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Socioeconomic disparity in cervical cancer screening among Korean women: 1998–2010

  • Minjee Lee1,
  • Eun-Cheol Park2,
  • Hoo-Sun Chang2,
  • Jeoung A Kwon1,
  • Ki Bong Yoo1 and
  • Tae Hyun Kim3Email author
BMC Public HealthBMC series ¿ open, inclusive and trusted201313:553

DOI: 10.1186/1471-2458-13-553

Received: 9 July 2012

Accepted: 21 May 2013

Published: 6 June 2013

Abstract

Background

Cervical cancer is the sixth most common cause of cancer among Korean women and is one of the most preventable cancers in the world. This study aimed to investigate the change in cervical cancer screening rates, the level of socioeconomic disparities in cervical cancer screening participation, and whether there was a reduction in these disparities between 1998 and 2010.

Methods

Using the Korean Health and Nutrition Examination Survey, women 30 years or older without a history of cervical cancer and who completed a health questionnaire, physical examination, and nutritional survey were included (n = 17,105). Information about participation in cervical cancer screening was collected using a self-administered questionnaire. Multiple logistic regression analysis was performed to investigate the relationship between cervical cancer screening participation and the socioeconomic status of the women.

Results

The cervical cancer screening rate increased from 40.5% in 1998 to 52.5% in 2010. Socioeconomic disparities influenced participation, and women with lower educational levels and lower household income were less likely to be screened. Compared with the lowest educational level, the adjusted odds ratios (ORs) for screening in women with the highest educational level were 1.56 (95% confidence interval (CI): 1.05–2.30) in 1998, and 1.44 (95% CI: 1.12–1.87) in 2010. Compared with women with the lowest household income level, the adjusted ORs for screening in women with the highest household income level were 1.80 (95% CI: 1.22–2.68), 2.82 (95% CI: 2.01–3.96), and 1.45 (95% CI: 1.08–1.94) in 2001, 2005, and 2010, respectively.

Conclusion

Although population-wide progress has been made in participation in cervical cancer screening over the 12-year period, socioeconomic status remained an important factor in reducing compliance with cancer screening.

Keywords

Cervical cancer Screening Socioeconomic status Disparity

Background

Cervical cancer is one of the most preventable cancers in the world but it is the eighth leading cause of cancer-related deaths in Korea [1, 2]. Regular Papanicolaou (Pap) tests are an excellent diagnostic tool for detecting not only cancerous, but also precancerous cells, both of which can be removed [35]. Previous observational studies have consistently shown dramatic reductions in the cervical cancer mortality rate after the implementation of population-based screening programs [6, 7].

Since its introduction in the 1940s, the Pap smear has been associated with sharp declines in cervical cancer incidence and mortality [8, 9]. In Korea, the age-adjusted incidence of cervical cancer dropped from 18.6 (per 100,000) in 1999 to 12.0 in 2009, and its mortality declined from6.2 per 100,000 in 1995 to 3.8 per 100,000 in 2009 [1, 10].

In Korea, there are currently three main cancer screening programs [10], namely the National Cancer Screening Program (NCSP), the Korea National Health Insurance (NHI) program, and screening services voluntarily provided by independent medical facilities. In 1999, the Korean government created the NCSP and established a 10-year plan for cancer control [11]. The NCSP provided free cancer screening services for stomach, breast, and cervical cancers to medical aid recipients between 1999 and 2001 [12]. In 2002, coverage of free cancer screening was expanded to NHI beneficiaries within the lowest 20% income bracket, and in 2003, those within the lowest 30% income bracket were included in the target population. From 2005, the NCSP expanded coverage of free screening for stomach, breast, cervical, liver and colorectal cancer to Medical Aid recipients, and the NHI included beneficiaries who were within the lower 50% of income earners [13].

Despite these public health efforts, the rate of cervical cancer screening may not be uniform across groups with different socioeconomic status. Previous studies suggested that socioeconomic disparities existed in cancer screening rates [14, 15], and, in particular, global evidence suggested that the cervical cancer screening rate was influenced by socioeconomic factors as well as demographic factors such as race [1621]. Studies in the United States and Korea also showed that socioeconomic disparities continued in cervical cancer screening participation, though there has been an improvement in overall screening rate [14, 22].

Although the above-mentioned studies are informative in identifying important factors influencing cervical cancer screening, they are either cross-sectional studies or not nationally representative, or their study periods were in the late 1990s or the early 2000s. To achieve timely and challenging objectives in public health, such as improvement in cancer screening rates with a reduction in socioeconomic disparities, it is necessary to monitor the long-term trend. Therefore, the objective of this study was to investigate the changes in cervical cancer screening rate over the 12-year period from 1998 to 2010 in a nationally representative sample of Korean women, and to examine whether socioeconomic disparities in cervical cancer screening rates have been reduced over this period.

Methods

Data source and subjects

This study used data from the 1998–2010 Korea National Health and Nutrition Examination Survey (KNHANES). The KNHANES is a nationally-representative study managed by the Korean Ministry of Health and Welfare. Participants were enrolled from the household registry using a stratified multistage probability design. The KNHANES consists of four parts: a health interview survey, a health behavior survey, a physical examination, and a nutritional survey. Trained interviewers conducted all surveys and trained healthcare professionals conducted all physical examinations. All participants provided informed consent before participation in the KNHANES.

There were 211,116 women aged 30 years or older who completely answered the health behavior survey between 1998 and 2010. Women who did not provide information about cervical cancer screening or nutrition or who did not have an additional physical examination were excluded from the study. Finally, a total of 17,105 women (2,725 in 1998, 1,622 in 2001, 2,596 in 2005, 2,944 in 2008, and 2,737 in 2010) were included in the analysis.

Independent variables and outcome variables

From 1998 to 2001, participants were asked, “Have you ever been screened for cervical cancer?” and answers were recorded as either yes or no. From 2005 to 2010, participants were asked, “When was the last time you were screened for cervical cancer?” and answers were recorded as either never, less than 1 year ago, 1–2 years ago, or more than 2 years ago. According to the Korean NCSP guidelines, women 30 years of age and older should receive a Pap smear test every 2 years. In the present study, the outcome variable was whether participants adhered to the Korean NCSP guidelines. We defined participants as not adhering to the NCSP guidelines if they reported never being screened for cervical cancer or were examined more than 2 years prior to completing the questionnaire.

Based on a literature review, we chose several variables as possible factors related to screening participation. Thus, our primary variables of interest were socioeconomic factors, including education, household income, and occupation. Other variables included in the study were age, marital status, health insurance type, health status (limitation in general activities and perceived health status), and health behavior (smoking and obesity). Educational status was divided into three groups: none or elementary school, middle school to high school, and university or higher. Household income, provided by the KNHANES, was calculated by dividing the monthly household income by the square root of the household size, and grouped into four household income quartiles. Occupation was categorized as “white collar (manager, professional level, office workers, service workers, sales)”, “blue collar (agriculture, fishery, technicians, mechanics, assemblers, simple labor)”, and “others (student, housewife, unemployed)”. Marital status was “married” vs. “not married”. Health insurance type was categorized as national health insurance for the self-employed, national health insurance for those not self-employed, and being in receipt of Medical Aid. Health status and health behavioral factors included limitation in general activities (yes, no), perceived health status (good or regular vs. bad), smoking (non, ex or current), and body mass index (BMI), categorized as < 18.5, 18.5– < 23, 23– < 25, and ≥ 25 kg/m2 according to the guidelines provided by the World Health Organization West Pacific Region (2000).

Statistical analysis

The KNHANES was based on a complex sample design. Therefore, all statistical analyses were performed using the survey procedure of SAS version 9.2 (SAS Inc., Cary, NC, USA), specifically designed to analyze such sample survey results. In the survey procedure, information pertaining to complex sample designs such as stratification, clustering, and unequal weighting is combined to analyze the parameters.

We used descriptive statistics for the characteristics of the subjects, and reported the number and percentage for each variable. The participation rates in cervical screening were calculated according to all variables. The odds ratios (ORs) and 95% confidence intervals (CIs) were calculated to measure the strength of the association between the measured variables and screening participation. We regarded a p-value of less than 0.05 as statistically significant.

Results

Baseline characteristics and participation in cervical cancer screening

The characteristics of the study population and participation rate in cervical cancer screening from 1998 to 2010 are summarized in Table 1. In this study, the majority of women were married, and enrolled in the NHI program. Most women reported no limitation in their daily activities and were non-smokers. The cervical cancer participation rates increased from 40.5% in 1998 to 52.5% in 2010.
Table 1

Basic characteristics of the study population and participation rate in cervical cancer screening in women ≥30 years, 1998–2010

Variables

1998

2001

2005

2008

2010

 

Total

%

Screen

%

p-value

Total

%

Screen

%

p-value

Total

%

Screen

%

p-value

Total

%

Screen

%

p-value

Total

%

Screen

%

p-value

Age (years)

                         

30-39

715

30.1

362

50.9

<.0001

369

23.6

191

50.6

<.0001

710

29.7

362

51.3

<.0001

707

26.4

363

51.8

<.0001

617

24.1

317

51.9

<.0001

40-49

641

24.9

358

55.9

 

373

23.8

217

58.8

 

709

27.7

421

59.0

 

663

28.1

393

60.2

 

556

26.6

340

61.1

 

50-59

557

18.5

219

39.0

 

310

20.1

132

43.9

 

469

17.5

217

44.1

 

562

20.6

312

54.3

 

623

22.3

385

60.8

 

60-69

497

15.6

101

21.6

 

315

18.3

79

26.3

 

397

13.1

123

34.2

 

536

13.4

208

40.7

 

502

13.6

250

49.1

 

70+

315

11.0

25

6.4

 

255

14.1

27

9.1

 

311

11.9

43

14.7

 

476

11.5

86

17.9

 

439

13.4

116

26.3

 

Education

                         

None or elementary school

1,414

45.5

381

26.1

<.0001

751

44.3

186

25.4

<.0001

897

32.1

260

29.9

<.0001

1,138

29.9

375

35.5

<.0001

1,294

43.8

563

43.6

<.0001

Middle or high school

1,089

44.6

564

52.0

 

688

44.2

360

53.1

 

1,224

48.8

641

52.1

 

1,239

48.6

643

51.9

 

1,023

40.9

588

59.4

 

University or higher

222

10.0

120

54.4

 

183

11.6

100

53.4

 

475

19.1

265

55.2

 

567

21.5

344

62.6

 

420

15.3

257

59.5

 

Marital status

                         

Married

2,073

77.2

944

46.8

<.0001

1,181

73.0

539

45.8

<.0001

1,984

76.0

999

50.6

<.0001

664

18.6

199

32.0

<.0001

2,202

81.3

1,202

55.2

<.0001

not married

652

22.8

121

19.1

 

441

27.0

107

27.6

 

612

24.0

167

29.6

 

2,280

81.4

1,163

53.2

 

535

18.7

206

40.8

 

Household income

                         

Quartile 1

770

24.6

184

24.8

<.0001

509

30.4

109

23.8

<.0001

666

23.0

187

27.6

<.0001

694

17.0

220

33.8

<.0001

635

20.6

252

40.7

<.0001

Quartile 2

643

22.0

247

39.6

 

407

23.8

175

44.0

 

624

25.6

255

40.8

 

756

27.3

328

47.5

 

685

27.1

336

51.5

 

Quartile 3

708

27.6

345

49.0

 

347

22.4

170

49.1

 

669

26.5

343

51.2

 

759

28.1

382

50.9

 

710

27.3

391

55.0

 

Quartile 4

604

25.8

289

47.0

 

359

23.5

192

52.1

 

637

24.9

381

61.0

 

735

27.6

432

58.9

 

707

25.0

429

60.6

 

Health insurance type

                         

NHI (self-employed)

1,482

53.7

597

41.3

<.0001

748

46.2

296

40.0

0.002

1,066

42.5

451

44.0

0.064

1,156

39.9

524

48.4

0.001

932

36.7

446

49.8

0.252

NHI (employee)

1,120

42.3

453

42.3

 

780

48.1

333

44.0

 

1,412

53.5

671

47.5

 

1,662

56.9

805

51.1

 

1,712

59.6

919

54.0

 

Medical Aid

123

4.0

15

9.6

 

94

5.7

17

22.1

 

118

4.0

44

35.5

 

126

3.2

33

28.0

 

93

3.8

43

56.1

 

Occupation

                         

white collar

481

20.3

236

48.9

<.0001

312

19.4

165

50.5

0.002

663

25.8

352

52.7

0.003

628

23.9

344

54.0

0.024

670

27.7

369

55.0

0.233

blue collar

836

23.8

290

35.4

 

324

20.1

124

40.9

 

545

18.8

232

43.6

 

751

21.4

315

45.3

 

569

21.4

282

54.0

 

others

1,408

55.9

539

39.6

 

986

60.6

357

37.8

 

1,388

55.4

582

42.9

 

1,562

54.7

700

48.7

 

1,498

50.8

757

50.5

 

Limitation in general activities

                         

Yes

709

27.4

293

44.5

0.013

201

12.8

62

33.7

0.045

349

12.5

104

30.8

<.0001

743

21.4

279

44.1

0.019

929

31.3

433

49.1

0.024

No

2,016

72.6

772

38.9

 

1,421

87.2

584

41.9

 

2,247

87.5

1,062

47.7

 

2,201

78.6

1,083

50.7

 

1,808

68.7

975

54.1

 

Perceived health status

                         

Good or regular

1,675

63.9

699

43.0

0.001

1,014

63.3

456

45.5

<.0001

1,807

70.7

891

49.8

<.0001

1,993

71.9

956

50.2

0.165

2,029

74.8

1,093

54.1

0.016

Bad

1,050

36.1

366

36.0

 

608

36.7

190

32.9

 

789

29.3

275

35.3

 

951

28.1

406

46.8

 

708

25.2

315

47.8

 

Smoking

                         

Non-smoker

2,445

89.7

1,004

42.2

<.0001

1,499

92.1

618

42.4

0.001

2,375

90.8

1,101

46.9

0.000

2,644

88.7

1,248

49.9

0.094

2,503

90.1

1,299

52.7

0.026

Ex-smoker

72

3.0

15

23.4

 

24

1.6

4

17.7

 

104

4.3

38

53.9

 

148

5.5

61

49.7

 

133

5.4

72

60.1

 

Current smoker

208

7.2

46

25.4

 

99

6.2

24

25.0

 

117

4.9

27

28.4

 

152

5.8

53

38.8

 

101

4.5

37

40.7

 

Body mass index (kg/m 2 )

                         

<18.5

106

3.8

24

26.8

0.007

65

3.7

21

31.0

0.165

81

3.0

35

42.2

0.066

123

4.3

50

40.9

0.030

101

3.7

45

45.5

0.000

18.5 ≤ 23

1,076

40.4

437

43.1

 

601

37.9

257

43.4

 

4,050

41.3

493

48.0

 

1,209

43.1

580

52.3

 

1,150

42.5

624

55.8

 

23 ≤ 25

637

23.6

262

41.8

 

399

24.4

160

42.3

 

637

23.7

292

47.4

 

683

23.1

320

50.4

 

640

23.5

358

56.6

 

25≤

906

32.2

342

37.7

 

557

33.9

208

38.2

 

828

31.9

346

41.3

 

929

29.5

412

45.2

 

846

30.3

381

45.6

 

total

2,725

100.0

1,065

40.5

 

1,622

100.0

646

40.9

 

2,596

100.0

1,166

45.5

 

2,944

100.0

1,362

49.3

 

2,737

100.0

1,408

52.5

 

NHI, National health insurance.

Women with the lowest educational status had a participation rate of 26.1% in 1998 and 43.6% in 2010. However, women with the highest educational status reported a higher participation rate of 54.4% in 1998 and 59.5% in 2010. Women in the lowest household income group had a participation rate of 24.8% in 1998 and 40.7% in 2010. Women in the highest household income group had a participation rate of 47.0% in 1998 and 60.6% in 2010.

Figure 1 indicates that the gaps between the highest and lowest educational status and income groups narrowed during the 12 years in Korea.
https://static-content.springer.com/image/art%3A10.1186%2F1471-2458-13-553/MediaObjects/12889_2012_Article_5478_Fig1_HTML.jpg
Figure 1

Cervical cancer screening rate by education and household income and occupation, 1998–2010.

Factors associated with cervical cancer screening participation

Table 2 shows the results of the multivariate logistic regression analysis for cancer screening. Of the socioeconomic factors considered, higher educational level was found to be associated with a higher OR in 1998, 2001, 2008, and 2010. Compared with the lowest educational level, the adjusted ORs of the highest education level were 1.56 (95% CI: 1.05–2.30), 1.90 (95% CI: 1.26–2.87), and 1.73 (95% CI: 1.12–2.66) in 1998, 2008, and 2010. A higher household income was also found to be associated with a higher OR in 2001, 2005, and 2010. Compared with the lowest household income level, the adjusted ORs of the highest household income level were 1.80 (95% CI: 1.22–2.68), 2.82 (95% CI: 2.01–3.96), and 1.45 (95% CI: 1.08–1.94) in 2001, 2005, and 2010, respectively.
Table 2

Factors associated with cervical cancer screening among women ≥30 years, 1998–2010

Variables

1998

2001

2005

2008

2010

Education

          

None or elementary school

1.00

 

1.00

 

1.00

 

1.00

 

1.00

 

Middle or high school

1.43

(1.13-1.82)

1.67

(1.18-2.38)

1.15

(0.82-1.61)

1.24

(0.93-1.66)

1.71

(1.24-2.35)

University or higher

1.56

(1.05-2.30)

1.56

(0.94-2.61)

1.00

(0.64-1.56)

1.90

(1.26-2.87)

1.73

(1.12-2.66)

Household income

          

Quartile 1

1.00

 

1.00

 

1.00

 

1.00

 

1.00

 

Quartile 2

1.22

(0.92-1.62)

1.65

(1.16-2.34)

1.39

(1.00-1.93)

1.09

(0.82-1.46)

1.12

(0.84-1.49)

Quartile 3

1.52

(1.11-2.07)

1.72

(1.15-2.59)

1.93

(1.44-2.59)

1.05

(0.78-1.40)

1.21

(0.89-1.66)

Quartile 4

1.31

(0.95-1.81)

1.80

(1.22-2.68)

2.82

(2.01-3.96)

1.34

(0.97-1.84)

1.45

(1.08-1.94)

Occupation

          

white collar

1.00

 

1.00

 

1.00

 

1.00

 

1.00

 

blue collar

0.92

(0.69-1.23)

1.08

(0.70-1.66)

1.01

(0.72-1.41)

1.01

(0.78-1.32)

1.29

(0.95-1.76)

others

1.12

(0.87-1.44)

1.02

(0.79-1.35)

1.04

(0.79-1.35)

1.18

(0.93-1.49)

1.20

(0.92-1.57)

Results are presented as adjusted odds ratios and (95% confidence intervals), and adjusted for age, marital status, health insurance type, limitation in general activities, perceived health status, smoking, and body mass index.

Among the other variables, age was a statistically significant factor which was inversely related to cervical cancer screening during 1998–2010, suggesting that older women were less likely to participate in screening. Although marital status, health insurance type, and smoking status were statistically significant factors in one or two study years, their significance was either not as strong as socioeconomic status or somewhat inconsistent.

Discussion

The objective of this study was to examine the change in rates of participation in cervical cancer screening among Korean women from 1998 to 2010, and to test whether socioeconomic disparities in cervical cancer screening decreased, stayed the same, or worsened. We observed that the participation rate of Korean women 30 years or older in cervical cancer screening was 40.5% in 1998, 40.9% in 2001, 45.5% in 2005, 49.3% in 2008, and 52.5% in 2010. Although this suggests that there has been steady progress in improving the cervical cancer screening rate over the past decade, there is certainly room for improvement because the rate is still around 50%, significantly lower than in other economically developed countries. There were particularly low rates of participation in women with the lowest educational level (26.1% in 1998, 25.4% in 2001, 29.9% in 2005, 35.5% in 2008, and 43.6% in 2010), and in women with the lowest household income (24.8% in 1998, 23.8% in 2001, 27.6% in 2005, 33.8% in 2008, and 40.7% in 2010). Importantly, the participation rates of women in the lowest education and income groups markedly improved over the years, and the gaps with the highest education and income groups were reduced. The results of our study suggest important policy implications for policymakers to improve participation rates and to further reduce the difference in rates according to socioeconomic status.

Previous studies have found educational level to be a significant predictor of cervical cancer screening participation [23, 24], and educational level has a huge effect on knowledge of the advantages of participation in cervical cancer screening after controlling for other covariates [25, 26]. The results of our study are consistent with previous studies in showing that educational level was significantly associated with participation in cervical cancer screening among Korean women, and, more importantly, that the association lasted over a decade. It is worth noting that two previous studies found that disparities in cancer screening by household income were improved, but there was no improvement for disparities in cancer screening by education level among Korean women [27, 28].

Previous studies also found that household income was a significant predictor of cervical cancer screening participation [28, 29]. It was suggested that to improve cancer screening participation rates in lower income individuals, a primary health care intervention such as an organized program of cervical screening that focuses on deprived groups is needed [30]. Therefore, it is important to keep monitoring how public health policies impact on participation rates over time, such as that which expanded the scope of free cervical cancer examinations to women in the lower 50% income bracket of households [13].

Our study has several limitations. First, although this study examined data in a 12-year study period, it was based on pooled cross-sectional data, from which we cannot detect a causal relationship. Second, the KNHANES is based on self-reported responses to participation in cervical cancer screening, which may raise acquiescence bias or recall bias. To minimize recall bias in collecting the data, the KNHANES was conducted by educated and trained interviewers. However, we acknowledge that the survey was unable to perform a cross-check with medical records. Therefore, recall and acquiescence (social desirability) bias can remain, and may result in misclassification. Although misclassification can be either random or nonrandom, we believe that, in a large nationwide survey such as KNHANES, it was random. Therefore, potential recall bias may lead to an association toward null, and an underestimate of the true association. A previous study also pointed out a similar possibility of underestimation of the actual participation rate [3133]. Finally, other factors that may be significant determinants of cervical cancer screening participation were not included in the current study. For example, there was no control for family history of cervical cancer, age at first sexual intercourse, and knowledge and attitudes about cervical cancer risk factors and benefits of the Pap test.

Conclusion

In conclusion, in the analysis of nationally representative data over a decade, we found that there was an increase in participation in cervical cancer screening programs by Korean women from 40.5% in 1998 to 52.5% in 2010, though the rate remained lower than in other developed countries. We also observed that despite the overall increase in screening rates, socioeconomic disparities continued to exist. Although screening rates in women with the lowest educational levels and household incomes improved over the period, they remained lower than in women of the highest education and income groups.

These results demonstrate the need for more aggressive interventions and policies to improve participation in cervical cancer screening especially for those at a lower income and education level. Analyses of cervical cancer screening rates by measures of household income, educational level, and other factors over the long term may help policy-makers to better direct their resources to those of greatest need. Ensuring that free cervical cancer screening programs or other public health programs remain available for women in the lower income groups can lead us closer to national screening goals, yet policies or campaigns still need to address disparities in cervical cancer screening according to educational level.

Declarations

Acknowledgments

This study was funded by a grant from the Korean Foundation for Cancer Research (7-2011-0489).

Authors’ Affiliations

(1)
Department of Public Health, Institute of Health Services Research, Yonsei University
(2)
Department of Preventive Medicine and Public Health, Institute of Health Services Research, College of Medicine, Yonsei University
(3)
Graduate School of Public Health, Institute of Health Services Research, College of Medicine, Yonsei University

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  34. Pre-publication history

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© Lee et al.; licensee BioMed Central Ltd. 2013

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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