Chromosome aberrations frequency in peripheral blood lymphocytes in young tobacco smoking and non-smoking people

  • Anja Haverić Institute for Genetic Engineering and Biotechnology, University of Sarajevo
  • Sanin Haverić Institute for Genetic Engineering and Biotechnology, University of Sarajevo
  • Slavka Ibrulj Faculty of Medicine, University of Sarajevo


Introduction: Cigarette smoking is associated with severe health problems, especially cancers. In addition, cigarette smoking causes different genotoxic effects. Chromosome aberrations are one of well-known intermediate end points in carcinogenesis. The aim of this study was to compare frequencies of chromosome aberrations in peripheral blood lymphocytes between young smokers and non-smokes groups.

Methods: The study was conducted with 30 smokers (average age 26.93 years) and 30 non-smokers (average age 26.96 years), and included the analysis of 100 metaphases per each blood sample. Differences in the arithmetic means of determined frequencies of chromosome aberrations were tested by two-tailed t-test for independent samples with the significance level of p < 0.05.

Results: The results showed a significant increase in the frequencies of chromatid-type aberrations and total structural chromosome aberrations in smoker group. Frequencies of numerical aberrations did not differ significantly between two groups.

Conclusions: This study confirmed genotoxicity of cigarette smoking and provided new evidence about its clastogenic activity.


1. Agudo A, Bonet C, Travier N, González CA, Vineis P, Bueno-de-Mesquita HB, et al. Impact of cigarette smoking on cancer risk in the European prospective investigation into cancer and nutrition study. J Clin Oncol. 2012;30(36):4550-7.
2. Pereira CS, Juchniuk de Vozzi MS, Dos Santos SA, Vasconcelos MA, de Paz CC, Squire JA, et al. Smoking-induced chromosomal segregation anomalies identified by FISH analysis of sperm. Mol Cytogenet. 2014;7(1):58.
3. DeMarini DM. Genotoxicity of tobacco smoke and tobacco smoke condensate: a review. Mutat Res. 2004;567(2-3):447-74.
4. Pfeiffer P, Goedecke W, Obe G. Mechanisms of DNA double-strand break repair and their potential to induce chromosomal aberrations. Mutagenesis. 2000;15(4):289-302.
5. Iliakis G, Wang H, Perrault AR, Boecker W, Rosidi B, Windhofer F, et al. Mechanisms of DNA double strand break repair and chromosome aberration formation. Cytogenet Genome Res. 2004;104(1-4):14-20.
6. Hoffmann D, Hoffmann I. Letters to the editor, tobacco smoke components. Beitr Tabaksforsch Int. 1998;18(1):49-52. DOI: 10.2478/cttr-2013-0668.
7. Thielen A, Klus H, Muller L. Tobacco smoke: unraveling a controversial subject. Exp Toxicol Pathol. 2008;60(2-3):141-56.
8. Borgerding M, Klus H. Analysis of complex mixtures-cigarette smoke. Exp Toxicol Pathol. 2005;57(Suppl 1):43-73.
9. Kaina B, Ziouta A, Ochs K, Coquerelle T. Chromosomal instability, reproductive cell death and apoptosis induced by O6-methyleguanine in Mex-, Mex+, and methylation-tolerant mismatch repair compromised cells: facts and models. Mutat Res. 1997;381(2):227-41.

10. Christmann M, Kaina B. O(6)-methylguanine-DNA methyltransferase (MGMT): impact on cancer risk in response to tobacco smoke. Mutat Res. 2012;736(1-2):64-74.
11. Hagmar L, Stromberg U, Tinnerberg H, Mikoczy Z. The usefulness of cytogenetic biomarkers as intermediate endpoints in carcinogenesis. Int J Hyg Environ Health. 2001;204(1):43-7.
12. Bonassi S, Znaor A, Ceppi M, Lando C, Chang WP, Holland N, et al. An increased micronucleus frequency in peripheral blood lymphocytes predicts the risk of cancer in humans. Carcinogenesis. 2007;28(3):625-31.
13. Pryor WA. Cigarette smoke radicals and the role of free radicals in chemical carcinogenicity. Environ Health Perspect. 1997;105(4):875-82.
14. Uma AN, Dhananjay SK, Aroul TT. Chromosomal aberrations: a tool for early diagnosis of cancer in smokers in a rural Pondicherry population, India. Int J Curr Micobiol App Sci. 2014;3(10):587-93.
15. Yadav JS, Kler RS, Chadha P, Yadav AS. Spontaneous chromosomal aberrations in human populations of five endogamous groups of Haryana. J Cytol Genet. 2002;3(NS):121-6.
16. Sierra-Torres MS, Arboleda-Moreno YY, Hoyos LS, Sierra-Torres CH. Chromosome aberrations among cigarette smokers in Colombia. Mutat Res. 2004;562(1-2):67-75.
17. Bonassi S, Coskun E, Ceppi M, Lando C, Bolognesi C, Burgaz S, et al. The HUman MicroNucleus project on eXfoLiated buccal cells (HUMN(XL)): the role of life-style, host factors, occupational exposures, health status, and assay protocol. Mutat Res Rev Mutat Res. 2011;728(3):88-97.
18. Yadav AS, Saini M. Increased frequency of nuclear anomalies in exfoliated buccal mucosa of cigarette smokers. J Entomol Zool Stud. 2015;3(2):07-10.

19. Feki-Tounsi M, Khlifi R, Mhiri MN, Rebai A, Hamza-Chaffai A. Cytogenetic damage in the oral mucosa cells of bladder cancer patients exposed to tobacco in Southern Tunisia. Environ Sci Pollut Res Int. 2014;21(22):12922-7.
20. Naderi NJ, Farhadi S, Sarshar S. Micronucleus assay of buccal mucosa cells in smokers with the history of smoking less and more than 10 years. Indian J Pathol Microbiol. 2012;55(4):433-8.
21. Balansky R, Izzotti A, D'Agostini F, Longobardi M, Micale RT, La Maestra S, et al. Assay of lapatinib in murine models of cigarette smoke carcinogenesis. Carcinogenesis. 2014;35(10):2300-7.
22. Haverić A, Haverić S, Ibrulj S. Micronuclei frequencies in peripheral blood and buccal exfoliated cells of young smokers and non-smokers. Toxicol Mech Methods. 2010;20(5):260-6.
23. Bonassi S, Hagmar L, Strömberg U, Montagud AH, Tinnerberg H, Forni A, et al. Chromosomal aberrations in lymphocytes predict human cancer independently of exposure to carcinogens. European Study Group on Cytogenetic Biomarkers and Health. Cancer Res. 2000;60(6):1619-25.
24. Mitelman F. An International System for Human Cytogenetic Nomenclature (1995): Recommendations of the International Standing Committee on Human Cytogenetic Nomenclature. Memphis, Tenn: Karger; 1995.
25. Hammer O, Harper DAT, Ryan PD. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica. 2001;4(1):9.
26. Klebaner D, Huang Y, Hui Q, Taylor JY, Goldberg J, Vaccarino V, et al. X chromosome-wide analysis identifies DNA methylation sites influenced by cigarette smoking. Clin Epigenetics. 2016;8:20.
27. Lee KWK, Richmond R, Hu P, French L, Shin J, Bourdon C. Prenatal exposure to maternal cigarette smoking and DNA methylation: epigenome-wide association in a discovery sample of adolescents and replication in an independent cohort at birth through 17 years of age. Environ Health Perspect. 2015;123(2):193-9. DOI: 10.1289/ehp.1408614.
28. Bonassi S, Norppa H, Ceppi M, Strömberg U, Vermeulen R, Znaor A, et al. Chromosomal aberration frequency in lymphocytes predicts the risk of cancer: results from a pooled cohort study of 22 358 subjects in 11 countries. Carcinogenesis. 2008;29:1178-83.
29. Ibrulj S, Krunic-Haveric A, Haveric S, Pojskic N, Hadziselimovic R. Micronuclei occurrence in population exposed to depleted uranium and control human group in correlation with sex, age and smoking habit. Med Arh. 2003;58(6):335-8.
30. Nefic H, Handzic I. The effect of age, sex, and lifestyle factors on micronucleus frequency in peripheral blood lymphocytes of the Bosnian population. Mutat Res. 2013;753(1):1-11.
31. Ibrulj S, Haverić S, Haverić A. Chromosome aberrations as bioindicators of environmental genotoxicity. Bosn J Basic Med Sci. 2007;7(4):311-6.
32. OECD. In vitro mammalian chromosomal aberration test - OECD guideline for the testing of chemicals, TG 473. Adopted 26 September 2014.
33. Shi Q, Ko E, Barclay L, Hoang T, Rademaker A, Martin RE. Cigarette smoking and aneuploidy in human sperm. Mol Reprod Dev. 2001;59(4):417-21.
34. Dumanski JP, Rasi C, Lönn M, Davies H, Ingelsson M, Giedraitis V, et al. Smoking is associated with mosaic loss of chromosome Y. Science. 2015;347(6217):81-3.
35. Ibrulj S, Haverić S, Haverić A. Complementarity of standard cytogenetic assays.
Bosn J Basic Med Sci. 2008;8(1):27-33.
36. Garaj-Vrhovac V, Fucić A, Horvat D. The correlation between the frequency of micronuclei and specific chromosome aberrations in human lymphocytes exposed to microwave radiation in vitro. Mutat Res. 1992;281(3):181-6.

37. Fenech M, Kirsch-Volders M, Natarajan AT, Surralles J, Crott JW, Parry J, et al. Molecular mechanisms of micronucleus, nucleoplasmic bridge and nuclear bud formation in mammalian and human cells. Mutagen. 2011;26(1):125-32.
38. Zenic N, Terzic A, Rodek J, Spasic M, Sekulic D. Gender-specific analyses of the prevalence and factors associated with substance use and misuse among Bosniak adolescents. Int J Environ Res Public Health. 2015;12(6):6626-40.
39. Ibisevic M, Avdic A, Osmanovic E, Kadric N, Avdic S. Cigarette smoking among students at the University of Tuzla. Med Arch. 2015;69(2):127-9.
40. Padjen I, Dabić M, Glivetić T, Biloglav Z, Biočina-Lukenda D, Lukenda J. The analysis of tobacco consumption in Croatia - Are we successfully facing the epidemic? Cent Eur J Public Health. 2012;20(1):5-10.
41. Idrizovic K, Zenic N, Tahirail E, Rausavljevic N, Sekulic D. Cigarette smoking among 17-18 year old adolescents - prevalence and association with sociodemographic, familial, sport, and scholastic factors. Med Pr. 2015;66(2):153-63.
42. Hublet A, Bendtsen P, de Looze ME, Fotiou A, Donnelly P, Vilhjalmsson R, et al. Trends in the co-occurrence of tobacco and canabis use in 15-year olds from 2002 to 2010 in 28 countries of Europe and North America. Eur J Public Health. 2015;25(2):73-5.
43. Zenic N, Ostojic L, Sisic N, Pojskic H, Peric M, Uljevic O, et al. Examination of the community-specific prevalence and factors associated with substance use and misuse among rural and urban adolescents: a cross-sectional analysis in Bosnia and Herzegovina. BMJ Open. 2015;6(5):e009446.

44. Ibrulj S, Haverić S, Haverić A, Durmić-Pašić A, Marjanović D. Effect of war and postwar genotoxins on micronuclei frequency in Sarajevo study group. Bosn J Basic Med Sci. 2006;6(4):54-7.
45. Balachandar V, Kumar BL, Suresh K, Sasikala K. Evaluation of chromosome aberrations in subjects exposed to environmental tobacco smoke in Tamilnadu, India. Bull Environ Contam Toxicol. 2008;81(3):270-6.
46. Chandirasekar R, Suresh K, Jayakumar R, Venkatesan R, Lakshman Kumar B, Sasikala K. XRCC1 gene variants and possible links with chromosome aberrations and micronucleus in active and passive smokers. Environ Toxicol Pharmacol. 2011;32(2):185-92.
47. Hemminki K, Frank C, Försti A, Musak L, Kazimirova A, Barancokova M, et al. Metabolic gene variants associated with chromosomal aberrations in healthy humans. Genes Chromosomes Cancer. 2015;54(4):260-6.
48. Pirini F, Guida E, Lawson F, Mancinelli A, Guerrero-Preston R. Nuclear and mitochondrial DNA alterations in newborns with prenatal exposure to cigarette smoke. Int J Environ Res Public Health. 2015;12(2):1135-55.
How to Cite
HAVERIĆ, Anja; HAVERIĆ, Sanin; IBRULJ, Slavka. Chromosome aberrations frequency in peripheral blood lymphocytes in young tobacco smoking and non-smoking people. Journal of Health Sciences, [S.l.], v. 6, n. 2, p. 121-127, oct. 2016. ISSN 1986-8049. Available at: <>. Date accessed: 19 june 2018. doi:
Research articles


Tobacco genotoxicity; cytogenetic markers; lymphocytes culture.