Relationship between renal function and periodontal disease in community-dwelling elderly women with different genotypes
Corresponding Author
Akihiro Yoshihara
Department of Oral Health and Welfare, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
Address:
Akihiro Yoshihara
Department of Oral Health and Welfare
Niigata University Graduate School of Medical and Dental Sciences
2-5274 Gakkocho-dori, Chuo-Ku
Niigata 951-8514
Japan
E-mail: [email protected]
Search for more papers by this authorNoriko Sugita
Department of Oral Biological Science, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
Search for more papers by this authorMasanori Iwasaki
Department of Community Oral Health Development, Kyushu Dental University, Kitakyushu, Fukuoka, Japan
Search for more papers by this authorYanming Wang
Department of Oral Biological Science, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
Search for more papers by this authorHideo Miyazaki
Department of Oral Health Science, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
Search for more papers by this authorHiromasa Yoshie
Department of Oral Biological Science, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
Search for more papers by this authorKazutoshi Nakamura
Department of Community Preventive Medicine, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
Search for more papers by this authorCorresponding Author
Akihiro Yoshihara
Department of Oral Health and Welfare, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
Address:
Akihiro Yoshihara
Department of Oral Health and Welfare
Niigata University Graduate School of Medical and Dental Sciences
2-5274 Gakkocho-dori, Chuo-Ku
Niigata 951-8514
Japan
E-mail: [email protected]
Search for more papers by this authorNoriko Sugita
Department of Oral Biological Science, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
Search for more papers by this authorMasanori Iwasaki
Department of Community Oral Health Development, Kyushu Dental University, Kitakyushu, Fukuoka, Japan
Search for more papers by this authorYanming Wang
Department of Oral Biological Science, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
Search for more papers by this authorHideo Miyazaki
Department of Oral Health Science, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
Search for more papers by this authorHiromasa Yoshie
Department of Oral Biological Science, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
Search for more papers by this authorKazutoshi Nakamura
Department of Community Preventive Medicine, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan
Search for more papers by this authorConflict of interest and source of funding statement
We certify that this research is original, not presently under consideration for publication elsewhere, free of conflicts of interest, and conducted in accordance with the highest principles of human subject and animal welfare.
This work was supported by a Grant-in-Aid from MEXT KAKENHI (No. 15H050560001, Tokyo, Japan).
Abstract
Objectives
The aim of this study was to examine the association between periodontal disease and renal function in elderly women with different genotypes.
Material and Methods
A total of 332 postmenopausal never-smoking women were analysed. Poor renal function was defined as serum cystatin C > 0.91 mg/l. Periodontal disease markers such as periodontal inflamed surface area (PISA) were evaluated. Selected variables, including PISA quartile, body mass index (BMI), HbA1C and age in Arg allele carriers and non-carriers based on the beta-3 adrenergic receptor, or between Ala allele carriers and non-carriers based on peroxisome proliferator-activated receptor gamma, were analysed using multiple logistic regression analysis.
Results
The odds ratios of serum cystatin C level and PISA (fourth quartile) were significantly positive for both Arg (2.52; p = 0.035) and Ala allele non-carriers (2.36; p = 0.021). A significant association was also found between serum cystatin C level and BMI for both Arg (1.18; p = 0.001) and Ala allele non-carriers (1.12; p = 0.003).
Conclusion
The results of this study suggest that periodontal inflammation might be associated with renal function. Furthermore, in both the Arg and Ala allele non-carriers, the associations between BMI and PISA for renal function became stronger.
References
- Altshuler, D., Hirschhorn, J. N., Klannemark, M., Lindgren, C. M., Vohl, M. C., Nemesh, J., Lane, C. R., Schaffner, S. F., Bolk, S., Brewer, C., Tuomi, T., Gaudet, D., Hudson, T. J., Daly, M., Groop, L. & Lander, E. S. (2000) The common PPARgamma Pro12Ala polymorphism is associated with decreased risk of type 2 diabetes. Nature Genetics 26, 76–80.
- Barbe, P., Millet, L., Galitzky, J., Lafontan, M. & Berlan, M. (1996) In situ assessment of the role of the beta 1-, beta 2- and beta 3-adrenoceptors in the control of lipolysis and nutritive blood flow in human subcutaneous adipose tissue. British Journal of Pharmacology 117, 907–913.
- Chambrone, L., Foz, A. M., Guglielmetti, M. R., Pannuti, C. M., Artese, H. P., Feres, M. & Romito, G. A. (2013) Periodontitis and chronic kidney disease: a systematic review of the association of diseases and the effect of periodontal treatment on estimated glomerular filtration rate. Journal of Clinical Periodontology 40, 443–456.
- da Costa, T. A., Silva, M. J., Alves, P. M., Chica, J. E., Barcelos, E. Z., Giani, M. A., Garlet, G. P., da Silva, J. S., Rodrigues Junior, V., Rodrigues, D. B. & Cardoso, C. R. (2015) Inflammation biomarkers of advanced disease in nongingival tissues of chronic periodontitis patients. Mediators of Inflammation 2015, 983782.
- Cypess, A. M., Lehman, S., Williams, G., Tal, I., Rodman, D., Goldfine, A. B., Kuo, F. C., Palmer, E. L., Tseng, Y. H., Doria, A., Kolodny, G. M. & Kahn, C. R. (2009) Identification and importance of brown adipose tissue in adult humans. The New England Journal of Medicine 360, 1509–1517.
- Dharnidharka, V. R., Kwon, C. & Stevens, G. (2002) Serum cystatin C is superior to serum creatinine as a marker of kidney function: a meta-analysis. American Journal of Kidney Diseases 40, 221–226.
- Etemadifar, R., Konarizadeh, S., Zarei, A., Farshidi, H. & Sobhani, A. (2015) Relationship between periodontal status and C-reactive protein and interleuckin-6 levels among atherosclerotic patients in Bandar Abbas, Iran in 2014. Electronic Physician 7, 1010–1016.
- Fisher, M. A., Taylor, G. W., West, B. T. & McCarthy, E. T. (2011) Bidirectional relationship between chronic kidney and periodontal disease: a study using structural equation modeling. Kidney International 79, 347–355.
- Fuentes, E., Guzman-Jofre, L., Moore-Carrasco, R. & Palomo, I. (2013) Role of PPARs in inflammatory processes associated with metabolic syndrome (Review). Molecular Medicine Reports 8, 1611–1616.
- Garaulet, M., Smith, C. E., Hernandez-Gonzalez, T., Lee, Y. C. & Ordovas, J. M. (2011) PPARgamma Pro12Ala interacts with fat intake for obesity and weight loss in a behavioural treatment based on the Mediterranean diet. Molecular Nutrition and Food Research 55, 1771–1779.
- Gjesing, A. P., Andersen, G., Burgdorf, K. S., Borch-Johnsen, K., Jorgensen, T., Hansen, T. & Pedersen, O. (2007) Studies of the associations between functional beta2-adrenergic receptor variants and obesity, hypertension and type 2 diabetes in 7,808 white subjects. Diabetologia 50, 563–568.
- Greenberg, A. S. & Obin, M. S. (2006) Obesity and the role of adipose tissue in inflammation and metabolism. The American Journal of Clinical Nutrition 83, 461S–465S.
- Grubb, A., Bjork, J., Lindstrom, V., Sterner, G., Bondesson, P. & Nyman, U. (2005b) A cystatin C-based formula without anthropometric variables estimates glomerular filtration rate better than creatinine clearance using the Cockcroft-Gault formula. Scandinavian Journal of Clinical and Laboratory Investigation 65, 153–162.
- Grubb, A., Nyman, U., Bjork, J., Lindstrom, V., Rippe, B., Sterner, G. & Christensson, A. (2005a) Simple cystatin C-based prediction equations for glomerular filtration rate compared with the modification of diet in renal disease prediction equation for adults and the Schwartz and the Counahan-Barratt prediction equations for children. Clinical Chemistry 51, 1420–1431.
- Hara, K., Okada, T., Tobe, K., Yasuda, K., Mori, Y., Kadowaki, H., Hagura, R., Akanuma, Y., Kimura, S., Ito, C. & Kadowaki, T. (2000) The Pro12Ala polymorphism in PPAR gamma2 may confer resistance to type 2 diabetes. Biochemical and Biophysical Research Communications 271, 212–216.
- Hirano, E., Sugita, N., Kikuchi, A., Shimada, Y., Sasahara, J., Iwanaga, R., Tanaka, K. & Yoshie, H. (2012) The association of Aggregatibacter actinomycetemcomitans with preeclampsia in a subset of Japanese pregnant women. Journal of Clinical Periodontology 39, 229–238.
- Hsu, C. Y., Chertow, G. M. & Curhan, G. C. (2002) Methodological issues in studying the epidemiology of mild to moderate chronic renal insufficiency. Kidney International 61, 1567–1576.
- Iwasaki, M., Taylor, G. W., Nesse, W., Vissink, A., Yoshihara, A. & Miyazaki, H. (2012) Periodontal disease and decreased kidney function in Japanese elderly. American Journal of Kidney Diseases 59, 202–209.
- Katz, M. H. (2006) Multivariable Analysis, a Practical Guide for Clinicians 2nd edition, pp. 87–88. Cambridge: Cambridge University Press.
- Kaufmann, J., Martinka, P., Moede, O., Sendeski, M., Steege, A., Fahling, M., Hultstrom, M., Gaestel, M., Moraes-Silva, I. C., Nikitina, T., Liu, Z. Z., Zavaritskaya, O. & Patzak, A. (2015) Noradrenaline enhances angiotensin II responses via p38 MAPK activation after hypoxia/re-oxygenation in renal interlobar arteries. Acta Physiologica 213, 920–932.
- Lapice, E., Monticelli, A., Cocozza, S., Pinelli, M., Cocozza, S., Bruzzese, D., Riccardi, G. & Vaccaro, O. (2015) The PPARgamma2 Pro12Ala variant is protective against progression of nephropathy in people with type 2 diabetes. Journal of Translational Medicine 13, 85.
- de Luis, D. A., Aller, R., Izaola, O., Gonzalez Sagrado, M. & Conde, R. (2008) Relation of Trp64Arg polymorphism of beta 3-adrenergic receptor gene to adipocytokines and fat distribution in obese patients. Annals of Nutrition & Metabolism 52, 267–271.
- Maeda, A., Gohda, T., Funabiki, K., Horikoshi, S. & Tomino, Y. (2004) Peroxisome proliferator-activated receptor gamma gene polymorphism is associated with serum triglyceride levels and body mass index in Japanese type 2 diabetic patients. Journal of Clinical Laboratory Analysis 18, 317–321.
- Malta, M., Cardoso, L. O., Bastos, F. I., Magnanini, M. M. & Silva, C. M. (2010) STROBE initiative: guidelines on reporting observational studies. Revista de Saude Publica 44, 559–565.
- Masud, S. & Ye, S. (2003) Effect of the peroxisome proliferator activated receptor-gamma gene Pro12Ala variant on body mass index: a meta-analysis. Journal of Medical Genetics 40, 773–780.
- Masuo, K. & Lambert, G. W. (2011) Relationships of adrenoceptor polymorphisms with obesity. Journal of Obesity 2011, 609485.
- Nanba, S., Okuda, Y., Tanaka, M., Kanbara, K., Fujisawa, M. & Yoshino, G. (2002) Development of latex agglutination method for the quantitative determination of cystatin C in serum and urine. Journal of Medicine and Pharmaceutical Science 48, 685–692.
- Nesse, W., Abbas, F., van der Ploeg, I., Spijkervet, F. K., Dijkstra, P. U. & Vissink, A. (2008) Periodontal inflamed surface area: quantifying inflammatory burden. Journal of Clinical Periodontology 35, 668–673.
- Porter, S. R., Scully, C. & Hegarty, A. M. (2004) An update of the etiology and management of xerostomia. Oral surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics 97, 28–46.
- Procino, G., Carmosino, M., Milano, S., Dal Monte, M., Schena, G., Mastrodonato, M., Gerbino, A., Bagnoli, P. & Svelto, M. (2016) β3 adrenergic receptor in the kidney may be a new player in sympathetic regulation of renal function. Kidney International 90, 555–567.
- Rankinen, T., Zuberi, A., Chagnon, Y. C., Weisnagel, S. J., Argyropoulos, G., Walts, B., Perusse, L. & Bouchard, C. (2006) The human obesity gene map: the 2005 update. Obesity 14, 529–644.
- Ritchie, C. S. (2007) Obesity and periodontal disease. Periodontology 2000 44, 154–163.
- Rizvi, S., Raza, S. T. & Mahdi, F. (2014) Association of genetic variants with diabetic nephropathy. World Journal of Diabetes 5, 809–816.
- Stelzl, U., Worm, U., Lalowski, M., Haenig, C., Brembeck, F. H., Goehler, H., Stroedicke, M., Zenkner, M., Schoenherr, A., Koeppen, S., Timm, J., Mintzlaff, S., Abraham, C., Bock, N., Kietzmann, S., Goedde, A., Toksoz, E., Droege, A., Krobitsch, S., Korn, B., Birchmeier, W., Lehrach, H. & Wanker, E. E. (2005) A human protein-protein interaction network: a resource for annotating the proteome. Cell 122, 957–968.
- Susanto, H., Nesse, W., Dijkstra, P. U., Agustina, D., Vissink, A. & Abbas, F. (2011) Periodontitis prevalence and severity in Indonesians with type 2 diabetes. Journal of Periodontology 82, 550–557.
- WHO (1997) Oral Health Surveys – Basic Methods, 4th edition, pp. 38–39. Geneva: World Health Organization.
- Yamauchi, T., Kuno, T., Takada, H., Mishima, K., Nagura, Y., Takahashi, S. & Kanmatsuse, K. (2001) The impact of Trp64Arg mutation in the beta3-adrenergic receptor gene on haemodialysis patients. Nephrology, Dialysis, Transplantation 16, 641–642.
- Yoshihara, A., Iwasaki, M., Miyazaki, H. & Nakamura, K. (2014) Association between low renal function and tooth loss over 5 years. Gerodontology 31, 111–116.
Citing Literature
