Abstract
Objectives
The aim of this study was to investigate the association between serum biomarkers and oral health parameters in children with chronic kidney disease (CKD).
Materials and methods
Serum hemoglobin, blood urea nitrogen, serum creatinine, calcium, parathormone, magnesium, and phosphorus levels were measured in 62 children with CKD aged between 4 and 17 years. Intraoral examinations of the patients were performed by two different pediatric dentists. Dental caries was assessed using the decayed-missing-filled-teeth (DMFT/dmft) indexes, and oral hygiene was assessed using the debris (DI), calculus (CI), and simplified oral hygiene (OHI-S) indexes. Spearman’s rho coefficient and generalized linear modeling were used to examine the association between serum biomarkers and oral health parameters.
Results
The results of the study showed that there were negative and statistically significant correlations between serum hemoglobin and creatinine levels and dmft scores in pediatric patients with CKD (p = 0.021 and p = 0.019, respectively). Furthermore, blood urea nitrogen levels and DI and OHI-S scores (p = 0.047 and p = 0.050, respectively); serum creatinine levels and DI, CI, and OHI-S scores (p = 0.005, p = 0.047, p = 0.043, respectively); and parathormone levels and CI and OHI-S scores (p = 0.001 and p = 0.017, respectively) were found to be positively and statistically significantly related.
Conclusions
There are associations between various serum biomarker levels and dental caries and oral hygiene parameters in pediatric patients with CKD.
Clinical relevance
The impact of changes in serum biomarkers on oral and dental health is important for dentists’ and medical professionals' approaches to patients' oral and systemic health.
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Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Levey AS, de Jong PE, Coresh J, El Nahas M, Astor BC, Matsushita K, Gansevoort RT, Kasiske BL, Eckardt KU (2011) The definition, classification, and prognosis of chronic kidney disease: a KDIGO Controversies Conference report. Kidney Int 80:17–28. https://doi.org/10.1038/ki.2010.483
Harambat J, Van Stralen KJ, Kim JJ, Tizard EJ (2012) Epidemiology of chronic kidney disease in children. Pediatr Nephrol 27:363–373. https://doi.org/10.1007/s00467-011-1939-1
Amanullah F, Malik AA, Zaidi Z (2022) Chronic kidney disease causes and outcomes in children: Perspective from a LMIC setting. PLoS One 17:e0269632. https://doi.org/10.1371/journal.pone.0269632
Velan E, Sheller B (2021) Oral health in children with chronic kidney disease. Pediatr Nephrol 36:3067–3075. https://doi.org/10.1007/s00467-020-04913-9
Nylund KM, Meurman JH, Heikkinen AM, Furuholm JO, Ortiz F, Ruokonen HM (2018) Oral health in patients with renal disease: a longitudinal study from predialysis to kidney transplantation. Clin Oral Investig 22:339–347. https://doi.org/10.1007/s00784-017-2118-y
Ruokonen H, Nylund K, Meurman JH, Heikkinen AM, Furuholm J, Sorsa T, Roine R, Ortiz F (2019) Oral symptoms and oral health-related quality of life in patients with chronic kidney disease from predialysis to posttransplantation. Clin Oral Investig 23:2207–2213. https://doi.org/10.1007/s00784-018-2647-z
Sezer B, Kaya R, Kodaman Dokumacıgil N, Sıddıkoğlu D, Güven S, Yıldız N, Alpay H, Kargül B (2023) Assessment of the oral health status of children with chronic kidney disease. Pediatr Nephrol 38:269–277. https://doi.org/10.1007/s00467-022-05590-6
Lin YL, Chen SY, Lai YH, Wang CH, Kuo CH, Liou HH, Hsu BG (2020) Serum creatinine to cystatin C ratio predicts skeletal muscle mass and strength in patients with non-dialysis chronic kidney disease. Clin Nutr 39:2435–2441. https://doi.org/10.1016/j.clnu.2019.10.027
Seki M, Nakayama M, Sakoh T, Yoshitomi R, Fukui A, Katafuchi E, Tsuda S, Nakano T, Tsuruya K, Kitazono T (2019) Blood urea nitrogen is independently associated with renal outcomes in Japanese patients with stage 3–5 chronic kidney disease: a prospective observational study. BMC Nephrol 20:115. https://doi.org/10.1186/s12882-019-1306-1
Nogalcheva AN, Konstantinova D, Pechalova P (2018) Salivary creatinine and urea in patients with end-stage chronic kidney disease could not be used as diagnostic biomarkers for the effectiveness of dialysis treatment. G Ital Nefrol 35:119–125
Freitas-Fernandes LB, Fidalgo TKS, de Almeida PA, Souza IPR, Valente AP (2021) Salivary metabolome of children and adolescents under peritoneal dialysis. Clin Oral Investig 25:2345–2351. https://doi.org/10.1007/s00784-020-03557-1
Solak B, Acikgoz SB, Sipahi S, Erdem T (2016) Epidemiology and determinants of pruritus in pre-dialysis chronic kidney disease patients. Int Urol Nephrol 48:585–591. https://doi.org/10.1007/s11255-015-1208-5
Andrade MR, Antunes LA, Soares RM, Leão AT, Maia LC, Primo LG (2014) Lower dental caries prevalence associated to chronic kidney disease: a systematic review. Pediatr Nephrol 29:771–778. https://doi.org/10.1007/s00467-013-2437-4
Davidovich E, Davidovits M, Peretz B, Shapira J, Aframian DJ (2009) The correlation between dental calculus and disturbed mineral metabolism in paediatric patients with chronic kidney disease. Nephrol Dial Transplant 24:2439–2445. https://doi.org/10.1093/ndt/gfp101
Andaloro C, Sessa C, Bua N, Mantia I (2018) Chronic kidney disease in children: Assessment of oral health status. Dent Med Probl 55:23–28. https://doi.org/10.17219/dmp/81747
Maciejczyk M, Szulimowska J, Skutnik A, Taranta-Janusz K, Wasilewska A, Wiśniewska N, Zalewska A (2018) Salivary Biomarkers of Oxidative Stress in Children with Chronic Kidney Disease. J Clin Med 7:209. https://doi.org/10.3390/jcm7080209
Celec P, Tóthová Ľ, Šebeková K, Podracká Ľ, Boor P (2016) Salivary markers of kidney function - Potentials and limitations. Clin Chim Acta 453:28–37. https://doi.org/10.1016/j.cca.2015.11.028
Katz AL, Webb SA, COMMITTEE ON BIOETHICS (2016) Informed Consent in Decision-Making in Pediatric Practice. Pediatrics 13:e20161485. https://doi.org/10.1542/peds.2016-1485
Kidney Disease: Improving Global Outcomes (KDIGO) CKD Work Group (2013) KDIGO 2012 clinical practice guideline for the evaluation and management of chronic kidney disease. Kidney Int Suppl 3:1–150
Inker LA, Astor BC, Fox CH, Isakova T, Lash JP, Peralta CA, Kurella Tamura M, Feldman HI (2014) KDOQI US commentary on the 2012 KDIGO clinical practice guideline for the evaluation and management of CKD. Am J Kidney Dis 63:713–735. https://doi.org/10.1053/j.ajkd.2014.01.416
Chondros P, Nikolidakis D, Christodoulides N, Rössler R, Gutknecht N, Sculean A (2009) Photodynamic therapy as adjunct to non-surgical periodontal treatment in patients on periodontal maintenance: a randomized controlled clinical trial. Lasers Med Sci 24:681–688. https://doi.org/10.1007/s10103-008-0565-z
Avorn J, Bohn RL, Levy E, Levin R, Owen WF Jr, Winkelmayer WC, Glynn RJ (2002) Nephrologist care and mortality in patients with chronic renal insufficiency. Arch Intern Med 162:2002–2006. https://doi.org/10.1001/archinte.162.17.2002
World Health Organization (2013) Oral Health Surveys Basic Methods. WHO Press, Geneva
Moradi G, Mohamadi Bolbanabad A, Moinafshar A, Adabi H, Sharafi M, Zareie B (2019) Evaluation of Oral Health Status Based on the Decayed, Missing and Filled Teeth (DMFT) Index. Iran J Public Health 48:2050–2057
Greene JC, Vermillion JR (1964) The simplified oral hygiene index. J Am Dent Assoc 68:7–13. https://doi.org/10.14219/jada.archive.1964.0034
Pham TAV, Le DD (2019) Dental condition and salivary characteristics in Vietnamese patients with chronic kidney disease. Int J Dent Hyg 17:253–260. https://doi.org/10.1111/idh.12380
Rodrigues RPCB, de Andrade VW, Siqueira WL, Blumenberg C, de Macedo BÍ, Cardoso SV, Flores-Mir C, Paranhos LR (2020) Saliva as an alternative to blood in the determination of uremic state in adult patients with chronic kidney disease: a systematic review and meta-analysis. Clin Oral Investig 24:2203–2217. https://doi.org/10.1007/s00784-020-03340-2
Martí-Álamo S, Mancheño-Franch A, Marzal-Gamarra C, Carlos-Fabuel L (2012) Saliva as a diagnostic fluid. Literature review J Clin Exp Dent 4:e237-243. https://doi.org/10.4317/jced.50865
Goll RD, Mookerjee BK (1978) Correlation of biochemical parameters in serum and saliva in chronic azotemic patients and patients on chronic hemodialysis. J Dial 2:399–444. https://doi.org/10.3109/08860227809079326
Vuletic L, Peros K, Spalj S, Rogic D, Alajbeg I (2014) Time-related Changes in pH, Buffering Capacity and Phosphate and Urea Concentration of Stimulated Saliva. Oral Health Prev Dent 12:45–53. https://doi.org/10.3290/j.ohpd.a31221
Bhatsange A, Patil SR (2012) Assessment of periodontal health status in patients undergoing renal dialysis: A descriptive, cross-sectional study. J Indian Soc Periodontol 16:37–42. https://doi.org/10.4103/0972-124X.94602
Franco R, Navarro G, Martínez-Pinilla E (2019) Antioxidant Defense Mechanisms in Erythrocytes and in the Central Nervous System. Antioxidants (Basel) 8:46. https://doi.org/10.3390/antiox8020046
Gluba-Brzózka A, Franczyk B, Olszewski R, Rysz J (2020) The Influence of Inflammation on Anemia in CKD Patients. Int J Mol Sci 21:725. https://doi.org/10.3390/ijms21030725
Atkinson MA, Martz K, Warady BA, Neu AM (2010) Risk for anemia in pediatric chronic kidney disease patients: a report of NAPRTCS. Pediatr Nephrol 25:1699–1706. https://doi.org/10.1007/s00467-010-1538-6
Tang RS, Huang MC, Huang ST (2013) Relationship between dental caries status and anemia in children with severe early childhood caries. Kaohsiung J Med Sci 29:330–336. https://doi.org/10.1016/j.kjms.2012.10.003
Folayan MO, El Tantawi M, Schroth RJ, Vukovic A, Kemoli A, Gaffar B, Obiyan M, Early Childhood Caries Advocacy Group (2020) Associations between early childhood caries, malnutrition and anemia: a global perspective. BMC Nutr 6:16. https://doi.org/10.1186/s40795-020-00340-z
Faheem S, Maqsood S, Hasan A, Imtiaz F, Shaikh F, Farooqui WA (2021) Associations of early childhood caries with salivary beta defensin-3 and childhood anemia: a case-control study. BMC Oral Health 21:445. https://doi.org/10.1186/s12903-021-01810-x
Bahdila D, Markowitz K, Pawar S, Chavan K, Fine DH, Velliyagounder K (2019) The effect of iron deficiency anemia on experimental dental caries in mice. Arch Oral Biol 105:13–19. https://doi.org/10.1016/j.archoralbio.2019.05.002
Kim HJ, Kim TE, Han M, Yi Y, Jeong JC, Chin HJ, Song SH, Lee J, Lee KB, Sung S, Han SH, Seong EY, Ahn C, Oh KH, Chae DW (2021) Effects of blood urea nitrogen independent of the estimated glomerular filtration rate on the development of anemia in non-dialysis chronic kidney disease: The results of the KNOW-CKD study. PLoS One 16:e0257305. https://doi.org/10.1371/journal.pone.0257305
Calice-Silva V, Sacomboio E, Raimann JG, Evans R, Dos Santos SC, Tchivango AT, Kotanko P, Levin N, Pecoits-Filho R (2018) Diagnostic performance of salivary urea nitrogen dipstick to detect and monitor acute kidney disease in patients with malaria. Malar J 17:477. https://doi.org/10.1186/s12936-018-2627-4
Tadakamadla J, Kumar S, Mamatha GP (2014) Comparative evaluation of oral health status of chronic kidney disease (CKD) patients in various stages and healthy controls. Spec Care Dentist 34:122–126. https://doi.org/10.1111/scd.12040
Pakpour AH, Kumar S, Fridlund B, Zimmer S (2015) A case-control study on oral health-related quality of life in kidney disease patients undergoing haemodialysis. Clin Oral Investig 19:1235–1243. https://doi.org/10.1007/s00784-014-1355-6
Andrade MR, Salazar SL, de Sá LF, Portela M, Ferreira-Pereira A, Soares RM, Leão AT, Primo LG (2015) Role of saliva in the caries experience and calculus formation of young patients undergoing hemodialysis. Clin Oral Investig 19:1973–1980. https://doi.org/10.1007/s00784-015-1441-4
Silva TMC, Alves LAC, Garrido D, Watanabe A, Mendes FM, Ciamponi AL (2019) Health and oral health-related quality of life of children and adolescents with chronic kidney disease: a cross-sectional study. Qual Life Res 28:2481–2489. https://doi.org/10.1007/s11136-019-02196-8
Renda R (2017) Can salivary creatinine and urea levels be used to diagnose chronic kidney disease in children as accurately as serum creatinine and urea levels? A case-control study. Ren Fail 39:452–457. https://doi.org/10.1080/0886022X.2017.1308256
Shimazaki Y, Kushiyama M, Murakami M, Yamashita Y (2013) Relationship between normal serum creatinine concentration and periodontal disease in Japanese middle-aged males. J Periodontol 84:94–99. https://doi.org/10.1902/jop.2012.110528
Limeira FIR, Yamauti M, Moreira AN, Galdino TM, de Magalhães CS, Abreu LG (2019) Dental caries and developmental defects of enamel in individuals with chronic kidney disease: Systematic review and meta-analysis. Oral Dis 25:1446–1464. https://doi.org/10.1111/odi.12993
Kritmetapak K, Pongchaiyakul C (2019) Parathyroid Hormone Measurement in Chronic Kidney Disease: From Basics to Clinical Implications. Int J Nephrol 17:5496710. https://doi.org/10.1155/2019/5496710
Frankenthal S, Nakhoul F, Machtei EE, Green J, Ardekian L, Laufer D, Peled M (2002) The effect of secondary hyperparathyroidism and hemodialysis therapy on alveolar bone and periodontium. J Clin Periodontol 29:479–483. https://doi.org/10.1034/j.1600-051x.2002.290601.x
Cholewa M, Madziarska K, Radwan-Oczko M (2018) The association between periodontal conditions, inflammation, nutritional status and calcium-phosphate metabolism disorders in hemodialysis patients. J Appl Oral Sci 26:e20170495. https://doi.org/10.1590/1678-7757-2017-0495
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Conceptualization: [Berkant Sezer], [Harika Alpay], [Betül Kargül]; Methodology: [Berkant Sezer], [Harika Alpay], [Betül Kargül]; Formal analysis and investigation: [Berkant Sezer], [Nur Kodaman Dokumacıgil], [Remziye Kaya], [Serçin Güven], [Özde Nisa Türkkan], [Neslihan Çiçek]; Writing—original draft preparation: [Berkant Sezer]; Writing—review and editing: [Berkant Sezer], [Serçin Güven], [Özde Nisa Türkkan], [Neslihan Çiçek], [Harika Alpay], [Betül Kargül]; Supervision: [Harika Alpay], [Betül Kargül].
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This cross-sectional study was approved by the Clinical Research Ethical Committee of the School of Medicine, Marmara University with a protocol number of 09.2021.290. The study was conducted in accordance with all the ethical principles of the Declaration of Helsinki.
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Sezer, B., Kodaman Dokumacıgil, N., Kaya, R. et al. Association between serum biomarkers and oral health status in children with chronic kidney disease: A cross-sectional study. Clin Oral Invest 27, 3731–3740 (2023). https://doi.org/10.1007/s00784-023-04989-1
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DOI: https://doi.org/10.1007/s00784-023-04989-1