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Biological Trace Element Research

, Volume 176, Issue 2, pp 225–238 | Cite as

Trace Mineral Micronutrients and Chronic Periodontitis—a Review

  • Sumit Gaur
  • Rupali AgnihotriEmail author
Article

Abstract

Trace mineral micronutrients are imperative for optimum host response. Populations worldwide are prone to their insufficiency owing to lifestyle changes or poor nutritional intake. Balanced levels of trace minerals like iron (Fe), zinc (Zn), selenium (Se) and copper (Cu) are essential to prevent progression of chronic conditions like periodontitis. Their excess as well as deficiency is detrimental to periodontal health. This is specifically true in relation to Fe. Furthermore, some trace elements, e.g. Se, Zn and Cu are integral components of antioxidant enzymes and prevent reactive oxygen species induced destruction of tissues. Their deficiency can worsen periodontitis associated with systemic conditions like diabetes mellitus. With this background, the present review first focusses on the role of four trace minerals, namely, Fe, Zn, Se and Cu in periodontal health followed by an appraisal of the data from case control studies related to their association with chronic periodontitis.

Keywords

Chronic periodontitis Copper Iron Selenium Trace minerals Zinc 

Notes

Acknowledgments

None.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Funding Source

None.

References

  1. 1.
    Schifferle RE (2009) Periodontal disease and nutrition: separating the evidence from current fads. Periodontol 50:78–89CrossRefGoogle Scholar
  2. 2.
    Nishida M, Grossi SG, Dunford RG, Ho AW, Trevisan M, Genco RJ (2000) Dietary vitamin C and the risk for periodontal disease. J Periodontol 71:1215–1223PubMedCrossRefGoogle Scholar
  3. 3.
    Petersen PE, Ogawa H (2005) Strengthening the prevention of periodontal disease: the WHO approach. J Periodontol 76:2187–2193PubMedCrossRefGoogle Scholar
  4. 4.
    Yoshida T (2008) Micronutrients and health research. Nova Science Publishers, New YorkGoogle Scholar
  5. 5.
    Tulchinsky TH (2015) The key role of government in addressing the pandemic of micronutrient deficiency conditions in Southeast Asia. Nutrients 7:2518–2523PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Allen L, Dary O, de Benoist B, Hurrel R (2006) WHO guidelines on food fortification with micronutrients. WHO, Geneva http://www.who.int/nutrition/publications/guide_food_fortification_micronutrients.pdf. Accessed on 20 May 2015]Google Scholar
  7. 7.
    Micronutrient Initiative/World Bank/UNICEF (2009) Investing in the future: a united call to action on vitamin and mineral deficiencies: global health report. WHO, Toronto http://www.unitedcalltoaction.org/documents/Investing_in_the_future.pdf. Accessed on 20 May 2015Google Scholar
  8. 8.
    Chernoff R (2009) Issues in geriatric nutrition. Nutr Clin Pract 24:176–178PubMedCrossRefGoogle Scholar
  9. 9.
    Montgomery SC, Streit SM, Beebe ML, Maxwell PJ 4th (2014) Micronutrient needs of the elderly. Nutr Clin Pract 29:435–444PubMedCrossRefGoogle Scholar
  10. 10.
    Mason JB (2012) Vitamins, trace minerals, and other micronutrients. In: Goldman L, Schafer AI, (eds). Goldman’s Cecil Medicine, 24th edn. Saunders, Philadelphia, pp. 1397–1405.Google Scholar
  11. 11.
    Willershausen B, Ross A, Försch M, Willershausen I, Mohaupt P, Callaway A (2011) The influence of micronutrients on oral and general health. Eur J Med Res 16:514–518PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Navia JM (1996) Nutrition and dental caries: ten findings to be remembered. Int Dent J 46(Suppl. 1):381–387Google Scholar
  13. 13.
    Thomas B, Gautam A, Prasad BR, Kumari S (2013) Evaluation of micronutrient (zinc, copper and iron) levels in periodontitis patients with and without diabetes mellitus type 2: a biochemical study. Indian J Dent Res 24:468–473PubMedCrossRefGoogle Scholar
  14. 14.
    Shetty SR, Babu SG, Rao PK, Kishor SK, Rao KA, Castelino R (2014) Interdependence of antioxidants and micronutrients in oral cancer and potentially malignant oral disorders: a serum and saliva study. J Dent (Tehran) 11:696–702Google Scholar
  15. 15.
    Scardina GA, Messina P (2012) Good oral health and diet. J Biomed Biotechnol. doi: 10.1155/2012/720692 PubMedPubMedCentralGoogle Scholar
  16. 16.
    Grossi SG, Zambon JJ, Ho AW, et al. (1994) Assessment of risk for periodontal disease. I. Risk indicators for attachment loss. J Periodontol 65:260–267PubMedCrossRefGoogle Scholar
  17. 17.
    Grossi SG, Genco RJ, Machtei EE, et al. (1995) Assessment of risk for periodontal disease. II. Risk indicators for alveolar bone loss. J Periodontol 66:23–29PubMedCrossRefGoogle Scholar
  18. 18.
    Meyle J, Chapple I (2015) Molecular aspects of the pathogenesis of periodontitis. Periodontol 69:7–17CrossRefGoogle Scholar
  19. 19.
    Karched M, Bhardwaj RG, Asikainen SG (2015) Coaggregation and biofilm growth of Granulicatella spp. with Fusobacterium nucleatum and Aggregatibacter actinomycetemcomitans. BMC Microbiol. doi: 10.1186/s12866-015-0439-z PubMedPubMedCentralGoogle Scholar
  20. 20.
    El-Shinnawi U, Soory M (2013) Associations between periodontitis and systemic inflammatory diseases: response to treatment. Recent Pat Endocr Metab Immune Drug Discov 7:169–188PubMedCrossRefGoogle Scholar
  21. 21.
    Elavarasu S, Sekar S, Murugan T (2012) Host modulation by therapeutic agents. J Pharm Bioallied Sci. doi: 10.4103/0975-7406.100244 Google Scholar
  22. 22.
    Gulati M, Anand V, Govila V, Jain N (2014) Host modulation therapy: an indispensable part of perioceutics. J Indian Soc Periodontol 18:282–288PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Trumbo P, Yates AA, Schlicker S, Poos M (2001) Dietary reference intakes: vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. J Am Diet Assoc 101:294–301PubMedCrossRefGoogle Scholar
  24. 24.
    Nutritional anaemias (1968) Report of a WHO scientific group. World Health Organ Tech Rep Ser 405:5–37Google Scholar
  25. 25.
    Matzner Y, Levy S, Grossowicz N, Izak G, Hershko C (1979) Prevalence and causes of anemia in elderly hospitalized patients. Gerontology 25:113–119PubMedCrossRefGoogle Scholar
  26. 26.
    Touitou Y, Proust J, Carayon A, et al. (1985) Plasma ferritin in old age. Influence of biological and pathological factors in a large elderly population. Clin Chim Acta 149:37–45PubMedCrossRefGoogle Scholar
  27. 27.
    Mukopadhyay D, Mohanaruban K (2002) Iron deficiency anaemia in older people: investigation, management and treatment. Age Aging 31:87–91CrossRefGoogle Scholar
  28. 28.
    Chakraborty S, Tewari S, Sharma RK, Narula SC, Ghalaut PS, Ghalaut V (2014) Impact of iron deficiency anemia on chronic periodontitis and superoxide dismutase activity: a cross-sectional study. J Periodontal Implant Sci 44:57–64PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Patel MD, Shakir QJ, Shetty A (2014) Inter-relationship between chronic periodontitis and anemia: a 6-month follow-up study. J Indian Soc Periodontol 18:19–25PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Jenabian N, Sattari FD, Salar N, Bijani A, Ghasemi N (2013) The relation between periodontitis and anemia associated parameters. J Dentomaxillofacial Radiol, Pathol Surg 2:26–33Google Scholar
  31. 31.
    Pradeep AR, Anuj S (2011) Anemia of chronic disease and chronic periodontitis: does periodontal therapy have an effect on anemic status? J Periodontol 82:388–394PubMedCrossRefGoogle Scholar
  32. 32.
    Enhos S, Duran I, Erdem S, Buyukbas S (2009) Relationship between iron- deficiency anemia and periodontal status in female patients. J Periodontol 80:1750–1755PubMedCrossRefGoogle Scholar
  33. 33.
    Weiss G, Goodnough LT (2005) Anemia of chronic disease. N Engl J Med 352:1011–1023PubMedCrossRefGoogle Scholar
  34. 34.
    Gokhale SR, Sumanth S, Padhye AM (2010) Evaluation of blood parameters in patients with chronic periodontitis for signs of anemia. J Periodontol 81:1202–1206PubMedCrossRefGoogle Scholar
  35. 35.
    Hou J, Yamada S, Kajikawa T, et al. (2014) Iron plays a key role in the cytodifferentiation of human periodontal ligament cells. J Periodontal Res 49:260–267PubMedCrossRefGoogle Scholar
  36. 36.
    Hou J, Yamada S, Kajikawa T, et al. (2012) Role of ferritin in the cytodifferentiation of periodontal ligament cells. Biochem Biophys Res Commun 426:643–648PubMedCrossRefGoogle Scholar
  37. 37.
    Medeiros DM, Plattner A, Jennings D, Stoecker B (2002) Bone morphology, strength and density are compromised in iron deficient rats and exacerbated by calcium restriction. J Nutr 132:3135–3141PubMedGoogle Scholar
  38. 38.
    Medeiros DM, Stoecker B, Plattner A, Jennings D, Haub M (2004) Iron deficiency negatively affects vertebrae and femurs of rats independently of energy intake and body weight. J Nutr 134:3061–3067PubMedGoogle Scholar
  39. 39.
    Hatipoglu H, Hatipoglu MG, Cagirankaya LB, Caglayan F (2012) Severe periodontal destruction in a patient with advanced anemia: a case report. Eur J Dent 6:95–100PubMedPubMedCentralGoogle Scholar
  40. 40.
    Messer JG, Kilbarger AK, Erikson KM, Kipp DE (2009) Iron overload alters iron regulatory genes and proteins, downregulates osteoblastic phenotype, and is associated with apoptosis in fetal rat calvaria cultures. Bone 45:972–979PubMedCrossRefGoogle Scholar
  41. 41.
    Guggenbuhl P, Deugnier Y, Boisdet JF, et al. (2005) Bone mineral density in men with genetic hemochromatosis and HFE gene mutation. Osteoporos Int 16:1809–1814PubMedCrossRefGoogle Scholar
  42. 42.
    Mahachoklertwattana P, Sirikulchayanonta V, Chuansumrit A, et al. (2003) Bone histomorphometry in children and adolescents with beta-thalassemia disease: iron-associated focal osteomalacia. J Clin Endocrinol Metab 88:3966–3972PubMedCrossRefGoogle Scholar
  43. 43.
    Kim BJ, Ahn SH, Bae SJ, et al. (2012) Iron overload accelerates bone loss in healthy postmenopausal women and middle-aged men: a 3-year retrospective longitudinal study. J Bone Miner Res 27:2279–2290PubMedCrossRefGoogle Scholar
  44. 44.
    Messenger AJM, Barclay R (1983) Bacteria, iron and pathogenicity. Biochem Educ 11:54–63CrossRefGoogle Scholar
  45. 45.
    Lewis JP (2010) Metal uptake in host-pathogen interactions: role of iron in Porphyromonas gingivalis interactions with host organisms. Periodontol 52:94–116CrossRefGoogle Scholar
  46. 46.
    Dashper SG, Ang CS, Veith PD, et al. (2009) Response of Porphyromonas gingivalis to heme limitation in continuous culture. J Bacteriol 191:1044–1055PubMedCrossRefGoogle Scholar
  47. 47.
    Leung KP, Folk SP (2002) Effects of porphyrins and inorganic iron on the growth of Prevotella intermedia. FEMS Microbiol Lett 209:15–21PubMedCrossRefGoogle Scholar
  48. 48.
    Xu X, Holt SC, Kolodrubetz D (2001) Cloning and expression of two novel hemin binding protein genes from Treponema denticola. Infect Immun 69:4465–4472PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Liu LY, McGregor N, Wong BK, Butt H, Darby IB (2015) The association between clinical periodontal parameters and free haem concentration within the gingival crevicular fluid: a pilot study. J Periodontal Res 51:86–94PubMedCrossRefGoogle Scholar
  50. 50.
    Wong BKJ, McGregor NR, Butt HL, Knight R, Liu LY, Darby IB (2016) Association of clinical parameters with periodontal bacterial haemolytic activity. J Clin Periodontol 2016 43:503–511CrossRefGoogle Scholar
  51. 51.
    Ganz T (2009) Iron in innate immunity: starve the invaders. Curr Opin Immunol 21:63–67PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Hutter JW, van der Velden U, Varoufaki A, Huffels RAM, Hoek FJ, Loos BG (2001) Lower numbers of erythrocytes and lower levels of hemoglobin in periodontitis patients compared to control subjects. J Clin Periodontol 28:930–936PubMedCrossRefGoogle Scholar
  53. 53.
    Yamamoto T, Tsuneishi M, Furuta M, Ekuni D, Morita M, Hirata Y (2011) Relationship between decrease of erythrocyte count and progression of periodontal disease in a rural Japanese population. J Periodontol 82:106–113PubMedCrossRefGoogle Scholar
  54. 54.
    Musalaiah SV, Anupama M, Nagasree M, Krishna CM, Kumar A, Kumar PM (2014) Evaluation of nonsurgical periodontal therapy in chronic periodontitis patients with anemia by estimating hematological parameters and high-sensitivity C-reactive protein levels. JPharm Bioallied Sci. doi: 10.4103/0975-7406.137390 Google Scholar
  55. 55.
    Dao MC, Meydani SN (2013) Iron biology, immunology, aging, and obesity: four fields connected by the small peptide hormone hepcidin. Adv Nutr 4:602–617PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Joynson DH, Walker DM, Jacobs A, Dolby AE (1972) Defect of cell-mediated immunity in patients with iron-deficiency anaemia. Lancet 2:1058–1059PubMedCrossRefGoogle Scholar
  57. 57.
    Omara FO, Blakley BR (1994) The effects of iron deficiency and iron overload on cell-mediated immunity in the mouse. Br J Nutr 72:899–909PubMedCrossRefGoogle Scholar
  58. 58.
    Porto G, De Sousa M (2007) Iron overload and immunity. World J Gastroenterol 13:4707–4715PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Brock JH, Mulero V (2000) Cellular and molecular aspects of iron and immune function. Proc Nutr Soc 59:537–540PubMedCrossRefGoogle Scholar
  60. 60.
    Ghio AJ, Piantadosi CA, Crumbliss AL (1997) Hypothesis: iron chelation plays a vital role in neutrophilic inflammation. Biometals 10:135–142PubMedCrossRefGoogle Scholar
  61. 61.
    Dawson DR 3rd, Branch-Mays G, Gonzalez OA, Ebersole JL (2014) Dietary modulation of the inflammatory cascade. Periodontol 64:161–197CrossRefGoogle Scholar
  62. 62.
    Meunier N, O’Connor JM, Maiani G, et al. (2005) Importance of zinc in the elderly: the ZENITH study. Eur J Clin Nutr 59 :S1–S4Suppl 2PubMedCrossRefGoogle Scholar
  63. 63.
    Orbak R, Kara C, Ozbek E, Tezel A, Demir T (2007) Effects of zinc deficiency on oral and periodontal diseases in rats. J Periodontal Res 42:138–143PubMedCrossRefGoogle Scholar
  64. 64.
    Seyedmajidi SA, Seyedmajidi M, Moghadamnia A (2014) Effect of zinc-deficient diet on oral tissues and periodontal indices in rats. Int J Mol Cell Med 3:81–87PubMedPubMedCentralGoogle Scholar
  65. 65.
    Bettger WJ (1993) Zinc and selenium, site specific vs general antioxidant. Can J Physiol Pharmacol 71:721–724PubMedCrossRefGoogle Scholar
  66. 66.
    Jacoby BH, Davis WL (1991) The electron microscopic immunolocalization of a copper-zinc superoxide dismutase in association with collagen fibers of periodontal soft tissues. J Periodontol 62:413–420PubMedCrossRefGoogle Scholar
  67. 67.
    Gür A, Colpan L, Nas K, et al. (2002) The role of trace minerals in the pathogenesis of postmenopausal osteoporosis and a new effect of calcitonin. J Bone Miner Metab 20:39–43PubMedCrossRefGoogle Scholar
  68. 68.
    Mahdavi-Roshan M, Ebrahimi M, Ebrahimi A (2015) Copper, magnesium, zinc and calcium status in osteopenic and osteoporotic post-menopausal women. Clin Cases Miner Bone Metab 12:18–21PubMedPubMedCentralGoogle Scholar
  69. 69.
    Sadighi A, Roshan MM, Moradi A, Ostadrahimi A (2008) The effects of zinc supplementation on serum zinc, alkaline phosphatase activity and fracture healing of bones. Saudi Med J 29:1276–1279PubMedGoogle Scholar
  70. 70.
    Frithiof L, Lavstedt S, Eklund G, et al. (1980) The relationship between marginal bone loss and serum zinc levels. Acta Med Scand 207:67–70PubMedCrossRefGoogle Scholar
  71. 71.
    Starcher BC, Hill CH, Madaras JG (1980) Effect of zinc deficiency on bone collagenase and collagen turnover. J Nutr 110:2095–2102PubMedGoogle Scholar
  72. 72.
    Huang Z, Rose AH, Hoffmann PR (2012) The role of selenium in inflammation and immunity: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 16:705–743PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Hill KE, Xia Y, Akesson B, Boeglin ME, Burk RF (1996) Selenoprotein P concentration in plasma is an index of selenium status in selenium-deficient and selenium-supplemented Chinese subjects. J Nutr 126:138–145PubMedGoogle Scholar
  74. 74.
    Duffield AJ, Thomson CD, Hill KE, Williams S (1999) An estimation of selenium requirements for New Zealanders. Am J Clin Nutr 70:896–903PubMedGoogle Scholar
  75. 75.
    Thomson CD (2004) Assessment of requirements for selenium and adequacy of selenium status: a review. Eur J Clin Nutr 58:391–402PubMedCrossRefGoogle Scholar
  76. 76.
    Broome CS, McArdle F, Kyle JA, et al. (2004) An increase in selenium intake improves immune function and poliovirus handling in adults with marginal selenium status. Am J Clin Nutr 80:154–162PubMedGoogle Scholar
  77. 77.
    Borawska MH, Witkowska AM, Hukałowicz K, Markiewicz R (2004) Influence of dietary habits on serum selenium concentration. Ann Nutr Metab 48:134–140PubMedCrossRefGoogle Scholar
  78. 78.
    Wolters M, Hermann S, Golf S, Katz N, Hahn A (2006) Selenium and antioxidant vitamin status of elderly German women. Eur J Clin Nutr 60:85–91PubMedCrossRefGoogle Scholar
  79. 79.
    Asman B, Wijkander P, Hjerpe A (1994) Reduction of collagen degradation in experimental granulation tissue by vitamin E and selenium. J Clin Periodontol 21:45–47PubMedCrossRefGoogle Scholar
  80. 80.
    Nizam N, Discioglu F, Saygun I, et al. (2014) The effect of α-tocopherol and selenium on human gingival fibroblasts and periodontal ligament fibroblasts in vitro. J Periodontol 85:636–644PubMedCrossRefGoogle Scholar
  81. 81.
    Thomas B, Ramesh A, Suresh S, Prasad BR (2013) A comparative evaluation of antioxidant enzymes and selenium in the serum of periodontitis patients with diabetes mellitus type 2. Contemp Clin Dent 4:176–180PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Percival SS (1998) Copper and immunity. Am J Clin Nutr 67:1064S–1068SPubMedGoogle Scholar
  83. 83.
    Matak P, Zumerle S, Mastrogiannaki M, et al. (2013) Copper deficiency leads to anemia, duodenal hypoxia, upregulation of HIF-2α and altered expression of iron absorption genes in mice. PLoS One. doi: 10.1371/journal.pone.0059538 PubMedPubMedCentralGoogle Scholar
  84. 84.
    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 118:439–449PubMedGoogle Scholar
  85. 85.
    Mahmood A, Shukri M (2012) Assessment of salivary elements (zinc, copper and magnesium) among groups of patients with rheumatoid arthritis and chronic periodontitis and its correlation to periodontal health status. J Bagh Coll Dent 24:87–92Google Scholar
  86. 86.
    Pushparani DS, Nirmala S, Theagarayan P (2013) Low serum vitamin C and zinc is associated with the development of oxidative stress in type 2 diabetes mellitus with periodontitis. Int J Pharm Sci Rev Res 23:259–264Google Scholar
  87. 87.
    Pushparani DS, Nirmala S (2014) High level of serum calcium and iron influences the risk of type 2 diabetes mellitus with periodontitis. J Asian Sci Res 4:70Google Scholar
  88. 88.
    Pushparani DS, Anandan SN, Theagarayan P (2014) Serum zinc and magnesium concentrations in type 2 diabetes mellitus with periodontitis. J Indian Soc Periodontol 18:187–193PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Medikeri RS, Lele SV, Mali PP, Jain PM, Darawade DA, Medikeri MR (2015) Effect of campylobacter rectus on serum iron and transferrin—in-vivo findings. J Clin Diagn Res 9:26–30Google Scholar
  90. 90.
    Pushparani DS (2015) Low serum zinc and increased acid phosphatase activity in type 2 diabetes mellitus with periodontitis subjects. Biochem Pharmacol (Los Angel). doi: 10.4172/2167-0501.1000162 Google Scholar
  91. 91.
    Pushparani DS (2015) Serum zinc and iron level in type 2 diabetes mellitus with periodontitis. Int J Pharm Tech Res 7:165–171Google Scholar
  92. 92.
    Herman M, Golasik M, Piekoszewski W, et al. (2016) Essential and toxic metals in oral fluid—a potential role in the diagnosis of periodontal diseases. Biol Trace Elem Res 170:1–8CrossRefGoogle Scholar
  93. 93.
    Boras VV, Brailo V, Rogić D, et al. (2016) Salivary electrolytes in patients with periodontal disease. Res J Pharm, Biol Chem Sci 7:8–14Google Scholar
  94. 94.
    Carvalho RCC, Leite SAM, Rodrigues VP, et al. (2016) Chronic periodontitis and serum levels of hepcidin and hemoglobin. Oral Dis 22:75–76PubMedCrossRefGoogle Scholar
  95. 95.
    Kasuma N, Oenzil F, Lipoeto NI (2016) Correlation between matrix metalloproteinase 8 in gingival crevicular fluid and zinc consumption. Pak J Nutr 15:72–75CrossRefGoogle Scholar
  96. 96.
    Mukherjee S (1985) The role of crevicular fluid iron in periodontal disease. J Periodontol 56(11 Suppl):22–27PubMedCrossRefGoogle Scholar
  97. 97.
    Poleník P (1993) Zinc in etiology of periodontal disease. Med Hypotheses 40:1825CrossRefGoogle Scholar
  98. 98.
    Northrop-Clewes CA, Thurnham DI (2007) Monitoring micronutrients in cigarette smokers. Clin Chim Acta 377:14–38PubMedCrossRefGoogle Scholar
  99. 99.
    McCormick DB (2012) Vitamin/trace mineral supplements for the elderly. Adv Nutr 3:822–824PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Mayne ST, Ferrucci LM, Cartmel B (2012) Lessons learned from randomized clinical trials of micronutrient supplementation for cancer prevention. Annu Rev Nutr 32:369–390PubMedCrossRefGoogle Scholar
  101. 101.
    Daiya S, Sharma RK, Tewari S, Narula SC, Kumar Sehgal P (2014) Micronutrients and superoxide dismutase in postmenopausal women with chronic periodontitis: a pilot interventional study. J Periodontal Implant Sci 44:207–213PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Muñoz CA, Kiger RD, Stephens JA, Kim J, Wilson AC (2001) Effects of a nutritional supplement on periodontal status. Compend Contin Educ Dent 22:425–428PubMedGoogle Scholar
  103. 103.
    Chapple ILC, Milward MR, Ling-Mountford N, et al. (2012) Adjunctive daily supplementation with encapsulated fruit, vegetable and berry juice powder concentrates and clinical periodontal outcomes: a double-blind RCT. J Clin Periodontol 39:62–72PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Ebersole JL, Dawson DR, Morford LA, Peyyala R, Miller CS, Gonzaléz OA (2013) Periodontal disease immunology: “double indemnity” in protecting the host. Periodontol 62:163–202CrossRefGoogle Scholar
  105. 105.
    Mathur A, Mathur L, Manohar B (2013) Antioxidant therapy as monotherapy or as an adjunct to treatment of periodontal diseases. J Indian Soc Periodontol 17:21–24PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Uçkardeş Y, Tekçiçek M, Ozmert EN, Yurdakök K (2009) The effect of systemic zinc supplementation on oral health in low socioeconomic level children. Turk J Pediatr 51:424–428PubMedGoogle Scholar
  107. 107.
    Ahmed T, Haboubi N (2010) Assessment and management of nutrition in older people and its importance to health. Clin Interv Aging 5:207–216PubMedPubMedCentralGoogle Scholar
  108. 108.
    Henderson S, Moore N, Lee E, Witham MD (2008) Do the malnutrition universal screening tool (MUST) and Birmingham nutrition risk (BNR) score predict mortality in older hospitalised patients? BMC Geriatr. doi: 10.1186/1471-2318-8-26 PubMedPubMedCentralGoogle Scholar
  109. 109.
    Zhang L, Su Y, Wang C, et al. (2013) Assessing the nutritional status of elderly Chinese lung cancer patients using the Mini-Nutritional Assessment (MNA®) tool. Clin Interv Aging 8:287–291PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Beck AM, Ovesen L, Osler M (1999) The ‘Mini Nutritional Assessment’ (MNA) and the ‘Determine Your Nutritional Health’ Checklist (NSI Checklist) as predictors of morbidity and mortality in an elderly Danish population. Br J Nutr 81:31–36PubMedCrossRefGoogle Scholar
  111. 111.
    Pichard C, Kyle UG, Bracco D, Slosman DO, Morabia A, Schutz Y (2000) Reference values of fat-free and fat masses by bioelectrical impedance analysis in 3393 healthy subjects. Nutrition 16:245–254PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Department of Pedodontics and Preventive Dentistry, Manipal College of Dental SciencesManipal UniversityManipalIndia
  2. 2.Department of Periodontology, Manipal College of Dental SciencesManipal UniversityManipalIndia

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