Abstract
Workers in the petroleum industry are potentially exposed to a variety of petrochemicals, including benzene or benzene-containing liquids. Although a large number of studies of petroleum workers have been conducted to examine leukemia and other cancer risks, few existing studies have investigated cell-type-specific leukemias. One of the major reasons for the lack of cell-type-specific analysis was the small number of deaths by cell type in individual studies. In the present investigation, all cohort studies of petroleum workers in the United States and the United Kingdom were combined into a single database for cell-type-specific leukemia analysis. The majority of these workers were petroleum refinery employees, but production, pipeline, and distribution workers in the petroleum industry were also included. The combined cohort consisted of more than 208,000 petroleum workers, who contributed more than 4.6 million person-years of observation. Based on a meta-analysis of the combined data, cell-type-specific leukemia risks were expressed in terms of standardized mortality ratios (meta-SMRs). The meta-SMR for acute myeloid leukemia was 0.96. The lack of an increase of acute myeloid leukemia was attributed to the low levels of benzene exposure in the petroleum industry, particularly in comparison to benzene exposure levels in some previous studies of workers in other industries, who had been found to experience an increased risk of acute myeloid leukemia. Similarly, no increase in chronic myeloid, acute lymphocytic, or chronic lymphocytic leukemias was found in petroleum workers (meta-SMRs of 0.89, 1.16, and 0.84, respectively). Stratified meta-analyses restricted to refinery studies or to studies with at least 15 years of follow-up yielded similar results. The findings of the present investigation are consistent with those from several recent case-control studies of cell-type-specific leukemia. Patterns and levels of benzene exposure in the petroleum industry are reviewed. The results of the present epidemiologic investigation are discussed in conjunction with recent advances in leukemogenesis from other scientific disciplines.
Full text
PDF











Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Aksoy M. Benzene as a leukemogenic and carcinogenic agent. Am J Ind Med. 1985;8(1):9–20. doi: 10.1002/ajim.4700080103. [DOI] [PubMed] [Google Scholar]
- Aksoy M., Dinçol K., Erdem S., Dinçol G. Acute leukemia due to chronic exposure to benzene. Am J Med. 1972 Feb;52(2):160–166. doi: 10.1016/0002-9343(72)90065-4. [DOI] [PubMed] [Google Scholar]
- Aksoy M., Erdem S., Dinçol G. Types of leukemia in chronic benzene poisoning. A study in thirty-four patients. Acta Haematol. 1976;55(2):65–72. doi: 10.1159/000207996. [DOI] [PubMed] [Google Scholar]
- Austin H., Cole P., McCraw D. S. A case-control study of leukemia at an oil refinery. J Occup Med. 1986 Nov;28(11):1169–1173. [PubMed] [Google Scholar]
- Brandt L. Environmental factors and leukaemia. Med Oncol Tumor Pharmacother. 1985;2(1):7–10. doi: 10.1007/BF02934774. [DOI] [PubMed] [Google Scholar]
- Brandt L., Nilsson P. G., Mitelman F. Occupational exposure to petroleum products in men with acute non-lymphocytic leukaemia. Br Med J. 1978 Mar 4;1(6112):553–553. doi: 10.1136/bmj.1.6112.553. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Christie D., Robinson K., Gordon I., Bisby J. A prospective study in the Australian petroleum industry. II. Incidence of cancer. Br J Ind Med. 1991 Aug;48(8):511–514. doi: 10.1136/oem.48.8.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dagg T. G., Satin K. P., Bailey W. J., Wong O., Harmon L. L., Swencicki R. E. An updated cause specific mortality study of petroleum refinery workers. Br J Ind Med. 1992 Mar;49(3):203–212. doi: 10.1136/oem.49.3.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Divine B. J., Barron V., Kaplan S. D. Texaco mortality study. I. Mortality among refinery, petrochemical, and research workers. J Occup Med. 1985 Jun;27(6):445–447. [PubMed] [Google Scholar]
- 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):371–381. doi: 10.1002/ajim.4700100405. [DOI] [PubMed] [Google Scholar]
- Divine B. J., Barron V. Texaco mortality study: III. A cohort study of producing and pipeline workers. Am J Ind Med. 1987;11(2):189–202. doi: 10.1002/ajim.4700110208. [DOI] [PubMed] [Google Scholar]
- Friedman G. D. Cigarette smoking, leukemia, and multiple myeloma. Ann Epidemiol. 1993 Jul;3(4):425–428. doi: 10.1016/1047-2797(93)90071-b. [DOI] [PubMed] [Google Scholar]
- Girard R., Revol L. La fréquence d'une exposition benzénique au cours des hémpathies graves. Nouv Rev Fr Hematol. 1970 Jul-Aug;10(4):477–483. [PubMed] [Google Scholar]
- Goguel A., Cavigneaux A., Bernard J. Les leucémies benzéniques. Bull Inst Natl Sante Rech Med. 1967 May-Jun;22(3):421–441. [PubMed] [Google Scholar]
- Hanis N. M., Holmes T. M., Shallenberger G., Jones K. E. Epidemiologic study of refinery and chemical plant workers. J Occup Med. 1982 Mar;24(3):203–212. doi: 10.1097/00043764-198203000-00012. [DOI] [PubMed] [Google Scholar]
- Hanis N. M., Shallenberger L. G., Donaleski D. L., Sales E. A. A retrospective mortality study of workers in three major U.S. refineries and chemical plants. Part 1: Comparisons with U.S. population. J Occup Med. 1985 Apr;27(4):283–292. [PubMed] [Google Scholar]
- Hanis N. M., Shallenberger L. G., Donaleski D. L., Sales E. A. A retrospective mortality study of workers in three major U.S. refineries and chemical plants. Part II: Internal comparisons by geographic site, occupation, and smoking history. J Occup Med. 1985 May;27(5):361–369. doi: 10.1097/00043764-198505000-00016. [DOI] [PubMed] [Google Scholar]
- Honda Y., Delzell E., Cole P. An updated study of mortality among workers at a petroleum manufacturing plant. J Occup Environ Med. 1995 Feb;37(2):194–200. doi: 10.1097/00043764-199502000-00020. [DOI] [PubMed] [Google Scholar]
- Infante P. F., Rinsky R. A., Wagoner J. K., Young R. J. Leukaemia in benzene workers. Lancet. 1977 Jul 9;2(8028):76–78. doi: 10.1016/s0140-6736(77)90074-5. [DOI] [PubMed] [Google Scholar]
- Jakobsson R., Ahlbom A., Bellander T., Lundberg I. Acute myeloid leukemia among petrol station attendants. Arch Environ Health. 1993 Jul-Aug;48(4):255–259. doi: 10.1080/00039896.1993.9940369. [DOI] [PubMed] [Google Scholar]
- Linet M. S., Stewart W. F., Van Natta M. L., McCaffrey L. D., Szklo M. Comparison of methods for determining occupational exposure in a case-control interview study of chronic lymphocytic leukemia. J Occup Med. 1987 Feb;29(2):136–141. [PubMed] [Google Scholar]
- Loomis D. P., Savitz D. A. Occupation and leukemia mortality among men in 16 states: 1985-1987. Am J Ind Med. 1991;19(4):509–521. doi: 10.1002/ajim.4700190408. [DOI] [PubMed] [Google Scholar]
- Malone K. E., Koepsell T. D., Daling J. R., Weiss N. S., Morris P. D., Taylor J. W., Swanson G. M., Lyon J. L. Chronic lymphocytic leukemia in relation to chemical exposures. Am J Epidemiol. 1989 Dec;130(6):1152–1158. doi: 10.1093/oxfordjournals.aje.a115442. [DOI] [PubMed] [Google Scholar]
- Marsh G. M., Enterline P. E., McCraw D. Mortality patterns among petroleum refinery and chemical plant workers. Am J Ind Med. 1991;19(1):29–42. doi: 10.1002/ajim.4700190105. [DOI] [PubMed] [Google Scholar]
- Matanoski G. M., Elliott E. A. Bladder cancer epidemiology. Epidemiol Rev. 1981;3:203–229. doi: 10.1093/oxfordjournals.epirev.a036234. [DOI] [PubMed] [Google Scholar]
- McCraw D. S., Joyner R. E., Cole P. Excess leukemia in a refinery population. J Occup Med. 1985 Mar;27(3):220–222. [PubMed] [Google Scholar]
- McKinney P. A., Roberts B. E., O'Brien C., Bird C. C., Richards I. D., Alexander F., Cartwright R. A. Chronic myeloid leukaemia in Yorkshire: a case control study. Acta Haematol. 1990;83(1):35–38. doi: 10.1159/000205160. [DOI] [PubMed] [Google Scholar]
- Morgan R. W., Foliart D. E., Wong O. Asbestos and gastrointestinal cancer. A review of the literature. West J Med. 1985 Jul;143(1):60–65. [PMC free article] [PubMed] [Google Scholar]
- Morgan R. W., Wong O. A review of epidemiological studies on artificial sweeteners and bladder cancer. Food Chem Toxicol. 1985 Apr-May;23(4-5):529–533. doi: 10.1016/0278-6915(85)90147-4. [DOI] [PubMed] [Google Scholar]
- Nelson N., Levine R. J., Albert R. E., Blair A. E., Griesemer R. A., Landrigan P. J., Stayner L. T., Swenberg J. A. Contribution of formaldehyde to respiratory cancer. Environ Health Perspect. 1986 Dec;70:23–35. doi: 10.1289/ehp.867023. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Olsen J. H., Jensen O. M. Occupation and risk of cancer in Denmark. An analysis of 93,810 cancer cases, 1970-1979. Scand J Work Environ Health. 1987;13 (Suppl 1):1–91. [PubMed] [Google Scholar]
- Paustenbach D. J., Price P. S., Ollison W., Blank C., Jernigan J. D., Bass R. D., Peterson H. D. Reevaluation of benzene exposure for the Pliofilm (rubberworker) cohort (1936-1976). J Toxicol Environ Health. 1992 Jul;36(3):177–231. doi: 10.1080/15287399209531633. [DOI] [PubMed] [Google Scholar]
- Raabe G. K. Review of the carcinogenic potential of gasoline. Environ Health Perspect. 1993 Dec;101 (Suppl 6):35–38. doi: 10.1289/ehp.93101s635. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reeve G. R., Thomas T. L., Kelly V. F., Waxweiler R. J., Itaya S. A proportionate mortality study of an Oil, Chemical and Atomic Workers Local in Texas City, Texas. Ann N Y Acad Sci. 1982;381:54–61. doi: 10.1111/j.1749-6632.1982.tb50367.x. [DOI] [PubMed] [Google Scholar]
- Rinsky R. A., Smith A. B., Hornung R., Filloon T. G., Young R. J., Okun A. H., Landrigan P. J. Benzene and leukemia. An epidemiologic risk assessment. N Engl J Med. 1987 Apr 23;316(17):1044–1050. doi: 10.1056/NEJM198704233161702. [DOI] [PubMed] [Google Scholar]
- Rinsky R. A., Young R. J., Smith A. B. Leukemia in benzene workers. Am J Ind Med. 1981;2(3):217–245. doi: 10.1002/ajim.4700020305. [DOI] [PubMed] [Google Scholar]
- Runion H. E. Occupational exposures to potentially hazardous agents in the petroleum industry. Occup Med. 1988 Jul-Sep;3(3):431–444. [PubMed] [Google Scholar]
- Rushton L. A 39-year follow-up of the U.K. oil refinery and distribution center studies: results for kidney cancer and leukemia. Environ Health Perspect. 1993 Dec;101 (Suppl 6):77–84. doi: 10.1289/ehp.93101s677. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rushton L., Alderson M. R. An epidemiological survey of eight oil refineries in Britain. Br J Ind Med. 1981 Aug;38(3):225–234. doi: 10.1136/oem.38.3.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rushton L., Alderson M. R. Epidemiological survey of oil distribution centres in Britain. Br J Ind Med. 1983 Aug;40(3):330–339. doi: 10.1136/oem.40.3.330. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rushton L. Further follow up of mortality in a United Kingdom oil distribution centre cohort. Br J Ind Med. 1993 Jun;50(6):561–569. doi: 10.1136/oem.50.6.561. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rushton L. Further follow up of mortality in a United Kingdom oil refinery cohort. Br J Ind Med. 1993 Jun;50(6):549–560. doi: 10.1136/oem.50.6.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schnatter A. R., Thériault G., Katz A. M., Thompson F. S., Donaleski D., Murray N. A retrospective mortality study within operating segments of a petroleum company. Am J Ind Med. 1992;22(2):209–229. doi: 10.1002/ajim.4700220207. [DOI] [PubMed] [Google Scholar]
- Selvin S., Levin L. I., Merrill D. W., Winkelstein W., Jr Selected epidemiologic observations of cell-specific leukemia mortality in the United States, 1969-1977. Am J Epidemiol. 1983 Feb;117(2):140–152. doi: 10.1093/oxfordjournals.aje.a113524. [DOI] [PubMed] [Google Scholar]
- Severson R. K., Davis S., Heuser L., Daling J. R., Thomas D. B. Cigarette smoking and acute nonlymphocytic leukemia. Am J Epidemiol. 1990 Sep;132(3):418–422. doi: 10.1093/oxfordjournals.aje.a115676. [DOI] [PubMed] [Google Scholar]
- Shallenberger L. G., Acquavella J. F., Donaleski D. An updated mortality study of workers in three major United States refineries and chemical plants. Br J Ind Med. 1992 May;49(5):345–354. doi: 10.1136/oem.49.5.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith T. J., Hammond S. K., Wong O. Health effects of gasoline exposure. I. Exposure assessment for U.S. distribution workers. Environ Health Perspect. 1993 Dec;101 (Suppl 6):13–21. doi: 10.1289/ehp.93101s613. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Snyder R., Kalf G. F. A perspective on benzene leukemogenesis. Crit Rev Toxicol. 1994;24(3):177–209. doi: 10.3109/10408449409021605. [DOI] [PubMed] [Google Scholar]
- Thomas T. L., Decoufle P., Moure-Eraso R. Mortality among workers employed in petroleum refining and petrochemical plants. J Occup Med. 1980 Feb;22(2):97–103. doi: 10.1097/00043764-198002000-00007. [DOI] [PubMed] [Google Scholar]
- Thomas T. L., Waxweiler R. J., Crandall M. S., White D. W., Moure-Eraso R., Fraumeni J. F., Jr Cancer mortality patterns by work category in three Texas oil refineries. Am J Ind Med. 1984;6(1):3–16. doi: 10.1002/ajim.4700060103. [DOI] [PubMed] [Google Scholar]
- Thorpe J. J. Epidemiologic survey of leukemia in persons potentially exposed to benzene. J Occup Med. 1974 Jun;16(6):375–382. [PubMed] [Google Scholar]
- Tsai S. P., Gilstrap E. L., Cowles S. R., Snyder P. J., Ross C. E. A cohort mortality study of two California refinery and petrochemical plants. J Occup Med. 1993 Apr;35(4):415–421. [PubMed] [Google Scholar]
- VIGLIANI E. C., SAITA G. BENZENE AND LEUKEMIA. N Engl J Med. 1964 Oct 22;271:872–876. doi: 10.1056/NEJM196410222711703. [DOI] [PubMed] [Google Scholar]
- Wen C. P., Tsai S. P., McClellan W. A., Gibson R. L. Long-term mortality study of oil refinery workers. I. Mortality of hourly and salaried workers. Am J Epidemiol. 1983 Oct;118(4):526–542. doi: 10.1093/oxfordjournals.aje.a113658. [DOI] [PubMed] [Google Scholar]
- Wong O. An industry wide mortality study of chemical workers occupationally exposed to benzene. I. General results. Br J Ind Med. 1987 Jun;44(6):365–381. doi: 10.1136/oem.44.6.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wong O. An industry wide mortality study of chemical workers occupationally exposed to benzene. II. Dose response analyses. Br J Ind Med. 1987 Jun;44(6):382–395. doi: 10.1136/oem.44.6.382. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wong O., Decoufle P. Methodological issues involving the standardized mortality ratio and proportionate mortality ratio in occupational studies. J Occup Med. 1982 Apr;24(4):299–304. [PubMed] [Google Scholar]
- Wong O., Harris F., Smith T. J. Health effects of gasoline exposure. II. Mortality patterns of distribution workers in the United States. Environ Health Perspect. 1993 Dec;101 (Suppl 6):63–76. doi: 10.1289/ehp.93101s663. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wong O., Morgan R. W., Bailey W. J., Swencicki R. E., Claxton K., Kheifets L. An epidemiological study of petroleum refinery employees. Br J Ind Med. 1986 Jan;43(1):6–17. doi: 10.1136/oem.43.1.6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wong O., Morgan R. W., Kheifets L., Larson S. R., Whorton M. D. Mortality among members of a heavy construction equipment operators union with potential exposure to diesel exhaust emissions. Br J Ind Med. 1985 Jul;42(7):435–448. doi: 10.1136/oem.42.7.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wong O., Raabe G. K. Critical review of cancer epidemiology in petroleum industry employees, with a quantitative meta-analysis by cancer site. Am J Ind Med. 1989;15(3):283–310. doi: 10.1002/ajim.4700150305. [DOI] [PubMed] [Google Scholar]
- Wong O., Raabe G. K. Proper interpretation of meta-analysis in occupational epidemiological studies: a response. Am J Ind Med. 1990;17(2):273–276. doi: 10.1002/ajim.4700170213. [DOI] [PubMed] [Google Scholar]
- Wong O. Risk of acute myeloid leukaemia and multiple myeloma in workers exposed to benzene. Occup Environ Med. 1995 Jun;52(6):380–384. doi: 10.1136/oem.52.6.380. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wong O., Tabershaw I. R. Comments on mortality among workers employed in petroleum refining and petrochemical plants. J Occup Med. 1980 Oct;22(10):638–640. doi: 10.1097/00043764-198010000-00001. [DOI] [PubMed] [Google Scholar]
- Wongsrichanalai C., Delzell E., Cole P. Mortality from leukemia and other diseases among workers at a petroleum refinery. J Occup Med. 1989 Feb;31(2):106–111. [PubMed] [Google Scholar]