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Bypass gastroplasty impacts oral health, salivary inflammatory biomarkers, and microbiota: a controlled study

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Abstract

Objectives

Knowledge about the impact of gastroplasty on oral health and salivary biomarkers is limited. The aim was to prospectively evaluate oral health status, salivary inflammatory markers, and microbiota in patients undergoing gastroplasty compared with a control group undergoing a dietary program.

Materials and methods

Forty participants with obesity class II/III were included (20 individuals in each sex-matched group; 23–44 years). Dental status, salivary flow, buffering capacity, inflammatory cytokines, and uric acid were assessed. Salivary microbiological analysis (16S-rRNA sequencing) assessed the abundance of genus, species, and alpha diversity. Cluster analysis and mixed-model ANOVA were applied.

Results

Oral health status, waist-to-hip ratio, and salivary alpha diversity were associated at baseline. A subtle improvement in food consumption markers was observed, although caries activity increased in both groups, and the gastroplasty group showed worse periodontal status after three months. IFNγ and IL10 levels decreased in the gastroplasty group at 3 months, while a decrease was observed in the control group at 6 months; IL6 decreased in both groups (p < 0.001). Salivary flow and buffering capacity did not change. Significant changes in Prevotella nigrescens and Porphyromonas endodontalis abundance were observed in both groups, while alpha diversity (Sobs, Chao1, Ace, Shannon, and Simpson) increased in the gastroplasty group.

Conclusions

Both interventions changed in different degrees the salivary inflammatory biomarkers and microbiota, but did not improve the periodontal status after 6 months.

Clinical relevance

Although the observed discrete improvement in dietary habits, caries activity increased with no clinical improvement in the periodontal status, emphasizing the need of oral health monitoring during obesity treatment.

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Data availability

Data will be made available upon reasonable request to the corresponding author.

Abbreviations

BMI:

Body mass index

CPI:

Community Periodontal Index

DMFT:

Decayed, missed, and filled teeth

OUT:

Operational taxonomic units

ANOVA:

Analysis of variance

References

  1. NCD Risk Factor Collaboration (NCD-RisC) (2017) Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128·9 million children, adolescents, and adults. Lancet 390(10113):2627–2642. https://doi.org/10.1016/S0140-6736(17)32129-3

    Article  Google Scholar 

  2. Brasil. Ministério da Saúde (2020) Vigitel Brasil 2019: vigilância de fatores de risco e proteção para doenças crônicas por inquérito telefônico. Ministério da Saúde, Brasília

    Google Scholar 

  3. Ricci MA, De Vuono S, Scavizzi M, Gentili A, Lupattelli G (2016) Facing morbid obesity: how to approach it. Angiology 67:391–397. https://doi.org/10.1177/0003319715595735

    Article  PubMed  Google Scholar 

  4. Hales CM, Fryar CD, Carroll MD, Freedman DS, Ogden CL (2018) Trends in obesity and severe obesity prevalence in US youth and adults by sex and age, 2007–2008 to 2015–2016. JAMA 319:1723–1725. https://doi.org/10.1001/jama.2018.3060

    Article  PubMed  PubMed Central  Google Scholar 

  5. Malta DC, Silva AGD, Tonaco LAB, Freitas MIF, Velasquez-Melendez G (2019) Time trends in morbid obesity prevalence in the Brazilian adult population from 2006 to 2017. Cad Saude Publica 35:e00223518. https://doi.org/10.1590/0102-311X00223518

    Article  PubMed  Google Scholar 

  6. Rosa SC, Macedo JLS, Canedo LR, Casulari LA (2019) Quality of life and predictive factors for complications in patients undergoing abdominoplasty after gastric bypass: a retrospective cohort. Surg Obes Relat Dis 15:447–455. https://doi.org/10.1016/j.soard.2018.12.034

    Article  PubMed  Google Scholar 

  7. Madan AK, Orth W, Ternovits CA, Tichansky DS (2006) Metabolic syndrome: yet another co-morbidity gastric bypass helps cure. Surg Obes Relat Dis 2:48–51. https://doi.org/10.1016/j.soard.2005.09.014. (discussion 51)

    Article  PubMed  Google Scholar 

  8. de Moura-Grec PG, Yamashita JM, Marsicano JA, Ceneviva R, de Souza Leite CV, de Brito GB et al (2014) Impact of bariatric surgery on oral health conditions: 6-months cohort study. Int Dent J 64:144–149. https://doi.org/10.1111/idj.12090

    Article  PubMed  Google Scholar 

  9. Marquezin MCS, Scudine KGO, Lamy E, Finassi CM, Carreira L, Segura WD et al (2022) Impact of gastroplasty on salivary characteristics, dental health status and oral sensory aspects: a controlled clinical study. J Oral Rehabil 25. https://doi.org/10.1111/joor.13353

  10. Alves MSC, Silva FACC, Araújo SG, Carvalho ACA, Santos AM, Carvalho ALA (2012) Tooth wear in patients submitted to bariatric surgery. Braz Dental J 23:160–166. https://doi.org/10.1590/S0103-64402012000200012

    Article  Google Scholar 

  11. Castilho AVSS, Foratori-Junior GA, Sales-Peres SHC (2019) Bariatric surgery impact on gastroesophageal reflux and dental wear: a systematic review. ABCD Arq Bras Cir Dig 32:e1466. https://doi.org/10.1590/0102-672020190001e1466

    Article  PubMed  Google Scholar 

  12. Miranda-Rius J, Brunet-Llobet L, Lahor-Soler E, Farré M (2015) Salivary secretory disorders, inducing drugs, and clinical management. Int J Med Sci 12:811–824. https://doi.org/10.7150/ijms.12912

    Article  PubMed  PubMed Central  Google Scholar 

  13. Turner MD (2016) Hyposalivation and xerostomia: etiology, complications, and medical management. Dent Clin North Am 60:435–443. https://doi.org/10.1016/j.cden.2015.11.003

    Article  PubMed  Google Scholar 

  14. Hashizume LN, Bastos LF, Cardozo DD, Hilgert JB, Hugo FN, Stein AT et al (2015) Impact of bariatric surgery on the saliva of patients with morbid obesity. Obes Surg 25:1550–1555. https://doi.org/10.1007/s11695-015-1741-4

    Article  PubMed  Google Scholar 

  15. Yamashita Y, Takeshita T (2017) The oral microbiome and human health. J Oral Sci 59:201–206. https://doi.org/10.2334/josnusd.16-0856

    Article  PubMed  Google Scholar 

  16. Belstrøm D (2020) The salivary microbiota in health and disease. J Oral Microbiol 12:1723975. https://doi.org/10.1080/20002297.2020.1723975

    Article  PubMed  PubMed Central  Google Scholar 

  17. Socransky SS, Haffajee AD (2005) Periodontal microbial ecology. Periodontol 2000 38:135–187. https://doi.org/10.1111/j.1600-0757.2005.00107.x

    Article  PubMed  Google Scholar 

  18. Raju SC, Lagström S, Ellonen P, de Vos WM, Eriksson JG, Weiderpass E et al (2019) Gender-specific associations between saliva microbiota and body size. Front Microbiol 10:767. https://doi.org/10.3389/fmicb.2019.00767

    Article  PubMed  PubMed Central  Google Scholar 

  19. Koliarakis I, Messaritakis I, Nikolouzakis TK, Hamilos G, Souglakos J, Tsiaoussis J (2019) Oral bacteria and intestinal dysbiosis in colorectal cancer. Int J Mol Sci 20:4146. https://doi.org/10.3390/ijms20174146

    Article  PubMed  PubMed Central  Google Scholar 

  20. Dupim Souza AC, Franco CF, Pataro AL, Guerra T, de Oliveira CF, da Costa JE (2013) Halitosis in obese patients and those undergoing bariatric surgery. Surg Obes Relat Dis 9:315–321. https://doi.org/10.1016/j.soard.2011.10.020

    Article  PubMed  Google Scholar 

  21. Brasil (2015) Orientações para avaliação de marcadores de consumo alimentar na atenção básica. Ministério da Saúde, Secretaria de Atenção à Saúde, Departamento de Atenção Básica. Brasília: Ministério da Saúde. Available online at: http://bvsms.saude.gov.br/bvs/publicacoes/marcadores_consumo_alimentar_atencao_basica.pdf . Last access 10 Aug 2022

  22. Marquezin MCS, Chaves-Júnior SC, Rasera I Jr, Pacheco ERP, Gavião MBD, Lamy E et al (2020) Oral health and nutritional characteristics of adults with morbid obesity: a multivariate analysis. Front Nutr 7:589510. https://doi.org/10.3389/fnut.2020.589510

    Article  PubMed  PubMed Central  Google Scholar 

  23. World Health Organization (2013) Oral health surveys: basic methods. World Health Organization, Geneva

    Google Scholar 

  24. Araujo DS, Scudine KGO, Pedroni-Pereira A, Gavião MBD, Pereira EC, Fonseca FLA et al (2020) Salivary uric acid is a predictive marker of body fat percentage in adolescents. Nutr Res 74:62–70. https://doi.org/10.1016/j.nutres.2019.11.007

    Article  PubMed  Google Scholar 

  25. Vakh C, Koronkiewicz S, Kalinowski S, Moskvin L, Bulatov A (2017) An automatic chemiluminescence method based on the multi-pumping flow system coupled with the fluidized reactor and direct-injection detector: determination of uric acid in saliva samples. Talanta 15(167):725–732. https://doi.org/10.1016/j.talanta.2017.02.009

    Article  Google Scholar 

  26. Griffen AL, Beall CJ, Campbell JH, Firestone ND, Kumar PS, Yang ZK et al (2012) Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J 6:1176–1185. https://doi.org/10.1038/ismej.2011.191

    Article  PubMed  Google Scholar 

  27. Chen H, Liu Y, Zhang M, Wang G, Qi Z, Bridgewater L et al (2015) A Filifactor alocis-centered co-occurrence group associates with periodontitis across different oral habitats. Sci Rep 12(5):9053. https://doi.org/10.1038/srep09053

    Article  Google Scholar 

  28. Genco RJ, LaMonte MJ, McSkimming DI, Buck MJ, Li L, Hovey KM et al (2019) The subgingival microbiome relationship to periodontal disease in older women. J Dent Res 98:975–984. https://doi.org/10.1177/0022034519860449

    Article  PubMed  PubMed Central  Google Scholar 

  29. Takeshita T, Kageyama S, Furuta M, Tsuboi H, Takeuchi K, Shibata Y et al (2016) Bacterial diversity in saliva and oral health-related conditions: the Hisayama Study. Sci Rep 24(6):22164. https://doi.org/10.1038/srep22164

    Article  Google Scholar 

  30. Marsicano JA, Sales-Peres A, Ceneviva R, de C Sales-Peres SH (2012) Evaluation of oral health status and salivary flow rate in obese patients after bariatric surgery. Eur J Dent 6:191–192

    Article  PubMed  PubMed Central  Google Scholar 

  31. Doğan GE, Toraman A, Şebin SÖ, Doğan Ç, Güngör A, Aksoy H et al (2016) Salivary IL-6 and IL-10 levels in subjects with obesity and gingivitis. Am J Dent 29:261–265

    PubMed  Google Scholar 

  32. İnanir M (2020) Serum uric acid (SUA) in morbidly obese patients and its relationship with metabolic syndrome. Aging male 23:1165–1169. https://doi.org/10.1080/13685538.2020.1713742

    Article  PubMed  Google Scholar 

  33. Soukup M, Biesiada I, Henderson A, Idowu B, Rodeback D, Ridpath L et al (2012) Salivary uric acid as a noninvasive biomarker of metabolic syndrome. Diabetol Metab Syndr 19(4):14. https://doi.org/10.1186/1758-5996-4-14

    Article  Google Scholar 

  34. Troisi J, Belmonte F, Bisogno A, Lausi O, Marciano F, Cavallo P et al (2019) Salivary markers of hepato-metabolic comorbidities in pediatric obesity. Dig Liver Dis 51:516–523. https://doi.org/10.1016/j.dld.2018.11.009

    Article  PubMed  Google Scholar 

  35. Fontanille I, Boillot A, Rangé H, Carra MC, Sales-Peres SHC, Czernichow S et al (2018) Bariatric surgery and periodontal status: a systematic review with meta-analysis. Surg Obes Relat Dis 14:1618–1631. https://doi.org/10.1016/j.soard.2018.07.017

    Article  PubMed  Google Scholar 

  36. Serpa Neto A, Rossi FM, Valle LG, Teixeira GK, Rossi M (2011) Relation of uric acid with components of metabolic syndrome before and after Roux-en-Y gastric bypass in morbidly obese subjects. Arq Bras Endocrinol Metabol 55:38–45. https://doi.org/10.1590/s0004-27302011000100005

    Article  PubMed  Google Scholar 

  37. Menenakos E, Doulami G, Tzanetakou IP, Natoudi M, Kokoroskos N, Almpanopoulos K et al (2015) The use of serum uric acid concentration as an indicator of laparoscopic sleeve gastrectomy success. Int Surg 100:173–179. https://doi.org/10.9738/INTSURG-D-13-00186.1

    Article  PubMed  PubMed Central  Google Scholar 

  38. Oberbach A, Neuhaus J, Schlichting N, Kugler J, Baumann S, Till H (2014) Sleeve gastrectomy reduces xanthine oxidase and uric acid in a rat model of morbid obesity. Surg Obes Relat Dis 10:684–690. https://doi.org/10.1016/j.soard.2013.12.010

    Article  PubMed  Google Scholar 

  39. Lu C, Li Y, Li L, Kong Y, Shi T, Xiao H et al (2020) Alterations of serum uric acid level and gut microbiota after Roux-en-Y gastric bypass and sleeve gastrectomy in a hyperuricemic rat model. Obes Surg 30:1799–1807. https://doi.org/10.1007/s11695-019-04328-y

    Article  PubMed  PubMed Central  Google Scholar 

  40. Valm AM (2019) The structure of dental plaque microbial communities in the transition from health to dental caries and periodontal disease. J Mol Biol 26(431):2957–2969. https://doi.org/10.1016/j.jmb.2019.05.016

    Article  Google Scholar 

  41. Maitre I, Lourtioux F, Picouet P, Braud A (2020) Oral health-related food selectivity among French independently living elders. J Oral Rehabil 47:511–522. https://doi.org/10.1111/joor.12931

    Article  Google Scholar 

  42. Northridge ME, Kumar A, Kaur R (2020) Disparities in access to oral health care. Annu Rev Public Health 2(41):513–535. https://doi.org/10.1146/annurev-publhealth-040119-094318

    Article  Google Scholar 

  43. Paes Leme AF, Koo H, Bellato CM, Bedi G, Cury JA (2006) The role of sucrose in cariogenic dental biofilm formation–new insight. J Dent Res 85:878–887. https://doi.org/10.1177/154405910608501002

    Article  PubMed  Google Scholar 

  44. Araujo DS, Klein MI, Scudine KGO, de Sales LL, Parisotto TM, Ferreira CM et al (2020) Salivary microbiological and gingival health status evaluation of adolescents with overweight and obesity: a cluster analysis. Front Pediatr 31(8):429. https://doi.org/10.3389/fped.2020.00429

    Article  Google Scholar 

  45. Piombino P, Genovese A, Esposito S, Moio L, Cutolo PP, Chambery A et al (2014) Saliva from obese individuals suppresses the release of aroma compounds from wine. PLoS One 9:e85611. https://doi.org/10.1371/journal.pone.0085611

    Article  PubMed  PubMed Central  Google Scholar 

  46. Bombin A, Yan S, Bombin S, Mosley JD, Ferguson JF (2022) Obesity influences composition of salivary and fecal microbiota and impacts the interactions between bacterial taxa. Physiol Rep 10:e15254. https://doi.org/10.14814/phy2.15254

    Article  PubMed  PubMed Central  Google Scholar 

  47. Bartold PM, Cantley MD, Haynes DR (2010) Mechanisms and control of pathologic bone loss in periodontitis. Periodontol 2000 53:55–69. https://doi.org/10.1111/j.1600-0757.2010.00347.x

    Article  PubMed  Google Scholar 

  48. Costalonga M, Herzberg MC (2014) The oral microbiome and the immunobiology of periodontal disease and caries. Immunol Lett 162:22–38. https://doi.org/10.1016/j.imlet.2014.08.017

    Article  PubMed  PubMed Central  Google Scholar 

  49. Hajishengallis G, Lamont RJ (2012) Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol 27:409–419. https://doi.org/10.1111/j.2041-1014.2012.00663.x

    Article  PubMed  PubMed Central  Google Scholar 

  50. Moraes LC, Fatturi-Parolo CC, Ferreira MB, Só MV, Montagner F (2015) Saliva, supragingival biofilm and root canals can harbor gene associated with resistance to lactamic agents. Braz Oral Res 29:52

    Article  PubMed  Google Scholar 

  51. Vancauwenberghe F, Dadamio J, Laleman I, Van Tornout M, Teughels W, Coucke W et al (2013) The role of Solobacterium moorei in oral malodour. J Breath Res 7:046006

    Article  PubMed  Google Scholar 

  52. Wilmanski T, Rappaport N, Earls JC, Magis AT, Manor O, Lovejoy J et al (2019) Blood metabolome predicts gut microbiome α-diversity in humans. Nat Biotechnol 37:1217–1228. https://doi.org/10.1038/s41587-019-0233-9

    Article  PubMed  Google Scholar 

  53. Chumponsuk T, Gruneck L, Gentekaki E et al (2021) The salivary microbiota of Thai adults with metabolic disorders and association with diet. Arch Oral Biol 122:105036. https://doi.org/10.1016/j.archoralbio.2020.105036

    Article  PubMed  Google Scholar 

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Funding

This work was supported by the State of São Paulo Research Foundation (FAPESP, SP, Brazil, grants number 2016/10940-9, 2017/26400-6 and 2020/16020-4) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/financial code 001 - scholarship). The funding sources were not involved in the data collection, analysis, and interpretation; neither in the manuscript writing and in the decision to submit it for publication.

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Authors and Affiliations

Authors

Contributions

Aianne Souto Pizzolato Ribeiro: design of methodology, formal analysis, investigation, data curation, writing—original draft preparation;

Maria Carolina Salomé Marquezin: conceptualization, design of methodology, investigation, data curation, project administration, writing—review and editing;

Elisane Rossin Pessotti Pacheco: investigation, resources, data curation, visualization, project administration, writing—review and editing;

Irineu Rasera Jr: investigation, resources, visualization, project administration, writing—review and editing;

Marlise Inês Klein: conceptualization, design of methodology, formal analysis, visualization, writing—review and editing;

Suzan Pantaroto de Vasconcellos: conceptualization, design of methodology, formal analysis, writing—original draft preparation, visualization, writing—review and editing;

Richardt Gama Landgraf: Investigation, resources, data curation, writing—review and editing;

Debora Okamoto: design of methodology, investigation, data curation, visualization, writing—review and editing;

Leandro Augusto Calixto: design of methodology, investigation, data curation, visualization, writing—review and editing;

Paula Midori Castelo: conceptualization, formal analysis, resources, writing—original draft preparation, supervision, funding acquisition.

Corresponding author

Correspondence to Paula Midori Castelo.

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Ethical approval

This study was approved by the Research Ethics Committee of the Universidade Federal de São Paulo (CAAE 78018517.1.0000.5505). All procedures performed were in accordance with the ethical standards of the institutional and national research committees and with the latest version of the Helsinki Declaration.

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Written free and informed consent was obtained from all participants included in the study.

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The authors declare no competing interests.

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Ribeiro, A.S.P., Marquezin, M.C.S., Pacheco, E.R.P. et al. Bypass gastroplasty impacts oral health, salivary inflammatory biomarkers, and microbiota: a controlled study. Clin Oral Invest 27, 4735–4746 (2023). https://doi.org/10.1007/s00784-023-05101-3

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