The European Journal of Public Health Advance Access originally published online on July 15, 2008
The European Journal of Public Health 2008 18(5):466-472; doi:10.1093/eurpub/ckn052
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Social factors and health |
Education in relation to incidence of and mortality from cancer and cardiovascular disease in Japan
Shinichiro Ito1, Ribeka Takachi2,3, Manami Inoue3, Norie Kurahashi3, Motoki Iwasaki3, Shizuka Sasazuki3, Hiroyasu Iso4, Yoshitaka Tsubono2,5, Shoichiro Tsugane3 and for the JPHC Study Group*
1 Tohoku University School of Law, Sendai, Japan
2 Department of Clinical Epidemiology, Tohoku University Graduate School of Medicine, Sendai, Japan
3 Epidemiology and Prevention Division, Research Center for Cancer Prevention and Screening, National Cancer Center, Tokyo, Japan
4 Public Health, Department of Social and Environmental Medicine, Graduate School of Medicine, Osaka University, Osaka, Japan
5 Division of Health Policy, Tohoku University School of Public Policy, Sendai, Japan
Correspondence: Yoshitaka Tsubono, Division of Health Policy, Tohoku University School of Public Policy, 27-1 Kawauchi, Aoba-ku, Sendai-shi, Miyagi 980-8576 Japan, tel: +81-22-795-5940, fax: +81-22-795-5940, e-mail: ytsubono{at}gmail.com
Received September 26, 2007, accepted May 8, 2008
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Abstract |
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Background: Although lower education has been associated with poorer health, few studies have examined whether lower education affects mortality, incidence, both or neither of cancer and cardiovascular disease. Methods: The authors conducted a population-based prospective cohort study among 39 228 men and women who were aged 40–59 years and lived in four areas in Japan. Information on education and lifestyle variables were obtained by a self-administered questionnaire in 1990. Follow-up until the end of 2002 (for incidence) or 2003 (for mortality) ascertained 2573 and 1251 incident cases of cancer and cardiovascular disease, respectively, and 2430 deaths (1064 from cancer, 548 from cardiovascular disease and 818 from other causes). Results: After adjustment for demographic and lifestyle variables, <10 years of education, as compared with >12 years of education, was associated with significantly higher mortality from all causes [hazard ratio (HR) = 1.22, 95% confidence interval (CI): 1.05–1.42] and cardiovascular disease (HR = 1.44, 95% CI: 1.01–2.06), but was not associated with higher incidence of cardiovascular disease (HR = 0.96, 95% CI: 0.78–1.18) or higher mortality or incidence of cancer. Conclusion: The findings suggest that lower education is associated with higher mortality from all causes and cardiovascular disease among the Japanese population that is not totally attributable to lifestyle differences or higher cardiovascular disease incidence.
Keywords: cancer, cardiovascular disease, education, prospective study, socioeconomic status
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Introduction |
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Disparities in socioeconomic status, such as in income, education and occupation, are associated with disparities in health.1,2 There is growing recognition that such associations exist in affluent western countries3–5 as well as in poorer Asian and African countries.6–8 Japan is one of the most affluent countries with the longest life expectancy in the world,9 and the country has been known to have lower inequality of socioeconomic status than other developed countries. However, socioeconomic disparities in Japan have been increasing during the past few decades,10 and their possible detrimental effect on the health of the population has recently become public health and policy issues.
Educational level has been widely used as an indicator of socioeconomic status, because it is easily recorded, unaffected by poor health in adulthood and remains stable throughout life.11,12 Although a number of studies in Western populations found that lower educational level were associated with higher risk of mortality and morbidity,13–15 relatively few studies have been reported from Asian populations.16–20 Furthermore, most studies have used either mortality or incidence of disease as endpoints. Only a few studies in Western populations have simultaneously used mortality and incidence of the same disease,21–23 and there have been no reports of such studies on Asian populations.
The objective of this study was to examine the association between educational level and health status in a population-based, prospective cohort study in Japan. The endpoints used were mortality from all causes, cancer, cardiovascular disease (CVD), and other causes, as well as incidence of cancer and CVD, and we investigated whether the associations of educational level for mortality from cancer and CVD differs from the associations for incidence of these diseases.
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Methods |
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Study cohort
The Japan Public Health Center-based Prospective Study (JPHC study) Cohort I is a prospective cohort study that began in January 1990. The study protocol was approved by the institutional review board of the National Cancer Center, Japan. The study population was defined as all registered Japanese residents who were 40–59 years of age in five public health center (PHC) areas (29 981 men and 31 614 women). Four of the five PHC areas were located in the Mainland (Honshu) and one in Okinawa Island. One PHC area in metropolitan Tokyo was excluded from the present analysis, because its study population was defined differently from the others, and no data on incidence were available. The remaining four areas represent municipalities in relatively rural regions, and no metropolitan regions were included. The details of the study design have been described elsewhere.24 The remaining 54 498 members of the cohort were identified as potential participants of this study. Of them, 121 were found to be ineligible during the follow-up period and were excluded for any of several reasons (29 with non-Japanese nationality, 86 with the delayed reports of out-migration before the start of the follow-up, 3 with incorrect birth date and 3 with duplicate data). Then, the remaining 54 377 persons (26 988 men and 27 389 women) were considered eligible for the present study.
Baseline survey
A self-administered questionnaire was distributed to all registered residents in 1990, and they were asked to report on education and other sociodemographic information, personal medical history, smoking and drinking history and dietary habits. A total of 43 108 participants (20 641 men and 22 467 women) responded to the questionnaire, and the response rate was 79.3% (men 76.5%, women 82.0%).
With regard to educational level, participants were asked to choose if they completed education up to junior high school, high school, junior college or vocational school, university or higher or others. Education up to junior high school corresponded to 0–9 years of education, high school to 10–12 years of education, and junior college, vocational school and university to 13–16 years of education. For the purpose of this study, participants were assigned to three groups according to their educational level: a primary education (junior high school) group, a secondary education (high school) group and a tertiary education [junior college or vocational school, and university or higher (including post-graduate degrees)] group.
Of 43 108 participants who responded to the questionnaire, we excluded 1267 participants who did not report their educational level. We further excluded 712 participants who chose ‘others’ as their educational level, 1472 participants who reported a past history of cancer, ischaemic heart disease or stroke, and 429 participants who did not report their occupation. The 39 228 participants (18 940 men and 20 288 women) who remained after these exclusions were adopted as the participants of the analysis.
Follow-up
The endpoints of this study were mortality from all causes, cancer, CVD and other causes, and incidence of cancer and CVD. CVD was defined as stroke and myocardial infarction. With the follow-up described below, 2430 deaths (1064 from cancer, 548 from CVD and 818 from other causes) and 2573 incident cases of cancer and 1251 incident cases of CVD were ascertained.
Mortality
Participants were followed from the time of the baseline survey until 31 December 2003. Residence status, including survival, was confirmed annually through the residential registry maintained in each municipality in the areas where the participants resided. Japanese law requires registration of residency and deaths, and the registries are believed to be complete. According to the Resident Registration Law, anyone may inspect the resident registry. Information on the cause of each death was supplemented by checking the death certificate files, and the cause of death was classified according to the International Classification of Diseases, 10th Version (ICD-10). Person-years were accrued from the time of the baseline survey until one of the following endpoints, whichever came first: date of death, date of emigration from the study area, or date of the end of the study period. Persons who were lost to follow-up were censored at the last confirmed date of presence in the study area. Of 39 228 participants, 2430 (6.2%) died from all causes, 2418 (6.2%) moved out of study areas and 26 (0.07%) were lost to follow-up during the study period. For this study, follow-up period runs up to 527 696 person years. The 1064 cancer deaths (ICD10: C00-C97) ascertained during follow-up included gastric (172), lung (199), colorectum (131), liver (91), pancreas (75) and other cancers. The 548 deaths form CVD included 112 ischaemic heart disease (ICD10: I20-I25), 157 other heart disease (ICD10: I26-I52) and 279 stroke (I60-I69).
Incidence of cancer
Participants were followed from the time of the baseline survey until 31 December 2002. Cancers were identified by active patient notification from the local major hospitals in the study area and by data linkage with the population-based cancer registries. Death certificates were used as a supplementary information source. Cases were coded according to the International Classification of Diseases for Oncology, Third Edition (ICD-O-3). The earliest date of diagnosis was used in cases of metachronous multiple primary cancers, and the information on the most advanced cancer was used in cases of synchronous multiple primary cancers. Person-years were accrued from the time of the baseline survey until one of the following endpoints, whichever came first: date of diagnosis of cancer, date of death, date of emigration from the study area or date of the end of the study period. Persons who were lost to follow-up were censored at the last confirmed date of presence in the study area. The 2573 cancer incidence ascertained during follow-up included gastric (540), lung (248), colorectum (518), liver (107), breast (233) and other cancers.
Incidence of CVD
Participants were followed from the time of the baseline survey until 31 December 2002. We registered all major hospitals in the four PHC areas that admitted patients with stroke and myocardial infarction.25,26 Myocardial infarction was diagnosed according to the criteria of the MONICA project,27 and stroke was diagnosed by computer tomographic scan and/or magnetic resonance images according to the criteria of the National Survey of Stroke.28 The medical records of each hospital were reviewed by hospital physicians or PHC physicians who were blinded to the lifestyle data. The earliest date of diagnosis was used in cases in which stroke and myocardial infarction had occurred at different times. Person-years were accrued from the time of the baseline survey until one of the following endpoints, whichever came first: date of diagnosis of CVD, date of death, date of emigration from the study area or date of the end of the study period. Persons who were lost to follow-up were censored at the last confirmed date of presence in the study area. The 1251 incident cases of CVD ascertained during follow-up included 211 myocardial infarction and 1040 stroke cases.
Statistical analysis
We used the Cox proportional-hazards regression model to estimate hazard ratios by the SAS software, version 9.1 (SAS Institute, Inc., Cary, NC, USA). We chose tertiary education as the reference category. Hazard ratios (HRs) were adjusted for sex, age (5-year age groups) and Public Health Center area. Further adjustment was conducted using the following variables: smoking status (never, former, current), weekly ethanol intake (none, occasionally, 1–149, 150–299, 300–449 and 450 g or more/week), frequency of sports (never, 1–3 times/month, 1 day/week or more), body mass index (less than 19, 19–22.9, 23–26.9, 27 or more), energy intake (kcal/day), whether or not receiving screening tests in the last year (blood pressure, chest X-ray, photofluorography, gastrointestinal endoscopy, fecal occult blood test, barium enema, colonoscopy), fruit intake (occasionally, 3–4 times/week, every day), green vegetables intake (occasionally, 3–4 times/week, every day), yellow vegetables intake (occasionally, 3–4 times/week, every day) and other vegetables intake (occasionally, 3–4 times/week, or every day). Trend for linear association between education level and each outcome was tested with a single ordinal variable for education (tertiary = 1, secondary = 2, primary = 3). Finally, occupation at baseline was also adjusted to calculate relative risks.
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Results |
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The age-standardized distribution of the baseline characteristics according to educational level by sex is shown in table 1. Compared with participants with primary education, both men and women with tertiary education were less likely to smoke cigarettes, and more likely to consume fruit and vegetables, engage in sports and have screening tests. Participants with tertiary education were more likely to be management, professionals or clerical workers, and less likely to be engaged in farming, forestry, fishing, construction or other manual labors than those with a primary education.
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Table 2 shows the HRs for mortality from all causes, cancer, CVD and other causes, and incidence of cancer and CVD by educational level. The analyses for mortality among men and women showed that primary education was significantly associated with higher risk of death from all causes and CVD, but not from cancer, as compared with tertiary education (HR1). The higher risk of mortality from all causes remained significant after adjustment for potential confounders (HR2) and occupation (HR3), whereas the higher risk of mortality from CVD remained significant after adjustment for potential confounders (HR2) but was attenuated after adjustment for occupation (HR3). Secondary education was not associated with higher risk of mortality from all causes, cancer or CVD, although P-values for linear trend on HR2 were significant for mortality from all causes (P < 0.001) and CVD (P = 0.016), and marginally significant for cancer (P = 0.039). When tertiary and secondary education groups were combined into a single referent category, HR2 (95% CI) for primary education group were 1.19 (1.09–1.30) for all-cause mortality, 1.17 (1.03–1.34) for cancer mortality, 1.25 (1.03–1.51) for CVD mortality and 1.16 (1.00–1.35) for mortality from other causes. The analyses for incidence showed that primary or secondary education was not significantly associated with higher risk of cancer or CVD.
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The higher risk for mortality from all causes associated with primary education was more apparent among younger participants as compared with older participants: HR3 (95% CI) were 1.42 (1.08–1.86) and 1.15 (0.92–1.43) for men and women who were younger than 50 years of age and those who were 50 years of age or older, respectively. For other mortality and incidence endpoints, no remarkable differences in results were observed according to the age groups (data not shown).
As shown in table 2, the analyses stratified by sex demonstrated that men with a primary education had a higher risk of mortality from all causes and CVD than men with tertiary education (HR1 and HR2), but the higher risks were attenuated after adjustment for occupation (HR3). Primary education was not significantly associated with higher risk of mortality or incidence of cancer or higher incidence of CVD. Women with primary education had a higher risk of mortality from all causes than women with tertiary education. Primary education was not significantly associated with higher mortality or incidence of cancer or CVD.
When the two major endpoints of CVD, ischaemic heart disease and stroke, were considered, HR1 (95% CI) of mortality for primary education as compared with tertiary education, for men and women combined, were 2.05 (0.94–4.48) and 1.36 (0.88–2.10), respectively. The corresponding HR1 (95% CI) of incidence were 0.71 (0.47–1.08) and 1.07 (0.87–1.32), respectively.
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Discussion |
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In this population-based prospective cohort study in Japan, lower education was associated with significantly higher risk of mortality from all causes and CVD, but was not associated with higher incidence of CVD or higher mortality or incidence of cancer.
A large number of studies in Western populations have found that lower educational level was associated with higher risk of mortality and morbidity.13–15 However, there have been relatively few reports of studies on Asian populations other than Japan.16–20 Although the studies used a variety of endpoints, including mortality from all causes,16–18 neoplasms and circulatory diseases,18 communicable diseases, non-communicable diseases and injuries,19 and other diseases,18 and incidence of esophageal and gastric cancers,20 they were consistent in reporting that higher education was associated with significantly lower risk. However, none of the Asian studies simultaneously used mortality and incidence of the same diseases as endpoints.
There have been a few prospective cohort studies in Japan.29–33 The largest study involving 39 999 participants and 6628 deaths found that lower education was significantly associated with higher mortality from all causes and external causes (men and women), cancer (men only), circulatory system diseases and cerebrovascular diseases (women only).29 The second largest study with 11 081 participants and 588 deaths found that lower education was significantly associated with higher risk of mortality from CVD (men only).30 In a smaller study of only 5627 men and 368 deaths, lower education in a rural group was associated with significantly higher risk of mortality from all causes.31 The other studies did not find significant associations for several mortality endpoints, in part due to the small number of participants (2200)32 or cases (379 stomach cancer deaths).33 None of the studies used incidence endpoints.
To our knowledge, this is the first prospective cohort study in an Asian population that simultaneously examined the association between educational level and mortality and incidence of the same diseases. A few cohort studies in Western countries have used both mortality and incidence of the same disease such as breast cancer,21 myocardial infarction22 or coronary heart disease.23 The first study found that higher education was associated with higher incidence of breast cancer but not mortality, and the remaining two studies showed that lower education was associated with significantly higher mortality and incidence of myocardial infarction or coronary heart disease.
In the present study, we found an inverse association between educational level and mortality from CVD, but not incidence of CVD. These findings suggest that lower education is associated with higher case fatality among patients with CVD. Although a nationwide comprehensive health insurance system has been established in Japan since 1961, there may be socioeconomic disparities in the utilization of medical care services, as well as disparities in severity of disease at diagnosis. Studies in Western countries have found an association between lower educational level and higher case fatality,34–36 and similar studies in Japanese populations, including the present data, are needed.
In the present study, lower education was associated with higher mortality from all causes, and the higher risk associated with the lower education remained significant after adjustment for lifestyle variables and occupation in the combined analysis of men and women. These findings indicate that the disparity in mortality from all causes according to educational level cannot be totally explained by differences in lifestyle or occupation according to educational level. The association between lower education and higher mortality may be in part explained by psychological factors such as life events and locus of control,37 in addition to potential differences in medical care use and residual confounding due to measurement errors in the lifestyle and occupational variables or unmeasured lifestyle variables.
In contrast, although the higher risk of mortality from CVD remained significant after adjustment for lifestyle variables, it was attenuated after subsequent adjustment for occupation. We therefore examined the effect of occupation on mortality from CVD. Participants with lower education were more likely to be engaged in farming, forestry, fishing, construction and other manual labors than participants with higher education (table 1). Farming, forestry, fishing, construction and other manual labors were associated with higher risk of mortality from CVD than management, professionals and clerical workers (data not shown). Another nation-wide prospective study in Japan found a suggestive increase in cerebrovascular mortality among men engaged in manual work as compared with men engaged in office work.38 These observations suggest that the participants with lower education were more likely to be engaged in occupations with higher risk for cardiovascular mortality, which would explain in part the observed association between lower education and higher cardiovascular mortality.
As a limitation of the study, we did not examine the effect of income, another indicator of socioeconomic status, because our data did not include variables on income in the questionnaire. Also, the information on educational level was based on self-reports, and thus some misclassification of educational levels was inevitable. Additionally, age-standardized prevalence for past history of cancer and CVD at baseline was higher in participants with primary education (3.9%) than in those with secondary and tertiary educations (3.2 and 3.0%, respectively). The exclusion from the analyses of participants with past history of diseases could have underestimated the true magnitude of health disparity by education in this population.
In conclusion, this population-based prospective cohort study in Japan showed that lower education was associated with higher risk of mortality from all causes and CVD that is not totally attributable to poorer lifestyles or higher incidence of CVD. Studies examining the roles of psychological factors and medical care utilization are warranted to better understand the underlying mechanism by which lower education leads to higher mortality in the Japanese population.
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Appendix |
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The Members of the JPHC Study Group (principal investigator: S. Tsugane) are: S. Tsugane, M. Inoue, T. Sobue and T. Hanaoka, Research Center for Cancer Prevention and Screening, National Cancer Center; J. Ogata, S. Baba, T. Mannami and A. Okayama, National Cardiovascular Center; K. Miyakawa, F. Saito, A. Koizumi, Y. Sano and I. Hashimoto, Iwate Prefectural Ninohe PHC; Y. Miyajima, N. Suzuki, S. Nagasawa and Y. Furusugi, Akita Prefectural Yokote PHC; H. Sanada, Y. Hatayama, F. Kobayashi, H. Uchino, Y. Shirai, T. Kondo, R. Sasaki, Y. Watanabe and Y. Miyagawa, Nagano Prefectural Saku PHC; Y. Kishimoto, E. Takara, T. Fukuyama, M. Kinjo, M. Irei and H. Sakiyama, Okinawa Prefectural Chubu PHC; K. Imoto, H. Yazawa, T. Seo, A. Seiko, F. Ito and F. Shoji, Katsushika PHC; A. Murata, K. Minato, K. Motegi, and T. Fujieda, Ibaraki Prefectural Mito PHC; K. Matsui, T. Abe, M. Katagiri and M. Suzuki, Niigata Prefectural Kashiwazaki and Nagaoka PHC; M. Doi, A. Terao and Y. Ishikawa, Kochi Prefectural Chuo-higashi PHC; H. Sueta, H. Doi, M. Urata, N. Okamoto and F. Ide, Nagasaki Prefectural Kamigoto PHC; H. Sakiyama, N. Onga and H. Takaesu, Okinawa Prefectural Miyako PHC; F. Horii, I. Asano, H. Yamaguchi, K. Aoki, S. Maruyama and M. Ichii, Osaka Prefectural Suita PHC; S. Matsushima and S. Natsukawa, Saku General Hospital; M. Akabane, Tokyo University of Agriculture; M. Konishi and K. Okada, Ehime University; H. Iso, Osaka University; Y. Honda and K. Yamagishi, Tsukuba University; H. Sugimura, Hamamatsu University; Y. Tsubono, Tohoku University; M. Kabuto, National Institute for Environmental Studies; S. Tominaga, Aichi Cancer Center Research Institute; M. Iida and W. Ajiki, Osaka Medical Center for Cancer and Cardiovascular Disease; S. Sato, Osaka Medical Center for Health Science and Promotion; N. Yasuda, Kochi University; S. Kono, Kyushu University; K. Suzuki, Research Institute for Brain and Blood Vessels Akita; Y. Takashima, Kyorin University; E. Maruyama, Kobe University; the late M. Yamaguchi, Y. Matsumura, S. Sasaki and S. Watanabe, National Institute of Health and Nutrition; T. Kadowaki, Tokyo University; Y. Kawaguchi, Tokyo Medical and Dental University; and H. Shimizu, Sakihae Institute.
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Acknowledgements |
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This study was supported by Grants in Aid for Cancer Research and for the Third-Term Comprehensive Ten year Strategy for Cancer Control from the Ministry of Health, Labor and Welfare of Japan.
Conflicts of interest: None declared.
Key points
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Footnotes |
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*The members of the JPHC study group are listed in the Appendix.
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