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      Reply to “Limitations of the Digestible Indispensable Amino Acid Score (DIAAS) and Choice of Statistical Reporting. Comment on “A Comparison of Dietary Protein Digestibility, Based on DIAAS Scoring, in Vegetarian and Non-Vegetarian Athletes.” Nutrients 2019, 11, 3106”

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          Abstract

          We appreciate the critique of our paper (Ciuris et al. [1]) by Genoni et al. [2]. Our research group has a track record of investigating the benefits of vegetarian nutrition, such as demonstrating that vegetarian diets promote healthful mood states [3,4] and improve acid-base balance [5], along with, developing an evidence-based vegetarian food guide [6]. However, our research also suggests that lower protein intakes among vegetarians may pose challenges for some health outcomes; specifically we have linked lower protein intakes in vegetarians to lower bone mineral density [7] and strength [8]. To follow on the latter finding, we recently conducted a randomized trial to examine the impact of supplemental plant protein on strength in sedentary vegetarians [9]. Participants were randomized to a mung bean food supplement (18 g protein/d) or control bar (4 g protein/d). (Note that both supplements were vegan friendly.) After 8 weeks, the average percent change for grip, flexor, and extensor strength differed between groups (+2.9 ± 7.2% and −2.6 ± 7.3%, respectively for the mung bean group versus the control group; p = 0.05). These results suggest that supplementary protein (plant-based) may improve strength in the absence of exercise, a finding that was independent of lean mass [9]. In this trial, we also reported that the mean grip strength of participants at baseline (25.9 ± 7.3 kg) was significantly below the reference value for North American females (31 kg; p < 0.001), which may further indicate protein inadequacy in this population. Genoni et al. [2] stated three concerns with our paper. First, they suggested that the absence of fruit and vegetable foods in our Digestible Indispensable Amino Acid Score (DIAAS) analysis skewed the results since these foods contribute substantially to dietary protein. For our analyses, we utilized the food categories presented in the 2011 report of the Food and Agriculture Organization Expert subcommittee [10]. To our knowledge, the true ileal amino acid digestibility is not known for fruits and vegetables aside from legumes, which were utilized in our analyses (see Table A2, [1]). We acknowledged in our paper “the DIAAS spreadsheet utilized in this research was not extensive, as it was limited by the availability of true ileal digestibility values that have been derived for foods.” Note that the Dietary Reference Intake for protein, released in 2005 by the Food and Nutrition Board of the Institute of Medicine [11], refers only to grain (wheat) and legumes (chickpea) when discussing non-animal dietary protein quality. Hence, to date, data are not available to assess the usability of plant proteins aside from the grain and legume categories. Although Genoni et al. cite the Papier et al. paper [12] in support of their argument, these authors list legumes, pulses, protein alternatives (soya, tofu), nuts, cheese, yogurt, milk, plant milk, and eggs—but not fruits and vegetables—as the major protein foods for vegetarians. Secondly, Genoni et al. are critical of our use of the DIAAS in athletes stating that DIAAS analyses do not consider the metabolic demand for protein in the context of exercise. Citing Burd et al. [13], Genoni et al. argue that, in comparison to a sedentary state, physical activity (specifically, strength training) ‘lowers’ the amount of dietary protein required to support muscle synthesis since amino acid sensitivity of muscles is enhanced. Yet, Burd et al. clearly acknowledge that endurance exercise appears to have the opposite effect on the total daily dietary protein requirement for athletes compared to sedentary people, with regular endurance exercise training placing “more demand on dietary protein,” a phenomenon that is accentuated by intensity and exercise duration [13]. Our athletes were competitive endurance athletes (triathletes, runners, or cyclists); hence, if the assertions of Burd et al. are indeed true, our DIAAS analyses may have underestimated the protein needs of these athletes. Finally, Genoni et al. suggest that our statistical analyses were “flawed” for comparing strength differences between diet groups since we did not control for age, gender, energy intake, and lean mass. The stated purpose of our study was to “analyze dietary protein availability using the DIAAS method and to relate available protein to muscle mass and strength.” We demonstrated significant relationships between available protein and muscle mass (r = 0.541) and available protein and peak torque (r = 0.315) in our participants. We also reported that peak torque between diet groups was not significant (p = 0.074); furthermore, we reported that this statistic was further attenuated when gender was controlled. Had we controlled for gender, age, and energy intake, the resulting p value was similar to the unadjusted value (p = 0.078). We did not control for lean mass in this comparison between diet groups as our premise was that lean mass was a reflection of diet type. Indeed, peak torque per kilogram lean mass was virtually identical between diet groups. Tong et al. also reported a slight but significant reduction in strength for vegetarians versus omnivores from a large UK cohort (n = 229,806) and concluded that the differences in height, lean mass, and physical activity likely contributed to the difference in strength in vegetarians versus omnivores [14]. We were transparent in our analyses and followed all statistical assumptions, and we acknowledged in our report that additional research is necessary to comprehend the effect of protein quality on physical performance. We hope that these comments adequately address the concerns of Genoni et al. We value the opportunity to discuss our results in further detail.

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          Vegetarian diets are associated with healthy mood states: a cross-sectional study in Seventh Day Adventist adults

          Background The physical health status of vegetarians has been extensively reported, but there is limited research regarding the mental health status of vegetarians, particularly with regard to mood. Vegetarian diets exclude fish, the major dietary source of eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), critical regulators of brain cell structure and function. Omnivorous diets low in EPA and DHA are linked to impaired mood states in observational and experimental studies. Methods We examined associations between mood state and polyunsaturated fatty acid intake as a result of adherence to a vegetarian or omnivorous diet in a cross-sectional study of 138 healthy Seventh Day Adventist men and women residing in the Southwest. Participants completed a quantitative food frequency questionnaire, Depression Anxiety Stress Scale (DASS), and Profile of Mood States (POMS) questionnaires. Results Vegetarians (VEG:n = 60) reported significantly less negative emotion than omnivores (OMN:n = 78) as measured by both mean total DASS and POMS scores (8.32 ± 0.88 vs 17.51 ± 1.88, p = .000 and 0.10 ± 1.99 vs 15.33 ± 3.10, p = .007, respectively). VEG reported significantly lower mean intakes of EPA (p < .001), DHA (p < .001), as well as the omega-6 fatty acid, arachidonic acid (AA; p < .001), and reported higher mean intakes of shorter-chain α-linolenic acid (p < .001) and linoleic acid (p < .001) than OMN. Mean total DASS and POMS scores were positively related to mean intakes of EPA (p < 0.05), DHA (p < 0.05), and AA (p < 0.05), and inversely related to intakes of ALA (p < 0.05), and LA (p < 0.05), indicating that participants with low intakes of EPA, DHA, and AA and high intakes of ALA and LA had better mood. Conclusions The vegetarian diet profile does not appear to adversely affect mood despite low intake of long-chain omega-3 fatty acids.
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            Dietary Protein Quantity, Quality, and Exercise Are Key to Healthy Living: A Muscle-Centric Perspective Across the Lifespan

            A healthy eating pattern, regardless of age, should consist of ingesting high quality protein preferably in adequate amounts across all meals throughout the day. Of particular relevance to overall health is the growth, development, and maintenance of skeletal muscle tissue. Skeletal muscle not only contributes to physical strength and performance, but also contributes to efficient macronutrient utilization and storage. Achieving an optimal amount of muscle mass begins early in life with transitions to “steady-state” maintenance as an adult, and then safeguarding against ultimate decline of muscle mass with age, all of which are influenced by physical activity and dietary (e.g., protein) factors. Current protein recommendations, as defined by recommended dietary allowances (RDA) for the US population or the population reference intakes (PRI) in Europe, are set to cover basic needs; however, it is thought that a higher protein intake might be necessary for optimizing muscle mass, especially for adults and individuals with an active lifestyle. It is necessary to balance the accurate assessment of protein quality (e.g., digestible indispensable amino acid score; DIAAS) with methods that provide a physiological correlate (e.g., established measures of protein synthesis, substrate oxidation, lean mass retention, or accrual, etc.) in order to accurately define protein requirements for these physiological outcomes. Moreover, current recommendations need to shift from single nutrient guidelines to whole food based guidelines in order to practically acknowledge food matrix interactions and other required nutrients for potentially optimizing the health effects of food. The aim of this paper is to discuss protein quality and amount that should be consumed with consideration to the presence of non-protein constituents within a food matrix and potential interactions with physical activity to maximize muscle mass throughout life.
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              Restriction of meat, fish, and poultry in omnivores improves mood: A pilot randomized controlled trial

              Background Omnivorous diets are high in arachidonic acid (AA) compared to vegetarian diets. Research shows that high intakes of AA promote changes in brain that can disturb mood. Omnivores who eat fish regularly increase their intakes of eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), fats that oppose the negative effects of AA in vivo. In a recent cross-sectional study, omnivores reported significantly worse mood than vegetarians despite higher intakes of EPA and DHA. This study investigated the impact of restricting meat, fish, and poultry on mood. Findings Thirty-nine omnivores were randomly assigned to a control group consuming meat, fish, and poultry daily (OMN); a group consuming fish 3-4 times weekly but avoiding meat and poultry (FISH), or a vegetarian group avoiding meat, fish, and poultry (VEG). At baseline and after two weeks, participants completed a food frequency questionnaire, the Profile of Mood States questionnaire and the Depression Anxiety and Stress Scales. After the diet intervention, VEG participants reduced their EPA, DHA, and AA intakes, while FISH participants increased their EPA and DHA intakes. Mood scores were unchanged for OMN or FISH participants, but several mood scores for VEG participants improved significantly after two weeks. Conclusions Restricting meat, fish, and poultry improved some domains of short-term mood state in modern omnivores. To our knowledge, this is the first trial to examine the impact of restricting meat, fish, and poultry on mood state in omnivores.
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                Author and article information

                Journal
                Nutrients
                Nutrients
                nutrients
                Nutrients
                MDPI
                2072-6643
                23 April 2020
                April 2020
                : 12
                : 4
                : 1184
                Affiliations
                [1 ]College of Health Solutions, Nutrition Program, Arizona State University, 550 N. 3rd St., Phoenix, AZ 85004, USA
                [2 ]Kinesiology Department, 3900 Lomaland Dr., Point Loma Nazarene University, San Diego, CA 92106, USA; hlynch@ 123456pointloma.edu
                [3 ]College of Health Solutions, Voluntary Radical Simplicity lab, Arizona State University, 550 N. 3rd St., Phoenix, AZ 85004, USA; christopher.wharton@ 123456asu.edu
                Author notes
                Author information
                https://orcid.org/0000-0001-9540-6860
                https://orcid.org/0000-0002-6492-9754
                https://orcid.org/0000-0003-3622-3225
                Article
                nutrients-12-01184
                10.3390/nu12041184
                7230256
                32340169
                ee052072-a073-4cba-9406-08eeeafaede1
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 18 March 2020
                : 20 March 2020
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