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Gender-associated differences in oral microbiota and salivary biochemical parameters in response to feeding

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Abstract

Saliva plays a key role in food absorption and digestion mainly due to both its enzymes and microbiota. The main objective of this study was to compare the oral microbiota and salivary parameters between men and women in response to feeding. To answer this question, we set up a pilot study on 10 male and 10 female subjects to examine the role of saliva in glycaemia physiology. Biological parameters and the microbiotal composition of saliva were analyzed in fasted and fed states. The results show that the level of blood glucose was not different between men and women in the fasted state (88.00 mg/dL ± 6.38 vs 87.00 mg/dL ±8.07, p = 0.9149) or in the fed state (102.44 mg/dL ± 14.03 vs 116.9 mg/dL ± 25, p = 0.1362). Free fatty acids (FFA 0.15 mmol/L ± 0.15 vs 0.07 mmol/L ± 0.07, p = 0,0078), cholesterol (0.53 mmol/L ± 0.30 vs 0.15 mmol/L ± 0.14, p < 0.0001), and total saliva proteins (13.2 g/L ± 4.31 vs 9.02 g/L ± 6.98, p = 0.0168) were decreased after feeding, as well as the saliva lipase (27.89 U/L ± 25.7 vs 12.28 U/L ± 4.85, p = 0.0126). A very significant increase in the relative abundance of Streptococcaceae (24.56 ± 9.32 vs 13.53 ± 7.47, p = 0.00055) and a decrease in Prevotellaceae (34.45 ± 9.30 vs 17.43 ± 9.03, p = 0.00055) were observed in the fed condition. When investigating gender-related differences in the fasted state, men showed higher levels of cholesterol (0.71 mmol/L ± 0.26 vs 0.40 mmol/L ± 0.27, p = 0.0329), FFA (0.25 mmol/L ± 0.18 vs 0.08 mmol/L ± 0.06, p = 0.0049), and triglycerides (0.24 mmol/L ± 0.15 vs 0.09 mmol/L ± 0.04, p = 0.006) than women. Finally, differences could be observed in saliva microbiota between men and women in the fasted condition but even more in the fed condition, where Porphyromonas and Capnocytophaga were overrepresented in the male salivary samples compared with female saliva. Thus, biological parameters and microbiota in saliva could be the signatures of the feeding conditions and sex gender status.

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References

  1. Ansari-Pour N, Jafari M (2019) Why, when and how to adjust your P values? Cell J 20(4):604–607

    PubMed  Google Scholar 

  2. Beale AL, Kaye DM, Marques FZ (2019) The role of the gut microbiome in sex differences in arterial pressure. Biol Sex Differ 10:22. https://doi.org/10.1186/s13293-019-0236-8

    Article  PubMed  PubMed Central  Google Scholar 

  3. Blasco-Baque V, Coupe B, Fabre A, Handgraaf S, Gourdy P, Arnal JF, Courtney M, Schuster-Klein C, Guardiola B, Terce F, Burcelin R, Serino M (2017) Associations between hepatic miRNA expression, liver triacylglycerols and gut microbiota during metabolic adaptation to high-fat diet in mice. Diabetologia 60:690–700. https://doi.org/10.1007/s00125-017-4209-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Blasco-Baque V, Garidou L, Pomie C, Escoula Q, Loubieres P, Le Gall-David S, Lemaitre M, Nicolas S, Klopp P, Waget A, Azalbert V, Colom A, Bonnaure-Mallet M, Kemoun P, Serino M, Burcelin R (2017) Periodontitis induced by Porphyromonas gingivalis drives periodontal microbiota dysbiosis and insulin resistance via an impaired adaptive immune response. Gut 66:872–885. https://doi.org/10.1136/gutjnl-2015-309897

    Article  CAS  PubMed  Google Scholar 

  5. Bollero P, Di Renzo L, Franco R, Rampello T, Pujia A, Merra G, De Lorenzo A, Docimo R (2017) Effects of new probiotic mouthwash in patients with diabetes mellitus and cardiovascular diseases. Eur Rev Med Pharmacol Sci 21:5827–5836. https://doi.org/10.26355/eurrev_201712_14031

    Article  CAS  PubMed  Google Scholar 

  6. Burcelin R, Serino M, Chabo C, Blasco-Baque V, Amar J (2011) Gut microbiota and diabetes: from pathogenesis to therapeutic perspective. Acta Diabetol 48:257–273. https://doi.org/10.1007/s00592-011-0333-6

    Article  PubMed  PubMed Central  Google Scholar 

  7. Champagne NYC, Oetjen JA, Riché EL, Beck JD, Offenbacher S (2009) Gender differences in systemic inflammation and atheroma formation following Porphyromonas Gingivalis infection in heterozygous apolipoprotein E-deficient mice. J Periodontal Res 44(5):569–577

    Article  CAS  PubMed  Google Scholar 

  8. Cani PD, Neyrinck AM, Fava F, Knauf C, Burcelin RG, Tuohy KM, Gibson GR, Delzenne NM (2007) Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50:2374–2383. https://doi.org/10.1007/s00125-007-0791-0

    Article  CAS  PubMed  Google Scholar 

  9. Chan EC, McLaughlin R (2000) Taxonomy and virulence of oral spirochetes. Oral Microbiol Immunol 15:1–9

    Article  CAS  PubMed  Google Scholar 

  10. Clegg DJ, Mauvais-Jarvis F (2018) An integrated view of sex differences in metabolic physiology and disease. Mol Metab 15:1–2. https://doi.org/10.1016/j.molmet.2018.06.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. de Toro-Martin J, Arsenault BJ, Despres JP, Vohl MC (2017) Precision nutrition: a review of personalized nutritional approaches for the prevention and management of metabolic syndrome. Nutrients 9. https://doi.org/10.3390/nu9080913

  12. Drazewski D, Grzymislawska M, Korybalska K, Czepulis N, Grzymislawski M, Witowski J, Surdacka A (2017) Oral health status of patients with Lysosomal storage diseases in Poland. Int J Environ Res Public Health 14. https://doi.org/10.3390/ijerph14030281

  13. Leadbetter ER, Holt SC, Socransky SS (1979) Capnocytophaga: new genus of gram-negative gliding Bacteria. I. General characteristics, taxonomic considerations and significance. Arch Microbiol 122(1):9–16. https://doi.org/10.1007/BF00408040

    Article  CAS  PubMed  Google Scholar 

  14. Edgar Ricardo Vázquez-Martínez EG-G, Camacho-Arroyo I, González-Pedrajo B (2018) Sexual dimorphism in bacterial infections. Biol Sex Differ 9(1). https://doi.org/10.1186/s13293-018-0187-5

  15. Escudié FAL, Bernard M, Mariadassou M, Cauquil L, Vidal K, Maman S, Hernandez-Raquet G, Combes S, Pascal G (2018) FROGS: find, rapidly, OTUs with Galaxy Solution. Bioinformatics 34:1287–1294. https://doi.org/10.1093/bioinformatics/btx791

    Article  CAS  PubMed  Google Scholar 

  16. Goodson JMHM, Shi P, Hasturk H, Yaskell T, Vargas J, Song X, Cugini M, Barake R, Alsmadi O, Al-Mutawa S, Ariga J, Soparkar P, Behbehani J, Behbehani K (2017) The salivary microbiome is altered in the presence of a high salivary glucose concentration. PLoS One 35:9–15. https://doi.org/10.1371/journal.pone.0170437

    Article  CAS  Google Scholar 

  17. Hamosh MGD, Hamosh P (1979) Rat lingual lipase. Characteristics of enzyme activity. J Biol Chem 254(23):12121–12125

    Article  CAS  PubMed  Google Scholar 

  18. Hamosh M, Scow RO (1973) Lingual lipase and its role in the digestion of dietary lipid. J Clin Invest 52:88–95. https://doi.org/10.1172/JCI107177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Hodes GE, Epperson CN (2019) Sex differences in vulnerability and resilience to stress across the life span. Biol Psychiatry 86:421–432. https://doi.org/10.1016/j.biopsych.2019.04.028

    Article  PubMed  PubMed Central  Google Scholar 

  20. Holde GE, Oscarson N, Trovik TA, Tillberg A, Jonsson B (2017) Periodontitis prevalence and severity in adults: a cross-sectional study in Norwegian circumpolar communities. J Periodontol 88:1–17. https://doi.org/10.1902/jop.2017.170164

    Article  Google Scholar 

  21. Huebschmann AG, Huxley RR, Kohrt WM, Zeitler P, Regensteiner JG, Reusch JEB (2019) Sex differences in the burden of type 2 diabetes and cardiovascular risk across the life course. Diabetologia 62:1761–1772. https://doi.org/10.1007/s00125-019-4939-5

    Article  PubMed  PubMed Central  Google Scholar 

  22. Abranches LZJ, Kajfasz JK, Palmer SR, Chakraborty B, Wen ZT, Richards VP, Brady LJ, Lemos JA (2018) Biology of Oral Streptococci. Microbiol Spectr (5):10. https://doi.org/10.1128/microbiolspec.GPP3-0042-2018

  23. Janice M, Yoshizawa CAS, Schafer JJ, Farrell JJ, Paster BJ, Wong DTW (2013) Salivary biomarkers: toward future clinical and diagnostic utilities. Clin Microbiol Rev 26(4):781–791

    Article  Google Scholar 

  24. Kahrstrom CT, Pariente N, Weiss U (2016) Intestinal microbiota in health and disease. Nature 535:47. https://doi.org/10.1038/535047a

    Article  CAS  PubMed  Google Scholar 

  25. Karjalainen S, Sewon L, Soderling E, Larsson B, Johansson I, Simell O, Lapinleimu H, Seppanen R (1997) Salivary cholesterol of healthy adults in relation to serum cholesterol concentration and oral health. J Dent Res 76:1637–1643. https://doi.org/10.1177/00220345970760100401

    Article  CAS  PubMed  Google Scholar 

  26. Khaled Hamden SC, Boujbiha MA, Lajmi S, Aloulou D, Kchaou D, Elfeki A (2008) Hyperglycaemia, stress oxidant, liver dysfunction and histological changes in diabetic male rat pancreas and liver: protective effect of 17 Beta-estradiol. Steroids 73(5):495–501. https://doi.org/10.1016/j.steroids.2007.12.026

    Article  CAS  PubMed  Google Scholar 

  27. Lakhssassi N, Elhajoui N, Lodter JP, Pineill JL, Sixou M (2005) Antimicrobial susceptibility variation of 50 anaerobic periopathogens in aggressive periodontitis: an interindividual variability study. Oral Microbiol Immunol 20:244–252. https://doi.org/10.1111/j.1399-302X.2005.00225.x

    Article  CAS  PubMed  Google Scholar 

  28. Ley REBF, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 102(31):11070–11075. https://doi.org/10.1073/pnas.0504978102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Li BGY, Cheng L, Zeng B, Yu J, Peng X, Zhao J, Li W, Ren B, Li M, Wei H, Zhou X (2019) Oral bacteria colonize and compete with gut microbiota in gnotobiotic mice. Int J Oral Sci 11:1–10. https://doi.org/10.1038/s41368-018-0043-9

    Article  Google Scholar 

  30. Madonna R, Balistreri CR, De Rosa S, Muscoli S, Selvaggio S, Selvaggio G, Ferdinandy P, De Caterina R (2019) Impact of sex differences and diabetes on coronary atherosclerosis and ischemic heart disease. J Clin med 8doi. https://doi.org/10.3390/jcm8010098

  31. Mannoor MS, Tao H, Clayton JD, Sengupta A, Kaplan DL, Naik RR, Verma N, Omenetto FG, McAlpine MC (2012) Graphene-based wireless bacteria detection on tooth enamel. Nat Commun 3:763. https://doi.org/10.1038/ncomms1767

    Article  CAS  PubMed  Google Scholar 

  32. Minty M, Canceill T, Le S, Dubois P, Amestoy O, Loubieres P, Christensen JE, Champion C, Azalbert V, Grasset E, Hardy S, Loubes JM, Mallet JP, Terce F, Vergnes JN, Burcelin R, Serino M, Diemer F, Blasco-Baque V (2018) Oral health and microbiota status in professional rugby players: a case-control study. J Dent 79:53–60. https://doi.org/10.1016/j.jdent.2018.10.001

    Article  PubMed  Google Scholar 

  33. Morzel M, Truntzer C, Neyraud E, Brignot H, Ducoroy P, Lucchi G, Canlet C, Gaillard S, Nicod F, Nicklaus S, Peretti N, Feron G (2017) Associations between food consumption patterns and saliva composition: specificities of eating difficulties children. Physiol Behav 173:116–123. https://doi.org/10.1016/j.physbeh.2017.02.005

    Article  CAS  PubMed  Google Scholar 

  34. Nicholas S, Jakubovics SAY, Rickard AH (2014) Community interactions of oral streptococci. Adv Appl Microbiol 87:43–110. https://doi.org/10.1016/B978-0-12-800261-2.00002-5

    Article  CAS  Google Scholar 

  35. Nicolas S, Blasco-Baque V, Fournel A, Gilleron J, Klopp P, Waget A, Ceppo F, Marlin A, Padmanabhan R, Iacovoni JS, Terce F, Cani PD, Tanti JF, Burcelin R, Knauf C, Cormont M, Serino M (2017) Transfer of dysbiotic gut microbiota has beneficial effects on host liver metabolism. Mol Syst Biol 13:921. https://doi.org/10.15252/msb.20167356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Ortiz S, Herrman E, Lyashenko C, Purcell A, Raslan K, Khor B, Snow M, Forsyth A, Choi D, Maier T, Machida CA (2019) Sex-specific differences in the salivary microbiome of caries-active children. J Oral Microbiol 11:1653124. https://doi.org/10.1080/20002297.2019.1653124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Palmerini CA, Saccardi C, Ferracci F, Arienti S (2011) Lipid patterns in the saliva of smoking young adults. Hum Exp Toxicol 30:1482–1488. https://doi.org/10.1177/0960327111398672

    Article  CAS  PubMed  Google Scholar 

  38. Pedersen ASC, Proctor GB, Carpenter GH (2018) Salivary functions in mastication, taste and textural perception, swallowing and initial digestion. Oral Dis 24:1399–1416. https://doi.org/10.1111/odi.12867

    Article  PubMed  Google Scholar 

  39. Redekop WK, Mladsi D (2013) The faces of personalized medicine: a framework for understanding its meaning and scope. Value Health 16:S4–S9. https://doi.org/10.1016/j.jval.2013.06.005

    Article  PubMed  Google Scholar 

  40. Robinson DS, Speake BK (1989) Role of insulin and other hormones in the control of lipoprotein lipase activity. Biochem Soc Trans 17:40–42. https://doi.org/10.1042/bst0170040

    Article  CAS  PubMed  Google Scholar 

  41. Sayaka Katagiri TS, Tohara H, Yamaguchi K, Hara K, Nakagawa K, Komatsu K, Watanabe K, Ohsugi Y, Maekawa S, Iwata T (2019) Re-initiation of oral food intake following enteral nutrition alters oral and gut microbiota communities. Front Cell Infect Microbiol 9:434. https://doi.org/10.3389/fcimb.2019.00434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. https://doi.org/10.1186/gb-2011-12-6-r60

    Article  PubMed  PubMed Central  Google Scholar 

  43. Snell DM, Turner JMA (2018) Sex chromosome effects on male-female differences in mammals. Curr Biol 28:R1313–R1324. https://doi.org/10.1016/j.cub.2018.09.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Subramaniam P, Sharma A, Kaje K (2015) Association of salivary triglycerides and cholesterol with dental caries in children with type 1 diabetes mellitus. Spec Care Dentist 35:120–122. https://doi.org/10.1111/scd.12097

    Article  PubMed  Google Scholar 

  45. Thomas FHJ, Rebuffet E, Czjzek M, Michel G (2011) Environmental and gut bacteroidetes: the food connection. Front Microbiol 30. https://doi.org/10.3389/fmicb.2011.00093

  46. Vari R, Scazzocchio B, D'Amore A, Giovannini C, Gessani S, Masella R (2016) Gender-related differences in lifestyle may affect health status. Ann Ist Super Sanita 52:158–166. https://doi.org/10.4415/ANN_16_02_06

    Article  PubMed  Google Scholar 

  47. Villanueva-Millan MJ, Perez-Matute P, Oteo JA (2015) Gut microbiota: a key player in health and disease. A review focused on obesity. J Physiol Biochem 71:509–525. https://doi.org/10.1007/s13105-015-0390-3

    Article  CAS  PubMed  Google Scholar 

  48. Voigt N, Stein J, Galindo MM, Dunkel A, Raguse JD, Meyerhof W, Hofmann T, Behrens M (2014) The role of lipolysis in human orosensory fat perception. J Lipid Res 55:870–882. https://doi.org/10.1194/jlr.M046029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP, Initiative S (2014) The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Int J Surg 12:1495–1499. https://doi.org/10.1016/j.ijsu.2014.07.013

    Article  Google Scholar 

  50. W.M M (2014) Definitions of quality of life: what has happened and how to move on. Top Spinal Cord Inj Rehabil 20(3):167–180. doi: https://doi.org/10.1310/sci2003-167

  51. Wong DT (2006) Towards a simple, saliva-based test for the detection of oral cancer 'oral fluid (saliva), which is the mirror of the body, is a perfect medium to be explored for health and disease surveillance'. Expert Rev Mol Diagn 6:267–272. https://doi.org/10.1586/14737159.6.3.267

    Article  PubMed  Google Scholar 

  52. Zaura E BB, Teixeira de Mattos MJ, Buijs MJ, Caspers MP, Rashid MU, Weintraub A, Nord CE, Savell A, Hu Y, Coates AR, Hubank M, Spratt DA, Wilson M, Keijser BJ, Crielaard W. (2015) Same Exposure but Two Radically Different Responses to Antibiotics: Resilience of the Salivary Microbiome versus Long-Term Microbial Shifts in Feces. mbio

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Acknowledgements

We would also like to show our gratitude to the technical staff of Vaiomer for sequencing and taxonomic analysis for oral microbiota and Anexplo platform for biochemistry analysis of saliva and blood.

We thank Dr. Adrian Minty for his comments for editing the English.

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Correspondence to V. Blasco-Baque.

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Key points

1. Feeding modified the salivary biological parameters of saliva.

2. The oral microbiota was also modified after feeding.

3. The sex gender was associated with a particular “signature” of oral microbiota in fed and fasted conditions.

4. Saliva showed differences in both microbiota composition and biological parameters between males and females.

Electronic supplementary material

ESM 1

Linear correlation between the glycaemic fold change and oral microbiota. Linear correlation tests were performed using GraphPad Prism (GraphPad Software. San Diego. CA) for finding statistical relationships between the glycaemic fold change (the ratio fed glycaemia/ fasted glycaemia): (A) and the Bacteroidetes fold change, (B) and the Firmicutes fold change, (C) and the Prevotellacae fold change, (D) and the Streptococcaceae fold change, (E) and the Oribacterium fold change.) (JPG 3375 kb)

ESM 2

Linear correlation between the glycaemic fold change and lipase fold change. Linear correlation tests were performed using GraphPad Prism (GraphPad Software. San Diego. CA) for finding statistical relationships between the glycaemic fold change (the ratio fed glycaemia/ fasted glycaemia) and lipase fold change. (JPG 707 kb)

ESM 3

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Minty, M., Loubières, P., Canceill, T. et al. Gender-associated differences in oral microbiota and salivary biochemical parameters in response to feeding. J Physiol Biochem 77, 155–166 (2021). https://doi.org/10.1007/s13105-020-00757-x

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