1. Introduction
Nuts and dried fruit (DF) are traditional dietary components in many countries, and have been included in healthy diet patterns, such as the Dietary Approaches to Stop Hypertension (DASH) diet [
1,
2] and the Mediterranean diet (MedDiet) [
3], as they are a good source of dietary fibre, potassium, magnesium and antioxidants such as polyphenols [
4,
5]. The consumption of nuts was encouraged by the American Diabetes Association (ADA) in their nutrition recommendations [
6] as their benefits in cardiovascular disease prevention [
7] and glycaemic control [
8] had been well established. However, in contrast to nuts, DF may not be as easily accepted as a group of healthy food by the diabetic and people of impaired glucose tolerance because these dried fruits are considered to be high in sugar.
Recent studies showed that DFs such as raisins were medium-to-low glycaemic index (GI) food [
9,
10,
11], and could elicit favourable physiologic responses in terms of insulin secretion and appetite modulating hormones [
12]. Raisins were also reported for their benefits to cardiovascular disease risk factors including inflammation status, vascular endothelial functions, lipoprotein profiles [
11] and blood pressure control, when consumed as a substitution of highly processed snacks [
13]. Dried plums and dried apples showed effects on lowering serum hydroperoxides, C-reaction protein and low-density lipoprotein cholesterol (LDL-c) levels [
14]. Dried jujubes were traditionally regarded as healthy food and a source of phytochemicals in East Asian countries [
15,
16]. Based on these previous studies, it is reasonable to investigate the possibility of incorporating DF into a nutritious, low-GI and high-fibre diet, which has been suggested to be beneficial to the people at a high risk of diabetes.
Given the fact that DFs are high in sugar, in order to avoid a shift of the energy balance and macronutrient distribution, the consumption of DF should be considered to be a replacement of other foods rich in sugar or starch. In fact, DFs are traditionally consumed as an ingredient of carbohydrate-based food, such as bread, steamed bread, other baked foods and rice foods, in many cultures. However, the glycaemic response of mixed meal consisting of DFs and starch food, on the basis of the same amount of available carbohydrate, is rarely reported.
Previous studies showed that adding nuts such as almonds into white bread meals could suppress the postprandial glycaemic response [
17]. However, the effect of the combination of nuts and DF on blood glucose after a carbohydrate-based meal has not yet been investigated.
The aim of this study was to investigate the effect of several DFs on acute postprandial glycaemia in 240 min, either consumed alone or included in mixed meals of the same level of carbohydrate intake. We also examined the synergic contribution of DFs and nuts on the glycaemic excursion pattern when co-ingested with high-GI white rice.
4. Discussion
The present study demonstrated that the adding of dried fruits to white rice meals, on the basis of isoenergetic exchange for other carbohydrates (the total amount of carbohydrate was kept constant at about 50 g), did not increase the GI of the mixed meals, despite of the considerate amount of simple carbohydrates including glucose and fructose. The joint effect of DF and nuts resulted in significant reduction of GI values as well as the glycaemic excursion in 240 min.
To our knowledge, this is the first report on GI value of dried jujubes. Additionally, the GI values of dried apples and dried apricots in the present study were higher than those in previous reports, which were 29 and 30 [
29], respectively, while the GI of raisins (56) was comparable to the values for 64 [
29], 49 [
11] and 49–55 [
9] in previous reports. The differences of GI values could be explained by the variety differencesof the DFs, methods used to determine GIs, e.g., the glucose oxidase method, the hexokinase method, the glucose dehydrogenase method, etc., as well as the physiological and ethnic differences of subjects. It was reported that the same sample might elicit a higher postprandial glucose response in Asian subjects compared with that in Western subjects [
30].
Given the fact that the GI value of raisins in type 2 diabetes patients was lower than that determined in healthy subjects [
31], it could possibly incur hypoglycaemic episodes after 120 min when ingested in a large amount. The dried apple and dried jujube, which demonstrated stable blood glucose levels through 120–240 min, might be regarded as better snack choice for people of impaired glucose control.
There may be multiple factors affecting the glycaemic properties of DFs, which include: (1) unavailable carbohydrates such as insoluble fibre, oligosaccharides and pectin [
32,
33]; (2) the amount and profile of sugar, i.e., the contents of glucose, fructose and sucrose [
34,
35]; (3) digestion enzyme inhibitors such as polyphenols [
36]; (4) organic acid [
37]; (5) the physical texture and chewy properties of the food [
38].
Most of the abovementioned components were determined in this study. It was found that the glycaemic characteristics had no significant correlation with the contents of the total carbohydrate, dietary fibre, pectin, or organic acid. The dried apricot, which had the highest contents of total acid and pectin, and the raisins, which had the highest polyphenol contents and highest ORAC among the four dried fruits, failed to produce low GI values as the dried apple did. An analysis of 121 food GI tests showed that the dietary fibre content had no correlation with GI value [
39]. Another study found that neither the carbohydrate content nor the dietary fibre content was the determinant of the GI value of potato varieties [
40].
However, the sugar profile seemed to have an important impact on glycaemic responses of dried fruits. High intake of glucose component led to a rapid elevation of blood glucose within 60 min and a large range of fluctuation. The ratio of the amount of total fructose and total glucose in test meals had a very strong negative correlation with the iAUC
0–60, iAUC
0–120 and peak value. The low GI value of apples [
29] and its benefit to type 2 diabetes prevention found in prospective cohort studies [
41] may partly be explained by the fact that apples had a high content of total fructose and fructose/glucose ratio [
4].
Although a large amount of fructose may incur an adverse metabolic impact [
34], there is evidence that ‘catalytic’ doses of fructose from fruits could decrease the glycaemic response to high GI meals in human subjects without any unfavourable effects [
42]. Small amounts of fructose have been shown to decrease the hepatic glucose production while accelerate the glycogen production [
43], and thus, enhance hepatic glucose metabolism and result in better glycaemic control. A meta-analysis showed that isocaloric exchange of fructose for other carbohydrates could decrease the level of glycated blood proteins without affecting insulin in diabetes patients [
34]. However, another meta-analysis of diet-intervention studies found that 26–293 g of fructose ingestion promoted the development of hepatic insulin resistance in non-diabetic subjects [
44]. In the present study, the amount of total fructose in DApp + R, DJ + R and Ra + R diet was calculated to be 16.9 g, 12.9 g and 11.5 g, respectively, well below the threshold of 60 g/day [
45]. Such a low dose of isocaloric fructose exposure (35–45 g dried fruit) is unlikely to incur any adverse effect on other aspects of metabolic control.
A previous study showed that as low as 30 g of almonds exerted acute post-prandial benefits when added to a high GI carbohydrate-based meal [
17]. Preloading protein and fat prior to the ingestion of high carbohydrate could raise glucagon-like peptide 1 (GLP-1) levels and slow gastric empty rates, which contributes to reducing and delaying postprandial glycaemia [
46]. However, in the present study, the addition of almond reduced the peak glucose concentrations and the iAUC of the meals without changing the time when peak values were attained.
It is worth noting that in the Ra + A + R meal, the addition of rice to raisins prevented the possible hypoglycaemia after 120 min which was seen in a pure raisin diet, while the incorporation of almonds effectively attenuated the hyperglycaemia at 15, 60 and 90 min seen in a pure rice or raisin meal. The combinations of almonds, dried fruit and rice could produce a smaller MAGE
0–240 on a fixed amount of carbohydrate-based meal, while the minimised glycaemic excursion in the long term would be desirable for prevention of many complications associated with diabetes [
47]. Thus, the mixture of DF and nuts could possibly be developed as a healthy snack, tea break food or preload food for people who need to monitor their blood glucose levels, either the hyperglycaemia or hypoglycaemia patients.
To our knowledge, this is the first report on the joint effect of DF and nuts on glycaemic responses in carbohydrate-based meals. In the present study, all test meals were based on almost equal amounts of carbohydrates, and well accepted by all the subjects. The chemical components including dietary fibre, the pectin content, the polyphenol content, the sugar profile and the organic acid, which were possible contributors to postprandial glucose control, were determined before the blood glucose tests. The correlation analysis between food components and glycaemic characteristics of test meals led to a better explanation of research results.
There are several limitations of the present study. First, the study was carried out on healthy subjects. The results need to be confirmed in people of impaired glucose control in further studies. Second, this is an acute feeding study, which could not be directly extrapolated to a sustainable glycaemic mitigating effect in a longer period of time. Third, the insulinaemic response and the gastrointestinal hormones were not determined in this study, while they would provide a more in-depth glycaemic control mechanism of the mixed diet. Finally, we used a ONETOUCH
® Ultra
® blood glucose glucometer as a device to measure blood glucose. While a study found this small glucometer met ISO 15197 [
48], the evidence of accuracy of it is not strong. So, a comparison ofthe glycaemic responses using a ONETOUCH
® Ultra
® glucometer and a standard laboratory glucose analyser should be involved in the further study.
In conclusion, the present study demonstrated that dried fruits, including dried apples, dried jujubes, dried apricots and raisins, are medium or low GI foods, which would not elicit the excess rise in blood glucose concentrations when consumed as a substitute of high GI carbohydrate-based food. Moderate amounts of sugar, especially the fructose from dried fruit, may help postprandial glycaemic control. Taking the nutrient profile and antioxidants of dried fruits into account, they may have the potential of being included into a blood-glucose-managing diet without altering the total carbohydrate intake. The combination of dried fruit and nuts could further ensure a small postprandial glycaemic excursion in a diet and the underlying mechanism of their synergic effects deserves future investigation.