Factors related with colorectal and stomach cancer screening practice among disease-free lung cancer survivors in Korea

Although advanced stage lung cancer has a poor prognosis, [ 1] early stage lung cancer can be treated with surgical resection, resulting in an improved prognosis [ 2, 3]. Recently, the US Preventive Services Task Force (USPSTF) recommended annual screening for lung cancer, using low dose computed tomography (CT) for individuals at a high risk for this disorder [ 4]. Furthermore, the clinical practice of low dose CT scanning as an early detection tool, as well as advances in cancer treatment, could lead to an increased number of lung cancer survivors [ 3, 4].

Previous studies have reported that lung cancer patients were at an increased risk for second primary cancers (SPCs) [ 5, 6]. For second primary gastrointestinal cancers, a recent study reported that early stage lung cancer patients had approximately a 40% increased risk of colorectal and stomach cancer than the general population [ 6]. The Global Burden of Disease Study in 2017 has demonstrated that colorectal cancer and stomach cancer are ranked within global top 5 cancers, [ 7] colorectal cancer screening and stomach cancer screening are introduced in several countries [ 8– 10]. Cancer survivors were recommended to adhere routine age- and sex-appropriate cancer screening guideline in general population [ 11– 13]. Especially, as colorectal cancer is the most common cancer, and stomach cancer remains the second common cancer in Korea, [ 14] continued surveillance program regarding gastrointestinal cancer screening for Korean lung cancer survivors will be needed. However, little is known about the gastrointestinal cancer screening practices in lung cancer survivors. The aim of our survey was to determine the patterns of screening for colorectal and stomach cancer screening and related factors in lung cancer survivors who were disease free in Korea. We hypothesized that not only low social-demographic status but also lack of physicians’ advice for SPC screening or patients’ misperception about their risk of SPC would have negative impacts on the gastrointestinal cancer screening behaviors in lung cancer survivors.

Among the potentially eligible population, 126 (6.1%) had died, 290 (14.2%) could not be contacted in spite of multiple attempts. Excluded from this study were patients whose cancer had recurred at the time of the survey. All participants provided written informed consent. Of the 1633 contacted patients, 727 (35.5%) refused to participate, and 906 (44.2%) consented to participate. Among the respondents, 76 patients had cancer which had recurred, or were receiving cancer therapy at the time. One subject <40 years of age was excluded. The analysis included 829 lung cancer survivors ≥40 years of age.

The mean age of 829 lung cancer survivors was 62.9 years (40–78 years). Of these, 44.2% had no more than a 6th grade education, and 63.1% was diagnosed as stage I lung cancer. Among disease-free lung cancer survivors, 40.7% reported receiving physician advice to screen for other cancers. About one out of ten reported a perception that they had a lower risk of other cancers than the general population, and 60.1% believed that they had a higher risk of other cancers than general population (Table 1). When we compared the characteristics of the participants and non-participants among1633 contacted patients, responders were more likely to be men and to live in metropolitan areas than non-participants (Additional file 2: Table S1).

The proportions for receiving appropriate stomach cancer screening and colorectal cancer screening were 22.7 and 26.1%, respectively (Fig. 1). Both male and female lung cancer survivors showed similar trends of SPC cancer screening.

Our study showed that colorectal and gastric cancer screening practices among lung cancer survivors was less than optimal. In addition, half of these patients did not recall receiving advice from their physicians about SPC screening. Lack of a physicians’ advice for SPC screening and lower educational status might have negative impact on the gastrointestinal cancer screening rates of lung cancer survivors.

Because lung cancer survivors have an increased risk of colorectal and stomach cancer development, [ 5, 6] following the recommendations of gastrointestinal cancer screening for the average risk population should be needed at a minimum. However, our study showed that less than 30% of disease-free lung cancer survivors adhered to these colorectal and stomach screening recommendations. Several previous studies [ 20, 21] and one recent meta-analysis [ 22] reported that many cancer survivors did not receive screening tests recommended for the detection of SPCs, although cancer survivors received more frequent screening for cancers than non-cancer controls. These findings emphasized the need to identify effective methods to increase cancer screening practices for cancer survivors. Several interventions, such as reminders, small media, and face-to-face education have been reported to increase screening rates in general population [ 23]. However, little is known about whether these interventions of increasing appropriate knowledge could lead to increased SPC screening among cancer survivors. Furthermore, an interventional trial using educational materials to increase knowledge about SPC screening reported no increase in actual cancer screening for cancer survivors [ 24].

The present study showed that a lack of recommendation for SPC screening from physicians might have a negative impact on the colorectal and stomach cancer screening behaviors among lung cancer survivors. Similarly, a previous study reported that cervical cancer survivors who received, to whom their health care providers had recommended other cancer screening, were more likely to receive breast cancer screening [ 25]. After experiencing cancer, survivors usually have high levels of trust in their physicians, [ 26, 27] and physicians’ advice for screening might provide good opportunities to improve SPC screening behaviors.

Only 40.7% of disease-free lung cancer survivors, however, recalled being informed about the need for SPC screening or referred for such tests. Together with the results of previous studies, our results suggests that more information and training regarding appropriate cancer screening guidelines for cancer survivors will be needed for health care providers. Because there were few guidelines regarding such specific SPC screening, a feasible step should be started with increasing cancer survivors’ compliance to cancer screening guidelines for the general population. If physicians’ recommendation for SPC screening would be incorporated in the survivorship care plan, it might foster physician communication and shared care in monitoring SPC screening for cancer survivors.

We also found educational disparities in stomach and colorectal cancer screening among lung cancer survivors, and found income disparities in colorectal cancer screening among female subjects. Although several studies have reported educational and income disparities in cancer screening practices among the general population, [ 28, 29] little is known about these disparities among cancer survivors. In order to provide equal access to SPC screening services for cancer survivors, further collaborative efforts by policy makers, third party payers, and healthcare providers are needed. Several previous studied have suggested that educational disparity on receipt of cancer screening might be mediated by the role of health literacy [ 30, 31]. Further study for low-educated cancer patients will be needed to increase appropriate knowledge and attitude for SPC screening during or after the cancer treatment periods. Furthermore, because cancer survivors are more financially vulnerable, [ 32, 33] decreasing economic barrier for SPC screening should be considered.

Our study had several limitations. First, we used self-reported survey to assess the cancer screening compliance and physicians’ advice for SPC screening, which were not confirmed by medical record reviews or claims. Second, the response rate was only 44.2%. As participants could have been more likely to have preventive health behaviors than non-participants, our estimates of SPC screening practices among lung cancer survivors might therefore have been overestimated. Third, our study population consisted of Korean lung cancer survivors and stomach cancer screening is not recommended in western countries, which may limit the generalizability of our results. Although recent study has demonstrated that those who received an upper endoscopy were less likely to die from stomach cancer within the Korean national cancer screening program, [ 34] and cancer survivors were usually recommended to receive routine cancer screening guideline which is recommended in general population, [ 11– 13] further evidences will be needed among other ethnicities.

The present study showed that only a quarter of lung cancer survivors included were meeting existing guidelines for second primary cancer screening, particularly gastric and colorectal cancer. Physician must more proactive in communicating the need for screening and referring patients for such screening tests. In addition, further public policy will be needed to decrease educational disparities in SPC screening practices.