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Contribution of income-related inequality andhealthcare utilisation to survival in cancers of thelung, liver, stomach and colon

Jun Yim,1 Seung-sik Hwang,2 Keun-young Yoo,3 Chang-yup Kim4

ABSTRACTObjectives To examine differences in the survival ratesof cancer patients according to socioeconomic status,focusing on the role of the degree of healthcare

utilisation by the patient.Methods An observational follow-up study was done for261 lung cancer, 259 liver cancer, 268 stomach cancerand 270 colon cancer patients, diagnosed during

1999e2002. Income status and healthcare utilisationwere assessed with National Health Insurance (NHI)data; survival during 1999e2002 was identified by deathcertificate. HRs and 95% CI were derived from Cox

proportional hazards regression.Results and Conclusions The HRs for low incomestatus are larger for colon cancer (2.37, 95% CI 1.17 to4.80), followed by stomach (1.67, 95% CI 1.01 to 2.78),liver (1.57, 95% CI 1.03 to 2.39) and lung cancers (1.46,95% CI 0.99 to 2.14). In the model including the variableof healthcare utilisation, colon and stomach cancersexhibited a lower HR in the moderate healthcareutilisation groups (0.40, 95% CI 0.21 to 0.76 in colon;0.59, 95% CI 0.37 to 0.96 in stomach), whereas for livercancer, the high utilisation group exhibited a higherhazard (1.72, 95% CI 1.07 to 2.75). A lower incomestatus is independently related to a shorter survival timein cancer patients, especially in less fatal cancers.Healthcare utilisation independently affects the likelihoodof survival from colon and stomach cancers, implyingthat a moderate degree of healthcare utilisationcontributes to a longer survival time.

INTRODUCTIONCancer incidence and mortality have increasedsharply in South Korea (Korea) in recent years. Thefraction of deaths attributable to cancer has morethan doubled from 10.5% of the total number ofdeaths in 1981 to 24% in 2000.1 As in manydeveloped countries, cancer has emerged as one of

the most critical health problems in Korea.However, the burden of cancer is not equal amongall population groups. It is already known thatsocioeconomic status (SES) affects the mortalityrate from cancersdmortality is particularly high inpatients with low incomes.2e7

The overall mortality rate due to a fatal disease isdetermined by the occurrence of the disease and thesurvival rate. However, the effect of SES on thesurvival rate of cancer patients has been studied lessthoroughly than has the occurrence of the disease,8

although such effects have been noted for mostcancer types and for several countries. In particular,

there are only a few studies that have dealtspecifically with the aetiology of different cancer

survival among different SES groups. Variousfactors have been proposed as possible underlyingreasons for this SES effect: stage at diagnosis,treatment modality, quality of treatment, hostfactors and psychosocial factors.8 Among them, ithas been accepted that stage of cancer at diagnosisis probably the most important contributing factorto the different rates of survival among thedifferent SES groups, but the contribution ofquality and mode of treatment and psychosocialfactors has scarcely been studied. Moreover, verylittle attention has been paid to the degree of

healthcare utilisation compared to other treatmentfactors such as modality and quality.

Therefore, the aim of this study was to analysedifferences in the survival rates of cancer patientsaccording to SES, focusing on the role of the degreeof healthcare utilisation by the patient. Wehypothesised that patients with a lower SES wouldutilise healthcare less and have a shorter survivaltime.

METHODSData

All cases registered during 2000 were initially

sampled from the five major hospitals that had thelargest number of registered cancer patientsnationally in the Korean National Cancer Registry.For each cancer, a cohort of 300 patients wassampled from the five hospitals using stratifiedrandom sampling according to the total number ofpatients, and a survey of their medical records wasconducted by four trained medical record adminis-trators. Patients diagnosed prior to 1999 wereexcluded and the final analysis was carried out on261 cases with lung cancer, 259 with liver cancer,268 with stomach cancer and 270 with coloncancer.

Morphology of lung cancer was composed of

squamous cell carcinoma, not otherwise specified(NOS) (32.8%), adenocarcinoma, NOS (32.1%) andsmall cell carcinoma, NOS (11.5%). Morphology ofliver cancer was composed of hepatocarcinoma(79.5%), cholangiocarcinoma (8.1%) and neoplasm,NOS (6.6%). Morphology of stomach cancer wascomposed of adenocarcinoma, NOS (50.4%), signetring cell carcinoma (16.0%) and tubular adenocar-cinoma (13.8%). Morphology of colon cancer wascomposed of adenocarcinoma, NOS (75.4%),tubular adenocarcinoma (7.0%) and neoplasm,NOS (5.5%).

The patients general information and risk

factors, including Karnofsky performance statusscale (KPSS) for physical performance,9 were

1Department of PreventiveMedicine, Gachon University ofMedicine and Science, Incheon,Korea2Department of Social andPreventive Medicine, InhaUniversity School of Medicine,Incheon, Korea3Department of PreventiveMedicine, Seoul NationalUniversity College of Medicine,Seoul, Korea4School of Public Health, SeoulNational University, Seoul,Korea

Correspondence toJun Yim, Department ofPreventive Medicine, GachonUniversity of Medicine andScience, 534-2 Yeonsu3-dong,Yeonsu-gu, Incheon, 406-799,Korea; yim99@gachon.ac.kr

Accepted 12 June 2010

Yim J, Hwang S-s, Yoo K-y, et al. J Epidemiol Community Health (2010). doi:10.1136/jech.2009.104554 1 of 4

Research reportJECH Online First, published on October 19, 2010 as 10.1136/jech.2009.104554

Copyright Article author (or their employer) 2010. Produced by BMJ Publishing Group Ltd under licence.

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extracted from their medical records, and the cancers werestaged according to the summary staging of the surveillance,epidemiology and end results programme (SEER) of the USNational Cancer Institute.10 The death or survival of patientswas confirmed by the 1999e2002 death certificate statistics ofthe Korean National Statistical Office. The maximum observa-tion period was 48 months.

Estimates of income and degree of healthcare utilisationSince the payroll of the employed and the means-tested incomeof the self-employed determines the National Health Insurance(NHI) premium paid by individuals (the level of premium thusreflecting the income status of the insured), the income status ofpatients could be obtained from their NHI insurance profile. Theestimated income level was quartered from the total populationregistered with NHI and Medicaid, but for the analysis, incomelevel was divided into three groups, high, middle and low, afterthe interquartile range of estimated income levels had beenintegrated into the middle group. The population of Medicaidwas included in the low-income group.

Every healthcare institution has to submit all claims data to

the insurer to be reimbursed, and payment for cancer treatmentby private insurance is only supplementary to the NHI, and soalmost all healthcare utilisation of cancer patients is included inthe NHI database. Information about healthcare utilisation foreach patient was therefore obtained from NHI claims data. Thedegree of healthcare utilisation was defined by the number ofoutpatient visits per month. Since the number of outpatientvisits was significantly correlated with whether the patient hadbeen admitted or not using the ManteleHaenszel c2 test(p

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and survival for the more fatal cancers, such as lung cancer.

These findings suggest that survival of less fatal cancers isinfluenced more strongly by income-related factors, such asnutrition, housing, level of healthcare utilisation and socialsupport.1 1 1 2 Another factor that may explain the differentsurvival times among those with differing SES is the quality oftreatment received.8 In this study, we have not explored directlythe quality of treatment received by each patient, but eachhospital may have a different level of quality and hospitalfactors could affect the quality of treatment given. Hospitalfactors, however, were not found to be significant for unadjustedHRs and were excluded in models 1 and 2.

Inconsistent with our hypothesis, the degree of healthcareutilisation was not significantly different among the differentincome status groups. This is probably attributable to the

universal coverage of the NHI for the entire population, inwhich basic healthcare utilisation is ensured even for those inthe lower-income groups, although there is still a high rate of co-payment that sometimes hinders access to healthcare. Moreover,healthcare utilisation independently affects the survival ofstomach and colon cancers, implying that a moderate degree ofhealthcare utilisation contributes to a longer survival period,even after adjusting for income status. Appropriate healthcareutilisation should be ensured in cancer patients to improvesurvival across all levels of income status.

In spite of a partially beneficial effect, healthcare utilisationdoes not exhibit a doseeresponse relationship, the highest levelof utilisation being related to a higher hazard than in moderate-

utilisation groups for all of the cancers studied. Thesefi

ndingscan be explained partly by the fact that some of the healthcare

utilisation was probably the result of an aggravated clinical

course for patients rather than being initiated by the patientsthemselves or their providers in order to contribute to a betteroutcome. Consequently, if we suggest that appropriate health-care utilisation is beneficial to the survival of cancer patients,cases for which utilisation is a result of a more serious healthcondition should be excluded from further analyses.

Methodological issuesOur study has some limitations. First, the NHI premium shouldbe justified as an appropriate measure of income status. Sincethe premium of the employed is based on the payroll and that ofthe self-employed is based on their estimated income fromvarious sources, the extent to which the actual income level isreflected in the premium would be different between these two

groups. However, the NHI premium is continuously revised toaccurately reflect income, and so no other measure was thoughtto be superior as a proxy for real income. In particular, the resultanalysed on the population of employed was not different fromthat of employed and self-employed. Another limitation is thatthe death certificate statistics of the National Statistical Officewere not fully validated due to the limited information availableon the cause of death. Although most of the data contain someinformation about the cause of death, it was difficult to estab-lish whether or not the cause was directly related to cancer.Therefore, cancer patients who died of other causes might havebeen included in the cancer mortality statistics. However,because death from cancer is far more dominant than from other

causes,

8

this type of inaccuracy is unlikely to alter the resultsof this study to any large extent. A third limitation is that

Figure 1 KaplaneMeier curves forlung cancer (A), liver cancer (B),stomach cancer (C), and colon cancer(D) among three different incomegroups: highest, 2nd to 3rd, lowestincome group in Korea, 1999e2002.The log-rank test was used forstatistical comparisons.

Yim J, Hwang S-s, Yoo K-y, et al. J Epidemiol Community Health (2010). doi:10.1136/jech.2009.104554 3 of 4

Research report

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area-based measures of SES were not available. These wouldhave allowed us to evaluate independently the area and indi-vidual effects using multilevel analysis. Moreover, we could notexclude cases with serious health conditions, which probably

induced high healthcare utilisation, due to the limitation ofmedical records. The final limitation is that only patientsregistered in five hospitals were sampled. Consequently, it isdifficult to represent a tendency of the total population. If thisproblem could be solved, we would have to consider the relativesurvival of total population with cancer, but have not done so.However, the total number of cancer patients who are registeredin these hospitals represents more than 25% of the total numberof cancer patients registered in hospitals throughout Korea.

Therefore, we do not believe that this limitation is critical withregard to the formulation of the data pool.

Conclusions A lower income status is independently related to a shortersurvival time in cancer patients, particularly in less fatal cancers.Healthcare utilisation independently affects the survival ofcolon and stomach cancers, implying that a moderate degree ofhealthcare utilisation contributes to a longer survival period.

Funding Ministry of Health and Welfare, Republic of Korea.

Competing interests None declared.

Provenance and peer review Not commissioned; externally peer reviewed.

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Table 2 Adjusted HRs from multivariable Cox models for differentmortality according to income status among 1058 cancer patients,1999e2002

Unadjusted HR Model 1* Model 2y(95% CI) Adjusted HR (95% CI) Adjusted HR (95% CI)

Lung

Income status

High 1.00 ref. 1.00 ref. 1.00 ref.

Middle 1.17 (0.84 to 1.65) 1.07 (0.76 to 1.52) 1.11 (0.78 to 1.57)Low 1.25 (0.87 to 1.80) 1.48 (1.01 to 2.17) 1.46 (0.99 to 2.14)

Outpatient visit