Micronuclei and other nuclear anomalies in buccal epithelial cells of children with chronic kidney disease

1. Clark LE, Khan I. Outcomes in CKD: what we know and what we need to know. Nephron Clin Pract 2010;114:c95-102. doi: 10.1159/000254381Search in Google Scholar

2. Wright J, Hutchison A. Cardiovascular disease in patients with chronic kidney disease. Vasc Health Risk Manag 2009;5:713-22. doi: 10.2147/VHRM.S6206Search in Google Scholar

3. Fabrizi F, Messa P, Basile C, Martin P. Hepatic disorders in chronic kidney disease. Nat Rev Nephrol 2010;6:395-403. doi: 10.1038/nrneph.2010.37Search in Google Scholar

4. Filiopoulos V, Hadjiyannakos D, Takouli L, Metaxaki P, Sideris V, Vlassopoulos D. Inflammation and oxidative stress in end-stage renal disease patients treated with hemodialysis or peritoneal dialysis. Int J Artif Organs 2009;32:872-82. PMID: 2003789210.1177/03913988090320120620037892Search in Google Scholar

5. Kao MP, Ang DS, Pall A, Struthers AD. Oxidative stress in renal dysfunction: mechanisms, clinical sequelae and therapeutic options. J Hum Hypertens 2010;24:1-8. doi: 10.1038/jhh.2009.70Search in Google Scholar

6. Schupp N, Schinzel R, Heidland A, Stopper H. Genotoxicity of advanced glycation end products: involvement of oxidative stress and of angiotensin II type 1 receptors. Ann N Y Acad Sci 2005;1043:685-95. doi: 10.1196/annals.1333.079Search in Google Scholar

7. Stopper H, Treutlein AT, Bahner U, Schupp N, Schmid U, Brink A, Perna A, Heidland A. Reduction of the genomic damage level in haemodialysis patients by folic acid and vitamin B12 supplementation. Nephrol Dial Transplant 2008;23:3272-9. doi: 10.1093/ndt/gfn254Search in Google Scholar

8. Coutinho HM, Groothoff JW, Offringa M, Gruppen MP, Heymans HSA. De novo malignancy after paediatric renal replacement therapy. Arch Dis Child 2001;85:478-83. doi: 10.1136/adc.85.6.478Search in Google Scholar

9. Roth JM, Restani RG, Goncalves TTS, Sphor SL, Ness AB, Martino-Roth MG, Garcias GL. Genotoxicity evaluation in chronic renal patients undergoing hemodialysis and peritoneal dialysis, using the micronucleus test. Genet Mol Res 2008;7:433-43. PMID: 1855141010.4238/vol7-2gmr44118551410Search in Google Scholar

10. Agraharkar ML, Cinclair RD, Kou YF, Daller JA, Shahinian VB. Risk of malignancy with long-term immunosuppression in renal transplant recipients. Kidney Int 2004;66:383-9. doi: 10.1111/j.1523-1755.2004.00741.xSearch in Google Scholar

11. Fenech M. Biomarkers of genetic damage for cancer epidemiology. Toxicology 2002;181:411-6. doi: 10.1016/ S0300-483X(02)00480-8Search in Google Scholar

12. Martins RA, Gomes GA, Aguiar OJr, Ribeiro DA. Biomonitoring of oral epithelial cells in petrol station attendants: comparison between buccal mucosa and lateral border of the tongue. Environ Int 2009;35:1062-5. doi: 10.1016/j.envint.2009.06.001Search in Google Scholar

13. Burgaz S, Coskun E, Demircigil GC, Kocabas NA, Cetindag F, Sunter O, Edinsel H. Micronucleus frequencies in lymphocytes and buccal epithelial cells from patients having head and neck cancer and their first-degree relatives. Mutagenesis 2011;26:351-6. doi: 10.1093/mutage/geq101Search in Google Scholar

14. Holland N, Bolognesi C, Kirsch-Volders M, Bonassi S, Zeiger E, Knasmueller S, Fenech M. The micronucleus assay in human buccal cells as a tool for biomonitoring DNA damage: the HUMN project perspective on current status and knowledge gaps. Mutat Res 2008;659:93-108. doi: 10.1016/j. mrrev.2008.03.007Search in Google Scholar

15. Aykanat B, Demircigil GC, Fidan K, Buyan N, Gulleroglu K, Baskin E, Bayrakci US, Sepici A, Buyukkaragoz B, Karakayali H, Haberal M, Burgaz S. Basal and oxidative DNA damage in children with chronic kidney disease by comet assay. Mutat Res 2011;725:22-8. doi: 10.1016/j. mrgentox.2011.07.005Search in Google Scholar

16. Demircigil CG, Aykanat B, Fidan K, Gulleroglu K, Bayrakci US, Sepici A, Buyukkaragoz B, Karakayali H, Haberal M, Baskin E, Buyan N, Burgaz S. Micronucleus frequencies in peripheral blood lymphocytes of children with chronic kidney disease. Mutagenesis 2011;26:643-50. doi: 10.1093/mutage/ ger027Search in Google Scholar

17. Stich HG, Rosin MP. Micronuclei in exfoliated human cells as tool for studies in cancer risk and cancer intervention. Cancer Lett 1984;22:241-53. doi: 10.1016/0304-3835(84)90159-9Search in Google Scholar

18. Tolbert PE, Shy CM, Allen JW. Micronuclei and other nuclear anomalies in buccal smears: methods development. Mutat Res 1992;271:69-77. doi: 10.1016/0165-1161(92)90033-ISearch in Google Scholar

19. Thomas P, Holland N, Bolognesi C, Kirsch-Volders M, Bonassi S, Zeiger E, Knasmueller S, Fenech M. Buccal micronucleus cytome assay. Nat Protoc 2009;4:825-37. doi: 10.1038/nprot.2009.53Search in Google Scholar

20. Serdengeçti K, Süleymanlar G, Altıparmak MR, Seyahi N. Registry of the nephrology, dialysis and transplantation in Turkey registry. In: Söylemezoğlu O, editor. Pediatric hemodialysis. Istanbul: Turkish Society of Nephrology, Pasifik Reklam ve Tanıtım Hizmetleri / Metris Matbaacılık; 2010. p. 37-53.Search in Google Scholar

21. Schup N, Heidland A, Stopper H. Genomic damage in endstage renal disease contribution of uremic toxins. Toxins 2010;2:2340-58. doi: 10.3390/toxins2102340Search in Google Scholar

22. Groothoff JW. Long-term outcomes of children with endstage renal disease. Pediatr Nephrol 2005;20:849-53. doi: 10.1007/s00467-005-1878-9Search in Google Scholar

23. Maisonneuve P, Agodoa L, Gellert R, Stewart JH, Buccianti G, Lowenfels AB, Wolfe RA, Jones E, Disney AP, Briggs D, McCredie M, Boyle P. Cancer in patients on dialysis for endstage renal disease: an international collaborative study. Lancet 1999;354:93-9. doi: 10.1016/S0140-6736(99)06154-1Search in Google Scholar

24. Rath T, Oliveira-Frick V. Mutagenicity of immunosuppressive medications among renal transplant recipients. Am J Nephrol 2009;30:514-20. doi: 10.1159/000244646Search in Google Scholar

25. Oliveira VD, Zanki H, Rath T. Mutagenic and cytotoxic effects of immunosuppressive drugs on human lymphocyte cultures. Exp Clin Transplant 2004;2:273-9. PMID: 15859941Search in Google Scholar

26. Sandoval SB, Stoyanova E, Coll E, Pastor S, Reyes J, Andrés E, Ballarin J, Xamena N, Marcos R. Genetic damage in chronic renal failure patients is associated with the glomerular filtration rate index. Mutagenesis 2010;25:603-8. doi: 10.1093/mutage/geq047Search in Google Scholar

27. Stoyanova E, Sandoval SB, Zúñiga LA, El-Yamani N, Coll E, Pastor S, Reyes J, Andrés E, Ballarin J, Xamena N, Marcos R. Oxidative DNA damage in chronic renal failure patients. Nephrol Dial Transplant 2010;25:879-85. doi: 10.1093/ndt/ gfp575Search in Google Scholar

28. Buemi M, Floccari F, Costa C, Caccamo C, Belghity N, Campo S, Pernice F, Bonvissuto G, Coppolino G, Barillà A, Criseo M, Crascì E, Nostro L, Arena A. Dialysis-related genotoxicity: sister chromatid exchanges and DNA lesions in T and B lymphocytes of uremic patients. Genomic damage in patients on hemodiafiltration. Blood Purif 2006;24:569-74. doi: 10.1159/000097080Search in Google Scholar

29. Lialiaris T, Mavromatidou P, Digkas E, Passadaki T, Mpountoukas P, Panagoutsos S, Vargemezis V. Chromosome instability in patients with chronic renal failure. Genet Test Mol Biomarkers 2010;14:37-41. doi: 10.1089/ gtmb.2009.0109Search in Google Scholar

30. Kobras K, Schupp N, Nehrlich K, Adelhardt M, Bahner U, Vienken J, Heidland A, Sebekova K, Stopper H. Relation between different treatment modalities and genomic damage of end-stage renal failure patients. Kidney Blood Press Res 2006;29:10-17. doi: 10.1159/000092482Search in Google Scholar

31. Stopper H, Boullay F, Heidland A, Vienken J, Bahner U. Comet-assay analysis identifies genomics damage in lymphocytes of uremic patients. Am J Kidney Dis 2001;38:296-301. doi: 10.1053/ajkd.2001.26094Search in Google Scholar

32. Fenech M, Holland N, Chang WP, Zeiger E, Bonassi S. The human micronucleus project-an international collaborative study on the use of the micronucleus technique for measuring DNA damage in humans. Mutat Res 1999;428:271-83. doi: 10.1016/S1383-5742(99)00053-8Search in Google Scholar

33. Stich HF, Rosin MP. Micronuclei in exfoliated human cells as an internal dosimeter for exposures to carcinogens. In: Stich HF, editor. Carcinogens and mutagens in the environment. Vol. II. Boca Raton (FL): CRC Press; 1983. p. 17-25.Search in Google Scholar

34. Bolognesi C, Bonassi S, Knasmueller S, Fenech M, Bruzzone M, Lando C, Ceppi M. Clinical application of micronucleus test in exfoliated buccal cells: A systematic review and metanalysis. Mutat Res Rev Mutat Res 2015;766:20-31. doi: 10.1016/j.mrrev.2015.07.002Search in Google Scholar

35. Schupp N, Dette EM, Schmid U, Bahner U, Winkler M, Stopper H. Benfotiamine reduces genomic damage in peripheral lymphocytes of hemodialysis patients. Naunyn Schmiedebergs Arch Pharmacol 2008;378:283-91. doi: 10.1007/s00210-008-0310-ySearch in Google Scholar

36. Fenech M, Crott JW. Micronuclei, nucleoplasmic bridges and nuclear buds induced in folic acid deficient human lymphocytes-evidence for breakage-fusion-bridge cycles in the cytokinesis-block micronucleus assay. Mutat Res 2002;504:131-6. doi: 10.1016/S0027-5107(02)00086-6Search in Google Scholar

37. Bonassi S, Coskun E, Ceppi M, Lando C, Bolognesi C, Burgaz S, Holland N, Kirsh-Volders M, Knasmueller S, Zeiger E, Carnesoltas D, Cavallo D, da Silva J, de Andrade VM, Demircigil GC, Domínguez Odio A, Donmez-Altuntas H, Gattas G, Giri A, Giri S, Gómez-Meda B, Gómez-Arroyo S, Hadjidekova V, Haveric A, Kamboj M, Kurteshi K, Martino-Roth MG, Montero Montoya R, Nersesyan A, Pastor-Benito S, Favero Salvadori DM, Shaposhnikova A, Stopper H, Thomas P, Torres-Bugarín O, Yadav AS, Zúñiga González G, Fenech M. The HUman MicroNucleus project on eXfoLiated buccal cells (HUMN(XL): The role of lifestyle, host factors, occupational exposures, health status, and assay protocol. Mutat Res 2011;728:88-97. doi: 10.1016/j. mrrev.2011.06.005Search in Google Scholar

38. Ceppi M, Biasotti B, Fenech M, Bonassi S. Human population studies with the exfoliated buccal micronucleus assay: statistical and epidemiological issues. Mutat Res 2010;705:11-9. doi: 10.1016/j.mrrev.2009.11.001Search in Google Scholar

39. Angelieri F, de Oliveira GR, Sannomiya EK, Ribeiro DA. DNA damage and cellular death in oral mucosa cells of children who have undergone panoramic dental radiography. Pediatr Radiol 2007;37:561-5. doi: 10.1007/s00247-007-0478-1Search in Google Scholar

40. Lorenzoni DC, Fracalossi AC, Carlin V, Ribeiro DA, Sant’anna EF. Cytogenetic biomonitoring in children submitting to a complete set of radiographs for orthodontic planning. Angle Orthod 2012;82:585-90. doi: 10.2319/072311-468.1Search in Google Scholar

41. Ribeiro DA, de Oliveira G, de Castro G, Angelieri F. Cytogenetic biomonitoring in patients exposed to dental X-rays: comparison between adults and children. Dentomaxillofac Radiol 2008;37:404-7. doi: 10.1259/ dmfr/58548698Search in Google Scholar

42. Cerqueira EM, Gomes-Filho IS, Trindade S, Lopes MA, Passos JS, Machado-Santelli GM. Genetic damage in exfoliated cells from oral mucosa of individuals exposed to X-rays during panoramic dental radiographies. Mutat Res 2004;562:111-7. doi: 10.1016/j.mrgentox.2004.05.008Search in Google Scholar

43. Choi J-W. Assessment of panoramic radiography as a national oral examination tool: review of the literature. Imaging Sci Dent 2011;41:1-6. doi: 10.5624/isd.2011.41.1.1Search in Google Scholar

44. Milić M, Rozgaj R, Kašuba V, Jazbec A-M, Starčević B, Lyzbicki B, Ravegnini G, Zenesini C, Musti M, Hrelia P, Angelini S. Polymorphisms in DNA repair genes: link with biomarkers of the CBMN cytome assay in hospital workers chronically exposed to low doses of ionising radiation. Arh Hig Rada Toksikol 2015;66:109-120. doi: 10.1515/aiht-2015-66-2655Search in Google Scholar

45. Ferreira FLS, Pra D, Martino-Roth MG, Garcias GL. Buccal micronucleus frequency is associated with age in Down syndrome. Genet Mol Res 2009;8:1231-7. doi: 10.4238/ vol8-4gmr636Search in Google Scholar

46. Holland N, Harmatz P, Golden D, Hubbard A, Wu YY, Bae J, Chen C, Huen K, Heyman MB. Cytogenetic damage in blood lymphocytes and exfoliated epithelial cells of children with inflammatory bowel disease. Pediatr Res 2007;61:209-14. doi: 10.1203/pdr.0b013e31802d77c7Search in Google Scholar

47. Minicucci EM, Ribeiro DA, de Camargo B, Costa MC, Ribeiro LR, Salvador DMF. DNA damage in lymphocytes and buccal mucosa cells of children with malignant tumours undergoing chemotherapy. Clin Exp Med 2008;8:79-85. doi: 10.1007/s10238-008-0161-3Search in Google Scholar

48. Ünal M, Çelik A, Ateş NA, Micozkadioğlu D, Derici E, Pata YS, Akbaş Y. Cytogenetic biomonitoring in children with chronic tonsillitis: Micronucleus frequency in exfoliated buccal epithelium cells. Int J Pediatr Otorhinolaryngol 2005;69:1483-8. doi: 10.1016/j.ijporl.2005.04.002Search in Google Scholar

49. Karahalil B, Karakaya AE, Burgaz S. The micronucleus assay in exfoliated buccal cells: application to occupational exposure to polycyclic aromatic hydrocarbons. Mutat Res 1999;442:29-35. doi: 10.1016/S1383-5718(99)00055-8Search in Google Scholar

50. Ceretti E, Feretti D, Viola GC, Zerbini I, Limina RM, Zani C, Capelli M, Lamera R, Donato F, Gelatti U. DNA damage in buccal mucosa cells of pre-school children exposed to high levels of urban air pollutants. PLoS One 2014;9:e96524. doi: 10. 1371/ journal. pone.0096524Search in Google Scholar

51. El-Ashiry EA, Abo-Hager EA, Gawish AS. Genotoxic effects of dental panoramic radiograph in children. J Clin Pediatr Dent 2010;35:69-74. doi: 10.17796/jcpd.35.1.y61382473 5287307Search in Google Scholar

52. Thomas P, Harvey S, Gruner T, Fenech M. The buccal cytome and micronucleus frequency is substantially altered in Down’s syndrome and normal ageing compared to young healthy controls. Mutat Res 2008;638:37-47. doi: 10.1016/j. mrfmmm.2007.08.012Search in Google Scholar

53. Bolognesi C, Roggieri P, Ropolo M, Thomas P, Hor M, Fenech M, Nersesyan A, Knasmueller S. Buccal micronucleus cytome assay: results of an intra- and inter-laboratory scoring comparison. Mutagenesis 2015;30:545-55. doi: 10.1093/ mutage/gev017 Search in Google Scholar