Periodontal Disease in Patients Receiving Dialysis
Abstract
:1. Introduction
2. Peritoneal Dialysis
2.1. Impact of Periodontal Disease
2.2. Impact of Periodontal Care and Treatment
3. Hemodialysis
3.1. Correlations with Blood Test Indices
3.1.1. Serum CRP Levels
3.1.2. Serum Albumin Levels
3.1.3. Calcium, Phosphorus, Alkaline Phosphatase, and PTH
3.1.4. Hematological Data
3.2. Correlation with Duration of HD
3.3. Correlation with an Immune Response
3.4. Correlation with Cardiovascular Diseases, Metabolic Syndromes, and Pneumonia
3.4.1. Cardiovascular Disease
3.4.2. Metabolic Syndromes and Pneumonia
3.5. Diabetic and Non-Diabetic Nephropathy
3.5.1. Comparison of the Prevalence
3.5.2. Objective and Subjective Manifestations
3.5.3. The Community Periodontal Index and DMFT Index
3.5.4. Properties of Saliva
3.6. Periodontal Indices and Salivary Status with Peritoneal Dialysis
4. Management of Periodontal Disease
5. Conclusions and Future Perspectives
Funding
Acknowledgments
Conflicts of Interest
References
- Fenton, S.S.; Schaubel, D.E.; Desmeules, M.; Morrison, H.I.; Mao, Y.; Copleston, P.; Jeffery, J.R.; Kjellstrand, C.M. Hemodialysis versus peritoneal dialysis: A comparison of adjusted mortality rates. Am. J. Kidney Dis. 1997, 30, 334–342. [Google Scholar] [CrossRef]
- Pihlstrom, B.L.; Michalowicz, B.S.; Johnson, N.W. Periodontal diseases. Lancet 2005, 366, 1809–1820. [Google Scholar] [CrossRef] [Green Version]
- Kshirsagar, A.V.; Craig, R.G.; Moss, K.L.; Beck, J.D.; Offenbacher, S.; Kotanko, P.; Klemmer, P.J.; Yoshino, M.; Levin, N.W.; Yip, J.K.; et al. Periodontal disease adversely affects the survival of patients with end-stage renal disease. Kidney Int. 2009, 75, 746–751. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Borawski, J.; Wilczyńska-Borawska, M.; Stokowska, W.; Myśliwiec, M. The periodontal status of pre-dialysis chronic kidney disease and maintenance dialysis patients. Nephrol. Dial. Transplant. 2007, 22, 457–464. [Google Scholar] [CrossRef] [PubMed]
- Kocyigit, I.; Yucel, H.E.; Cakmak, O.; Dogruel, F.; Durukan, D.B.; Korkar, H.; Unal, A.; Sipahioglu, M.H.; Oymak, O.; Gurgan, C.A.; et al. An ignored cause of inflammation in patients undergoing continuous ambulatory peritoneal dialysis: Periodontal problems. Int. Urol. Nephrol. 2014, 46, 2021–2028. [Google Scholar] [CrossRef] [PubMed]
- Cengiz, M.I.; Bal, S.; Gökçay, S.; Cengiz, K. Does periodontal disease reflect atherosclerosis in continuous ambulatory peritoneal dialysis patients? J. Periodontol. 2007, 78, 1926–1934. [Google Scholar] [CrossRef] [PubMed]
- Thorman, R.; Neovius, M.; Hylander, B. Clinical findings in oral health during progression of chronic kidney disease to end-stage renal disease in a Swedish population. Scand. J. Urol. Nephrol. 2009, 43, 154–159. [Google Scholar] [CrossRef]
- Brito, F.; Almeida, S.; Figueredo, C.M.; Bregman, R.; Suassuna, J.H.; Fischer, R.G. Extent and severity of chronic periodontitis in chronic kidney disease patients. J. Periodontal. Res. 2012, 47, 426–430. [Google Scholar] [CrossRef]
- Kim, Y.J.; Moura, L.M.; Caldas, C.P.; Perozini, C.; Ruivo, G.F.; Pallos, D. Evaluation of periodontal condition and risk in patients with chronic kidney disease on hemodialysis. Einstein (Sao Paulo) 2017, 15, 173–177. [Google Scholar] [CrossRef] [Green Version]
- Cholewa, M.; Madziarska, K.; Radwan-Oczko, M. The association between periodontal conditions, inflammation, nutritional status and calcium-phosphate metabolism disorders in hemodialysis patients. J. Appl. Oral Sci. 2018, 26, e20170495. [Google Scholar] [CrossRef]
- Chen, L.P.; Chiang, C.K.; Peng, Y.S.; Hsu, S.P.; Lin, C.Y.; Lai, C.F.; Hung, K.Y. Relationship between periodontal disease and mortality in patients treated with maintenance hemodialysis. Am. J. Kidney Dis. 2011, 57, 276–282. [Google Scholar] [CrossRef]
- Yazdi, F.K.; Karimi, N.; Rasouli, M.; Roozbeh, J. Effect of nonsurgical periodontal treatment on C-reactive protein levels in maintenance hemodialysis patients. Ren. Fail. 2013, 35, 711–717. [Google Scholar] [CrossRef]
- Rodrigues, V.P.; Libério, S.A.; Lopes, F.F.; Thomaz, E.B.; Guerra, R.N.; Gomes-Filho, I.S.; Pereira, A.L. Periodontal status and serum biomarkers levels in haemodialysis patients. J. Clin. Periodontol. 2014, 41, 862–868. [Google Scholar] [CrossRef]
- Iwasaki, M.; Borgnakke, W.S.; Awano, S.; Yoshida, A.; Hamasaki, T.; Teratani, G.; Kataoka, S.; Kakuta, S.; Soh, I.; Ansai, T.; et al. Periodontitis and health-related quality of life in hemodialysis patients. Clin. Exp. Dent. Res. 2016, 3, 13–18. [Google Scholar] [CrossRef]
- Bayraktar, G.; Kurtulus, I.; Duraduryan, A.; Cintan, S.; Kazancioglu, R.; Yildiz, A.; Bural, C.; Bozfakioglu, S.; Besler, M.; Trablus, S.; et al. Dental and periodontal findings in hemodialysis patients. Oral Dis. 2007, 13, 393–397. [Google Scholar] [CrossRef]
- Cengiz, M.I.; Sümer, P.; Cengiz, S.; Yavuz, U. The effect of the duration of the dialysis in hemodialysis patients on dental and periodontal findings. Oral Dis. 2009, 15, 336–341. [Google Scholar] [CrossRef]
- Altamimi, A.G.; AlBakr, S.A.; Alanazi, T.A.; Alshahrani, F.A.; Chalisserry, E.P.; Anil, S. Prevalence of periodontitis in patients undergoing hemodialysis: A case control study. Mater. Sociomed. 2018, 30, 58–61. [Google Scholar] [CrossRef]
- Boros, P.; Miller, C.M. Hepatocyte growth factor: A multifunctional cytokine. Lancet 1995, 345, 293–295. [Google Scholar] [CrossRef]
- Ohshima, M.; Noguchi, Y.; Ito, M.; Maeno, M.; Otsuka, K. Hepatocyte growth factor secreted by periodontal ligament and gingival fibroblasts is a major chemoattractant for gingival epithelial cells. J. Periodontal. Res. 2001, 36, 377–383. [Google Scholar] [CrossRef]
- Ohshima, M.; Fujikawa, K.; Akutagawa, H.; Kato, T.; Ito, K.; Otsuka, K. Hepatocyte growth factor in saliva: A possible marker for periodontal disease status. J. Oral Sci. 2002, 44, 35–39. [Google Scholar] [CrossRef]
- Ohshima, M.; Sakai, A.; Ito, K.; Otsuka, K. Hepatocyte growth factor (HGF) in periodontal disease: Detection of HGF in gingival crevicular fluid. J. Periodontal. Res. 2002, 37, 8–14. [Google Scholar] [CrossRef]
- Wilczyńska-Borawska, M.; Borawski, J.; Bagińska, J.; Małyszko, J.; Myśliwiec, M. Hepatocyte growth factor in saliva of patients with renal failure and periodontal disease. Ren. Fail. 2012, 34, 942–951. [Google Scholar] [CrossRef]
- Tasdemir, Z.; Özsarı Tasdemir, F.; Gürgan, C.; Eroglu, E.; Gunturk, I.; Kocyigit, I. The effect of periodontal disease treatment in patients with continuous ambulatory peritoneal dialysis. Int. Urol. Nephrol. 2018, 50, 1519–1528. [Google Scholar] [CrossRef]
- Keles, M.; Tozoglu, U.; Uyanik, A.; Eltas, A.; Bayindir, Y.Z.; Cetinkaya, R.; Bilge, O.M. Does peritoneal dialysis affect halitosis in patients with end-stage renal disease? Perit. Dial. Int. 2011, 31, 168–172. [Google Scholar]
- Trimarchi, H.; Dicugno, M.; Muryan, A.; Lombi, F.; Iturbe, L.; Raña, M.S.; Young, P.; Nau, K.; Iriarte, R.; Pomeranz, V.; et al. Pro-calcitonin and inflammation in chronic hemodialysis. Medicina (B Aires) 2013, 73, 411–416. [Google Scholar]
- Guo, M.; Chen, R.; Xiang, F.; Cao, X.; Hu, J.; Lu, Z.; Gong, S.; Chen, X.; Chen, X.; Ding, X.; et al. Decreased percentage of memory B cells is independently associated with increased susceptibility to infection in patients on maintenance hemodialysis. Int. Urol. Nephrol. 2018, 50, 2081–2090. [Google Scholar] [CrossRef]
- Omari, A.M.; Omari, L.S.; Dagash, H.H.; Sweileh, W.M.; Natour, N.; Zyoud, S.H. Assessment of nutritional status in the maintenance of haemodialysis patients: A cross-sectional study from Palestine. BMC Nephrol. 2019, 20, 92. [Google Scholar] [CrossRef]
- Noack, B.; Genco, R.J.; Trevisan, M.; Grossi, S.; Zambon, J.J.; De Nardin, E. Periodontal infections contribute to elevated systemic C-reactive protein level. J. Periodontol. 2001, 72, 1221–1227. [Google Scholar] [CrossRef]
- D’Aiuto, F.; Nibali, L.; Parkar, M.; Suvan, J.; Tonetti, M.S. Short-term effects of intensive periodontal therapy on serum inflammatory markers and cholesterol. J. Dent. Res. 2005, 84, 269–273. [Google Scholar] [CrossRef]
- Kadiroglu, A.K.; Kadiroglu, E.T.; Sit, D.; Dag, A.; Yilmaz, M.E. Periodontitis is an important and occult source of inflammation in hemodialysis patients. Blood. Purif. 2006, 24, 400–404. [Google Scholar] [CrossRef]
- Zhao, D.; Zhang, S.; Chen, X.; Liu, W.; Sun, N.; Guo, Y.; Dong, Y.; Mo, A.; Yuan, Q. Evaluation of periodontitis and bone loss in patients undergoing hemodialysis. J. Periodontol. 2014, 85, 1515–1520. [Google Scholar] [CrossRef]
- Franek, E.; Blaschyk, R.; Kolonko, A.; Mazur-Psonka, L.; Łangowska-Adamczyk, H.; Kokot, F.; Wiecek, A. Chronic periodontitis in hemodialysis patients with chronic kidney disease is associated with elevated serum C-reactive protein concentration and greater intima-media thickness of the carotid artery. J. Nephrol. 2006, 19, 346–351. [Google Scholar]
- Kshirsagar, A.V.; Craig, R.G.; Beck, J.D.; Moss, K.; Offenbacher, S.; Kotanko, P.; Yoshino, M.; Levin, N.W.; Yip, J.K.; Almas, K.; et al. Severe periodontitis is associated with low serum albumin among patients on maintenance hemodialysis therapy. Clin. J. Am. Soc. Nephrol. 2007, 2, 239–244. [Google Scholar] [CrossRef]
- Pallos, D.; Leão, M.V.; Togeiro, F.C.; Alegre, L.; Ricardo, L.H.; Perozini, C.; Ruivo, G.F. Salivary markers in patients with chronic renal failure. Arch. Oral Biol. 2015, 60, 1784–1788. [Google Scholar] [CrossRef]
- Chen, L.P.; Chiang, C.K.; Chan, C.P.; Hung, K.Y.; Huang, C.S. Does periodontitis reflect inflammation and malnutrition status in hemodialysis patients? Am. J. Kidney Dis. 2006, 47, 815–822. [Google Scholar] [CrossRef]
- Hou, Y.; Wang, X.; Zhang, C.X.; Wei, Y.D.; Jiang, L.L.; Zhu, X.Y.; Du, Y.J. Risk factors of periodontal disease in maintenance hemodialysis patients. Medicina (Baltim.) 2017, 96, e7892. [Google Scholar] [CrossRef]
- de Souza, C.M.; Braosi, A.P.; Luczyszyn, S.M.; Olandoski, M.; Kotanko, P.; Craig, R.G.; Trevilatto, P.C.; Pecoits-Filho, R. Association among oral health parameters, periodontitis, and its treatment and mortality in patients undergoing hemodialysis. J. Periodontol. 2014, 85, e169–178. [Google Scholar] [CrossRef]
- Siribamrungwong, M.; Puangpanngam, K. Treatment of periodontal diseases reduces chronic systemic inflammation in maintenance hemodialysis patients. Ren. Fail. 2012, 34, 171–175. [Google Scholar] [CrossRef]
- Rahmati, M.A.; Craig, R.G.; Homel, P.; Kaysen, G.A.; Levin, N.W. Serum markers of periodontal disease status and inflammation in hemodialysis patients. Am. J. Kidney Dis. 2002, 40, 983–989. [Google Scholar] [CrossRef]
- Mandic, A.; Cavar, I.; Skoro, I.; Tomic, I.; Ljubic, K.; Coric, S.; Mikulic, I.; Azinovic, I.; Pravdic, D. Body composition and inflammation in hemodialysis patients. Apher. Dial. 2017, 21, 556–564. [Google Scholar] [CrossRef]
- Iwasaki, M.; Taylor, G.W.; Awano, S.; Yoshida, A.; Kataoka, S.; Ansai, T.; Nakamura, H. Periodontal disease and pneumonia mortality in haemodialysis patients: A 7-year cohort study. J. Clin. Periodontol. 2018, 45, 38–45. [Google Scholar] [CrossRef]
- Choi, S.R.; Lee, Y.K.; Cho, A.J.; Park, H.C.; Han, C.H.; Choi, M.J.; Koo, J.R.; Yoon, J.W.; Noh, J.W. Malnutrition, inflammation, progression of vascular calcification and survival: Inter-relationships in hemodialysis patients. PLoS ONE 2019, 14, e0216415. [Google Scholar] [CrossRef]
- Kanda, E.; Kato, A.; Masakane, I.; Kanno, Y. A new nutritional risk index for predicting mortality in hemodialysis patients: Nationwide cohort study. PLoS ONE 2019, 14, e0214524. [Google Scholar] [CrossRef]
- Ruospo, M.; Palmer, S.C.; Wong, G.; Craig, J.C.; Petruzzi, M.; De Benedittis, M.; Ford, P.; Johnson, D.W.; Tonelli, M.; Natale, P.; et al. Periodontitis and early mortality among adults treated with hemodialysis: A multinational propensity-matched cohort study. BMC Nephrol. 2017, 18, 166. [Google Scholar] [CrossRef]
- Matsuura, S.; Shirai, Y.; Kubo, M.; Nayama, C.; Okitsu, M.; Oiwa, Y.; Yasui, S.; Suzuki, Y.; Murata, T.; Ishikawa, E.; et al. Body fat mass is correlated with serum transthyretin levels in maintenance hemodialysis patients. J. Med. Invest. 2017, 64, 222–227. [Google Scholar] [CrossRef] [Green Version]
- Avramovski, P.; Avramovska, M.; Sotiroski, K.; Sikole, A. Acute-phase proteins as promoters of abdominal aortic calcification in chronic dialysis patients. Saudi. J. Kidney Dis. Transpl. 2019, 30, 376–386. [Google Scholar] [CrossRef]
- Kim, M.; Kim, C.S.; Bae, E.H.; Ma, S.K.; Kim, S.W. Risk factors for peptic ulcer disease in patients with end-stage renal disease receiving dialysis. Kidney Res. Clin. Pr. 2019, 38, 81–89. [Google Scholar] [CrossRef] [Green Version]
- Naghsh, N.; Sabet, N.K.; Vahidi, F.; Mogharehabed, A.; Yaghini, J. Relationship between periodontal disease and serum factors in patients undergoing hemodialysis. Open Dent. J. 2017, 11, 701–709. [Google Scholar] [CrossRef]
- Malhotra, R.; Grover, V.; Kapoor, A.; Kapur, R. Alkaline phosphatase as a periodontal disease marker. Indian J. Dent. Res. 2010, 21, 531–536. [Google Scholar] [CrossRef]
- Tanaka, K.; Miyake, Y.; Okubo, H.; Hanioka, T.; Sasaki, S.; Miyatake, N.; Arakawa, M. Calcium intake is associated with decreased prevalence of periodontal disease in young Japanese women. Nutr. J. 2014, 13, 109. [Google Scholar] [CrossRef]
- Frankenthal, S.; Nakhoul, F.; Machtei, E.E.; Green, J.; Ardekian, L.; Laufer, D.; Peled, M. The effect of secondary hyperparathyroidism and hemodialysis therapy on alveolar bone and periodontium. J. Clin. Periodontol. 2002, 29, 479–483. [Google Scholar] [CrossRef]
- Sousa, L.H.; Linhares, E.V.; Alexandre, J.T.; Lisboa, M.R.; Furlaneto, F.; Freitas, R.; Ribeiro, I.; Val, D.; Marques, M.; Chaves, H.V.; et al. Effects of atorvastatin on periodontitis of rats subjected to glucocorticoid-induced osteoporosis. J. Periodontol. 2016, 87, 1206–1216. [Google Scholar] [CrossRef]
- Dağ, A.; Firat, E.T.; Kadiroğlu, A.K.; Kale, E.; Yilmaz, M.E. Significance of elevated gingival crevicular fluid tumor necrosis factor-alpha and interleukin-8 levels in chronic hemodialysis patients with periodontal disease. J. Periodontal. Res. 2010, 45, 445–450. [Google Scholar]
- Rocha, L.A.; Barreto, D.V.; Barreto, F.C.; Dias, C.B.; Moysés, R.; Silva, M.R.; Moura, L.A.; Draibe, S.A.; Jorgetti, V.; Carvalho, A.B.; et al. Serum ferritin level remains a reliable marker of bone marrow iron stores evaluated by histomorphometry in hemodialysis patients. Clin. J. Am. Soc. Nephrol. 2009, 4, 105–109. [Google Scholar] [CrossRef]
- Kell, D.B.; Pretorius, E. Serum ferritin is an important inflammatory disease marker, as it is mainly a leakage product from damaged cells. Metallomics 2014, 6, 748–773. [Google Scholar] [CrossRef] [Green Version]
- Kalantar-Zadeh, K.; Rodriguez, R.A.; Humphreys, M.H. Association between serum ferritin and measures of inflammation, nutrition and iron in haemodialysis patients. Nephrol. Dial. Transpl. 2004, 19, 141–149. [Google Scholar] [CrossRef]
- Ganu, V.J.; Boima, V.; Adjei, D.N.; Yendork, J.S.; Dey, I.D.; Yorke, E.; Mate-Kole, C.C.; Mate-Kole, M.O. Depression and quality of life in patients on long term hemodialysis at a nationalhospital in Ghana: A cross-sectional study. Ghana Med. J. 2018, 52, 22–28. [Google Scholar] [CrossRef]
- Kondo, T.; Sasa, N.; Yamada, H.; Takagi, T.; Iizuka, J.; Kobayashi, H.; Yoshida, K.; Fukuda, H.; Ishihara, H.; Tanabe, K.; et al. Acquired cystic disease-associated renal cell carcinoma is the most common subtype in long-term dialyzed patients: Central pathology results according to the 2016 WHO classification in a multi-institutional study. Pathol. Int. 2018, 68, 543–549. [Google Scholar] [CrossRef] [Green Version]
- El-Gamasy, M.A. Study of some pulmonary function tests in Egyptian children with end-stage renal disease under regular hemodialysis in correlation with dialysis duration. Saudi. J. Kidney Dis. Transpl. 2019, 30, 119–128. [Google Scholar] [CrossRef]
- Matsumoto, Y.; Mori, Y.; Kageyama, S.; Arihara, K.; Sato, H.; Nagata, K.; Shimada, Y.; Nojima, Y.; Iguchi, K.; Sugiyama, T. Changes in QTc interval in long-term hemodialysis patients. PLoS ONE 2019, 14, e0209297. [Google Scholar] [CrossRef]
- Parkar, S.M.; Ajithkrishnan, C.G. Periodontal status in patients undergoing hemodialysis. Indian J. Nephrol. 2012, 22, 246–250. [Google Scholar] [CrossRef]
- Sekiguchi, R.T.; Pannuti, C.M.; Silva, H.T., Jr.; Medina-Pestana, J.O.; Romito, G.A. Decrease in oral health may be associated with length of time since beginning dialysis. Spec. Care Dent. 2012, 32, 6–10. [Google Scholar] [CrossRef]
- Castillo, A.; Mesa, F.; Liébana, J.; García-Martinez, O.; Ruiz, S.; García-Valdecasas, J.; O’Valle, F. Periodontal and oral microbiological status of an adult population undergoing haemodialysis: A cross-sectional study. Oral Dis. 2007, 13, 198–205. [Google Scholar] [CrossRef]
- Tonetti, M.S.; Freiburghaus, K.; Lang, N.P.; Bickel, M. Detection of interleukin-8 and matrix metalloproteinases transcripts in healthy and diseased gingival biopsies by RNA/PCR. J. Periodontal. Res. 1993, 28, 511–513. [Google Scholar] [CrossRef]
- Afacan, B.; Öztürk, V.Ö.; Paşalı, Ç.; Bozkurt, E.; Köse, T.; Emingil, G. Gingival crevicular fluid and salivary HIF-1α, VEGF, and TNF-α levels in periodontal health and disease. J. Periodontol. 2018, in press. [Google Scholar] [CrossRef]
- Sedý, J.; Horká, E.; Foltán, R.; Spacková, J.; Dusková, J. Mechanism of increased mortality in hemodialysed patients with periodontitis. Med. Hypotheses 2010, 74, 374–376. [Google Scholar] [CrossRef]
- Craig, R.G. Interactions between chronic renal disease and periodontal disease. Oral Dis. 2008, 14, 1–7. [Google Scholar] [CrossRef]
- Bayraktar, G.; Kurtulus, I.; Kazancioglu, R.; Bayramgurler, I.; Cintan, S.; Bural, C.; Bozfakioglu, S.; Issever, H.; Yildiz, A. Oral health and inflammation in patients with end-stage renal failure. Perit. Dial. Int. 2009, 29, 472–479. [Google Scholar]
- Malekmakan, L.; Haghpanah, S.; Pakfetrat, M.; Ebrahimic, Z.; Hasanlic, E. Oral health status in Iranian hemodialysis patients. Indian J. Nephrol. 2011, 21, 235–238. [Google Scholar]
- Palmer, S.C.; Ruospo, M.; Wong, G.; Craig, J.C.; Petruzzi, M.; De Benedittis, M.; Ford, P.; Johnson, D.W.; Tonelli, M.; Natale, P.; et al. ORAL-D Study Investigators. Dental health and mortality in people with end-stage kidney disease treated with hemodialysis: A multinational cohort study. Am. J. Kidney Dis. 2015, 66, 666–676. [Google Scholar] [CrossRef]
- Lagdive, S.S.; Marawar, P.P.; Byakod, G.; Lagdive, S.B. Evaluation and comparison of interleukin-8 (IL-8) level in gingival crevicular fluid in health and severity of periodontal disease: A clinico-biochemical study. Indian J. Dent. Res. 2013, 24, 188–192. [Google Scholar] [CrossRef]
- Branco-de-Almeida, L.S.; Cruz-Almeida, Y.; Gonzalez-Marrero, Y.; Huang, H.; Aukhil, I.; Harrison, P.; Wallet, S.M.; Shaddox, L.M. Local and plasma biomarker profiles in localized aggressive periodontitis. JDR Clin. Trans. Res. 2017, 2, 258–268. [Google Scholar] [CrossRef]
- Chatzopoulos, G.S.; Mansky, K.C.; Lunos, S.; Costalonga, M.; Wolff, L.F. Sclerostin and WNT-5a gingival protein levels in chronic periodontitis and health. J. Periodontal. Res. 2019, in press. [Google Scholar] [CrossRef]
- Zekeridou, A.; Mombelli, A.; Cancela, J.; Courvoisier, D.; Giannopoulou, C. Systemic inflammatory burden and local inflammation in periodontitis: What is the link between inflammatory biomarkers in serum and gingival crevicular fluid? Clin. Exp. Dent. Res. 2019, 5, 128–135. [Google Scholar] [CrossRef]
- Palmer, S.C.; Ruospo, M.; Wong, G.; Craig, J.C.; Petruzzi, M.; De Benedittis, M.; Ford, P.; Johnson, D.W.; Tonelli, M.; Natale, P.; et al. Patterns of oral disease in adults with chronic kidney disease treated with hemodialysis. Nephrol. Dial. Transpl. 2016, 31, 1647–1653. [Google Scholar] [CrossRef]
- Chen, L.P.; Hsu, S.P.; Peng, Y.S.; Chiang, C.K.; Hung, K.Y. Periodontal disease is associated with metabolic syndrome in hemodialysis patients. Nephrol. Dial. Transpl. 2011, 26, 4068–4073. [Google Scholar] [CrossRef] [Green Version]
- Tavakoli, M.; Izadi, M.; Yaghini, J.; Rastegari, A.; Abed, A.M. A survey on the effects of metabolic syndrome on the periodontal indices of hemodialysis patients. Dent. Res. J. (Isfahan) 2016, 13, 333–337. [Google Scholar]
- Huang, S.T.; Lin, C.L.; Yu, T.M.; Wu, M.J.; Kao, C.H. Intensive periodontal treatment reduces risk of infection-related hospitalization in hemodialysis population: A nationwide population-based cohort study. Medicina (Baltim.) 2015, 94, e1436. [Google Scholar] [CrossRef]
- Casanova, L.; Hughes, F.J.; Preshaw, P.M. Diabetes and periodontal disease: A two-way relationship. Br. Dent. J. 2014, 217, 433–437. [Google Scholar] [CrossRef]
- Gayathri, S.; Elizabeth, K.; Sadasivan, A.; Arunima, P.R.; Jaya Kumar, K. Effect of initial periodontal therapy on serum nitric oxide levels in chronic periodontitis patients with or without type 2 diabetes mellitus. J. Contemp. Dent. Pract. 2019, 20, 197–203. [Google Scholar] [CrossRef]
- Teratani, G.; Awano, S.; Soh, I.; Yoshida, A.; Kinoshita, N.; Hamasaki, T.; Takata, Y.; Sonoki, K.; Nakamura, H.; Ansai, T. Oral health in patients on haemodialysis for diabetic nephropathy and chronic glomerulonephritis. Clin. Oral Investig. 2013, 17, 483–489. [Google Scholar] [CrossRef]
- Chambrone, L.; Chambrone, D.; Lima, L.A.; Chambrone, L.A. Predictors of tooth loss during long-term periodontal maintenance: A systematic review of observational studies. J. Clin. Periodontol. 2010, 37, 675–684. [Google Scholar] [CrossRef]
- Psaltopoulou, T.; Ilias, I.; Alevizaki, M. The role of diet and lifestyle in primary, secondary, and tertiary diabetes prevention: A review of meta-analyses. Rev. Diabet. Stud. 2010, 7, 26–35. [Google Scholar] [CrossRef]
- Schmalz, G.; Schiffers, N.; Schwabe, S.; Vasko, R.; Müller, G.A.; Haak, R.; Mausberg, R.F.; Ziebolz, D. Dental and periodontal health, and microbiological and salivary conditions in patients with or without diabetes undergoing haemodialysis. Int. Dent. J. 2017, 67, 186–193. [Google Scholar] [CrossRef]
- Chuang, S.F.; Sung, J.M.; Kuo, S.C.; Huang, J.J.; Lee, S.Y. Oral and dental manifestations in diabetic and nondiabetic uremic patients receiving hemodialysis. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 2005, 99, 689–695. [Google Scholar] [CrossRef]
- Murali, P.; Narasimhan, M.; Periasamy, S.; Harikrishnan, T.C. A comparison of oral and dental manifestations in diabetic and non-diabetic uremic patients receiving hemodialysis. J. Oral Maxillofac. Pathol. 2012, 16, 374–379. [Google Scholar] [CrossRef]
- Swapna, L.A.; Reddy, R.S.; Ramesh, T.; Reddy, R.L.; Vijayalaxmi, N.; Karmakar, P.; Pradeep, K. Oral health status in haemodialysis patients. J. Clin. Diagn. Res. 2013, 7, 2047–2050. [Google Scholar] [CrossRef]
- Pilot, T.; Miyazaki, H. Global results: 15 years of CPITN epidemiology. Int. Dent. J. 1994, 44, 553–560. [Google Scholar]
- Sung, J.M.; Kuo, S.C.; Guo, H.R.; Chuang, S.F.; Lee, S.Y.; Huang, J.J. The role of oral dryness in interdialytic weight gain by diabetic and non-diabetic haemodialysis patients. Nephrol. Dial. Transpl. 2006, 21, 2521–2528. [Google Scholar] [CrossRef]
- Bayraktar, G.; Kurtulus, I.; Kazancioglu, R.; Bayramgurler, I.; Cintan, S.; Bural, C.; Bozfakioglu, S.; Besler, M.; Trablus, S.; Issever, H.; et al. Evaluation of periodontal parameters in patients undergoing peritoneal dialysis or hemodialysis. Oral Dis. 2008, 14, 185–189. [Google Scholar] [CrossRef]
- Vissink, A.; Panders, A.K.; Gravenmade, E.J.; Vermey, A. The causes and consequences of hyposalivation. Ear Nose Throat J. 1988, 67, 166–168, 173–176. [Google Scholar]
- Sakallioğlu, E.E.; Lütfioğlu, M.; Ozkaya, O.; Aliyev, E.; Açikgöz, G.; Firatli, E. Fluid dynamics of gingiva and gingival health in children with end stage renal failure. Arch. Oral Biol. 2007, 52, 1194–1199. [Google Scholar] [CrossRef]
- Yoshioka, M.; Shirayama, Y.; Imoto, I.; Hinode, D.; Yanagisawa, S.; Takeuchi, Y. Current status of collaborative relationships between dialysis facilities and dental facilities in Japan: Results of a nationwide survey. BMC Nephrol. 2015, 16, 17. [Google Scholar] [CrossRef]
- Yoshioka, M.; Shirayama, Y.; Imoto, I.; Hinode, D.; Yanagisawa, S.; Takeuchi, Y.; Bando, T.; Yokota, N. Factors associated with regular dental visits among hemodialysis patients. World J. Nephrol. 2016, 5, 455–460. [Google Scholar] [CrossRef] [Green Version]
- Ohyama, K.; Yoshimi, H.; Aibara, N.; Nakamura, Y.; Miyata, Y.; Sakai, H.; Fujita, F.; Imaizumi, Y.; Chauhan, A.K.; Kishikawa, N.; et al. Immune complexome analysis reveals the specific and frequent presence of immune complex antigens in lung cancer patients: A pilot study. Int. J. Cancer. 2017, 140, 370–380. [Google Scholar] [CrossRef]
- Aibara, N.; Kamohara, C.; Chauhan, A.K.; Kishikawa, N.; Miyata, Y.; Nakashima, M.; Kuroda, N.; Ohyama, K. Selective, sensitive and comprehensive detection of immune complex antigens by immune complexome analysis with papain-digestion and elution. J. Immunol. Methods 2018, 461, 85–90. [Google Scholar] [CrossRef]
Plaque Index | |
0 | No plaque in the gingival area |
1 | A film of plaque adhering to the free gingival margin and adjacent area of the tooth; may be recognized only by running a probe across the tooth surface |
2 | Moderate accumulation of soft deposits within the gingival pocket and on the gingival margin and/or adjacent tooth surface; can be seen by the naked eye |
3 | Abundance of soft material within the gingival pocket and/or on the gingival margin and adjacent tooth surface |
Papillary Bleeding Index | |
0 | No bleeding on probing |
1 | Single ecchymosis of the gingiva on probing |
2 | Multiple ecchymoses or minor single spot extravasation from the gingiva on probing |
3 | Bleeding into the pocket immediately after probe insertion |
4 | Intensive extra pocket bleeding on probing |
Gingival Index | |
0 | Normal gingiva |
1 | Mild inflammation, slight change in color, slight edema, no bleeding on palpation |
2 | Moderate inflammation, redness, edema, glazing, bleeding on palpation |
3 | Severe inflammation, marked redness and edema, ulceration, tendency to spontaneous bleeding |
Community Periodontal Index | |
0 | Healthy gingiva |
1 | Bleeding observed, directly or by using mouth mirror, after probing |
2 | Calculus detected during probing, but all the black band on the probe visible |
3 | Pocket 4–5 mm (gingival margin within the black band on the probe) |
4 | Pocket 6 mm or more (black band on the probe not visible) |
X | Excluded sextant (less than two teeth present) |
n | Correlation with Periodontal Disease and Its Severity | Author/Year/Ref |
---|---|---|
253 * | Positively correlated with periodontitis severity | Chen/2006/[35] |
44 | Higher in advanced periodontitis versus non-cases | Franek/2006/[32] |
154 | Not different between non-cases and periodontitis | Kshirsagar/2007/[33] |
253 * | Positively correlated with periodontitis severity | Chen/2011/[11] |
77 | Not correlated with periodontitis severity | Yazdi/2013/[12] |
136 * | Higher in periodontal disease versus non-cases | Hou/2017/[36] |
128 | Not different between healthy/gingivitis and periodontitis | Cholewa/2018/[10] |
211 | Higher in periodontal disease versus non-cases | Iwasaki/2018/[41] |
n | Correlation with Periodontal Disease and Its Severity | Author/Year/Ref |
---|---|---|
253 | Negatively correlated with periodontitis severity | Chen/2006/[35] |
154 | No difference between non-patients and periodontitis patients | Kshirsagar/2007/[33] |
154 | Lower in severe periodontitis versus no periodontitis | Kshirsagar/2007/[33] |
253 | Negatively correlated with periodontitis severity | Chen/2011/[11] |
96 | Lower in periodontal disease versus no periodontal disease | Rodrigues/2014/[13] |
188 | Not correlated with periodontitis severity | Iwasaki/2016/[14] |
1355 | Positively correlated with periodontitis severity | Ruospo/2017/[44] |
57 | Lower in periodontitis versus gingivitis cases | Naghsh/2017/[48] |
128 | No difference between healthy/gingivitis and periodontitis | Cholewa/2018/[10] |
n | Correlation with Periodontal Disease or Its Severity | Author/Year/Ref | |
---|---|---|---|
ALP | 96 | Not different between no disease and periodontal disease | Rodrigues/2014/[13] |
128 | Not different between no disease and periodontal disease | Cholewa/2018/[10] | |
Ca | 96 | Not different between no disease and periodontal disease | Rodrigues/2014/[13] |
136 | Not different between no disease and periodontal disease | Hou/2017/[36] | |
57 | Not different between gingivitis and periodontitis | Naghsh/2017/[48] | |
128 | Not different between healthy/gingivitis and periodontitis | Cholewa/2018/[10] | |
PTH | 35 | Not correlated with periodontal indices | Frankenthal/2002/[51] |
253 | Not correlated with periodontitis severity | Chen/2006/[35] | |
136 | Not different between no disease and periodontal disease | Hou/2017/[36] | |
128 | Not different between healthy/gingivitis and periodontitis | Cholewa/2018/[10] | |
P | 96 | Lower in periodontal disease versus no disease | Rodrigues/2014/[13] |
136 | Not different between no disease and periodontal disease | Hou/2017/[36] | |
57 | Not different between gingivitis and periodontitis | Naghsh/2017/[48] | |
128 | Not different between healthy/gingivitis and periodontitis | Cholewa/2018/[10] |
Author/Year/Ref | Decay | Missing | Filled | Overall |
---|---|---|---|---|
Chuang/2005/[85] | Not significant | ↑ (p = 0.039) | Not significant | ↑ (p = 0.001) |
Murali/2012/[86] | – | – | – | Not significant |
Swapna/2013/[87] | ↑ (p < 0.001) | Not significant | ↑ (p < 0.001) | ↑ (p < 0.001) |
Schmalz/2017/[84] | Not significant | Not significant | Not significant | Not significant |
Properties of Saliva | No. of DM/non-DM | Compared tonon-Diabetic Patients | Author/Year/Ref |
---|---|---|---|
Salivary flow rate | 116/68 | Lower | Sung/2006/[89] |
29/69 | Not significant | Teratani/2013/[81] | |
66/93 | Not significant | Schmalz/2017/[84] | |
Salivary pH level | 85/43 | Not significant | Chung/2005/[85] |
47/50 | Not significant | Swapna/2013/[87] | |
66/93 | Lower | Schmalz/2017/[84] |
Variables | PD Compared in the Healthy Group | PD Compared to HD | ||
---|---|---|---|---|
Difference | Author/Years/Ref | Differences | Author/Years/Ref | |
GI | NS | Bayrakter/2008, 2009/[68,90] | Lower | Borawski/2007, 2008/[4,90] |
PBI | NS | Bayrakter/2008, 2009/[68,90] | Lower | Borawski/2007/[4] Bayrakter/2008/[90] |
PI | Higher | Borawski/2007/[4] Bayrakter/2008/[90] | NS | Bayrakter/2008, 2009 /[68,90] |
CSI | Higher | Bayrakter/2008/[90] | NS | Bayrakter/2008/[90] |
S-pH | Higher | Bayrakter/2009/[68] | Higher | Bayrakter/2009/[68] |
SFR | NS | Bayrakter/2009/[68] | Higher | Bayrakter/2009/[68] |
PPD | NS | Bayrakter/2008/[90] | NS | Bayrakter/2008/[90] |
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Miyata, Y.; Obata, Y.; Mochizuki, Y.; Kitamura, M.; Mitsunari, K.; Matsuo, T.; Ohba, K.; Mukae, H.; Nishino, T.; Yoshimura, A.; et al. Periodontal Disease in Patients Receiving Dialysis. Int. J. Mol. Sci. 2019, 20, 3805. https://doi.org/10.3390/ijms20153805
Miyata Y, Obata Y, Mochizuki Y, Kitamura M, Mitsunari K, Matsuo T, Ohba K, Mukae H, Nishino T, Yoshimura A, et al. Periodontal Disease in Patients Receiving Dialysis. International Journal of Molecular Sciences. 2019; 20(15):3805. https://doi.org/10.3390/ijms20153805
Chicago/Turabian StyleMiyata, Yasuyoshi, Yoko Obata, Yasushi Mochizuki, Mineaki Kitamura, Kensuke Mitsunari, Tomohiro Matsuo, Kojiro Ohba, Hiroshi Mukae, Tomoya Nishino, Atsutoshi Yoshimura, and et al. 2019. "Periodontal Disease in Patients Receiving Dialysis" International Journal of Molecular Sciences 20, no. 15: 3805. https://doi.org/10.3390/ijms20153805