a Cancer Bureau, Laboratory Centre for Disease Control, Health Canada, Ottawa, Canada.
b Alberta Cancer Board, Department of Epidemiology, Prevention & Screening, Canada.
Abstract
Background Several epidemiological studies have found that lung cancer is inversely related to socioeconomic status (SES) and suggest it as a possible risk factor for lung cancer. This study examines SES and lung cancer risk in Canada.
Methods Mailed questionnaires with telephone follow-up were used to obtain data on 3280 newly diagnosed, histologically confirmed lung cancer cases and 5073 population controls, between 1994 and 1997, in eight Canadian provinces. Measurement included information on SES, smoking habits, alcohol use, diet, residential and occupational histories and both residential and occupational exposure to environmental tobacco smoke (ETS). Odds ratios (OR) and 95% CI were derived from unconditional logistic regression analysis.
Results Compared with high income adequacy, an increased risk was found among low income males and females, with adjusted OR of 1.7 (95% CI : 1.32.2) and 1.5 (95% CI : 1.12.0), respectively. Compared with 8 years of education, the adjusted OR were 0.6 (95% CI : 0.50.7) and 0.6 (95% CI : 0.50.8) for
14 years education among males and females, respectively. Lung cancer risk was significantly increased for males of some social classes. The population attributable risk for income adequacy, education and social class was 24%, 25% and 21% among males, respectively, and 14% and 19% for income adequacy and education among females, respectively, in this Canadian population.
Conclusions A statistically significant association between income adequacy, education social class and lung cancer risk was found.
Keywords Socioeconomic status, lung cancer, income, education, social class, odds ratio
Accepted 27 July 2000
Since the late nineteenth century, socioeconomic status (SES) has been considered an important factor in cancer epidemiology. Associations between specific cancers and SES have been observed in studies around the world. There is consistent evidence of a significant association between SES and cancer incidence and mortality.
Incidence and mortality from lung cancer are greater in lower socioeconomic groups,18 and some studies indicate an association between SES and lung cancer survivorship.9,10 In a 17-year follow-up study, Hein et al.11 concluded that the substantial social inequalities in lung cancer risk are only partially explained by differences in smoking habits between social classes. A study in the Netherlands12 indicates that occupational exposure to asbestos, paint dust, polycyclic aromatic hydrocarbons, and welding fumes could not account for the inverse association between SES and lung cancer risk.
Data from the National Enhanced Cancer Surveillance System (NECSS) are used here to examine the impact of SES on lung cancer risk in Canada.
Methods
The NECSS collected individual data from a population-based sample including 18 types of cancer and 5073 population controls between 1994 and 1997, in the provinces of British Columbia, Alberta, Saskatchewan, Manitoba, Ontario, Prince Edward Island, Nova Scotia and Newfoundland. The overall methodology for the NECSS has been explained in The National Enhanced Cancer Surveillance System: A Case-Control Approach to Environment-related Cancer Surveillance in Canada.13
Cases
Cases were identified by Provincial Cancer Registries: 3280 eligible cases (1722 males and 1558 females) with histologically confirmed primary lung cancer newly diagnosed between 1994 and 1997 in eight provinces. After obtaining physician consent, the registries sent a letter and questionnaire to the lung cancer subjects.
Controls
In the NECSS population controls were frequency matched to the overall collection of cases for 18 types of cases. A total of 5073 controls without cancer were selected from a random sample of individuals within a province, with an age/sex distribution similar to that of all cancer cases (i.e. 18 cancer types: liver, testis, pancreas, brain, stomach, bladder, kidney, colon, rectum, prostate, breast, lung, bone, salivary, leukaemia, multiple myeloma, non-Hodgkin's lymphoma and mesothelioma). Provincial Cancer Registries collected information from controls using the same protocol as for the cases. The strategies for population controls varied by province depending on data availability and accessibility. In Prince Edward Island, Nova Scotia, Manitoba, Saskatchewan and British Columbia, age group- and sex-stratified random samples of the province's population were obtained through the Provincial Health Insurance Plans. In Ontario, Ministry of Finance data were used to obtain a stratified random sample. Newfoundland and Alberta used random digit dialling to obtain a population sample.
Data collection
The cancer registries identified most cases within 13 months of diagnosis through pathology reports. After obtaining physician consent, questionnaires were mailed to cancer cases and controls by cancer registries. If the questionnaire was not completed and returned, a reminder postcard was sent out after 14 days and a second copy of the questionnaire at 4 weeks; after 6 weeks telephone follow-up was used, if required, to complete the questionnaire. Information was collected on family income, education, marital status, employment history, residential history, height, weight, smoking history, alcohol use, dietary history, physical activity, and vitamin and mineral supplements. In addition, the NECSS collected histories on lifetime residential and occupational exposure to environmental tobacco smoke (ETS).
Employment history included each job or occupation that the subject had for at least 12 months in Canada or elsewhere; time period; type of industry, business, or service and company name; main job duties; job location(s); job title; and status (full-time, part-time, seasonal, other). In addition, each subject was also asked about exposure at work (or home) to any of 17 specified chemicals (for at least one year): asbestos, arsenic salts, chromium salts, cadmium salts, coal tar, soot, pitch, creosote, asphalt, mineral, cutting or lubricating oil, benzene, benzidine, isopropyl oil, dyestuffs, vinyl chloride, pesticides, herbicides, mustard gas, radiation sources, welding, or wood dust, and the duration of exposure in years.
Smokers, defined as those smoking at least 100 cigarettes in their lifetime, were asked the age at which they began smoking, the average number of cigarettes smoked daily, years of cigarette smoking, and years since quitting. In the analyses, never smokers formed the baseline group. Information on pipe or cigars and chewing tobacco was also recorded. In addition, information on alcohol consumption, specifically beer, wine and liquor, was collected.
The diet questionnaire, which examined eating habits 2 years previous, was based on the Block-NCI Health Habits and History Questionnaire14 and modified for the Canadian diet. This 70-item food frequency questionnaire provided data on Canadian eating patterns and the major source of nutrients in the Canadian diet, as well as the general changes in the individual's diet compared with 20 years ago. The food items were categorized based on the quartile cut-off points defined by consumption reported by controls.
Socioeconomic status indicators
Three SES measures were used.
Family income adequacy
A household income adequacy variable was derived to recognize that large households require more income than smaller households. Income adequacy was based on average annual household income in the 5 years preceding the survey. The household income was indicated as a categorical variable with the following values: <$10 000, $10 00019 999, $20 000 29 999, $30 00049 999, $50 00099 999, and $100 000. Low income: Income <$20 000 with
3 people, or <$30 000 with
4 people. Lower middle: Income $20 000<$30 000 with
3 people, or $30 000<$50 000 with
4 people. Upper middle: Income $30 000<$50 000 with
3 people, or $50 000 <$100 000 with
4 people. High income: Income of
$50 000 for up to 3 people, or
$100 000 for
4 people.
Education
Education was categorized to three levels: <8 years, 913 years, and 14 years.
Social class
Information concerning occupational history was coded to the 1980 Standard Occupation Classification.15 The codes were converted to social class indicators defined according to the British Registrar General's Classification.16 For each person, the total occupational years and the years within each social class were calculated according to lifetime occupation history. It was possible that a person's job title might have changed several times over their lifetime; social class was based on the longest duration working within a particular social class, and grouped into six levels: social class I (Professional), II (Intermediate), III N (Skilled non-manual), III M (Skilled manual), IV (Partly skilled) and V (Unskilled).17 If a person worked the same number of years in different social classes, the lowest social class would be chosen automatically.
The statistical analysis was performed using the analysis package SAS (version 6.12).18 Odds ratios (OR) and 95% CI were computed. Multivariate analysis was undertaken using unconditional logistic regression after adjusting for 10-year age groups, province (Newfoundland, Nova Scotia, Prince Edward Island, Ontario, Manitoba, Saskatchewan, Alberta, British Columbia), pack-years of smoking, cumulative years of residential and occupational exposure to ETS, and total consumption of vegetables and vegetable juices and of meat.
In addition, we estimated the per cent population attributable risk (PAR%) for lung cancer in relation to income adequacy, education and social class using the method described by Bruzzi et al.,19 which allows estimation of PAR on the basis of data from case-control studies; these risks are expressed as percentages in the article. The calculations of PAR apply the knowledge of OR and distribution of risk exposure only among case subjects, assuming that they are representative of all cases in the population.
Results
Of 5316 questionnaires sent to patients, 3280 were returned, a response rate for patient contact of 61.7%. Of 8105 questionnaires sent to selected potential controls, 5073 responded, representing 62.6% of controls ascertained and 67.4% (5073/7532) of controls contacted. In all, 573 questionnaires were returned because of a wrong address.
Table 1 shows the distribution of lung cancer cases and the control group according to sex, age and SES indicators. On average, the cases were older than controls: mean age of 63.8 and 61.7 years among male and female cases, respectively, and 57.4 and 55.7 years among controls; the differences were statistically significant. Both male and female controls were better educated and more often belonged to the highest family income group and social class. Income adequacy was not reported in 27.5% and 21.6% of males, and 30.9% and 27.8% of females in cases and controls, respectively.
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The impact of SES is likely manifest through other lifestyle risk factors. Socioeconomic status has been shown consistently to be related to lifestyle behaviours.20 Risk factors for lung cancer, for example, smoking,21 dietary factors,22 or occupational exposures to carcinogens,23 are highly influenced by, and vary according to, social class. Social inequalities associated with risk for lung cancer have been examined in previous studies3,11,12,24,25 and NECSS results sustain these findings, supporting an overall association between SES and lung cancer risk in Canada. In our study, however, the association of SES and lung cancer remained strong even when these major confounders were controlled in multiple logistic regression analyses.
The large national sample allowed us to examine numerous lifestyle variables separately for males and females. Results showed a strong inverse association between education and family income and lung cancer risk in both sexes, consistent with previous studies.12,25 We found that social class was associated with lung cancer risk among males only; males with social class IV and V had significantly elevated risks for lung cancer compared with social class I. This is consistent with a study in Denmark.11 For females, our findings revealed that the association between social class and lung cancer risk no longer existed after adjusting for smoking and other confounding variables. This might be explained by stronger associations in males than females and differences between genders in occupational experience and smoking habits and their effect on lung cancer. The proportion of Canadian women who had never smoked was higher (37%) than for men (24%).26
Socioeconomic circumstances play a major part in subsequent health differences, and differences in lifestyle can indeed account for some of the class differential in health.17 Differences in smoking habits between social classes could not, however, completely account for strong social inequalities in the risk of lung cancer in our study, in agreement with a Danish 17-year follow-up study.11 Kawaski and Lochner point out that smoking behaviour is one of the most glaring and persistent differentials in lifestyles comparing the poor with the non-poor27 and tobacco use has been causally connected with both lung and other cancers.28 An estimated 90% of all lung cancers are smoking related.29 There is a disproportional distribution of tobacco use among social classes,30 use being most common among lower SES urban males and females.7 Certainly higher rates of cigarette smoking among the manual labour group will contribute to poor health.31 In the present study, smoking pack-years and exposure to ETS from residence and occupation were included in the logistic regression model to control the confounding effect of smoking on the association between SES and lung cancer. The association between lung cancer and SES still displayed a strong negative (for education, income and social class) gradient.
The impact of smoking appears stronger for low social classes, for instance, in each strata of smoking pack-years, an increased risk of male lung cancer was observed among the lower social class, compared with higher classes. This may indicate the need for targeted health promotion: since the risk of lung cancer decreased with the increased years since quitting smoking, smoking cessation could have more impact within this group than the others. The highest risk for male lung cancer (OR = 3.4, 95% CI : 1.29.7) among quitters was in social class V among those who had quit smoking less than 10 years ago. More important, targeted programmes to reduce initiation of tobacco use among children and adolescents32 could potentially address these socioeconomic inequalities in health.
Diet is another potential factor contributing to inequalities in health. Diet mediates the risk of lung cancer: diet high in fat22 and high consumption of meat33 may increase the risk of lung cancer, while higher vegetable consumption may significantly reduce the risk.22 This is consistent with our results, that is, a positive (with total consumption of meat) and inverse (with consumption of total vegetables and vegetable juice) relationship were observed, respectively. In Canada, the lower SES adults reported consuming more fat, and reported a higher number of unhealthy behaviours than those from higher SES groups.34 A complex combination of these factors, such as smoking and dietary habits, may contribute to increased risk of lung cancer in subjects of low socioeconomic level.
The NECSS study found a strong positive association between occupational exposure to asbestos and to coal tar, soot, creosote, or asphalt and lung cancer among males (data not shown) and the statistically significant inverse association between level of education and family income and lung cancer risk did not change after adjustment for these exposures, i.e. occupational exposure to carcinogens could not explain all the differential in lung cancer risk due to SES. This is consistent with a study in the Netherlands.12 We also found that social class was associated with lung cancer risk among males after adjusting for occupational exposure to chemicals (data not shown).
The possible limitations of our data need to be considered. Air pollution35,36 and family history29 may also affect lung cancer risk, but our study did not include information on industrial air pollution or family history of lung cancer as potential confounding variables. Some selection bias may also have been introduced in our data. Although the NECSS study was conducted on a large population-based sample from eight Canadian provinces, the low case response rate (61.7%) might lend itself to potential selection bias. However, the significant association between SES and lung cancer risk observed in the present study is consistent with results from Denmark and the Netherlands.11,12,25
Our findings suggest that three potentially modifiable socioeconomic indicators (level of education, income adequacy and social class) accounted for one-fourth (education and income adequacy) and one-fifth (social class) of the cases of male lung cancer, and about one-fifth (for education) and one-seventh (for income adequacy) of the cases of female lung cancer in this Canadian population. It is important to note that the adjusted PAR% for separate factors do not necessarily add up to the PAR% for all factors acting simultaneously.19 The PAR% for a given factor is defined as the disease reduction if this factor were the first to be removed.37
This study supports the differential in lung cancer risk due to SES and provides evidence that determinants besides smoking and other factors contribute to this association. Socioeconomic status appears to be an independent contributor to health status,38 as a surrogate for lifestyle,34,39 diet,20 working and living conditions.40 These same factors are likely related to cancer; rates of lung cancer41 and other health outcomes34 are higher in Canadian communities with lower incomes. Socioeconomic status should not be overlooked as a risk factor in examining cancer aetiology; our results provide a theoretical basis to examine ways to reduce socioeconomic inequalities in health to further the control of lung cancer in Canada.
Conclusion
We found a significant inverse association between education, income adequacy, social class and lung cancer risk. These findings were examined by sex and smoking status. Social inequalities in Canada appear to influence the development of lung cancer. In terms of PAR, 25%, 24% and 21% of the cases of male lung cancer and 19% and 14% of the cases of female lung cancer in this Canadian population may be attributed to low level of education, income adequacy and social class.
Acknowledgments
We would like to express our gratitude to Kathy White for her help in preparing this paper for publication.
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