Skip to main content
Asian Pacific Journal of Cancer Prevention : APJCP logoLink to Asian Pacific Journal of Cancer Prevention : APJCP
. 2018;19(11):3193–3202. doi: 10.31557/APJCP.2018.19.11.3193

Influence of Income on Cancer Incidence and Death among Patients in Aomori, Japan

Rina Tanaka 1,*, Masashi Matsuzaka 2, Yoshihiro Sasaki 1,2
PMCID: PMC6318397  PMID: 30486610

Abstract

Background:

Aomori Prefecture has experienced the highest cancer-related mortality rates since the 2000s in Japan. In addition, income of residents in Aomori Prefecture is lower than that of a countrywide average. Aims of this study were to examine the relationships of the incidence and mortality rates of common cancers (stomach, colorectal, liver, lung, breast, cervical, and prostate) with the income levels of residential income area and clarify the factors contributing to the high mortality rates in Aomori prefecture.

Methods:

We included data on all patients diagnosed with stomach, colorectal, liver, lung, breast, cervical, or prostate cancer in the Aomori cancer registry database between 2010 and 2012. Age-standardized incidence rates and incidence rate ratios were calculated. Risk of cancer mortality related to economic disparities was determined via multivariable Cox regression analysis and adjusted for age, sex, and stage at diagnosis in the multivariable model.

Results:

We identified 21,240 eligible cancer patients. There were no differences in AIRs and IRRs among patients with stomach, colorectal, or lung cancer according to income. Contrarily, AIRs and IRRs were higher in higher-income areas than in lower-income areas among patients with breast, cervical, or prostate cancer. There were no significant differences in HRs according to income for any cancer type.

Conclusions:

Patients with higher income were diagnosed with early-stage disease more frequently, and they had higher AIRs for breast, cervical, and prostate cancers than those with middle and low incomes. However, there were no significant differences in hazard ratios.

Keywords: Incidence, mortality, socioeconomic status

Introduction

The incidence and mortality rates of stomach, liver, and cervical cancers are higher in lower-income countries than in higher-income countries (Ott et al., 2011). By contrast, those of lung, colorectal, and breast cancer are higher in higher-income countries (Torre et al., 2016). Individuals with higher levels of income and education are more likely to participate in cancer screening and treatment, thus explaining the lower rates of certain forms of cancer.

Meanwhile, risk factors for cancer include smoking, overweight and obesity, drinking, and certain chronic infections (Anand et al., 2008). Specifically, infections caused by Helicobacter pylori, human papillomavirus, and the hepatitis B and C viruses are the leading causes of stomach, cervical, and liver cancers, respectively (Oh et al., 2014). Previous studies reported that chronic infections are more likely to cause cancer in lower-income countries, further explaining differences in cancer incidence between lower- and higher-income nations (Ott et al., 2011; Bruni et al., 2016). Although the incidence of infection-related cancers declined in most higher-income countries, that of liver and stomach cancers is higher in Japan than in other countries (Ferlay et al., 2012).

In Japan, the overall incidence of cancer is increasing, and the disease has been a leading cause of death since 1981 (Vital statistics Japan). Specifically, the incidence of colorectal, lung, breast, pancreas, cervical, and prostate cancers has been increasing in Japan due to its aging society, although general cancer-related mortality has been decreasing (Vital statistics Japan). Some Japanese studies noted the inverse associations of cervical, endometrial, and colorectal cancer incidence and survival with area deprivation (Ueda et al., 2006; Miki et al., 2014). However, there have been few population-based studies of the association of area income with cancer death in Japan.

Aomori Prefecture has experienced the highest cancer-related mortality rates since the 2000s in Japan. Conversely, other prefectures successfully decreased cancer mortality rates. Thus, revealing the barriers to improving cancer-related mortality rates in Aomori Prefecture is of the utmost importance. It is assumed that access to hospitals and medical treatment may be an important factor in Aomori Prefecture because of its aging population and shortage of public transportation. In addition, the annual income of residents in Aomori Prefecture is lower than that of a countrywide average, 2,405,000 yen vs. 3,057,000 yen (System of National Accounts).

Aomori Prefecture consists of 40 municipal governments, and these regions have varied economic conditions (Supplement and supporting data). It is presumed that this inequality of economic conditions might be associated with cancer incidence and mortality. Therefore, the aims of this study were to examine the relationships of the incidence and mortality rates of common cancers (stomach, colorectal, liver, lung, breast, cervical, and prostate) in Japan with the income levels of the 40 municipalities in Aomori Prefecture and clarify the factors contributing to the high mortality rates in the prefecture.

Materials and Methods

Patients

We included data on all patients diagnosed with stomach, colorectal, liver, lung, breast, cervical, or prostate cancer in the Aomori cancer registry database between 2010 and 2012, and the patients were followed up until December 2013. Death certificate only (DCO) cases were excluded. The percentage of DCO cases (%DCO) is one of the quality indicators of cancer registry data, and the %DCO values of the Aomori cancer registry for 2010, 2011, and 2012 were 5.1%, 2.6%, and 2.0%, respectively.

Data collection

We obtained the following clinical and demographic information via data extraction: sex, age at diagnosis, date of diagnosis, survival duration, primary tumor site (International Classification of Disease for Oncology, Third Edition; site code C16, C18–C20, C22, C33–C34, C50, C53, C61), stage at diagnosis, treatment administered (surgery, endoscopy, radiotherapy, chemotherapy, endocrine therapy, and other treatment), and address code. Stage at diagnosis was classified as in situ, localized (confined to the organ of origin), regional (invasion of adjacent organs or tissues and/or regional lymph node metastasis), distant (the presence of any distant metastasis), or unknown according to the Surveillance, Epidemiology, and End Results summary stage at diagnosis (Young et al., 2001). Income data for the 40 municipalities in 2010 were obtained from the Aomori Prefectural Government homepage (Municipal inhabitant’s accounts statistics in Aomori prefecture), and income was classified into four groups by quartile as follows: lowest, mid-low, mid-high, and highest (Supplement and supporting data). The population of the municipalities in 2011–2012 was calculated using the interpolation method based on the population data of the National Census of Japan in 2010 and 2015 (National Census of Japan).

Statistical analysis

Age-standardized incidence rates (AIRs) were calculated using the direct method based on the Japanese standard population. The incidence rate ratios (IRRs) were calculated using the lowest income area as the reference. The risk of cancer mortality related to economic disparities was determined via multivariable Cox regression analysis and adjusted for age, sex, and stage at diagnosis in the multivariable model. Hazard ratios (HRs) were calculated using Stata 13 statistical software (StataCorp LLP, College Station, TX, USA).

Results

We identified 21,858 eligible patients, but the data for 618 patients were excluded for the following reasons: DCO, 616 cases; unknown address, 1 case; and unknown sex, 1 case.

Table 1 presents the characteristics of patients with various cancer. The proportions of patients with stomach or colorectal cancer who were diagnosed at early and late stages were similar among the income groups, although treatment was not equitable among the groups. The proportions of patients with stomach or colorectal cancer who were treated with surgery, radiotherapy, and chemotherapy were higher in higher-income areas than in lower-income areas. However, the proportion of patients with stomach cancer who were treated with endoscopic therapy was highest in the lowest income area. A higher proportion of patients with liver cancer received chemotherapy in higher-income areas than in lower-income areas. The proportion of patients who received other treatments (percutaneous ethanol injection therapy, radiofrequency ablation, and hepatic transcatheter arterial chemoembolization) was higher in higher-income areas than in lower-income areas. No significant differences in stage at diagnosis according to income were noted among patients with lung cancer. However, the proportion of patients with lung cancer who were treated with chemotherapy increased with increasing income. Meanwhile, the proportion of patients with breast cancer who were diagnosed at an early stage (in situ or localized) was higher in higher-income areas than in lower-income areas. Additionally, the proportions of patients with breast cancer who were treated with radiotherapy and endocrine therapy were highest in the highest income area. Among patients with cervical cancer, the proportion of patients who were diagnosed at an early stage (in situ or localized) was lowest in the lowest income area, and the proportion of patients treated with surgery was higher in higher-income areas than in lower-income areas. Conversely, the proportion of patients treated with chemotherapy was lower in lower-income areas. Among patients with prostate cancer, patients in the highest income group were most likely to be diagnosed at an early stage (localized). Additionally, the proportion of patients who received radiotherapy was higher in higher-income areas than in lower-income areas.

Table 1.

Characteristics of Patients with Cancer

Stomach
Community income Lowest Mid-low Mid-high Highest
n=496 n=583 n=1297 n=1933
N % N % N % N %
Sex
 Men 353 71.2 392 67.2 877 67.6 1,347 69.7
 Women 143 28.8 191 32.8 420 32.4 586 30.3
Age at diagnosis, years
 -59 54 10.9 66 11.3 160 12.3 304 15.7
 60-69 116 23.4 132 22.6 343 26.4 501 25.9
 70-79 193 38.9 219 37.6 445 34.3 671 34.7
 80+ 133 26.8 166 28.5 349 26.9 457 23.6
Stage at diagnosis
 In situ 9 1.8 6 1.0 4 0.3 3 0.2
 Localized 237 47.8 266 45.6 598 46.1 833 43.1
 Regional 97 19.6 119 20.4 243 18.7 462 23.9
 Distant 90 18.1 126 21.6 282 21.7 428 22.1
 Unknown 63 12.7 66 11.3 170 13.1 207 10.7
Surgical treatment
 Surgery 214 43.1 280 48.0 631 48.7 969 50.1
 Non-surgery 235 47.4 274 47.0 593 45.7 871 45.1
 Unknown 47 9.5 29 5.0 73 5.6 93 4.8
Endoscopic therapy
 Endoscopic therapy 121 24.4 105 18.0 224 17.3 363 18.8
 Non-endoscopic therapy 333 67.1 447 76.7 994 76.6 1,473 76.2
 Unknown 42 8.5 31 5.3 79 6.1 97 5.0
Radiotherapy treatment
 Radiotherapy 1 0.2 5 0.9 12 0.9 17 0.9
 Non-radiotherapy 444 89.5 548 94 1,208 93.1 1,819 94.1
 Unknown 51 10.3 30 5.1 77 5.9 97 5.0

Colorectal
Lowest Mid-low Mid-high Highest
n=664 n=810 n=1885 n=3119

Sex
 Men 382 57.5 483 59.6 1071 56.8 1785 57.2
 Women 282 42.5 327 40.4 814 43.2 1334 42.8
Age at diagnosis, years
 -59 121 18.2 108 13.3 338 17.9 514 16.5
 60-69 154 23.2 213 26.3 501 26.6 879 28.2
 70-79 219 33 293 36.2 620 32.9 1079 34.6
 80+ 170 25.6 196 24.2 426 22.6 647 20.7
Stage at diagnosis
 In situ 139 20.9 166 20.5 341 18.1 620 19.9
 Localized 191 28.8 244 30.1 585 31 1032 33.1
 Regional 135 20.3 176 21.7 429 22.8 690 22.1
 Distant 104 15.7 148 18.3 334 17.7 515 16.5
 Unknown 95 14.3 76 9.4 196 10.4 262 8.4
 Surgery 359 54.1 512 63.2 1,168 62.0 2,000 64.1
 Non-surgery 212 31.9 250 30.9 612 32.5 972 31.2
 Unknown 93 14.0 48 5.9 105 5.6 147 4.7
Endoscopic therapy
 Endoscopic therapy 169 25.5 166 20.5 404 21.4 721 23.1
 Non-endoscopic therapy 426 64.2 591 73.0 1,371 72.7 2229 71.5
 Unknown 69 10.4 53 6.5 110 5.8 169 5.4
Radiotherapy treatment
 Radiotherapy 2 0.3 3 0.4 12 0.6 27 0.9
 Non-radiotherapy 560 84.3 754 93.1 1758 93.3 2913 93.4
 Unknown 102 15.4 53 6.5 115 6.1 179 5.7

Liver
Lowest Mid-low Mid-high Highest
n=124 n=169 n=433 n=566

Sex
 Men 84 67.7 107 63.3 291 67.2 376 66.4
 Women 40 32.3 62 36.7 142 32.8 190 33.6
Age at diagnosis, years
 -59 22 17.7 18 10.7 62 14.3 73 12.9
 60-69 39 31.5 39 23.1 100 23.1 159 28.1
 70-79 39 31.5 70 41.4 149 34.4 189 33.4
 80+ 24 19.4 42 24.9 122 28.2 145 25.6
Stage at diagnosis
 Localized 57 46 93 55 218 50.3 262 46.3
 Regional 17 13.7 27 16 81 18.7 101 17.8
 Distant 20 16.1 25 14.8 49 11.3 77 13.6
 Unknown 30 24.2 24 14.2 85 19.6 126 22.3
Surgical treatment
 Surgery 20 16.1 30 17.8 41 9.5 63 11.1
 Non-surgery 87 70.2 130 76.9 346 79.9 434 76.7
 Unknown 17 13.7 9 5.3 46 10.6 69 12.2
Radiotherapy treatment
 Radiotherapy 1 0.8 3 1.8 2 0.5 11 1.9
 Non-radiotherapy 106 85.5 157 92.9 385 88.9 484 85.5
 Unknown 17 13.7 9 5.3 46 10.6 71 12.5
Other treatment
 Yes 51 41.1 58 34.3 194 44.8 248 43.8
 No 56 45.2 102 60.4 193 44.6 248 43.8
 Unknown 17 13.7 9 5.3 46 10.6 70 12.4

Lung
Lowest Mid-low Mid-high Highest
n=434 n=472 n=1,062 n=1,700

Sex
 Men 320 73.7 334 70.8 745 70.2 1,198 70.5
 Women 114 26.3 138 29.2 317 29.8 502 29.5
Age at diagnosis, years
 -59 55 12.7 44 9.3 106 10 208 12.2
 60-69 89 20.5 116 24.6 258 24.3 467 27.5
 70-79 155 35.7 175 37.1 405 38.1 602 35.4
 80+ 135 31.1 137 29.0 293 27.6 423 24.9
Stage at diagnosis
 In situ 1 0.2 0 0.0 1 0.1 1 0.1
 Localized 105 24.2 110 23.3 198 18.6 391 23.0
 Regional 100 23.0 121 25.6 250 23.5 404 23.8
 Distant 152 35.0 169 35.8 437 41.1 642 37.8
 Unknown 76 17.5 72 15.3 176 16.6 262 15.4
Surgical treatment
 Surgery 90 20.7 98 20.8 207 19.5 439 25.8
 Non-surgery 293 67.5 326 69.1 745 70.2 1,100 64.7
 Unknown 51 11.8 48 10.2 110 10.4 161 9.5
Radiotherapy treatment
 Radiotherapy 108 24.9 116 24.6 214 20.2 416 24.5
 Non-radiotherapy 276 63.6 305 64.6 739 69.6 1122 66.0
 Unknown 50 11.5 51 10.8 109 10.3 162 9.5

Breast
Lowest Mid-low Mid-high Highest
n=186 n=272 n=711 n=1,456

Sex
 Men 2 1.1 3 1.1 4 0.6 12 0.8
 Women 184 98.9 269 98.9 707 99.4 1,444 99.2
Age at diagnosis, years
 -59 84 45.2 143 52.6 362 50.9 750 51.5
 60-69 45 24.2 70 25.7 181 25.5 366 25.1
 70-79 36 19.4 42 15.4 108 15.2 225 15.5
 80+ 21 11.3 17 6.3 60 8.4 115 7.9
Stage at diagnosis
 In situ 15 8.1 15 5.5 75 10.5 132 9.1
 Localized 89 47.8 140 51.5 365 51.3 774 53.2
 Regional 52 28 70 25.7 169 23.8 366 25.1
 Distant 8 4.3 15 5.5 43 6 79 5.4
 Unknown 22 11.8 32 11.8 59 8.3 105 7.2
Surgical treatment
 Surgery 154 82.8 208 76.5 596 83.8 1179 81
 Non-surgery 16 8.6 40 14.7 79 11.1 201 13.8
 Unknown 16 8.6 24 8.8 36 5.1 76 5.2
Radiotherapy treatment
 Radiotherapy 36 19.4 49 18 152 21.4 547 37.6
 Non-radiotherapy 134 72 197 72.4 522 73.4 828 56.9
 Unknown 16 8.6 26 9.6 37 5.2 81 5.6
Endocrine treatment
 Endocrinotherapy 71 38.2 81 29.8 227 31.9 810 55.6
 Non-endocrinotherapy 99 53.2 164 60.3 446 62.7 566 38.9
 Unknown 16 8.6 27 9.9 38 5.3 80 5.5

Cervical
Lowest Mid-low Mid-high Highest
n=76 n=109 n=299 n=601

Sex
 Women 76 100 109 100 299 100 601 100
Age at diagnosis, years
 -59 58 76.3 86 78.9 244 81.6 500 83.2
 60-69 8 10.5 12 11 21 7.0 53 8.8
 70-79 6 7.9 9 8.3 18 6.0 33 5.5
 80+ 4 5.3 2 1.8 16 5.4 15 2.5
Stage at diagnosis
 In situ 44 57.9 75 68.8 204 68.2 401 66.7
 Localized 16 21.1 17 15.6 36 12.0 88 14.6
 Regional 13 17.1 12 11 32 10.7 56 9.3
 Distant 2 2.6 4 3.7 15 5.0 25 4.2
 Unknown 1 1.3 1 0.9 12 4.0 31 5.2
Surgical treatment
 Surgery 58 76.3 97 89 246 82.3 491 81.7
 Non-surgery 12 15.8 10 9.2 42 14.0 76 12.6
 Unknown 6 7.9 2 1.8 11 3.7 34 5.7
Radiotherapy treatment
 Radiotherapy 12 15.8 10 9.2 39 13.0 72 12.0
 Non-radiotherapy 57 75 96 88.1 243 81.3 466 77.5
 Unknown 7 9.2 3 2.8 17 5.7 63 10.5

Prostate
Lowest Mid-low Mid-high Highest
n=169 n=220 n=502 n=892

Sex
 Men 169 100 220 100 502 100 892 100
Age at diagnosis, years
 -59 9 5.3 13 5.9 29 5.8 53 5.9
 60-69 53 31.4 76 34.5 140 27.9 258 28.9
 70-79 78 46.2 89 40.5 249 49.6 433 48.5
 80+ 29 17.2 42 19.1 84 16.7 148 16.6
Stage at diagnosis
 In situ - - - -
 Localized 85 68.5 101 59.8 261 60.3 501 88.5
 Regional 35 28.2 47 27.8 101 23.3 138 24.4
 Distant 12 9.7 23 13.6 75 17.3 122 21.6
 Unknown 37 29.8 49 29 65 15 131 23.1
Surgical treatment
 Surgery 53 31.4 56 25.5 126 25.1 228 25.6
 Non-surgery 87 51.5 124 56.4 319 63.5 537 60.2
 Unknown 29 17.2 40 18.2 57 11.4 127 14.2
Radiotherapy treatment
 Radiotherapy 20 11.8 32 14.5 104 20.7 165 18.5
 Non-radiotherapy 121 71.6 148 67.3 341 67.9 601 67.4
 Unknown 28 16.6 40 18.2 57 11.4 126 14.1
Endocrine treatment
 Endocrinotherapy 76 45 96 43.6 264 52.6 462 51.8
 Non-endocrinotherapy 69 40.8 85 38.6 182 36.3 308 34.5
 Unknown 24 14.2 39 17.7 56 11.2 122 13.7

Table 2 shows the AIRs and IRRs by income and cancer type. Figure 1 shows scatter plot between AIRs and residential income. There were no differences in AIRs and IRRs among patients with stomach, colorectal, or lung cancer according to income. Contrarily, AIRs and IRRs were higher in higher-income areas than in lower-income areas among patients with breast, cervical, or prostate cancer.

Table 2.

Age-Standardized Incidence Rates (AIRs) and Incidence Rate Ratios (IRRs) for Various Cancers

Stomach Colorectal Liver Lung Breast Cervical Prostate
AIR IRR (95% CI) AIR IRR (95% CI) AIR IRR (95% CI) AIR IRR (95% CI) AIR IRR (95% CI) AIR IRR (95% CI) AIR IRR (95% CI)
Residential income Lowest 47.2 1.0 (reference) 71.5 1.0 (reference) 13.2 1.0 (reference) 40.9 1.0 (reference) 61.8 1.0 (reference) 43.4 1.0 (reference) 36.6 1.0 (reference)
Mid-low 53.1 1.1 (−0.8 to 7.0) 77.4 1.1 (−0.3 to 6.2) 15.4 1.2 (−4.1 to 10.5) 41.7 1.0 (−1.5 to 7.1) 88.1 1.4 (0.9 to 7.4) 57.3 1.3 (−0.2 to 7.7) 46.9 1.3 (−0.7 to 7.9)
Mid-high 51.3 1.1 (−1.0 to 6.9) 79.9 1.1 (−0.1 to 6.3) 16.9 1.3 (−3.6 to 10.8) 40.0 1.0 (−1.7 to 7.0) 86.6 1.4 (0.8 to 7.3) 58.4 1.3 (−0.1 to 7.8) 45.0 1.2 (−0.9 to 7.8)
Highest 47.8 1.0 (−1.3 to 6.8) 78.9 1.1 (−0.2 to 6.2) 13.5 1.0 (−4.8 to 10.3) 40.3 1.0 (−1.7 to 7.0) 101.8 1.6 (2.0 to 8.3) 62.8 1.4 (0.4 to 8.1) 47.6 1.3 (−0.6 to 8.0)

IRR, incidence rate ratio; CI, confidence interval

Figure 1.

Figure 1

Scatter Plots between AIRs and Residential Income for Various Cancers.

Table 3 presents the adjusted HRs for each income category. Although the adjusted HRs tended to be highest in the lowest income area, there were no significant differences according to income for any cancer type.

Table 3.

Adjusted Hazard Ratios (HRs) for Various Cancers

Stomach Colorectal Liver Lung Breast Cervical Prostate
HR* (95% CI) P value HR* (95% CI) P value HR* (95% CI) P value HR* (95% CI) P value HR* (95% CI) P value HR* (95% CI) P value HR* (95% CI) P value
Residential income Lowest 1 (reference) 1 (reference) 1 (reference) 1 (reference) 1 (reference) 1 (reference) 1 (reference)
Mid-low 0.97 (0.81 to 1.16) 0.72 1.07 (0.89 to 1.02) 0.46 0.86 (0.64 to 1.16) 0.34 1.09 (0.92 to 1.29) 0.31 0.71 (0.38 to 1.31) 0.27 0.72 (0.29 to 1.79) 0.48 0.65 (0.41 to 1.02) 0.06
Mid-high 0.89 (0.75 to 1.04) 0.14 0.95 (0.81 to 1.12) 0.56 0.73 (0.57 to 0.94) 0.01 1.06 (0.92 to 1.22) 0.45 1.08 (0.65 to 1.81) 0.77 0.77 (0.38 to 1.57) 0.47 0.7 (0.48 to 1.03) 0.07
Highest 1 (0.86 to 1.17) 0.99 1.02 (0.87 to 1.18) 0.84 0.85 (0.67 to 1.08) 0.19 1.18 (1.03 to 1.35) 0.02 0.91 (0.56 to 1.49) 0.71 0.57 (0.28 to 1.16) 0.12 0.82 (0.57 to 1.16) 0.26
*

Adjusted for age, sex, and stage at diagnosis.; CI, confidence interval

Discussion

Certain chronic infections are risk factors for cancer, and they can explain variations in cancer incidence among low-, middle-, and high-income countries. A study by Ott et al. clearly indicated that the AIRs and mortality rates of lung, colorectal, and breast cancers were higher in high-income countries than in low- and middle-income countries (Ott et al., 2011). Moreover, they said that the AIRs and mortality rates of infection-related cancers (stomach, liver, and cervical cancers) were higher in low- and middle-income than in high-income countries (Ott et al., 2011). This can be explained by the fact that infection-related cancers account for more than 26% of the total cancers in low- and middle-income countries (Parkin et al., 2006). Conversely, the incidence rate of non-infection-related cancers has continued to increase in many countries including high-, middle-, and low-income countries (Global Burden of Disease Cancer Collaboration, et al., 2015). This unfavorable increase reflects an increased prevalence of known risk factors (e.g., obesity, physical inactivity, smoking) and the increased use of screening modalities (e.g., mammography, pap smear). Although mammography is the most effective method for detecting breast cancer at an early stage, it also leads to overdiagnosis of the disease (Marmot et al., 2013). A recent study that estimated that the rate of overdiagnosis due to mammography ranged 0%–54% (Puliti et al., 2011). By contrast, cancer-related mortality is affected by patients’ access to cancer treatment. Because cancer treatment is not adequately accessible in low-income countries, cancer-related mortality rates have not declined in these countries (Fidler et al., 2017).

Our data identified disparities of AIRs for breast, cervical, and prostate cancers according to income, whereas those of stomach, colorectal, lung, and liver cancers were not influenced by income. However, the adjusted HRs were not significantly different according to income. Recent study investigated socioeconomic inequality in cancer mortality in South Korea (Khang et al., 2016). In this study, poor people had higher risk of cancer death. Although South Korea is similar to Japan, our results differed from previous study. These findings can be explained by several factors. First, the prevalence of risk factors for cervical, breast, and prostate cancers was higher in high-income areas than in middle- and low-income areas. Risk factors for these cancers include HPV infection, alcohol consumption habit, obesity, and aging (Key et al., 2002). In Aomori Prefecture, the average BMI among women was 23.2 in 2012, compared with a countrywide average of 22.5 (National Health and Nutrition Survey in 2012). In addition, 30.1% of people in Aomori Prefecture are older than 65, compared with 26.6% for the entire country (National Census of Japan). This higher proportion of elderly people might explain the findings in the prefecture. Second, because there were no significant differences in adjusted HRs according to age, overdiagnosis due to easy access to hospitals would increase the incidence rates and overtreatment for patients with breast, cervical, and prostate cancers simultaneously in higher-income areas. Several studies have underlined the problems of overdiagnosis and overtreatment (Nagler et al., 2017; Morgan et al., 2017; Jegerlehner et al., 2017). The Norwegian Breast Cancer Screening Program was conducted in 1995 and 1996 (Falk et al., 2013). This study reported the frequency of overdiagnosis among a cohort of women over a period of 10 years after they participated in cancer screening. Falk et al. estimated the number of women overdiagnosed in mammographic screening using English, Welsh, and Norwegian data (Falk et al., 2016). Moreover, Kilpeläinen et al., (2016) reported the association of prostate cancer with socioeconomic status in Finland. Their study found that higher socioeconomic status was associated with the overdiagnosis of low-risk prostate cancer, as well as a lower risk of incurable prostate cancer and lower prostate cancer-related mortality. Unnecessary treatment, higher treatment costs, and otiose anxiety might be burdensome to patients. Third, it was suspected that accessibility to cancer treatment was not significantly affected by residential income. Dreyer et al., (2017) reported socioeconomic disparities in the receipt of treatment for incident breast cancer. They observed that poor and near-poor women were less likely to receive treatment than women of a higher socioeconomic status. Kumachev et al., (2016) studied the associations among socioeconomic status, screening, and treatments. In this study, they demonstrated that higher socioeconomic status was associated with greater frequencies of screening and treatments and higher survival rates. Therefore, our results partially coincided with these previous findings. However, age standardized mortality rates for cancer in Aomori Prefecture are the highest in Japan. Thus, the quality of cancer treatment might not be sufficient to decrease the number of cancer-related deaths in this region.

Our study had several limitations. First, the income data do not exactly reflect patients’ individual income. Our data reflected the average annual income in municipal areas. However, residential income might not reflect access to health and medical services for cancer because local governments have a responsibility to formulate cancer policy and ensure cancer control. Second, we did not include data for cancer risk factors at the individual level. Third, we did not include patients’ individual educational levels and occupations. These socioeconomic factors have been examined to explain the disparities regarding cancer incidence and death. Because this study was designed to clarify the effect of income disparities on cancer, we did not include these data.

In conclusion, the relationships of mean residential income with cancer incidence and mortality differed from previous findings. Patients with higher income were diagnosed with early-stage disease more frequently, and they had higher AIRs for breast, cervical, and prostate cancers than those with middle and low incomes. However, there were no significant differences in cancer survival rates. Our results might be helpful for policymakers to develop a cancer policy. Policymakers should take steps HPV infection control and stopping excess prostatic specific antigen test in higher income area. Although the associations of socioeconomic status with cancer incidence and mortality have been reported for developed countries, socioeconomic disparities exist among individual areas in the countries. The differences in cancer mortality rates between affluent and poor individuals have reportedly widened in high-income countries. Thus, inequalities of cancer mortality rates between affluent and poor areas should be also investigated.

Conflict of interest

The authors declare no conflicts of interest associated with this manuscript.

References

  • 1.Anand P, Kunnumakkara AB, Sundaram C, et al. Cancer is a preventable disease that requires major lifestyle changes. Pharm Res. 2008;25:2097–116. doi: 10.1007/s11095-008-9661-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Bruni L, Diaz M, Barrionuevo-Rosas L, et al. Global estimates of human papillomavirus vaccination coverage by region and income level:a pooled analysis. Lancet Glob Health. 2016;4:453–63. doi: 10.1016/S2214-109X(16)30099-7. [DOI] [PubMed] [Google Scholar]
  • 3.Dreyer MS, Nattinger AB, Mc Ginley EL, et al. Socioeconomic status and breast cancer treatment. Breast Cancer Res Treat (Epub ahead of print) 2017 doi: 10.1007/s10549-017-4490-3. doi:10.1007/s10549-017-4490-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Falk RS, Hofvind S, Skaane P, et al. Overdiagnosis among women attending a population-based mammography screening program. Int J Cancer. 2013;133:705–12. doi: 10.1002/ijc.28052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Falk RS, Hofvind S. Overdiagnosis in mammographic screening because of competing risk of death. Cancer Epidemiol Biomarkers Prev. 2016;25:759–65. doi: 10.1158/1055-9965.EPI-15-0819. [DOI] [PubMed] [Google Scholar]
  • 6.Ferlay J, Soerjomataram I, Ervik M, et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide:IARC CancerBase No. 11. 2012. [Accessed Nov 2017]. http://globocan.iarc.fr .
  • 7.Fitzmaurice C, Dicker D, et al., editors. Global Burden of Disease Cancer Collaboration. The global burden of cancer 2013. JAMA Oncol. 2015;1:505–27. doi: 10.1001/jamaoncol.2015.0735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Jegerlehner S, Bulliard JL, Aujesky D, et al. Overdiagnosis and overtreatment of thyroid cancer:a population-based temporal trend study. PLoS One. 2017;12:e0179387. doi: 10.1371/journal.pone.0179387. doi:10.1371/journal.pone.0179387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Key TJ, Allen NE, Spencer EA, et al. The effect of diet on risk of cancer. Lancet. 2002;360:861–8. doi: 10.1016/S0140-6736(02)09958-0. [DOI] [PubMed] [Google Scholar]
  • 10.Khang YH, Kim HR. Socioeconomic inequality in mortality using 12-year follow-up data from nationally representative surveys in South Korea. Int J Equity Health. 2016;15:51. doi: 10.1186/s12939-016-0341-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Kilpeläinen TP, Talala K, Raitanen J, et al. Prostate cancer and socioeconomic status in the Finnish randomized study of screening for prostate cancer. Am J Epidemiol (Epub ahead of print) 2016 doi: 10.1093/aje/kww084. [DOI] [PubMed] [Google Scholar]
  • 12.Kumachev A, Trudeau ME, Chen KK. Associations among socioeconomic status, patterns of care and outcomes in breast cancer patients in a universal health care system:Ontario's experience. Cancer. 2016;122:893–8. doi: 10.1002/cncr.29838. [DOI] [PubMed] [Google Scholar]
  • 13.Nagler RH, Franklin Fowler E, Gollust SE. Women's awareness of and responses to messages about breast cancer overdiagnosis and overtreatment:results from a 2016 national survey. Med Care. 2017;55:879–85. doi: 10.1097/MLR.0000000000000798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.National Census of Japan, (Ministry of Internal Affairs and Communications, Statistics Bureau) (in Japanese) [Accessed Nov 2017]. http://www.e-stat.go.jp/SG1/estat/GL08020103.do?_toGL08020103_&tclassID=000001077438&cycleCode=0&requestSender=estat .
  • 15.National Health and Nutrition Survey in 2012 (Ministry of Health, Labour and Welfare), (in Japanese) [Accessed Nov 2017]. http://www.mhlw.go.jp/bunya/kenkou/eiyou/h24-houkoku.html .
  • 16.Marmot MG, Altman DG, Cameron DA, et al. The benefits and harms of breast cancer screening:an independent review. Br J Cancer. 2013;108:2205–40. doi: 10.1038/bjc.2013.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Miki Y, Inoue M, Ikeda A, et al. Neighborhood deprivation and risk of cancer incidence, mortality and survival:results from a population-based cohort study in Japan. PLoS One. 2014;9:e106729. doi: 10.1371/journal.pone.0106729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Morgan DJ, Dhruva SS, Coon ER, et al. 2017 update on medical overuse:a systematic review. JAMA Interm Med (in press) 2017 doi: 10.1001/jamainternmed.2017.4361. doi:10.1001/jamainternmed.2017.4361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Municipal inhabitant's accounts statistics in Aomori prefecture, Aomori Prefectural Government (in Japanese) [Accessed Nov 2017]. http://www6.pref.aomori.lg.jp/tokei/data/0000003207/0000003207_2_3.xlsx .
  • 20.Oh JK, Weiderpass E. Infection and cancer:global distribution and burden of diseases. Ann Glob Health. 2014;80:384–92. doi: 10.1016/j.aogh.2014.09.013. [DOI] [PubMed] [Google Scholar]
  • 21.Ott JJ, Ullrich A, Mascarenhas M, et al. Global cancer incidence and mortality caused by behavior and infection. J Public Health. 2011;33:223–33. doi: 10.1093/pubmed/fdq076. [DOI] [PubMed] [Google Scholar]
  • 22.Parkin DM. The global health burden of infection-associated cancers in the year 2002. Int J Cancer. 2006;118:30–44. doi: 10.1002/ijc.21731. [DOI] [PubMed] [Google Scholar]
  • 23.Puliti D, Miccinesi G, Paci E. Overdiagnosis in breast cancer:design and methods of estimation in observational studies. Prev Med. 2011;53:131–3. doi: 10.1016/j.ypmed.2011.05.012. [DOI] [PubMed] [Google Scholar]
  • 24.System of National Accounts (Cabinet Office, Government of Japan) (in Japanese) [Accessed Nov 2017]. http://www.esri.cao.go.jp/jp/sna/data/data_list/kenmin/files/files_kenmin.html .
  • 25.Torre LA, Siegel RL, Ward EM, et al. Global cancer incidence and mortality rates and trends-An update. Cancer Epidemiol Biomarkers Prev. 2016;25:16–27. doi: 10.1158/1055-9965.EPI-15-0578. [DOI] [PubMed] [Google Scholar]
  • 26.Ueda K, Kawachi I, Tsukuma H. Cervical and corpus cancer survival disparities by socioeconomic status in a metropolitan area of Japan. Cancer Sci. 2006;97:283–91. doi: 10.1111/j.1349-7006.2006.00179.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Vital statistics Japan (Ministry of Health, Labour and Welfare) [Accessed Nov 2017]. http://www.e-stat.go.jp/SG1/estat/List.do?lid=00000110∤ .
  • 28.Vital Statistics Japan (Ministry of Health, Labour and Welfare), Cancer Registry and Statistics. Cancer Information Service, National Cancer Center, Japan. [Accessed Nov 2017]. http://ganjoho.jp/reg_stat/statistics/dl/index.html .
  • 29.Young JL, Jr, Roffers SD, Ries LAG, et al. SEER Summary staging manual –2000 :codes and coding instructions. National Cancer Institute, NIH Pub No. 01-4969, Bethesda, MD. 2001 [Google Scholar]

Articles from Asian Pacific Journal of Cancer Prevention : APJCP are provided here courtesy of West Asia Organization for Cancer Prevention

RESOURCES