Free sugars and gingival inflammation: A systematic review and meta-analysis.
gingivitis
inflammation
periodontal disease
sucrose
sugars
Journal
Journal of clinical periodontology
ISSN: 1600-051X
Titre abrégé: J Clin Periodontol
Pays: United States
ID NLM: 0425123
Informations de publication
Date de publication:
09 2023
09 2023
Historique:
revised:
04
04
2023
received:
05
07
2022
accepted:
10
05
2023
medline:
18
8
2023
pubmed:
29
5
2023
entrez:
29
5
2023
Statut:
ppublish
Résumé
Consumption of free sugars has been associated with chronic non-communicable diseases. The aim of the study was to investigate the effect of free-sugar consumption on gingival inflammation using a systematic review and meta-analysis based on the PICO question 'What impact does the restriction of free sugars have on the inflammation of gingival tissue?' Literature review and analyses were based on the Cochrane Handbook for Systematic Reviews of Interventions. Controlled clinical studies reporting on free-sugar interventions and gingival inflammation were included. Risk of bias was performed with ROBINS-I and ROB-2, and effect sizes were estimated with robust variance meta-regressions. Of the 1777 primarily identified studies, 1768 were excluded, and 9 studies with 209 participants with gingival inflammation measures were included. Six of these studies reported on the dental plaque scores of 113 participants. Restriction of free sugars, when compared with no such restriction, was associated with statistically significantly improved gingival health scores (standard mean difference [SMD] = -0.92; 95% confidence interval [CI]: -1.43 to -0.42, p < .004; I Restriction of free sugar was shown to be associated with reduced gingival inflammation. The systematic review was registered at PROSPERO (CRD 42020157914).
Substances chimiques
Sugars
0
Types de publication
Meta-Analysis
Systematic Review
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1188-1201Informations de copyright
© 2023 The Authors. Journal of Clinical Periodontology published by John Wiley & Sons Ltd.
Références
Almas, K., Al-Qahtani, M., Al-Yami, M., & Khan, N. (2001). The relationship between periodontal disease and blood glucose level among type II diabetic patients. The Journal of Contemporary Dental Practice, 2(4), 18-25.
Bartha, V., Exner, L., Schweikert, D., Peter Woelber, J., Vach, K., Meyer, A.-L., Basrai, M., Bischoff, S. C., Meller, C., & Wolff, D. (2021). Effect of the Mediterranean diet on gingivitis: A randomized controlled trial. Journal of Clinical Periodontology, 49, 111-122. https://doi.org/10.1111/jcpe.13576
Baumgartner, S., Imfeld, T., Schicht, O., Rath, C., Persson, R. E., & Persson, G. R. (2009). The impact of the stone age diet on gingival conditions in the absence of oral hygiene. Journal of Periodontology, 80(5), 759-768. https://doi.org/10.1902/jop.2009.080376
Borenstein, M., Hedges, L. V., Higgins, J. P. T., & Rothstein, H. R. (2009). Introduction to meta-analysis. Wiley. https://doi.org/10.1002/9780470743386
Chapple, I. L. C., Mealey, B. L., Van Dyke, T. E., Bartold, P. M., Dommisch, H., Eickholz, P., Geisinger, M. L., Genco, R. J., Glogauer, M., Goldstein, M., Griffin, T. J., Holmstrup, P., Johnson, G. K., Kapila, Y., Lang, N. P., Meyle, J., Murakami, S., Plemons, J., Romito, G. A., … Yoshie, H. (2018). Periodontal health and gingival diseases and conditions on an intact and a reduced periodontium: Consensus report of workgroup 1 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. Journal of Periodontology, 89(Suppl 1), S74-S84. https://doi.org/10.1002/JPER.17-0719
Chapple, I. L. C., Van der Weijden, F., Doerfer, C., Herrera, D., Shapira, L., Polak, D., Madianos, P., Louropoulou, A., Machtei, E., Donos, N., Greenwell, H., Van Winkelhoff, A. J., Kuru, B. E., Arweiler, N., Teughels, W., Aimetti, M., Molina, A., Montero, E., & Graziani, F. (2015). Primary prevention of periodontitis: Managing gingivitis. Journal of Clinical Periodontology, 42(Suppl 16), S71-S76. https://doi.org/10.1111/jcpe.12366
Cheraskin, E. (1988). How quickly does diet make for change? A study in gingival inflammation. The New York Journal of Dentistry, 58(4), 133-135.
Cheraskin, E., Ringsdorf, W. M., Setyaadmadja, A. T., & Barrett, R. A. (1966). Stomatology and the total organism: A study in carbohydrate metabolism. Rivista Italiana di Stomatologia, 21(7), 651-667.
Chun, S., Choi, Y., Chang, Y., Cho, J., Zhang, Y., Rampal, S., Zhao, D., Ahn, J., Suh, B.-S., Pastor-Barriuso, R., Lima, J. A. C., Chung, E. C., Shin, H., Guallar, E., & Ryu, S. (2016). Sugar-sweetened carbonated beverage consumption and coronary artery calcification in asymptomatic men and women. American Heart Journal, 177, 17-24. https://doi.org/10.1016/j.ahj.2016.03.018
Frantsve-Hawley, J., Bader, J. D., Welsh, J. A., & Wright, J. T. (2017). A systematic review of the association between consumption of sugar-containing beverages and excess weight gain among children under age 12. Journal of Public Health Dentistry, 77(Suppl 1), S43-S66. https://doi.org/10.1111/jphd.12222
Fung, T. T., van Dam, R. M., Hankinson, S. E., Stampfer, M., Willett, W. C., & Hu, F. B. (2010). Low-carbohydrate diets and all-cause and cause-specific mortality: Two cohort studies. Annals of Internal Medicine, 153(5), 289-298. https://doi.org/10.7326/0003-4819-153-5-201009070-00003
Gaengler, P., Pfister, W., Sproessig, M., & Mirgorod, M. (1986). The effects of carbohydrate-reduced diet on development of gingivitis. Clinical Preventive Dentistry, 8(6), 17-23.
Guyenet, S. J. (2019). Impact of whole, fresh fruit consumption on energy intake and adiposity: A systematic review. Frontiers in Nutrition, 6, 66. https://doi.org/10.3389/fnut.2019.00066
Hall, K. D., Ayuketah, A., Brychta, R., Cai, H., Cassimatis, T., Chen, K. Y., Chung, S. T., Costa, E., Courville, A., Darcey, V., Fletcher, L. A., Forde, C. G., Gharib, A. M., Guo, J., Howard, R., Joseph, P. V., McGehee, S., Ouwerkerk, R., Raisinger, K., … Zhou, M. (2019). Ultra-processed diets cause excess calorie intake and weight gain: An inpatient randomized controlled trial of Ad libitum food intake. Cell Metabolism, 30(1), 67-77.e3. https://doi.org/10.1016/j.cmet.2019.05.008
Harjola, U., & Liesmaa, H. (1978). Effects of polyol and sucrose candies on plaque, gingivitis and lactobacillus index scores. Observations on Helsinki school children. Acta Odontologica Scandinavica, 36(4), 237-242. https://doi.org/10.3109/00016357809004674
Hedges, L. V., Tipton, E., & Johnson, M. C. (2010). Robust variance estimation in meta-regression with dependent effect size estimates. Research Synthesis Methods, 1(1), 39-65.
Higgins, J. P., Savović, J., Page, M. J., Elbers, R. G., & Sterne, J. A. (2019). Assessing risk of bias in a randomized trial. In Cochrane Handbook for Systematic Reviews of Interventions (pp. 205-228). The Cochrane Collaboration.
Higgins, J. P., Thomas, J., Chandler, J., Cumpston, M., Li, T., Page, M. J., & Welch, V. A. (2019). Cochrane handbook for systematic reviews of interventions. John Wiley & Sons.
Higgins, J. P. T., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003). Measuring inconsistency in meta-analyses. BMJ (Clinical Research Ed.), 327(7414), 557-560. https://doi.org/10.1136/bmj.327.7414.557
Holmer, H., Widén, C., Wallin Bengtsson, V., Coleman, M., Wohlfart, B., Steen, S., Persson, R., & Sjöberg, K. (2018). Improved general and oral health in diabetic patients by an Okinawan-based Nordic diet: A pilot study. International Journal of Molecular Sciences, 19(7), 1-13. https://doi.org/10.3390/ijms19071949
Hujoel, P. P., Kato, T., Hujoel, I. A., & Hujoel, M. L. A. (2021). Bleeding tendency and ascorbic acid requirements: Systematic review and meta-analysis of clinical trials. Nutrition Reviews, 79, nuaa115. https://doi.org/10.1093/nutrit/nuaa115
Hujoel, P. P., & Stott-Miller, M. (2011). Retinal and gingival hemorrhaging and chronic hyperglycemia. Diabetes Care, 34(1), 181-183. https://doi.org/10.2337/dc10-0901
Incalza, M. A., D'Oria, R., Natalicchio, A., Perrini, S., Laviola, L., & Giorgino, F. (2018). Oxidative stress and reactive oxygen species in endothelial dysfunction associated with cardiovascular and metabolic diseases. Vascular Pharmacology, 100, 1-19.
Jafar, N., Edriss, H., & Nugent, K. (2016). The effect of short-term hyperglycemia on the innate immune system. The American Journal of the Medical Sciences, 351(2), 201-211. https://doi.org/10.1016/j.amjms.2015.11.011
Jalil, R. A., Cornick, D. E., & Waite, I. M. (1983). Effect of variation in dietary sucrose intake on plaque removal by mechanical means. Journal of Clinical Periodontology, 10(4), 389-398. https://doi.org/10.1111/j.1600-051x.1983.tb01288.x
Jockel-Schneider, Y., Goßner, S. K., Petersen, N., Stölzel, P., Hägele, F., Schweiggert, R. M., Haubitz, I., Eigenthaler, M., Carle, R., & Schlagenhauf, U. (2016). Stimulation of the nitrate-nitrite-NO-metabolism by repeated lettuce juice consumption decreases gingival inflammation in periodontal recall patients: A randomized, double-blinded, placebo-controlled clinical trial. Journal of Clinical Periodontology, 43(7), 603-608. https://doi.org/10.1111/jcpe.12542
Johnson, R. J., Segal, M. S., Sautin, Y., Nakagawa, T., Feig, D. I., Kang, D.-H., Gersch, M. S., Benner, S., & Sánchez-Lozada, L. G. (2007). Potential role of sugar (fructose) in the epidemic of hypertension, obesity and the metabolic syndrome, diabetes, kidney disease, and cardiovascular disease. The American Journal of Clinical Nutrition, 86(4), 899-906. https://doi.org/10.1093/ajcn/86.4.899
Kashket, S., Zhang, J., & Niederman, R. (1998). Gingival inflammation induced by food and short-chain carboxylic acids. Journal of Dental Research, 77(2), 412-417. https://doi.org/10.1177/00220345980770021001
Kearns, C. E., & Bero, L. A. (2019). Conflicts of interest between the sugary food and beverage industry and dental research organisations: Time for reform. The Lancet, 394(10194), 194-196.
Kearns, C. E., Glantz, S. A., & Schmidt, L. A. (2015). Sugar industry influence on the scientific agenda of the National Institute of Dental Research's 1971 National Caries Program: A historical analysis of internal documents. PLoS Medicine, 12(3), e1001798. https://doi.org/10.1371/journal.pmed.1001798
Kulmer, S., & Kulmer, R. (1982). Experimental gingivitis and isolated carbohydrates. Osterreichische Zeitschrift Fur Stomatologie, 79(10), 352-359.
Laguna, J. C., Alegret, M., Cofán, M., Sánchez-Tainta, A., Díaz-López, A., Martínez-González, M. A., Sorlí, J. V., Salas-Salvadó, J., Fitó, M., Alonso-Gómez, Á. M., Serra-Majem, L., Lapetra, J., Fiol, M., Gómez-Gracia, E., Pintó, X., Muñoz, M. A., Castañer, O., Ramírez-Sabio, J. B., Portu, J. J., … Ros, E. (2021). Simple sugar intake and cancer incidence, cancer mortality and all-cause mortality: A cohort study from the PREDIMED trial. Clinical Nutrition (Edinburgh, Scotland), 40(10), 5269-5277. https://doi.org/10.1016/j.clnu.2021.07.031
Landis, J. R., & Koch, G. G. (1977). The measurement of observer agreement for categorical data. Biometrics, 33, 159-174.
Lang, N. P., Schätzle, M. A., & Löe, H. (2009). Gingivitis as a risk factor in periodontal disease. Journal of Clinical Periodontology, 36(Suppl 10), 3-8. https://doi.org/10.1111/j.1600-051X.2009.01415.x
Li, Y., Lee, S., Hujoel, P., Su, M., Zhang, W., Kim, J., Zhang, Y. P., & DeVizio, W. (2010). Prevalence and severity of gingivitis in American adults. American Journal of Dentistry, 23(1), 9-13.
Löe, H., Theilade, E., & Jensen, S. B. (1965). Experimental gingivitis in man. The Journal of Periodontology, 36(3), 177-187.
Lula, E. C. O., Ribeiro, C. C. C., Hugo, F. N., Alves, C. M. C., & Silva, A. A. M. (2014). Added sugars and periodontal disease in young adults: An analysis of NHANES III data. The American Journal of Clinical Nutrition, 100(4), 1182-1187. https://doi.org/10.3945/ajcn.114.089656
Malik, V. S., & Hu, F. B. (2012). Sweeteners and risk of obesity and type 2 diabetes: The role of sugar-sweetened beverages. Current Diabetes Reports, 12, 195-203. https://doi.org/10.1007/s11892-012-0259-6
May, C. E., Rosander, J., Gottfried, J., Dennis, E., & Dus, M. (2020). Dietary sugar inhibits satiation by decreasing the central processing of sweet taste. eLife, 9, e54530. https://doi.org/10.7554/eLife.54530
McGuinness, L. A., & Higgins, J. P. (2021). Risk-of-bias VISualization (robvis): An R package and Shiny web app for visualizing risk-of-bias assessments. Research Synthesis Methods, 12(1), 55-61.
Meier, T., Deumelandt, P., Christen, O., Stangl, G. I., Riedel, K., & Langer, M. (2017). Global burden of sugar-related dental diseases in 168 countries and corresponding health care costs. Journal of Dental Research, 96(8), 845-854. https://doi.org/10.1177/0022034517708315
Mohanty, P., Hamouda, W., Garg, R., Aljada, A., Ghanim, H., & Dandona, P. (2000). Glucose challenge stimulates reactive oxygen species (ROS) generation by leucocytes. The Journal of Clinical Endocrinology and Metabolism, 85(8), 2970-2973. https://doi.org/10.1210/jcem.85.8.6854
Moores, C. J., Kelly, S. A. M., & Moynihan, P. J. (2022). Systematic review of the effect on caries of sugars intake: Ten-year update. Journal of Dental Research, 101, 1034-1045. https://doi.org/10.1177/00220345221082918
Moreira, A. R. O., Batista, R. F. L., Ladeira, L. L. C., Thomaz, E. B. A. F., Alves, C. M. C., Saraiva, M. C., Silva, A. A. M., Brondani, M. A., & Ribeiro, C. C. C. (2021). Higher sugar intake is associated with periodontal disease in adolescents. Clinical Oral Investigations, 25(3), 983-991. https://doi.org/10.1007/s00784-020-03387-1
Moynihan, P. (2016). Sugars and dental caries: Evidence for setting a recommended threshold for intake. Advances in Nutrition (Bethesda, Md.), 7(1), 149-156. https://doi.org/10.3945/an.115.009365
Moynihan, P., Makino, Y., Petersen, P. E., & Ogawa, H. (2018). Implications of WHO guideline on sugars for dental health professionals. Community Dentistry and Oral Epidemiology, 46(1), 1-7. https://doi.org/10.1111/cdoe.12353
O'Keefe, J. H., & Bell, D. S. H. (2007). Postprandial hyperglycemia/hyperlipidemia (postprandial dysmetabolism) is a cardiovascular risk factor. The American Journal of Cardiology, 100(5), 899-904. https://doi.org/10.1016/j.amjcard.2007.03.107
Page, M. J., McKenzie, J. E., Bossuyt, P. M., Boutron, I., Hoffmann, T. C., Mulrow, C. D., Shamseer, L., Tetzlaff, J. M., Akl, E. A., Brennan, S. E., Chou, R., Glanville, J., Grimshaw, J. M., Hróbjartsson, A., Lalu, M. M., Li, T., Loder, E. W., Mayo-Wilson, E., McDonald, S., … Brennan, S. E. (2021). The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. International Journal of Surgery, 88, 105906.
Paunio, K., Hurttia, H., Tenovuo, J., Mäkinen, K. K., & Tiekso, J. (1984). Effects on oral health of mouthrinses containing xylitol, sodium cyclamate and sucrose sweeteners in the absence of oral hygiene. I. Clinical findings and analysis of gingival exudate. Proceedings of the Finnish Dental Society. Suomen Hammaslaakariseuran Toimituksia, 80(1), 3-12.
Petersen, P. E., & Ogawa, H. (2005). Strengthening the prevention of periodontal disease: The WHO approach. Journal of Periodontology, 76(12), 2187-2193. https://doi.org/10.1902/jop.2005.76.12.2187
Prior, R. L., Gu, L., Wu, X., Jacob, R. A., Sotoudeh, G., Kader, A. A., & Cook, R. A. (2007). Plasma antioxidant capacity changes following a meal as a measure of the ability of a food to alter in vivo antioxidant status. Journal of the American College of Nutrition, 26(2), 170-181. https://doi.org/10.1080/07315724.2007.10719599
Salazar, C. R., Laniado, N., Mossavar-Rahmani, Y., Borrell, L. N., Qi, Q., Sotres-Alvarez, D., Morse, D. E., Singer, R. H., Kaplan, R. C., Badner, V., & Lamster, I. B. (2018). Better-quality diet is associated with lower odds of severe periodontitis in US Hispanics/Latinos. Journal of Clinical Periodontology, 45(7), 780-790. https://doi.org/10.1111/jcpe.12926
Schulz, K. F., Altman, D. G., & Moher, D. (2010). CONSORT 2010 statement: Updated guidelines for reporting parallel group randomised trials. BMJ, 340, c332. https://doi.org/10.1136/bmj.c332
Sheiham, A., & Watt, R. G. (2000). The common risk factor approach: A rational basis for promoting oral health. Community Dentistry and Oral Epidemiology, 28(6), 399-406. https://doi.org/10.1034/j.1600-0528.2000.028006399.x
Sidi, A. D., & Ashley, F. P. (1984). Influence of frequent sugar intakes on experimental gingivitis. Journal of Periodontology, 55(7), 419-423. https://doi.org/10.1902/jop.1984.55.7.419
Silness, J., & Löe, H. (1964). Periodontal disease in pregnancy II. Correlation between oral hygiene and periodontal condition. Acta Odontologica Scandinavica, 22(1), 121-135.
Sterne, J. A., Hernán, M. A., Reeves, B. C., Savović, J., Berkman, N. D., Viswanathan, M., Henry, D., Altman, D. G., Ansari, M. T., Boutron, I., Carpenter, J. R., Chan, A.-W., Churchill, R., Deeks, J. J., Hróbjartsson, A., Kirkham, J., Jüni, P., Loke, Y. K., Pigott, T. D., … Higgins, J. P. (2016). ROBINS-I: A tool for assessing risk of bias in non-randomised studies of interventions. BMJ, 355, i4919. https://doi.org/10.1136/bmj.i4919
Tipton, E. (2015). Small sample adjustments for robust variance estimation with meta-regression. Psychological Methods, 20(3), 375-393.
Trombelli, L., Farina, R., Minenna, L., Carrieri, A., Scapoli, C., & Tatakis, D. N. (2008). Experimental gingivitis: Reproducibility of plaque accumulation and gingival inflammation parameters in selected populations during a repeat trial. Journal of Clinical Periodontology, 35(11), 955-960. https://doi.org/10.1111/j.1600-051X.2008.01315.x
van der Weijden, F., & Slot, D. E. (2011). Oral hygiene in the prevention of periodontal diseases: The evidence. Periodontology 2000, 55(1), 104-123. https://doi.org/10.1111/j.1600-0757.2009.00337.x
Von der Fehr, F. R., Löe, H., & Theilade, E. (1970). Experimental caries in man. Caries Research, 4(2), 131-148. https://doi.org/10.1159/000259635
Woelber, J. P., Bremer, K., Vach, K., König, D., Hellwig, E., Ratka-Krüger, P., Al-Ahmad, A., & Tennert, C. (2016). An oral health optimized diet can reduce gingival and periodontal inflammation in humans-A randomized controlled pilot study. BMC Oral Health, 17(1), 28. https://doi.org/10.1186/s12903-016-0257-1
Woelber, J. P., Gärtner, M., Breuninger, L., Anderson, A., König, D., Hellwig, E., Al-Ahmad, A., Vach, K., Dötsch, A., Ratka-Krüger, P., & Tennert, C. (2019). The influence of an anti-inflammatory diet on gingivitis. A randomized controlled trial. Journal of Clinical Periodontology, 46(4), 481-490. https://doi.org/10.1111/jcpe.13094
Wölnerhanssen, B. K., Meyer-Gerspach, A. C., Schmidt, A., Zimak, N., Peterli, R., Beglinger, C., & Borgwardt, S. (2015). Dissociable behavioral, physiological and neural effects of acute glucose and fructose ingestion: A pilot study. PLoS One, 10(6), e0130280. https://doi.org/10.1371/journal.pone.0130280
World Health Organization. (2015). Guideline: Sugars intake for adults and children. World Health Organization.