapy 1996, 8, 243–249. [Google Scholar] [CrossRef]
- Chan, A.H.; Schroder, K. Inflammasome signaling and regulation of interleukin-1 family cytokines. J. Exp. Med. 2020, 217, e20190314. [Google Scholar] [CrossRef]
- Feehan, K.T.; Gilroy, D.W. Is Resolution the End of Inflammation? Trends Mol. Med. 2019, 25, 198–214. [Google Scholar] [CrossRef]
- Feghali, C.A.; Wright, T.M. Cytokines in acute and chronic inflammation. Front. Biosci. 1997, 2, d12–d26. [Google Scholar] [CrossRef] [PubMed]
- Gabay, C.; Kushner, I. Acute-phase proteins and other systemic responses to inflammation. N. Engl. J. Med. 1999, 340, 448–454. [Google Scholar] [CrossRef] [PubMed]
- Roe, K. An inflammation classification system using cytokine parameters. Scand. J. Immunol. 2021, 93, e12970. [Google Scholar] [CrossRef] [PubMed]
- Physical Activity. Available online: https://www.who.int/health-topics/physical-activity#tab=tab_1 (accessed on 12 March 2025).
- Suzuki, K.; Tominaga, T.; Ruhee, R.T.; Ma, S. Characterization and Modulation of Systemic Inflammatory Response to Exhaustive Exercise in Relation to Oxidative Stress. Antioxidants 2020, 9, 401. [Google Scholar] [CrossRef]
- Suzuki, K. Chronic Inflammation as an Immunological Abnormality and Effectiveness of Exercise. Biomolecules 2019, 9, 223. [Google Scholar] [CrossRef]
- Suzuki, K. Characterization of Exercise-Induced Cytokine Release, the Impacts on the Body, the Mechanisms and Modulations. Int. J. Sports Exerc. Med. 2019, 5, 122. [Google Scholar] [CrossRef]
- Suzuki, K.; Naganuma, S.; Totsuka, M.; Suzuki, K.-J.; Mochizuki, M.; Shiraishi, M.; Nakaji, S.; Sugawara, K. Effects of exhaustive endurance exercise and its one-week daily repetition on neutrophil count and functional status in untrained men. Int. J. Sports Med. 1996, 17, 205–212. [Google Scholar] [CrossRef]
- Nieman, D.C.; Davis, J.M.; Henson, D.A.; Gross, S.J.; Dumke, C.L.; Utter, A.C.; Vinci, D.M.; Carson, J.A.; Brown, A.; Mcanulty, S.R. Muscle cytokine mRNA changes after 2.5 h of cycling: Influence of carbohydrate. Med. Sci. Sports Exerc. 2005, 37, 1283–1290. [Google Scholar] [CrossRef]
- Suzuki, K. Cytokine Response to Exercise and Its Modulation. Antioxidants 2018, 7, 17. [Google Scholar] [CrossRef]
- Kanda, K.; Sugama, K.; Hayashida, H.; Sakuma, J.; Kawakami, Y.; Miura, S.; Yoshioka, H.; Mori, Y.; Suzuki, K. Eccentric exercise-induced delayed-onset muscle soreness and changes in markers of muscle damage and inflammation. Exerc. Immunol. Rev. 2013, 19, 72–85. [Google Scholar] [PubMed]
- Banzet, S.; Koulmann, N.; Simler, N.; Birot, O.; Sanchez, H.; Chapot, R.; Peinnequin, A.; Bigard, X. Fibre-type specificity of interleukin-6 gene transcription during muscle contraction in rat: Association with calcineurin activity. J. Physiol. 2005, 566 Pt 3, 839–847. [Google Scholar] [CrossRef] [PubMed]
- Yamada, M.; Suzuki, K.; Kudo, S.; Totsuka, M.; Nakaji, S.; Sugawara, K. Raised plasma G-CSF and IL-6 after exercise may play a role in neutrophil mobilization into the circulation. J. Appl. Physiol. (1985) 2002, 92, 1789–1794. [Google Scholar] [CrossRef] [PubMed]
- Nieman, D.C.; Zwetsloot, K.A.; Lomiwes, D.D.; Meaney, M.P.; Hurst, R.D. Muscle glycogen depletion following 75-km of cycling is not linked to increased muscle IL-6, IL-8, and MCP-1 mRNA expression and protein content. Front. Physiol. 2016, 7, 431. [Google Scholar] [CrossRef]
- Febbraio, M.A.; Steensberg, A.; Keller, C.; Starkie, R.L.; Nielsen, H.B.; Krustrup, P.; Ott, P.; Secher, N.H.; Pedersen, B.K. Glucose ingestion attenuates interleukin-6 release from contracting skeletal muscle in humans. J. Physiol. 2003, 549 Pt 2, 607. [Google Scholar] [CrossRef]
- Keller, C.; Keller, P.; Marshal, S.; Pedersen, B.K. IL-6 gene expression in human adipose tissue in response to exercise—effect of carbohydrate ingestion. J. Physiol. 2003, 550 Pt 3, 927–931. [Google Scholar] [CrossRef]
- Ferreira, R.d.O.; dos Santos, V.R.N.; Sousa, J.M.M.; Peinado, B.R.R.; Souza-Monteiro, D.; Bittencourt, L.O.; Lima, M.L.d.S.; Rösing, C.K.; Collares, F.M.; de Araújo, A.A.; et al. Physical training minimizes immunological dysfunction, oxidative stress and tissue destruction on experimental periodontitis in rats. PLoS ONE 2024, 19, e0303374. [Google Scholar] [CrossRef]
- Minich, D.M.; Bland, J.S. Personalized lifestyle medicine: Relevance for nutrition and lifestyle recommendations. Sci. World J. 2013, 2013, 129841. [Google Scholar] [CrossRef]
- Ferreira, R.d.O.; Corrêa, M.G.; Magno, M.B.; Almeida, A.P.C.P.S.C.; Fagundes, N.C.F.; Rosing, C.K.; Maia, L.C.; Lima, R.R. Physical Activity Reduces the Prevalence of Periodontal Disease: Systematic Review and Meta-Analysis. Front. Physiol. 2019, 10, 234. [Google Scholar] [CrossRef]
- Shimazaki, Y.; Egami, Y.; Matsubara, T.; Koike, G.; Akifusa, S.; Jingu, S.; Yamashita, Y. Relationship Between Obesity and Physical Fitness and Periodontitis. J. Periodontol. 2010, 81, 1124–1131. [Google Scholar] [CrossRef]
- Wakai, K.; Kawamura, T.; Umemura, O.; Hara, Y.; Machida, J.; Anno, T.; Ichihara, Y.; Mizuno, Y.; Tamakoshi, A.; Lin, Y.; et al. Associations of medical status and physical fitness with periodontal disease. J. Clin. Periodontol. 1999, 26, 664–672. [Google Scholar] [CrossRef] [PubMed]
- You, Y.; Chen, Y.; Wei, M.; Tang, M.; Lu, Y.; Zhang, Q.; Cao, Q. Mediation Role of Recreational Physical Activity in the Relationship between the Dietary Intake of Live Microbes and the Systemic Immune-Inflammation Index: A Real-World Cross-Sectional Study. Nutrients 2024, 16, 777. [Google Scholar] [CrossRef] [PubMed]
- Bull, F.C.; Al-Ansari, S.S.; Biddle, S.; Borodulin, K.; Buman, M.P.; Cardon, G.; Carty, C.; Chaput, J.-P.; Chastin, S.; Chou, R.; et al. World Health Organization 2020 guidelines on physical activity and sedentary behaviour. Br. J. Sports Med. 2020, 54, 1451–1462. [Google Scholar] [CrossRef]
- Almohamad, M.; Kaye, E.K.; Mofleh, D.; Spartano, N.L. The association of sedentary behaviour and physical activity with periodontal disease in NHANES 2011–2012. J. Clin. Periodontol. 2022, 49, 758–767. [Google Scholar] [CrossRef] [PubMed]
- Pu, R.; Fu, M.; Yang, G.; Jiang, Z. The association of work physical activity and recreational physical activity with periodontitis in the NHANES (2009–2014). J. Periodontol. 2023, 94, 1220–1230. [Google Scholar] [CrossRef]
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Balice, G.; Paolantonio, M.; Murmura, G.; Serroni, M.; Di Gregorio, S.; Femminella, B. The Influence of Diet and Physical Activity on Periodontal Health: A Narrative Review. Dent. J. 2025, 13, 200. https://doi.org/10.3390/dj13050200
Balice G, Paolantonio M, Murmura G, Serroni M, Di Gregorio S, Femminella B. The Influence of Diet and Physical Activity on Periodontal Health: A Narrative Review. Dentistry Journal. 2025; 13(5):200. https://doi.org/10.3390/dj13050200
Chicago/Turabian StyleBalice, Giuseppe, Michele Paolantonio, Giovanna Murmura, Matteo Serroni, Stefania Di Gregorio, and Beatrice Femminella. 2025. "The Influence of Diet and Physical Activity on Periodontal Health: A Narrative Review" Dentistry Journal 13, no. 5: 200. https://doi.org/10.3390/dj13050200
APA StyleBalice, G., Paolantonio, M., Murmura, G., Serroni, M., Di Gregorio, S., & Femminella, B. (2025). The Influence of Diet and Physical Activity on Periodontal Health: A Narrative Review. Dentistry Journal, 13(5), 200. https://doi.org/10.3390/dj13050200