Effects of pulse grains on energy expenditure and substrate utilisation

Evidence is emerging to support that pulse grains modulate the gastrointestinal microbiome and facilitate the production of bacteria-derived bioactives which alter energy expenditure, substrate trafficking and substrate oxidation. Pulses are an excellent source of soluble and insoluble fibres. The fermentation of fibre by gastro-microbiota produces SCFA, specifically butyric acid, which can be absorbed from the large intestine and alter hepatic and muscle metabolism. For example, one study showed that when rat faeces were inoculated with pea-derived fibre, butyric acid was the most prominent SCFA produced⁽Reference Stark and Madar⁸⁾. In vitro fermentation of indigestible fractions of pulse grains by human microbiota demonstrated that, compared with chickpeas and a raffinose control, black beans and lentils facilitated the highest production of microbe-derived butyric acid⁽Reference Hernandez-Salazar, Osorio-Diaz and Loarca-Pina⁹⁾. Similarly, rats fed diets containing 25 % adzuki, kintoki or tebou beans significantly increased caecal butyric acid concentrations compared with a control diet rich in ‘cornstarch’⁽Reference Han, Fukushima and Shimizu¹⁰⁾. In addition, levels of propanoic acid and acetic acid did not differ between the bean and control diets⁽Reference Han, Fukushima and Shimizu¹⁰⁾. Butyric is a metabolically active SCFA. Mice supplemented with butyric acid demonstrated an increase in hepatic and muscle PPARγ coactivator α expression alongside enhanced hepatic and muscle energy expenditure, as well as fat oxidation, mitochondrial oxidation and biogenesis⁽Reference Gao, Yin and Zhang¹¹⁾. In addition, butyric acid has been shown to modulate hepatic trafficking of carbohydrates by increasing glycogen storage and decreasing glycolysis⁽Reference Anderson and Bridges^12, Reference Beauvieux, Roumes and Robert¹³⁾ (Fig. 1). Modulation of carbohydrate metabolism could increase hepatic fat oxidation if energy demands of the cell are high and/or less acetyl-CoA is available from carbohydrates.

Fig. 1

Pulse grains modulate thermogenesis, substrate trafficking and oxidation, as well as adipose tissue deposition. (1) Fermentation of pulse-derived fibres and resistant starch facilitates the production of SCFA such as butyrate. Butyrate has been shown to alter energy expenditure and fatty acid oxidation by promoting glycogen storage, decreasing glycolysis and increasing the expression of PPARγ coactivator α (Pgc-1α). (2) Cellulose and hemicellulose, two insoluble fibres found in pulses, have been shown to mitigate excess adipose deposition and weight gain, causing an increase in hepatic forkhead transcription factor (Foxa2) and PPARγ coactivator β (Pgc-1β) expression. Cellulose and hemicelluloses have also been shown to reduce the expression of adipose G-protein-coupled receptor-40 (Gpr40). De novo lipogenesis could also be reduced via decreased expression of fatty acid synthase (FAS) secondary to low levels of refined sugars in pulse grains and blunted postprandial glucose responses. (3) Modulation of genes that facilitate increases in energy expenditure could also be secondary to the ability for pulses to induce changes in genes that facilitate energy expenditure and fat oxidation directly. (4) Pulse grains could contribute to the consumption of phyto-oestrogens that interact with oestrogen receptor α (ERα) which facilitate subcutaneous (SC) adipose deposition and reduce visceral adipose deposition. CHO, carbohydrates.

In addition to soluble and insoluble fibres, pulse grains also contain substantial levels of resistant starch (RS). RS is characterised as starch polysaccharides that avoid digestion in the small intestine and have been shown to be highly fermentable in the colon⁽Reference Robertson, Bickerton and Dennis^14, Reference Weickert, Mohlig and Koebnick¹⁵⁾. In a recent review, Chibbar et al. ⁽Reference Chibbar, Ambigaipalan and Hoover¹⁶⁾ indicate that some beans contain 10–20 % RS. In vivo fermentation of pulse-derived RS was shown to predominately increase the levels of butyric acid⁽Reference Mahadevamma, Shamala and Tharanathan¹⁷⁾. Recently, Higgins et al. ⁽Reference Higgins, Higbee and Donahoo¹⁸⁾ demonstrated that diets containing RS increased endogenous fat oxidation and suggested that carbohydrate metabolism could have been modulated via the SCFA-based mechanisms described above. Given the products of pulse-derived fibre and RS fermentation, evidence suggests that pulse grains could modulate macronutrient metabolism and increase fat oxidation.

Within vegetarian populations, pulses exist as a major source of dietary protein. The high protein content of pulse grains suggests that pulses could increase energy expenditure directly because, compared with carbohydrate diets, protein produces the highest thermic effect of food secondary to the energetic costs associated with dietary peptide catabolism, protein synthesis and gluconeogenesis⁽Reference Robinson, Jaccard and Persaud^19–Reference Krebs, Brehm and Krssak²¹⁾. Abete et al. ⁽Reference Abete, Parra and Martinez²²⁾ showed that human subjects consuming legume-rich diets for 8 weeks demonstrated increased mitochondrial oxidation, contributing to greater weight loss compared with controls. In addition, enhancements in mitochondrial oxidation were similar to individuals consuming diets high in animal-based protein⁽Reference Abete, Parra and Martinez²²⁾. Furthermore, high-legume diets induced the greatest reductions in LDL-cholesterol levels, suggesting that a protein-rich diet that modulates metabolism does not need to incorporate protein sources that are high in saturated fats and cholesterol which promote hypercholesterolaemia. Nonetheless, it should be noted that the Abete et al. study does not specify the proportion of legumes in the diet comprised of pulses. Unpublished indirect calorimetry data from our laboratory have demonstrated that hamsters fed diets containing 10 % whole pea flour at the expense of ‘cornstarch’ consumed higher levels of oxygen compared with controls. However, given that diets were fairly isonitrogenous, we postulated that the amino acid composition could have facilitated an increase in energy expenditure. Published amino acid profiles of yellow peas⁽Reference Pownall, Udenigwe and Aluko²³⁾ suggest that the whole pea diets fed to hamsters contained approximately 24 % higher arginine levels compared with the control diet. Arginine has been shown to possess thermogenic properties which enhance carbohydrate and fat oxidation via increased mitochondrial biogenesis and the modulation of genes that regulate energy expenditure⁽Reference McKnight, Satterfield and Jobgen²⁴⁾. In addition, analysis of protein meal, protein concentrate and protein isolates of peas, faba beans and lentils has demonstrated that arginine is a major amino acid constituent of pulse-derived protein at 9·7–11·1, 10·5–12·0 and 11·3–11·0 g/16 g N, respectively⁽Reference Bhatty and Christison²⁵⁾. In addition to arginine, peas, faba beans and lentils also contain substantial amounts of glutamine at approximately 15·0 g/16 g N⁽Reference Bhatty and Christison²⁵⁾, which has been shown to increase postprandial energy expenditure by 49 % in human subjects⁽Reference Iwashita, Mikus and Baier²⁶⁾. Iwashita et al. ⁽Reference Iwashita, Mikus and Baier²⁶⁾ demonstrated that glutamine initially enhanced postprandial carbohydrate oxidation up to 180 min after a test meal while fat oxidation was enhanced after 210 min. It has been suggested that glutamine can improve insulin-mediated glucose disposal during the early postprandial period. Thus, reduced levels of carbohydrate would be available during the latter postprandial period and force cells to rely on fat as a source of energy⁽Reference Iwashita, Mikus and Baier²⁶⁾. Modern-day food processing techniques such as fractionation allow for isolation and concentration of pulse-derived proteins for future use in studies examining the direct effects of pulse grain peptides on thermogenesis.

Pulse grains and fat deposition

Excess waistline adipose deposition is primarily visceral/ectopic fat and is an independent risk factor for CVD, diabetes and the metabolic syndrome⁽Reference Carey, Jenkins and Campbell^27, Reference Tanko and Christiansen²⁸⁾. Thus, by shifting fat deposition away from visceral fat depots and into subcutaneous adipose tissue, risk factors related to excess weight could decline before weight loss. Although human clinical trial data are still forthcoming in examining the effects of pulse consumption on regional fat deposition, animal studies have suggested a beneficial effect. Rats consuming a high-fat diet with added chickpeas demonstrated similar energy intake compared with high fat-fed rats and increased energy consumption compared with rats on normal-fat diets⁽Reference Yang, Zhou and Gu²⁹⁾. Nonetheless, chickpeas significantly reduced epididymal fat deposition, a measure of visceral adipose tissue, compared with high fat-fed controls. Moreover, rats receiving chickpeas demonstrated similar levels of epididymal fat mass v. normal fat-fed rats. A reduction in epididymal fat deposition in rats receiving chickpeas was also reflected in decreased leptin mRNA expression. In addition, compared with the high-fat diet, chickpeas decreased muscle and hepatic TAG levels by 39 and 23 %, respectively⁽Reference Yang, Zhou and Gu²⁹⁾. Chickpea-enriched diets also normalised the activities of lipoprotein lipase and hepatic TAG lipase, as well as decreased lipoprotein lipase mRNA expression and postprandial glycaemic responses to levels that were similar to animals consuming normal levels of dietary fat⁽Reference Yang, Zhou and Gu²⁹⁾. In another study, despite identical energy intakes, rats fed diets containing mung beans demonstrated a 48 % reduction in retroperitoneal adipose tissue mass, a visceral fat depot, compared with control diets⁽Reference Morris and Zemel³⁰⁾. Moreover, mung beans were shown to induce a 40 % reduction in circulating leptin levels and a 62 % reduction in hepatic fatty acid synthase expression⁽Reference Morris and Zemel³⁰⁾. Researchers⁽Reference Morris and Zemel³⁰⁾ suggest that reduced levels of refined sugars and blunted postprandial glucose responses with mung bean diets could have blunted fatty acid synthase expression. SCFA from the fermentation of pulse-derived fibres could also modulate adipose deposition. In the study described above by Gao et al. ⁽Reference Gao, Yin and Zhang¹¹⁾, butyric acid-induced enhancements in energy expenditure and fat oxidation prevented obesity in high fat-fed mice. Finally, a human clinical trial using whole pea flour as a dietary intervention, alongside an energy-controlled paradigm that prevented fluctuations in weight, demonstrated a significant reduction in android:gynoid fat ratios in women, indicating that fat deposition was directed away from the waistline area⁽Reference Marinangeli and Jones³¹⁾.

The bioactive components of pulse grains that induce shifts in adipose tissue deposition are unknown. As described above, insoluble fibre is the primary fibre type found in pulses⁽Reference Tosh and Yada³²⁾. Fibre compositional analysis of pulses is scarce; however, yellow pea hulls consist primarily of cellulose (69 %), hemicellulose (7·5 %) and lignin (1·4 %)⁽Reference Reichert³³⁾. A recent study investigating the metabolic effects of insoluble fibres containing primarily cellulose and hemicellulose showed an increase in the expression of forkhead transcription factor (Foxa2) and PPARγ coactivator β (Pgc-1β), two genes that facilitate hepatic fat oxidation⁽Reference Isken, Klaus and Osterhoff³⁴⁾. In addition, compared with soluble fibre, mice consuming insoluble fibre demonstrated reduced adiposity despite no differences in dietary energy intake, digested energy or faecal energy output⁽Reference Isken, Klaus and Osterhoff³⁴⁾. Although researchers hypothesise that modulation of Foxa2 and Pgc-1β could be secondary to reduced weight gain and insulin resistance among insoluble fibre-fed mice, they do not discard the possibility of insoluble fibre having a direct effect on gene expression⁽Reference Isken, Klaus and Osterhoff³⁴⁾. Finally, insoluble fibre attenuated the expression of G-protein-coupled receptor-40⁽Reference Isken, Klaus and Osterhoff³⁴⁾, a G-coupled protein that is associated with obesity-induced hyperinsulinaemia, impaired glucose tolerance and hepatic glucose output⁽Reference Steneberg, Rubins and Bartoov-Shifman³⁵⁾. Data suggest that pulse grain-derived insoluble fibres could either directly or indirectly, via the production of microbe-derived bioactives, modulate visceral adiposity (Fig. 1).

Pulse grain-derived phyto-oestrogens could also contribute to the modulation of adipose deposition via their interaction with oestrogen receptors (ER). Phyto-oestrogens are plant-derived compounds that mimic the actions of human oestrogen, but with less potency⁽Reference Horn-Ross³⁶⁾. Regional fat deposition is, in part, regulated by sex hormones and their affinity for appropriate receptors dispersed throughout visceral and subcutaneous adipose⁽Reference Pallottini, Bulzomi and Galluzzo³⁷⁾. In fact, stimulation of ERα and ERβ decreases and increases subcutaneous adipose lipolysis, respectively⁽Reference Pallottini, Bulzomi and Galluzzo³⁷⁾. Thus, stimulation of specific ER with phyto-oestrogens could give rise to a healthier regional adipose profile. The most well-known phyto-oestrogens are genistein and daidzein, which are primarily soya-derived and not found in significant concentrations in pulse grains. Compared with ERα, the soya-derived phyto-oestrogen genistein has been shown to have a higher affinity for ERβ ⁽Reference Morito, Hirose and Kinjo³⁸⁾. In one study by Sites et al. ⁽Reference Sites, Cooper and Toth³⁹⁾, it has been hypothesised that the significant reduction in subcutaneous adipose tissue in postmenopausal women could have been secondary to the stimulatory effects of soya-derived phyto-oestrogens on ERβ. The lignan secoisolariciresinol is a phyto-oestrogen that is found in some pulses. Metabolism of secoisolariciresinol involves its conversion to enterolactone by gastrointestinal microflora. Contrary to genistein, enterolactone preferentially binds to ERα⁽Reference Penttinen, Jaehrling and Damdimopoulos⁴⁰⁾. Furthermore, compared with men, females express higher levels of ERα in subcutaneous adipose⁽Reference Richelsen^41, Reference Rodriguez-Cuenca, Monjo and Proenza⁴²⁾ and ERα favours subcutaneous adipose deposition⁽Reference Richelsen^41, Reference Pedersen, Kristensen and Hermann⁴³⁾. Recently, Morisset et al. ⁽Reference Morisset, Lemieux and Veilleux⁴⁴⁾ showed that, despite no difference in subcutaneous adiposity, postmenopausal women with the highest concentrations of circulating enterolactone have reduced visceral adiposity and waist circumferences compared with women with low levels of circulating enterolactone. Reduced visceral adipose deposition was accompanied by a decrease in hyperinsulinaemia and impaired glucose tolerance, as well as increased glucose disposal⁽Reference Morisset, Lemieux and Veilleux⁴⁴⁾. Published analysis of secoisolariciresinol levels in legumes/pulses indicates that kidney beans and black gram sprouts contain the highest levels of secoisolariciresinol at 153 and 468 μg/100 g, respectively⁽Reference Mazur⁴⁵⁾. Comparatively, levels of secoisolariciresinol in pulses are far below those of flax seeds (approximately 369 900 μg/100 g)⁽Reference Mazur⁴⁵⁾. However, it is unlikely that individuals, especially in North America, will consume upwards of 100 g/d flax. Thus, specific pulse grains could contribute to secoisolariciresinol intake and promote a healthier adipose phenotype among women.

Effects of pulse grains on satiety

A reduction in overall energy intake and a reduction in overall energy balance are ultimately the most effective means of reducing adiposity. Studies have demonstrated that pulse grains modulate satiety (Fig. 2). While controlling the subject's background diet, one study has revealed that chickpea flour increased satiety with volunteers feeling fewer cravings for sweet and fatty foods⁽Reference Pittaway, Ahuja and Robertson⁴⁶⁾. Recently, subjects consuming at least 1200 g/week canned chickpeas for 12 weeks reported a significant increase in satiety compared with when they consumed their habitual diet⁽Reference Murty, Pittaway and Ball⁴⁷⁾. However, despite an increase in dietary fibre intake, no differences in total energy intake were observed⁽Reference Murty, Pittaway and Ball⁴⁷⁾. Similar results were described by Wong et al. ⁽Reference Wong, Mollard and Zafar⁴⁸⁾ where, although various preparations of navy beans reduced appetite, compared with controls, there was no difference in cumulative food intake 120 min following a pizza meal. The fact that appetite was reduced, but overall energy intake was not deterred with pulse grain consumption emphasises the psychological component of eating, whereby satiety signals are not always effective when unlimited food is available. Moreover, Johnson et al. ⁽Reference Johnson, Thomas and Hall⁴⁹⁾ showed that regular and extruded chickpea flours had no effect on satiety. The authors suggest that the dose of chickpea flours could have been insufficient to mitigate volunteers' desire to eat. Assuming that sufficient quantities are consumed, available evidence is in support of pulse grains' ability to induce satiety.

Fig. 2

Mechanisms by which pulse grains could induce secretion of cholecystokinin. (1) Pulse grain fibres increase and prolong cholecystokinin (CCK) secretion by inducing gastric distension (GD) and decreasing the rate of gastric emptying, respectively. Decreasing the rate of gastric emptying can also prolong CCK secretion. (2) Pulse grain-derived lectins and trypsin inhibitors increase CCK secretion directly.

Physiological signals that stimulate satiety are not completely understood⁽Reference de Graaf, Blom and Smeets⁵⁰⁾. However, given the nutritional composition of pulse grains, hypotheses surrounding the mechanisms by which these dietary ingredients induce satiety can be formulated. In addition to dietary protein and fat, gastric distention induces the secretion cholecystokinin (CCK), a duodenum-derived hormone that delays gastric emptying and modulates satiety by interacting with receptors on the vagus nerve⁽Reference Moran, Baldessarini and Salorio^51, Reference Degen, Matzinger and Drewe⁵²⁾. High-fibre foods are believed to stimulate and prolong CCK secretion by facilitating gastric distention and slowing the rate of gastric emptying⁽Reference Santangelo, Peracchi and Conte⁵³⁾, respectively. Therefore, it is reasonable to hypothesise that appropriate dosages of pulse grain fibres can stimulate CCK release⁽Reference de Graaf, Blom and Smeets⁵⁰⁾. When added to a mixed meal, high-fibre bean flakes have been shown to increase satiety⁽Reference Leathwood and Pollet⁵⁴⁾ and CCK levels⁽Reference Bourdon, Olson and Backus⁵⁵⁾ compared with potato purée and rice with skimmed milk, respectively. Researchers suggest that trypsin inhibitors found in the bean flakes may also stimulate CCK release directly⁽Reference Bourdon, Olson and Backus⁵⁵⁾. Stimulation of CCK secretion by trypsin inhibitors has been demonstrated in the literature using soya⁽Reference Lu, Anderson and Gomez^56, Reference Grant, Alonso and Edwards⁵⁷⁾. In addition, consumption of bean-derived lectins, another class of anti-nutritional compounds found in pulses⁽Reference Champ⁵⁸⁾, has been shown to increase CCK secretion, compared with controls fed lactalbumin⁽Reference Herzig, Bardocz and Grant⁵⁹⁾. Similar results have been demonstrated when rats were fed kidney beans or had kidney bean-derived lectins infused into their duodenum⁽Reference Grant, Alonso and Edwards⁵⁷⁾. Overall, the fibre and anti-nutritional bioactive content of pulse grains could work in concert to facilitate CCK secretion and induce satiety. Nonetheless, future studies are needed to investigate the effects of whole pulse grains or their components on satiety and the secretion of satiety-modulating hormones such as ghrelin, glucagon-like peptide 1 and peptide YY.