Abstract
Objective
This study was aimed at investigating the screening behaviors of the first-degree relatives (FDRs) of Chinese patients with gastric cancer as well as the factors influencing screening behaviors.
Methods
In a cross-sectional design, 197 FDRs of patients with gastric cancer were enrolled at the Peking University Cancer Hospital. Four questionnaires were used: a demographic questionnaire, a knowledge questionnaire of risk factors and warning symptoms for gastric cancer, the Gastric Cancer Health Belief Scale, and a questionnaire screening for behavioral motivators and barriers. Logistic regression analysis was performed to determine the factors influencing screening behaviors.
Results
Among the 197 FDRs of patients with gastric cancer, 30.96% (61/197) of patients had undergone gastric cancer screening. Among those who participated in gastric cancer screening, the most common screening methods were gastroscopy and the Helicobacter pylori testing, both of which were applied in 63.93% (39/61) of participants, followed by serum tumor marker testing (55.74%, 34/61) and barium meal examination of the upper digestive tract (29.51%, 18/61). The gastric cancer risk factor knowledge score was 9.02 ± 3.95, and the gastric cancer warning symptom knowledge score was 4.39 ± 1.85. The participants’ knowledge score was moderate, at 13.41 ± 5.16. The total health beliefs score was low, at 88.91 ± 12.66. Factors independently associated with the screening behaviors of FDRs included educational background, knowledge of gastric cancer risk factors, and health motivation (P < 0.05).
Conclusions
The participation rate in gastric cancer screening of FDRs of patients with gastric cancer was relatively low and was affected by multiple factors. Our results highlighted the urgent need for educational campaigns and precision interventions to raise gastric cancer awareness.
Keywords: Gastric cancer, First-degree relatives, Early diagnosis, Gastric cancer screening, Health beliefs
Introduction
Gastric cancer is one of the most common malignancies worldwide and was responsible for more than 1 million new cases and an estimated 769,000 deaths in 2020.1 The high-risk areas are East Asia, Eastern Europe, and Central and South America.2 In China, gastric cancer ranks second among all cancers in terms of incidence and mortality.3 Decreasing gastric cancer incidence and mortality is a major public health issue. Study findings have suggested that decreased gastric cancer specific mortality and increased survival rates in patients with gastric cancer can be achieved through gastric cancer screening.4
Gastric cancer screening programs have been implemented in Japan, South Korea, and China,5, 6, 7 and gastric cancer screening for high-risk groups is strongly recommended in relevant guidelines and consensus statements to achieve early diagnosis and increase survival.5, 6, 7, 8 Family history of gastric cancer is an independent risk factor for gastric cancer.9,10 Studies have confirmed that the first-degree relatives (FDRs) of patients with gastric cancer are at high risk of gastric cancer, and the odds ratio of the relative risk of gastric cancer in FDRs of different races and different regions fluctuated from 2 to 10.11,12 Therefore, FDRs of patients with gastric cancer are at high risk of developing gastric cancer. FDRs refer to a person's parents, children, and siblings.
Currently, the recommendations for gastric cancer screening differ across countries regarding high-risk populations, screening methods, and intervals. The Guide and Consensus of Early Gastric Cancer Screening in China7,8 recommends that patients at high risk of atrophic gastritis or intestinal metaplasia (OLGA or OLGIM stage Ⅲ or above) undergo high quality endoscopy once every 2 years. Gastric cancer screening is considered one of the most efficient approaches to mitigating the severely high gastric cancer incidence in China. Screening methods for gastric cancer include serum screening (eg, pepsinogen, gastrin, and gastric cancer tumor markers), Helicobacter pylori (H. pylori) testing, gastroscopy, and barium meal examination.5,7,8 H. pylori eradication is the most important strategy for preventing gastric cancer in FDRs of patients with gastric cancer, particularly those in their 20s and 30s.13
Multiple studies have focused on the screening behaviors among FDRs of patients with breast and colorectal cancer.14, 15, 16, 17 Studies on gastric cancer screening have focused primarily on methods of selection and economic benefit analysis.18, 19, 20, 21 A study of early screening for gastric cancer in South Korea has indicated that the screening rate of relatives of patients with gastric cancer was slightly higher than that in the general population yet remains low.22 Moreover, no significant difference has been observed in preventive behaviors between the relatives of patients with gastric cancer who participate in cancer screening and the general public.22 Another study has suggested that sex and the screening experience affected cognition of gastric cancer screening behavior.23 In addition, knowledge may influence screening behaviors. Insufficient knowledge of the risk factors, warning symptoms, and screening methods for gastric cancer24,25 might lead to a lack of awareness of cancer risk and neglecting of gastric cancer screening, thus hindering early diagnosis and treatment. Health beliefs can also influence an individual's screening behaviors. Studies have shown that the perceived benefits and health motivations of FDRs are significantly correlated with colonoscopy screening behavior.16,17 A review conducted by Tan et al26 has indicated that barriers to cancer screening included fear of cancer diagnosis, cost of testing, accessibility of health care resources, and a lack of awareness regarding disease risk. Knowledge and health beliefs improve screening effectiveness.27
To our knowledge, little research has examined the factors influencing screening behavior of FDRs of patients with gastric cancer in China. This study, therefore, explored gastric cancer screening behaviors and influencing factors among the FDRs of patients with gastric cancer to provide a basis for hospital-based early diagnosis, screening programs, and high-risk population management.
Methods
Study design
This cross-sectional study was conducted in a grade three comprehensive cancer hospital in Beijing, China. A total of 197 FDRs of patients with gastric cancer were enrolled. The study was approved by the Ethical Committee of the hospital (IRB No. 2020YJZ78). The study followed the STROBE standards for cross-sectional studies. All patients provided written informed consent.
Participants
The FDRs of patients diagnosed with gastric cancer were selected through convenience sampling. The inclusion criteria were FDRs of patients with gastric cancer (including children, siblings, and parents of the patients) ≥ 18 years of age, who were able to communicate clearly and without barriers; were cancer-free with no prior history of cancer; were willing to participate in this study voluntarily via signed informed consent. The exclusion criteria were patients with mental diseases or with other serious diseases (such as severe cardiopulmonary insufficiency). According to sample size estimation methods for multi-factor studies,28 the necessary sample size was 5–10 times the number of variables in the study. To account for the rate of invalid questionnaire responses, we increased the sample size by 20%. This study included 16 independent variables, and the formula for calculating the sample size was N= (16 × 10) / (1 − 20%) = 200. The sample size was at least 200.
Instruments
Participant characteristics
The patients’ demographic characteristics and disease information were collected with a demographic questionnaire including age, gender, relationship with the patient, occupation, ethnicity, religious beliefs, educational background, marital status, family monthly income, payment method, place of residence, presence or absence of physical discomfort within the past 6 months, presence of chronic diseases, and primary caregiver status.
Knowledge questionnaire of risk factors and warning symptoms of gastric cancer
The questionnaire designed by Liu et al.24 was used to evaluate the cognitive status regarding risk factors and warning symptoms of gastric cancer in FDRs of patients with gastric cancer. We were authorized to use the questionnaire by Liu et al. The questionnaire included 22 items in two dimensions. The first part related to risk factors for gastric cancer and included 16 items. Responses included “yes,” “no,” and “not sure/do not know,” with “yes” indicating that the participants identified the items to be risk factors. A correct answer was scored as 1 point, and the total score ranged from 0 to 16 points. The second part related to the warning symptoms of gastric cancer and included 6 items. The answers were divided into “yes,” “no,” and “not sure/do not know.” A correct answer was scored as 1 point, and the total score ranged from 0 to 6 points. The two dimensions could be scored separately or combined to yield a total score ranging from 0 to 22 points. The respondents’ knowledge was quantified according to the total score. A total score of 15–22 was classified as high knowledge, 8 to 14 was classified as moderate knowledge, and 0 to 7 was classified as low knowledge. The Cronbach α coefficient of the questionnaire was 0.879, and the test–retest reliability was 0.852 in surveying the population at risk of gastric cancer.29 The Cronbach α coefficients of the two dimensions of the questionnaire were 0.879 and 0.890 in surveying the general public.24 The original questionnaire thus had good reliability.
Gastric cancer health belief scale
To evaluate the participants' health beliefs about gastric cancer, this scale was modified on the basis of the Chinese version of the Colorectal Cancer Health Belief Scale. The Colorectal Cancer Health Belief Scale was originally developed and first used in 2002 by Jacobs.30 This scale is based on the Champion Health Belief Model Scale,31 and it includes a total of six dimensions and 36 items. Wu et al.32 have translated the scale into Chinese and applied it to relatives of patients with colorectal cancer for reliability and validity testing. The Chinese version of the scale had high validity, and its content validity index (S-CVI) was 0.98. The reliability of each dimension as well as the total scale was high, with Cronbach α coefficients of 0.801–0.944 and 0.881, respectively.32 The Champion team has indicated that the items included in the original scale can be reasonably modified to be applied to different populations.31 In this study, with the permission of the original author, the Chinese version of the Colorectal Cancer Health Beliefs Scale was revised to investigate the health beliefs regarding gastric cancer in FDRs of patients with gastric cancer, by replacing the phrase “colorectal cancer” with “gastric cancer.” Considering the different types of cancer, we further adjusted two items in the gastric cancer health belief scale according to the experts' opinion. “Regular check-ups to detect colon cancer will be embarrassing for me” was changed to “Regular check-ups to detect gastric cancer will make me nervous and scared”; “I can recognize normal and abnormal changes in my bowel habits” was changed to “I can recognize normal and abnormal stomach upset.” The S-CVI/Ave of the total scale was 0.99, and the CVI of each item was 0.8–1.00. The total scale and each dimension had good internal reliability (Cronbach α = 0.792, 0.696–0.863) in our study. The scale contained 36 items in six dimensions: perceived susceptibility to gastric cancer, perceived severity of gastric cancer, perceived benefits of gastric cancer screening, perceived barriers to gastric cancer screening, health motivation, and self-efficacy in gastric cancer screening. Items were rated on a five-point Likert scale (1: “do not agree at all”; 5: “completely agree”). The dimension of perceived barriers to gastric cancer screening was scored with the reverse scoring method, and the total score ranged from 36 to 180. The higher the score, the higher the participants’ belief in using the appropriate health behavior. The scores of gastric cancer health beliefs were divided into three levels in our study. A health beliefs score accounting for less than 60% of the total score (< 108) was considered low, a score accounting for 60%–80% (108–144) was considered moderate, and a score accounting for greater than 80% (> 144) was considered high.
Screening behaviors, motivators, and barriers questionnaire
According to the guidelines for gastric cancer screening,5,7 the prevailing consensus,8 and relevant literature,24 we applied a self-designed questionnaire to investigate whether the participants had been screened for gastric cancer, determine the screening methods used, and explore the reasons for screening or not screening. Gastric cancer screening behavior was the main outcome in this study. The participants were considered to exhibit gastric cancer screening behaviors if they had undergone any of the four tests (ie, the serum tumor marker (pepsinogen/gastrin 17/gastric cancer tumor markers), gastroscopy, barium meal examination, and H. pylori tests) within the prior 2 years; otherwise, they did not exhibit gastric cancer screening behaviors. Participants with screening behaviors were further asked about their reasons for undergoing gastric cancer screening tests, including routine physical examination, experiencing physical discomfort, having family members/colleagues/friends with gastric cancer or other malignant tumors, results of personal physical examinations, and recommendations from physicians or other people. The participants who had never been screened were asked to explain their reasons for not undergoing screening, including ignorance of the benefits of screening, fear of discomfort, fear of discovering health problems, feeling that there was no need to be screened if there was no discomfort, financial factors, lack of time, and other factors.
Data collection
The four investigators in our study received unified training before the survey and used unified explanations when explaining informed consent and the questionnaires to the participants. When the patients with gastric cancer were admitted to the hospital, the investigators asked whether the patients had FDRs who met the inclusion criteria for this study. The investigators obtained the consent of the patients, who provided the contact information of their FDRs, and then the investigators contacted the FDRs by telephone, explained the purpose of this study in detail, and obtained informed consent from all participants. The investigators made appointments with the FDRs. All participants signed an informed consent form after the meeting. Then the FDRs completed all questionnaires alone. A total of 201 questionnaires were collected, and 197 were valid, with a response rate of 98.01%.
Data analysis
Statistical analysis was performed in IBM SPSS Statistics for Windows, Version 20.0. The results for continuous variables are reported as medians and ranges. Those for categorical variables are reported as frequencies and percentages. Chi-squared and Fisher's exact tests were used to compare the participants' screening behavior characteristics. Measurement data are represented as standard deviation of mean, and the differences in measurement data were compared with t tests. Logistic regression analysis was used to identify the factors associated with screening behaviors. Only variables significantly associated with screening in the bivariate analysis were included in the logistic regression analysis. Odds ratios and their 95% confidence intervals were obtained. Calculated P values less than 0.05 were considered to indicate statistical significance.
Results
Participant characteristics
The mean age of the 197 FDRs was 40.73 years (range: 23–63 years); 84.26% were married; 53.30% were men. Regarding educational background, 39.09% had obtained a bachelor's degree or higher. Regarding insurance status and income level, 94.42% of the participants had different types of insurance, and 36.04% had high income. An overview of the participants is presented in Table 1.
Table 1.
Characteristics of FDRs of patients with gastric cancer and screening behaviors (n = 197).
| Characteristics | n (%) | Underwent screening, n (%) |
χ2 | P | ||
|---|---|---|---|---|---|---|
| Yes | No | |||||
| Age | < 40 years | 88 (44.67) | 34 (38.64) | 54 (61.36) | 4.379 | 0.036a |
| ≥ 40 years | 109 (55.33) | 27 (24.77) | 82 (75.23) | |||
| Gender | Male | 105 (53.30) | 31 (29.52) | 74 (70.48) | 0.218 | 0.640a |
| Female | 92 (46.70) | 30 (32.61) | 62 (67.39) | |||
| Relationship with the patient | Parents | 13 (6.60) | 3 (23.08) | 10 (76.92) | 0.406 | 0.816b |
| Children | 152 (77.16) | 48 (31.58) | 104 (68.42) | |||
| Siblings | 32 (16.24) | 10 (31.25) | 22 (68.75) | |||
| Occupation | Employed | 155 (78.68) | 55 (35.48) | 100 (64.52) | 7.949 | 0.047b |
| Unemployed | 35 (17.77) | 4 (11.43) | 31 (88.57) | |||
| Retired | 7 (3.55) | 2 (28.57) | 5 (71.43) | |||
| Ethnicity | Ethnic Han | 179 (90.86) | 56 (31.28) | 123 (68.72) | 0.094 | 0.759a |
| Minorities | 18 (9.14) | 5 (27.78) | 13 (72.22) | |||
| Religious beliefs | No | 189 (95.94) | 60 (31.75) | 129 (68.25) | 0.439 | 0.231b |
| Yes | 8 (4.06) | 1 (12.50) | 7 (87.50) | |||
| Educational background | Senior high school or less | 68 (34.52) | 9 (13.24) | 59 (86.76) | 15.849 | <0.001a |
| Junior college | 52 (26.40) | 19 (36.54) | 33 (63.46) | |||
| College or higher | 77 (39.09) | 33 (42.86) | 44 (57.14) | |||
| Marital status | Unmarried | 22 (11.17) | 7 (31.82) | 15 (68.18) | 1.804 | 0.614b |
| Married | 166 (84.26) | 53 (31.93) | 113 (68.07) | |||
| Divorced/Widowed | 9 (4.57) | 1 (11.11) | 8 (88.89) | |||
| Family monthly income | <￥5000 | 44 (22.34) | 8 (18.18) | 36 (81.82) | 4.351 | 0.114a |
| ￥5,000−10,000 | 82 (41.62) | 28 (34.15) | 54 (65.85) | |||
| ≥￥10,000 | 71 (36.04) | 25 (35.21) | 46 (64.79) | |||
| Payment method | Private | 11 (5.58) | 5 (45.45) | 6 (54.55) | 3.322 | 0.345a |
| Public | 5 (2.54) | 3 (60.00) | 2 (40.00) | |||
| Health insurance | 135 (68.53) | 40 (29.63) | 95 (70.37) | |||
| Rural cooperative medical service | 46 (23.35) | 13 (28.26) | 33 (71.74) | |||
| Place of residence | Town | 150 (76.14) | 49 (32.67) | 101 (67.33) | 0.470 | 0.231a |
| Rural | 47 (23.86) | 12 (25.53) | 35 (74.47) | |||
| Presence or absence of physical discomfort within the past 6 months | Absence | 135 (68.53) | 42 (31.11) | 93 (68.89) | 0.004 | 0.948a |
| Presence | 62 (31.47) | 19 (30.65) | 43 (69.35) | |||
| Presence chronic diseases or not | No | 172 (87.31) | 52 (30.23) | 120 (69.77) | 0.340 | 0.560a |
| Yes | 25 (12.69) | 9 (36.00) | 16 (64.00) | |||
| Being primary caregiver or not | No | 31 (15.74) | 9 (29.03) | 22 (70.97) | 0.064 | 0.800a |
| Yes | 166 (84.26) | 52 (31.33) | 114 (68.67) | |||
Chi-squared test.
Fisher's exact test.
Knowledge among the FDRs of patients with gastric cancer
A total of 28 (14.21%) participants had low knowledge, 78 (39.59%) participants had moderate knowledge, and 91 (46.19%) participants had high knowledge. Statistically significant differences in overall knowledge of gastric cancer and its risks were observed among the FDRs of patients with gastric cancer with different screening behaviors, as shown in Table 2. The scores for gastric cancer risk knowledge and overall knowledge of gastric cancer in FDRs who underwent gastric cancer screening were significantly higher than those without screening.
Table 2.
Comparison of knowledge among the FDRs of patients with gastric cancer with different screening behaviors.
| Variables | n | Knowledge of risk factors of gastric cancer | Knowledge of warning symptoms of gastric cancer | Knowledge of gastric cancer | |
|---|---|---|---|---|---|
| Total | 197 | 9.02 ± 3.95 | 4.39 ± 1.85 | 13.41 ± 5.16 | |
| Undergoing screening | Yes | 61 | 10.39 ± 3.53 | 4.69 ± 1.72 | 15.08 ± 4.63 |
| No | 136 | 8.40 ± 3.98 | 4.25 ± 1.90 | 12.65 ± 5.22 | |
| t | 3.352 | 1.544 | 3.123 | ||
| P | 0.001∗ | 0.124 | 0.002∗ |
Health beliefs of the FDRs of patients with gastric cancer
The total health beliefs score of the FDRs of patients with gastric cancer was low, at 88.91 ± 12.66. Their health beliefs with different screening behaviors were compared, and statistically significant differences in the health motivation dimension were observed between groups (P < 0.05), as shown in Table 3.
Table 3.
Comparison of the health beliefs of the FDRs of patients with gastric cancer with different screening behaviors.
| Variables | n | Severity | Susceptibility | Barriers | Health motivation | Self-efficacy | Benefits | Health beliefs | |
|---|---|---|---|---|---|---|---|---|---|
| Total | 197 | 20.84 ± 5.80 | 16.94 ± 4.18 | 14.86 ± 5.33 | 14.45 ± 3.73 | 11.50 ± 2.97 | 10.32 ± 3.60 | 88.91 ± 12.66 | |
| Undergoing screening | Yes | 61 | 20.53 ± 5.97 | 16.99 ± 4.19 | 14.95 ± 5.34 | 14.88 ± 3.72 | 11.58 ± 3.05 | 10.52 ± 3.41 | 89.58 ± 12.87 |
| No | 136 | 21.29 ± 5.41 | 16.84 ± 4.18 | 14.63 ± 5.34 | 13.49 ± 3.58 | 11.31 ± 2.77 | 9.85 ± 3.98 | 87.42 ± 12.16 | |
| t | 0.732 | −0.242 | −0.384 | −2.452 | −0.588 | −1.220 | −1.105 | ||
| P | 0.465 | 0.809 | 0.701 | 0.015∗ | 0.557 | 0.224 | 0.271 |
Screening behavior, motivators, and barriers among the FDRs of patients with gastric cancer
Among the FDRs of patients with gastric cancer, 30.96% (61/197) of participants underwent screening for gastric cancer. The others had never been screened for gastric cancer. Among those who participated in screening for gastric cancer, the most common screening methods were gastroscopy and H. pylori testing, both of which were applied in 63.93% (39/61) of the participants, followed by serum tumor marker testing, which accounted for 55.74% (34/61). Only 29.51% (18/61) of the participants underwent gastric cancer screening through barium meal examination of the upper digestive tract.
The most common motivator for gastric cancer screening was an annual physical examination organized by an employer. Among the participants, 136 did not undergo screening for gastric cancer. The two main reasons were that most of them considered screening to be unnecessary when they did not feel uncomfortable, and many of them feared the potential discomfort caused by the examination. The results are shown in Table 4.
Table 4.
Screening behavior of the FDRs of patients with gastric cancer and the motivators and barriers (n = 197).
| Variables | n | Percentage (%) |
|---|---|---|
| Motivators for screening (n = 61) | ||
| Physical examination organized by the employer | 32 | 52.46 |
| Personal physical examination | 23 | 37.70 |
| A family member/colleague/friend is diagnosed with stomach cancer or malignant tumor | 22 | 36.07 |
| The body is unwell | 18 | 29.51 |
| Recommended by a doctor or other people | 13 | 21.31 |
| Barriers to screening (n = 136) | ||
| Do not feel uncomfortable and consider the examination unnecessary | 96 | 70.59 |
| Afraid of the discomfort caused by the examination | 46 | 33.82 |
| Do not know the benefits of screening | 38 | 27.94 |
| Do not have the time | 34 | 25.00 |
| Worry about the test results | 19 | 13.97 |
| Economic factors | 15 | 11.03 |
| Others | 11 | 8.09 |
Factors associated with screening behaviors
In the univariate analysis, the factors influencing screening behaviors included age, occupation, educational background, knowledge of gastric cancer, and health beliefs (Table 1, Table 2, Table 3). With gastric cancer screening as the dependent variable (No = 0, Yes = 1), variables entered into the equation were age, working status (employed served as the control), educational background (senior high school or less served as the control), knowledge of gastric cancer risk, knowledge of early warning of gastric cancer, and six dimensions of the health beliefs were all brought into the original value. As shown in Table 5, in the multivariate analysis, the variables associated with gastric cancer screening were educational background, knowledge of risk factors of gastric cancer, and health motivation.
Table 5.
Multivariate analysis of different screening behaviors of gastric cancer.
| Variables | β | SE | Wald | P-value | Odds ratio | Confidence interval | |
|---|---|---|---|---|---|---|---|
| Junior college | 1.119 | 0.511 | 4.797 | 0.029 | 3.063 | 1.125–8.338 | |
| College or higher | 1.420 | 0.506 | 7.873 | 0.005 | 4.139 | 1.534–11.162 | |
| Risk factors of gastric cancer | 0.146 | 0.058 | 6.315 | 0.012 | 1.158 | 1.033–1.297 | |
| Health motivation | 0.072 | 0.048 | 2.249 | 0.018 | 1.075 | 0.978–1.181 | |
| Constant | −3.692 | 1.874 | 3.881 | 0.049 | 0.025 | ||
Discussion
As a risk factor in gastric cancer, the screening behavior of FDRs is increasingly receiving researchers' much attention. This study investigated the screening behavior and related factors among the FDRs of patients with gastric cancer. The screening rate of FDRs was low, thus suggesting that interventions must be developed to increase this rate. In addition, education background, knowledge of gastric cancer risk, and health motivation positively affected the screening behavior among FDRs.
The rate of participation in screening behavior for gastric cancer in FDRs of patients with gastric cancer is low and must be increased. The FDRs of patients with gastric cancer are at high risk for gastric cancer.11, 12 Increasing the participation rate in gastric cancer screening among FDRs can effectively improve the early diagnosis and treatment cancer. In this study, only 30.96% of the FDRs of patients with gastric cancer had undergone early screening for gastric cancer. The screening rate of FDRs in this study was lower (30.96% vs. 39.2%) than that in a study by Jung et al.,22 and was similar to the gastric cancer screening rate (32.3%) reported in Koreans without a family history of gastric cancer. Therefore, promoting early diagnosis and screening for gastric cancer, raising awareness of screening, and improving the participation rate in early screening among FDRs of gastric cancer are essential.
Only 37.70% of the FDRs who underwent screening were screened through personal physical examination. The main reason why other participants underwent gastric cancer screening was associated with external forces, primarily employer-organized annual physical examinations (52.46%). The cancer diagnosis of an FDR might prompt people to pursue screening. Furthermore, 36.07% of the participants underwent gastric cancer screening because a family member/colleague/friend was diagnosed with cancer; thus, they were motivated by a fear of being diagnosed with cancer. Similar results have been presented by Humpel.33 In addition, 21.31% of the participants were screened according to the recommendations of physicians or others. Therefore, FDRs who underwent gastric screening may not realize the importance of active screening. Early detection, early diagnosis, and early treatment are at the core of any secondary cancer prevention strategy. The results suggest that public education should be strengthened, particularly among FDRs of patients with cancer, to improve their awareness of early diagnosis and screening.
Barriers preventing FDRs from undergoing cancer screening included a belief that screening was unnecessary if they did not feel uncomfortable, fearing the discomfort caused by the examination, not knowing the benefits of screening, being unavailable or worried about the test results, and economic factors. The first two were the main reasons, in agreement with the findings of Liu et al.24 Eliminating barriers is likely to increase the compliance of the FDRs in undergoing cancer screening. The results suggested that public education on cancer prevention and early diagnosis should be strengthened. For example, endoscopic screening is an effective method for the early identification of gastric cancer, which is particularly important for moderate and high-risk groups.34 However, 33.82% of the participants did not undergo screening in this study, owing to a fear of the discomfort caused by endoscopy, and more than one-third of the participants who underwent screening did not choose gastroscopy. Thus, in the future, efforts should be made to better inform the public about the gastroscopy procedure to decrease their fear and make the examination more comfortable. In South Korea, gastric cancer screening is a part of the national cancer screening program, and thus the population has few financial barriers.22 In the past three decades, China has promoted many early screening programs in areas with high incidences of gastric cancer and achieved remarkable success.35,36 However, much progress remains necessary in China. Education programs for the FDRs of patients with gastric cancer are necessary, which may improve their awareness of the risk factors of gastric cancer and remind them of the importance of cancer screening, thus increasing the early screening rate.
Education background and knowledge of gastric cancer risk are important factors influencing the screening behaviors among FDRs of patients with gastric cancer. In this study, higher education levels were associated with better gastric cancer screening behaviors. Highly educated people may be likely to learn and pay attention to their own health. Additionally, the gastric cancer risk knowledge score was associated with screening behavior, and more than half the participants had moderate or low gastric cancer-associated knowledge. A lack of awareness of the risk factors and warning symptoms of gastric cancer might explain the lack of screening behavior in this group of participants. This finding is similar to the results of Liu et al.24 We suggest that more attention should be paid to the population with a low education level and a lack of gastric cancer risk knowledge and that exploring appropriate approaches to improving health education is particularly important.
People at risk of gastric cancer may change their lifestyles only when they believe that unhealthful behaviors will increase their risk of diagnosis. Similarly, they are more likely to undergo gastric cancer screening only when they are aware of the risks. The diagnosis and treatment of patients with gastric cancer create educational opportunities for FDRs.33 Therefore, hospital-based educational programs for patients and family members may become an effective method for early diagnosis of and screening for gastric cancer as well as dissemination of gastric cancer-associated knowledge. Nurses can play an important role in these education programs, and case managers can play an important role in cancer prevention education for patients with cancer and their families in China. Case management is undertaken by nurses in China.37
Health motivation can promote screening among FDRs of patients with gastric cancer. Health motivation is the psychological state of individuals who are ready to take action and the internal impetus for individuals practicing health behaviors; it is considered a dimension of health beliefs.31 According to the Health Belief Model (HBM), whether an individual takes a health action is determined by the psychological state of the individual preparing to take action, and the trade-off between the perceived benefits and barriers associated with the action.30 The results of this study showed that the FDRs with higher health motivation scores exhibited better screening behaviors, in agreement with the findings of Koc et al.16 The FDRs of patients with gastric cancer who had insufficient health motivation did not perceive the benefits of healthy behaviors and thus tended to perceive more barriers. Therefore, they did not actively attempt to prevent disease or regularly participate in early cancer screening. The HBM has been widely used to predict and explain cancer screening behaviors.38,39 Variables derived from health beliefs have been identified as important goals in developing interventions to promote the screening of high-risk populations.40 The above results suggested that intervention measures can be built around the HBM while promoting public knowledge of cancer screening through multiple media, the Internet, and other forms, to improve the general perception of the benefits of screening, increase the motivation to be screened, and improve the screening participation rate.
Limitations
The first limitation of this study was that sample selection bias might have existed. In the study, the FDRs of patients with gastric cancer were selected from only one hospital. Multi-center studies will be conducted in the future. The second limitation was that self-reporting was used to collect the data on screening behaviors. The participants' recall of screening behavior might have been biased. The screening behavior of the FDRs would be able to be tracked more accurately in a prospective study. In addition, FDRs’ knowledge of screening methods was not measured and may be a topic for future study.
Conclusions
Family history of gastric cancer is a risk factor for gastric cancer. Health management and early screening for gastric cancer among the FDRs of patients are very important to achieve early detection, diagnosis, and treatment. Eliminating the barriers and encouraging cancer screening are essential for the early diagnosis and prevention of gastric cancer. Therefore, identifying factors that improve FDRs’ screening behaviors would provide a basis to construct an effective intervention program. This study supplemented and analyzed data on the gastric cancer screening status of the FDRs of gastric cancer and found that education level, knowledge of gastric cancer risk, and health motivation positively affected early cancer screening behaviors among this group of people, thereby indicating the importance of public education. With the continuing expansion of nursing functions, nurses play an increasingly important role in the prevention and early diagnosis of cancer. Accordingly, hospital-based gastric cancer screening and health management programs for FDRs may be a future direction worthy of consideration.
Credit author statement
Min Zhao: Conceptualization, Methodology, Software, Writing- Original draft preparation. Hui Li: Methodology, Investigation, Supervision. Hui Ren: Investigation. Jie Zhang: Investigation. Hong Yang :Conceptualization, Methodology, Supervision. Yuhan Lu: Conceptualization, Data curation, Writing, Reviewing and Editing. All authors had full access to all the data in the study, and the corresponding author had final responsibility for the decision, to submit for publication. The corresponding author attests that all listed authors meet authorship criteria and that no others meeting the criteria have been omitted.
Declaration of competing interest
The authors declare no conflict of interest. The corresponding author, Prof. Yuhan Lu, is an editorial board member of Asia-Pacific Journal of Oncology Nursing. The article was subject to the journal’s standard procedures, with peer review handled independently of Prof. Lu and their research groups.
Funding
This study received no external funding.
Ethics statement
The study was approved by the Ethical Committee of the hospital (IRB No. 2020YJZ78). All patients provided written informed consent.
Data availability statement
The data that support the findings of this study are available from the corresponding author, Prof. Yuhan Lu, upon reasonable request.
References
- 1.Sung H., Ferlay J., Siegel R.L., et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–249. doi: 10.3322/caac.21660. [DOI] [PubMed] [Google Scholar]
- 2.Sitarz R., Skierucha M., Mielko J., et al. Gastric cancer: epidemiology, prevention, classification, and treatment. Cancer Manag Res. 2018;7(10):239–248. doi: 10.2147/CMAR.S149619. eCollection 2018. eCollection 2018. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Chen W., Zheng R., Baade P.D., et al. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66(2):115–132. doi: 10.3322/caac.21338. [DOI] [PubMed] [Google Scholar]
- 4.Kim H., Hwang Y., Sung H., et al. Effectiveness of gastric cancer screening on gastric cancer incidence and mortality in a community-based prospective cohort. Cancer Res Treat. 2018;50(2):582–589. doi: 10.4143/crt.2017.048. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Hamashima C. Systematic review group and guideline development group for gastric cancer screening guidelines. Update version of the Japanese guidelines for gastric cancer screening. Jpn J Clin Oncol. 2018;48(7):673–683. doi: 10.1093/jjco/hyy077. [DOI] [PubMed] [Google Scholar]
- 6.Park H.A., Nam S.Y., Lee S.K., et al. The Korean guideline for gastric cancer screening. J Korean Med Assoc. 2015;58(5):373–384. https://doi:.org/10.5124/jkma.2015.58.5.373 [Google Scholar]
- 7.He J., Chen W.Q., Li Z.S., et al. China guideline for the screening, early detection and early treatment of gastric cancer (2022, Beijing) Chin J Oncol. 2022;44(7):634–666. doi: 10.3760/cma.j.cn112152-20220617-00430. [CHINESE] [CHINESE] [DOI] [PubMed] [Google Scholar]
- 8.National Clinical Research Center for Digestive Diseases. Chinese Society of Digestive Endoscopology. Chinese Society of Health Management. et al. China experts consensus on the protocol of early gastric cancer screening (2017, Shanghai) Chinese J Health Manag. 2018;12(1):8–14. doi: 10.3760/cma.j.issn.1674-0815.2018.01.003. [CHINESE] [DOI] [Google Scholar]
- 9.Jiang X., Tseng C.C., Bernstein L., et al. Family history of cancer and gastroesophageal disorders and risk of esophageal and gastric adenocarcinomas: a case-control study. BMC Cancer. 2014;14:60. doi: 10.1186/1471-2407-14-60. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Yusefi A.R., Bagheri Lankarani K., Bastani P., et al. Risk factors for gastric cancer: a systematic review. Asian Pac J Cancer Prev APJCP. 2018;19(3):591–603. doi: 10.22034/APJCP.2018.19.3.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Dhillon P.K., Farrow D.C., Vaughan T.L., et al. Family history of cancer and risk of esophageal and gastric cancers. Int J Cancer. 2001;93(1):148–152. doi: 10.1002/ijc.1294. [DOI] [PubMed] [Google Scholar]
- 12.Shin C.M., Kim N., Yang H.J., et al. Stomach cancer risk in gastric cancer relatives: interaction between Helicobacter pylori infection and family history of gastric cancer for the risk of stomach cancer. J Clin Gastroenterol. 2010;44:e34–e39. doi: 10.1097/MCG.0b013e3181a159c4. [DOI] [PubMed] [Google Scholar]
- 13.Choi Y.J., Kim N. Gastric cancer and family history. Korean J Intern Med. 2016;31(6):1042–1053. doi: 10.3904/kjim.2016.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Lipscomb J., Escoffery C., Gillespie T.W., et al. Improving screening uptake among breast cancer survivors and their first-degree relatives at elevated risk to breast cancer: Results and implications of a randomized study in the state of Georgia. Int J Environ Res Public Health. 2020;17(3):977. doi: 10.3390/ijerph17030977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Oleske D.M., Galvez A., Cobleigh M.A., et al. Are tri-ethnic low-income women with breast cancer effective teachers of the importance of breast cancer screening to their first-degree relatives? Results from a randomized clinical trial. Breast J. 2007;13(1):19–27. doi: 10.1111/j.1524-4741.2006.00358.x. [DOI] [PubMed] [Google Scholar]
- 16.Koc S., Esin M.N. Screening behaviors health beliefs, and related factors of first-degree relatives of colorectal cancer patients with ongoing treatment in Turkey. Cancer Nurs. 2014;37(6):E51–E60.. doi: 10.1097/NCC.0000000000000121. [DOI] [PubMed] [Google Scholar]
- 17.Bai Y., Wong C.L., Peng X., et al. Colonoscopy Screening behavior and associated factors amongst first-degree relatives of people with colorectal cancer in China: testing the health belief model using a cross-sectional design. Int J Environ Res Publ Health. 2020;17(14):4927. doi: 10.3390/ijerph17144927. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Areia M., Spaander M.C., Kuipers E.J., et al. Endoscopic screening for gastric cancer: a cost-utility analysis for countries with an intermediate gastric cancer risk. United European Gastroenterol J. 2018;6(2):192–202. doi: 10.1177/2050640617722902. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Lee S., Jun J.K., Suh M., et al. Gastric cancer screening uptake trends in Korea: results for the national cancer screening program from 2002 to 2011: a prospective cross-sectional study. Medicine (Baltimore) 2015;94(8):e533. doi: 10.1097/MD.0000000000000533. https://org.doi/10.1097/MD.0000000000000533 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Li W.Q., Qin X.X., Li Z.X., et al. Beneficial effects of endoscopic screening on gastric cancer and optimal screening interval: a population-based study. Endoscopy. 2022;54(9):848–858. doi: 10.1055/a-1728-5673. https://org.doi/10.1055/a-1728-5673 [DOI] [PubMed] [Google Scholar]
- 21.Dong E.Y., Giap A.Q., Lustigova E., et al. Gastric cancer screening in first-degree relatives: a pilot study in a diverse integrated healthcare system. Clin Transl Gastroenterol. 2022;13(11) doi: 10.14309/ctg.0000000000000531. https://org.doi/10.14309/ctg.0000000000000531 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Kang J.M., Shin D.W., Kwon Y.M., et al. Stomach cancer screening and preventive behaviors in relatives of gastric cancer patients. World J Gastroenterol. 2011;17(30):3518–3525. doi: 10.3748/wjg.v17.i30.3518. https://org.doi/10.3748/wjg.v17.i30.3518 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Li H.Q., Xue H., Yuan H., et al. Preferences of first-degree relatives of gastric cancer patients for gastric cancer screening: a discrete choice experiment. BMC Cancer. 2021;21(1):959. doi: 10.1186/s12885-021-08677-9. https://org.doi/10.1186/s12885-021-08677-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Liu Q., Zeng X., Wang W., et al. Awareness of risk factors and warning symptoms and attitude towards gastric cancer screening among the general public in China: a cross-sectional study. BMJ Open. 2019;9(7) doi: 10.1136/bmjopen-2019-029638. https://org.doi/10.1136/bmjopen-2019-029638 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Xiao F., Yuan X.H., Han T., et al. Investigation on awareness of gastric cancer risk factors and warning symptoms among first-degree relatives of gastric cancer patients. J Nurs Sci. 2022;37(12):26–29. doi: 10.3870/j.issn.1001-4152.2022.12.026. [CHINESE] [DOI] [Google Scholar]
- 26.Tan K.K., Lopez V., Wong M.L., et al. Uncovering the barriers to undergoing screening among first degree relatives of colorectal cancer patients: a review of qualitative literature. J Gastrointest Oncol. 2018;9(3):579–588. doi: 10.21037/jgo.2018.03.02. https://org.doi/10.21037/jgo.2018.03.02 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Ding Z. Investigation of status of colorectal cancer knowledge and health belief of community residents. China Med Univ. 2012 doi: 10.7666/dy2091982. [CHINESE] [DOI] [Google Scholar]
- 28.Wan X., Li Z.H., Liu J.P. Sample size estimation in clinical studies: (1) Clinical trials. J Tradit Chin Med. 2007;48(6):504–507. doi: 10.3321/j.issn:1001-1668.2007.06.009. [CHINESE] [DOI] [Google Scholar]
- 29.Liu Q., Zeng X., Huang R.L., et al. Analysis on the awareness of gastric cancer risk factors and warning symptoms among high-risk population of gastric cancer. Chinese Primary Health Care. 2019;33(11):57–61. doi: 10.3969/j.issn.1001-568X.2019.11.0019. [CHINESE] [DOI] [Google Scholar]
- 30.Jacobs LA. Health beliefs of first-degree relatives of individuals with colorectal cancer and participation in health maintenance visits: a population-based survey. Cancer Nurs. 2002;25(4):251–265. doi: 10.1097/00002820-200208000-00001. [DOI] [PubMed] [Google Scholar]
- 31.Champion VL, Scott CR. Reliability and validity of breast cancer screening belief scales in African American women. Nurs Res. 1997;46(6):331–337. doi: 10.1097/00006199-199711000-00006. [DOI] [PubMed] [Google Scholar]
- 32.Wu X.D., Zhang M.F., Zheng M.C., et al. Translation and reliability and validity of colorectal cancer Health Belief Scale. Chinese General Practice. 2020;23(1):155–160. doi: 10.12114/j.issn.1007-9572.2019.00.335. [CHINESE] [DOI] [Google Scholar]
- 33.Humpel N., Magee C., Jones S.C. The impact of a cancer diagnosis on the health behaviors of cancer survivors and their family and friends. Support Care Cancer. 2007;15(6):621–630. doi: 10.1007/s00520-006-0207-6. [DOI] [PubMed] [Google Scholar]
- 34.Leung W.K., Wu M.S., Kakugawa Y., et al. Screening for gastric cancer in Asia: current evidence and practice. Lancet Oncol. 2008;9(3):279–287. doi: 10.1016/S1470-2045(08)70072-X. [DOI] [PubMed] [Google Scholar]
- 35.Chen R., Liu Y., Song G., et al. Effectiveness of onetime endoscopic screening programme in prevention of upper gastrointestinal cancer in China: a multicentre population-based cohort study. Gut. 2021;70(2):251–260. doi: 10.1136/gutjnl-2019-320200. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Fan X.H., Qin X.X., Zhang Y., et al. Screening for gastric cancer in China: advances, challenges and visions. Chin J Cancer Res. 2021;33(2):168–180. doi: 10.21147/j.issn.1000-9604.2021.02.05. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Breast Cancer Case Manager Branch of Chinese Medical Education Association Expert consensus on Chinese breast cancer case management model. Natl Med J China. 2020;100(7):493–497. doi: 10.3760/cma.j.issn.0376-2491.2020.07.005. [CHINESE] [DOI] [Google Scholar]
- 38.So W.K.W., Law B.M.H., Choi K.C., et al. A family-based multimedia intervention to enhance the uptake of colorectal cancer screening among older South Asian adults in Hong Kong: a study protocol for a cluster randomized controlled trial. BMC Publ Health. 2019;19(1):652. doi: 10.1186/s12889-019-6995-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Zare M., Ghodsbin F., Jahanbin I., et al. The effect of health belief model-based education on knowledge and prostate cancer screening behaviors: a randomized controlled trial. Int J Community Based Nurs Midwifery. 2016;4(1):57–68. [PMC free article] [PubMed] [Google Scholar]
- 40.Bai Y., Wong C.L., He X., et al. Effectiveness of tailored communication intervention in increasing colonoscopy screening rates amongst first-degree relatives of individuals with colorectal cancer: a systematic review and meta-analysis. Int J Nurs Stud. 2020;101:103397. doi: 10.1016/j.ijnurstu.2019.103397. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data that support the findings of this study are available from the corresponding author, Prof. Yuhan Lu, upon reasonable request.