The effect of high‐polyphenol sumac (Rhus coriaria) on food intake using sensory and appetite analysis in younger and older adults: A randomized controlled trial

Abstract Aging is accompanied by a decline in appetite and food intake with associated deficiencies in both macronutrients and micronutrients. The aim of this study was to investigate the impact of adding Iranian brown sumac (Rhus coriaria) (CIBS) into butternut squash soup on sensory evaluation and food intake among older adults (n = 20; >65 years old) and younger adults (n = 20; 18–35 years old). To evaluate the polyphenol content and antioxidant activity of the sumac samples, a Folin–Ciocalteu assay (FCR) and ferric ion reducing antioxidant power (FRAP) assay were used, respectively. L‐glutamic acid was assessed using a Megazyme L‐glutamic acid assay. Compusense software was used to assess the sensory evaluation attributes of free‐living older adults and younger adults receiving different doses of sumac in butternut squash soup. Nutritics software was used to assess food intake following the addition of 0.37 g of sumac to soup. CIBS was selected based on a preliminary assessment in vitro for L‐glutamic acid, antioxidant, and polyphenol content of six varieties of sumac. Sensory evaluation results revealed that the difference in perceived intensity of brown color between the soup samples with different doses of CIBS was greater in the younger adults' group (p = .001) than in older adults (p = .037). In addition, the food intake study found that during the ad libitum lunch, older adults consumed more energy (kcal; p = .014), protein (g; p = .025), carbohydrate (g; p = .013), and fat (g; p = .002) after soup with sumac compared to control soup. The overall findings of this study suggest that the addition of sumac to food may have a potential benefit in enhancing ad libitum lunch intake in older adults leading to effective management of malnutrition. This may promote healthy aging and minimize the burden and the consequences of anorexia of aging as main public health concerns.


| INTRODUC TI ON
Herbs and spices were traditionally used to enhance the taste of food, as well as for medicinal purposes (Kaefer & Milner, 2008). They can also be added into low-salt dishes to improve appetite and food intake (Dougkas et al., 2019). Many traditional dishes are well known for their signature herbs and spices that enrich the taste and aroma of food and offer health benefits due to the presence of bioactive phenolic compounds (Asgharpanah & Saatti, 2014;Egharevba & Gamaniel, 2017).
Epidemiological studies have confirmed the association between a high level of antioxidant consumption and decreased rates of mortality and morbidity (Devasagayam et al., 2004). As a result, the enhancement of foods using natural antioxidants and polyphenols has been acknowledged by food researchers (Bashash et al., 2012).
Herbs and spices contain significant concentrations of free glutamic acids (Aremu et al., 2011). It has been found that nonessential amino acids (including glutamates) play a role as umami substances to enhance the taste of food by activating the chemical-detecting components of taste buds (Mouritsen, 2012).
Sumac (Rhus coriaria) is a spice that grows in the wild tropical regions including Mediterranean coastlines from the Canary Islands to Iran (Abu-Reidah et al., 2015;Rayne & Mazza, 2007) and it is commonly used in Middle Eastern dishes for seasoning and flavoring (Zargham & Zargham, 2008). Although sumac has some health benefits including antimicrobial (Fazeli et al., 2007;Sagdic & Ozcan, 2003) and antioxidant activity (Bozan et al., 2003;Kosar et al., 2007), antihyperlipidemic activity and hypoglycemic effects (Anwer et al., 2013;Madihi et al., 2013;Shafiei et al., 2011) uncertainty remains about the relationship between the consumption of sumac, appetite, and food intake. It is pertinent to investigate this in the context of aging when threshold perceptions of taste and flavor of food are altered resulting in malnutrition among older adults (Methven et al., 2012).
The benefits of using flavoring agents, including herbs and spices, to reduce salt intake resulting in a reduction in cardiovascular diseases, are noteworthy in healthy aging (Anderson et al., 2015).
The literature emphasizes the importance of older adults consuming food with sufficient energy in order to maintain their immune system levels and muscle mass (Baum et al., 2016). An increase in daily protein intake for healthy adults is recommended to almost 1.0 g/kg of body weight, and for those who are either malnourished or at risk of malnutrition, the amount should increase by half a gram/ kg (Deutz et al., 2014). Previous research has investigated methods that help to increase food consumption in the older population, with some studies demonstrating the impact of added herbs and spices on improving the liking and palatability of food (Dermiki et al., 2015;Dougkas et al., 2019;Fritts et al., 2018;Peters et al., 2014).
Moreover, monosodium glutamate (MSG) has been added to different foods, resulting in flavor enhancement and increased appetite (Dermiki et al., 2013;Dermiki et al., 2015;Schiffman, 2000). Hence, it can be hypothesized that sumac, as a potential natural flavor enhancer containing glutamic acid, might also increase appetite among older adults. The aim of this research was to identify sumac with high polyphenol and glutamic acid content for use as a food flavoring to enhance food intake in older adults and compare the results with younger adults.

| In vivo studies
The test food used was butternut squash soup prepared using 25% reduced salt vegetable stock cubes. Pasta, vegetable oil, and tomato sauce were used for the ad libitum lunch. All these ingredients were purchased from local supermarkets.

| In vitro testing of sumac samples for antioxidants, polyphenols, and L-glutamic acid
The FRS and FBS were first air-dried for 4 weeks, away from direct light and then ground into powder using mortar and pestle. The extraction for polyphenols was completed by adding 0.2 g of sumac sample into 4 mL of the solvents-distilled water, 80% acetone, and 80% ethanol.
The samples were transferred to a shaking water bath and then incubated for 2 h at room temperature away from light. The samples were then centrifuged at 3000 rpm for 10 min (Heraeus Instruments, D-37520 Osterode) to separate the supernatant used as sumac extract. The total antioxidant capacity (TAC) of each sumac extract was assessed using a Ferric ion reducing antioxidant power (FRAP) assay (Benzie & Strain, 1996;Ryan et al., 2011). The total phenolic content (TPC) of each sumac extract was analyzed using the method described by Coe et al. (2013). L-glutamic acid was measured using L-glutamic acid Megazyme assay procedure (K-GLUT 11/15) following the extraction of 0.2 g of sumac samples in 4 mL of distilled water. The results for L-glutamic acid in sumac samples were calculated as g/100 g (Aremu et al., 2011;Sakhr & El Khatib, 2020). The average g glutamic acid/100 g protein of each sample was calculated, as shown below: average of absorbance × 6.75 100 = (g ∕ g protein).

| Food intake study
Participants were given 150 g of butternut squash soup in each session: with no added sumac (SC), 1% CIBS added at the end of cooking (SSE), or 1% CIBS added during cooking (SSC). The soup was heated for 30 min before serving. The participants were provided with an ad libitum lunch (pasta with tomato sauce), 10 min after the soup was served. The participants were blinded to the soup sample they received. The pasta was weighed (180 ± 1 g) and served along with a glass of water (340 mL) at room temperature (Peters et al., 2014).
Participants were instructed to eat as much pasta and drink as much water as they desired.

| Participants
A study poster was used to recruit participants from different ven-

| In vitro studies
Based on the results for normally distributed data, a parametric oneway analysis of variance (ANOVA) with a post hoc test (using Tukey adjustment) was applied to determine significant differences within sumac samples and between solvents. The significance level was set to p < .05. For data not normally distributed, the results were analyzed using a nonparametric Kruskal-Wallis test between sumac samples' types, and the significance level was set to p < .05. In order to assess the relationship between the antioxidant activity and polyphenol content of all the sumac samples, a Pearson correlation test was run.

| In vivo sensory evaluation
A nonparametric Friedman test was used to evaluate the differences in sensory attributes between soup samples in older and younger adult groups, while a Wilcoxon test was run to determine differences in pairwise comparisons. Comparisons between the average intake of energy and macronutrients for older and younger adults were done using a Mann-Whitney test. The sample size determination was conducted using G*power (Version 3.1.9.7) which indicated that for a medium effect size of d = 0.5, α of 0.05 and power of (1-ß) 0.80, a total of 35 participants was required.

| In vivo food intake
To analyze the impact of adding CIBS (SSE and SSC) to energy and nutrient intakes within older and younger adult groups, repeated measures ANOVA was applied for normally distributed data.
Furthermore, comparisons of food intake between the two groups of adults were done using a Mann-Whitney test, or an independent t-test depending on the normality of the data. In this study, G*power (v. 3.1.9.7) indicated that for a two-tailed test with a medium effect size of d = 0.5, α of 0.05 and a power of (1-ß) 0.95, a sample size of 16 was required in each group to detect a difference in energy intake of 45 kcal (Flood & Rolls, 2007).

| Demographic characteristics of the participants In In vivo studies
Forty participants (20 older adults and 20 younger adults) volunteered to take part in the sensory evaluation study (Table 3). The results revealed, understandably, a significant difference between the ages of both groups of adults (t (38) = −32.6, p = .001, d = 10.4).
On average, the age of older adults, in the food intake study, was higher than that of younger adults, with a large effect size of d = 8.9 (t (38) = −26.8, p = .001). However, no difference was observed in the comparison between the weight and height of older and younger adults in both sensory evaluation and food intake studies (p > .05).

TA B L E 1
Nutritional composition of butternut squash soups with 1% CIBS per portion and the pasta served for ad libitum lunch.  TA B L E 2 Total antioxidant activity (mol/L), polyphenol content (mg GAE/g), and L-glutamic acid (g glutamic acid/100 g protein) of each type and form of sumac.
*is significantly higher than the other samples (one-way ANOVA test, at p < .05).
**is significantly different between solvents at p < .001. ***is significantly different between solvents at p < .003.
Column values with no superscript are not significantly different (p > .05).

TA B L E 3
Demographic characteristics of older adults and younger adults in sensory evaluation and food intake studies (mean ± SD).

Sensory evaluation Food intake
Older adults mean ± SD

Younger adults mean ± SD p-value
Older adults mean ± SD

Younger adults mean ± SD p-value
Age (

| Younger adults
The mean scores for the liking attributes' (acceptance, texture, aroma, flavor, appearance) and intensity attributes' (lemony flavor, salty flavor, brown color, red color) for different soup samples in the younger adults group are presented in Figure 2.    (Table 4). Comparison of the multiple tests showed that the SSE and SSC in comparison with the SC session had no impact on the intake of energy and macronutrients (p > .05). There was no impact on evening meal intake following the addition of CIBS sumac to soup samples between both groups of adults (p > .05). No statistical differences were observed in energy and macronutrient profiles of the all-day food intake between the test sessions in either older adults or younger adults.

| Energy and nutritional profiles of ad libitum lunch, evening meal, and the all-day food intake between participant groups
The macronutrient intake of ad libitum lunches, evening meals, and all-day after the test sessions (SC, SSE, and SSC) between older adults and younger adults was analyzed (Table 5). Added CIBS revealed no statistical differences in nutrient intake between older adults and younger adults (p > .05) following ad libitum lunch. However, protein intake was higher during the evening meal following the SSC soup test (p = .003) with higher intake by younger adults than older adults. Furthermore, more intake of protein was observed after SSE (p = .006) and SSC (p = .004) sessions on all-day food intake between the groups with greater consumption in younger adults.

| DISCUSS ION
The current study compared the food intake within and between older adults and younger adults and confirmed a reduction in food intake with aging, which has been reported previously (Giezenaar et al., 2016). The addition of spices such as sumac may compensate for the chemosensory impairment of older adult participants as the energy, carbohydrate, protein, and fat intake in the ad libitum lunch of these groups increased following consumption of soup with sumac, whereas the younger adults showed no changes. Sumac contains various volatile compounds that are released via the nasal route and trigger olfactory receptors (Bell et al., 2018;Farag et al., 2018).
Additionally, the consumption of food flavored with herbs and spices stimulates the sensory receptors located in the mouth and enhances the food intake (Field & Duizer, 2016). Thus, it can be speculated that the addition of sumac to older adults' food increases its palatability, resulting in greater food consumption.
In the current study, a higher intake of protein was observed in older adults in an evening meal following the consumption of soup in SSE session. Therefore, it can be hypothesized that the SSE session had a greater impact on protein intake compared with SSC and SC.
The importance of an adequate intake of protein for older adults' health and the prevention of malnutrition is highlighted in epidemiological studies (Baum et al., 2016). It has been reported that 35% of residents in care homes in Europe consume less protein than TA B L E 4 Ad libitum lunch, evening meal, and the all-day energy and macronutrient intake on three test sessions (SC, SSE, and SSC) within older adults and younger adults. is recommended (0.7 g/kg of their body weight per day) (Tieland et al., 2012). The consumption of 1.0-1.2 g protein/kg of body weight per day by healthy older adults, increasing to 1.2-1.5 g/kg for malnourished older adults, has been suggested (Deutz et al., 2014).

Evening meal
However, more investigation is required to substantiate the impact of added sumac on protein intake.
The findings of the current study demonstrated a marginally higher intake of energy, protein, carbohydrate, and fat in an ad libitum lunch among older adults following the addition of sumac in soup. In agreement, a positive influence of additive seasoning and sauce to older adults' food to enhance energy, protein, and fat intake was reported previously (Best & Appleton, 2011). The impact on the ad libitum lunch intake can possibly be explained by the presence of L-glutamic acid in sumac, which via the activation of umami subunits and coupling with G-protein stimulate appetite (Camilleri, 2015). On the other hand, the impact of polyphenol compounds in increasing glucagon-like peptide-1 hormone and decreasing ghrelin is reported (Boix-Castejon et al., 2018) in addition to the rapid omission of polyphenols and their weak absorption into the body's circulation that are well documented (Hollman, 2014). Therefore, these paradoxical findings require further assessment to understand the bioavailability of the polyphenol compounds following consumption.
In the current study, the perception of intensity of brown color of sumac in soups was significantly different between the older and younger adults and within each group; however, no other differences were observed. One reason could be the small differences between doses (0%-1%) of sumac, so it was difficult to differentiate the brown color and flavor of the samples . The most common doses of herbs and spices intake generally ranged between 1 and 5% (Vazquez-Fresno et al., 2019). Another reason could be the personal perception of taste and flavor preferences. Based on the variety of the chemical structure of aroma compounds, including acids, alcohol, and esters, various factors participate in the release of aroma from spices in foods. Moreover, multisensory interaction, for instance, olfactory, gustatory, and oral somatosensory, plays an important role in food flavor perception. This could be a reason why some participants found the samples more spicy, salty, or sweet.
However, this finding requires more research on taste perception of sumac, which can be affected by genetics, cultures, and habitual intakes.
The addition of sumac in this study did not contribute to sour or lemony flavor in soup. This could occur due to the method of cooking and interaction of low-salt vegetable stock ingredients in the soup (Opara & Chohan, 2014). The impact of viscosity on flavor recognition and the importance of organoleptic properties in food preferences have been reported previously (Bult et al., 2007). Volatile compounds in spices may interact with the food matrix via the saliva and nasopharynx pathway and, hence, flavor is released following olfactory activation. The interaction of sumac in the food matrix remains still unknown; however, the results of sensory evaluation TA B L E 5 Mean differences in the ad libitum lunch, evening meal, and all-day energy and macronutrient intake after the test sessions (SC, SSE, and SSC) in older adults (>65 years old) compared with younger adults (18-35 years old). were the most effective solvents for polyphenol and antioxidant activity, respectively. This may be due to solvent polarity, which has a major role in increasing solubility of phenolic compounds, depending on their structure (Zlotek et al., 2016). Acetone/water mixture is generally more effective in extracting more polar antioxidants from plant materials such as leaves, fruits, and vegetables, whereas ethanol/water mixture can solubilize a wide range of phenolic compounds (Alothman et al., 2009;Naczk & Shahidi, 2006).
Considering the impact of diverse analytical procedures and ensuing previous studies, acetone /water (80/20, v/v) and ethanol/water (80/20, v/v) were chosen in the current study to obtain robust and comparable results. Water was used as another extractant to determine potential bioaccessibility of phenolic compounds and glutamic acid in human studies. Previous studies revealed that sumac contains nearly 200 different phenolic compounds including gallic acids (Bozan et al., 2003), hydrolyzable tannins, anthocyanins, and flavonoids (Ardalani et al., 2016). Therefore, the authors acknowledge the difficulty in extracting all the phenolic compounds using one solvent mixture and there may be variations in the amount and type of compounds depending on the solvent system used.
The results for L-glutamic acid levels in the current study varied and were higher than earlier findings for Syrian and Chinese sumac (Kossah et al., 2010).  (Ghawi et al., 2014). Moreover, the stimulation of secretion of immunoglobin A and saliva by glutamic acid has been reported to show an association between nutrition and improved immune status (Schiffman, 2000). This is the first study seeking to ascertain the importance of the addition of sumac to enhance palatability and food intake among older adults in the short term. Future research could assess the impact of the addition of sumac to food over a longer period.
Additional sensory studies need to be carried out in order to validate the acceptability and liking of higher doses of sumac in different foods. The authors acknowledge some limitations. The study was conducted among a particular demographic of participants, with most being educated and white population in Oxford, UK. The lack of diversity in the social backgrounds of participants in the current study diminishes the generalizability of its findings. The study was limited by the accessibility to commercial forms of brown sumac from other regions, similar to Iranian sumac. Moreover, it was not possible to obtain fresh sumac from areas other than the UK and Iran.
Therefore, this would have caused a bias in selecting sumac with the highest concentrations of polyphenol compounds. Additionally, the specific phenolic compounds in sumac extracts were not identified in this study. Further studies are warranted to characterize these polyphenols using more robust methodologies such as highperformance liquid chromatography or capillary electrophoresis (Naczk & Shahidi, 2006). Another limitation of this study was the self-reported dietary intake, which may have resulted in inaccurate recording of consumed food. An extension of study intervention may improve the familiarization of sumac in older adults leading to higher food intake. Therefore, the influence of sumac consumption on food intake among older adults should be investigated using longer intervention periods.

| CON CLUS IONS
The findings of this study highlighted that commercial brown sumac had higher polyphenol, antioxidant, and L-glutamic content among all commercial sumac samples chosen in this study. To the best of our knowledge, this study is the first attempt to compare the sensory evaluation of different doses of sumac by older and younger adults.
The findings confirmed that the soup sample with commercial brown sumac (1%) was the sample most preferred by both groups of adults.
Additionally, the increase in doses of sumac had no adverse effects on the acceptability and liking attributes of soup samples. It can be suggested that sumac, which contains L-glutamic acid, is a promising natural additive, to replace salt, with the aim of increasing food intake in older adults and improving the taste and flavor of food.
Hence, the outcome of this study is a promising approach in response to global health concerns over malnutrition in older adults, potentially contributing to reductions in healthcare costs.

ACK N OWLED G M ENTS
The authors thank the participants who took part in these studies and facilitated for completion of these works.

CO N FLI C T O F I NTER E S T S TATEM ENT
The authors declare that they do not have any conflict of interest.

DATA AVA I L A B I L I T Y S TAT E M E N T
The data that support the findings of this study are available from the corresponding author upon reasonable request.

E TH I C S S TATEM ENT
This study was approved by the Institutional Review Board of Oxford Brookes University.

I N FO R M ED CO N S ENT
Written informed consent was obtained from all study participants.