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Effects of a Controlled Diet Supplemented with Chickpeas on Serum Lipids, Glucose Tolerance, Satiety and Bowel Function

School of Human Life Sciences, University of Tasmania, Launceston, AUSTRALIA

Address reprint requests to: Professor Madeleine Ball, Head of School of Human Life Sciences, University of Tasmania, Locked Bag 1320, Launceston, Tasmania 7250, AUSTRALIA. E-mail: Madeleine.Ball{at}utas.edu.au

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Objective: To compare the effect of a diet supplemented with chickpeas to a wheat-based diet of similar fibre content on serum lipids, glucose tolerance, satiety and bowel function. A third, lower-fibre wheat diet provided further information on dietary fibre quantity and bowel function and satiety.

Method: Twenty-seven free-living adults followed two randomized, crossover dietary interventions each of five weeks duration. The chickpea diet included canned drained chickpeas, bread and shortbread biscuits containing 30% chickpea flour. The wheat diet included high-fibre wheat breakfast cereals and wholemeal bread. The diets were isoenergetic to the participants’ usual diet, matched for macronutrient content and controlled for dietary fibre. Following on from the second randomised intervention, a sub-group of 18 participants underwent a third, isoenergetic lower-fibre wheat diet that included low-fibre breakfast cereals and bread.

Results: Repeated measures ANOVA revealed reductions in serum TC of 0.25 mmol/L (p < 0.01) and LDL-C of 0.20 mmol/L (p = 0.02) following the chickpea diet compared to the wheat. An unintended significant increase in PUFA and corresponding decrease in MUFA consumption occurred during the chickpea diet and statistical adjustment for this reduced but did not eliminate the effect on serum lipids. There was no significant difference in glucose tolerance. Perceived general bowel health improved significantly during the chickpea diet although there was considerable individual variation. Some participants reported greater satiety during the chickpea diet.

Conclusions: The small but significant decrease in serum TC and LDL-C during the chickpea diet compared to the equivalent fibre wheat diet was partly due to unintentional changes in macronutrient intake occurring because of chickpea ingestion. If dietary energy and macronutrients were not controlled, chickpea consumption might result in greater benefits via influence on these factors.

Key words: chickpeas, cardiovascular disease, cholesterol, diet, dietary fibre

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Examination of the literature reveals a gradual development of interest in the contribution of legumes and pulses to a healthy lifestyle, as awareness of ethnic diets and lifestyles has grown [1–5]. Chickpeas are a common component of traditional diets of Asian, Mediterranean, Arab and South American communities [6,7]. In contrast to most other pulses and cereals, chickpeas have a relatively high fat content [8–10]; however, the fat is composed mostly of polyunsaturated fatty acids (PUFA), with less than 1% saturated fatty acids (SFA). Although chickpeas contain less carbohydrate than, for example, wheat [9], the starch contained has a higher amylose content (30–40% compared to 20%) [10–12] and the amylose has a greater degree of polymerisation (1667 glucose residues compared to 540) [13]. This renders chickpea starch more resistant to digestion in the small intestine, resulting in lower bioavailability of glucose [11, 13, 14] and higher availability of substrate for colonic fermentation — contributing to improved bowel health [12,13].

Compared to cereal grains, legumes overall are a very good source of dietary fibre [15,16]. Dietary fibre includes resistant starch, non-starch polysaccharide (cellulose, hemicellulose, pectin, gums and ß-glucans), non-digestible oligosaccharides and lignin [15, 17–20]. Dietary fibre can be differentiated into soluble (pectin, gums and ß-glucans) and insoluble fibre (cellulose, hemicellulose, non-digestible oligosaccharides and lignin) [15, 19, 20]. While the ratio of soluble to insoluble fibre in legumes is comparable to grains (approximately 1:3 for both) [16] per 100g edible portion, chickpeas contain 17.4g total dietary fibre compared to 12.7g for wheat [9].

Increased consumption of soluble, viscous fibre has been associated with decreased serum total cholesterol (TC), decreased serum low density lipoprotein-cholesterol (LDL-C) and inversely correlated with coronary heart disease (CHD) mortality rates [17, 19–23]. The association between increased consumption of insoluble fibre and reduced risk of CHD is not as strong as with soluble fibre [23,24]. Higher consumption of dietary fibre, in particular resistant starch, has been associated with improved glucose tolerance and insulin sensitivity [15,20,25]. Dietary fibre may also be beneficial in the fight against obesity. It has been suggested that a state of satiety may be reached faster and last longer after ingestion of higher fibre foods because they are bulkier and take longer to eat than lower fibre foods [19,26] and delay gastric emptying [20,27]. Increased consumption of dietary fibre has also been associated with improved bowel health and stool consistency [15,27,28].

Even though chickpeas are a common constituent of many ethnic diets and are rich in PUFA and dietary fibre — resistant starch in particular, there has been little research into chickpeas and human health compared to other legumes. The focus of the current study was an investigation into the effect of substituting wheat-based foods with chickpeas on serum lipid profiles, long-term glucose tolerance, bowel function and satiety. The study compared the results of a chickpea-supplemented dietary intervention (test diet) to an isocaloric wheat-based intervention (control diet), both of five weeks duration. A small, sub-study compared the effects of a three-week, isocaloric, lower-fibre wheat diet to that of the wheat diet, to evaluate the effect of amount of fibre as well as source of fibre on bowel health and satiety.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Participants
Adults less than 70 years of age not taking medication for hyperglycaemia or hyperlipidaemia were invited to participate. All participants gave written informed consent and were free to leave the study at any time. The Northern Tasmanian Health and Medical Human Research Ethics Committee approved the study (application no. H7142).

Study Design
The study followed a randomised crossover design using two controlled dietary intervention periods - chickpea or wheat-based, each of five weeks duration. A washout-period of six to eight weeks separated the two dietary periods, during which time participants resumed their normal diet. Following on from the second randomised dietary phase, some participants commenced a third lower-fibre wheat-based dietary intervention (lower-fibre diet) of three weeks duration. Twelve participants agreed to have their bowel transit time (BTT) measured during the final week of each dietary period.

Diet Design
Prior to commencing the study, participants weighed and recorded four days of usual dietary intake, which was analysed using Foodworks 2.1 computer software (Xyris, Brisbane, Australia). This "usual" record helped formulate individual isoenergetic chickpea and wheat intervention diets. The diets were comparable in energy, protein, carbohydrate, total fat and dietary fibre - except for the lower-fibre diet that contained approximately half the amount of dietary fibre as the wheat. Every effort was made to maintain consistent consumption of type and quantity of dietary fats (oil, spread, cheese, milk, yoghurt, ice cream) during each phase. Four-day records of weighed dietary intake were analysed to determine participant nutrient intake for each dietary period.

Participants refrained from eating any foods with cholesterol-lowering claims, (e.g. margarine containing phytosterols), legumes (other than the chickpeas supplied) or foods with high fibre claims (e.g. "fibre enriched" yogurt or fruit juices) and maintained their usual pattern of physical activity throughout the study period.

Chickpea Diet (Test Diet).
This intervention was based on the daily consumption of 140g of canned, drained chickpeas (Edgell 300g net weight, Simplot Australia) plus bread and shortbread biscuits - made with 30% chickpea flour. Chickpea based foods contributed approximately 3.4 MJ of energy per day from protein (16%E), total fat (19%E), carbohydrate (65%E) and approximately 27g of dietary fibre. Wheat diet (control diet): This intervention was based on the daily consumption of wholemeal (wheat) bread and higher wheat fibre breakfast cereals (> 3.0g fibre /100g).

Lower-Fibre Wheat Diet.
Designed to provide comparative information on bowel function, utilised white bread and lower wheat fibre breakfast cereals (< 3.0g/100g).

Questionnaires
Participants completed questionnaires concerning stool consistency, bowel function and satiety after the first and final week of each dietary intervention. Visual analogue scales (150mm) anchored with descriptors aided assessment of frequency and ease of defecation, frequency of flatulence, perceived bowel health and satiety. To determine stool consistency, participants referred to the Bristol Stool Form Scale [29].

Laboratory Measurements
Collection of venous blood samples followed overnight fasting for ten hours. Serum and plasma aliquots were stored at –70°C until analysis. Serum TC, triacylglycerols, high-density lipoprotein cholesterol (HDL-C) and plasma glucose were assayed in the same run for each participant, using an RA 1000 auto analyser (Technicon, USA) and Thermotrace reagents (Thermo Electron Corporation, USA). Friedewald's equation was used to calculate LDL-C [30]. Serum insulin was measured using Insulin Radioimmunoassay Kits (Diagnostic Systems Laboratories Inc., Australia) and an LKB multi gamma counter plus RiaCalc software (Version 3). The homeostasis assessment model of insulin resistance (HOMA-IR) equation was used to calculate basal insulin resistance [31]:

HOMA-IR = fasting insulin (µIU/ml) x fasting glucose (mmol/L) / 22.5.

Bowel Transit Time (BTT)
Twelve consenting participants received gelatine capsules containing radio-opaque markers of different sizes and shapes. Ingestion of the markers and subsequent collection of the faecal samples used to ascertain BTT, occurred in the final week of each dietary period. Examination by x-ray determined the number and shape of radio-opaque markers present in each sample. Calculation of bowel transit time utilised the following equation [32]:

Statistical Analysis
STATA Statistical Data Analysis, version 8.2 (STATA 8.2 Statacorp, USA) was used for statistical analysis. Repeated measures ANOVA using General Linear Modelling (GLM) was used to compare results for each of the diets and to examine the effect of diet and dietary components on serum lipid profile and glucose tolerance. Answers from the questionnaires were analysed using Wilcoxon's Signed Rank Test for non-parametric data.

	RESULTS

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Subject Description
Thirty-one participants commenced the first, randomly assigned, intervention period - either chickpea- or wheat-based. Four participants failed to complete both the diets, three due to employment commitments and one due to discomfort attributed to chickpea consumption. The mean age (± SD) of the remaining twenty-seven participants (17 women and 10 men) was 50.6 ± 10.5 years and BMI 28.8 ± 4.4 m/kg². The mean fat content of their "usual" diets was 87.66 ± 28.31 g/day (33% of energy) and the amount of dietary fibre consumed was 27.9 ± 7.1 g/day. Eighteen participants (11 women, 7 men) agreed to undergo the third, low-fibre wheat diet during which they consumed 15.2 ± 1.6 grams of fibre per day.

Nutrient Content of Diets
Table 1 shows the nutrient intake as recorded by study participants in the final week of the chickpea- and wheat-based diets. Similarity in body weight at the end of each diet suggests total macronutrient intake was comparable. There was a significant difference in mean consumption of protein, as a percentage of energy consumed, between the diets even though the difference was only one percent of energy consumed (p=0.04). This difference may have been due to substitution of meat or other higher-protein foods with chickpeas during the chickpea phase.

Effect of Chickpea Diet on Serum Lipids and Glucose Tolerance
Table 2 shows the results of serum lipid profiles, glucose, insulin and insulin resistance (HOMA-IR score), for the chickpea- and wheat-based diets, adjusted for order of diet and chronological period of measurement. There was a significant reduction in mean serum TC of 0.25 mmol/L (p< 0.01) and LDL-C of 0.20 mmol/L (p=0.02) during the chickpea diet compared to the wheat (Table 2). Results for glucose, insulin and insulin resistance (HOMA-IR score) were not significantly different.

The diets were then classified into those components that the subjects were advised to include in their diet in order to create the differences between the diets (the chickpea- and wheat-based foods), and those components that were common to both diets. The effect of the chickpea versus the wheat diet was again compared, this time after adjustment of the common diet for PUFA and fibre content. The difference in mean serum TC was reduced on the chickpea diet from 0.25 mmol/L (p<0.01) to 0.12 mmol/L (p=0.18) and mean LDL-C from 0.20 mmol/L (p=0.02) to 0.07 mmol/L (p=0.27) by adjustment for PUFA. The singular effect of PUFA on serum TC and LDL-C was again much greater than the effect of dietary fibre. This time, one standard deviation increase in PUFA was associated with a mean decrease in serum LDL-C of 0.26 mmol/L, compared to a mean decrease of 0.05 mmol/L for one standard deviation increase in dietary fibre.

Effect of Diet on BTT and Appreciation of Bowel Function by Subjects
Table 2 also shows the results of BTT for the intervention diets, adjusted for order of diet and chronological period of measurement. For the chickpea-wheat comparison, results for eight of the 12 participants showed very little difference in BTT due to diet, while results for four individuals were markedly longer during the chickpea diet compared to the wheat. Consequently, the mean BTT was 10.6 hrs longer during the chickpea diet compared to the wheat (p=0.02). For the higher-lower wheat fibre comparison, the mean BTT was 8.8 hrs longer during the lower-wheat fibre diet compared to the higher (p=0.03), with the majority of participants showing a longer BTT during the lower-wheat fibre dietary period. Fig. 1 demonstrates the wide variability of results from participants who underwent a BTT during each of the three dietary periods.

View larger version (36K): [in this window] [in a new window]   Fig. 1. Comparison of bowel transit times between the chickpea, wheat and low-fibre wheat diets for each participant (n = 10).

For the higher-lower wheat fibre subgroup comparison, participants recorded a variety of effects on stool consistency (hard to mushy) throughout each of the dietary periods. There were no significant differences detected in frequency of defecation or perceived bowel health - the participant who reported "terrible" bowel health during the wheat phase of the chickpea-wheat comparison did not undertake the lower-fibre wheat diet. Ease of defecation was slightly reduced from usual during the lower-fibre wheat diet and marginally easier during the higher-fibre wheat but no significant difference was detected (p=0.06). Frequency of flatulence on the other hand, was reported as significantly greater during the higher-fibre wheat diet in week 5 (p=0.02). While the degree of satiety did not alter during the lower-fibre wheat diet, again, satiety was significantly higher during the higher-fibre wheat diet, after both one and five weeks (p0.01).

	DISCUSSION

 
Significant reductions in serum TC and LDL-C followed five weeks consumption of a chickpea-supplemented test diet compared to a wheat-based control diet of similar dietary fibre content. Statistical analysis suggested that an unanticipated change in fatty acid composition during the chickpea diet (particularly PUFA) was related to the reductions in serum TC and LDL-C. Adjusting the data to take account of the effect of PUFA substantially reduced, but did not abolish, the difference in serum TC and LDL-C between the chickpea and wheat diets. This suggests some other component or components of chickpeas were responsible for 40% of the effect of the chickpea diet on serum TC and LDL-C. A meta-analysis investigating the hypocholesterolaemic effect of non-soy pulses on serum lipids [33] concluded that while soluble dietary fibre contributed the greatest effect, other factors such as oligosaccharides, isoflavones, phospholipids and fatty acids, phytosterols, saponins, other vitamins and minerals also played an important role. Even so, the authors concluded it was the sum of the whole rather than individual components that were responsible for the hypocholesterolaemic effect of pulses.

The absence of observed effect of dietary fibre on serum TC and LDL-C may have been due to the similar dietary fibre content of the chickpea and wheat diets (28.73 vs. 27.86 g/day) coupled with the similar ratio of soluble to insoluble fibre present in chickpeas and wheat. Furthermore, the dietary fibre intake during the chickpea and wheat diets was very similar to the mean "usual" intake of this group of participants (27.9 ± 7.1 g/day). While a number of studies have investigated the effect of high fibre in addition to other dietary components on glucose tolerance and hyperlipidaemia [34–39] only a few have investigated the effect of high dietary fibre intake alone [40]. All of these studies compared intervention diets containing at least two to three times more dietary fibre (primarily insoluble fibre) than the control or usual diet - in some cases, five or six times greater [34,35,37]. It has been suggested that cholesterol-lowering by high fibre diets is best observed in studies where the dietary fibre intake is very high [41], as much as two to three times the recommended intake [42]. In the current study, the focus was to compare the effect of source of dietary fibre rather than quantity. Thus, the chickpea and wheat intervention diets contained a realistic amount of dietary fibre, consistent with recommended dietary guidelines, rather than an extreme amount that participants may have found difficult to consume; potentially affecting compliance.

The chickpea intervention did not have any significant effect on glucose tolerance or insulin resistance compared to the wheat diet, even though chickpeas contain more resistant starch than wheat. A recent study examining the post-prandial and longer-term effects of chickpeas on glucose tolerance and insulin sensitivity [11] reported a similar finding. The controlled, dietary intervention study [11] reported no change in plasma glucose, insulin concentrations or insulin resistance (HOMA-IR) after six weeks of chickpea-supplemented intervention compared to wheat, even though post-prandial results showed reduced plasma glucose and insulin responses following ingestion of a chickpea-based meal compared to a wheat meal. The authors postulated that the normoglycaemic state of their participant population (5.2 ± 0.4 mmol/L, n=19) might have contributed to the apparent lack of long-term improvement in glucose tolerance. The participant population for this study would also be considered normoglycaemic, with mean fasting glucose levels below 6.0 mmol/L and insulin concentrations of less than 30 µIU/ml [43].

The current study also surveyed the bowel function and perceived bowel health of participants during the dietary periods. The results suggest that increased consumption of chickpeas would not adversely affect bowel function compared to increased consumption of wheat. It may prove beneficial for gluten-sensitive individuals looking for alternatives to increase their dietary fibre content. Flatulence has generally been associated with ingestion of pulses [44] but in this study, although a significant reduction in frequency of flatulence was detected in the subgroup during the lower-fibre wheat phase, there was no difference between the chickpea and wheat diets. Chickpeas should thus, not be deemed unacceptable for this reason. The canning process and further cooking by participants could have reduced the oligosaccharide activity (and thus degree of flatulence) of the chickpeas.

Research generally supports an inverse relationship between fibre content of the diet and bowel transit time [15,27,28]. However, focus on the effect of particular fibre sources is not as clear-cut. Addition of wheat bran to the diet has been shown to reduce BTT but this effect may be due to the physical form of the wheat bran used rather than a particular constituent [28,41,45,46]. Other studies have reported no change in BTT after ingestion of wheat bran or pectin [47], oat hull fibre [48] or green lentils [49]. Dietary fibre consumption is one of many variables that influence colonic function. Other variables include gender, age, stress, hormones, hydration and the absorptive function of the small intestine [28]. Even though in the current study both the chickpea and lower-fibre BTT's were significantly longer than during the control wheat diet, they were still within the normal range of 1–4 days (24–96 hrs) [28]. Thus, any difference is difficult to interpret and may just highlight the variation in individual response to dietary change.

The majority of participants had no trouble adjusting to the chickpea diet and there was high acceptance of both the chickpea bread and shortbread biscuits. Most appetites were satisfied during the chickpea and wheat diets. The significant reduction in satiety noted during the lower-wheat fibre phase may have been due to an unplanned reduction in energy consumption during this intervention where, to keep dietary fibre to a minimum, participants consumed white rice rather than pasta or potato along with lower fibre fruit and vegetables. Some participants commented that during the chickpea diet they no longer "craved" the sweet and fatty "treats" to which they were normally "addicted". This fits with comments to the American Dietetics Association that the less quantifiable effects of dietary fibre such as satiety are just as important as the statistically significant effects of fibre consumption [19].

	CONCLUSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Substitution of chickpeas for wheat-based foods in a controlled dietary intervention resulted in small but significant reductions in serum TC and LDL-C that were partly due to changes in fatty acid content. Chickpeas as a whole may have contributed a small benefit - both in their own right and/or through dietary substitution. Chickpeas are rich in PUFA and may have provided improvements related to this. In addition, inclusion of chickpeas may have caused other beneficial physiological and dietary changes associated with increased satiety. These aspects need to be explored in studies that do not attempt to control the overall macronutrient or non-chickpea fibre content of the intervention diets, as this study indicates that more beneficial physiological and biochemical changes may result via this mechanism.

	ACKNOWLEDGMENTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
We would like to thank the participants of the study, the Clifford Craig Medical Research Trust and the Northern Tasmanian Pathology Service. The Grains Research and Development Corporation (GRDC), Australia provided sponsorship.

Received February 27, 2005. Accepted July 11, 2006.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 

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