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An investigation of the nutritional quality of common plant-based A summary of findings and implications for global development

Background Selecting adequate plant sources Plants provide a sustainable source of protein in comparison To explore the nutritional quality of common plant-based to animal-source proteins produced through traditional proteins and understand how they compare to animal-source agricultural practices.1 Although animal-source foods proteins with respect to human protein requirements, PATH supply easily digestible protein with adequate amounts conducted a structured literature review. The primary objective of all essential amino acids (EAAs) needed to fulfill human of this analysis was to examine the amino acid composition requirements for growth and development,2-6 livestock of common plant-based proteins and identify a high-quality production is associated with significant greenhouse gas subset that meets estimated amino acid requirements for emissions and environmental impact.7,8 For many vulnerable children under age five, exhibits high digestibility, and thus populations in low- and middle-income countries, plant compares favorably to animal-source proteins such as foods (e.g., , tubers, legumes) play central roles in those found in and eggs. A secondary objective was to diets and are typically much more accessible and affordable review the potential implications of production, processing than animal-source foods. However, plant proteins typically techniques, and relevant environmental considerations of each contain lower levels of certain amino acids (e.g., and of these identified plant-based proteins. Here, we summarize the sulfur amino acids and ).2,9,10 Protein high-level findings from this analysis. quality is of critical importance for populations with low From an initial literature search, we identified 26 commonly energy intake, low protein intake, and/or elevated protein cited plant protein sources and created a list of prioritized needs associated with infection and other pathological attributes to help characterize their relative nutritional conditions. As such, evaluating the nutritional quality quality and down select protein sources for further of plant-based protein sources is an important step in investigation (Figure 1). Specifically, we reviewed the achieving a sustainable future protein economy.11

FIGURE 1. Methods for down-selection of high-quality plant proteins based on prioritized attributes.

Context of use Target population To provide high-quality plant-based protein for Children under five years general consumption or use in food aid products of age

Prioritized quality Acceptable standards set for down-selection attributes

Provides adequate amount of lysine and Amino acid methionine based on FAO scoring pattern for profile children 6 months to 3 years of age Review of Preliminary literature production review to identify Digestibility of the plant protein of greater implications, processing commonly cited plant Digestibility than 75 percent techniques, and proteins of interest environmental (N=26) considerations

PDCAAS/ PDCAAS of greater than 70 percent DIAAS

Abbreviations: DIAAS, digestible indispensable amino acid score; FAO, Food and Agriculture Organization of the United Nations; PDCAAS, protein-digestibility corrected amino acid score. literature on these 26 proteins to describe their amino to age-specific EAA scoring patterns and represented in acid composition, digestibility, and protein-digestibility milligrams of amino acid per gram of protein requirement.11 For corrected amino acid scores (PDCAAS) or digestible the purposes of this analysis, acceptable amino acid scoring indispensable amino acid scores (DIAAS). Proteins identified patterns were set to ensure that the dietary requirements of as high quality according to these attributes were then growing children under the age of five would be met.12 further reviewed to understand the potential implications For each of the 26 plant proteins identified through the of production, processing techniques, and relevant preliminary literature search, Figure 1 shows the EAA environmental considerations. concentrations in each plant protein isolate (mg/g). Amino acid scores are also provided for skim milk and Amino acid scores egg whites as a comparison. Of the plants reviewed, chia seed, chickpea, duckweed, , rapeseed, , and Dietary protein adequacy encompasses both protein quantity spirulina protein isolates were able to provide adequate and quality.2 Adequate quantities of dietary protein for amounts (within 10 percent) of all EAAs. As plant-based consumption are determined by the minimum amount of total diets are limited by lysine and sulfur amino acids, potato and protein required for maintenance and growth (g/kg/d), and groundnut were also included because they have sufficient more specifically the minimum EAA requirements (mg/kg/ concentrations of both EAAs to meet the requirements of day).12 Protein quality requirements are defined according infants and young children.

FIGURE 2. The amino acid scores of common plant proteins using food composition data, arranged according to total protein content (g/100g).

HIS ILE LEU LYS SAA AAA THR TRP VAL Protein content (g/100g) Rice 1.18 1.35 1.25 0.63 1.63 1.67 1.16 1.36 1.42 6.5 Coconut 1.15 1.23 1.13 0.78 1.43 1.57 1.18 1.39 1.41 6.9 Amino Acid Score Color Key 0.51 0.37 0.62 0.16 0.48 0.57 0.40 0.28 0.39 8.1 0 - 0.49 Largely deficient Potato 0.95 1.07 0.81 1.00 1.10 1.74 1.09 1.16 1.25 8.2 0.5-0.89 Deficient Sorghum 1.16 1.27 2.13 0.38 1.03 1.57 1.05 1.37 1.23 10.6 0.90-0.99 Slightly deficient 1.13 1.14 1.03 0.47 1.54 1.49 0.93 1.49 1.03 12.6 >1.0 Adequate

Quinoa 1.44 1.12 0.90 0.95 1.34 1.17 0.96 1.39 0.98 14.1 Abbreviations AAA, aromatic amino acids ( and ) Chia seed 1.61 1.51 1.26 1.03 2.23 1.84 1.38 3.10 1.34 16.5 HIS, 1.20 1.28 1.15 0.73 1.58 1.67 1.10 1.63 1.29 16.9 ILE, LEU, Cashew 1.25 1.35 1.22 0.89 1.53 1.54 1.22 1.85 1.40 18.2 LYS, lysine SAA, sulfur amino acids (methionine and cysteine) Flax seed 1.29 1.53 1.02 0.83 1.44 1.52 1.35 0.51 1.36 18.3 THR, TRP, Groundnut 1.07 1.47 1.24 1.16 1.09 1.50 1.46 0.73 1.05 20.3 VAL, . Amino acid content was determined for edible Almond 1.25 1.09 1.04 0.46 0.64 1.42 0.90 1.15 0.92 21.5 portions on a dry matter basis. Amino acid scores were calculated based on FAO child scoring patterns Chickpea 1.46 1.30 1.12 1.17 0.95 1.71 1.19 1.21 0.97 22.4 using 0.5–year amino acid requirements.12

Mung bean 1.33 0.90 1.07 0.98 0.68 1.44 1.19 1.17 1.04 23.2 Data sources: USDA Food Composition Databases,13 FAO/INFOODS Global Database,14 Tanzania Food Duckweed 0.90 1.13 1.18 0.98 1.15 1.52 1.32 ND 1.12 25.0 Composition Table,15 Feedipedia Nutritional Tables,16 Appenroth et al. 2018.17 Cowpea 1.70 1.44 1.18 1.18 0.85 1.63 1.28 1.32 1.04 25.2 1.26 1.10 0.98 0.63 0.93 1.81 1.10 1.14 0.98 25.8 1.21 1.24 1.08 1.23 0.77 1.54 1.22 1.04 1.09 26.4 Lentil 1.14 1.25 1.14 1.23 0.65 1.42 1.02 1.15 1.16 27.0 Fava bean 1.29 1.25 1.09 1.09 0.69 1.42 1.11 1.01 1.03 28.4 Hemp seed 1.54 1.27 1.04 0.71 1.88 1.65 1.30 1.38 1.31 31.6 Milk (skim) 1.36 1.89 1.48 1.39 1.27 1.86 1.46 1.66 1.56 36.2 Soybean 1.65 1.69 1.37 1.30 1.22 1.93 1.56 1.91 1.29 36.5 Lupin 1.30 1.24 1.10 0.85 0.90 1.39 1.10 0.97 0.89 37.6 Rapeseed 1.30 1.25 1.03 0.96 1.59 1.31 1.39 1.41 1.19 38.3 Spirulina 0.94 1.74 1.30 0.92 1.17 1.79 1.67 1.90 1.42 57.5 Egg white 1.13 1.77 1.28 1.19 2.23 1.87 1.47 1.45 1.48 81.1 Digestibility 1. Willett W, Rockström J, Loken B, et al. Food in the Anthropocene: the EAT-Lancet Commission on healthy diets from sustainable The bioavailability of EAAs is largely determined from the food systems. Lancet. 2019;393(10170):447–492. doi:10.1016/ digestibility of a food, or the proportion of consumed amino S0140-6736(18)31788-4. acid that is absorbed. The digestibility estimates of purified 2. Institute of Medicine (US), Institute of Medicine (US), eds. Dietary forms of plant protein are typically better than the digestibility Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty of unpurified forms. Of the nine plant proteins that met the Acids, Cholesterol, Protein, and Amino Acids. Washington, DC: The amino acid criteria for this analysis, all of the protein isolates National Academies Press; 2005. exceeded the minimum acceptable criteria of greater than 75 3. Mariotti F, ed. Vegetarian and Plant-Based Diets in Health and percent digestibility. In fact, several (chickpea, soybean, and Disease Prevention. London: Elsevier/Academic Press, an imprint potato) exceeded 95 percent digestibility.18,19,20,21 of Elsevier; 2017.

4. Huang S, Wang LM, Sivendiran T, Bohrer BM. Review: Amino acid concentration of high protein food products and an overview of the PDCAAS/DIAAS current methods used to determine protein quality. Critical Reviews The protein-digestibility corrected amino acid score in Food Science and Nutrition. 2018;58(15):2673–2678. (PDCAAS) and digestible indispensable amino acid score 5. Michaelsen KF, Hoppe C, Roos N, et al. Choice of foods and (DIAAS) are measures of protein quality that account for both ingredients for moderately malnourished children 6 months amino acid patterns and digestibility.22,23 Overall, there was to 5 years of age. Food and Nutrition Bulletin. 2009;30(3_ limited availability of reliable PDCAAS/DIAAS values for the suppl3):S343-S404. doi:10.1177/15648265090303S303. nine plant protein isolates, thereby limiting our ability to use 6. Iannotti LL, Lutter CK, Bunn DA, Stewart CP. Eggs: the uncracked these indicators as definitive measures of protein quality. potential for improving maternal and young child nutrition among Groundnut has a PDCAAS of 25 percent and was therefore the world’s poor. Nutrition Reviews. 2014;72(6):355–368. doi:10.1111/ excluded from the final list as it fell below the pre-established nure.12107. cutoff of 70 percent.24 7. Clark MA, Springmann M, Hill J, Tilman D. Multiple health and environmental impacts of foods. Proceedings of the National Academy of Sciences. 2019;116(46):23357–23362. doi:10.1073/ Beyond nutrient adequacy, examining pnas.1906908116. sustainability 8. Godfray CJ, Aveyard P, Garnett T, et al. Meat consumption, health, and the environment. Science. 2018;361(6399):eaam5324. Through this down-selection process, we identified eight doi:10.1126/science.aam5324. high-quality plant protein isolates. However, beyond nutrient 9. Wang G, Xu M, Wang W, Galili G. Fortifying horticultural crops with quality, it is also important to consider the sustainability essential amino acids: a review. International Journal of Molecular and appropriateness of a food crop before investing in Science. 2017;18(6):1306. doi:10.3390/ijms18061306. its advancement for use among vulnerable populations. Balancing the social, economic, and environmental 10. Galili G, Amir R. Fortifying plants with the essential amino acids lysine and methionine to improve nutritional quality. Plant dimensions of the food system will be critical to achieve Biotechnology Journal. 2013;11(2):211–222. doi:10.1111/pbi.12025. sustainability in food and agriculture. Additional considerations for these plant protein isolates include their 11. Leinonen I, Iannetta PPM, Rees RM, et al. Lysine supply is a critical versatility as an ingredient in food products, extraction factor in achieving sustainable global protein economy. Frontier Sustainable Food Systems. 2019;3. doi:10.3389/fsufs.2019.00027. processes, organoleptic features, and proven efficacy in improving health outcomes. 12. Food and Agriculture Organization of the United Nations, ed. Dietary Protein Quality Evaluation in : Report of an To further refine our list, we reviewed the literature on the FAO Expert Consultation, 31 March–2 April, 2011, Auckland, New production, processing techniques, and environmental Zealand. Rome: Food and Agriculture Organization of the United considerations for each of the eight proteins with high Nations; 2013. nutritional quality. Ultimately, this review elevated chickpea, 13. USDA. Food Composition Databases. https://ndb.nal.usda.gov. soybean, quinoa, spirulina, duckweed, and potato protein Accessed September 3, 2019. isolates for further consideration in their applications for 14. INFOODS: FAO/INFOODS Databases. http://www.fao.org/infoods/ addressing malnutrition among vulnerable populations in infoods/tables-and-databases/faoinfoods-databases/en/. low- and middle-income countries, including for use in food Accessed September 3, 2019. aid products. 15. Lukmanji Z, Hertzmark E, Mlingi N, Assey V, Ndossi G, Fawzi W. Tanzania Food Composition Tables. Dar es Salaam: Muhimbili University of Health and Allied Sciences, Tanzania Food and For more information Nutrition Centre and Harvard School of Public Health; December For more information on the full report, please contact: 2009. Dr. Megan Parker, Senior Nutrition Research Officer, 16. Feedipedia website. Rapeseed meal page. https://www. [email protected] feedipedia.org/node/52. Accessed September 3, 2019.

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