Increased DNA Damage of Radiology Personnel Chronically Exposed to Low Levels of Ionizing Radiations
Yıl 2020,
Cilt: 11 Sayı: 2, 212 - 216, 15.06.2020
Vehbi Atahan Toğay
,
Funda Yıldırım Baş
,
Dilek Aşcı Çelik
,
Nurten Özçelik
,
Gülçin Yavuz Türel
,
Mustafa Calapoğlu
,
Pinar Aslan Kosar
Öz
Objective:
Occupational life has a direct relation with health. People working in the
hospital units such as Radiology and Nuclear Medicine are subject to higher
doses of ionizing radiation than ordinary person. We examined the association
between DNA damage and ionizing radiation exposure in the personnel working in
university hospital and considered different variables such as smoking, age
etc. Material - Method: DNA Damage
levels were estimated via comet assay in peripheral lymphocytes from 48 exposed
and from 51 non-exposed subjects, aged between 18-57 years old. Tail DNA
percentage parameter, obtained through Open Comet program, was chosen to assess
DNA damage and the results were evaluated by the One - Way Anova statistical test.
Results: The results, obtained from
statistical comparison of tail DNA percentage parameter, indicate that even the
low dose radiation caused DNA damage and age, gender, smoking habits and
working years did not show any significant differences except for dosimetry
value. Increasing dosimetry value resulted in increased DNA damage. Conclusion: This work supports the
previous results of biomonitoring of radiology workers chronically exposed to
ionizing radiation. This means ionizing radiation is still an important DNA
damaging agent despite many improvements such as exposed time reduction,
working conditions and technology.
Destekleyen Kurum
Süleyman Demirel Üniversitesi (ÖYP)
Proje Numarası
ÖYP05708-YL-13
Teşekkür
Research permission has been obtained from the Süleyman Demirel University Ethics Committee for Clinical Research (N: 135). We thank to volunteers who participated in this work. This work was supported by Süleyman Demirel University ÖYP Coordination Unit under grant [ÖYP05708-YL-13].
Kaynakça
- 1. Parlar S. Sağlık Çalışanlarında Göz Ardı Edilen Bir Durum: Sağlıklı Çalışma Ortamı. TAF Preventive Medicine Bulletin. 2008;7(6):547-54.
- 2. Valentin J. The 2007 recommendations of the international commission on radiological protection: Elsevier Oxford; 2007.
- 3. ICRP. Radiation and your patient: A guide for medical practitioners: International Commission on Radiological Protection; 2001 [Available from: http://www.icrp.org/docs/Rad_for_GP_for_web.pdf.
- 4. Nassef M, Kinsara A. Occupational radiation dose for medical workers at a University Hospital. Journal of Taibah University for Science. 2017;11(6):1259-66.
- 5. IAEA. Occupational Radiation Protection. Austria: International Atomic Energy Agency; 1999. 73 p.
- 6. IAEA. Occupational Radiation Protection General Safety Guide GSG-7. Vienna: International Atomic Energy Agency; 2018. 335 p.
- 7. Al-Abdulsalam A, Brindhaban A. Occupational radiation exposure among the staff of departments of nuclear medicine and diagnostic radiology in Kuwait. Medical Principles and Practice. 2014;23(2):129-33.
- 8. Zakeri F, Hirobe T. A cytogenetic approach to the effects of low levels of ionizing radiations on occupationally exposed individuals. European journal of radiology. 2010;73(1):191-5.
- 9. Thompson LH. Recognition, signaling, and repair of DNA double-strand breaks produced by ionizing radiation in mammalian cells: the molecular choreography. Mutation Research/Reviews in Mutation Research. 2012;751(2):158-246.
- 10. Riley PA. Free Radicals in Biology: Oxidative Stress and the Effects of Ionizing Radiation. International Journal of Radiation Biology. 1994;65(1):27-33.
- 11. Sutherland BM, Bennett PV, Sidorkina O, Laval J. Clustered DNA damages induced in isolated DNA and in human cells by low doses of ionizing radiation. Proceedings of the National Academy of Sciences. 2000;97(1):103-8.
- 12. Engin AB, Ergun MA, Yurtcu E, Kan D, Sahin G. Effect of ionizing radiation on the pteridine metabolic pathway and evaluation of its cytotoxicity in exposed hospital staff. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2005;585(1):184-92.
- 13. Kaya A. İyonize Radyasyonun Siyolojik Etkileri. Dicle Tıp Dergisi (Journal of Medical School). 2002;100(29):3.
- 14. Ueno S, Kashimoto T, Susa N, Natsume H, Toya M, Ito N, et al. Assessment of DNA damage in multiple organs of mice after whole body X-irradiation using the comet assay. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2007;634(1):135-45.
15. Al-Baker EA, Oshin M, Hutchison CJ, Kill IR. Analysis of UV-induced damage and repair in young and senescent human dermal fibroblasts using the comet assay. Mechanisms of ageing and development. 2005;126(6):664-72.
- 16. Olive PL. The role of DNA single-and double-strand breaks in cell killing by ionizing radiation. Radiat Res. 1998;150(5s):S42-S51.
- 17. Klaude M, Eriksson S, Nygren J, Ahnström G. The comet assay: mechanisms and technical considerations. Mutation Research/DNA Repair. 1996;363(2):89-96.
- 18. Tice R, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, et al. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environmental and molecular mutagenesis. 2000;35(3):206-21.
- 19. Nandhakumar S, Parasuraman S, Shanmugam M, Rao KR, Chand P, Bhat BV. Evaluation of DNA damage using single-cell gel electrophoresis (Comet Assay). Journal of pharmacology & pharmacotherapeutics. 2011;2(2):107.
- 20. Collins AR. The comet assay for DNA damage and repair. Molecular biotechnology. 2004;26(3):249-61.
- 21. Liao W, McNutt MA, Zhu W-G. The comet assay: a sensitive method for detecting DNA damage in individual cells. Methods. 2009;48(1):46-53.
- 22. Olive PL, Banáth JP. The comet assay: a method to measure DNA damage in individual cells. Nature Protocols (Electronic Edition). 2006;1(1):23.
- 23. Garaj-Vrhovac V, Kopjar N. The alkaline Comet assay as biomarker in assessment of DNA damage in medical personnel occupationally exposed to ionizing radiation. Mutagenesis. 2003;18(3):265-71.
- 24. Dinçer Y, Kankaya S. DNA hasarının belirlenmesinde Comet assay. Turkiye Klinikleri Journal of Medical Sciences. 2010;30(4):1365-73.
- 25. Valverde M, Rojas E. Environmental and occupational biomonitoring using the Comet assay. Mutation Research/Reviews in Mutation Research. 2009;681(1):93-109.
- 26. Dusinska M, Collins AR. The comet assay in human biomonitoring: gene–environment interactions. Mutagenesis. 2008;23(3):191-205.
- 27. Anderson D, Dhawan A, Laubenthal J. The comet assay in human biomonitoring. Genotoxicity Assessment: Methods and Protocols. 2013:347-62.
- 28. Cemeli E, Baumgartner A, Anderson D. Antioxidants and the Comet assay. Mutation Research/Reviews in Mutation Research. 2009;681(1):51-67.
- 29. Moon JM, Chun BJ, Cho YS, Lee SD, Hong YJ, Shin MH, et al. Cardiovascular Effects and Fatality May Differ According to the Formulation of Glyphosate Salt Herbicide. Cardiovascular Toxicology. 2018;18(1):99-107.
- 30. Gyori BM, Venkatachalam G, Thiagarajan P, Hsu D, Clement M-V. OpenComet: An automated tool for comet assay image analysis. Redox biology. 2014;2:457-65.
- 31. Singh NP, McCoy MT, Tice RR, Schneider EL. A simple technique for quantitation of low levels of DNA damage in individual cells. Experimental cell research. 1988;175(1):184-91.
- 32. Kumaravel TS, Jha AN. Reliable Comet assay measurements for detecting DNA damage induced by ionising radiation and chemicals. Mutation Research-Genetic Toxicology and Environmental Mutagenesis. 2006;605(1-2):7-16.
- 33. IBM. IBM SPSS Statistics for Windows, Version 20.0. . Armonk, NY:: IBM Corp.; 2012.
- 34. Hızarcı S. Radyasyon Kaynakları ve Radyasyondan Korunma Ankara: Radyasyon Sağlığı ve Güvenliği Dairesi-Turkish Atomic Energy Authority; 2010 [Available from: http://www.cygm.gov.tr/CYGM/Files/Guncelbelgeler/Radyasyon_olcum_sunum.pdf.
- 35. Wang Y, Xu C, Du LQ, Cao J, Liu JX, Su X, et al. Evaluation of the Comet Assay for Assessing the Dose-Response Relationship of DNA Damage Induced by Ionizing Radiation. International Journal of Molecular Sciences. 2013;14(11):22449-61.
- 36. Vellingiri B, Shanmugam S, Subramaniam MD, Balasubramanian B, Meyyazhagan A, Alagamuthu K, et al. Cytogenetic endpoints and Xenobiotic gene polymorphism in lymphocytes of hospital workers chronically exposed to ionizing radiation in Cardiology, Radiology and Orthopedic Laboratories. Ecotoxicology and environmental safety. 2014;100:266-74.
- 37. Ündeger Ü, Zorlu AF, Basaran N. Use of the alkaline comet assay to monitor DNA damage in technicians exposed to low-dose radiation. Journal of occupational and environmental medicine. 1999;41(8):693-8.
- 38. Wojewódzka M, Kruszewski M, Iwaneñko T, Collins AR, Szumiel I. Application of the comet assay for monitoring DNA damage in workers exposed to chronic low-dose irradiation: I. Strand breakage. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 1998;416(1):21-35.
- 39. Bedir A, Bilgici B, Yurdakul Z, Gürsel BŞ, Alvur A. DNA Hasarı Analizinde µ-Fadu ve Comet Yöntemlerinin Karşılaştırılması. Türk Klinik Biyokimya Dergisi. 2004;2(3):97-103.
- 40. Martinez A, Coleman M, Romero-Talamas CA, Frias S. An assessment of immediate DNA damage to occupationally exposed workers to low dose ionizing radiation by using the comet assay. Revista De Investigacion Clinica-Clinical and Translational Investigation. 2010;62(1):23-30.
- 41. Dias FL, Antunes LM, Rezende PA, Carvalho FE, Silva CM, Matheus JM, et al. Cytogenetic analysis in lymphocytes from workers occupationally exposed to low levels of ionizing radiation. Environmental toxicology and pharmacology. 2007;23(2):228-33.
- 42. Bozkurt G, Yuksel M, Karabogaz G, Sut N, Savran FO, Palanduz S, et al. Sister chromatid exchanges in lymphocytes of nuclear medicine physicians. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2003;535(2):205-13.
- 43. Leal BZ, Deahl TS, Meltz ML. Variability in adaptive response to low dose radiation in human blood lymphocytes: consistent results from chromosome aberrations and micronuclei. Mutation Research Letters. 1995;348(1):45-50.
- 44. Zakeri F, Assaei RG. Cytogenetic monitoring of personnel working in angiocardiography laboratories in Iran hospitals. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2004;562(1):1-9.
- 45. Ballardin M, Antonelli A, Cipollini M, Fallahi P, Scarpato R, Tomei A, et al. Induction of chromatid-type aberrations in peripheral lymphocytes of hospital workers exposed to very low doses of radiation. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2007;626(1):61-8.
- 46. Sari-Minodier I, Orsière T, Auquier P, Martin F, Botta A. Cytogenetic monitoring by use of the micronucleus assay among hospital workers exposed to low doses of ionizing radiation. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2007;629(2):111-21.
- 47. Tug E, Kayhan G, Kan D, Guntekin S, Ergun M. The evaluation of long-term effects of ionizing radiation through measurement of current sister chromatid exchange (SCE) rates in radiology technologists, compared with previous SCE values. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2013;757(1):28-30.
- 48. Martínez A, Coleman M, Romero-Talamás CA, Frías S. An assessment of immediate DNA damage to occupationally exposed workers to low dose ionizing radiation by using the comet assay. Rev Invest Clin. 2010;62(1):23-30.
- 49. Cardoso R, Takahashi‐Hyodo S, Peitl Jr P, Ghilardi‐Neto T, Sakamoto‐Hojo E. Evaluation of chromosomal aberrations, micronuclei, and sister chromatid exchanges in hospital workers chronically exposed to ionizing radiation. Teratogenesis, carcinogenesis, and mutagenesis. 2001;21(6):431-9.
- 50. Güerci AM, Grillo CA, Dulout FN, Seoane AI. Assessment of genotoxic damage in lymphocytes of hospital workers exposed to ionizing radiation in Argentina. Archives of environmental & occupational health. 2006;61(4):163-9.
- 51. Hoffmann H, Speit G. Assessment of DNA damage in peripheral blood of heavy smokers with the comet assay and the micronucleus test. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2005;581(1):105-14.
- 52. Hoffmann H, Högel J, Speit G. The effect of smoking on DNA effects in the comet assay: a meta-analysis. Mutagenesis. 2005;20(6):455-66.
Increased DNA Damage of Radiology Personnel Chronically Exposed to Low Levels of Ionizing Radiations
Yıl 2020,
Cilt: 11 Sayı: 2, 212 - 216, 15.06.2020
Vehbi Atahan Toğay
,
Funda Yıldırım Baş
,
Dilek Aşcı Çelik
,
Nurten Özçelik
,
Gülçin Yavuz Türel
,
Mustafa Calapoğlu
,
Pinar Aslan Kosar
Öz
Amaç: Çalışma
yaşamının sağlıkla doğrudan ilişkisi bulunmaktadır. Hastanelerin radyoloji veya
nükleer tıp birimlerinde çalışanlar, sıradan insanlara göre daha yüksek
dozlarda iyonize radyasyona maruz kalmaktadır. Çalışmamızda radyoloji
personelinin DNA hasarı ile iyonize radyasyona maruziyetleri arasındaki ilişki
incelenmiş ve sigara içme alışkanlığı ile yaş gibi farklı parametreler de
hesaba katılmıştır. Materyal – Metot:
18 ila 57 yaş aralığında, 48 kişiden
oluşan radyolojik birimlerde çalışan personel grubu ile 51 kişiden oluşan
kontrol grubunun DNA hasar miktarları komet metodu ile tespit edilmiştir. Open
Comet programı aracılığı ile elde edilen Kuyruk DNA yüzdesi parametresi DNA
hasarını göstermesi için seçilmiş ve sonuçlar tek yönlü anova istatistik testi
ile değerlendirilmiştir. Bulgular: Kuyruk
DNA yüzdesi parametresinin istatistiksel olarak karşılaştırılması sonucunda elde
edilen veriler düşük doz radyasyonun bile DNA hasarına sebep olduğunu ve dozimetre
değerinin önemli bir değişken olduğunu göstermektedir. Dozimetre değeri
arttıkça daha yüksek DNA hasarı tespit edilmiştir. Yaş, cinsiyet, sigara içme
alışkanlığı ve çalışma yılı ise anlamlı bir farklılığa sebep olmamıştır. Sonuç: Sonuçlar, radyoloji personelini
konu alan benzer çalışmalarda bildirilen biyo-izleme verileri ile paralellik
göstermektedir. Bu durum, gelişen teknoloji ve çalışma koşullarının geliştirilmesi
gibi önemli iyileştirmelere rağmen iyonize radyasyonun radyolojik birimlerde
çalışan personel için halen önemli bir DNA hasar ajanı olduğunu ortaya
koymaktadır.
Proje Numarası
ÖYP05708-YL-13
Kaynakça
- 1. Parlar S. Sağlık Çalışanlarında Göz Ardı Edilen Bir Durum: Sağlıklı Çalışma Ortamı. TAF Preventive Medicine Bulletin. 2008;7(6):547-54.
- 2. Valentin J. The 2007 recommendations of the international commission on radiological protection: Elsevier Oxford; 2007.
- 3. ICRP. Radiation and your patient: A guide for medical practitioners: International Commission on Radiological Protection; 2001 [Available from: http://www.icrp.org/docs/Rad_for_GP_for_web.pdf.
- 4. Nassef M, Kinsara A. Occupational radiation dose for medical workers at a University Hospital. Journal of Taibah University for Science. 2017;11(6):1259-66.
- 5. IAEA. Occupational Radiation Protection. Austria: International Atomic Energy Agency; 1999. 73 p.
- 6. IAEA. Occupational Radiation Protection General Safety Guide GSG-7. Vienna: International Atomic Energy Agency; 2018. 335 p.
- 7. Al-Abdulsalam A, Brindhaban A. Occupational radiation exposure among the staff of departments of nuclear medicine and diagnostic radiology in Kuwait. Medical Principles and Practice. 2014;23(2):129-33.
- 8. Zakeri F, Hirobe T. A cytogenetic approach to the effects of low levels of ionizing radiations on occupationally exposed individuals. European journal of radiology. 2010;73(1):191-5.
- 9. Thompson LH. Recognition, signaling, and repair of DNA double-strand breaks produced by ionizing radiation in mammalian cells: the molecular choreography. Mutation Research/Reviews in Mutation Research. 2012;751(2):158-246.
- 10. Riley PA. Free Radicals in Biology: Oxidative Stress and the Effects of Ionizing Radiation. International Journal of Radiation Biology. 1994;65(1):27-33.
- 11. Sutherland BM, Bennett PV, Sidorkina O, Laval J. Clustered DNA damages induced in isolated DNA and in human cells by low doses of ionizing radiation. Proceedings of the National Academy of Sciences. 2000;97(1):103-8.
- 12. Engin AB, Ergun MA, Yurtcu E, Kan D, Sahin G. Effect of ionizing radiation on the pteridine metabolic pathway and evaluation of its cytotoxicity in exposed hospital staff. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2005;585(1):184-92.
- 13. Kaya A. İyonize Radyasyonun Siyolojik Etkileri. Dicle Tıp Dergisi (Journal of Medical School). 2002;100(29):3.
- 14. Ueno S, Kashimoto T, Susa N, Natsume H, Toya M, Ito N, et al. Assessment of DNA damage in multiple organs of mice after whole body X-irradiation using the comet assay. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2007;634(1):135-45.
15. Al-Baker EA, Oshin M, Hutchison CJ, Kill IR. Analysis of UV-induced damage and repair in young and senescent human dermal fibroblasts using the comet assay. Mechanisms of ageing and development. 2005;126(6):664-72.
- 16. Olive PL. The role of DNA single-and double-strand breaks in cell killing by ionizing radiation. Radiat Res. 1998;150(5s):S42-S51.
- 17. Klaude M, Eriksson S, Nygren J, Ahnström G. The comet assay: mechanisms and technical considerations. Mutation Research/DNA Repair. 1996;363(2):89-96.
- 18. Tice R, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, et al. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environmental and molecular mutagenesis. 2000;35(3):206-21.
- 19. Nandhakumar S, Parasuraman S, Shanmugam M, Rao KR, Chand P, Bhat BV. Evaluation of DNA damage using single-cell gel electrophoresis (Comet Assay). Journal of pharmacology & pharmacotherapeutics. 2011;2(2):107.
- 20. Collins AR. The comet assay for DNA damage and repair. Molecular biotechnology. 2004;26(3):249-61.
- 21. Liao W, McNutt MA, Zhu W-G. The comet assay: a sensitive method for detecting DNA damage in individual cells. Methods. 2009;48(1):46-53.
- 22. Olive PL, Banáth JP. The comet assay: a method to measure DNA damage in individual cells. Nature Protocols (Electronic Edition). 2006;1(1):23.
- 23. Garaj-Vrhovac V, Kopjar N. The alkaline Comet assay as biomarker in assessment of DNA damage in medical personnel occupationally exposed to ionizing radiation. Mutagenesis. 2003;18(3):265-71.
- 24. Dinçer Y, Kankaya S. DNA hasarının belirlenmesinde Comet assay. Turkiye Klinikleri Journal of Medical Sciences. 2010;30(4):1365-73.
- 25. Valverde M, Rojas E. Environmental and occupational biomonitoring using the Comet assay. Mutation Research/Reviews in Mutation Research. 2009;681(1):93-109.
- 26. Dusinska M, Collins AR. The comet assay in human biomonitoring: gene–environment interactions. Mutagenesis. 2008;23(3):191-205.
- 27. Anderson D, Dhawan A, Laubenthal J. The comet assay in human biomonitoring. Genotoxicity Assessment: Methods and Protocols. 2013:347-62.
- 28. Cemeli E, Baumgartner A, Anderson D. Antioxidants and the Comet assay. Mutation Research/Reviews in Mutation Research. 2009;681(1):51-67.
- 29. Moon JM, Chun BJ, Cho YS, Lee SD, Hong YJ, Shin MH, et al. Cardiovascular Effects and Fatality May Differ According to the Formulation of Glyphosate Salt Herbicide. Cardiovascular Toxicology. 2018;18(1):99-107.
- 30. Gyori BM, Venkatachalam G, Thiagarajan P, Hsu D, Clement M-V. OpenComet: An automated tool for comet assay image analysis. Redox biology. 2014;2:457-65.
- 31. Singh NP, McCoy MT, Tice RR, Schneider EL. A simple technique for quantitation of low levels of DNA damage in individual cells. Experimental cell research. 1988;175(1):184-91.
- 32. Kumaravel TS, Jha AN. Reliable Comet assay measurements for detecting DNA damage induced by ionising radiation and chemicals. Mutation Research-Genetic Toxicology and Environmental Mutagenesis. 2006;605(1-2):7-16.
- 33. IBM. IBM SPSS Statistics for Windows, Version 20.0. . Armonk, NY:: IBM Corp.; 2012.
- 34. Hızarcı S. Radyasyon Kaynakları ve Radyasyondan Korunma Ankara: Radyasyon Sağlığı ve Güvenliği Dairesi-Turkish Atomic Energy Authority; 2010 [Available from: http://www.cygm.gov.tr/CYGM/Files/Guncelbelgeler/Radyasyon_olcum_sunum.pdf.
- 35. Wang Y, Xu C, Du LQ, Cao J, Liu JX, Su X, et al. Evaluation of the Comet Assay for Assessing the Dose-Response Relationship of DNA Damage Induced by Ionizing Radiation. International Journal of Molecular Sciences. 2013;14(11):22449-61.
- 36. Vellingiri B, Shanmugam S, Subramaniam MD, Balasubramanian B, Meyyazhagan A, Alagamuthu K, et al. Cytogenetic endpoints and Xenobiotic gene polymorphism in lymphocytes of hospital workers chronically exposed to ionizing radiation in Cardiology, Radiology and Orthopedic Laboratories. Ecotoxicology and environmental safety. 2014;100:266-74.
- 37. Ündeger Ü, Zorlu AF, Basaran N. Use of the alkaline comet assay to monitor DNA damage in technicians exposed to low-dose radiation. Journal of occupational and environmental medicine. 1999;41(8):693-8.
- 38. Wojewódzka M, Kruszewski M, Iwaneñko T, Collins AR, Szumiel I. Application of the comet assay for monitoring DNA damage in workers exposed to chronic low-dose irradiation: I. Strand breakage. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 1998;416(1):21-35.
- 39. Bedir A, Bilgici B, Yurdakul Z, Gürsel BŞ, Alvur A. DNA Hasarı Analizinde µ-Fadu ve Comet Yöntemlerinin Karşılaştırılması. Türk Klinik Biyokimya Dergisi. 2004;2(3):97-103.
- 40. Martinez A, Coleman M, Romero-Talamas CA, Frias S. An assessment of immediate DNA damage to occupationally exposed workers to low dose ionizing radiation by using the comet assay. Revista De Investigacion Clinica-Clinical and Translational Investigation. 2010;62(1):23-30.
- 41. Dias FL, Antunes LM, Rezende PA, Carvalho FE, Silva CM, Matheus JM, et al. Cytogenetic analysis in lymphocytes from workers occupationally exposed to low levels of ionizing radiation. Environmental toxicology and pharmacology. 2007;23(2):228-33.
- 42. Bozkurt G, Yuksel M, Karabogaz G, Sut N, Savran FO, Palanduz S, et al. Sister chromatid exchanges in lymphocytes of nuclear medicine physicians. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2003;535(2):205-13.
- 43. Leal BZ, Deahl TS, Meltz ML. Variability in adaptive response to low dose radiation in human blood lymphocytes: consistent results from chromosome aberrations and micronuclei. Mutation Research Letters. 1995;348(1):45-50.
- 44. Zakeri F, Assaei RG. Cytogenetic monitoring of personnel working in angiocardiography laboratories in Iran hospitals. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2004;562(1):1-9.
- 45. Ballardin M, Antonelli A, Cipollini M, Fallahi P, Scarpato R, Tomei A, et al. Induction of chromatid-type aberrations in peripheral lymphocytes of hospital workers exposed to very low doses of radiation. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2007;626(1):61-8.
- 46. Sari-Minodier I, Orsière T, Auquier P, Martin F, Botta A. Cytogenetic monitoring by use of the micronucleus assay among hospital workers exposed to low doses of ionizing radiation. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2007;629(2):111-21.
- 47. Tug E, Kayhan G, Kan D, Guntekin S, Ergun M. The evaluation of long-term effects of ionizing radiation through measurement of current sister chromatid exchange (SCE) rates in radiology technologists, compared with previous SCE values. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2013;757(1):28-30.
- 48. Martínez A, Coleman M, Romero-Talamás CA, Frías S. An assessment of immediate DNA damage to occupationally exposed workers to low dose ionizing radiation by using the comet assay. Rev Invest Clin. 2010;62(1):23-30.
- 49. Cardoso R, Takahashi‐Hyodo S, Peitl Jr P, Ghilardi‐Neto T, Sakamoto‐Hojo E. Evaluation of chromosomal aberrations, micronuclei, and sister chromatid exchanges in hospital workers chronically exposed to ionizing radiation. Teratogenesis, carcinogenesis, and mutagenesis. 2001;21(6):431-9.
- 50. Güerci AM, Grillo CA, Dulout FN, Seoane AI. Assessment of genotoxic damage in lymphocytes of hospital workers exposed to ionizing radiation in Argentina. Archives of environmental & occupational health. 2006;61(4):163-9.
- 51. Hoffmann H, Speit G. Assessment of DNA damage in peripheral blood of heavy smokers with the comet assay and the micronucleus test. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2005;581(1):105-14.
- 52. Hoffmann H, Högel J, Speit G. The effect of smoking on DNA effects in the comet assay: a meta-analysis. Mutagenesis. 2005;20(6):455-66.