Skip to main content

Advertisement

Log in

The Association Between Some Macro and Trace Elements in Saliva and Periodontal Status

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Changes in the macro and trace element composition of saliva might be indicative for pathological changes in periodontal tissues. However, there is a lack of evidence in the literature showing associations between mineral elements and periodontal status. The aim of this study was to determine whether such associations occur. Totally, 190 systemically healthy non-smoker participants (mean age 32.2 ± 6.02; 50 periodontally healthy, 50 gingivitis, 50 chronic periodontitis, and 40 aggressive periodontitis individuals) were included in this cross-sectional study. Salivary levels of some macro and trace elements were measured by using inductively coupled plasma mass spectrometry (ICP-MS). Kruskal-Wallis’s test was used for statistical analysis. Statistically significant differences were found in sodium (Na), magnesium (Mg), potassium (K), calcium (Ca), vanadium (V), chromium Cr), manganese (Mn), iron (Fe), rubidium (Rb), strontium (Sr), and selenium (Se) concentrations among the groups. Significant increases in the essential minerals Na, Mg, K, Ca, Fe, and Se occurred in both periodontitis groups when compared to the gingivitis and periodontally healthy groups. Lower Se, Sr, Fe, Mn, and V concentrations were found in the aggressive periodontitis group than in the chronic periodontitis group. The results of this study demonstrated that assessment of mineral element concentrations in saliva might be useful in assessing periodontal health and disease. However, further studies are required to determine whether the change in a specific mineral element is the result of periodontal disease or is involved in its pathogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Berezow AB, Darveau RP (2011) Microbial shift and periodontitis. Periodontol 55:36–47

    Google Scholar 

  2. Cullinan MP, Seymour GJ (2013) Periodontal disease and systemic illness: will the evidence ever be enough? Periodontol 62:271–286

    Google Scholar 

  3. Bartold PM, Van Dyke TE (2013) Periodontitis: a host-mediated disruption of microbial homeostasis. Unlearning learned concepts. Periodontol 62:203–217

    Google Scholar 

  4. Hong BY, Furtado Araujo MV, Strausbaugh LD, Terzi E, Ioannidou E, Diaz PI (2015) Microbiome profiles in periodontitis in relation to host and disease characteristics. PLoS One 10(5):e0127077. https://doi.org/10.1371/journal.pone.0127077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Giannobile WV, Beikler T, Kinney JS, Ramseier CA, Morelli T, Wong DT (2009) Saliva as a diagnostic tool for periodontal disease: current state and future directions. Periodontol 50:52–64

    Google Scholar 

  6. Bonassi S, Neri M, Puntoni R (2001) Validation of biomarkers as early predictors of disease. Mutat Res 480:349–358

    PubMed  Google Scholar 

  7. Kaufman E, Lamster IB (2000) Analysis of saliva for periodontal diagnosis-a review. J Clin Periodontol 27:453–465

    CAS  PubMed  Google Scholar 

  8. Javaid MA, Ahmed AS, Durand R, Tran SD (2015) Saliva as a diagnostic tool for oral and systemic diseases. J Oral Biol Craniofac Res 6:66–75

    PubMed  PubMed Central  Google Scholar 

  9. Gaur S, Agnihotri R (2017) Trace mineral micronutrients and chronic periodontitis-a review. Biol Trace Elem Res 176:225–238

    CAS  PubMed  Google Scholar 

  10. Jakubovics NS, Smith AW, Jenkinson HF (2002) Oxidative stress tolerance is manganese (Mn2+) regulated in Streptococcus gordonii. Microbiology 148:3255–3263

    CAS  PubMed  Google Scholar 

  11. Nizel AE, Papas AS (1989) Nutrition in Clinical Dentistry, 3rd edn. Saunders, Philadelphia

    Google Scholar 

  12. Dawson DR, Branch-Mays G, Gonzalez OA, Ebersole JL (2014) Dietary modulation of the inflammatory cascade. Periodontol 64:161–197

    Google Scholar 

  13. Ahmed T, Haboubi N (2010) Assessment and management of nutrition in older people and its importance to health. Clin Interv Aging 5:207–216

    PubMed  PubMed Central  Google Scholar 

  14. Hartman C, Eliakim R, Shamir R (2009) Nutritional status and nutritional therapy in inflammatory bowel diseases. World J Gastroenterol 7:2570–2578

    Google Scholar 

  15. Herman M, Golasik M, Piekoszewski W, Walas S, Napierala M, Wyganowska-Swiatkowska M, Kurhanska-Flisykowska A, Wozniak A, Florek E (2016) Essential and toxic metals in oral fluid-a potential role in the diagnosis of periodontal diseases. Biol Trace Elem Res 173:275–282

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Todorovic T, Dozic I, Vicente-Barrero M et al (2006) Salivary enzymes and periodontal disease. Med Oral Patol Oral Cir Bucal 11:E115–E119

    PubMed  Google Scholar 

  17. Chu M, Beauchemin D (2004) Simple method to assess the maximum bio-accessibility of elements from food using flow injection and inductively coupled plasma mass spectrometry. J Anal At Spectrom 19:1213–1216

    CAS  Google Scholar 

  18. Silness J, Löe H (1964) Periodontal disease in pregnancy II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 22:121–135

    CAS  PubMed  Google Scholar 

  19. Löe H (1967) The gingival ındex, the plaque index and the retention index systems. J Periodontol 38:610–616

    Google Scholar 

  20. Isaza-Guzmán DM, Hernández-Viana M, Bonilla-León DM, Hurtado-Cadavid MC, Tobón-Arroyave (2016) Determination of NLRP3 (rs4612666) and IL-1B (rs1143634) genetic polymorphisms in periodontally diseased and healthy subjects. Arch Oral Biol 65:44-51

  21. Armitage GC (1999) Development of a classification system for periodontal diseases and conditions. Ann Periodontol 4:1–6

    CAS  PubMed  Google Scholar 

  22. Alves C, Brandão M, Andion J, Menezes R (2010) Use of graduated syringes for measuring salivary flow rate: a pilot study. Braz Dent J 2:401–404

    Google Scholar 

  23. R Core Team (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, https://www.R-project.org/

    Google Scholar 

  24. Tomofuji T, Irie K, Sanbe T et al (2009) Periodontitis and increase in circulating oxidative stress. Japanese Dental Science Review 45:46–51

    Google Scholar 

  25. Boyd LD, Madden TE (2003) Nutrition, infection, and periodontal disease. Dental Clinics of North America 47:337–354

    PubMed  Google Scholar 

  26. Chen M, Cai W, Zhao S, Shi L, Chen Y, Li X, Sun X, Mao Y, He B, Hou Y, Zhou Y, Zhou Q, Ma J, Huang S (2019) Oxidative stress-related biomarkers in saliva and gingival crevicular fluid associated with chronic periodontitis: a systematic review and meta-analysis. J Clin Periodontol 46:608–622

    CAS  PubMed  Google Scholar 

  27. Hassona Y, Scully C (2016) Salivary changes in oral mucosal diseases. Periodontol 70:111–127

    Google Scholar 

  28. TalalAbd S, Abbas HA, Jasim HS, Fadhil NH, Gathwan KH, Obadi DH (2017) Evaluation of some salivary elements in chronic periodontitis patients. IOSR Journal of Dental and Medical Sciences 16:46–50

    Google Scholar 

  29. Júnior AAB, Pallos D, Cortelli JR, Saraceni CHC, Queiroz CS (2010) Evaluation of organic and inorganic compounds in the saliva of patients with chronic periodontal disease. Revista Odonto Ciência 25:234–238

    Google Scholar 

  30. Hung CT, Allen FD, Pollack SR, Brighton CT (1996) Intracellular Ca2 + stores and extracellular Ca2+ are required in the real-time Ca2 + response of bone cells experiencing fluid flow. J Biomech 29:1411–1417

    CAS  PubMed  Google Scholar 

  31. Shibata K, Warbington ML, Gordon BJ, Kurihara H, Van Dyke TE (2000) Defective calcium influx factor activity in neutrophils from patients with localized juvenile periodontitis. J Periodontol 71:797–802

    CAS  PubMed  Google Scholar 

  32. Watanabe N, Suzuki J, Kobayashi Y (1996) Role of calcium in tumor necrosis factor-alpha production by activated macrophages. J Biochem 120:1190–1195

    CAS  PubMed  Google Scholar 

  33. Seabra V, Stachlewitz RF, Thurman RG (1998) Taurine blunts LPS-induced increases in intracellular calcium and TNF-alpha production by Kupffer cells. J Leukoc Biol 64:615–621

    CAS  PubMed  Google Scholar 

  34. Chapple IL, Matthews JB (2007) The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 43:160–232

    Google Scholar 

  35. Chen M, Cai W, Zhao S, Shi L, Chen Y, Li X, Sun X, Mao Y, He B, Hou Y, Zhou Y, Zhou Q, Ma J, Huang S (2019) Oxidative stress-related biomarkers in saliva and gingival crevicular fluid associated with chronic periodontitis: a systematic review and meta-analysis. J Clin Periodontol 46:608–622

    CAS  PubMed  Google Scholar 

  36. Sapna G, Gokul S, Bagri-Manjrekar K (2014) Matrix metalloproteinases and periodontal diseases. Oral Dis 20:538–550

    CAS  PubMed  Google Scholar 

  37. Mauramo M, Ramseier AM, Mauramo E, Buser A, Tervahartiala T, Sorsa T, Waltimo T (2018) Associations of oral fluid MMP-8 with periodontitis in Swiss adult subjects. Oral Dis 24:449–455

    CAS  PubMed  Google Scholar 

  38. Ashley FP, Coward PY, Jalil RA, Wilson RF (1991) Relationship between calcium and inorganic phosphorus concentrations of both resting and stimulated saliva and dental plaque in children and young adults. Arch Oral Biol 36:431–434

    CAS  PubMed  Google Scholar 

  39. Acharyaa A, Kharadia MD, Dhavalea R, Deshmukha VL, Sontakkeb AN (2011) High salivary calcium level associated with periodontal disease in Indian subjects - a pilot study. Oral Health Prev Dent 9:195–200

    Google Scholar 

  40. Kuraner T, Beksac MS, Kayakirilmaz K, Cağlayan F, Onderoğlu LS, Ozgünes H (1991) Serum and parotid saliva testosterone, calcium, magnesium, and zinc levels in males, with and without periodontitis. Biol Trace Elem Res 31:43–49

    CAS  PubMed  Google Scholar 

  41. Sewón LA, Karjalainen SM, Söderling E, Lapinleimu H, Simell O (1998) Association between salivary calcium and oral health. J Clin Periodontol 25:915–919

    PubMed  Google Scholar 

  42. Sewón L, Makela M (1990) A study of possible correlation between high salivary calcium level and dental conditions in young adults. Arch Oral Biol 35:211–212

    Google Scholar 

  43. Gupta VV, Chitkara N, Gupta HV, Singh A, Gambhir RS, Kaur H (2016) Comparison of salivary calcium level and pH in patients with aggressive periodontitis and healthy individuals: a clinico -biochemical study. Oral health and dental management 15:122–126

    Google Scholar 

  44. Sevón L, Laine MA, Karjalainen S, Doroguinskaia A, Helenius H, Kiss E, Lehtonen-Veromaa M (2008) Effect of age on flow-rate, protein and electrolyte composition of stimulated whole saliva in healthy, non-smoking women. The Open Dentistry Journal 2:89–92

    PubMed  PubMed Central  Google Scholar 

  45. Kambalyal P, Kambalyal P, Hungund S (2015) Comparison of salivary calcium level in smokers and non-smokers with chronic periodontitis, aggressive periodontitis, and healthy controls. J Int Soc Prev Community Dent 5:68–S73

    Google Scholar 

  46. Rude RK, Shils ME (2006) Magnesium. In: Shils ME, Ross AC, Caballero B, Cousins RI, eds. Modern Nutrition in Health and Disease, 10th ed. Philadelphia: Lippincott Williams & Wilkins pp 223-247

  47. Manea A, Nechifor M (2014) Research on plasma and saliva levels of some bivalent cations in patients with chronic periodontitis (salivary cations in chronic periodontitis). Rev Med Chir Soc Med Nat Iasi 118:439–449

    CAS  PubMed  Google Scholar 

  48. Nielsen FH (2019) The problematic use of dietary reference intakes to assess magnesium status and clinical importance. Biol Trace Elem Res 188:52–59

    CAS  PubMed  Google Scholar 

  49. Shelty TJ, Sameer AZ, Girish S, Siddhartha V, Keshava A, Vishwajeet K (2017) A biochemical study to assess and compare salivary magnesium levels in periodontal health and diseases. J Orofac Sci 9:111–113

    Google Scholar 

  50. Manea A, Nechifor M (2014) Research on plasma and saliva levels of some bivalent cations in patients with chronic periodontitis (salivary cations in chronic periodontitis). Rev Med Chir Soc Med Nat Iasi 118:439–449

    CAS  PubMed  Google Scholar 

  51. Kaslick RS, Chasens AI, Bressman E, Lazzara R, Egitto J (1971) Investigation of periodontosis with periodontitis: ultra microanalysis of gingival fluid, gross examination of the periodontal ligament and approach to treatment. J Periodontol 42:428–434

    CAS  PubMed  Google Scholar 

  52. Kaslick RS, Chasens AI, Mandel ID, Weinstein D, Waldman R, Pluhar T (1970) Quantitative analysis of sodium, potassium and calcium in gingival fluid from gingiva in varying degrees of inflammation. J Periodontol 41:93–97

    CAS  PubMed  Google Scholar 

  53. Bang J, Cimasoni G, Rosenbusch CS, Duckert A. (1973) Sodium, potassium and calcium contents of crevicular exudate:their relations to gingivitis and periodontitis. J Periodontol 44:770–774

    CAS  PubMed  Google Scholar 

  54. Kaslick RS, Chasens AI, Mandel ID, Weinstein D, Waldman R, Pluhar T, Lazzara R (1970) Relationship of sodium, potassium and calcium to one another, to circadian rhythms, gingival bleeding, purulence and to conservative periodontal therapy. J Periodontol 41:442–448

    CAS  PubMed  Google Scholar 

  55. Aun WA (2012) Inorganic ions level in saliva of patients with chronic periodontitis and healthy subjects. J Bagh Coll Dent 24:93–73

    Google Scholar 

  56. Koregol AC, More SP, Nainegali S, Kalburgi N, Verma S (2011) Analysis of inorganic ions in gingival crevicular fluid as indicators of periodontal disease activity: a clinico-biochemical study. Contemp Clin Dent 2:278–282

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Yoshimura S, Suemizu H, Taniguchi Y, Arimori K, Kawabe N, Moriuchi T (1994) The human plasma glutathione peroxidase-encoding gene: organization, sequence and localization to chromosome 5q32. Gene 145:293–297

    CAS  PubMed  Google Scholar 

  58. Patel SP, Rao NS, Pradeep A (2012) Effect of nonsurgical periodontal therapy on crevicular fluid and serum glutathione peroxidase levels. Dis Markers 32:1–7

    PubMed  PubMed Central  Google Scholar 

  59. Weinberg ED (1978) Iron and infection. Microbiol Rev 42:45–66

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Finkelstein R, Sciortino CV, Mclntosh MA (1983) Role of iron in microbe-host interactions. Rev Infect Dis 4:S759–S777

    Google Scholar 

  61. Groenink J, Walgreen-Weterings E, Nazmi K, Bolscher JGM, Veerman ECI, Van Winkelhoff AJ, Nieuw Amerongen AV (1999) Salivary lactoferrin and low-Mr mucin MG2 in Actinobacillus actinomycetemcomitans-associated periodontitis. J Clin Periodontol 26:269–275

    CAS  PubMed  Google Scholar 

  62. Davis JH, Yull AB (1964) A toxic factor in abdominal injury II. The role of the red cell component. J Trauma 4:84–90

    CAS  PubMed  Google Scholar 

  63. Schroeder E, Lindhe J (1980) Conditions and pathological features of rapidly destructive, experimental periodontitis in dogs. J Periodontol 5:6–19

    Google Scholar 

  64. Mukherjee S (1985) The role of crevicular fluid iron in periodontal disease. J Periodontol 56:22–27

    CAS  PubMed  Google Scholar 

  65. Kang JH, Lee YH, Kho HS (2018) Clinical factors affecting salivary transferrin level, a marker of blood contamination in salivary analysis. BMC Oral Health 21:18–49

    Google Scholar 

  66. Finney M, Walker JT, Marsh PD, Brading MG (2003) Antimicrobial effects of a novel triclosan/zinc citrate dentifrice against mixed culture oral biofilms. Int Dent J S6P1:371–378

    Google Scholar 

  67. Harrap G, Best J, Saxton C (1984) Human oral retention of zinc from mouthwashes containing zinc salts and its relevance to dental plaque control. Arch Oral Biol 29:87–91

    CAS  PubMed  Google Scholar 

  68. Lynch RJ (2011) Zinc in the mouth, its interactions with dental enamel and possible effects on caries; a review of the literature. Int Dent J.;Suppl 3:46-54

  69. Burch RE, Hahn HK, Sullivan JF (1975) Newer aspects of the roles of zinc, manganese and copper in human nutrition. Clin Chem 21:501–520

    CAS  PubMed  Google Scholar 

  70. Frithiof L, Lavstedt S, Eklund G, Söderberg U, Skårberg KO, Blomqvist J, Asman B, Eriksson W (1980) The relationship between marginal bone loss and serum zinc levels. Acta Med Scand 207:67–70

    CAS  PubMed  Google Scholar 

  71. Thomas B, Kumari S, Ramitha K, Ashwini Kumari MB (2010) Comparative evaluation of micronutrient status in the serum of diabetes mellitus patients and healthy individuals with periodontitis. J Indian Soc Periodontol 14:46–49

    PubMed  PubMed Central  Google Scholar 

  72. Wataha JC, Nelson SK, Lockwood PE (2001) Elemental release from dental casting alloys into biological media with and without protein. Dent Mater 17:409–414

    CAS  PubMed  Google Scholar 

  73. Wataha JC, Lockwood PE, Khajotia SS, Turner R (1998) Effect of pH on element release from dental casting alloys. J Prosthet Dent 80:691–698

    CAS  PubMed  Google Scholar 

  74. Laurent F, Grosgogeat B, Reclaru L, Dalard F, Lissac M (2001) Comparison of corrosion behaviour in presence of oral bacteria. Biomaterials 22:2273–2282

    CAS  PubMed  Google Scholar 

  75. Nielsen FH (2012) Manganese, molybdenum, boron, chromium, and other trace element. In: Erdman JW Jr, Macdonald IA, Zeisel SH (eds) Present Knowledge in Nutrition, 10th edn. Wiley-Blackwell, Ames, pp 586–607

    Google Scholar 

  76. Marie PJ (2007) Strontium ranelate: new insights into its dual mode of action. Bone 40:S5–S8

    CAS  Google Scholar 

  77. Caton JG, Armitage G, Berglundh T et al (2018) A new classification scheme for periodontal and peri-implant diseases and conditions - introduction and key changes from the 1999 classification. J Periodontol 89:S1–S8

    PubMed  Google Scholar 

Download references

Funding

This study was supported by a grant from the Scientific Research Projects of Selcuk University (SELCUK/BAP-14102025).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elif Inonu.

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Inonu, E., Hakki, S.S., Kayis, S.A. et al. The Association Between Some Macro and Trace Elements in Saliva and Periodontal Status. Biol Trace Elem Res 197, 35–42 (2020). https://doi.org/10.1007/s12011-019-01977-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-019-01977-z

Keywords

Navigation