Knowledge, attitudes, risk perception, and cancer screening behaviors among cancer survivors

Authors

  • Dong Wook Shin MD, MBA,

    1. Department of Family Medicine, Seoul National University Hospital, Seoul, Republic of Korea
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  • Young-Woo Kim MD, PhD,

    1. Center for Gastric Cancer, Research Institute & Hospital, National Cancer Center, Goyang, Republic of Korea
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  • Jae Hwan Oh MD, PhD,

    1. Center for Colorectal Cancer, Research Institute & Hospital, National Cancer Center, Goyang, Republic of Korea
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  • Seok Won Kim MD, PhD,

    1. Center for Breast Cancer, Research Institute & Hospital, National Cancer Center, Goyang, Republic of Korea
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  • Ki-Wook Chung MD, PhD,

    1. Center for Thyroid Cancer, Research Institute & Hospital, National Cancer Center, Goyang, Republic of Korea
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  • Woo Yong Lee MD, PhD,

    1. Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
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  • Jeong Eon Lee MD, PhD,

    1. Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
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  • Won Chul Lee MD, PhD,

    1. Department of Preventive, Medicine, College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea
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  • Eliseo Guallar MD, DrPH,

    1. Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
    2. Department of Medicine, Welch Center for Prevention, Epidemiology, and Clinical Research, Johns Hopkins Medical Institutions, Baltimore, Maryland
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  • Juhee Cho MA, PhD

    Corresponding author
    1. Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
    2. Department of Health, Behavior and Society, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
    3. Cancer Education Center, Samsung Comprehensive Cancer Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
    • Cancer Education Center, Samsung Comprehensive Cancer Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 Irwon-dong, Gangnam-gu, Seoul 135-710, Republic of Korea
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    • Fax: (011) 82 2 3410 6639


Abstract

BACKGROUND:

Knowledge, attitudes, and risk perception in relation to second primary cancer (SPC) screening and their impact on screening practices in cancer survivors are largely unknown.

METHODS:

A total of 326 cancer survivors who had completed primary treatment for cancer >1 year previously were recruited from 6 oncology care outpatient clinics in the Republic of Korea. Survivors' knowledge, attitudes, perceived risk, and screening practices were assessed along with sociodemographic, behavioral, and clinical characteristics. Multivariate logistic regression was used to examine behavioral factors associated with the completion of all appropriate SPC screening according to national guidelines.

RESULTS:

Approximately 37.7% of survivors had undergone all appropriate SPC screening tests. Survivors were found to have a high perceived risk of SPC, high perceived benefits of screening, and positive attitudes toward cancer screening. However, they had limited knowledge regarding SPC screening tests and few had received a recommendation from a physician to undergo SPC screening. Although there was no association found between perceived risk and positive attitudes with screening behavior, higher knowledge was noted to be significantly associated with the completion of all appropriate SPC screening (adjusted odds ratio, 1.81; 95% confidence interval, 1.03-3.33).

CONCLUSIONS:

In the current study, cancer survivors were found to have limited knowledge regarding second cancer screening tests, which may have resulted in lower rates of completion of screening practices in this population. Cancer 2011. © 2011 American Cancer Society.

With improved cancer survival, second primary cancer (SPC) is becoming an important health issue among a growing population of cancer survivors (11.1 million in the United States in 2005).1, 2 Cancer survivors are at an increased risk of developing cancers.3, 4 Because SPC is associated with increased mortality,5 reducing this risk is a major public health concern.

Screening for SPC has been recommended to facilitate early identification and to reduce the frequency of severe complications and morbidity in cancer survivors. Studies in the United States have found that cancer survivors were more likely to undergo cancer screening compared with people without cancer.6-8 Although a similar pattern was also observed in Korea, the absolute screening rates in cancer survivors were not optimal.9

Knowledge, attitudes, and risk perceptions facilitate the adoption of desirable health behaviors,10 and their role in cancer screening practices has been studied in the general population. Better knowledge,11, 12 a positive attitude,13 and perceived susceptibility14 were all found to be positively associated with cancer screening practices in the general population. The role of perceived risk of SPC has been studied in cervical cancer survivors,15 but there appears to be no other data regarding the role of knowledge and attitudes concerning SPC screening among cancer survivors.

Several reasons have been proposed to explain the higher screening rates noted among cancer survivors compared with the general population, including differences in health beliefs such as perceived risk, self-efficacy, and risk perceptions related to cancer screening.6-8, 16-18 However, the majority of studies have used secondary data such as Medicare claims7, 17 or national health surveys,6, 8, 9, 16, 18 with only limited ability to examine the attitudes and behaviors of cancer survivors in relation to SPC screening. The current study targeted a population of cancer survivors to specifically examine knowledge, attitudes, and risk perception in relation to SPC screening, and their impact on screening practices in cancer survivors.

MATERIALS AND METHODS

The current study was performed as the baseline (preintervention) survey for a multicenter randomized controlled trial (ClinicalTrials.gov ID: NCT00948337) to evaluate the effectiveness of educational material on SPC screening behaviors among survivors of stomach, colorectal, breast, and thyroid cancers. These cancers were selected because of their high incidence and 5-year survival rates in Korea (Table 1).19 Study participants were recruited in 2009 from 6 oncology care outpatient clinics located at 2 cancer centers in the Seoul metropolitan area.

Table 1. Incidence and 5-Year Relative Survival Rates of 4 Cancers in Korea
 Crude Incidencea5-Year Relative Survival Rate, %
 MaleFemaleMaleFemale
  • a

    Per 100,000 persons per year.

Stomach65.526.357.055.1
Colorectal39.622.266.762.4
Breast0.231.087.187.3
Thyroid5.835.095.798.5

Subjects were eligible to participate if they were ages 40 to 79 years; had a histologically confirmed diagnosis of cancer (TNM Stage I to III); had finished primary treatment for cancer at least 1 year before the time of study recruitment; had no evidence of disease recurrence, metastasis, or SPC; and had no evidence of hereditary cancer. We excluded cancer survivors with poor general performance status (Eastern Cooperative Oncology Group ≥3) or who were unable to read Korean. We approached 646 cancer survivors, 326 of whom (50.5%) agreed to participate in the study.

Measures and Outcomes

We developed a self-administered questionnaire using items derived from standard questions used in previous surveys of cancer screening behaviors.9, 16 The survey asked about sociodemographic factors known to be associated with screening practices, including age,20, 21 sex,22 marital status,18, 20 education,20, 21, 23 monthly household income,18, 24, 25 employment status,24 smoking status,21 alcohol consumption,25 and perceived health status.20-22 Information regarding the presence of comorbidities was also collected because the frequent medical encounters because of such conditions are associated with cancer screening practices23, 26 and included hypertension; dyslipidemia; diabetes; osteoarthritis; rheumatoid arthritis; and cerebrovascular, cardiovascular, chronic liver, lung, kidney, or gastrointestinal disease. Clinical variables, including the date of the primary cancer diagnosis, stage of disease at the time of diagnosis, and types of cancer treatment patients had received, were collected through the review of medical records.

To develop a questionnaire regarding cancer screening knowledge and attitudes, we conducted focus groups using semistructured interviews with 13 disease-free cancer survivors. Details of the methods used are described elsewhere.27 In brief, we conducted 3 focus group interviews using a predeveloped, semistructured interview guide. For the analysis, we used the standard qualitative research methods of transcribing, coding, displaying, verifying, and reducing the data. Recurrent issues were identified and then placed into thematic categories. A draft study questionnaire was created based on the findings from the interviews, and minor revisions were made based on the responses of a pretest subsample of 5 survivors. We found that survivors had difficulty in differentiating “second cancer screening” from “routine surveillance test.” They also believed that routine surveillance tests such as blood tests or chest x-rays would detect all possible diseases, including SPC. For attitudes toward screening, survivors perceived that cancer screening was beneficial not only for their own health but also for decreasing the burden of the disease in their family.

The final questionnaire for assessing knowledge concerning SPC screening thus included 5 true-false questions covering: 1) the occurrence of SPC, 2) the difference between a “routine surveillance test” and “second cancer screening,” 3) cancer screening needs and recommendation for cancer survivors, 4) risk of developing SPC, and 5) the meaning of routine surveillance tests (blood tests and chest x-rays). Participants were categorized as having appropriate knowledge if they responded correctly to at least 4 of the 5 questions concerning knowledge.

For assessing attitudes toward SPC screening, we used 6 questions regarding: 1) needs of cancer screening, 2) intention to undergo screening, 3) intention to undergo screening after a physician's recommendation, 4) perceived health benefits, 5) perceived benefits for the family, and 6) perceived benefit of cancer screening. Response choices were “strongly disagree,” “disagree,” “agree,” and “strongly agree.” Each response was assigned a numeric score (3 for strongly agree, 2 for agree, 1 for disagree, and 0 for strongly disagree) and the scores for all questions regarding attitudes were averaged for each participant. Participants were then considered to have a positive attitude if their average score was equal to or above the median sample score. Analyses using the scores as continuous variables or using alternative categorizations resulted in similar conclusions (data not shown).

To assess the perceived risk of developing a SPC, participants were asked “What would you say is your risk of getting another cancer compared with the cancer risk in the general population?” The response choices were “much lower,” “lower,” “same,” “higher,” and “much higher.” We then dichotomized participants into “higher/much higher risk” and “same/lower/much lower risk.”

Questions regarding screening practices addressed whether individuals had ever undergone examinations for breast cancer (mammogram or breast sonography), stomach cancer (endoscopy or upper gastrointestinal series), cervical cancer (Papanicolaou test), or colorectal cancer (fecal occult blood test, sigmoidoscopy, colonoscopy, or barium enema). Because patients had difficulty with the description of the various cancer screening tests,10 questions were simplified so that patients were not asked to identify specific types of screening tests (eg, “Have you ever had a stomach screening test? Stomach cancer screening tests include gastrofibroscopy or upper gastrointestinal series.”) and were presented with relevant pictures (eg, patients undergoing gastrofibroscopy). Screening questions were appropriate for the respondents' gender (eg, males were not asked about Papanicolaou tests).

A positive answer to any screening question was followed by questions about the timing of the most recent examination (<1 year, 1-2 years, 2-5 years, >5 years, or none). Because to our knowledge there is no consensus regarding the optimal cancer screening strategy in Korean cancer survivors, an operational definition of appropriate screening in the current study was developed based on the National Cancer Screening Program in Korea,28 but modified in consideration of other relevant cancer screening guidelines,29-32 epidemiological evidence from cancer survivors4, 33 and Asians,19, 34, 35 and current cancer screening practices in Korea (Table 2).36 Recommendations for screening from physicians were also ascertained for cancer screening behaviors.15, 37, 38

Table 2. Korean Recommendations and Operational Definition of Appropriate Cancer Screening Used in the Current Study
 Stomach Cancer ScreeningColorectal Cancer ScreeningBreast Cancer ScreeningCervical Cancer Screening
  1. UGIS indicates upper gastrointestinal series; FOBT, fecal occult blood testing.

National Cancer Screening Guideline29• Males and females aged ≥40 y• Males and females aged ≥50 y• Females aged ≥40 y• Females aged ≥20 y
 • Every 2 y• Every 5-10 y• Every 1-2 y• Every y
 • Gastrofibroscopy or UGIS• Colonoscopy or barium enema and sigmoidoscopy• Mammogram and clinical breast examination• Papanicolaou test
  • Earlier and more frequent screening for high-risk groups  
National Cancer Screening Program28• Males and females aged ≥40 y• Males and females aged ≥50 y• Females aged ≥40 y• Females aged ≥30 y
 • Every 2 y• Every y• Every 2 y• Every 2 y
 • Gastrofibroscopy or UGIS• FOBT; if positive, colonoscopy or barium enema follows• Mammogram and clinical breast examination• Papanicolaou test
Lifetime health promotion for Koreans30• Males aged ≥40 y and females aged ≥50 y• Males and females aged ≥50 y• Females aged ≥40 y• Females with a history of sexual contact
 • Every 2 y• Gastrofibroscopy or UGIS• FOBT every y, or barium enema or sigmoidoscopy every 5 y, or colonoscopy every 10 y• Every 2 y (ages 40–49 y) or every 3 y (aged ≥50 y)• Every 3 y
   • Mammogram• Papanicolaou test
Screening guideline for 7 major cancers31• Males and females aged ≥40 y• Males and females aged ≥50 y• Females aged ≥40 y• Females aged ≥20 y
 • Every 2 y• Every 5-10 y• Every 1-2 y• Every y
 • Gastrofibroscopy or UGIS• Colonoscopy or barium enema and sigmoidoscopy• Mammogram and clinical breast examination• Papanicolaou test
  • Earlier and more frequent screening for high-risk groups  
Other considerations • Korean male cancer survivors have 4.0 times the risk of colorectal cancer compared with the general population4• Korean women have a peak incidence of breast cancer in their 40s19 
  • Colonoscopy every 3 y has been suggested as the most cost-effective strategy for male cancer survivors33• Asian women have a high prevalence of dense breasts34, 35 
   • Breast sonography is commonly practiced in combination with or as a replacement for mammography in Korea35 
Operational definition of appropriate cancer screening used in the current study• Within 2 y• Within 2 y• Within 2 y• Within 2 y
 • Gastrofibroscopy or UGIS• FOBT or sigmoidoscopy or colonoscopy or barium enema• Mammography or breast sonography• Papanicolaou test

Statistical Analysis

We used “completion of all appropriate screening” as the study outcome to examine the relation between knowledge, attitudes, risk perception, and screening. Cancer survivors who had had the specific cancer that the screening aimed to detect were excluded from each calculation.8 Descriptive statistics were used to report screening practices of cancer survivors, and their knowledge, attitudes, and risk perception regarding SPC screening. We used multivariate logistic regression models to examine the association between different behavioral factors and the study outcome. Missing data were <1% for all variables except for income (9 cases; 2.8%), most likely because income is considered by Koreans as a private and sensitive issue. The number of cases included in the final multivariate model (excluding cases with any missing data) was 306 from the total sample of 326 (93.9%). All analyses were conducted using SAS 9.1.3 statistical software (SAS Institute Inc, Cary, NC).

RESULTS

Study Population

Colorectal cancer survivors comprised the largest group of study participants, followed by survivors of breast, stomach, and thyroid cancer. The mean (standard deviation [SD]) age was 56.9 (10.0) years, 59.5% of study participants were female, and 88.9% were married. The mean time since diagnosis (SD) was 3.3 (2.1) years, approximately 45% of participants had stage I disease, and 56.6% had other chronic conditions. The majority of study participants (91.3%) reported “fair” or “good” health. Only 21.5% of survivors had ever received a recommendation from a physician regarding SPC screening (Table 3).

Table 3. Characteristics of the Study Participants
CharacteristicsAll Survivors N=326 (%)Stomach Cancer Survivors N=61 (%)Breast Cancer Survivors N=85 (%)Colon Cancer Survivors N=120 (%)Thyroid Cancer Survivors N=60 (%)Pa
  • SD indicates standard deviation; KRW, Korean won.

  • a

    The P value was determined using analysis of variance or the chi-square test as appropriate.

Mean age (±SD), y56.9 (10.0)60.9 (10.1)53.7 (8.7)59.8 (10.0)51.9 (7.8)<.01
Gender     <.01
 Female194 (59.5)17 (27.9)85 (100.0)38 (31.7)54 (90.0) 
 Male132 (40.5)44 (72.1)0 (0.0)82 (68.3)6 (10.0) 
Marital status     .45
 Single/divorced/separated36 (11.1)9 (15.3)8 (9.4)15 (12.5)4 (6.8) 
 Married287 (88.9)50 (84.7)77 (90.6)105 (87.5)55 (93.2) 
Level of education     .06
 <12 y87 (26.9)24 (40.0)19 (22.6)32 (26.7)12 (20.3) 
 ≥12 y236 (73.1)36 (60.0)65 (77.4)88 (77.3)47 (79.7) 
Monthly income, KRW     .03
 <3,000,000171 (53.9)39 (66.1)44 (52.4)65 (56.5)23 (38.9) 
 ≥3,000,000146 (46.1)20 (33.9)40 (47.6)50 (43.5)36 (61.0) 
Employment     .13
 Unemployed188 (58.2)35 (59.3)58 (68.2)65 (54.2)30 (50.8) 
 Employed135 (41.8)24 (40.7)27 (31.8)55 (45.8)29 (49.2) 
Mean time since diagnosis (±SD), y3.3 ± 2.13.5 ± 1.43.9 ± 2.73.0 ± 2.13.1 ± 1.5.08
Stage of disease     <.01
 I145 (44.5)40 (65.6)53 (62.4)28 (23.3)24 (40.0) 
 II82 (25.2)15 (24.6)22 (25.9)43 (35.8)2 (3.3) 
 III99 (30.4)6 (9.8)10 (11.8)49 (40.8)34 (56.7) 
Comorbidity     .89
 Yes (≥1)184 (56.6)34 (56.7)47 (55.3)71 (59.2)32 (53.3) 
 No141 (43.4)26 (43.3)38 (44.7)49 (40.8)28 (46.7) 
Current smoking status     .07
 Yes12 (3.8)3 (5.2)0 (0.0)8 (6.7)1 (1.7) 
 No305 (96.2)55 (94.8)81 (100.0)111 (93.3)58 (98.3) 
Current drinking status     <.01
 Yes66 (20.5)18 (30.5)7 (8.2)29 (24.4)12 (20.3) 
 No256 (79.5)41 (69.5)78 (91.8)90 (75.6)47 (79.7) 
Perceived health status     .13
 Very good27 (8.4)6 (10.0)7 (8.3)14 (11.8)0 (0.0) 
 Good111 (34.5)18 (30.0)32 (38.1)44 (37.0)17 (28.8) 
 Fair156 (48.4)29 (48.3)36 (42.9)55 (46.2)36 (61.0) 
 Poor27 (8.4)6 (10.0)9 (10.7)6 (5.0)6 (10.2) 
 Very poor1 (0.3)1 (1.7)0 (0.0)0 (0.0)0 (0.0) 
Had physician recommendation    .61
 Yes70 (21.5)14 (23.3)22 (25.9)23 (19.2)11 (18.3) 
 No255 (88.5)46 (76.7)63 (74.1)97 (80.8)49 (81.7) 

SPC Screening Practices

The overall percentages of screening within the last 2 years for cervical, stomach, breast, and colorectal cancer were 65.5%, 63.0%, 62.4%, and 35.0%, respectively. The screening rates varied by primary cancer type and gender, but only 37.7% of study participants had completed all appropriate cancer screening (Table 4).

Table 4. Screening Practice for Second Primary Cancer Among Cancer Survivors
 Stomach Cancer Survivors No. (%)Colorectal Cancer Survivors No. (%)Breast Cancer Survivors No. (%)Thyroid Cancer Survivors No. (%)All Survivors No. (%)
 Men N=44Women N=17Men N=82Women N=38N=85Men N=6Women N=54N=326
  • NA indicates not applicable.

  • a

    Patient underwent gastrofibroscopy or upper gastrointestinal series within 2 years.

  • b

    Patient underwent fecal occult blood test, colonoscopy, sigmoidoscopy, or barium enema within 2 years.

  • c

    Patient underwent mammography or breast sonography within 2 years.

  • d

    Patient underwent Papanicolaou test within 2 years.

Stomach cancer screeninga  52 (63.4)27 (71.1)51 (60.0)5 (83.3)32 (59.3)167/265 (63.0)
Colorectal cancer screeningb12 (27.3)8 (47.1)  35 (41.2)2 (33.3)15 (27.8)72/206 (35.0)
Breast cancer screeningcNA12 (70.6)NA18 (47.4) NA38 (70.4)68/109 (62.4)
Cervical cancer screeningdNA13 (76.5)NA16 (42.1)61 (71.8)NA37 (68.5)127/194 (65.5)
Complete cancer screening12 (27.3)7 (41.2)52 (63.4)12 (31.6)25 (29.4)2 (33.3)13 (24.1)123/326 (37.7)

Knowledge, Attitudes, and Risk Perception Regarding SPC Screening

With respect to knowledge assessment, the majority of survivors chose the correct answers for the questions regarding the occurrence of SPC (question 1; 92.6%), cancer screening needs (question 3; 82.0%), and risk of developing SPC (question 4; 85.8%). However, <60% of the participants knew the difference between a “routine surveillance test” and “second cancer screening” (question 2; 58.3%) or the meaning of routine surveillance tests (question 5; 56.7%).

Greater than 75% of cancer survivors strongly agreed that cancer survivors need screening for SPC and 73.8% also strongly agreed that screening is one of the best ways to deal with SPC. The majority of participants had the intention to undergo screening for SPC (94%), and agreed that cancer screening was beneficial for their health and their family (95%). The majority of participants considered themselves to be at much higher or higher risk of developing cancer than the general population (12.7% and 49.5%, respectively) (Table 5).

Table 5. Risk Perception, Knowledge, and Attitude Regarding Secondary Primary Cancer Screening
Knowledge
 YesNo   
  • a

    Yes /No in the parentheses denotes the intended (correct) answer.

Question 1. Cancer survivors can develop another cancer. (Yes)a300 (92.6)24 (7.4)   
Question 2. Periodic cancer screening is not necessary if cancer survivors take routine follow-up tests as recommended. (No)a133 (41.7)186 (58.3)   
Question 3. Cancer survivors have to receive cancer screening tests that are recommended to individuals without cancer. (Yes)a264 (82.0)58 (18.0)   
Question 4. Cancer survivors are at a higher risk of developing another cancer than individuals without cancer. (Yes)a279 (85.8)46 (14.2)   
Question 5. Routine tests done during the follow-up such as blood test or x-ray can detect all health problems including second cancers.(No)a140 (43.3)183 (56.7)   
Attitude
 Strongly AgreeAgreeDisagreeStrongly Disagree 
Question 1. I think cancer patients need to receive screening for another cancer.249 (76.4)74 (22.7)2 (0.6)1 (0.3) 
Question 2. I would like to receive screening for another cancer.211 (64.7)96 (29.4)13 (4.0)6 (1.8) 
Question 3. If a doctor recommended me, I would like to receive screening for another cancer.247 (75.8)72 (22.1)6 (1.8)1 (0.3) 
Question 4. I think receiving cancer screening will be good for my health.227 (70.1)82 (25.3)11 (3.4)4 (1.2) 
Question 5. I think receiving cancer screening will be good for my family.229 (70.2)81 (24.8)12 (3.7)4 (1.2) 
Question 6. Cancer screening is the best way to deal with another cancer.240 (73.8)76 (23.4)9 (2.8)0 (0) 
Risk Perception
 Much LowerLowerSameHigherMuch Higher
Question: Compared with the cancer risk in the general population, would you say that your risk of the second cancer is…12 (3.7)40 (12.4)70 (21.7)160 (49.5)41 (12.7)

Factors Associated With the Completion of All Appropriate SPC Screening

On multivariate-adjusted analysis, higher education (adjusted odds ratio [aOR], 2.04; 95% confidence interval [95% CI], 1.02-4.07), shorter time since diagnosis (aOR, 2.18; 95% CI, 1.25-3.80), presence of comorbidities (aOR, 2.05; 95% CI, 1.17-3.59), and higher knowledge (aOR, 1.85; 95% CI, 1.03-3.33) were found to be significantly associated with the completion of all appropriate screening. Survivors who had received a physician's recommendation for screening had increased odds of undergoing screening, but this difference was not found to be statistically significant (aOR, 1.39; 95% CI, 0.74-2.62). The association between perceived risk and SPC screening was not found to be statistically significant (Table 6).

Table 6. Factors Associated With Completion of All Appropriate Screening
CharacteristicsAll SPC ScreeningUnivariate OR (95% CI)Multivariate OR (95% CI)
NoYes
  1. SPC indicates second primary cancer; OR, odds ratio; 95% CI, 95% confidence interval; KRW, Korean won; GP, general population.

Age1.03 (0.98-1.03)1.01 (0.97-1.04)
Sex
 Female137 (70.6)57 (29.4)ReferenceReference
 Male66 (50.0)66 (50.0)2.40 (1.52-3.81)1.99 (0.90-4.38)
Marital status
 Unmarried28 (77.8)8 (22.2)ReferenceReference
 Married172 (59.9)115 (40.1)2.34 (1.03-5.32)2.06 (0.75-5.66)
Level of education
 <12 y66 (75.9)21 (24.1)ReferenceReference
 ≥12 y134 (56.8)102 (43.2)2.39 (1.37-4.17)2.04 (1.02-4.07)
Monthly income, KRW
 <3,000,000117 (68.4)54 (31.6)ReferenceReference
 ≥3,000,00080 (54.8)66 (45.2)1.79 (1.13-2.83)1.56 (0.88-2.78)
Employment
 Unemployed120 (63.8)68 (36.2)ReferenceReference
 Employed80 (59.3)55 (40.7)1.21 (0.77-1.91)0.92 (0.51-1.68)
Primary cancer type
 Stomach42 (68.9)19 (31.1)ReferenceReference
 Colorectal60 (70.6)25 (29.4)0.61 (0.36-1.04)1.03 (0.39-2.74)
 Breast56 (46.7)64 (53.3)2.85 (1.78-4.55)2.13 (0.96-4.75)
 Thyroid45 (75.0)15 (25.0)0.49 (0.26-0.92)0.77 (0.26-2.27)
Time since diagnosis, y
 >2145 (68.1)68 (31.9)ReferenceReference
 ≤258 (51.3)55 (48.7)2.02 (1.27-3.23)2.18 (1.25-3.80)
Stage of disease
 I93 (64.1)52 (35.9)ReferenceReference
 II47 (57.3)35 (42.7)1.32 (0.79-2.20)0.92 (0.47-1.81)
 III63 (63.6)36 (36.4)0.92 (0.56-1.50)0.81 (0.41-1.63)
Comorbidity, any
 No97 (68.8)44 (31.2)ReferenceReference
 Yes105 (57.1)79 (42.9)1.66 (1.05-2.63)2.05 (1.17-3.59)
Smoking, current
 No190 (62.3)115 (37.7)ReferenceReference
 Yes6 (50.0)6 (50.0)1.65 (0.52-5.24)1.15 (0.27-4.93)
Drinking, current
 No160 (62.5)96 (37.5)ReferenceReference
 Yes39 (59.1)27 (40.9)1.15 (0.66-2.00)0.83 (0.42-1.66)
Perceived health status
 Very good, good84 (60.9)54 (39.1)ReferenceReference
 Fair, poor, very poor117 (63.6)67 (36.4)0.89 (0.57-1.4)0.84 (0.49-1.44)
Physician recommendation for screening
 No165 (64.7)90 (35.3)ReferenceReference
 Yes37 (52.9)33 (47.1)1.64 (0.96-2.79)1.39 (0.74-2.62)
Perceived risk
 Lower than/same as the GP82 (67.2)40 (32.8)ReferenceReference
 Higher than the GP118 (58.7)83 (41.3)1.44 (0.90-2.31)1.37 (0.76-2.46)
Knowledge
 Low84 (68.3)39 (31.7)ReferenceReference
 High119 (58.6)84 (41.4)1.52 (0.95-2.44)1.85 (1.03-3.33)
Attitude regarding SPC screening
 Less positive87 (62.6)52 (37.4)ReferenceReference
 Positive116 (62.0)71 (38.0)1.02 (0.65-1.61)0.75 (0.43-1.32)

DISCUSSION

To our knowledge, the current study is the first to examine knowledge, attitudes, and risk perception regarding SPC screening among cancer survivors in a clinical practice setting. Although screening rates for breast, stomach, and cervical cancers were relatively high, only 37.7% of the survivors had undergone all appropriate screenings. Survivors knew that they were at a higher risk of cancer than the general population, acknowledged the benefits of screening, and demonstrated positive attitudes regarding cancer screening. However, they had limited knowledge regarding SPC screening, and <25% had ever received a recommendation for SPC screening from a physician.

In the current study, knowledge regarding SPC screening among cancer survivors was limited. Cancer survivors could not differentiate cancer screening from routine surveillance tests, and they often misunderstood the concept of screening. Approximately one-half of the survivors believed that cancer screening was not necessary if they underwent routine surveillance tests such as blood tests or chest x-rays. Such inadequate knowledge may keep the survivors from undergoing SPC screening regardless of their positive attitudes and risk perception, and it could explain why only 37.7% of survivors had completed all appropriate screening tests. Indeed, knowledge was found to be significantly associated with the completion of all appropriate screening, and survivors with high knowledge regarding SPC screening had approximately twice the odds of completing SPC screening compared with patients with low knowledge. Future studies should design and test interventions to increase SPC screening knowledge among cancer patients.

Physician recommendation was found to be one of the strongest factors affecting screening behavior and several studies have found positive relations between physician recommendation and screening practice.15, 37 In the current study, only 21.5% of study participants reported having received a recommendation for SPC screening, but 98% of the participants said that they would undergo cancer screening if physicians recommended it. The low screening rates in the current study may thus be in part because of a lack of physician recommendation. Cancer survivors have a high level of trust in physicians, and the survivors' willingness to comply with physicians' recommendations appears to provide excellent opportunities to modify cancer screening behaviors.

Oncologists have multiple competing demands, including their primary role in the follow-up for disease recurrence and the management of cancer-related symptoms. Studies have demonstrated that survivors who visited both oncologists and primary care physicians received more cancer screening than those who visited only the oncologists.17, 26 A shared care model between the oncologist and primary care provider would be an ideal model with which to promote the provision of currently underused primary and preventive services, including screening for SPC.39 However, further research is warranted concerning the discordant expectations among patients and physicians with respect to the roles of primary care physicians and oncologists in cancer survivorship care.40

Previous studies have found inconsistent associations between perceived risks and benefits and screening practices.15, 16 Although some studies have found that increased perceived vulnerability among cancer survivors resulted in increased screening,15 Mayer et al found no association in an analysis of the 2003 US Health Information National Trends Survey (HINTS).16 In the current study, perceived risk and screening practice were not found to be significantly associated. This may be because of the highly positive attitude toward cancer screening of the population,16 which prevents it from being a discriminative factor.

There are several limitations to the current study. First, the assessment of cancer screening practices was based on participants' self-report. Although we used carefully phrased questions to maximize accuracy, it is possible that survivors with less knowledge may have also had more difficulty understanding the questions correctly or may have undergone screening tests without realizing that they were performed for screening purposes. Second, the questionnaire used to assess knowledge, attitudes, and risk perception had not been formally tested for validity and reliability before administration. The Cronbach α of the attitude and knowledge scales was .81 and .27, respectively. The low Cronbach α of the knowledge scale most likely reflects the heterogeneity of the items41 and the lack of familiarity of survivors with the topic.42 Third, our participants were recruited from 2 major cancer centers in a metropolitan area and may not be representative of cancer survivors in Korea. Participants in the current study would be better educated and have a higher income compared with the general Korean population. Furthermore, cancer survivors in general may have lower risk perception, lower knowledge, and less positive attitudes toward SPC screening compared with the study participants. Fourth, to the best of our knowledge there are no specific guidelines for cancer screening in cancer survivors, and we adapted general guidelines from different organizations in Korea to define appropriate cancer screening (Table 2). Because different practitioners may follow different guidelines, our analysis may underestimate the proportion of patients who are following other recommendations for screening. This is particularly important for colorectal cancer screening, because the age at which to initiate screening and the interval between screening visits vary across recommendations. Indeed, this may contribute to the lower proportion of patients with appropriate screening for colorectal cancer according to our operational definition. Finally, we had a limited sample size, and some positive associations could not be confirmed because of insufficient statistical power.

Cancer survivors face multiple challenges after primary cancer treatment including disease recurrence, metastasis, and SPC. In this complex situation, it is important to address issues related to SPC along with other long-term care and promote SPC screening practices among cancer survivors. The data from the current study indicated that cancer survivors had positive attitudes toward cancer screening and that they understood that they could be at higher risk of developing a SPC. However, cancer survivors were found to have limited knowledge regarding SPC screening tests and few had received a recommendation from their physician about SPC screening, which likely resulted in lower SPC screening rates. Indeed, the results of the current study support the theory that poor knowledge and understanding of SPC screening may be a limiting factor in screening practices among cancer survivors. Therefore, the current study data demonstrate substantial potential for physician and patient education in SPC screening, and provide a firm basis for designing and testing educational interventions to improve screening among cancer survivors.

CONFLICT OF INTEREST DISCLOSURES

Supported by National Cancer Center Grant No. 0710422-3.

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