Association between awareness of nutrition labeling and high-density lipoprotein cholesterol concentration in cancer survivors and the general population: The Korean National Health and Nutrition Examination Survey (KNHANES) 2010–2016

In South Korea, more than 200,000 patients were newly diagnosed with cancer in 2014. Improvements in early detection and treatment has increased the 5-year survival rate for all cancers, from 41.2% for patients diagnosed between 1993 and 1995 to 70.3% for those diagnosed between 2010 and 2014 [1]. Cancer survivors have a greater risk for cardiovascular disease, cancer recurrence, and second primary malignancies [2, 3]. Therefore, cancer survivors should be more invested in maintaining ideal body weight, a healthy diet, and a physical activity level to prevent chronic diseases, cancer recurrence, and second primary cancers [4]. Dietary interventions have been shown to improve diet quality, body weight, and nutrition-related biomarkers [4]. Low-fat diets have been found to promote changes in serum lipids, cytokines, and angiogenic factors [5]. Plasma concentrations of high-density lipoprotein-cholesterol (HDL-C) have shown a strong inverse relationship to the risk of developing coronary artery disease (CAD) and cancer [6‐8]. On the other hand, a low concentration of HDL-C is associated with obesity [7].

Nutrition labeling of foods became compulsory in South Korea in 1995 [9], to assist consumers in making reasonable choices based on nutrition values by confirming the nutritional properties of processed foods [9, 10]. Nutrition labeling has been found to affect the intake of total fats, carbohydrates and saturated fats, as well as awareness of the nutritional contents of foods, which may be helpful in managing certain chronic diseases [11]. Moreover, greater awareness of nutrition labeling in a South Korean population was inversely related to the risk of dyslipidemia, especially regarding imbalances of HDL-C and triglycerides [12]. The introduction of nutrition labeling of foods in South Korea was expected to provide food-related health information to the South Korean population, cancer survivors included, to help them better manage their health. For that reason, this comparative study aimed to assess the association between individual nutrition concerns and HDL-C concentration among South Korean cancer survivors and the general population without a history of cancer.

Of the 25,156 subjects, 724 (2.88%) were cancer survivors and 24,432 (97.12%) had no history of cancer. Table 1 shows the characteristics of both groups. We found that approximately 20% of all respondents actively checked and made purchase decisions based on nutrition information, but that the percentage was significantly lower in cancer survivors than in the general population (16.30% vs. 19.32%, p < 0.0001). Cancer survivors were significantly older and of lower socioeconomic status but had healthier lifestyles than the general population in their behaviors of smoking, drinking, eating-out habits, and daily nutritional intake.

Based on previous reports, nutrition factors could have a positive effect on the management of triglyceride and HDL-C [14]. Among four key indicators: total cholesterol, triglyceride, HDL-C, and LDL-C, the triglyceride and HDL-C concentrations were associated with active use of nutrition information. Similarly positive impacts of nutrition labelling were reported in a previous study, showing a decrease of triglycerides and an increase of HDL-C by active use of nutrition information [12]. In this study, we focused on comparing the positive impacts of nutrition information awareness between cancer survivors and the general population. However, triglyceride results alone were not meaningful among cancer survivors (Additional file 1: Table S2). Thus, we decided to only focus on HDL-C to compare the positive impact of using nutrition information. Table 2 shows the findings of multiple gamma linear regression analysis for the relationship between nutrition information awareness and HDL-C level in all respondents. HDL-C concentrations were higher in subjects who checked, or were aware of, nutrition information (Relative Risk [RR]: 1.0017, 95% Confidence Interval [CI]: 1.0004–1.0031, p = 0.0131), and while there was no significant difference in these subjects, those who made purchase decisions based on nutrition labelling had positive increases of HDL-C (p = 0.1785).

HDL-C concentrations did not differ between cancer survivors and the general population. By other covariate analyses, female or younger subjects had higher HDL-C level than male or older subjects. Additionally, subjects with lower BMI were more likely to have higher HDL-C concentrations than the obese group. Subjects with heathy behaviors: non-smoker, mild drinker, or people with less frequency of eating-out, had healthier HDL-C concentrations. The results of the daily intake of nutrition survey show that respondents with lower carbohydrate or fat intake had higher HDL-C. In addition, triglyceride and LDL-C concentrations were inversely related to HDL-C concentration.

Table 3 displays the results of multiple linear regression analysis for cancer survivors and the general population. The active use of nutrition information had a positive correlation with higher HDL levels, particularly in cancer survivors. When compared to cancer survivors who did not check nutrition information, significantly higher HDL-C concentrations were seen in cancer survivors who checked and made label-dependent purchase decisions (RR: 1.0117, 95% CI: 1.0001–1.0233, p = 0.0479), as well as those who checked or were aware of nutrition information, but did not make labeling-dependent purchase decisions (RR: 1.0121, 95% CI: 1.0036–1.0205, p = 0.0050). In the general population, only those who checked or were aware of nutrition information had significantly higher HDL-C concentrations compared to those unaware of nutrition information (RR: 1.0015, 95% CI: 1.0001–1.0028, p = 0.0349). Covariate analyses showed that female, younger, or low BMI was associated with higher HDL-C in only the general population, and not cancer survivors. Similar results were observed among those with unhealthy behaviors such as smoking, drinking, or eating-out, which were only significant in the general population. However, daily carbohydrate or fat intake was inversely associated with HDL-C concentrations in both groups, and triglyceride and LDL-C concentrations were inversely related to HDL-C concentration.

We performed subgroup analysis to identify factors that influence the association between awareness of nutrition information and HDL-C levels. Based on descriptive statistics for subgroups, linear differences of HDL-C levels were observed in females regardless of their group type. In the general population, females with less eating-out behavior had more linear trends than the cancer survivors. On the other hand, when compared to others, cancer survivors with good subjective health had more associations (Table 4). The results of subgroup analysis for multiple linear regression show that female gender and a reduced frequency of eating-out were significantly related to this association, regardless of cancer status. However, the impact of nutrition labelling awareness was greater in cancer survivors than the general population. In contrast, subjective health status had slightly different effects in cancer survivors and the general population (Additional file 1: Figure S1).

Healthy lifestyles, including physically activity, a normal body weight, and a healthy diet, have been associated with a reduced risk of primary cancer [15, 16]. Such lifestyles have been shown to prevent tumor recurrence, second primary cancers, and other chronic diseases in cancer survivors [4]. Therefore, many cancer survivors seek information on healthy food, dietary supplement use, complementary nutrition products, and physical activity to improve their response to cancer treatment, achieve a rapid recovery, reduce the risk of cancer recurrence, and have a good quality of life [4, 17]. In addition, improvements in dietary behavior may also reduce the adverse effects of cancer and its treatment [3, 4]. The American Cancer Society (ACS) and the World Cancer Research Fund/American Institute for Cancer Research (WCF/AICR) proposed recommendations for diet to further emphasize the importance of weight management and nutrition. These recommendations encourage the consumption of fruits, vegetables, and unrefined whole grains, and limit the intake of energy dense foods such as sugars, fats, and a variety of processed foods [3, 4, 16]. In South Korea, nutrition labeling of food products reveals nutrition information such as serving size, calories, and carbohydrate, protein, fat, sodium, sugar, cholesterol, saturated fatty acid, trans fatty acid, and unsaturated fatty acid content. Awareness of nutrition labeling has been associated with positive results on lipid profiles, especially on HDL-C and triglyceride concentrations in the South Korean population [12]. A low serum concentration of HDL-C is a risk factor for cardiovascular disease [6, 18]. Moreover, each 1 mg/dL increase in HDL-C levels reduces the risk of coronary artery disease by 2 to 3%, independent of low-density lipoprotein (LDL) and triglycerides levels [19]. Furthermore, HDL-C concentration is inversely associated with cancer incidence, regardless of sex, age, smoking status, LDL-C, BMI, and diabetes [8, 20, 21]. We therefore hypothesized that nutrition label awareness would significantly affect diet-related health status, especially HDL-C in cancer survivors, and explored the possible association between awareness and HDL-C.

This study showed that HDL-C levels were higher in respondents who checked or were aware of nutrition information than in those who did not, but the HDL-C levels did not differ between respondents who checked nutrition information and made purchase decisions based on this information. Subgroup analysis showed a similar pattern in both cancer survivors and the general population when aware of nutrition labelling and checking it. In cancer survivors, HDL-C concentrations were significantly higher in those who check nutrition facts and make labeling-dependent purchase decisions, than in cancer survivors unaware of nutrition information. This pattern was not observed in the general population. Similarly, a previous study showed that nutrition awareness, i.e., checking nutrition information and actively using it, had positive effects on outcome indicators such as HDL-C and triglyceride levels in a South Korean population that included cancer survivors [12].

This study also shows that awareness of nutrition labeling (checking) or healthy behavior groups such as low BMI, non-smoking status, less eating-out, and low daily carbohydrate/ fat intake measured in grams, were independently associated with higher HDL-C levels in the general population. High awareness of nutrition labelling may lead to improved nutritional intake, including low-fat and low-carbohydrate diets. On other hand, among cancer survivors, there were no significant associations of healthy behaviors. The appearance of these results may be caused by their clinical condition following cancer treatment as compared to the general population. Thus, they might not be as responsive to healthy behaviors as the general population. Our finding that aerobic exercise habits were not independently associated with HDL-C levels in cancer survivors, suggests that a better diet may be a more important factor for increasing HDL-C levels in South Korea. Similarly, greater adherence to ACS guidelines was related to higher social functioning scores, suggesting that diet may be an important indicator in quality of life among Korean breast cancer survivors [22].

To the best of our knowledge, this is the first study to describe the association between awareness of nutrition labeling and HDL-C level among cancer survivors in a general population in South Korea. Our use of nationwide sampling data over a 5-year period may help establish long-term health policy at the national level [12]. However, this study had some limitations. First, KNHANES collected information, including cancer history and awareness of nutrition labeling, using self-reported questionnaires, but did not collect information about cancer stage or phase of care. Thus, there may have been recall bias, which may have influenced our outcomes of interest. Second, KNHANES is conducted for the general Korean people and the survey takes 1.5 to 2 h to complete. Therefore, the number of cancer survivors was relatively small, and only healthy cancer survivors might have been able to participate. Third, nutrition label awareness could be a proxy variable for health awareness or other healthy behavior variable. Therefore, self-reported nutrition label awareness may not fully reflect their actual behavior, e.g., reading nutrition label once out of every 100 opportunities.

This study showed that high awareness of nutrition labelling is associated with high HDL-C level, which is associated with reduced risks of cardiovascular disease and/or cancer. Moreover, this association was greater in cancer survivors than in the general population. The concerns of healthy behaviors by cancer survivors the need for guidelines directed to South Korean cancer survivors are increasing. Health policy makers and medical professionals may be aided by the results of this study in developing effective measures such as body weight control, smoking cessation, reducing and maintaining a low daily fat intake as well as promoting the use of nutrition labeling across this population. Further research is needed to determine the methods of increasing individual interest in nutrition. Moreover, randomized controlled trials are needed to show the benefits of a healthy diet on HDL-C levels in cancer survivors.

Awareness of nutrition labeling increased serum concentrations of HDL-C, a factor associated with coronary artery disease and the risk of cancer incidence. Active use of nutrition information correlated positively with higher HDL-C levels, especially among cancer survivors. Our findings suggest that health policy in South Korea should include the promotion of nutrition labeling for cancer survivors.