Fruit form influences postprandial glycemic response in elderly and young adults

Abstract

Objectives

This study compared the effects of consuming different forms (bite size, puree) and two fruit types (guava, papaya) on glycemic response (GR) in elderly and young adults.

Design

This study was conducted using a randomized, crossover design.

Participants

Nineteen healthy participants (9 elderly, 10 young adults) were recruited from the general public in Singapore. Intervention: Participants consumed glucose (reference food) on three occasions and test fruits (guava bites, guava puree, papaya bites, and papaya puree) on one occasion each.

Measurements

Blood glucose was analyzed prior to consuming the test food, at 15, 30, 45, 60, 90 and 120 minutes after food consumption.

Results

The incremental area under the blood glucose response curve (iAUC) over 120 minutes for all the treatments was significantly lower than glucose (all P < 0.001). All fruit forms and types studied were low glycemic index (GI) (guava bites: 29; papaya bites: 38; papaya puree: 42; guava puree: 47), albeit a significant difference in GI between the treatments was found (P = 0.003). Elderly exhibited significantly greater GR than young participants (P = 0.019).

Conclusion

Although fruit form influences GR in the elderly and young adults, all fruit types and forms studied were found to be low GI. This study indicates that fruits are a valuable source of nutrient irrespective of the form of delivery in elderly and young adults. This study was registered at www.anzctr.org.au as ACTRN12614000655640.

Abbreviations

CV

coefficient of variation

GI

glycemic index

GR

glycemic response

iAUC

incremental area under the curve

VAS

visual analog scale

Introduction

Ageing is often associated with a decline in skeletal muscle mass while an increase in fat accumulation (1, 2, 3, 4). These agerelated physiological changes coupled with unfavorable dietary patterns may predispose elderly to insulin resistance and metabolic syndrome (5, 6, 7, 8, 9). Fruits are naturally rich in fiber, bioactive constituents and water content while low in energy density. A diet high in fruits, which is nutrient-dense but low in energy density, may aid in body weight management and lower chronic disease risk (10, 11, 12). Despite the current recommendation to consume fruits regularly as part of a healthy diet (13, 14, 15), previous studies have demonstrated that individuals, particularly those with type 2 diabetes, avoid fruit consumption due to the misconception that the consumption of fruits which are high in fructose, sucrose, and glucose may adversely affect glycemic response (16, 17, 18). However it is important to highlight that fruits contain a wide array of phytochemicals and is an important source of dietary fiber (10, 11, 19). Previous studies have shown that glucose results in much greater spike in blood glucose compared to fructose and the glycemic index of glucose is almost 7-fold higher than fructose (100 vs. 15) (20, 21).

Epidemiological studies have shown that fruit juices were positively associated with incidence of type 2 diabetes, whereas whole fruits may contribute to a decreased incidence of type 2 diabetes (22, 23, 24, 25). It is important to note that there are a few subgroups of the population such as elderly or people with dentures who may find whole fruits difficult to consume (26, 27). Hence fruits in smaller particle size like puree may be more acceptable for these individuals. However, the consumption of small particle size fruits (e.g. puree) with short oral residence time and high eating rate may lead to larger spikes in glycemic response than fruits with larger particle size (e.g. bites) (28). Further to this, it is unclear whether age modifies the effect of fruit form on postprandial glucose. Thus, it will be of interest to compare the glycemic response to different forms of fruits in elderly and young adults due to differences in chewing behaviors, blood glucose and insulin sensitivity between these two age groups (6, 7, 8, 27, 29, 30). The GI values for fruits range widely, thus understanding the role of fruit forms and types in glycemic response in different population groups could influence advocacy for pre-diabetics and diabetics. This finding could also facilitate better public health approaches to promote fruit consumption as a means to improve health outcomes in the general population.

Methods

Participants

Nineteen healthy participants (9 elderly and 10 young adults) were recruited from the general public in Singapore through the distribution of flyers around the university campus and participants from previous studies who had consented to be contacted for future studies. The inclusion criteria were healthy adults between the ages of 21 and 35 years (young adults) or between the ages of 56 and 75 years (elderly). The exclusion criteria were people with major chronic disease such as cancer, diabetes or heart disease, people with family history of diabetes, individuals with food intolerances or allergies to study foods, individuals who are taking insulin or drugs known to affect glucose metabolism and body fat distribution, people with a major medical or surgical event requiring hospitalization within the preceding three months, individuals with the presence of disease or drugs which influence digestion and absorption of nutrients, and pregnant women.

Singapore National Healthcare Group Domain Specific Review Board approved the study protocol (reference number: 2014/00057). All participants provided written informed consent.

Test foods

The four test foods included guava bites, guava puree, papaya bites, and papaya puree. Guava and papaya were chosen as the test fruits as they are popular tropical fruits in Southeast Asia and they differ in their sensory properties, i.e. color, smell, taste, and texture. Glucose beverage was used as a reference food. All the test products (guava: 280 g; papaya: 274 g; glucose beverage: 250 mL) were given in portions containing 25 g of available carbohydrates. The nutrient composition of the test products were obtained from USDA National Nutrient Database for standard reference 26 software v1.4. The total soluble solids content of the fruits were estimated immediately before serving to the participants by using a refractometer (Atago PAL-1) to measure the refractive index (°Brix) of puree from guava (mean ± SD: 8.8 ± 1.4) and papaya (mean ± SD: 9.5 ± 1.6).

Study procedures

The study was conducted using a randomized, crossover design. All participants were asked to attend eight visits in total; one screening session and seven testing sessions. The seven testing sessions, consisted of three testing sessions for glucose beverage and one testing session for each fruit product (guava bites, guava puree, papaya bites, papaya puree). Participants were randomly allocated to the seven testing sessions, with the order balanced.

During the screening visit, participants were asked to complete a questionnaire, in regards to food allergies or intolerance, chronic diseases, and physical activity level. Body weight and body composition were measured using Cosmed BodPod Gold Standard (Bod Pod 2007A). A stadiometer (Seca) was used to measure participants' height in order to calculate body mass index (BMI). Blood pressure was measured using an Omron blood pressure monitor (HEM-907).

During each testing session, participant's glycemic response to the test product was measured. Participants were asked to refrain from vigorous physical activity the day before the testing session. They were also asked to consume a meal of similar composition and quantity on the evening before the test session. Participants attended the testing session after an overnight fast of ten hours. Fingerprick blood samples were obtained 5 minutes apart (–5 and 0) for blood glucose measurement using HemoCue® cuvette (Helsingborg, Sweden). Participants were then given the glucose beverage or the test food (guava or papaya, bites or puree) to consume within 15 minutes. Further blood samples were obtained at 15, 30, 45, 60, 90 and 120 minutes for blood glucose measurements after the commencement of test food consumption. Participants were asked to rest and keep their physical activity to a minimum during testing. Blood glucose measurements were performed by two qualified researchers.

Calculation of glycemic index

Glycemic index was determined using the international standard guidelines described in ISO 26642:2010 (31). For each participant, the iAUC for blood glucose was calculated for both the reference food and test fruits. The total GR over 120 minutes was expressed as the iAUC ignoring the area under the baseline using the trapezoidal rule (32). The mean, SD and coefficient of variation (CV) of the iAUC of each participant's repeated glucose beverage was calculated. Using the iAUC values, the GI of the test fruits were calculated using the following formula: GI= (iAUC for the test fruit/Average iAUC for the reference food)*100.

Statistical analysis

A sample size of 6 to 10 participants was recommended for GI and GR studies to avoid type 2 errors (31, 32, 33). In order to detect a difference of 15 unit in GI [equivalent to the difference between products classified as low GI (e.g. 55) and high GI (e.g. 70)] between any two treatments, 10 participants would be required for each age group.

Baseline characteristics of the study participants were presented as arithmetic means and standard deviations. An independent samples t-test was used to compare the baseline characteristics between the two age groups (i.e. elderly and young adults). Linear mixed models with a random subject effect were used to investigate the effects of different forms and types of fruits on ‘glycemic response' and ‘glycemic index'. The models included a term ‘age' for assessing the influence of age on ‘glycaemic response' and ‘glycaemic index'. The influence of the following variables: ‘fasting blood glucose', ‘gender', ‘BMI', ‘waist circumference', ‘hip circumference', and ‘percent body fat measured by BODPOD' on study outcomes were also assessed in separate models. Stata 11.1 (StataCorp, College Station, Tex, USA) was used to perform all statistical analyses. Two sided P < 0.05 was considered statistically significant in all cases.

Results

As shown in Table 1, ten young adults (5 male, 5 female) and nine elderly (5 male, 4 female) completed the study. The mean (SD) age of the young adults and elderly were 24.4 (2.35) years and 64.2 (5.10) years respectively, mean (SD) BMI of the young adults and elderly were 21.2 (2.63) kg/m² and 24.4 (5.97) kg/m² respectively, and mean percent body fat from BODPOD for the young adults and elderly were 23.9% and 31.1% respectively. There was no significant difference in any of the anthropometric measurements between the young adults and elderly (all P ≥ 0.061). However the fasting blood glucose (4.54 vs. 5.08 mmol/L, P = 0.010), systolic blood pressure (102 vs. 130mm Hg, P = 0.003) and diastolic blood pressure (62 vs. 75 mm Hg, P = 0.026) were statistically significantly lower in the young adults compared to elderly. The mean intraindividual CV for the reference glucose beverage was 16.8% in the young adult group and 10.1% in the elderly group.

Table 1.

Baseline characteristics of study participants

	Young Adults (n= 10)	Elderly (n = 9)	P value
Age (years)	24.4 (2.35)	64.2 (5.10)	<0.001
Height (cm)	167 (8.17)	164 (10.4)	0.530
Weight (kg)	59.1 (10.4)	68.7 (14.9)	0.116
BMI (kg.m-2)	21.2 (2.63)	24.4 (5.97)	0.136
Waist circumference (cm)	69.3 (7.70)	79.2 (13.4)	0.061
Hip circumference (cm)	91.3 (6.90)	95.1 (10.9)	0.377
Fasting blood glucose (mmol/L)	4.54 (0.11)	5.08 (0.15)	0.010
Systolic blood pressure (mm Hg)	102 (15.5)	130 (20.5)	0.003
Diastolic blood pressure (mm Hg)	62.1 (9.37)	74.9 (13.3)	0.026
Pulse (bpm)	67.9 (9.24)	64.5 (12.6)	0.508
Body fat (%)	23.9 (10.0)	31.1 (14.1)	0.235
Fat Mass (kg)	14.0 (6.30)	21.3 (12.4)	0.135
Fat Free Mass (kg)	45.3 (12.2)	44.6 (12.1)	0.917
Estimated RMR (kcal/day)	1224 (310)	1238 (321)	0.927

All values are means (standard deviations)

There were significant differences in the iAUC for the glycemic response over 120 minutes between the treatments (Figure 1). The iAUC for all the fruit types and forms were significantly lower than the glucose beverage (all P < 0.001). In addition, the iAUC for guava bites was significantly lower than the iAUC for guava puree (mean difference = -32, P = 0.002), papaya bites (mean difference = -22, P = 0.040), and papaya puree (mean difference = -25, P = 0.016). No statistical significant difference was found between guava puree and papaya bites (P = 0.320), guava puree and papaya puree (P = 0.526), as well as papaya bites and papaya puree (P = 0.719). The mean ± standard error iAUC for glucose beverage was 194 ± 18 (young adults = 162 ± 19; elderly = 231 ± 26), guava bites was 55 ± 7 (young adults = 43 ± 9; elderly = 68 ± 8), guava puree was 87 ± 8 (young adults = 69 ± 9; elderly = 107 ± 9), papaya bites was 76 ± 10 (young adults = 62 ± 12; elderly = 93 ± 14), and papaya puree was 80 ± 10 (young adults = 61 ± 8; elderly = 101 ± 16). There was significant difference in glycemic response between the young adults and elderly, in which the iAUC increased by 0.91 with each increase in one year of age (P = 0.019). Results remained unchanged after adjusting for fasting blood glucose (P = 0.102), gender (P = 0.247), BMI (P = 0.422), waist circumference (P = 0.405), hip circumference (P = 0.139), and percent body fat measured by BODPOD (P = 0.564).

Figure 1.

Mean (± SE) temporal curves of the blood glucose response for glucose beverage, guava bites, guava puree, papaya bites, and papaya puree in young adults (n = 10) (Figure 1A), elderly (n = T 9) (Figure 1B), and all participants (n = 19) (Figure 1C)

A statistically significant difference in GI was found between the treatments (overall P = 0.003) (Figure 2). The GI for guava puree and papaya puree were significantly higher than the guava bites (both P < 0.01). There was also a tendency that the GI for the papaya bites was higher than the guava bites (P = 0.068) and the GI for the papaya bites to be lower than the guava puree (P = 0.079). However, no significant differences were found between guava puree and papaya puree (P = 0.351) as well as papaya bites and papaya puree (P = 0.409). The mean ± standard error glycemic index for guava bites was 29 ± 4 (young adults = 28 ± 7; elderly = 31 ± 4), guava puree was 47 ± 4 (young adults = 45 ± 6; elderly = 49 ± 4), papaya bites was 38 ± 2 (young adults = 38 ± 4; elderly = 39 ± 2), and papaya puree was 42 ± 5 (young adults = 40 ± 6; elderly = 46 ± 9). Results remained the same after adjusting for age (P = 0.749), gender (P = 0.889), BMI (P = 0.341), waist circumference (P = 0.199), hip circumference (P = 0.238), and percent body fat measured by BODPOD (P = 0.899).

Figure 2.

Glycemic index for guava bites (white bars), guava puree (dark gray bars), papaya bites (light gray bars), and papaya puree (black bars) in young adults (n = 10), elderly (n = 9), and all participants (n = 19). Bars with different lower case letters are significantly different, P < 0.05

Discussion

To our knowledge, this is the first trial of its kind to investigate the effects of consuming different types and forms of fruits on postprandial glycemic response in elderly and young adults. Our study showed that fruit form influences GR in both elderly and young adults. It is reassuring that all forms and types of fruits were found to be low GI. Public health messages should promote the intake of fruits, which is low energy-dense but nutrient-dense foods, as a means to improve glycemic control and diet quality in the elderly.

The present study showed that consumption of the guava bites and papaya bites resulted in a lower glycemic response compared to guava puree and papaya puree. This is in line with the previous research by Bolton and colleagues, who reported that participants who consumed oranges with a larger particle size had lower plasma glucose values during their post absorptive period compared to orange juice (34). In addition, the present study found a significant difference in glycemic response between the elderly and young adults, in which the iAUC increased by 0.91 with each increase in one year of age. We postulate that the different glycemic response to different forms and types of fruits between the elderly and young adults could be due to the differences in their oral processing ability. Walls and Steele reported that elderly may have loss of muscle mass, muscle forces and lack of teeth, hence leading to less mastication efficiency compared to the younger population (30). This was supported by Laguna and colleagues, whereby participants from the United Kingdom showed a decline in their biting force as age progressed (29). One would hypothesize that the reduced efficiency of food particle size reduction and bolus formation would blunt the glycemic response (35) in elderly. However the opposite was found in the current study, whereby the elderly consistently exhibited greater GR to the test fruits and the glucose beverage. Hence the GI values (GR to the test fruit divide by the GR to the glucose beverage) of all the test fruits obtained in young adults were similar to the elderly. Future studies should elucidate the mechanisms underlying the exaggerated GR in the elderly, e.g. decreased β cell function or reduced insulin sensitivity (6, 7, 8).

Glycemic index is a useful method for classifying carbohydrates, by comparing carbohydrates gram for gram in food (36). A lower GI food is believed to be better with a slower rate of digestion and absorption of the sugars and starches in food. Consequently, it may keep the consumers fuller for longer. Although a significant difference in GI was found between the treatments, it is important to highlight that guava and papaya in both bite size and puree forms were low GI. This can be explained by the comparable amount of total soluble solids content (°Brix) in guava (8.8 ± 1.4) and papaya (9.5 ± 1.6). Previous studies performed in a healthy population or people with type 2 diabetes reported that the GI of papaya range from 45 to 60 (20, 37, 38). Currently there is very limited evidence on the health benefits of guava consumption in humans (39). The present study is the first to show that guava in bite size and puree forms are low glycemic index and hence guava has the potential to exert hypoglycemic effect in both elderly and young adults. Guava and papaya are high in fiber, antioxidants and phytochemicals which may explain the low glycemic indices found in the present study (12). A recent long-term study has shown that low GI fruit consumption was associated with significant improvement in HbA1c concentration, blood lipid, and coronary heart disease risk in 152 individuals with type 2 diabetes (40). Given that fruits contain varying amount and types of antioxidants and phytochemicals, the public should be encouraged to consume a variety of fruits. In addition, it is important to promote fruit intake among elderly as a means to improve their diet quality as a recent study reported that Japanese elderly living alone or those living with non-spouse family had poor dietary intake, e.g. low fruit intake (41).

Conclusion

The present study found that fruit form appears to influence GR in the elderly and young adults. Fruits with smaller bite size showed a greater spike in GR compared to fruits with larger bite size. The GI of fruits was not significantly different between elderly and young adults. Given that all the fruit types and forms studied were low GI, elderly or individuals with dentures who find whole fruits difficult to consume can be encouraged to consume fruit puree. Elderly who restricts fruits with the assumption that fruits increase blood glucose may be reassured that consuming guava and papaya in either puree or whole is both practical and useful nutritional advice.

Acknowledgments: This work was supported by the Singapore Institute for Clinical Sciences, Agency for Science, Technology and Research (A*STAR), Singapore. The authors would like to thank the volunteers for taking the time to participate in the Fruit Study and Alexander Mok for his assistance with data collection.

Authors' contributions: SLT and DEML contributed equally to this work. SLT, DEML, and CJH designed the study; SLT and DEML conducted the research; SLT analyzed the data; SLT and DEML wrote the manuscript; CJH revised the manuscript. All authors read and approved the final manuscript.

Conflicts of Interest: The authors declare no conflicts of interest.

Ethical standards: Singapore National Health Care Group Domain Specific Review Board approved the Study Protocol (reference number: 2014/00051). All participants provided written informed cosent.