16. The fraction of cancer attributable to lifestyle and environmental factorsin the UK in 2010
Summary and conclusions
This chapter summarises the results of the preceding sections, which estimate thefraction of cancers occurring in the UK in 2010 that can be attributed tosub-optimal, past exposures of 14 lifestyle and environmental risk factors. Foreach of 18 cancer types, we present the percentage of cases attributable to oneor all of the risk factors considered (tobacco, alcohol, four elements of diet(consumption of meat, fruit and vegetables, fibre, and salt), overweight, lackof physical exercise, occupation, infections, radiation (ionising and solar),use of hormones, and reproductive history (breast feeding)).
Exposure to less than optimum levels of the 14 factors was responsible for42.7% of cancers in the UK in 2010 (45.3% in men, 40.1% inwomen) – a total of about 134 000 cases.
Tobacco smoking is by far the most important risk factor for cancer in the UK,responsible for 60 000 cases (19.4% of all new cancer cases) in2010. The relative importance of other exposures differs by sex. In men,deficient intake of fruits and vegetables (6.1%), occupational exposures(4.9%) and alcohol consumption (4.6%) are next in importance,while in women, it is overweight and obesity (because of the effect on breastcancer) – responsible for 6.9% of cancers, followed by infectiousagents (3.7%).
Population-attributable fractions provide a valuable quantitative appraisal ofthe impact of different factors in cancer causation, and are thus helpful inprioritising cancer control strategies. However, quantifying the likely impactof preventive interventions requires rather complex scenario modelling,including specification of realistically achievable population distributions ofrisk factors, and the timescale of change, as well as the latent periods betweenexposure and outcome, and the rate of change following modification in exposurelevel.
In this study, we have estimated the fraction of cancers occurring in the UK in 2010that can be attributed to sub-optimal past exposures of 14 lifestyle andenvironmental risk factors. The optimum level of exposure or the theoretical minimumrisk exposure distribution for each of the risk factors is summarised in Table 1.
Table 2 provides a summary of the percentage of cancersat each site that can be attributed to the 14 risk factors (thepopulation-attributable fraction (PAF)). The total number of cancer cases (allsites) attributable to each risk factor was obtained by summing the numbers at theindividual sites. Cases of different cancers attributable to a single risk factorare additive because each cancer case is assigned to a single ICD category.
However, cancers are caused by multiple factors acting simultaneously, and hencecould be prevented by intervening on single or multiple risk factors; for example,some oesophageal cancer cases may be prevented by reducing smoking, alcohol or bodyweight, increasing the intake of fruits and vegetables, or by combinations of thesesteps. The percentages presented in Table 2 reflect theeffect of removing one cause of cancer independently of other causes. But becausecancers have multiple causes, the same cancers can be attributed to more than onecause, so summing the figures in the tables would overestimate the total burden ofcancer attributable to the 14 risk factors. Thus, an estimate of the burden ofcancer attributable to multiple causes should take into account the overlap betweenthe effects of different carcinogens, which means that, for a specific cancer, theattributable fraction for all risk factors combined will be less than the sum of thePAFs associated with each risk factor.
When risk factors are independent (i.e., they act on different carcinogenicpathways), their effects on relative risks (RRs) will be multiplicative. This iswell documented for some factors (for example, the joint effects of tobacco andalcohol), although for most there is a lack of detailed quantitative data on therisks resulting from combined exposure to several risk factors. The hypothesis ofthe multiplicative effect of RRs is a reasonable one, however, and allows estimationof PAFs from combined exposures. Thus, in Table 2, toobtain the last row (PAF due to all of the exposures), for each cancer, the PAF forthe first exposure (e.g., tobacco smoking) was subtracted from 100%, and thePAF for the second exposure was applied to the remainder (the percentagenot attributable to smoking). This process was performed sequentiallyfor all relevant exposures, resulting in an estimate of the PAF for all exposurescombined.
Exposure to less than optimum levels of the 14 factors was responsible for42.7% of cancers in the UK in 2010 (45.3% in men, 40.1% inwomen) – a total of about 134 000 cases.
Tobacco smoking is by far the most important risk factor for cancer in the UK,responsible for 60 000 cases (19.4% of all new cancer cases) in 2010.The relative importance of other exposures differs by sex. In men, deficient intakeof fruits and vegetables (6.1%), occupational exposures (4.9%) andalcohol consumption (4.6%) are next in importance, while in women, it isoverweight and obesity (because of the effect on breast cancer) – responsiblefor 6.9% of cancers, followed by infectious agents (3.7%).
Sources of uncertainty
Results are presented as the estimated percentages of different cancersattributable to specific causes in the UK population of 2010. There are severalsources of uncertainty around the estimates. Some of these are quantifiable(e.g., confidence intervals of RRs and exposure prevalence, alternative choiceof ‘optimal exposure'), while in other cases quantification would beeither very difficult (e.g., modelling lag time to provide a biologically-drivenestimate of cumulative exposure) or be practically impossible (e.g., using theindirect method to estimate PAFs due to smoking).
Doll and Peto (1981, 2005) provided a ‘range of acceptable estimates' foreach exposure, to reflect the difference between those for which the risk iscertain and well quantified, such as tobacco smoking, and those for which thereis considerably more controversy, such as diet. We have not attempted to do soin this section; the uncertainties concerning each exposure are, however,discussed in the relevant sections. Furthermore, as we discuss below, the PAFsshould not be used uncritically as a guide to the proportion of cancer casesthat can be prevented by interventions.
Comparison with other studies
Comprehensive estimates of the fractions of cancer cases or deaths attributableto various environmental exposures have been made for world regions (Ezzati et al, 2002; Danaeiet al, 2005), the United States (Danaei et al, 2009), France (IARC,2007) and the Nordic countries (Olsen etal, 1997). For the UK, the most widely quoted arepossibly those of Doll and Peto (2005), althoughrecently the World Cancer Research Fund/American Institute for CancerResearch published an estimate of cancers attributable to food, nutrition andphysical activity in the UK and three other countries (WCRF/AICR, 2009).
The Doll and Peto (2005) estimates relate to deathsfrom cancer, and the methodology used is that from their 1981 monograph(Doll and Peto, 1981). The estimation methodis somewhat variable for the different exposures considered. For example, theyattribute to alcohol two-thirds of deaths from alcohol-related cancers (mouth,pharynx, larynx, oesophagus) in men and one-third in women, plus ‘a smallproportion' of liver cancer deaths. For diet, the fraction is arrived atby summing ‘guestimated' fractions by which death rates of differentcancers might be reduced by practical dietary means (for example: stomach90% breast 50% cervix 20%).
The WCRF/AICR report (2009), on the otherhand, uses estimates of prevalence of exposures to various nutritional factorsin the UK, and estimates of RR associated with them, to calculate attributablefractions using the conventional formula. The attributable fractions so derivedare generally rather greater than those estimated in this set of papers (Table 3). There are several reasons for this.
First, the WCRF/AICR estimates use current estimates of exposure prevalenceapplied to numbers of cancer cases in 2002. This is unrealistic. The effects ofthe exposures considered are not instantaneous, and renouncing alcohol, say,would not reduce one's excess risk to zero immediately. Therefore, in thecurrent exercise, similar to that of IARC (2007)for France, the relevant exposures are taken to be those several years earlier.This is generally 10 years, based on the follow-up periods for which most of theRRs were calculated. However, for some exposures – for example, use ofpost-menopausal hormones – the risk is raised in current users, butdeclines rapidly once exposure ceases. As most of the exposures considered havebeen becoming more prevalent with time, the WCRF/AICR estimates are too highfor current cancer cases.
Second, the current estimates make use, whenever they are available, ofdose–response summary estimates from meta-analyses by reputableauthorities such as IARC, or WCRF itself, in its report ‘Food, NutritionPhysical Activity and the Prevention of Cancer' (WCRF/AICR, 2007). The WCRF/AICR estimates use RRestimates from a single study, generally in a different country, to estimate theeffects in the UK. This seems highly unlikely to result in a less biasedresult.
Finally, the current estimates use, whenever possible, per unit exposure riskestimates, and calculate attributable fractions among the proportions of thepopulation with exposures greater or less than an acceptable‘optimum' recommended for the UK. These are dismissed byWCRF/AICR as ‘associated with a number of limitations', andtheir estimates use RRs associated with tertiles of exposure prevalence, andestimate the effect of moving the entire UK population to the lowest tertile ofexposure, defined by the study selected for the RR estimate. The baselineexposure varies, therefore, from one cancer to another; for BMI, for example, itis <25 kg m−2 for colorectum, and<21 kg m−2 for breast cancer.
There are a few other, perhaps more minor, points that contribute to thediscrepancies: it is obviously not correct to assume all breast cancer ispost-menopausal – it is only 80% of the total in UK, so that PAFsfor breast cancer related to overweight/obesity are overestimated. The sameapplies to PAFs for body weight and oesophagus cancer, where only the risk foradenocarcinomas is increased, and these constitute some 55% of theoesophageal cancers in the UK.
Figure 1 summarises the estimates of the numbers (andpercentages) of incident cancer cases in the UK in 2010 that are attributable tothe 14 lifestyle and environmental exposures considered. For the most part theseexposures are avoidable (ionising radiation is the exception), especially as formany (the dietary variables, physical exercise, overweight) the‘optimum' exposure represents a relatively modest recommendedtarget. ‘Avoidability' is in terms of the proportion of cancercases that might be prevented. If the focus had been on avoidabledeaths, then other interventions – especially throughachieving earlier diagnosis (Richards, 2009) orgeneralising state-of-the-art treatment (Scottish ExecutiveHealth Department, 2001; National AuditOffice, 2004) – would contribute to the total.
The four most important lifestyle exposures in Table2 and Figure 1, tobacco smoking,dietary factors, alcohol drinking and bodyweight, account for 34% of thecancers occuring in 2010 – almost four-fifths of the total from all 14exposures.
It is clear that tobacco smoking remains by far the most important avoidablecause of cancer in the UK. Reducing the prevalence of smoking has been aconsistent public health objective for almost 50 years since the publication ofthe first report on smoking and health by the Royal College of Physicians(RCP, 1962). The prevalence of cigarettesmoking fell substantially in the 1970s and the early 1980s, from 45% in1974 to 35% in 1982, but the rate of decline then slowed, with prevalencefalling by only about one percentage point every 2 years until 1994, after whichit levelled out at about 27% before resuming a slow decline in the 2000s(Robinson and Bugler, 2010). The differencein prevalence between men and women has decreased considerably since the 1970s,and by 2008 the difference between men and women was not statisticallysignificant, with 22% of men and 21% of women being currentcigarette smokers. The overall reported number of cigarettes smoked per male andfemale smoker has changed little since the early 1980s. Changes insmoking-related cancer incidence lag several years behind changes in smokingprevalence, so that the current decreases in smoking-related cancer incidenceand mortality will slow and eventual stop unless further progress can beachieved in reducing exposure to carcinogens in tobacco smoke.
Although it is currently not possible to pinpoint exactly what constituents ofdiet are protective against cancer, there is a consensus that diet is animportant component of cancer risk. In the current exercise, we examine thelikely impact of four components of diet for which the evidence appears to bemost persuasive: fruit and vegetables and fibre (protective) and meat and salt(carcinogenic). In combination, deviation from the recommended intake levels isresponsible for 9.2% of cancers in 2010 (the individual contributions are4.7% from deficient fruit and vegetables, 2.7% from consumption ofred and processed meat, 1.5% from a deficit of fibre and 0.5% fromexcess salt).
Excess body weight is the third most common avoidable cause of cancer in the UK,estimated to be responsible for 5.5% of cancers in 2010 (4.1% inmen, 6.9% in women). In the last 15 years there have been significantincreases in levels of overweight and obesity, and currently in England, a totalof 66% of men and 57% of women have a BMI of⩾25 kg m−2: this includes 22% ofmen and 25% of women who are obese (NHS InformationCentre, 2010), defined as a BMI>30 kg m−2. Trends among children andyoung people suggest that we are yet to experience the full health impact of theoverweight and obesity epidemic in the UK.
Alcohol consumption is the fourth most important cause of cancer in the UK, andpopular belief is that alcohol use is a highly prevalent and growing problem forthe UK population. In fact, data from the national General Lifestyle Survey(Robinson and Bugler, 2010) show that theaverage number of units of alcohol consumed in a week rose in the 1990s to apeak in the period 2000–2002 of around 17 units for men, and 7.5 units forwomen, but has fallen since that time in both sexes. The proportion of men andwomen drinking more than the recommended maximum (21 units a week in men and 14units in women) has also been falling. The fall in consumption occurred amongmen and women in all age groups, but was most evident among those aged16–24. It is quite possible, therefore, that the burden of alcohol-relatedcancers is around its maximum at present, and will fall in future.
Population-attributable fractions provide a valuable quantitative appraisal ofthe impact of different factors in cancer causation, and are thus helpful inprioritising cancer control strategies. However, they should not be used toindicate the percentage of cancers that can currently be prevented by practicalmeans without reference to the individual sections that discuss some of theuncertainties involved. Furthermore, quantifying the likely impact of preventiveinterventions requires rather complex scenario modelling, includingspecification of realistically achievable population distributions of riskfactors, and the timescale of change, as well as the latent periods betweenexposure and outcome, and the rate of change following modification in exposurelevel (e.g., Soerjomataram et al, 2010).Thus, although 50% of colorectal cancer cases diagnosed in the UK in 2010are attributable to lifestyle (diet, alcohol, physical inactivity andoverweight), it has been estimated that only about half of this number ispreventable in a reasonable (∼20-year) timescale (Parkin et al, 2009).
See acknowledgements on page Si.
|Exposure||Optimum exposure level|
|1 Deficit in intake of fruit and vegetables||⩾5 servings (400 g) per day|
|2 Red and preserved meat||Nil|
|3 Deficit in intake of dietary fibre||⩾23 g per day|
|4 Excess intake of salt||⩽6 g per day|
|Overweight and obesity||BMI⩽25 kg m−2|
|Physical exercise||⩾30 min 5 times per week|
|Radiation – ionising||Nil|
|Radiation – solar (UV)||As in the 1903 birth cohort|
|Reproduction: breast feeding||Minimum of 6 months|
|% cancers attributable torisk factor exposure, by cancer site|
|Exposure||Oral cavity and pharynx||Oeso- phagus||Stomach||Colon– rectum||Liver||Pancreas||Gall- bladder||Larynx||Lung||Meso- thelioma||Melanoma||Breast||Cervix uteri||Corpus uteri||Ovary||Bladder||Kidney||Leukaemia||Alla|
|Fruit and vegetables||57.2||46.6||37.0||—||—||—||—||45.9||8.5||—||—||—||—||—||—||—||—||—||6.1|
|Overweight and obesity||—||26.9||—||13.6||—||12.8||19.7||—||—||—||—||—||—||—||—||—||25.0||—||4.1|
|Radiation – ionising||—||2.0||0.9||1.1||0.6||—||—||—||4.2||—||—||—||—||—||—||2.6||—||7.8||1.7|
|Radiation – UV||—||—||—||—||—||—||—||—||—||—||89.8||—||—||—||—||—||—||—||3.5|
|All of the above||92.9||89.7||78.1||56.5||48.6||35.7||19.7||92.8||91.1||97.0||89.8||—||—||—||—||43.5||47.0||16.4||45.3|
|Fruit and vegetables||53.6||45.1||33.9||—||—||—||—||43.5||9.3||—||—||—||—||—||—||—||—||—||3.4|
|Overweight and obesity||—||11.2||—||12.2||—||11.5||17.8||—||—||—||—||8.7||—||33.7||—||—||22.2||—||6.9|
|Radiation – ionising||—||3.9||1.7||2.2||1.1||—||—||—||5.4||—||—||0.9||—||—||—||2.3||—||10.4||2.0|
|Radiation – UV||—||—||—||—||—||—||—||—||—||—||82.4||—||—||—||—||—||—||—||3.6|
|All of the above||85.0||88.2||69.2||51.9||28.0||38.9||17.8||90.9||86.5||82.5||82.4||26.8||100||36.9||20.7||37.1||33.9||13.6||40.1|
|Fruit and vegetables||56.0||46.1||35.8||—||—||—||—||45.4||8.8||—||—||—||—||—||—||—||—||—||4.7|
|Overweight and obesity||—||21.7||—||13.0||—||12.2||18.3||—||—||—||—||8.7||—||33.7||—||—||24.0||—||5.5|
|Radiation – ionising||—||2.7||1.2||1.6||0.8||—||—||—||4.7||—||—||0.9||—||—||—||2.5||—||8.9||1.8|
|Radiation – UV||—||—||—||—||—||—||—||—||—||—||85.9||—||—||—||—||—||—||—||3.5|
|All of the above||90.6||89.0||74.9||54.4||41.6||37.3||18.3||92.5||89.2||94.4||85.9||26.8||100||36.9||20.7||41.8||42.3||15.2||42.7|
aExcluding non-melanoma skin cancer.
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