Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Pediatrics

Comparison of salivary proteome of children with different sensitivities for bitter and sweet tastes: association with body mass index

International Journal of Obesity volume 43, pages 701–712 (2019)Cite this article

Subjects

Abstract

Background/objectives

Oral sensorial perception is a key aspect in food choices and knowing the mechanisms modulating such perception is of major importance in the context of child obesity, which is reaching high rates in Mediterranean countries. Salivary proteome has been linked to taste sensitivity in adults. The aim of this study was to search for differences in salivary proteomes of children with different bitter or sweet taste sensitivities and to assess if these potential differences are associated with their body mass index percentile (BMI percentile).

Subjects/methods

387 children aged 8–9 years old were assessed for BMI percentile and classified according to their sensitivity to bitter and sweet tastes, according to their caffeine and sucrose detection thresholds, respectively. Saliva protein composition was compared among taste sensitivity groups, taking into account BMI percentile and gender, using gel-based proteomics approaches, coupled to mass spectrometry for protein identification.

Results

Among the salivary proteins related to bitter taste sensitivity, higher levels of cystatins were observed in bitter-sensitive children, in the case of those of normal weight, and in bitter low-sensitive, in the case of overweight children. For sweetness, the relationship between saliva and taste perception was also dependent on BMI percentile, with several proteins (including salivary cystatins) differing between taste sensitivity groups, with disparities arising between normal-weight and overweight children. Cystatin isoforms A, B and SA were observed to be considerably increased in saliva from obese children.

Conclusions

Salivary proteome is related with sensitivities to bitter and sweet tastes in children, but the association is dependent on BMI percentile and gender.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Wijnhoven TM, Van Raaij JM, Spinelli A, Starc G, Hassapidou M, Spiroski I et al. WHO European Childhood Obesity Surveillance Initiative: body mass index and level of overweight among 6-9-year-old children from school year 2007/2008 to school year 2009/2010. BMC Public Health. 2014. https://doi.org/10.1186/1471-2458-14-806.

  2. WHO. Downward trend in overweight and obesity among Portuguese school children. 2018. http://www.euro.who.int/en/health-topics/disease-prevention/nutrition/news/news/2018/2/downward-trend-in-overweight-and-obesity-among-portuguese-school-children (accessed 12 Jun2018).

  3. Lamy E, Pinheiro C, Rodrigues L, Capela e Silva F, Lopes OS, Tavares S et al. Determinants of tannin-rich food and beverage consumption: Oral perception vs. psychosocial aspects. 2016.

  4. Drewnowski A, Gomez-Carneros C Bitter taste, phytonutrients, and the consumer: A review. Am. J. Clin. Nutr. 2000. https://doi.org/10.1111/j.1750-3841.2011.02471.x.

    Article  Google Scholar 

  5. Bell KI, Tepper BJ. Short-term vegetable intake by young children classified by 6-n-propylthoiuracil bitter-taste phenotype. Am. J. Clin. Nutr. 2006;245–51.

    Article  CAS  Google Scholar 

  6. Keller KL, Adise S. Variation in the ability to taste bitter thiourea compounds: implications for food acceptance, dietary intake, and obesity risk in children. Annu Rev Nutr 2016. https://doi.org/10.1146/annurev-nutr-071715-050916.

    Article  CAS  Google Scholar 

  7. Kildegaard H, Tønning E, Thybo AK. Preference, liking and wanting for beverages in children aged 9-14years: role of sourness perception, chemical composition and background variables. Food Qual Prefer 2011. https://doi.org/10.1016/j.foodqual.2011.03.005.

    Article  Google Scholar 

  8. Joseph PV, Reed DR, Mennella JA. Individual differences among children in sucrose detection thresholds: relationship with age, gender, and bitter taste genotype. Nurs Res 2016. https://doi.org/10.1097/NNR.0000000000000138.

  9. Barbarossa IT, Melis M, Mattes MZ, Calò C, Muroni P, Crnjar R, et al. The gustin (CA6) gene polymorphism, rs2274333 (A/G), is associated with fungiform papilla density, whereas PROP bitterness is mostly due to TAS2R38 in an ethnically-mixed population. Physiol Behav. 2015;138:6–12.

    Article  CAS  Google Scholar 

  10. Dsamou M, Palicki O, Septier C, Chabanet C, Lucchi G, Ducoroy P, et al. Salivary protein profiles and sensitivity to the bitter taste of caffeine. Chem Senses. 2012;37:87–95.

    Article  CAS  Google Scholar 

  11. Cabras T, Melis M, Castagnola M, Padiglia A, Tepper BJ, Messana I, et al. Responsiveness to 6-n-propylthiouracil (PROP) is associated with salivary levels of two specific basic proline-rich proteins in humans. PLoS ONE. 2012;7:e30962.

    Article  CAS  Google Scholar 

  12. Rodrigues L, da Costa G, Cordeiro C, Pinheiro CC, Amado F, Lamy E. Relationship between saliva protein composition and 6-n-Propylthiouracil bitter taste responsiveness in young adults. J Sens Stud. 2017; 32. https://doi.org/10.1111/joss.12275.

    Article  Google Scholar 

  13. Rodrigues L, Costa G, Cordeiro C, Pinheiro C, Amado F, Lamy E. Salivary proteome and glucose levels are related with sweet taste sensitivity in young adults. Food Nutr Res. 2017;61:1389208.

    Article  CAS  Google Scholar 

  14. Stolle T, Grondinger F, Dunkel A, Meng C, Médard G, Kuster B et al. Salivary Proteome Patterns Affecting Human Salt Taste Sensitivity. J Agric Food Chem. 2017. https://doi.org/10.1021/acs.jafc.7b03862.

    Article  CAS  Google Scholar 

  15. Morzel M, Chabanet C, Schwartz C, Lucchi G, Ducoroy P, Nicklaus S. Salivary protein profiles are linked to bitter taste acceptance in infants. Eur J Pediatr. 2014;173:575–82.

    Article  CAS  Google Scholar 

  16. Rodrigues L, Espanca R, Costa AR, Antunes CM, Pomar C, Capela-Silva F et al. Association between salivary leptin levels and taste perception in children. J Nutr Metab 2017; 2017. https://doi.org/10.1155/2017/7260169.

    Article  Google Scholar 

  17. Tepper BJ, Melis M, Koelliker Y, Gasparini P, Ahijevych KL, Barbarossa IT. Factors influencing the phenotypic characterization of the oral marker, PROP. Nutrients. 2017. https://doi.org/10.3390/nu9121275.

    Article  Google Scholar 

  18. Lamy E, Simões C, Rodrigues L, Costa AR, Vitorino R, Amado F, et al. Changes in the salivary protein profile of morbidly obese women either previously subjected to bariatric surgery or not. J Physiol Biochem. 2015;71:691–702.

    Article  CAS  Google Scholar 

  19. LAEMMLI UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–5.

    Article  Google Scholar 

  20. Rodrigues L, da Costa G, Cordeiro C, Pinheiro CC, Amado F, Lamy E. Relationship between saliva protein composition and 6- n -Propylthiouracil bitter taste responsiveness in young adults. J Sens Stud 2017: e12275.

    Article  Google Scholar 

  21. Rodrigues L, Mouta R, Costa AR, Pereira A, Capela e Silva F, Amado F, et al. Effects of high fat diet on salivary α-amylase, serum parameters and food consumption in rats. Arch Oral Biol. 2015;60:854–62.

    Article  Google Scholar 

  22. Pallaro A, Barbeito S, Taberner P, Marino P, Franchello A, Strasnoy I, et al. Total salivary IgA, serum C3c and IgA in obese school children. J Nutr Biochem. 2002;13:539–42.

    Article  CAS  Google Scholar 

  23. Baron AC, DeCarlo AA, Featherstone JDB. Functional aspects of the human salivary cystatins in the oral environment. Oral Dis 1999. https://doi.org/10.1111/j.1601-0825.1999.tb00307.x.

    Article  Google Scholar 

  24. Lafarge JC, Naour N, Clément K, Guerre-Millo M. Cathepsins and cystatin C in atherosclerosis and obesity. Biochimie. 2010. https://doi.org/10.1016/j.biochi.2010.04.011.

    Article  CAS  Google Scholar 

  25. Yang M, Sun J, Zhang T, Liu J, Zhang J, Shi MA et al. Deficiency and inhibition of cathepsin K reduce body weight gain and increase glucose metabolism in mice. Arterioscler Thromb Vasc Biol 2008. https://doi.org/10.1161/ATVBAHA.108.172320.

    Article  CAS  Google Scholar 

  26. Wasen E, Isoaho R, Mattila K, Vahlberg T, Kivela S-L, Irjala K. Serum cystatin C in the aged: relationships with health status. Am J Kidney Dis. 2003.

  27. Luc G, Bard JM, Lesueur C, Arveiler D, Evans A, Amouyel P et al. Plasma cystatin-C and development of coronary heart disease: The PRIME Study. Atherosclerosis. 2006;375–80. https://doi.org/10.1016/j.atherosclerosis.2005.06.017.

    Article  CAS  Google Scholar 

  28. Veerman EC, van den Keybus PA, Vissink A, Nieuw Amerongen AV. Human glandular salivas: their separate collection and analysis. Eur J Oral Sci. 1996;104:346–52.

    Article  CAS  Google Scholar 

  29. Dickinson DP. Salivary (SD-type) cystatins: over one billion years in the making—but to what purpose? Crit. Rev. Oral Biol. Med. 2002. https://doi.org/10.1177/154411130201300606.

    Article  CAS  Google Scholar 

  30. Morzel M, Neyraud E, Brignot H, Ducoroy P, Jeannin A, Lucchi G et al. Multi-omics profiling reveals that eating difficulties developed consecutively to artificial nutrition in the neonatal period are associated to specific saliva composition. J Proteomics. 2015. https://doi.org/10.1016/j.jprot.2015.07.028.

    Article  CAS  Google Scholar 

  31. Shatzman AR, Henkin RI. Gustin concentration changes relative to salivary zinc and taste in humans. Proc Natl Acad Sci USA. 1981;78:3867–71.

    Article  CAS  Google Scholar 

  32. Henkin RI, Martin BM, Agarwal RP. Efficacy of exogenous oral zinc in treatment of patients with carbonic anhydrase VI deficiency. Am J Med Sci. 1999. https://doi.org/10.1097/00000441-199912000-00006.

    Article  CAS  Google Scholar 

  33. Feeney EL, Hayes JE. Exploring associations between taste perception, oral anatomy and polymorphisms in the carbonic anhydrase (gustin) gene CA6. Physiol Behav. 2014;128:148–54.

    Article  CAS  Google Scholar 

  34. Sivakumar T, Hand AR, Mednieks M. Secretory proteins in the saliva of children. J Oral Sci. 2009. https://doi.org/10.2334/josnusd.51.573.

    Article  CAS  Google Scholar 

  35. Yang ZM, Chen LH, Zhang M, Lin J, Zhang J, Chen WW et al. Age differences of salivary alpha-amylase levels of basal and acute responses to citric acid stimulation between chinese children and adults. Front Physiol. 2015. https://doi.org/10.3389/fphys.2015.00340.

  36. James CE, Laing DG, Oram N. A comparison of the ability of 8-9-Year-old children and adults to detect taste stimuli. Physiol Behav. 1997. https://doi.org/10.1016/S0031-9384(97)00030-9.

    Article  CAS  Google Scholar 

  37. Lorenz K, Bader M, Klaus A, Weiss W, Görg A, Hofmann T. Orosensory stimulation effects on human saliva proteome. J Agric Food Chem. 2011. https://doi.org/10.1021/jf2024352.

    Article  CAS  Google Scholar 

  38. Santos JL, Saus E, Smalley SV, Cataldo LR, Alberti G, Parada J, et al. Copy number polymorphism of the salivary amylase gene: implications in human nutrition research. J Nutr Nutr. 2012;5:117–31.

    CAS  Google Scholar 

  39. Lima DP, Diniz DG, Moimaz SAS, Sumida DH, Okamoto AC. Saliva: reflection of the body. Int J Infect Dis. 2010;14:e184–e188.

    Article  Google Scholar 

  40. Butchibabu K, Kiran K, Koppolu P, Kumar S, Muralikrishna T, Swaminathan M. Estimation of salivary immunoglobulin A levels in gingivitis and chronic periodontitis patients before and after phase I periodontal therapy. J Dr NTR Univ Heal Sci. 2014;3:23.

    Article  Google Scholar 

Download references

Acknowledgements

This paper was supported by national funding from the Portuguese Science Foundation (FCT) under the project UID/AGR/00115/2013 (ICAAM – University of Évora). The authors also acknowledge financial support from FCT in the form of Elsa Lamy’s FCT investigator contract IF/01778/2013. FCT played no role in the development of this work or in its submission for publication.

Author information

Authors and Affiliations

  1. Institute of Mediterranean Agricultural and Environmental Sciences (ICAAM), University of Évora, Évora, Portugal

    Lénia Rodrigues & Elsa Lamy

  2. Grouping of Health Centres of Central Alentejo (ACES, AC), Évora, Portugal

    Rosa Espanca

  3. Institute of Earth Sciences (ICT), Institute of Mediterranean Agricultural and Environmental Sciences (ICAAM) and Department of Chemistry, University of Évora, Évora, Portugal

    Ana Rodrigues Costa & Célia Miguel Antunes

  4. Centre of Research in Education and Psychology (CIEP) and Department of Pedagogy and Education, University of Évora, Évora, Portugal

    Clarinda Pomar

  5. Institute of Mediterranean Agricultural and Environmental Sciences (ICAAM) and Department of Biology, University of Évora, Évora, Portugal

    Fernando Capela-Silva

  6. Institute of Mediterranean Agricultural and Environmental Sciences (ICAAM) and Department of Zootechnics, University of Évora, Évora, Portugal

    Cristina Conceição Pinheiro

  7. Organic Chemistry, Natural and Agrofood Products (QOPNA) and Department of Chemistry, University of Aveiro, Aveiro, Portugal

    Pedro Domingues & Francisco Amado

Authors
  1. Lénia Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rosa Espanca
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ana Rodrigues Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Célia Miguel Antunes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Clarinda Pomar
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fernando Capela-Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cristina Conceição Pinheiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Pedro Domingues
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Francisco Amado
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Elsa Lamy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Francisco Amado or Elsa Lamy.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rodrigues, L., Espanca, R., Costa, A.R. et al. Comparison of salivary proteome of children with different sensitivities for bitter and sweet tastes: association with body mass index. Int J Obes 43, 701–712 (2019). https://doi.org/10.1038/s41366-018-0289-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41366-018-0289-5

This article is cited by

Search

Advanced search

Quick links