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Tongue coating frequency and its colonization by yeasts in chronic kidney disease patients

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Abstract

The objective of this study was to investigate tongue coating (TC) frequency and its colonization by yeasts in a group of chronic kidney disease (CKD) patients. Clinical examination of the oral mucosa of 33 CKD patients was performed to investigate oral and tongue lesions. TC was diagnosed according to its clinical characteristics. Stimulated saliva and TC samples were collected to verify the salivary flow, and determine yeast frequency, species and counts. TC was found in 18/33 of the patients (54.55 %) and was the most frequent oral lesion found. Of 18 patients with TC, 13 (72.22 %) presented positive cultures for yeasts on the tongue dorsum, and one (5.55 %) in the saliva only. Yeasts were significantly more frequent in the tongue dorsum when compared to the saliva (p = 0.0106). The most frequent yeast species found was C. albicans (55.55 %), while C. parapsilosis comprised 50 % of non-albicans Candida species. This study demonstrated high amounts of yeasts on the cultures from TC samples of CKD patients, strongly suggesting that TC is a clinical representation of a polymicrobial biofilm, which could serve as a gateway for disseminated infection in immunosuppressed patients undergoing frequent hospitalization.

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References

  1. Jha V, Garcia-garcia G, Iseki K, Li Z, Naicker S, Plattner B, Saran R, Wang AY, Yang CW (2013) Chronic kidney disease: global dimension and perspectives. Lancet 382(9888):260–272. doi:10.1016/S0140-6736(13)60687-X

    Article  PubMed  Google Scholar 

  2. Martínez-Castelao A, Górriz JL, Bover J, Segura-de la Morena J, Cebollada J, Escalada J, Esmatjes E, Fácila L, Gamarra J, Gràcia S, Hernández-Moreno J, Llisterri-Caro JL, Mazón P, Montañés R, Morales-Olivas F, Muñoz-Torres M, de Pablos-Velasco P, de Santiago A, Sánchez-Celaya M, Suárez C, Tranche S (2014) Consensus document for the detection and management of chronic kidney disease. Endocrinol Nutr 61(9):e25–e43. doi:10.1016/j.endonu.2014.06.003

    Article  PubMed  Google Scholar 

  3. de la Rosa-García E, Miramontes-Zapata M, Sánchez-Vargas LO, Mondragón-Padilla A (2013) Oral colonisation and infection by Candida sp. in diabetic and non-diabetic patients with chronic kidney disease on dialysis. Nefrologia 33(6):764–770. doi:10.3265/Nefrologia.pre2013.Aug.11790

    PubMed  Google Scholar 

  4. Sharif MR, Chitsazian Z, Moosavian M, Raygan F, Nikoueinejad H, Sharif AR, Einollahi B (2015) Immune disorders in hemodialysis patients review. Iran J Kidney Dis 9(2):84–96

    PubMed  Google Scholar 

  5. Dirschnabel AJ, Martins Ade S, Dantas SA, Ribas MO, Grégio AM, Alanis LR, Ignacio SA, Trevilatto PC, Casagrande RW, de Lima AA, Machado MÂ (2011) Clinical oral findings in dialysis and kidney-transplant patients. Quintessence Int 42(2):127–133

    PubMed  Google Scholar 

  6. Pieralisi N, Godoy J, Yamada S, Santana R, Svidzinski T (2014) Oral lesions and colonization by yeasts in hemodialysis patients. J Oral Pathol Med 44(8):585–590. doi:10.1111/jop.12277

    Article  PubMed  Google Scholar 

  7. Popovska M, Spasovski G, Orovcanec N, Cekovska S, Simonceva M, Bexeti-Zendeli L, Masin-Spasovska E, Atanasovska-Stojanovska A, Radojkova-Nikolovska V, Mitic K (2013) Oral findings in end-stage renal disease. Prilozi 34(3):85–92

    PubMed  Google Scholar 

  8. Gemaque K, Giacomelli Nascimento G, Cintra Junqueira JL, Cavalcanti de Araújo V, Furuse C (2014) Prevalence of oral lesions in hospitalized patients with infectious diseases in northern Brazil. Sci World J 2014:586075. doi:10.1155/2014/586075

    Article  Google Scholar 

  9. Elahi M, Telkabadi M, Samadi V, Vakili H (2012) Association of oral manifestations with ulcerative colitis. Gastroenterol Hepatol Bed Bench 5(3):155–160

    PubMed  PubMed Central  Google Scholar 

  10. Picciani BL, Michalski-Santos B, Carneiro S, Sampaio AL, Avelleira JC, Azulay DR, Pinto JM, Dias EP (2013) Oral candidiasis in patients with psoriasis: correlation of oral examination and cytopathological evaluation with psoriasis disease severity and treatment. J Am Acad Dermatol 68(6):986–991. doi:10.1016/j.jaad.2012.11.033

    Article  PubMed  Google Scholar 

  11. Koga C, Yoneda M, Nakayama K, Yokoue S, Haraga M, Oie T, Suga A, Okada F, Matsuura H, Tsue F, Suzuki N, Hirofuji T (2014) The detection of Candida species in patients with halitosis. Int J Dent 2014:857647. doi:10.1155/2014/857647

    Article  PubMed  PubMed Central  Google Scholar 

  12. Van Tornout M, Dadamio J, Coucke W, Quirynen M (2013) Tongue coating: related factors. J Clin Periodontol 40(2):180–185. doi:10.1111/jcpe.12031

    Article  PubMed  Google Scholar 

  13. Takeshita T, Tomioka M, Shimazaki Y, Matsuyama M, Koyano K, Matsuda K, Yamashita Y (2010) Microfloral characterization of the tongue coating and associated risk for pneumonia-related health problems in institutionalized older adults. J Am Geriatr Soc 58(6):1050–1057. doi:10.1111/j.1532-5415.2010.02867.x

    Article  PubMed  Google Scholar 

  14. Patil S, Kaswan S, Rahman F, Doni B (2013) Prevalence of tongue lesions in the Indian population. J Clin Exp Dent 5(3):128–132. doi:10.4317/jced.51102

    Article  Google Scholar 

  15. de la Rosa-García E, Mondragón-Padilla A, Irigoyen-Camacho ME, Bustamante-Ramírez MA (2005) Oral lesions in a group of kidney transplant patients. Med Oral Patol Oral Cir Bucal 10(3):196–204

    PubMed  Google Scholar 

  16. Díaz-Ortiz ML, Micó-Llorens JM, Gargallo-Albiol J, Baliellas-Comellas C, Berini-Aytés L, Gay-Escoda C (2005) Dental health in liver transplant patients. Med Oral Patol Oral Cir Bucal 10(1):72–76, 66–72

    PubMed  Google Scholar 

  17. Hayashi Y, Saito T, Ohshima T, Nakagawa Y, Arita T, Yashima A, Makino T, Konnai R, Gomi K, Arai T, Maeda N (2014) Terminal RFLP analysis to determine the oral microbiota with hyposalivation. Arch Microbiol 196(7):489–496. doi:10.1007/s00203-014-0987-x

    Article  CAS  PubMed  Google Scholar 

  18. Williams DW, Kuriyama T, Silva S, Malic S (2000) Lewis MA (2011) Candida biofilms and oral candidosis: treatment and prevention. Periodontol 55(79):250–265. doi:10.1111/j.1600-0757.2009.00338.x

    Google Scholar 

  19. Watanabe H (2006) Observation of the ultrastructure of the tongue coating. Kokubyo Gakkai Zasshi 73(1):26–39

    Article  PubMed  Google Scholar 

  20. Wei C, Cheng Z, Zhang L, Yang J (2013) Microbiology and prognostic factors of hospital-and community-acquired aspiration pneumonia in respiratory intensive care unit. Am J Infect Control 41(10):880–884. doi:10.1016/j.ajic.2013.01.007

    Article  PubMed  Google Scholar 

  21. Kong EF, Kucharíková S, Van Dijck P, Peters BM, Shirtliff ME, Jabra-Rizk MA (2015) Clinical implications of oral candidiasis: host tissue damage and disseminated bacterial disease. Infect Immun 83(2):604–613. doi:10.1128/IAI.02843-14

    Article  PubMed  Google Scholar 

  22. Badiee P, Alborzi A (2011) Invasive fungal infections in renal transplant recipients. Exp Clin Transplant 9(6):355–362

    PubMed  Google Scholar 

  23. Navazesh M, Kumar SK (2008) University of Southern California School of Dentistry. Measuring salivary flow: challenges and opportunities. J Am Dent Assoc 139 Suppl:35S–40S

    Article  PubMed  Google Scholar 

  24. Qvarnström M, Janket SJ, Nuutinen P, Furuholm J, Meurman JH (2007) Salivary constituents and acidogenic microbial counts in coronary artery bypass graft patients from baseline to three-years after operation. Clin Oral Investig 11(3):217–223

    Article  PubMed  Google Scholar 

  25. Navazesh M, Christensen CM (1982) A comparison of whole mouth resting and stimulated salivary measurement procedures. J Dent Res 61(10):1158–1162

    Article  CAS  PubMed  Google Scholar 

  26. Kramer IR, Pindborg JJ, Bezroukov V, Infirri JS (1980) Guide to epidemiology and diagnosis of oral mucosal diseases and conditions. World Health Organization. Community Dent Oral Epidemiol 8(1):1–26

    Article  CAS  PubMed  Google Scholar 

  27. Ainamo J, Bay I (1975) Problems and proposals for recording gingivitis and plaque. Int Dent J 25(4):229–235

    CAS  PubMed  Google Scholar 

  28. Dongari-Bagtzoglou A, Dwivedi P, Ioannidou E, Shaqman M, Hull D, Burleson J (2009) Oral Candida infection and colonization in solid organ transplant recipients. Oral Microbiol Immunol 24(3):249–254. doi:10.1111/j.1399-302X.2009.00505.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Schelenz S, Abdallah S, Gray G, Stubbings H, Gow I, Baker P, Hunter PR (2011) Epidemiology of oral yeast colonization and infection in patients with hematological malignancies, head neck and solid tumors. J Oral Pathol Med 40(1):83–89. doi:10.1111/j.1600-0714.2010.00937.x

    Article  PubMed  Google Scholar 

  30. Godoy JS, de Souza Bonfim-Mendonça P, Nakamura SS, Yamada SS, Shinobu-Mesquita C, Pieralisi N, Fiorini A, Svidzinski TI (2013) Colonization of the oral cavity by yeasts in patients with chronic renal failure undergoing hemodialysis. J Oral Pathol Med 42(3):229–234. doi:10.1111/jop.12003

    Article  CAS  PubMed  Google Scholar 

  31. Larone DH (2014) Medically important fungi: a guide to identification. Lab Med 45(2):68–69

    Article  Google Scholar 

  32. Stevens PE, Levin A (2013) Evaluation and management of chronic kidney disease: synopsis of the kidney disease: improving global outcomes 2012 clinical practice guideline. Ann Intern Med 158(11):825–830. doi:10.7326/0003-4819-158-11-201306040-00007

    Article  PubMed  Google Scholar 

  33. Tinoco-Araujo JE, Araújo DF, Barbosa PG, Santos PS, Medeiros AM (2013) Invasive candidiasis and oral manifestations in premature newborns. Einstein 11(1):71–75

    Article  PubMed  PubMed Central  Google Scholar 

  34. Arendorf TM, Walker DM (1979) Oral candidal populations in health and disease. Br Dent J 147(10):267–272

    Article  CAS  PubMed  Google Scholar 

  35. Ryu M, Ueda T, Saito T, Yasui M, Ishihara K, Sakurai K (2010) Oral environmental factors affecting number of microbes in saliva of complete denture wearers. J Oral Rehabil 37(3):194–201. doi:10.1111/j.1365-2842.2009.02042.x

    Article  CAS  PubMed  Google Scholar 

  36. Kamaraj DR, Bhushan KS, Laxman VK, Mathew J (2011) Detection of odoriferous subgingival and tongue microbiota in diabetic and nondiabetic patients with oral malodor using polymerase chain reaction. Indian J Dent Res 22(2):260–265. doi:10.4103/0970-9290.84301

    Article  PubMed  Google Scholar 

  37. Gulsahi A, Evirgen S, Öztaş B, Genç Y, Çetinel Y (2014) Volatile sulphur compound levels and related factors in patients with chronic renal failure. J Clin Periodontol 41(8):814–819. doi:10.1111/jcpe.12280

    Article  CAS  PubMed  Google Scholar 

  38. 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(3):122–126

    Article  PubMed  Google Scholar 

  39. Oyetola EO, Owotade FJ, Agbelusi GA, Fatusi OA, Sanusi AA (2015) Oral findings in chronic kidney disease: implications for management in developing countries. BMC Oral Health 15(24):1–8. doi:10.1186/s12903-015-0004-z

    Google Scholar 

  40. Marsh PD, Head DA, Devine DA (2014) Prospects of oral disease control in the future—an opinion. J Oral Microbiol 6:26176. doi:10.3402/jom.v6.26176

    Article  PubMed  Google Scholar 

  41. Miranda TT, Vianna CR, Rodrigues L, Monteiro AS, Rosa CA, Corrêa A Jr (2009) Diversity and frequency of yeasts from the dorsum of the tongue and necrotic root canals associated with primary apical periodontitis. Int Endod J 42(9):839–844

    Article  CAS  PubMed  Google Scholar 

  42. da Silva-Rocha WP, Lemos VL, Svidizisnki TI, Milan EP, Chaves GM (2014) Candida species distribution, genotyping and virulence factors of Candida albicans isolated from the oral cavity of kidney transplant recipients of two geographic regions of Brazil. BMC Oral Health 14:20

    Article  PubMed  PubMed Central  Google Scholar 

  43. Caggiano G, Coretti C, Bartolomeo N, Lovero G, De Giglio O, Montagna MT (2015) Candida bloodstream infections in Italy: changing epidemiology during 16 years of surveillance. Biomed Res Int 2015:256580

    Article  PubMed  PubMed Central  Google Scholar 

  44. Kim EK, Jang SH, Choi YH, Lee KS, Kim YJ, Kim SH, Lee HK (2014) Effect of an oral hygienic care program for stroke patients in the intensive care unit. Yonsei Med J 55(1):240–246

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank professor Fabio Luiz Grassi for the schematic illustration of tongue coating design (Fig. 3) and Mr. Antonio Carlos Correa for his contribution with the English version of this paper.

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Authors and Affiliations

  1. Department of Dentistry, State University of Maringá, Maringá, Paraná, Brazil

    N. Pieralisi

  2. Medical Mycology, Department of Clinical Analysis, State University of Maringá, Maringá, Paraná, Brazil

    P. de Souza Bonfim-Mendonça, M. Negri, I. C. Jarros & T. Svidzinski

  3. Medical Mycology, Teaching and Research Laboratory, Department of Clinical Analysis, State University of Maringá, Av. Colombo, 5790, 87020-900, Maringá, Paraná, Brazil

    T. Svidzinski

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  1. N. Pieralisi
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Corresponding author

Correspondence to T. Svidzinski.

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Funding

This study was conducted with the financial support of Programa Nacional de Cooperação Academica (CAPES/PROCAD), Conselho Nacional de Desenvolvimento Científico e Tecnológico (Cnpq), and Fundação Araucária, Brazil.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in this study were in accordance with the ethical standards of the Resolution 466/2012 of the Brazilian National Health Council and with the 1964 Helsinki Declaration and its later amendments.

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Informed consent was obtained from all individual participants included in the study.

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Pieralisi, N., de Souza Bonfim-Mendonça, P., Negri, M. et al. Tongue coating frequency and its colonization by yeasts in chronic kidney disease patients. Eur J Clin Microbiol Infect Dis 35, 1455–1462 (2016). https://doi.org/10.1007/s10096-016-2684-y

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  • DOI: https://doi.org/10.1007/s10096-016-2684-y

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