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Original Article
Diabetes, obesity and metabolism Intake of Fruit and Glycemic Control in Korean Patients with Diabetes Mellitus Using the Korea National Health and Nutrition Examination Survey
Keypoint
The study investigated the relationship between fresh fruit consumption and glycemic control in patients with type 2 diabetes mellitus using data from the 6th Korea National Health and Nutrition Examination Survey. The results showed that patients with the highest fruit intake were older and predominantly women, and that fruit consumption was negatively correlated with smoking and alcohol intake. A positive correlation was found between fruit consumption and better hemoglobin A1c levels, indicating that higher fruit intake may contribute to improved glycemic control in Korean type 2 diabetes mellitus patients.
Eunju Yoon1orcid, Ji Cheol Bae2orcid, Sunghwan Suh2orcid
Endocrinology and Metabolism 2023;38(5):538-544.
DOI: https://doi.org/10.3803/EnM.2023.1730
Published online: August 8, 2023
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1Department of Food Science and Nutrition, Dong-A University, Busan, Korea

2Department of Internal Medicine, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon, Korea

Corresponding author: Sunghwan Suh Department of Internal Medicine, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, 158 Paryong-ro, Masanhoewon-gu, Changwon 51353, Korea Tel: +82-55-233-5830, Fax: +82-55-233-5109, E-mail: taret@daum.net
• Received: May 8, 2023   • Revised: June 26, 2023   • Accepted: July 24, 2023

Copyright © 2023 Korean Endocrine Society

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

  • Background
    Despite the well-recognized health benefits of fresh fruit consumption, there is still substantial uncertainty about its potential effects on glycemic control in patients with type 2 diabetes mellitus (T2DM).
  • Methods
    We examined the association of fresh fruit consumption and glycemic control in patients with T2DM using data from the 6th Korea National Health and Nutrition Examination Survey. The study sample was divided into three groups based on weekly fruit consumption frequency for the analysis.
  • Results
    Patients with the highest fruit intake were older than those in the other two groups, and women were more likely to consume fruits in general. Being a current smoker and weekly alcohol intake also showed negative correlations according to the fruit intake tertiles. Fruit consumption was positively correlated with better hemoglobin A1c (HbA1c) levels. Moreover, patients in the highest tertile of fruit intake were 3.48 times more likely to be in good glycemic control defined as HbA1c <7%.
  • Conclusion
    We observed that fruit consumption can be helpful in glycemic control in Korean patients with T2DM.
Type 2 diabetes mellitus (T2DM) is an important public health issue worldwide [1]. There has been a steady increase in the global prevalence of diabetes, along with a high prevalence and low control rate of diabetes and its comorbidities in Korean adults, which has led to a huge burden on our society [2]. Therefore, glucose-lowering therapy remains a mainstay of diabetes management, in conjunction with a healthy lifestyle and other medications that specifically address the prevention or therapy of diabetes-related complications [3].
Accumulating evidence suggests that lifestyle changes, including eating healthy foods can help prevent or delay the development of T2DM [4,5]. The goals of medical nutrition therapy (MNT) are to promote healthy eating patterns satisfying individual’s nutrition needs while maintaining the pleasure of eating [6]. MNT provided by a registered dietitian or nutritionist can significantly reduce hemoglobin A1c (HbA1c) and help to prevent, delay and treat complications related with diabetes [7]. Therefore, MNT is recognized as one of the cornerstones in the treatment of T2DM.
Two core dimensions of MNT that can improve glycemic management are dietary quality and energy restriction [7]. Eating a combination of fruits and vegetables is recommended for a healthy diet. As a result, dietary pattern with an emphasis on the consumption of plant foods with little consumption of processed and animal-based foods may have benefits on the prevention and management of T2DM [8]. Health professionals often have concerns about the higher sugar content of fruit compared to vegetables and its potential harmful impacts on blood glucose levels. Therefore, we advise patients with T2DM to restrict their intake to a maximum of two pieces a day [9].
Despite the well-recognized health benefits of fresh fruit consumption [10], there are still substantial uncertainties about its potential effects on glycemic control in patients with T2DM. Hence, we examined the association of fresh fruit consumption and glycemic control in patients with T2DM using data from the 6th Korea National Health and Nutrition Examination Survey (KNHANES).
The KNHANES is a national ongoing cross-sectional survey evaluating the heath and nutritional status of the Korean population [11]. The present study used the 6th KNHANES data which was delivered from 2013 to 2015 since Food Frequency Questionnaire (FFQ) has been excluded since the 7th KNHANES. Individuals who have special dietary needs such as pregnant women, breast-feeding mothers, and persons with cancers or other severe underlying diseases were excluded from the study sample along with those who consume less than 500 kcal or more than 5,000 kcal per day. After the exclusion from the 7,242 participants (male 3,196 and female 4,046) who completed FFQ, 460 patients in total were included in this study. The fresh fruit consumption levels of the patients were assessed by summing the weekly average consumption frequencies for 13 fresh fruits, i.e., strawberries, tomatoes, oriental melons, watermelons, peaches, grapes, apples, pears, persimmons, tangerines, bananas, oranges, and kiwis, over the prior year. Patients also identified whether or not their daily energy intake from fruits exceeded 100 kcal.
Dietary assessment
Dietary assessments were conducted by using FFQ. FFQ lists the 112 most often consumed food items in South Korea with 10 categories of frequency value [12]. We also assessed scores of The Korean Healthy Eating Index (KHEI). KHEI was developed as a tool for monitoring the diet quality of the Korean population and subpopulations as well as evaluating nutrition interventions and research for assessing healthy Korean adults’ adherence to national dietary guidelines and comprehensive diet quality [13].
Statistical analysis
All statistical analyses were performed using IBM SPSS Statistics version 27.0 Program (IBM Corp., Armonk, NY, USA). Because the participants of the KNHANES are selected using complex, stratified multistage probability-cluster sampling design [11], statistical analyses were delivered applying the combined sample weights to prevent underestimation of standard errors. Odds ratios (ORs) and 95% confidence intervals (CIs) for the glycemic control in relation to fruit consumption levels were estimated using complex sample logistic regression while adjusting for sex, age, body mass index (BMI), systolic blood pressure, triglycerides, low-density lipoprotein cholesterol, current smoking and alcohol intake, total energy consumption, weekly walking frequency and dietary fiber intakes as confounders.
Ethics statement
The present study protocol was reviewed and approved by the Institutional Review Board of Dong-A University Medical Center (approval No. DAUHIRB-EXP-21-224). The requirement of written informed consent from the patients was waived due to the retrospective nature of this study of previously collected and deidentified data. This study was conducted in accordance with the ethical standards established in the 1964 Declaration of Helsinki and its later amendments.
The baseline characteristics and daily dietary intake of the 460 patients with diabetes mellitus (DM) according to tertiles of weekly fruit consumption frequency are presented in Table 1. The study sample was divided into three groups based on weekly fruit consumption frequency: less than 2.82 times (tertile 1), 2.82–7.63 times (tertile 2), and more than 7.63 times (tertile 3). Nearly 80% of the patients in tertile 3 was taking fruit above the recommendation per day (100 kcal, which is equivalent to 2 exchange units of fruits). The patients in the group with the highest fruit intake were older compared to those in the other two groups, and women were more likely to consume fruits than men. Currents smokers and weekly alcohol intake also showed negative correlations according to the fruit intake tertiles. Fruit consumption was positively correlated with better HbA1c levels in the study sample. Moreover, KHEI score was significantly associated with levels of fruit consumption in patients with DM. On the other hand, DM duration, proportion of patients with insulin treatment, and baseline BMI and lipid profiles did not significantly differ among the three groups. We conducted an additional analysis of the energy and nutrient intake of the study population, with the results presented in Table 2. As expected, total energy intake, dietary fiber, vitamins, and minerals were significantly higher according to fruit consumption frequency. The intake of macronutrients (e.g., carbohydrate, protein, and fat) was also found to be higher with increasing fruit intake. Table 3 presents the ORs for dietary fruit intake and glycemic control as estimated by logistic regression models adjusted for risk factors. The OR for patients with good glycemic control (defined as HbA1c <7%) in the third tertile for fruit consumption was 3.48 (95% CI, 1.11 to 10.89; P<0.05) compared to the first tertile after adjusting for confounding variables.
In this study, we observed that fruit consumption had a significant beneficial impact on glycemic control in Korean patients with DM. There was a significant negative correlation between fruit consumption and HbA1c levels. Moreover, patients with the highest tertile of fruit intake were 3.48 times more likely to be in good glycemic control defined as HbA1c <7%. These results are expected to be very helpful for amending dietary recommendations for Korean patients with T2DM because 80% of these patients were consuming more fruits than the daily recommendations [14].
There has been a small number of prospective studies attempting to assess the effects of fruit intake on risk of diabetes, but the results have been inconsistent [15]. And these previous studies were primarily conducted among Western populations, and they tended to combine fresh fruit with processed fruit (and sometimes included fruit juice), rather than focusing only on fresh fruit, as our study did [15]. Compared to T2DM patients in Western countries, those in East Asian countries including Korea, are known to have different features regarding cardiovascular complications [2]. Moreover, there is very limited evidence about the effects of fruit consumption on risks of death and major vascular complications among people with established diabetes [16-18]. In two reports from the European Prospective Investigation into Cancer and Nutrition (EPIC) study, which involved patients with self-reported diabetes, one portion of fruit per day was found to be significantly associated with 12%± 15% lower all-cause [16] and cardiovascular mortalities [17]. There has only been one small study, in Japan, which reported the beneficial association of fruit consumption with diabetic retinopathy [19]. The previous Western studies [20-22] suggest that a high fruit intake does not have a negative impact on glycemic control. A previous study with Korean patients with T2DM found that the frequent intake of fish in all populations and the frequent intake of legumes in women were associated with good glycemic control [23]. In addition, the frequent intake of carbohydrates was associated with elevated HbA1c in women in this study. There is increasing evidence suggesting that dietary patterns emphasizing the consumption of plant foods may be effective at not only preventing the incidence of T2DM but also improving its management [24]. Fruit also contains sugars (i.e., glucose and fructose), which may have negative impacts on glycemic control [25]. However, the natural sugars in fruit may not be metabolized in the same way as refined sugars [26]. In particular, naturally occurring fructose from whole fruits is unlikely to be deleterious because of its relatively slow digestion and absorption [27]. The results of a related study showed that fruit intake may have no deleterious effect on HbA1c, weight loss, or waist circumference in patients with T2DM [20]. A recent review of most relevant studies concluded that higher fruit intake dietary pattern has beneficial effect on body weight and no studies have found a negative impact [28]. These benefits are partly attributed to a high fiber content and a low glycemic index of fruits which contribute to a lower postprandial rise in glucose by delaying gastric emptying which slows absorption of macronutrients [29]. A previous meta-analysis found that increased consumption of dietary fibers can reduce both fasting glucose concentration and HbA1c [30]. We found significant increased intake of dietary fibers according to fruit intake in this study. In addition to dietary fiber, fruits contain a wide range of specific bioactive substances that can act as merits to oxidation, inflammation, hypertension, atherosclerosis, and dyslipidemia through multiple metabolic pathways in the human body [10,31]. Intake of vitamins and minerals were also positively correlated with fruit consumption frequency in this study as shown in Table 2 [32]. These pleotropic effects of fruit consumption could result in positive effects on glycemic control in patients with T2DM. Moreover, patients with higher intake of fruit tend to have healthier lifestyles (more walking, better healthy eating index, less smoking and drinking), which may have resulted in better glycemic control. We did not find any effect on BMI or lipid profiles despite the difference in fruit intake among these three groups.
By contrast, it is still inconclusive whether fruit juices possess similar protective effects as whole fruits, and a meta-analysis showed that fruit juice may have no overall effect on fasting glucose and insulin concentrations [33]. One possible explanation for this is that fruit juice has less fiber than whole fruit and some added sugar in fruit juice products.
To our knowledge, this is the first study reporting beneficial associations of fresh fruit consumption in Korean patients with T2DM. In this type of study, whole dietary pattern is more important than specific nutrient intake [34]. Therefore, we measured total energy intake and adjusted total energy intake in logistic regression analysis. However, this study also has limitations. First, the potential for bias, i.e., measurement errors in dietary assessments, confounding factors, and informative censoring, cannot be ruled out entirely [35]. Second, in an observational study, as opposed to a randomized trial, it is impossible to conclude whether medical nutritional treatment encouraging increased intake of dietary fiber or vegetables and fruits would improve glycemic control in patients with T2DM in clinical practice. However, the findings of our study are statistically robust. Lastly, a difference in the baseline use of oral hypoglycemic agents could bias the results. We do not have detailed information regarding patient’s medication. However, we adjusted those on insulin treatment for the logistic regression analysis. We also admit that we cannot rule out the possibility that healthier people with better glycemic control may have consumed more fruit.
In conclusion, the overall evidence suggests that patients with T2DM will not deteriorate their glycemic control by adopting dietary patterns with more fruit intake. However, these results should be interpreted carefully and individually in Korea and other Asian countries where there are widespread doubts about eating fresh fruit among people with T2DM [36]. Additional large, well-conducted randomized clinical trials evaluating the effect of these dietary patterns on the incidence of complications in patients with T2DM are needed to further confirm their effectiveness and develop solid evidence-based scientific guidelines for diabetes prevention and management.

CONFLICTS OF INTEREST

No potential conflict of interest relevant to this article was reported.

AUTHOR CONTRIBUTIONS

Conception or design: Y.S.S. Acquisition, analysis, or interpretation of data: J.L., H.S.L., Y.S.S. Drafting the work or revising: J.L., Y.S.S. Final approval of the manuscript: J.L., H.S.L., J.P., K.S.K., S.K.K., Y.W.C., Y.S.S.

Acknowledgements
This work was supported by the Dong-A University research fund. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
This work was presented in 25th European Congress of Endocrinology as poster presentation (https://www.endocrine-abstracts.org/ea/0090/ea0090P638).
enm-2023-1730f1.jpg
Table 1.
Background Characteristics
Characteristic Tertile 1 Tertile 2 Tertile 3 P value
Number (sample count) 153 154 153
Weekly fruit consumption frequency 1.33±0.09 5.21±0.13 13.18±0.45 <0.001
Fruit consumption per day above the recommendation, %a 0.0 12.1 79.3 <0.001
Age, yr 51.84±0.93 51.45±0.82 54.39±0.78 0.021
Women, % 26.9 33.6 52.2 <0.001
BMI, kg/m2 25.61±0.47 25.24±0.34 24.87±0.24 0.300
Mean HbA1c, % 7.91±0.19 7.80±0.15 7.32±0.14 0.018
HbA1c <7%, % 42.0 35.9 51.3 0.080
Fasting plasma glucose, mg/dL 152.62±5.14 153.35±6.00 144.50±4.68 0.384
Duration of diabetes, yr 8.08±0.68 6.41±0.69 7.65±0.55 0.204
Treated with insulin, % 17.1 12.4 5.5 0.055
Treated with OHA, % 76.5 85.8 84.8 0.166
SBP, mm Hg 125.00±1.59 121.80±1.55 120.39±1.35 0.080
DBP, mm Hg 78.07±1.05 78.49±1.02 75.68±0.94 0.081
LDL cholesterol, mg/dL 102.96±4.42 103.12±3.86 101.14±4.11 0.930
HDL cholesterol, mg/dL 43.83±1.17 46.17±1.07 46.71±1.12 0.179
Triglycerides, mg/dL 234.12±28.60 215.25±26.89 162.16±9.25 0.016
Current smoker, % 36.9 33.2 16.0 0.009
Alcohol intake frequency per week, %b 0.030
 Never 28.5 25.5 34.3
 ≤Once 34.8 45.1 48.3
 >Once 36.7 29.4 17.4
KHEI total score (0–100)c 60.24±1.15 65.37±1.05 70.02±0.98 <0.001
Walking for ≥10 minutes, % 0.022
 7 days/week 27.0 34.1 30.2
 5–6 days/week 10.1 13.0 25.7
 3–4 days/week 22.8 19.6 15.3
 1–2 days/week 21.2 10.4 16.4
 0 day/week 18.8 23.0 12.3

Values are expressed as mean±standard deviation. All values except numbers are sample weighted. The study sample was divided into three groups based on weekly fruit consumption frequency: less than 2.82 times (tertile 1), 2.82–7.63 times (tertile 2), and more than 7.63 times (tertile 3).

BMI, body mass index; HbA1c, hemoglobin A1c; OHA, oral hypoglycemic agent; SBP, systolic blood pressure; DBP, diastolic blood pressure; LDL-C, low-density lipoprotein cholesterol; HDL-C, high-density lipoprotein cholesterol; KHEI, Korean Healthy Eating Index.

a Energy intake from fruits exceeds 100 kcal, which is equivalent to 2 exchange units of fruits [12];

b Values in the same row are significantly different at α=0.05;

c KHEI score range [13].

Table 2.
Energy and Nutrients Intake of the Study Population
Variable Tertile 1 Tertile 2 Tertile 3 P value
Total energy, kcal 1,781.74±71.251 (0.82±0.03)a 1,962.32±71.31 (0.92±0.03)a 2,111.62±68.91 (1.04±0.03)a 0.007 (<0.001)
Carbohydrate, g 287.03±10.31 (0.66±0.01)b 310.88±9.56 (0.65±0.01)b 349.58±10.10 (0.68±0.01)b <0.001 (0.032)
Protein, g 51.77±2.69 (0.11±0.002)b 62.45±2.83 (0.13±0.002)b 68.10±2.71 (0.13±0.002)b <0.001 (<0.001)
Fat, g 27.15±2.10 (0.06±0.003)b 34.47±2.00 (0.07±0.002)b 37.79±2.05 (0.07±0.002)b 0.002 (0.001)
Dietary fiber, g 15.30±0.63 (0.65±0.03)c 20.69±0.82 (0.89±0.03)c 27.19±0.92 (1.22±0.04)c <0.001 (<0.001)
Vitamin A, μgRE 412.62±26.83 (0.60±0.04)c 628.47±32.63 (0.92±0.04)c 763.01±36.65 (1.16±0.06)c <0.001 (<0.001)
Vitamin B1, mg 1.48±0.06 (1.26±0.05)c 1.78±0.07 (1.52±0.06)c 2.04±0.07 (1.77±0.06)c <0.001 (<0.001)
Vitamin B2, mg 0.93±0.06 (0.66±0.04)c 1.21±0.06 (0.86±0.04)c 1.35±0.06 (1.01±0.04)c <0.001 (<0.001)
Niacin, mg 10.20±0.52 (0.66±0.03)c 12.76±0.53 (0.83±0.03)c 15.09±0.58 (1.01±0.04)c <0.001 (<0.001)
Vitamin C, mg 41.46±2.21 (0.41±0.02)c 91.63±3.28 (0.92±0.03)c 170.69±5.64 (1.71±0.06)c <0.001 (<0.001)
Calcium, mg 346.95±18.35 (0.49±0.03)c 468.68±23.20 (0.66±0.03)c 539.55±23.50 (0.77±0.03)c <0.001 (<0.001)
Phosphorous, mg 794.98±34.74 (1.14±0.05)c 982.01±42.62 (1.40±0.06)c 1,108.26±39.41 (1.58±0.06)c <0.001 (<0.001)
Iron, mg 11.21±0.52 (1.20±0.06)c 14.13±0.59 (1.50±0.07)c 16.32±0.59 (1.83±0.07)c <0.001 (<0.001)
Potassium, mg 1,918.95±81.12 (0.55±0.02)c 2,669.39±108.43 (0.76±0.03)c 3,468.85±116.16 (0.99±0.03)c <0.001 (<0.001)
Sodium, mg 2,550.31±152.57 (1.28±0.08)c 3,272.59±160.75 (1.64±0.08)c 3,574.83±168.46 (1.79±0.08)c <0.001 (<0.001)

Values are expressed as mean±standard deviation.

a Energy intake ratio compared to Estimated Energy Requirements recommended by the Dietary Reference Intake for Koreans (KDRIs) [32];

b Macronutrient distribution into total energy intake;

c Nutrient intake ratio compared to adequate intake recommended by the KDRIs.

Table 3.
Odds Ratios and 95% Confidence Intervals (Logistic Regression Analysis) for Patients in Good Glycemic Control (Hemoglobin A1c <7%)
Variable Tertile 1 Tertile 2 Tertile 3
Crude model 1.00 (reference) 0.77 (0.45–1.34) 1.46 (0.84–2.55)
Model 1 1.00 (reference) 0.78 (0.45–1.35) 1.42 (0.81–2.48)
Model 2 1.00 (reference) 1.49 (0.62–3.59) 1.94 (0.79–4.77)
Model 3 1.00 (reference) 1.59 (0.67–3.81) 2.28 (0.88–5.89)
Model 4 1.00 (reference) 1.83(0.69–4.88) 3.63 (1.20–11.03)
Model 5 1.00 (reference) 1.92 (0.71–5.22) 3.48 (1.11–10.89)

Model 1 is adjusted by sex and age; Model 2 is adjusted by sex, age, body mass index, systolic blood pressure, triglycerides, low-density lipoprotein cholesterol, current smoking, and alcohol intake; Model 3 is adjusted by Model 2 plus total energy intake; Model 4 is adjusted by Model 3 plus walking per week and dietary fiber intake; Model 5 is adjusted by Model 4 plus insulin treatment.

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Figure & Data

References

    Citations

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    • The Relationship between Alcohol Consumption and Diabetes in Korean Adults
      Gi Tae Kim, Jae Woong Sull
      Biomedical Science Letters.2023; 29(3): 159.     CrossRef


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