Medical Radiology and Radiation Safety. 2025. Vol. 70. № 3
DOI:10.33266/1024-6177-2025-70-3-70-82
A.N. Koterov1, L.N. Ushenkova1, A.A. Wainson2,
D.Yu. Usupzhanova1, A.Yu. Bushmanov1
‘Healthy Worker Effect’ In Employees of Medical-Biological and Chemical Laboratories: Comparison with Effects in Nuclear Workers, in other Professional Contingents (Meta-Analyses),
and the Role of the Radiation Factor
1 A.I. Burnazyan Federal Medical Biophysical Center, Moscow, Russia
2 N.N. Blokhin Russian Cancer Research Center, Moscow, Russia
Contact person: Alexey N. Koterov, e-mail: Этот адрес электронной почты защищен от спам-ботов. У вас должен быть включен JavaScript для просмотра.
Abstract
Based on a search in a supported database of sources for standardized mortality ratio (SMR; compared with the general population) for all causes and all cancer mortality for various professions and types of employment, in PubMed, the Cochrane Library, Elibrary, through Google, Google Scholar and in the reference lists of found sources, a complete/representative sample of studies of SMR all causes and SMR all cancer for personnel of biomedical, agricultural, chemical and some other research laboratories (a total of 39 sources and 3 reviews) was formed. Meta-analyses performed on the basis of this sample demonstrated a high Healthy Worker Effect (HWE) for all causes for the total group of workers, for the group including biomedical, sanitary and agricultural laboratories, and for the group of chemists. SMR (±95 % confidence intervals) were, respectively: 0.63 (0.58; 0.68); 0.65 (0.57; 0.74) and 0.62 (0.56; 0.68). For SMR all cancer HWE, although of a smaller value, it was demonstrated for the first and second groups: 0.85 (95 % CI: 0.75; 0.96) and 0.78 (95 % CI: 0.70; 0.88), respectively. At the same time, for chemists, no excess in mortality from all cancers was noted either: 0.88 (95 % CI: 0.74; 1.05).
The HWE values for laboratory workers were compared with those for occupations characterized by the highest HWE values (cosmonauts/astronauts, athletes, pilots, nuclear workers, and the military; individual studies, meta- and pooled analyses). It was found that the scientific laboratory personnel had a HWE level for SMR all causes comparable to that of athletes and nuclear workers. However, the SMR all cancer index for laboratory researchers was significantly higher than in all comparison groups, with the exception of the military, which is obviously due to contacts with a variety of carcinogenic factors when working in laboratories.
Due to the absence of prerequisites for the formation of HWE characteristic of the compared contingents for the researchers, an assumption was made that the decrease in overall mortality among laboratory personnel may be primarily due to a scientific mindset, which allows them to better navigate the causal dependencies of life and more adequately prevent various consequences, rather than a special lifestyle, increased socioeconomic status and a decrease in the frequency of smoking (as some authors suggest).
Analysis of the influence of the radiation factor (external and internal irradiation) on the studied mortality rates for laboratory workers revealed some effects in relation to certain types of malignant neoplasms (leukemia, myeloma, lung cancer, bone cancer, etc.), but a number of them were not previously recognized as radiation-induced and their increase may be a consequence of the effect of other carcinogenic factors of work in chemical, biochemical, molecular biological and other laboratories.
Keywords: laboratory researchers, biomedical laboratories, chemists, all cause mortality, all cancer mortality, healthy worker effect, radiation exposure
For citation: Koterov AN, Ushenkova LN, Wainson AA, Usupzhanova DYu, Bushmanov AYu. ‘Healthy Worker Effect’ In Employees of Medical-Biological and Chemical Laboratories: Comparison with Effects in Nuclear Workers, in other Professional Contingents (Meta-Analyses), and the Role of the Radiation Factor. Medical Radiology and Radiation Safety. 2025;70(3):70–82. (In Russian). DOI:10.33266/1024-6177-2025-70-3-70-82
References
1. Котеров А.Н., Ушенкова Л.Н., Дибиргаджиев И.Г. База данных по стандартизованному отношению смертности (SMR all causes и SMR all cancer) для различных профессий (706 когорт/групп): максимальный «эффект здорового работника» – у космонавтов и врачей. Мед. труда и пром. экология // 2023a. Т.63. № 3. С. 179–192. https://doi.org/10.31089/1026-9428-2023-63-3-179-192. Koterov A.N., Ushenkova L.N., Dibirgadzhiev I.G. Database on standardized mortality ratio (SMR all causes and SMR all cancer) for various professions (706 cohorts/groups): the maximum ‘effect of a healthy worker’ – in astronauts and doctors. Meditsina truda i promyshlennaya ekologiya = Russian Journal of Occupational Health and Industrial Ecology. 2023a;63(3):179–92. (In Russ. Engl. abstr.) https://doi.org/10.31089/1026-9428-2023-63-3-179-192.
2. Котеров А.Н., Ушенкова Л.Н. Смертность профессиональных водителей 9 стран: систематический обзор и мета-анализ // Мед. труда и пром. экол. 2023b. Т.63. № 5. С. 315–326. https://doi.org/10.31089/1026-9428-2023-63-5-315-326. Koterov A.N., Ushenkova L.N. Professional driver mortality in 9 countries: a systematic review and meta-analysis. Meditsina truda i promyshlennaya ekologiya = Russian Journal of Occupational Health and Industrial Ecology. 2023b;63(5):315–326. (In Russ. Engl. abstr.) https://doi.org/10.31089/1026-9428-2023-63-5-315-326.
3. Котеров А.Н., Ушенкова Л.Н., Калинина М.В., Бирюков А.П. «Эффект здорового работника» по показателям общей смертности и смертности от злокачественных новообразований у персонала предприятий ядерной и химической индустрии: мета-анализы. Мед. радиология и радиац. безопасность // 2023c. Т.68. №4. С. 43–50. https://doi.org/10.33266/1024-6177-2023-68-4-43-50. Koterov A.N., Ushenkova L.N., Kalinina M.V., Biryukov A.P. The ‘Healthy worker effect’ on indexes of total mortality and malignant neoplasms mortality for nuclear and chemical workers: meta-analysis. Meditsinskaya radiologiya i radiatsionnaya bezopasnost’ = Medical Radiology and Radiation Safety. 2023c;68(4):43–50. (In Russ. Engl. abstr.) https://doi.org/10.33266/1024-6177-2023-68-4-43-50.
4. Котеров А.Н., Ушенкова Л.Н., Калинина М.В., Дибиргаджиев И.Г. Профессии, наиболее отражающиеся на здоровье: ядерная индустрия на последних местах по вредности (синтетическое исследование). В сборнике материалов международной научно-практической конференции «Здоровье и окружающая среда» (Минск, 23–24 ноября 2023 г.). М-во здравоохр. Респ. Беларусь. Науч.-практ. центр гигиены; редкол.: С.И. Сычик (гл. ред.). Минск: Изд. центр БГУ. 2023d. С. 96–100. Koterov A.N., Ushenkova L.N., Kalinina M.V., Dibirgadzhiev I.G. Professions that most affect health: the nuclear industry is in last place in terms of harmfulness (synthetic study). In the Collection of materials of the International Scientific and Practical conference ‘Health and the Environment’ (Minsk, November 23–24, 2023). Ministry of Health Rep. Belarus. Scientific-practical hygiene center; editorial board: S.I. Sychik (Chief editor). Minsk: Publishing house. BSU center 2023d: 96–100. (In Russ. Engl. abstr.)
5. Котеров А.Н., Ушенкова Л.Н., Дибиргаджиев И.Г., Калинина М.В. Смертность от всех причин и от всех раков для работников ядерной индустрии и шахтеров урановых рудников сравнительно с наиболее вредными/опасными профессиями (синтетическое исследование) // В сб. научн. тр. «Здоровье и окружающая среда». Под ред. С.И. Сычика и др. – Гомель: Редакция газеты «Гомельская прауда», 2024. С. 59–69. Koterov A.N., Ushenkova L.N., Kalinina M.V., Dibirgadzhiev I.G. All causes mortality and all cancers among nuclear industry workers and uranium miners compared with the most harmful/dangerous professions (synthetic study). In the collection of scientific papers ‘Health and the Environment’. Ed. by: S.I. Sychik et al. – Gomel: Editorial office of the newspaper ‘Gomelskaya Prauda’,: 2004: 59–69. (In Russ. Engl. abstr.)
6. Fawcett H.H. Exposures of personnel to laboratory hazards // Am. Ind. Hyg. Assoc. J. 1972. V.33. No.8. P. 559–567. https://doi.org/10.1080/0002889728506704. Fawcett H.H. Exposures of personnel to laboratory hazards. Am. Ind. Hyg. Assoc. J. 1972;33(8):559–67. https://doi.org/10.1080/0002889728506704.
7. Gusenbauer M., Haddaway N.R. Which academic search systems are suitable for systematic reviews or meta-analyses? Evaluating retrieval qualities of Google Scholar, PubMed, and 26 other resources// Res. Synth. Methods. 2020. Vol.11. No.2. P. 181–217. https://doi.org/10.1002/jrsm.1378. Gusenbauer M., Haddaway N.R. Which academic search systems are suitable for systematic reviews or meta-analyses? Evaluating retrieval qualities of Google Scholar, PubMed, and 26 other resources. Res. Synth. Methods. 2020;11(2):181–217. https://doi.org/10.1002/jrsm.1378.
8. Higgins J.P., Thompson S.G., Deeks J.J., Altman D.G. Measuring inconsistency in meta-analyses // Brit. Med. J. 2003. V.327. No.7414. P. 557–560. https://doi.org/10.1136/bmj.327.7414.557. Higgins J.P., Thompson S.G., Deeks J.J., Altman D.G. Measuring inconsistency in meta-analyses. Brit. Med. J. 2003;327(7414):557–60. https://doi.org/10.1136/bmj.327.7414.557.
9. Blettner M, Sauerbrei W, Schlehofer B, et al. Traditional reviews, meta-analyses and pooled analyses in epidemiology // Int. J. Epidemiol. 1999. V.28. No.1. P. 1–9. https://doi.org/10.1093/ije/28.1.1. Blettner M, Sauerbrei W, Schlehofer B, et al. Traditional reviews, meta-analyses and pooled analyses in epidemiology. Int. J. Epidemiol. 1999;28(1):1–9. https://doi.org/10.1093/ije/28.1.1.
10. Омельяновский В.В., Авксентьева М.В., Сура М.В., Хачатрян Г.Р., Федяева В.К. Методические рекомендации по проведению мета-анализа. М.: ФГБУ «ЦЭККМП» Минздрава России, 2017. 28 с. Omelyanovsky V.V., Avxentyeva M.V., Sura M.V., Khachatryan G.R., Fedyaeva V.K. Guidelines for conducting a meta-analysis. M.: FSBI ‘Center for Healthcare Quality Assessment and Control’ of the Ministry of Health of the Russian Federation, 2017. 28 p. (In Russ.)
11. Egger M., Davey Smith G., Schneider M., Minder C. Bias in meta-analysis detected by a simple, graphical test // Brit. Med. J. 1997. V.315. No.7109. P. 629–634. https://doi.org/10.1136/bmj.315.7109.629. Egger M., Davey Smith G., Schneider M., Minder C. Bias in meta-analysis detected by a simple, graphical test. Brit. Med. J. 1997;315(7109):629–34. https://doi.org/10.1136/bmj.315.7109.629.
12. Sterne J.A.C., Egger M. Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis // J. Clin. Epidemiol. 2001. V.54. No.10. P. 1046–1155. https://doi.org/10.1016/s0895-4356(01)00377-8. Sterne J.A.C., Egger M. Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J. Clin. Epidemiol. 2001;54(10):1046–155. https://doi.org/10.1016/s0895-4356(01)00377-8.
13. Кокунин В.А. Статистическая обработка данных при малом числе опытов // Украинский биохимический журнал. 1975. Т.47. №6. С.776–790. Kokunin V.A. Statistical processing of data from a small number of experiments. Ukrainskiy biokhimicheskiy zhurnal = Ukrainian Journal of Biochemistry. 1975;47(6):776–91. (In Russ.)
14. Li F.P., Fraumeni J.F., Mantel N., Miller R.W. Cancer mortality among chemists // J. Natl. Cancer Inst. 1969. V.43. No.5. P. 1159–1164. Li F.P., Fraumeni J.F., Mantel N., Miller R.W. Cancer mortality among chemists. J. Natl. Cancer Inst. 1969;43(5):1159–64.
15. Dement J.M., Cromer J.R. Cancer and reproductive risks among chemists and laboratory workers: a review // Appl. Occupat. Environ. Hyg. 1992. V.7. No.2. P. 120–126. https://doi.org/10.1080/1047322X.1992.10388032. Dement J.M., Cromer J.R. Cancer and reproductive risks among chemists and laboratory workers: a review. Appl. Occupat. Environ. Hyg. 1992;7(2):120–6. https://doi.org/10.1080/1047322X.1992.10388032.
16. Burrows G.E. Health care of people at work: screening of workers in research laboratories // J. Soc. Occup. Med. 1980. V.30. No.4. P. 164–168. https://doi.org/10.1093/occmed/30.4.164. Burrows G.E. Health care of people at work: screening of workers in research laboratories. J. Soc. Occup. Med. 1980;30(4):164–8. https://doi.org/10.1093/occmed/30.4.164.
17. Hoar S.K., Pell S. A retrospective cohort study of mortality and cancer incidence among chemists // J. Occup. Med. 1981. V.23. No.7. P. 485–494. https://doi.org/10.1097/00043764-198107000-00016. Hoar S.K., Pell S. A retrospective cohort study of mortality and cancer incidence among chemists. J. Occup. Med. 1981;23(7):485–94. https://doi.org/10.1097/00043764-198107000-00016.
18. Walrath J., Li F.P., Hoar S.K., Mead M.W., Fraumeni J.F. Jr. Causes of death among female chemists // Am. J. Public Health. 1985. V.75. No.8. P. 883–885. https://doi.org/10.2105/ajph.75.8.883. Walrath J., Li F.P., Hoar S.K., Mead M.W., Fraumeni J.F. Jr. Causes of death among female chemists. Am. J. Public Health. 1985;75(8):883–5. https://doi.org/10.2105/ajph.75.8.883.
19. Checkoway H., Mathew R.M., Shy C.M., Watson J.E. Jr, Tankersley W.G., Wolf S.H. et al. Radiation, work experience, and cause specific mortality among workers at an energy research laboratory // Br. J. Ind. Med. 1985. V.42. No.8. P. 525–533. https://doi.org/10.1136/oem.42.8.525. Checkoway H., Mathew R.M., Shy C.M., Watson J.E. Jr, Tankersley W.G., Wolf S.H. et al. Radiation, work experience, and cause specific mortality among workers at an energy research laboratory. Br. J. Ind. Med. 1985;42(8):525–33. https://doi.org/10.1136/oem.42.8.525.
20. Chiazze L. Jr, Waif P., Ference L.D. An historical study of mortality among salaried research and development workers of the Allied Corporation // J. Occup. Med. 1986. V.28. No.11. P. 1185–1188. Chiazze L. Jr, Waif P., Ference L.D. An historical study of mortality among salaried research and development workers of the Allied Corporation. J. Occup. Med. 1986;28(11):1185–8.
21. Divine B.J., Barron V. Texaco mortality study. II. Patterns of mortality among white males by specific job groups // Am. J. Ind. Med. 1986. V.10. No.4. P. 371–381. https://doi.org/10.1002/ajim.4700100405. Divine B.J., Barron V. Texaco mortality study. II. Patterns of mortality among white males by specific job groups. Am. J. Ind. Med. 1986;10(4):371–81. https://doi.org/10.1002/ajim.4700100405.
22. Maher K.V., DeFonso L.R. An historical cohort study of mortality among chemical researchers // Arch. Environ. Health. 1986. V.41. No.2. P.109–116. https://doi.org/10.1080/00039896.1986.9937419. Maher K.V., DeFonso L.R. An historical cohort study of mortality among chemical researchers. Arch. Environ. Health. 1986;41(2):109–16. https://doi.org/10.1080/00039896.1986.9937419.
23. Delzell E., Macaluso M., Cole P. A follow-up study of workers at a dye and resin manufacturing plant // J. Occup. Med. 1989. V.31. No.3. P. 273–278. https://doi.org/10.1097/00043764-198903000-00016. Delzell E., Macaluso M., Cole P. A follow-up study of workers at a dye and resin manufacturing plant. J. Occup. Med. 1989;31(3):273–8. https://doi.org/10.1097/00043764-198903000-00016.
24. Arnetz B.B., Raymond L.W., Nicolich M.J., Vargo L. Mortality among petrochemical science and engineering employees // Arch. Environ. Health. 1991. V.46. No.4. P. 237–248. https://doi.org/10.1080/00039896.1991.9937455. Arnetz B.B., Raymond L.W., Nicolich M.J., Vargo L. Mortality among petrochemical science and engineering employees. Arch Environ Health. 1991;46(4):237–48. https://doi.org/10.1080/00039896.1991.9937455.
25. Delzell E., Sathiakumar N., Hovinga M., Macaluso M., Julian J., Larson R. et al. A follow-up study of synthetic rubber workers // Toxicology. 1996. V.28. No.113(1–3). P. 182–189. https://doi.org/10.1016/0300-483x(96)03443-9. Delzell E., Sathiakumar N., Hovinga M., Macaluso M., Julian J., Larson R. et al. A follow-up study of synthetic rubber workers. Toxicology. 1996;113(1–3):182–9. https://doi.org/10.1016/0300-483x(96)03443-9.
26. 37. Himmelstein M.W., Acquavella J.F., Recio L., Medinsky M.A., Bond J.A. Toxicology and epidemiology of 1,3-butadiene // Crit. Rev. Toxicol. 1997. V. 27. No.1. P. 1–108. https://doi.org/10.3109/10408449709037482. Himmelstein M.W., Acquavella J.F., Recio L., Medinsky M.A., Bond J.A. Toxicology and epidemiology of 1,3-butadiene. Crit. Rev. Toxicol. 1997;27(1):1–108. https://doi.org/10.3109/10408449709037482.
27. Rodu B., Delzell E., Beall C., Sathiakumar N. Mortality among employees at a petrochemical research facility // Am. J. Ind. Med. 2001. V.39. No.1. P. 29–41. https://doi.org/10.1002/1097-0274(200101)39:1<29::AID-AJIM3>3.0.CO;2-K. Rodu B., Delzell E., Beall C., Sathiakumar N. Mortality among employees at a petrochemical research facility. Am J Ind Med. 2001;39(1):29–41. https://doi.org/10.1002/1097-0274(200101)39:1<29::AID-AJIM3>3.0.CO;2-K.
28. Buffler P.A., Kelsh M., Chapman P., Wood S., Lau E., Golembesky A. et al. Primary brain tumor mortality at a petroleum exploration and extraction research facility // J. Occup. Environ. Med. 2004. V.46. No.3. P. 257–270. https://doi.org/10.1097/01.jom.0000116816.09199.6d. Buffler P.A., Kelsh M., Chapman P., Wood S., Lau E., Golembesky A., Wood R., Kalmes R., Brorby G. Primary brain tumor mortality at a petroleum exploration and extraction research facility. J. Occup. Environ. Med. 2004;46(3):257–70. https://doi.org/10.1097/01.jom.0000116816.09199.6d.
29. Kubale T., Hiratzka S., Henn S., Markey A., Daniels R., Utterback D. A cohort mortality study of chemical laboratory workers at Department of Energy Nuclear Plants // Am. J. Ind. Med. 2008. V.51. No.9. P. 656–667. https://doi.org/10.1002/ajim.20601. Kubale T., Hiratzka S., Henn S., Markey A., Daniels R., Utterback D. A cohort mortality study of chemical laboratory workers at Department of Energy Nuclear Plants. Am. J. Ind. Med. 2008;51(9):656–67. https://doi.org/10.1002/ajim.20601.
30. Alexander B.H., Mandel J.H., Scott L.L.F., Ramachandran G., Chen Y.C. Brain cancer in workers employed at a specialty chemical research facility // Arch. Environ. Occup. Health. 2013. V.68. No.4. P. 218–227. https://doi.org/10.1080/19338244.2012.701248. Alexander B.H., Mandel J.H., Scott L.L.F., Ramachandran G., Chen Y.C. Brain cancer in workers employed at a specialty chemical research facility. Arch. Environ. Occup. Health. 2013;68(4):218–27. https://doi.org/10.1080/19338244.2012.701248.
31. Collins J.J., Bender T.J., Bonner E.M., Bodner K.M., Kreft A.M. Brain cancer in workers employed at a laboratory research facility // PLoS One. 2014. V.9. No.12. Article e113997. 12 p. https://doi.org/10.1371/journal.pone.0113997. Collins J.J., Bender T.J., Bonner E.M., Bodner K.M., Kreft A.M. Brain cancer in workers employed at a laboratory research facility. PLoS One. 2014;9(12):Article e113997. 12 p. https://doi.org/10.1371/journal.pone.0113997.
32. Olin R. Leukaemia and Hodgkin’s disease among Swedish chemistry graduates // Lancet. 1976. V.2. No.7991. P. 916. https://doi.org/10.1016/s0140-6736(76)90589-4. Olin R. Leukaemia and Hodgkin’s disease among Swedish chemistry graduates. Lancet. 1976;2(7991):916. https://doi.org/10.1016/s0140-6736(76)90589-4.
33. Olin G.R. The hazards of chemical laboratory environment: a study of the mortality in two cohorts of Swedish chemists // Am. Ind. Hyg. Assoc. J. 1978. V.39. No.7. P. 557–562. https://doi.org/10.1080/0002889778507808. Olin G.R. The hazards of chemical laboratory environment: a study of the mortality in two cohorts of Swedish chemists. Am. Ind. Hyg. Assoc. J. 1978;39(7):557–62. https://doi.org/10.1080/0002889778507808.
34. Olin G.R., Ahlbom A. The cancer mortality among Swedish chemists graduated during three decades. A comparison with the general population and with a cohort of architects // Environ. Res. 1980. V.22. No.1. P. 154–161. https://doi.org/10.1016/0013-9351(80)90127-9. Olin G.R., Ahlbom A. The cancer mortality among Swedish chemists graduated during three decades. A comparison with the general population and with a cohort of architects. Environ. Res. 1980;22(1):154–61. https://doi.org/10.1016/0013-9351(80)90127-9.
35. Olin G.R., Ahlbom A. Cancer mortality among three Swedish male academic cohorts: Chemists, architects and mining engineers/metallurgists // In: ‘Brain Tumours in the Chemical Industry’. Ed. by I.J. Selikoff, E.C. Hammond. Ann. N.Y. Acad. Sci. 1982. V.381. P.197–201. https://doi.org/10.1111/j.1749-6632.1982.tb50385.x. Olin G.R., Ahlbom A. Cancer mortality among three Swedish male academic cohorts: Chemists, architects and mining engineers/metallurgists. In: ‘Brain Tumours in the Chemical Industry’. Ed. by I.J. Selikoff, E.C. Hammond. Ann. N.Y. Acad. Sci. 1982;381: 197–201. https://doi.org/10.1111/j.1749-6632.1982.tb50385.x.
36. Searle C.E., Waterhouse J.A.H. Epidemiological study of the mortality of British chemists // Br. J. Cancer. 1978. V.38. No.1. P. 192–193 (abstract). Searle C.E., Waterhouse J.A.H. Epidemiological study of the mortality of British chemists. Br. J. Cancer. 1978;38(1):192–93 (abstract).
37. Hunter W.J., Henman B.A., Bartlett D.M., Le Geyt I.P. Mortality of professional chemists in England and Wales, 1965–1989 // Am. J. Ind. Med. 1993. V.23. No.4. P. 615–627. https://doi.org/10.1002/ajim.4700230409. Hunter W.J., Henman B.A., Bartlett D.M., Le Geyt I.P. Mortality of professional chemists in England and Wales, 1965–1989. Am. J. Ind. Med. 1993;23(4):615–27. https://doi.org/10.1002/ajim.4700230409.
38. t’Mannetje A., McLean D., Cheng S., Boffetta P., Colin D., Pearce N. Mortality in New Zealand workers exposed to phenoxy herbicides and dioxins // Occup. Environ. Med. 2005. V.62. No.1. P. 34–40. https://doi.org/10.1136/oem.2004.015776. t’Mannetje A., McLean D., Cheng S., Boffetta P., Colin D., Pearce N. Mortality in New Zealand workers exposed to phenoxy herbicides and dioxins. Occup. Environ. Med. 2005;62(1):34–40. https://doi.org/10.1136/oem.2004.015776.
39. Brown T.P., Paulson J., Pannett B., Coupland C., Coggon D., Chilvers C.E., Sasco A.J. Mortality pattern among biological research laboratory workers // Br. J. Cancer. 1996. V.73. No.9. P. 1152–1155. https://doi.org/10.1038/bjc.1996.221. Brown T.P., Paulson J., Pannett B., Coupland C., Coggon D., Chilvers C.E., Sasco A.J. Mortality pattern among biological research laboratory workers. Br. J. Cancer. 1996;73(9):1152–5. https://doi.org/10.1038/bjc.1996.221.
40. Cordier S. Risk of cancer among laboratory workers (letter) // Lancet. 1990. V.335. No.8697. P. 1097. https://doi.org/10.1016/0140-6736(90)92670-d. Cordier S. Risk of cancer among laboratory workers (letter). Lancet. 1990;335(8697):1097. https://doi.org/10.1016/0140-6736(90)92670-d.
41. Cordier S., Mousel M.-L., Le Goaster C., Gachelin G., Le Moual N., Mandereau L. et al. Cancer risk among workers in biomedical research // Scand. J. Work Environ. Health. 1995. V.21. No.6. P. 450–459. https://doi.org/10.5271/sjweh.61. Cordier S., Mousel M.-L., Le Goaster C., Gachelin G., Le Moual N., Mandereau L. et al. Cancer risk among workers in biomedical research. Scand. J. Work Environ. Health. 1995;21(6):450–9. https://doi.org/10.5271/sjweh.61.
42. Guseva Canu I., Rogel A., Samson E., Benhamou S., Laplanche A., Tirmarche M. Cancer mortality risk among biology research workers in France: first results of two retrospective cohorts studies // Int. Arch. Occup. Environ. Health. 2008. V.81. No.6. P. 777–785. https://doi.org/10.1007/s00420-007-0260-6. Guseva Canu I., Rogel A., Samson E., Benhamou S., Laplanche A., Tirmarche M. Cancer mortality risk among biology research workers in France: first results of two retrospective cohorts studies. Int. Arch. Occup. Environ. Health. 2008;81(6):777–85. https://doi.org/10.1007/s00420-007-0260-6.
43. Wennborg H., Yuen J., Axelsson G., Ahlbom A., Gustavsson P., Sasco A.J. Mortality and cancer incidence in biomedical laboratory personnel in Sweden // Am. J. Ind. Med. 1999. V.35. No.4. P. 382–389. https://doi.org/10.1002/(sici)1097-0274(199904)35:4<382::aid-ajim9>3.0.co;2-f. Wennborg H., Yuen J., Axelsson G., Ahlbom A., Gustavsson P., Sasco A.J. Mortality and cancer incidence in biomedical laboratory personnel in Sweden. Am. J. Ind. Med. 1999;35(4):382–9. https://doi.org/10.1002/(sici)1097-0274(199904)35:4<382::aid-ajim9>3.0.co;2-f.
44. Gustavsson P., Reuterwall C., Sadigh J., Soderholm M. Mortality and cancer incidence among laboratory technicians in medical research and routine laboratories (Sweden) // Cancer Causes Control. 1999. V.10. No.1. P. 59–64. https://doi.org/10.1023/a:1008892830922. Gustavsson P., Reuterwall C., Sadigh J., Soderholm M. Mortality and cancer incidence among laboratory technicians in medical research and routine laboratories (Sweden). Cancer Causes Control. 1999;10(1):59–64. https://doi.org/10.1023/a:1008892830922.
45. Van Barneveld T.A., Sasco A.J., van Leeuwen F.E. A cohort study of cancer mortality among Biology Research Laboratory workers in The Netherlands // Cancer Causes Control. 2004. V.15. No.1. P. 55–66. https://doi.org/10.1023/B:CACO.0000016607.70457.47. Van Barneveld T.A., Sasco A.J., van Leeuwen F.E. A cohort study of cancer mortality among Biology Research Laboratory workers in The Netherlands. Cancer Causes Control. 2004;15(1):55–66. https://doi.org/10.1023/B:CACO.0000016607.70457.47.
46. Harrington J.M., Shannon H.S. Mortality study of pathologists and medical laboratory technicians // Br Med J. 1975. V.4. No.5992. P. 329–332. https://doi.org/10.1136/bmj.4.5992.329. Harrington JM, Shannon HS. Mortality study of pathologists and medical laboratory technicians. Br Med J. 1975 Nov 8;4(5992):329–32. https://doi.org/10.1136/bmj.4.5992.329.
47. Belli S., Comba P., De Santis M., Grignoli M., Sasco A.J. Cancer mortality patterns among laboratory workers // Lancet. 1990. V.335. No.8705. P. 1597–1598. https://doi.org/10.1016/0140-6736(90)91432-a. Belli S., Comba P., De Santis M., Grignoli M., Sasco A.J. Cancer mortality patterns among laboratory workers. Lancet. 1990;335(8705):1597–8. https://doi.org/10.1016/0140-6736(90)91432-a.
48. Belli S., Comba P., De Santis M., Grignoli M., Sasco A.J. Mortality study of workers employed by the Italian National Institute of Health, 1960–1989 // Scand. J. Work Environ. Health. 1992. V.18. No.1. P. 64–67. https://doi.org/10.5271/sjweh.1607. Belli S., Comba P., De Santis M., Grignoli M., Sasco A.J. Mortality study of workers employed by the Italian National Institute of Health, 1960–1989. Scand. J. Work Environ. Health. 1992;18(1):64–7. https://doi.org/10.5271/sjweh.1607.
49. Dosemeci M., Alavanja M., Vetter R., Eaton B., Blair A. Mortality among laboratory workers employed at the U.S. Department of Agriculture // Epidemiology. 1992. V.3. No.3. P. 258–262. https://doi.org/10.1097/00001648-199205000-00012. Dosemeci M., Alavanja M., Vetter R., Eaton B., Blair A. Mortality among laboratory workers employed at the U.S. Department of Agriculture. Epidemiology. 1992;3(3):258–62. https://doi.org/10.1097/00001648-199205000-00012.
50. Daly L., Herity B., Bourke G.J. An investigation of brain tumours and other malignancies in an agricultural research institute // Occup Environ Med. 1994. V.51. No.5. P. 295–298. https://doi.org/10.1136/oem.51.5.295. Daly L., Herity B., Bourke G.J. An investigation of brain tumours and other malignancies in an agricultural research institute. Occup Environ Med. 1994;51(5):295–8. https://doi.org/10.1136/oem.51.5.295.
51. Sasco A.J. Cancer risk in laboratory workers // Lancet. 1992a. V.339. No.8794. P. 684. https://doi.org/10.1016/0140-6736(92)90849-x. Sasco A.J. Cancer risk in laboratory workers. Lancet. 1992a;339(8794):684. https://doi.org/10.1016/0140-6736(92)90849-x.
52. Sasco A.J. International study of cancer risk in biology research laboratory workers in Europe. In: ‘Update of the protocol for the retrospective cohort study’ // International Agency for Research on Cancer, Lyon. 1992b. 34 p. Sasco A.J. International study of cancer risk in biology research laboratory workers in Europe. In: ‘Update of the protocol for the retrospective cohort study’. International Agency for Research on Cancer, Lyon. 1992b. 34 p.
53. Rachet B., Partanen T., Kauppinen T., Sasco A.J. Cancer risk in laboratory workers: an emphasis on biological research // Am. J. Ind. Med. 2000. V.38. No.6. P. 651–665. https://doi.org/10.1002/1097-0274(200012)38:6<651::aid-ajim6>3.0.co;2-j. Rachet B., Partanen T., Kauppinen T., Sasco A.J. Cancer risk in laboratory workers: an emphasis on biological research. Am. J. Ind. Med. 2000;38(6):651–65. https://doi.org/10.1002/1097-0274(200012)38:6<651::aid-ajim6>3.0.co;2-j.
54. Sasco A.J., Rachet B. Biology research laboratory workers. In: ‘Biennial Report, 1998–1999’ // World Health Organization; International Agency for Research on Cancer. IARC, Lyon, France, 2000. P. 28. Sasco A.J., Rachet B. Biology research laboratory workers. In: ‘Biennial Report, 1998–1999’. World Health Organization; International Agency for Research on Cancer. IARC, Lyon, France, 2000:28.
55. Miettinen O.S. Standardization of risk ratios // Am. J. Epidemiol. 1972. V.96. No.6. P. 383–388. https://doi.org/10.1093/oxfordjournals.aje.a121470. Miettinen O.S. Standardization of risk ratios. Am. J. Epidemiol. 1972;96(6):383–8. https://doi.org/10.1093/oxfordjournals.aje.a121470.
56. A dictionary of epidemiology. Ed. by M. Porta. 6th Edition. New York: Oxford University Press, 2014. 344 p. A dictionary of epidemiology. Ed. by M. Porta. 6th Edition. New York: Oxford University Press, 2014. 344 p.
57. Stewart W., Hunting K. Mortality odds ratio, proportionate mortality ratio, and healthy worker effect // Am. J. Ind. Med. 1988. V.14. No.3. P. 345–353. https://doi.org/10.1002/ajim.4700140312. 44. Stewart W., Hunting K. Mortality odds ratio, proportionate mortality ratio, and healthy worker effect. Am. J. Ind. Med. 1988;14(3):345–53. https://doi.org/10.1002/ajim.4700140312.
58. Vecchio D., Sasco A.J., Cann C.I. Occupational risk in health care and research // Am. J. Ind. Med. 2003. V.43. No.4. P. 369–397. https://doi.org/10.1002/ajim.10191. Vecchio D., Sasco A.J., Cann C.I. Occupational risk in health care and research. Am. J. Ind. Med. 2003;43(4):369–97. https://doi.org/10.1002/ajim.10191.
59. Соленова Л.Г. Эпидемиологический мониторинг онкологического риска у работников онкологического центра // Успехи молекулярной онкологии. 2019. Т.6. №3. С. 63–70. https://doi.org/10.17650/2313-805X-2019-6-3-63-70. Solenova L. G. Epidemiological monitoring of cancer risk in cancer center workers. Uspekhi molekulyarnoy onkologii = Advances in Molecular Oncology. 2019;6(3):63–70. https://doi.org/10.17650/2313-805X-2019-6-3-63-70.
60. Moher D., Liberati A., Tetzlaff J., Altman D.G. ( PRISMA Group). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement // PLoS Med. 2009. V.6. No.7. Article e1000097. 6 p. https://doi.org/10.1371/journal.pmed.1000097. Moher D., Liberati A., Tetzlaff J., Altman D.G. ( PRISMA Group). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):Article e1000097. 6 p. https://doi.org/10.1371/journal.pmed.1000097.
61. Aschengrau A., Seage G.R., III. Epidemiology in Public Health. 3rd edition. Burlington: Jones & Bartlett Learning, LLC, 2014. 596 p. Aschengrau A., Seage G.R., III. Epidemiology in Public Health. 3rd edition. Burlington: Jones & Bartlett Learning, LLC, 2014. 596 p.
62. Takada S., Okamoto S., Yamada C., Ukai H., Samoto H., Ohashi F., Ikeda M. Chemical exposures in research laboratories in a university // Ind. Health. 2008. V.46. No.2. P. 166–173. https://doi.org/10.2486/indhealth.46.166. Takada S., Okamoto S., Yamada C., Ukai H., Samoto H., Ohashi F., Ikeda M. Chemical exposures in research laboratories in a university. Ind. Health. 2008;46(2):166–73. https://doi.org/10.2486/indhealth.46.166.
63. Ushakov I.B., Voronkov Y.I., Bukhtiyarov I.V. Tikhonova G.I., Gorchakova T.Yu., Bryleva M.S. A cohort mortality study among Soviet and Russian cosmonauts, 1961–2014 // Aerosp. Med. Hum. Perform. 2017. V.88. No.12. P. 1060–1065. https://doi.org/10.3357/AMHP.4701.2017. Ushakov I.B., Voronkov Y.I., Bukhtiyarov I.V. Tikhonova G.I., Gorchakova T.Yu., Bryleva M.S. A cohort mortality study among Soviet and Russian cosmonauts, 1961–2014. Aerosp. Med. Hum. Perform. 2017;88(12):1060–5. https://doi.org/10.3357/AMHP.4701.2017.
64. Reynolds R.J., Day S.M. Mortality of US astronauts: comparisons with professional athletes // Occup. Environ. Med. 2019. V.76. No.2. P. 114–117. https://doi.org/10.1136/oemed-2018-105304. Reynolds R.J., Day S.M. Mortality of US astronauts: comparisons with professional athletes. Occup. Environ. Med. 2019;76(2):114–7. https://doi.org/10.1136/oemed-2018-105304.
65. Gajewski A.K., Poznanska A. Mortality of top athletes, actors and clergy in Poland: 1924-2000 follow-up study of the long term effect of physical activity // Eur. J. Epidemiol. 2008. V.23. No.5. P. 335–340. https://doi.org/10.1007/s10654-008-9237-3. Gajewski A.K., Poznanska A. Mortality of top athletes, actors and clergy in Poland: 1924-2000 follow-up study of the long term effect of physical activity. Eur. J. Epidemiol. 2008;23(5):335–40. https://doi.org/10.1007/s10654-008-9237-3.
66. Hammer G.P., Auvinen A., De Stavola B.L., Grajewski B., Gundestrup M., Haldorsen T. et al. Mortality from cancer and other causes in commercial airline crews: a joint analysis of cohorts from 10 countries // Occup. Environ. Med. 2014. V.71. No.5. P. 313–322. https://doi.org/10.1136/oemed-2013-101395. Hammer G.P., Auvinen A., De Stavola B.L., Grajewski B., Gundestrup M., Haldorsen T. et al. Mortality from cancer and other causes in commercial airline crews: a joint analysis of cohorts from 10 countries. Occup. Environ. Med. 2014;71(5):313–22. https://doi.org/10.1136/oemed-2013-101395.
67. Qu S.G., Gao J., Tang B., Yu B., Shen Y.P., Tu Y. Low-dose ionizing radiation increases the mortality risk of solid cancers in nuclear industry workers: A meta-analysis // Mol. Clin. Oncol. 2018. V.8. No.5. P. 703–711. https://doi.org/10.3892/mco.2018.1590. Qu S.G., Gao J., Tang B., Yu B., Shen Y.P., Tu Y. Low-dose ionizing radiation increases the mortality risk of solid cancers in nuclear industry workers: A meta-analysis // Mol. Clin. Oncol. 2018;8(5):703–11. https://doi.org/10.3892/mco.2018.1590.
68. McLaughlin R., Nielsen L., Waller M. An evaluation of the effect of military service on mortality: quantifying the healthy soldier effect // Ann. Epidemiol. 2008. V.18. No.12. P. 928–936. https://doi.org/10.1016/j.annepidem.2008.09.002. McLaughlin R., Nielsen L., Waller M. An evaluation of the effect of military service on mortality: quantifying the healthy soldier effect. Ann. Epidemiol. 2008;18(12):928–36. https://doi.org/10.1016/j.annepidem.2008.09.002.
69. Kroenke C., Kawachi I. Socioeconomic disparities in cancer incidence and mortality // In: ‘Schottenfeld and Fraumeni Cancer Epidemiology and Prevention’. 4th Edition. Ed. by M.J. Thun, M.S. Linet, J.R. Cerhan, C. Haiman, D. Schottenfeld. – New York: Oxford University Press, Sheridan Books, Inc., USA, 2018. P. 141–168. Kroenke C., Kawachi I. Socioeconomic disparities in cancer incidence and mortality // In: ‘Schottenfeld and Fraumeni Cancer Epidemiology and Prevention’. 4th Edition. Ed. by M.J. Thun, M.S. Linet, J.R. Cerhan, C. Haiman, D. Schottenfeld. – New York: Oxford University Press, Sheridan Books, Inc., USA, 2018:141–68.
70. Steenland K., Pinkerton L.E. Mortality patterns following downsizing at Pan American World Airways // Am. J. Epidemiol. 2008. V.167. No.1. P. 1–6. https://doi.org/10.1093/aje/kwm328. Steenland K., Pinkerton L.E. Mortality patterns following downsizing at Pan American World Airways. Am. J. Epidemiol. 2008;167(1):1–6. https://doi.org/10.1093/aje/kwm328.
71. Ичас М. О природе живого: механизмы и смысл. Пер. с англ. – М.: Мир, 1994. – 496 с. Ycas M. The Nature of Life: Mechanisms and Meaning. – Moscow: Mir, 1994. – 496 p. (In Russ.)
72. Boice J.D., Jr. Ionizing Radiation // In: ‘Schottenfeld and Fraumeni Cancer Epidemiology and Prevention’. 3th edition. Ed. by D. Schottenfeld, J.F. Fraumeni. – New York: Oxford University Press. 2006. P. 259–293. Boice J.D., Jr. Ionizing Radiation. In: ‘Schottenfeld and Fraumeni Cancer Epidemiology and Prevention’. 3th edition. Ed. by D. Schottenfeld, J.F. Fraumeni. – New York: Oxford University Press. 2006:259–93.
73. Котеров А.Н. От очень малых до очень больших доз радиации: новые данные по установлению диапазонов и их экспериментально-эпидемиологические обоснования // Мед. радиология и радиац. безопасность. 2013. Т.58. №2. С. 5–21. Koterov A.N. From very low to very large doses of radiation: new data on ranges definitions and its experimental and epidemiological basing. Meditsinskaya radiologiya i radiatsionnaya bezopasnost’ = Medical Radiology and Radiation Safety. 2013;58(2):5–21. (In Russ., Engl. abst.)
PDF (RUS) Full-text article (in Russian)
Conflict of interest. The authors declare no conflict of interest.
Financing. The study had no sponsorship.
Contribution. Article was prepared with equal participation of the authors.
Article received: 20.02.2025. Accepted for publication: 25.03.2025.