The Role of Nutrition in Periodontal Diseases

Chapter
Part of the Oxidative Stress in Applied Basic Research and Clinical Practice book series (OXISTRESS)

Abstract

Dietary unbalances have been related to be risk factors for several chronic diseases. There is increasing evidence linking periodontitis to systemic diseases such as diabetes, metabolic syndrome, and, especially, cardiovascular diseases. Traditionally, much of the research on diet and periodontal diseases has been focused on only a few nutrients with well-established roles in the formation and maintenance of structural components of oral tissue. More recently, research has expanded to include nutrients shown to attenuate the inflammatory process, reactive oxygen species production, or to have anti-inflammatory properties. In the present review, we will discuss on major nutrients (those consumed in gram quantities) and on minor nutrients (required in milligram to microgram quantities, including vitamins and minerals). For each nutrient, a brief introduction considering main functions of this nutrient in health will be exposed. Then, main studies performed on each nutrient in relation to periodontitis will be analyzed, distinguishing human from experimental studies.

Keywords

Placebo Magnesium Carbohydrate Pancreatitis Anemia 

Abbreviations

1,25(OH)2D

1,25-Dihydroxyvitamin D

25(OH)D

25-Hydroxyvitamin D concentrations

8OHdG

8-Hydroxy-deoxyguanosine

DHA

Docosahexaenoic acid

EPA

Eicosapentaenoic acid

GLA

γ-Linolenic acid

GSH/GSSG

Reduced glutathione reduced/oxidized ratio

IgG

Immunoglobulin G

IL-1β

Interleukin-1β

iNOS

Nitric oxide synthase inducible

LNA

Linolenic acid

MUFA

Monounsaturated fatty acids

NHANES

National health and nutrition examination survey

P. gingivalis

Porphyromonas gingivalis

PGE2

Prostaglandin E2

PLS

Papillon–Lefèvre syndrome

PUFA

Polyunsaturated fatty acids

RANKL

Receptor activator of nuclear factor kappa-B ligand

ROS

Reactive oxygen species

Th

T-helper

TNF

Tumor necrosis factor-α

VD

Vitamin D

VDR

Vitamin D receptor

Notes

Acknowledgments

A. Varela-López was supported by a predoctoral FPU grant from the Spanish Ministry of Science and Innovation. Authors acknowledge the University of Granada and the Andalusian Regional government for supporting research of the group.

References

  1. 1.
    Scardina GA, Messina P (2012) Good oral health and diet. J Biomed Biotechnol. doi: 10.1155/2012/720692 PubMedCentralPubMedGoogle Scholar
  2. 2.
    Boyd LD, Lampi KJ (2001) Importance of nutrition for optimum health of the periodontium. J Contemp Dent Pract 2:1–14Google Scholar
  3. 3.
    Battino M, Ferreiro MS, Fattorini D, Bullon P (2002) In vitro antioxidant activities of mouthrinses and their components. J Clin Periodontol 29:462–467PubMedGoogle Scholar
  4. 4.
    Battino M, Ferreiro MS, Gallardo I, Newman HN, Bullon P (2002) The antioxidant capacity of saliva. J Clin Periodontol 29:189–194PubMedGoogle Scholar
  5. 5.
    Battino M, Bompadre S, Leone L, Pugnaloni A, Rubini C, Ferreiro MS, Gallardo I, Bullon P (2003) The effect of cyclosporine A chronic administration on the antioxidant pattern of rat liver mitochondria: structural and functional consequences. Biofactors 18:271–275PubMedGoogle Scholar
  6. 6.
    Battino M, Bompadre S, Politi A, Fioroni M, Rubini C, Bullon P (2005) Antioxidant status (CoQ10 and Vit. E levels) and immunohistochemical analysis of soft tissues in periodontal diseases. Biofactors 25:213–217PubMedGoogle Scholar
  7. 7.
    Battino M, Ferreiro MS, Armeni T, Politi A, Bompadre S, Massoli A, Bullon P (2005) In vitro antioxidant activities of antioxidant-enriched toothpastes. Free Radic Res 39:343–350PubMedGoogle Scholar
  8. 8.
    Bullon P, Pugnaloni A, Gallardo I, Machuca G, Hevia A, Battino M (2003) Ultrastructure of the gingiva in cardiac patients treated with or without calcium channel blockers. J Clin Periodontol 30:682–690PubMedGoogle Scholar
  9. 9.
    Bullon P, Fioroni M, Goteri G, Rubini C, Battino M (2004) Immunohistochemical analysis of soft tissues in implants with healthy and peri-implantitis condition, and aggressive periodontitis. Clin Oral Implants Res 15:553–559PubMedGoogle Scholar
  10. 10.
    Bullon P, Gallardo I, Goteri G, Rubini C, Battino M, Ribas J, Newman HN (2007) Nifedipine and cyclosporin affect fibroblast calcium and gingiva. J Dent Res 86:357–362PubMedGoogle Scholar
  11. 11.
    Bullon P, Morillo JM, Ramirez-Tortosa MC, Quiles JL, Newman HN, Battino M (2009) Metabolic syndrome and periodontitis: is oxidative stress a common link? J Dent Res 88:503–518PubMedGoogle Scholar
  12. 12.
    Bullon P, Quiles JL, Morillo JM, Rubini C, Goteri G, Granados-Principal S, Battino M, Ramirez-Tortosa M (2009) Gingival vascular damage in atherosclerotic rabbits: hydroxytyrosol and squalene benefits. Food Chem Toxicol 47:2327–2331. doi: 10.1016/j.fct.2009.06.026 PubMedGoogle Scholar
  13. 13.
    Bullon P, Cordero MD, Quiles JL, Morillo JM, del Carmen Ramirez-Tortosa M, Battino M (2011) Mitochondrial dysfunction promoted by Porphyromonas gingivalis lipopolysaccharide as a possible link between cardiovascular disease and periodontitis. Free Radic Biol Med 50:1336–1343. doi: 10.1016/j.freeradbiomed.2011.02.018 PubMedGoogle Scholar
  14. 14.
    Bullon P, Cordero MD, Quiles JL, del Carmen Ramirez-Tortosa M, Gonzalez-Alonso A, Alfonsi S, García-Marín R, de Miguel M, Battino M (2012) Autophagy in periodontitis patients and gingival fibroblasts: unraveling the link between chronic diseases and inflammation. BMC Med 10:122. doi: 10.1186/1741-7015-10-122 PubMedCentralPubMedGoogle Scholar
  15. 15.
    Kaye EK (2010) n-3 fatty acid intake and periodontal disease. J Am Diet Assoc 110:1650–1652PubMedGoogle Scholar
  16. 16.
    Ramirez-Tortosa MC, Quiles JL, Battino M, Granados S, Morillo JM, Bompadre S, Newman HN, Bullon P (2010) Periodontitis is associated with altered plasma fatty acids and cardiovascular risk markers. Nutr Metab Cardiovasc Dis 20:133–139. doi: 10.1016/j.numecd.2009.03.003 PubMedGoogle Scholar
  17. 17.
    Schifferle RE (2005) Nutrition and periodontal disease. Dent Clin N Am 49:595–610. doi: 10.1016/j.cden.2005.03.008 PubMedGoogle Scholar
  18. 18.
    Schifferle RE (2009) Periodontal disease and nutrition: separating the evidence from current fads. Periodontol 2000 50:78–89. doi: 10.1111/j.1600-0757.2008.00297.x PubMedGoogle Scholar
  19. 19.
    Enwonwu CO (1995) Interface of malnutrition and periodontal diseases. Am J Clin Nutr 61:430S–436SPubMedGoogle Scholar
  20. 20.
    Enwonwu CO (1994) Cellular and molecular effects of malnutrition and their relevance to periodontal disease. J Clin Periodontol 21:643–657. doi: 10.1111/j.1600-051X.1994.tb00782.x PubMedGoogle Scholar
  21. 21.
    Enwonwu CO, Meeks VI (1996) Oral candidiasis, HIV, and saliva glucocorticoids. Am J Pathol 148:1313–1318PubMedCentralPubMedGoogle Scholar
  22. 22.
    Baelum V, Scheutz F (2002) Periodontal diseases in Africa. Periodontol 2000 29:79–103. doi: 10.1034/j.1600-0757.2002.290105.x PubMedGoogle Scholar
  23. 23.
    Navia JM (1996) Nutrition and dental caries: ten findings to be remembered. Int Dent J 46:381–387Google Scholar
  24. 24.
    Johansson I, Ericson T (1987) Saliva composition and caries development during protein deficiency and β-receptor stimulation or inhibition. J Oral Pathol 16:145PubMedGoogle Scholar
  25. 25.
    Agarwal PK, Agarwal KN, Agarwal DK (1984) Biochemical changes in saliva of malnourished children. Am J Clin Nutr 39:181–184PubMedGoogle Scholar
  26. 26.
    Reddy V, Raghuramulu N, Bhaskaram C (1976) Secretory IgA in protein-calorie malnutrition. Arch Dis Child 51:871–874. doi: 10.1136/adc.51.11.871 PubMedCentralPubMedGoogle Scholar
  27. 27.
    McMurray DN, Rey H, Casazza LJ, Watson RR (1977) Effect of moderate malnutrition on concentrations of immunoglobulins and enzymes in tears and saliva of young Colombian children. Am J Clin Nutr 30:1944–1948PubMedGoogle Scholar
  28. 28.
    Johansson I, Ericson T (1986) Effect of chewing on the secretion of salivary components during fasting. Caries Res 20:141–147. doi: 10.1159/000260933 PubMedGoogle Scholar
  29. 29.
    Menaker L, Navia JM (1974) Effect of undernutrition during the perinatal period on caries development in the rat: V. Changes in whole saliva volume and protein content. J Dent Res 53:592–597. doi: 10.1177/00220345740530031201 Google Scholar
  30. 30.
    Johansson I, Alm P (1989) Effect of moderate protein-deficiency on ultrastructure in parotid and submandibuar acinar cells in the adult rat. Scand J Dent Res 97:505–510. doi: 10.1111/j.1600-0722.1989.tb00924.x PubMedGoogle Scholar
  31. 31.
    Johansson I, Ryberg M (1991) The effects of moderate protein deficiency on β-adrenoceptor density in rat parotid and submandibular salivary glands. Arch Oral Biol 36:591–594. doi: 10.1016/0003-9969(91)90109-8 Google Scholar
  32. 32.
    Enwonwu CO, Phillips RS, Ibrahim CD, Danfillo IS (2004) Nutrition and oral health in Africa. Int Dent J 54:344–351. doi: 10.1111/j.1875-595X.2004.tb00010.x PubMedGoogle Scholar
  33. 33.
    Morhart RE, Fitzgerald RJ (1976) Nutritional determinants of the ecology of the oral flora. Dent Clin North Am 20:473–489PubMedGoogle Scholar
  34. 34.
    Hujoel P (2009) Dietary carbohydrates and dental-systemic diseases. J Dent Res 88:490–502. doi: 10.1177/0022034509337700 PubMedGoogle Scholar
  35. 35.
    Chung CS, Hankin JH, Miyamoto W, Kau MK (1977) Dental plaque and dietary intakes in school children in Hawaii. J Dent Res 56:11–16. doi: 10.1177/00220345770560010101 PubMedGoogle Scholar
  36. 36.
    Harjola U, Liesma H (1978) Effect of polyol and sucrose candies on plaque, gingivitis and lactobacillus index scores. Acta Odontol Scand 36:237–242. doi: 10.3109/00016357809004674 PubMedGoogle Scholar
  37. 37.
    Roberts IF, Roberts GJ (1979) Relation between medicines sweetened with sucrose and dental disease. Br Med J 2:14–16PubMedCentralPubMedGoogle Scholar
  38. 38.
    Sidi AD, Ashley FP (1984) Influence of frequent sugar intakes on experimental gingivitis. J Periodontol 55:419–423PubMedGoogle Scholar
  39. 39.
    Yoshihara A, Watanabe R, Hanada N, Miyazaki H (2009) Longitudinal study of the relationship between diet intake and dental caries and periodontal disease in elderly Japanese subjects. Gerodontology 26:130–136. doi: 10.1111/j.1741-2358.2008.00244.x PubMedGoogle Scholar
  40. 40.
    Carlsson J, Sundström B (1968) Variations in composition of early dental plaque following ingestion of sucrose and glucose. Odontol Revy 19:161–169PubMedGoogle Scholar
  41. 41.
    Fry AJ, Grenby TH (1972) The effects of reduced sucrose intake on the formation and composition of dental plaque in a group of men in the Antartic. Arch Oral Biol 17:873–882. doi: 10.1016/0003-9969(72)90030-1 PubMedGoogle Scholar
  42. 42.
    Scheinin A, Makinen KK, Ylitalo K (1976) Turku sugar studies. V. Final report on the effect of sucrose, fructose and xylitol diets on the caries incidence in man. Acta Odontol Scand 34:179–198PubMedGoogle Scholar
  43. 43.
    Auskaps AM, Gupta OP, Shaw JH (1957) Periodontal disease in the rice rat. III. Survey of dietary influences. J Nutr 63:325–343PubMedGoogle Scholar
  44. 44.
    Aguirre JI, Akhter MP, Kimmel DB, Pingel J, Xia X, Williams A, Jorgensen M, Edmonds K, Lee JY, Reinhard MK, Battles AH, Kesavalu L, Wronski TJ (2012) Enhanced alveolar bone loss in a model of non-invasive periodontitis in rice rats. Oral Dis 18:459–468. doi: 10.1111/j.1601-0825.2011.01893.x PubMedCentralPubMedGoogle Scholar
  45. 45.
    Keyes PH, Jordan HV (1964) Periodontal lesions in the Syrian hamster. III. Findings related to an infectious and transmissible component. Arch Oral Biol 9:377–400. doi: 10.1016/0003-9969(64)90024-X PubMedGoogle Scholar
  46. 46.
    Jordan HV, Keyes PH, Lim S (1969) Plaque formation and implantation of Odontomyces viscosus in hamsters fed different carbohydrates. J Dent Res 48:824–831. doi: 10.1177/00220345690480053601 PubMedGoogle Scholar
  47. 47.
    Socransky SS, Huberas kC, Propas D (1970) Induction of periodontal destruction in gnotobiotic rats by a human oral strain of Actinomyces naeslundii. Arch Oral Biol 15:993–995PubMedGoogle Scholar
  48. 48.
    Galvão MP, Chapper A, Rösing CK, Ferreira MB, de Souza MA (2003) Methodological considerations on descriptive studies of induced periodontal diseases in rats. Pesqui Odontol Bras 17:56–62. doi: 10.1590/S1517-74912003000100011 PubMedGoogle Scholar
  49. 49.
    Liu S (2002) Intake of refined carbohydrates and whole grain foods in relation to risk of type 2 diabetes mellitus and coronary heart disease. J Am Coll Nutr 21:298–306PubMedGoogle Scholar
  50. 50.
    Ripsin CM, Keenan JM, Jacobs DR Jr, Elmer PJ, Welch RR, Van Horn L, Liu K, Turnbull WH, Thye FW, Kestin M, Hegsted M, Davidson DM, Davidson MH MD, Dugan LD, Demark-Wahnefried W, Beling S (1992) Oat products and lipid lowering. A meta-analysis. JAMA 267:3317–3325. doi: 10.1001/jama.1992.03480240079039 PubMedGoogle Scholar
  51. 51.
    Alfieri MA, Pomerleau J, Grace DM, Anderson L (1995) Fiber intake of normal weight, moderately obese and severely obese subjects. Obes Res 3:541–547. doi: 10.1002/j.1550-8528.1995.tb00188.x PubMedGoogle Scholar
  52. 52.
    Beck B, Burlet A, Nicolas JP, Burlet C (1996) Opposite influence of carbohydrates and fat on hypothalamic neurotensin in Long-Evans rats. Life Sci 59:349–356PubMedGoogle Scholar
  53. 53.
    Montague CT, O’Rahilly S (2000) The perils of portliness: causes and consequences of visceral adiposity. Diabetes 49:883–888. doi: 10.2337/diabetes.49.6.883 PubMedGoogle Scholar
  54. 54.
    Esposito K, Marfella R, Ciotola M, Di Palo C, Giugliano F, Giugliano G, D'Armiento M, D'Andrea F, Giugliano D (2004) Effect of a Mediterranean-style diet on endothelial dysfunction on markers of vascular inflammation in the metabolic syndrome: a randomized trial. JAMA 292:1440–1446. doi: 10.1001/jama.292.12.1440 PubMedGoogle Scholar
  55. 55.
    Slattery ML, Curtin KP, Edwards SL, Schaffer DM (2004) Plant foods, fiber, and rectal cancer. Am J Clin Nutr 79:274–281PubMedGoogle Scholar
  56. 56.
    Mann J (2007) Dietary carbohydrate: relationship to cardiovascular disease and disorders of carbohydrate metabolism. Eur J Clin Nutr 61:S100–S111. doi: 10.1038/sj.ejcn.1602940 PubMedGoogle Scholar
  57. 57.
    Pischon N, Heng N, Bernimoulin J-P, Kleber B-M, Willich SN, Pischon T (2007) Obesity, inflammation, and periodontal disease. J Dent Res 86:400–409. doi: 10.1177/154405910708600503 PubMedGoogle Scholar
  58. 58.
    Schulze MB, Schulz M, Heidemann C, Schienkiewitz A, Hoffmann K, Boeing H (2007) Fiber and magnesium intake and incidence of type 2 diabetes: a prospective study and meta-analysis. Arch Intern Med 167:956–965. doi: 10.1001/archinte.167.9.956 PubMedGoogle Scholar
  59. 59.
    König KG, Navia JM (1995) Nutritional role of sugars in oral health. Am J Clin Nutr 62:275S–283SPubMedGoogle Scholar
  60. 60.
    Proctor GB, Carpenter GH (2001) Chewing stimulates secretion of human salivary secretory immunoglobulin A. J Dent Res 80:909–913. doi: 10.1111/j.1532-5415.2011.03866.x PubMedGoogle Scholar
  61. 61.
    Schwartz N, Kaye EK, Nunn ME, Spiro A 3rd, Garcia RI (2012) High-fiber foods reduce periodontal disease progression in men aged 65 and older: the Veterans Affairs normative aging study/Dental Longitudinal Study. J Am Geriatr Soc 60:676–683. doi: 10.1111/j.1532-5415.2011.03866.x PubMedGoogle Scholar
  62. 62.
    Yamori M, Njelekela M, Mtabaji J, Yamori Y, Bessho K (2011) Hypertension, periodontal disease, and potassium intake in nonsmoking, nondrinker African women on no medication. Int J Hypertens 2011:695719. doi: 10.4061/2011/695719 PubMedCentralPubMedGoogle Scholar
  63. 63.
    Petti S, Cairella G, Tarsitani G (2000) Nutritional variables related to gingival health in adolescent girls. Community Dent Oral Epidemiol 28:407–413. doi: 10.1034/j.1600-0528.2000.028006407.x PubMedGoogle Scholar
  64. 64.
    Hung HC, Colditz G, Joshipura KJ (2005) The association between tooth loss and the self-reported intake of selected CVD-related nutrients and foods among US women. Community Dent Oral Epidemiol 33:167–173. doi: 10.1111/j.1600-0528.2005.00200.x PubMedGoogle Scholar
  65. 65.
    Merchant AT, Pitiphat W, Franz M, Joshipura KJ (2006) Whole-grain and fiber intakes and periodontitis risk in men. Am J Clin Nutr 83:1395–1400PubMedGoogle Scholar
  66. 66.
    Hornecker E, Muuß T, Ehrenreich MD, Mausberg RF (2003) A pilot study on the oral conditions of severely alcohol addicted persons. J Contemp Dent Pract 4:51–59PubMedGoogle Scholar
  67. 67.
    WHO (1992) The classification of mental and behavioral disorders. Clinical descriptions and diagnostic guidelines. World Health Organization, GenevaGoogle Scholar
  68. 68.
    Larato DC (1972) Oral tissue changes in the chronic alcoholic. J Periodontol 43:772–773PubMedGoogle Scholar
  69. 69.
    Harris CK, Warnakularsuriya KA, Johnson NW, Gelbier S, Peters TJ (1996) Oral health in alcohol misusers. Community Dent Health 13:199–203PubMedGoogle Scholar
  70. 70.
    Enberg N, Wolf J, Ainamo A, Alho H, Heinälä P, Lenander-Lumikari M (2001) Dental diseases and loss of teeth in a group of Finnish alcoholics: a radiological study. Acta Odontol Scand 59:341–347. doi: 10.1080/000163501317153176 PubMedGoogle Scholar
  71. 71.
    Shizukuishi S, Hayashi N, Tamagawa H, Hanioka T, Maruyama S, Takeshita T, Morimoto K (1998) Lifestyle and periodontal health status of Japanese factory workers. Ann Periodontol 3:303–311PubMedGoogle Scholar
  72. 72.
    Tezal M, Grossi SG, Ho AW, Genco RJ (2001) The effect of alcohol consumption on periodontal disease. J Periodontol 72:183–189. doi: 10.1902/jop.2001.72.2.183 PubMedGoogle Scholar
  73. 73.
    Shimazaki Y, Saito T, Kiyohara Y, Kato I, Kubo M, Iida M, Yamashita Y (2005) Relationship between drinking and periodontitis: the Hisayama Study. J Periodontol 76:1534–1541. doi: 10.1902/jop.2005.76.9.1534 PubMedGoogle Scholar
  74. 74.
    Nishida N, Tanaka M, Sekine S, Takeshita T, Nakayama K, Morimoto K, Shizukuishi S (2010) Association of ALDH2 genotypes with periodontitis progression. J Dent Res 89:138–142. doi: 10.1177/0022034509356045 PubMedGoogle Scholar
  75. 75.
    Tezal M, Grossi SG, Ho AW, Genco RJ (2004) Alcohol consumption and periodontal disease. The Third National Health and Nutrition Examination Survey. J Clin Periodontol 31:484–488. doi: 10.1111/j.1600-051X.2004.00503.x PubMedGoogle Scholar
  76. 76.
    Lages EJ, Costa FO, Lages EM, Cota LO, Cortelli SC, Nobre-Franco GC, Cyrino RM, Cortelli JR (2012) Risk variables in the association between frequency of alcohol consumption and periodontitis. J Clin Periodontol 39:115–122. doi: 10.1111/j.1600-051X.2011.01809.x PubMedGoogle Scholar
  77. 77.
    Pitiphat W, Merchant AT, Rimm EB, Joshipura KJ (2003) Alcohol consumption increases periodontitis risk. J Dent Res 82:509–513. doi: 10.1177/154405910308200704 PubMedGoogle Scholar
  78. 78.
    Okamoto Y, Tsuboi S, Suzuki S, Nakagaki H, Ogura Y, Maeda K, Tokudome S (2006) Effects of smoking and drinking habits on the incidence of periodontal disease and tooth loss among Japanese males: a 4-yr longitudinal study. J Periodontal Res 41:560–566. doi: 10.1111/j.1600-0765.2006.00907.x PubMedGoogle Scholar
  79. 79.
    Jansson L (2008) Association between alcohol consumption and dental health. J Clin Periodontol 35:379–384. doi: 10.1111/j.1600-051X.2008.01210.x PubMedGoogle Scholar
  80. 80.
    Torrungruang K, Tamsailom S, Rojanasomsith K, Sutdhibhisal S, Nisapakultorn K, Vanichjakvong O, Prapakamol S, Premsirinirund T, Pusiri T, Jaratkulangkoon O, Unkurapinun N, Sritara P (2005) Risk indicators of periodontal disease in older Thai adults. J Periodontol 76:558–565. doi: 10.1902/jop.2005.76.4.558 PubMedGoogle Scholar
  81. 81.
    Kongstad J, Hvidtfeldt UA, Grønbaek M, Jontell M, Stoltze K, Holmstrup P (2008) Amount and type of alcohol and periodontitis in the Copenhagen City Heart Study. J Clin Periodontol 35:1032–1039. doi: 10.1111/j.1600-051X.2008.01325.x PubMedGoogle Scholar
  82. 82.
    de Souza DM, Ricardo LH, Prado Mde A, Prado Fde A, da Rocha RF (2006) The effect of alcohol consumption on periodontal bone support in experimental periodontitis in rats. J Appl Oral Sci 14:443–447. doi: 10.1590/S1678-77572006000600010 PubMedGoogle Scholar
  83. 83.
    Souza DM, Ricardo LH, Kantoski KZ, Rocha RF (2009) Influence of alcohol consumption on alveolar bone level associated with ligature-induced periodontitis in rats. Braz Oral Res 23:326–332. doi: 10.1590/S1806-83242009000300017 PubMedGoogle Scholar
  84. 84.
    Dantas AM, Mohn CE, Burdet B, Zorrilla Zubilete M, Mandalunis PM, Elverdin JC, Fernández-Solari J (2012) Ethanol consumption enhances periodontal inflammatory markers in rats. Arch Oral Biol 57:1211–1217. doi: 10.1016/j.archoralbio.2012.02.008 PubMedGoogle Scholar
  85. 85.
    Irie K, Tomofuji T, Tamaki N, Sanbe T, Ekuni D, Azuma T, Maruyama T, Yamamoto T (2008) Effects of ethanol consumption on periodontal inflammation in rats. J Dent Res 87:456–460. doi: 10.1177/154405910808700511 PubMedGoogle Scholar
  86. 86.
    Tomofuji T, Sanbe T, Ekuni D, Azuma T, Irie K, Maruyama T, Tamaki N, Yamamoto T (2008) Oxidative damage of rat liver induced by ligature-induced periodontitis and chronic ethanol consumption. Arch Oral Biol 53:1113–1118. doi: 10.1016/j.archoralbio.2008.05.015 PubMedGoogle Scholar
  87. 87.
    Liberman DN, Pilau RM, Gaio EJ, Orlandini LF, Rösing CK (2011) Low concentration alcohol intake may inhibit spontaneous alveolar bone loss in Wistar rats. Arch Oral Biol 56:109–113. doi: 10.1016/j.archoralbio.2010.09.012 PubMedGoogle Scholar
  88. 88.
    Campan P, Planchand P, Duran D (1997) Pilot study on n-3 polyunsaturated fatty acids in the treatment of human experimental gingivitis. J Clin Periodontol 24:907–913. doi: 10.1111/j.1600-051X.1997.tb01210.x PubMedGoogle Scholar
  89. 89.
    Eberhard J, Heilmann F, Açil Y, Albers KH, Jepsen S (2002) Local application of n-3 or n-6 polyunsaturated fatty acids in the treatment of human experimental gingivitis. J Clin Periodontol 29:364–369. doi: 10.1034/j.1600-051X.2002.290413.x PubMedGoogle Scholar
  90. 90.
    Rosenstein ED, Kushnera LJ, Kramera N, Kazandjian G (2003) Pilot study of dietary fatty acid supplementation in the treatment of adult periodontitis. Prostaglandins Leukot Essent Fatty Acids 68:213–218. doi: 10.1016/S0952-3278(02)00272-7 PubMedGoogle Scholar
  91. 91.
    El-Sharkawy H, Aboelsaad N, Eliwa M, Darweesh M, Alshahat M, Kantarci A, Hasturk H, Van Dyke TE (2010) Adjunctive treatment of chronic periodontitis with daily dietary supplementation with omega-3 fatty acids and low-dose aspirin. J Periodontol 81:1635–1643. doi: 10.1902/jop.2010.090628 PubMedGoogle Scholar
  92. 92.
    Iwasaki M, Yoshihara A, Moynihan P, Watanabe R, Taylor GW, Miyazaki H (2010) Longitudinal relationship between dietary ω-3 fatty acids and periodontal disease. Nutrition 26:1105–1109. doi: 10.1016/j.nut.2009.09.010 PubMedGoogle Scholar
  93. 93.
    Naqvi AZ, Buettner C, Phillips RS, Davis RB, Mukamal KJ (2010) n-3 fatty acids and periodontitis in US adults. J Am Diet Assoc 110:1669–1675. doi: 10.1016/j.jada.2010.08.009 PubMedCentralPubMedGoogle Scholar
  94. 94.
    Vardar S, Buduneli E, Türkoğlu O, Berdeli AH, Baylas H, Başkesen A, Atilla G (2004) Therapeutic versus prophylactic plus therapeutic administration of omega-3 fatty acid on endotoxin-induced periodontitis in rats. J Periodontol 75:1640–1646. doi: 10.1902/jop.2004.75.12.1640 PubMedGoogle Scholar
  95. 95.
    Vardar S, Buduneli E, Baylas H, Berdeli AH, Buduneli N, Atilla G (2005) Individual and combined effects of selective cyclooxygenase-2 inhibitor and omega-3 fatty acid on endotoxin-induced periodontitis in rats. J Periodontol 76:99–106. doi: 10.1902/jop.2005.76.1.99 PubMedGoogle Scholar
  96. 96.
    Vardar S, Buduneli N, Buduneli E, Kardesxler L, Baylas H, Atilla G, Lappin D, Kinane DF (2006) Dietary supplementation of omega-3 fatty acid and circulating levels of interleukin-1β, osteocalcin, and c-reactive protein in rats. J Periodontol 77:814–820. doi: 10.1902/jop.2006.050214 Google Scholar
  97. 97.
    Kesavalu L, Vasudevan B, Raghu B, Browning E, Dawson D, Novak JM, Correll MC, Steffen MJ, Bhattacharya A, Fernandes G, Ebersole JL (2006) Omega-3 fatty acid effect on alveolar bone loss in rats. J Dent Res 85:648–652. doi: 10.1177/154405910608500713 PubMedCentralPubMedGoogle Scholar
  98. 98.
    Kesavalu L, Bakthavatchalu V, Rahman MM, Su J, Raghu B, Dawson D, Fernandes G, Ebersole JL (2007) Omega-3 fatty acid regulates inflammatory cytokine/mediator messenger RNA expression in Porphyromonas gingivalis-induced experimental periodontal disease. Oral Microbiol Immunol 22:232–239. doi: 10.1111/j.1399-302X.2007.00346.x PubMedGoogle Scholar
  99. 99.
    Bendyk A, Marino V, Zilm PS, Howe P, Bartold PM (2009) Effect of dietary ω-3 polyunsaturated fatty acids on experimental periodontitis in the mouse. J Periodontal Res 44:211–216. doi: 10.1111/j.1600-0765.2008.01108.x PubMedGoogle Scholar
  100. 100.
    Rubinoff AB, Latner PA, Pasut CAL (1989) Vitamin C and oral health. J Can Dent Assoc 55:705–707PubMedGoogle Scholar
  101. 101.
    Pussinen PJ, Laatikainen T, Alfthan G, Asikainen S, Jousilahti P (2003) Periodontitis is associated with a low concentration of vitamin C in plasma. Clin Diagn Lab Immunol 10:897–902. doi: 10.1128/CDLI.10.5.897-902.2003 PubMedCentralPubMedGoogle Scholar
  102. 102.
    Amarasena N, Ogawa H, Yoshihara A, Hanada N, Miyazaki H (2005) Serum vitamin C periodontal relationship in community-dwelling elderly Japanese. J Clin Periodontol 32:93–97. doi: 10.1111/j.1600-051X.2004.00643.x PubMedGoogle Scholar
  103. 103.
    Amaliya, Timmerman MF, Abbas F, Loos BG, Van der Weijden GA, Van Winkelhoff AJ, Winkel EG, Van der Velden U (2007) Java project on periodontal diseases: the relationship between vitamin C and the severity of periodontitis. J Clin Periodontol 34:299–304. doi: 10.1111/j.1600-051X.2007.01053.x PubMedGoogle Scholar
  104. 104.
    Iwasaki M, Manz MC, Taylor GW, Yoshihara A, Miyazaki H (2012) Relations of serum ascorbic acid and α-tocopherol to periodontal disease. J Dent Res 91:167–172. doi: 10.1177/0022034511431702 PubMedGoogle Scholar
  105. 105.
    Chapple ILC, Milward MR, Dietrich T (2007) The prevalence of inflammatory periodontitis is negatively associated with serum antioxidant concentrations. J Nutr 137:657–664PubMedGoogle Scholar
  106. 106.
    Nishida M, Grossi SG, Dunford RG, Ho AW, Trevisan M, Genko RJ (2000) Dietary vitamin C and the risk for periodontal disease. J Periodontol 71:1215–1223PubMedGoogle Scholar
  107. 107.
    Eklund SA, Burt BA (1994) Risk factors for total tooth loss in the United States; longitudinal analysis of National data. J Public Health Dent 54:5–14PubMedGoogle Scholar
  108. 108.
    Iwasaki M, Moynihan P, Manz MC, Taylor GW, Yoshihara A, Muramatsu K, Watanabe R, Miyazaki H (2013) Dietary antioxidants and periodontal disease in community based older Japanese: a 2 year follow up study. Public Health Nutr 16:330–338. doi: 10.1017/S1368980012002637 PubMedGoogle Scholar
  109. 109.
    Diab-Ladki R, Pellat B, Chahine R (2003) Decrease in the total antioxidant activity of saliva in patients with periodontal diseases. Clin Oral Investig 7:103–107. doi: 10.1007/s00784-003-0208-5 PubMedGoogle Scholar
  110. 110.
    Buduneli N, Kardeşler L, Işik H, Willis CS, Hawkins SI, Kinane DF, Scott DA (2006) Effects of smoking and gingival inflammation on salivary antioxidant capacity. J Clin Periodontol 33:159–164. doi: 10.1111/j.1600-051X.2006.00892.x PubMedGoogle Scholar
  111. 111.
    Gümüş P, Buduneli N, Cxetinkalp S, Hawkins SI, Renaud D, Kinane DF, Scott DA (2009) Salivary antioxidants in patients with type 1 or 2 diabetes and inflammatory periodontal disease: a case-control study. J Periodontol 80:1440–1446. doi: 10.1902/jop.2009.090159 PubMedGoogle Scholar
  112. 112.
    Thomas B, Kumari S, Ramitha K, Kumari MBA (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. doi: 10.4103/0972-124X.65439 PubMedCentralPubMedGoogle Scholar
  113. 113.
    Kuzmanova D, Jansen IDC, Schoenmaker T, Nazmi K, Teeuw WJ, Bizzarro S, Loos BG, van der Velden U (2012) Vitamin C in plasma and leucocytes in relation to periodontitis. J Clin Periodontol 39:905–912. doi: 10.1111/j.1600-051X.2012.01927.x PubMedGoogle Scholar
  114. 114.
    Campbell HG, Cook RP (1941) Treatment of gingivitis with ascorbic acid. Br Med J 1:360–361. doi: 10.1136/bmj.1.4183.360 PubMedCentralPubMedGoogle Scholar
  115. 115.
    Leggott PJ, Robertson PB, Rothman DL, Murray PA, Jacobf RA (1986) The effect of controlled ascorbic acid depletion and supplementation on periodontal health. J Periodontol 57:480–485PubMedGoogle Scholar
  116. 116.
    Thomas AE, Busby MC Jr, Ringsdorf WM Jr, Cheraskin E (1962) Ascorbic acid and alveolar bone loss. Oral Surg Oral Med Oral Pathol 15:555–565. doi: 10.1016/0030-4220(62)90173-1 PubMedGoogle Scholar
  117. 117.
    Glickman I, Dines MM (1963) Effect of increased ascorbic acid blood levels on the ascorbic acid level in treated and non-treated. J Dent Res 42:1152–1158PubMedGoogle Scholar
  118. 118.
    Coven EM (1965) Effect of prophylasis and vitamin supplementation upon periodontal index on children 60-66. J Periodontol 36:494–500PubMedGoogle Scholar
  119. 119.
    Prentice AM, Lamb WH, Bates CJ (1983) A trial of ascorbic acid and of multivitamin supplementation on the oral health of West African children. Trans R Soc Trop Med Hyg 77:792–795PubMedGoogle Scholar
  120. 120.
    Vogel RI, Lamster IB, Wechsler SA, Macedo B, Hartley LJ, Macedo JA (1986) The effects of megadoses of ascorbic acid on PMN chemotaxis and experimental gingivitis. J Periodontol 57:472–479PubMedGoogle Scholar
  121. 121.
    Abou Sulaiman AEA, Shehadeh RMH (2010) Assessment of total antioxidant capacity and the use of vitamin C in the treatment of non-smokers with chronic periodontitis. J Periodontol 81:1547–1554. doi: 10.1902/jop.2010.100173 PubMedGoogle Scholar
  122. 122.
    Van der Velden U, Kuzmanova D, Chapple ILC (2011) Micronutritional approaches to periodontal therapy. J Clin Periodontol 38:142–158. doi: 10.1111/j.1600-051X.2010.01663.x PubMedGoogle Scholar
  123. 123.
    Shiga M, Kapila YL, Zhang Q, Hayami T, Kapila S (2003) Ascorbic acid induces collagenase-1 in human periodontal ligament cells but not in MC3T3-E1 osteoblast-like cells: potential association between collagenase expression and changes in alkaline phosphatase phenotype. J Bone Miner Res 18:67–77PubMedGoogle Scholar
  124. 124.
    Tsutsumi K, Fujikawa H, Kajikawa T, Takedachi M, Yamamoto T, Murakami S (2012) Effects of L-ascorbic acid 2-phosphate magnesium salt on the properties of human gingival fibroblasts. J Periodontal Res 47:263–271. doi: 10.1111/j.1600-0765.2011.01430.x PubMedGoogle Scholar
  125. 125.
    Sanbe T, Tomofuji T, Ekuni D, Azuma T, Tamaki N, Yamamoto T (2007) Oral administration of vitamin C prevents alveolar bone resorption induced by high dietary cholesterol in rats. J Periodontol 78:2165–2170PubMedGoogle Scholar
  126. 126.
    Staudte H, Güntsch A, Völpel A, Sigusch BW (2010) Vitamin C attenuates the cytotoxic effects of Porphyromonas gingivalis on human gingival fibroblasts. Arch Oral Biol 55:40–45PubMedGoogle Scholar
  127. 127.
    Chapple ILC, Matthews JB, Wright HJ, Scott AE, Griffiths HR, Grant MM (2012) Ascorbate and α-tocopherol differentially modulate reactive oxygen species generation by neutrophils in response to FcγR and TLR agonists. Innate Immun 0:1–8. doi: 10.1177/1753425912455207 Google Scholar
  128. 128.
    Tomofuji T, Ekuni D, Sanbe T, Irie K, Azuma T, Maruyama T, Tamaki N, Murakami J, Kokeguchi S, Yamamoto T (2009) Effects of vitamin C intake on gingival oxidative stress in rat periodontitis. Free Radic Biol Med 46:163–168PubMedGoogle Scholar
  129. 129.
    Akman S, Canakci V, Kara A, Tozoglu U, Arabaci T (2012) Therapeutic effects of alpha-lipoic acid and vitamin C on alveolar bone resorption after experimental periodontitis in rats. J Periodontol. doi: 10.1902/jop.2012.120252 Google Scholar
  130. 130.
    Neiva RF, Al-Shammari K, Nociti FH Jr, Soehren S, Wang H (2005) Effects of vitamin-B complex supplementation on periodontal wound healing. J Periodontol 76:1084–1091PubMedGoogle Scholar
  131. 131.
    Albina JE (1994) Nutrition and wound healing. J Parenter Enteral Nutr 18:367–376. doi: 10.1177/014860719401800417 Google Scholar
  132. 132.
    Yu YH, Kuo HK, Lai YL (2007) The association between serum folate levels and periodontal disease in older adults: data from the National Health and Nutrition Examination Survey 2001/02. J Am Geriatr Soc 55:108–113. doi: 10.1111/j.1532-5415.2006.01020.x PubMedGoogle Scholar
  133. 133.
    Esaki M, Morita M, Akhter R, Akino K, Honda O (2010) Relationship between folic acid intake and gingival health in non-smoking adults in Japan. Oral Dis 16:96–101. doi: 10.1111/j.1601-0825.2009.01619.x PubMedGoogle Scholar
  134. 134.
    Yoshihara A, Watanabe R, Nishimuta M, Hanada N, Miyazaki H (2005) The relationship between dietary intake and the number of teeth in elderly Japanese subjects. Gerodontology 22:211–218. doi: 10.1111/j.1741-2358.2005.00083.x PubMedGoogle Scholar
  135. 135.
    Erdemir EO, Bergstrom J (2006) Relationship between smoking and folic acid, vitamin B12 and some haematological variables in patients with chronic periodontal disease. J Clin Periodontol 33:878–884. doi: 10.1111/j.1600-051X.2006.01007.x PubMedGoogle Scholar
  136. 136.
    Erdemir EO, Bergstrom J (2007) Effect of smoking on folic acid and vitamin B12 after nonsurgical periodontal intervention. J Clin Periodontol 34:1074–1081. doi: 10.1111/j.1600-051X.2007.01154.x PubMedGoogle Scholar
  137. 137.
    da Costa M, Rothenberg S (1974) Appearance of folate binder in leukocytes and serum of women who are pregnant or taking oral contraceptives. J Lab Clin Med 83:207–214PubMedGoogle Scholar
  138. 138.
    Vogel RI, Fink RA, Schneider LC, Frank O, Baker H (1976) The effect of folic acid on gingival health. J Periodontol 47:667–668PubMedGoogle Scholar
  139. 139.
    Vogel RI, Fink RA, Frank O, Baker H (1978) The effect of topical application of folic acid on gingival health. J Oral Med 33:20–22Google Scholar
  140. 140.
    Pack AR, Thomson ME (1980) Effects of topical and systemic folic acid supplementation on gingivitis in pregnancy. J Clin Periodontol 7:402–414PubMedGoogle Scholar
  141. 141.
    Thomson ME, Pack AR (1982) Effects of extended systemic and topical folate supplementation on gingivitis of pregnancy. J Clin Periodontol 9:275–280PubMedGoogle Scholar
  142. 142.
    Pack AR (1984) Folate mouthwash: effects on established gingivitis in periodontal patients. J Clin Periodontol 11:619–628PubMedGoogle Scholar
  143. 143.
    Booth SL (2009) Roles for vitamin K beyond coagulation. Annu Rev Nutr 29:89–110. doi: 10.1146/annurev-nutr-080508-141217 PubMedGoogle Scholar
  144. 144.
    Rawlinson A, Walsh TF, Lee A, Hodges SJ (1998) Phyltoquinone in gingival crevicular fluid in adult periodontitis. J Clin Periodontol 25:662–665PubMedGoogle Scholar
  145. 145.
    Hojo K, Nagaoka S, Murata S, Taketomo N, Ohshima T, Maeda N (2007) Reduction of vitamin K concentration by salivary Bifidobacterium strains and their possible nutritional competition with Porphyromonas gingivalis. J Appl Microbiol 103:1969–1974. doi: 10.1111/j.1365-2672.2007.03436.x PubMedGoogle Scholar
  146. 146.
    D’Ambrosio DN, Clugston RD, Blaner WS (2011) Vitamin A metabolism: an update. Nutrients 3:63–103. doi: 10.3390/nu3010063 PubMedCentralPubMedGoogle Scholar
  147. 147.
    Freeland JH, Cousins RJ, Schwartz R (1976) Relationship of mineral status and intake to periodontal disease. Am J Clin Nutr 29:745–749PubMedGoogle Scholar
  148. 148.
    Linden GJ, McClean KM, Woodside JV, Patterson CC, Evans A, Young IS, Kee F (2009) Antioxidants and periodontitis in 60–70-year-old men. J Clin Periodontol 36:843–849. doi: 10.1111/j.1600-051X.2009.01468.x PubMedGoogle Scholar
  149. 149.
    Wood N, Johnson RB (2004) The relationship between tomato intake and congestive heart failure risk in periodontitis subjects. J Clin Periodontol 31:574–580. doi: 10.1111/j.1600-051X.2004.00531.x PubMedGoogle Scholar
  150. 150.
    Chandra RV, Prabhuji MLV, Roopa DA, Ravirajan S, Kishore HC (2007) Efficacy of lycopene in the treatment of gingivitis: a randomised placebo-controlled clinical Trial. Oral Health Prev Dent 5:327–336PubMedGoogle Scholar
  151. 151.
    Cheraskin E, Ringsdorf WM (1970) Relationship of reported oral symptoms and signs versus daily vitamin E consumption. Oral Surg Oral Med Oral Pathol 29:361–364. doi: 10.1016/0030-4220(70)90134-9 PubMedGoogle Scholar
  152. 152.
    Battino M, Ferreiro M-S, Bompadre S, Leone L, Mosca F, Bullon P (2001) Elevated hydroperoxide levels and antioxidants patterns in Papillon-Lefèvre syndrome. J Periodontol 72:1760–1766. doi: 10.1902/jop.2001.72.12.1760 PubMedGoogle Scholar
  153. 153.
    Hewitt C, McCormick D, Linden G, Turk D, Stern I, Wallace I, Southern L, Zhang L, Howard R, Bullon P, Wong M, Widmer R, Gaffar KA, Awawdeh L, Briggs J, Yaghmai R, Jabs EW, Hoeger P, Bleck O, Rüdiger SG, Petersilka G, Battino M, Brett P, Hattab F, Al-Hamed M, Sloan P, Toomes C, Dixon M, James J, Read AP, Thakker N (2004) The role of cathepsin C in Papillon-Lefèvre syndrome, prepubertal periodontitis, and aggressive periodontitis. Hum Mutat 23:222–228PubMedGoogle Scholar
  154. 154.
    Battino M, Ferreiro MS, Quiles JL, Bompadre S, Leone L, Bullon P (2003) Alterations in the oxidation products, antioxidant markers, antioxidant capacity and lipid patterns in plasma of patients affected by Papillon-Lefèvre syndrome. Free Radic Res 37:603–609PubMedGoogle Scholar
  155. 155.
    Slade EW Jr, Bartuska D, Rose LF, Cohen DW (1976) Vitamin E and periodontal disease. J Periodontol 32:1072–1077Google Scholar
  156. 156.
    Goodson JM, Bowles D (1973) The effect of α-tocopherol on sulcus fluid flow in periodontal disease. J Dent Res 52:217 (abstract)Google Scholar
  157. 157.
    Cerna H, Fiala B, Fingerov H, Pohanka J, Szwarcova E (1984) Contribution to indication of total therapy with vitamin E in chronic periodontal disease. Acta Univ Palacki Olomuc Fac Med 107:167–170PubMedGoogle Scholar
  158. 158.
    Cohen RE, Ciancio SG, Mather ML, Curro FA (1991) Effect of vitamin E gel, placebo gel, and chlorhexidine on periodontal diseases. Clin Prev Dent 13:20–24PubMedGoogle Scholar
  159. 159.
    Sheikhi M, Bouhafs RKL, Hammarström KJ, Jarstrand C (2001) Lipid peroxidation caused by oxygen radicals from Fusobacterium-stimulated neutrophils as a possible model for the emergence of periodontitis. Oral Dis 7:41–46PubMedGoogle Scholar
  160. 160.
    Cohen ME, Meyer DM (1993) Effect of dietary vitamin E supplementation and rotational stress on alveolar bone loss in rice rats. Arch Oral Biol 38:601–606. doi: 10.1016/0003-9969(93)90126-7 PubMedGoogle Scholar
  161. 161.
    Carvalho RS, de Souza CM, Neves JCS, Holanda-Pinto SA, Pinto LMS, Brito GAC, de Andrade GM (2013) Vitamin E does not prevent bone loss and induced anxiety in rats with ligature-induced periodontitis. Arch Oral Biol 58:50–58. doi: 10.1016/jarchoralbio.2012.04.020 Google Scholar
  162. 162.
    Liu K, Meng H, Tang X, Xu L, Zhang L, Chen Z, Shi D, Feng X, Lu R (2009) Elevated plasma calcifediol is associated with aggressive periodontitis. J Periodontol 80:1114–1120. doi: 10.1902/jop.2009.080675 PubMedGoogle Scholar
  163. 163.
    Millen AE, Hovey KM, LaMonte MJ, Swanson M, Andrews CA, Kluczynski MA, Genco RJ, Wactawski-Wende J (2012) Plasma 25-hydroxyvitamin D concentrations and periodontal disease in postmenopausal women. J Periodontol. doi: 10.1902/jop.2012.120445 PubMedCentralGoogle Scholar
  164. 164.
    Kyeyune-Nyombi E, Lau KH, Baylink DJ, Strong DD (1991) 1,25-Dihydroxyvitamin D3 stimulates both alkaline phosphatase gene transcription and mRNA stability in human bone cells. Arch Biochem Biophys 291:316–325PubMedGoogle Scholar
  165. 165.
    Ryhänen S, Mahonen A, Jääskeläinen T, Mäenpäá PH (1996) Synthetic 20-epi analogs of calcitriol are potent inducers of target-gene activation in osteoblastic cells. Eur J Biochem 238:97–103PubMedGoogle Scholar
  166. 166.
    Christakos S, Dhawan P, Liu Y, Peng X, Porta A (2003) New insights into the mechanisms of vitamin D action. J Cell Biochem 88:695–705. doi: 10.1002/jcb.10423 PubMedGoogle Scholar
  167. 167.
    Takahashi E, Nakagawa K, Suhara Y et al (2006) Biological activities of 2alpha-substituted analogues of 1alpha, 25-dihydroxyvitamin D3 in transcriptional regulation and human promyelocytic leukemia (HL-60) cell proliferation and differentiation. Biol Pharm Bull 29:2246–2250PubMedGoogle Scholar
  168. 168.
    Wang TT, Nestel FP, Bourdeau V, Nagai Y, Wang Q, Liao J, Tavera-Mendoza L, Lin R, Hanrahan JW, Mader S, White JH (2004) Cutting edge: 1,25-dihydroxyvitamin D3 is a direct inducer of antimicrobial peptide gene expression. J Immunol 173:2909–2912PubMedGoogle Scholar
  169. 169.
    Liu PT, Stenger S, Li H, Wenzel L, Tan BH, Krutzik SR, Ochoa MT, Schauber J, Wu K, Meinken C, Kamen DL, Wagner M, Bals R, Steinmeyer A, Zügel U, Gallo RL, Eisenberg D, Hewison M, Hollis BW, Adams JS, Bloom BR, Modlin RL (2006) Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311:1770–1773PubMedGoogle Scholar
  170. 170.
    Mora JR, Iwata M, von Andrian UH (2008) Vitamin effects on the immune system: vitamins A and D take centre stage. Nat Rev Immunol 8:685–698. doi: 10.1038/nri2378 PubMedCentralPubMedGoogle Scholar
  171. 171.
    Bikle DD (2009) Vitamin D and immune function: understanding common pathways. Curr Osteoporos Rep 7:58–63. doi: 10.1007/s11914-009-0011-6 PubMedGoogle Scholar
  172. 172.
    Kamen DL, Tangpricha V (2010) Vitamin D and molecular actions on the immune system: modulation of innate and autoimmunity. J Mol Med 88:441–450PubMedCentralPubMedGoogle Scholar
  173. 173.
    Rigby WF, Stacy T, Fanger MW (1984) Inhibition of T lymphocyte mitogenesis by 1,25-dihydroxyvitamin D3 (calcitriol). J Clin Invest 74:1451–1455PubMedCentralPubMedGoogle Scholar
  174. 174.
    Chen S, Sims GP, Chen XX, Gu YY, Chen S, Lipsky PE (2007) Modulatory effects of 1,25-dihydroxyvitamin D3 on human B cell differentiation. J Immunol 179:1634–1647. doi: 10.1016/0003-9969(93)90126-7 PubMedGoogle Scholar
  175. 175.
    Daniel C, Sartory NA, Zahn N, Radeke HH, Stein JM (2008) Immune modulatory treatment of trinitrobenzene sulfonic acid colitis with calcitriol is associated with a change of a T helper (Th) 1/Th17 to a Th2 and regulatory T cell profile. J Pharmacol Exp Ther 324:23–33. doi: 10.1124/jpet.107.127209 PubMedGoogle Scholar
  176. 176.
    Bhalla AK, Amento EP, Krane SM (1986) Differential effects of 1, 25-dihydroxyvitamin D3 on human lymphocytes and monocyte/macrophages: inhibition of interleukin-2 and augmentation of interleukin-1 production. Cell Immunol 98:311–322. doi: 10.1016/0008-8749(86)90291-1 PubMedGoogle Scholar
  177. 177.
    Boonstra A, Barrat FJ, Crain C, Heath VL, Savelkoul HF, O'Garra A (2001) 1α,25-Dihydroxyvitamin d3 has a direct effect on naive CD4(+) T cells to enhance the development of Th2 cells. J Immunol 167:4974–4980PubMedGoogle Scholar
  178. 178.
    Dietrich T, Kaumudi J, Joshipura KJ, Dawson-Hughes B, Bischoff-Ferrari HA (2004) Association between serum concentrations of 25-hydroxyvitamin D3 and periodontal disease in the US population. Am J Clin Nutr 80:108–113PubMedGoogle Scholar
  179. 179.
    US Department of Health and Human Services, National Center for Health Statistics (1996) NHANES III reference manuals and reports (CDROM). Centers for Disease Control and Prevention, HyattsvilleGoogle Scholar
  180. 180.
    Drury TF, Winn DM, Snowden CB, Kingman A, Kleinman DV, Lewis B (1996) An overview of the oral health component of the 1988-1991 National Health and Nutrition Examination Survey (NHANES III-Phase 1). J Dent Res 75:620–630PubMedGoogle Scholar
  181. 181.
    Tomar SL, Asma S (2000) Smoking-attributable periodontitis in the United States: findings from NHANES III. National Health and Nutrition Examination Survey. J Periodontol 71:743–751. doi: 10.1902/jop.2000.71.5.743 PubMedGoogle Scholar
  182. 182.
    Amarasena N, Yoshihara A, Hirotomi T, Takano N, Miyazaki H (2008) Association between serum calcium and periodontal disease progression in non-institutionalized elderly. Gerodontology 25:245–250. doi: 10.1111/j.1741-2358.2007.00211.x PubMedGoogle Scholar
  183. 183.
    Nishida M, Grossi SG, Dunford RG, Ho AW, Trevisan M, Genco RJ (2000) Calcium and the risk for periodontal disease. J Periodontol 71:1057–1066. doi: 10.1902/jop.2000.71.7.1057 PubMedGoogle Scholar
  184. 184.
    Takahashi O, Yoshihara A, Nakamura K, Miyazakia H (2012) Association between periodontitis and systemic bone mineral density in Japanese community-dwelling postmenopausal women. J Dent 40:304–311. doi: 10.1016/j.jdent.2012.01.005 PubMedGoogle Scholar
  185. 185.
    Famili P, Cauley J, Suzuki JB, Weyant R (2005) Longitudinal study of periodontal disease and edentulism with rates of bone loss in older women. J Periodontol 76:11–15. doi: 10.1902/jop.2005.76.1.11 PubMedCentralPubMedGoogle Scholar
  186. 186.
    Adegboye ARA, Fiehn N-E, Twetman S, Christensen LB, Heitmann BL (2010) Low calcium intake is related to increased risk of tooth loss in men. J Nutr 140:1864–1868. doi: 10.3945/jn.109.117770 PubMedGoogle Scholar
  187. 187.
    Adegboye ARA, Christensen LB, Holm-Pedersen P, Avlund K, Boucher BJ, Heitmann BL (2012) Intake of dairy products in relation to periodontitis in older Danish adults. Nutrients 4:1219–1229. doi: 10.3390/nu4091219 PubMedCentralPubMedGoogle Scholar
  188. 188.
    Al-Zahrani MS (2006) Increased intake of dairy products is related to lower periodontitis prevalence. J Periodontol 77:289–294. doi: 10.1902/jop.2006.050082 PubMedGoogle Scholar
  189. 189.
    Miley DD, Garcia MN, Hildebolt CF, Shannon WD, Couture RA, Anderson Spearie CL, Dixon DA, Langenwalter EM, Mueller C, Civitelli R (2009) Cross-sectional study of vitamin D and calcium supplementation effects on chronic periodontitis. J Periodontol 80:1433–1439. doi: 10.1902/jop.2009.090077 PubMedCentralPubMedGoogle Scholar
  190. 190.
    Wical KE, Brussee P (1979) Effects of a calcium and vitamin D supplement on alveolar ridge resorption in immediate denture patients. J Prosthet Dent 41:4–11. doi: 10.1016/0022-3913(79)90347-0 PubMedGoogle Scholar
  191. 191.
    Shoji K, Ohtsuka-Isoya M, Horiuchi H, Shinoda H (2000) Bone mineral density of alveolar bone in rats during pregnancy and lactation. J Periodontol 71:1073–1078. doi: 10.1902/jop.2000.71.7.1073 PubMedGoogle Scholar
  192. 192.
    Shoji K, Ohtsuka-Isoya M, Shimauchi H, Shinoda H (2007) Effects of lactation on alveolar bone loss in experimental periodontitis. J Periodontol 78:152–156. doi: 10.1902/jop.2007.060037 PubMedGoogle Scholar
  193. 193.
    Messer HH, Goebel NK, Wilcox L (1981) A comparison of bone loss from different skeletal sites during acute calcium deficiency in mice. Arch Oral Biol 26:1001–1004. doi: 10.1016/0003-9969(81)90110-2 PubMedGoogle Scholar
  194. 194.
    Wang PL, Shirasu S, Shinohara M, Murakawa N, Endo M, Sakata S, Okamura M, Daito M, Ohura K (1998) Salivary amylase activity of rats fed a low calcium diet. Jpn J Pharmacol 78:279–283. doi: 10.1254/jjp.78.279 PubMedGoogle Scholar
  195. 195.
    Laires MJ, Monteiro CP, Bicho M (2004) Role of cellular magnesium in health and human disease. Front Biosci 1:262–276. doi: 10.2741/1223 Google Scholar
  196. 196.
    Yoshihara A, Iwasaki M, Miyazaki H (2011) Mineral content of calcium and magnesium in the serum and longitudinal periodontal progression in Japanese elderly smokers. J Clin Periodontol 38:992–997. doi: 10.1111/j.1600-051X.2011.01769.x PubMedGoogle Scholar
  197. 197.
    Meisel P, Schwahn C, Luedemann J, John U, Kroemer HK, Kocher T (2005) Magnesium deficiency is associated with periodontal disease. J Dent Res 84:937–941. doi: 10.1177/154405910508401012 PubMedGoogle Scholar
  198. 198.
    Erdemir EO, Erdemir A (2006) The detection of salivary minerals in smokers and non-smokers with chronic periodontitis by the inductively coupled plasma-atomic emission spectrophotometry technique. J Periodontol 77:990–995. doi: 10.1902/jop.2006.050202 PubMedGoogle Scholar
  199. 199.
    Cutler CW, Kalmar JR, Arnold RR (1991) Antibody-dependent alternate pathway of complement activation in opsonophagocytosis of Porphyromonas gingivalis. Infect Immun 59:2105–2109PubMedCentralPubMedGoogle Scholar
  200. 200.
    Barnard JP, Stinson AW (1999) Influence of environmental conditions on hydrogen peroxide formation by Streptococcus gordonii. Infect Immun 67:6558–6564PubMedCentralPubMedGoogle Scholar
  201. 201.
    Strålfors A, Thilander H, Bergenholt A (1967) Simultaneous inhibition of caries and periodontal disease in hamsters by disinfection, tooth-brushing or phosphate addition. Arch Oral Biol 12:1367–1371. doi: 10.1016/9969(67)90175-6 PubMedGoogle Scholar
  202. 202.
    Yamaoka M, Uematsu T, Shiba T, Matsuura T, Ono Y, Ishizuka M, Naramoto H, Takahashi M, Sugiura-Tomita M, Iguchi K, Yamashita S, Furusawa K (2008) Effect of inorganic polyphosphate in periodontitis in the elderly. Gerodontology 25:10–17. doi: 10.1111/j.1741-2358.2007.00185.x PubMedGoogle Scholar
  203. 203.
    Takami Y, Nakagaki H, Morita I, Tsuboi S, Takami S, Suzuki N, Niwa H, Ogura Y (2003) Blood test values and community periodontal index scores in medical checkup recipients. J Periodontol 74:1778–1784. doi: 10.1902/jop.2003.74.12.1778 PubMedGoogle Scholar
  204. 204.
    Craig RG, Yip JK, So MK, Boylan RJ, Socransky SS, Haffajee AD (2003) Relationship of destructive periodontal disease to the acute-phase response. J Periodontol 74:1007–1016. doi: 10.1902/jop.2003.74.7.1007 PubMedGoogle Scholar
  205. 205.
    Hatipoglu H, Hatipoglu MG, Cagirankaya LB, Caglayan F (2012) Severe periodontal destruction in a patient with advanced anemia: a case report. Eur J Dent 6:95–100PubMedCentralPubMedGoogle Scholar
  206. 206.
    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 28:930–936. doi: 10.1034/j.1600-051x.2001.028010930.x PubMedGoogle Scholar
  207. 207.
    Gokhale SR, Sumanth S, Padhye AM (2010) Evaluation of blood parameters in patients with chronic periodontitis for signs of anemia. J Periodontol 81:1202–1206. doi: 10.1902/jop.2010.100079 PubMedGoogle Scholar
  208. 208.
    Prakash S, Dhingra K, Priya S (2012) Similar hematological and biochemical parameters among periodontitis and control group subjects. Eur J Dent 6:287–294PubMedCentralPubMedGoogle Scholar
  209. 209.
    Lainson PA, Brady PP, Fraleigh CM (1968) Anemia, a systemic cause of periodontal disease? J Periodontol 39:35–38PubMedGoogle Scholar
  210. 210.
    Chawla TN, Kapoor KK, Teotia SP, Singh NK (1971) Anemia and periodontal disease – a correlative study. J Indian Dent Assoc 43:67–78PubMedGoogle Scholar
  211. 211.
    Siegel EH (1945) Total erythrocyte, leukocyte and differential white cell counts of blood in chronic periodontal disease. J Dent Res 24:270–271Google Scholar
  212. 212.
    Lee GR (1983) The anemia of chronic disease. Semin Hematol 20:61–80PubMedGoogle Scholar
  213. 213.
    Johansson I, Fagernäs C (1994) Effect of iron-deficiency anemia on saliva secretion rate and composition in the rat. Arch Oral Biol 39:51–56. doi: 10.1016/0003-9969(94)90034-5 PubMedGoogle Scholar
  214. 214.
    Tovaru S, Parlatescu I, Dumitriu AS, Bucur A, Kaplan I (2010) Oral complications associated with D-penicillamine treatment for Wilson disease: a clinicopathologic report. J Periodontol 81:1231–1236. doi: 10.1902/jop.2010.090736 PubMedGoogle Scholar
  215. 215.
    Spacciapoli P, Buxton D, Rothstein D, Friden P (2001) Antimicrobial activity of silver nitrate against periodontal pathogens. J Periodontal Res 36:108–113. doi: 10.1034/j.1600-0765.2001.360207.x PubMedGoogle Scholar
  216. 216.
    Tamura M, Ochiai K (2009) Zinc and copper play a role in coaggregation inhibiting action of Porphyromonas gingivalis. Oral Microbiol Immunol 24:56–63. doi: 10.1111/j.1399-302X.2008.00476.x PubMedGoogle Scholar
  217. 217.
    Olczak T, Maszczak-Seneczko D, Smalley JW, Olczak M (2012) Gallium(III), cobalt(III) and copper(II) protoporphyrin IX exhibit antimicrobial activity against Porphyromonas gingivalis by reducing planktonic and biofilm growth and invasion of host epithelial cells. Arch Microbiol 194:719–724. doi: 10.1007/s00203-012-0804-3 PubMedGoogle Scholar
  218. 218.
    De Souza AP, Gerlach RF, Line SRP (2000) Inhibition of human gingival gelatinases (MMP-2 and MMP-9) by metal salts. Dent Mater 16:103–108. doi: 10.1016/S0109-5641(99)00084-6 PubMedGoogle Scholar
  219. 219.
    Üçkardeş Y, Tekçiçek M, Özmert 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
  220. 220.
    Johnson DA, Alvares OF (1984) Zinc deficiency-induced changes in rat parotid salivary proteins. J Nutr 114:1955–1964PubMedGoogle Scholar
  221. 221.
    Orbak R, Kara C, Özbek E, Tezel A, Demir T (2007) Effects of zinc deficiency on oral and periodontal diseases in rats. J Periodontal Res 42:138–143. doi: 10.1111/j.1600-0765.2006.00939.x PubMedGoogle Scholar
  222. 222.
    Di Paola R, Emanuela Mazzon E, Rotondo R, Dattola F, Britti D, De Majo M, Genovese T, Cuzzocrea S (2005) Reduced development of experimental periodontitis by treatment with M40403, a superoxide dismutase mimetic. Eur J Pharmacol 516:151–157. doi: 10.1016/j.ephar.2005.04.039 PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Departamento de Fisiología, Instituto de Nutrición y Tecnología de los Alimentos “José Mataix Verdú,” Laboratorio 120, Parque Tecnológico de Ciencias de la SaludUniversidad de GranadaGranadaSpain

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