Doll and Peto's quantitative estimates of cancer risks: holding generally true for 35 years.

In late 1980, Sir Richard Doll and his colleague Richard Peto (now also Sir Richard) at Oxford University submitted a landmark review of factors known at the time to affect cancer risk (1). The report had been commissioned by the US Congress Office of Technology Assessment to help determine the percentage of cancer because of avoidable causes, and the 117-page document was published in the Journal of the National Cancer Institute in June 1981. The article became a reference standard when estimates were made of the relative roles of lifestyle vs environmental vs host factors as causes of cancer in the US population. Herein we review the estimates Doll and Peto provided, what new knowledge has accumulated since, and how the proportions of cancer estimated to be attributable to tobacco, diet, occupation, and infection compare now vs then. The Doll-Peto article is one of the few, if only, reports in the Journal’s 75 years that was generated by Congressional request. At the time there was considerable controversy over the burden of cancer associated with exposures to various chemicals in the workplace, air and water, in part because of a report by 10 National Institutes of Health researchers submitted to the Occupational Safety and Health Administration (hereafter referred to as the OSHA report) claiming that a minimum of 20% of all cancer deaths in the United States were because of occupational exposures, with up to 18% of all cancers arising because of asbestos exposure alone (2). Questions for one of us (WJB) following a seminar on geographic patterns of cancer with Doll’s group in Oxford in the summer of 1979 were not so much on the specific topic presented as on this OSHA report, its authors, and its evidence basis. Doll was the world’s leading epidemiologist of the day, having designed and led some of the original epidemiologic research studies documenting that smoking was the dominant cause of lung cancer and that groups heavily occupationally exposed to asbestos also were at elevated risk of this cancer, but the OSHA report projections seemed too high to the Oxford group. The issue of attribution of risks remained topical, and thus Doll and Peto were invited by congressional representatives to prepare a comprehensive report on the known causes of cancer and the amount of cancer in the United States because of tobacco, occupation, and other known etiologic factors. Below we comment on the specific cancer risk factors described in the Doll-Peto article and the evidence regarding the causes of cancer incidence and mortality then and now. We focus on four major exposures leading to cancer covered by Doll and Peto, namely tobacco (the most important), diet and nutrition (the most uncertain), occupation (at the time the most controversial), and infection (possibly the most looming [3]). We also comment on the role of chance, or bad luck, in the attribution of cancer causes, including the recent report that about two-thirds of a large group of cancers may be because of uncontrollable and naturally occurring random DNA replication errors during cell division (4).