production and supply of high-quality food protein for human consumption: sustainability,...

Ann. N.Y. Acad. Sci. ISSN 0077-8923

ANNALS OF THE NEW YORK ACADEMY OF SCIENCESIssue: Annals Reports

Production and supply of high-quality food proteinfor human consumption: sustainability, challenges, andinnovations

Guoyao Wu,1 Jessica Fanzo,2 Dennis D. Miller,3 Prabhu Pingali,4 Mark Post,5 Jean L. Steiner,6

and Anna E. Thalacker-Mercer7

1Department of Animal Science, Texas A&M University, College Station, Texas. 2The Institute of Human Nutrition and theCenter on Globalization and Sustainable Development, Columbia University, New York, New York. 3Department of FoodScience, Cornell University, Ithaca, New York. 4Charles H. Dyson School of Applied Economics and Management, CornellUniversity, Ithaca, New York. 5Department of Physiology, Maastricht University, the Netherlands. 6Agricultural ResearchService, Grazinglands Research Laboratory, U.S. Department of Agriculture, El Reno, Oklahoma. 7Division of NutritionalSciences, Cornell University, Ithaca, New York

Address for correspondence: Guoyao Wu, Department of Animal Science, Texas A&M University, College Station, [email protected]

The Food and Agriculture Organization of the United Nations estimates that 843 million people worldwide are hun-gry and a greater number suffer from nutrient deficiencies. Approximately one billion people have inadequate proteinintake. The challenge of preventing hunger and malnutrition will become even greater as the global population growsfrom the current 7.2 billion people to 9.6 billion by 2050. With increases in income, population, and demand for morenutrient-dense foods, global meat production is projected to increase by 206 million tons per year during the next35 years. These changes in population and dietary practices have led to a tremendous rise in the demand forfood protein, especially animal-source protein. Consuming the required amounts of protein is fundamental to hu-man growth and health. Protein needs can be met through intakes of animal and plant-source foods. Increasedconsumption of food proteins is associated with increased greenhouse gas emissions and overutilization of water.Consequently, concerns exist regarding impacts of agricultural production, processing and distribution of food pro-tein on the environment, ecosystem, and sustainability. To address these challenging issues, the New York Academy ofSciences organized the conference “Frontiers in Agricultural Sustainability: Studying the Protein Supply Chain toImprove Dietary Quality” to explore sustainable innovations in food science and programming aimed at producingthe required quality and quantity of protein through improved supply chains worldwide. This report provides anextensive discussion of these issues and summaries of the presentations from the conference.

Keywords: agriculture; livestock; plant; protein; production; sustainability; undernutrition; stunting; food science

Introduction

The Food and Agriculture Organization (FAO) ofthe United Nations recently estimated that 843 mil-lion people, nearly a seventh of the world’s popu-lation, are chronically hungry and a greater num-ber suffer from nutrient deficiencies.1 In centralAfrica and South Asia, 10% to 30% of children haveprotein malnutrition.2,3 Approximately one billionpeople worldwide have inadequate protein intake,contributing to impaired growth and suboptimal

health.1–3 For example, globally 165 million chil-dren under five years of age are stunted.1 Thesenumbers could increase substantially, as the UnitedNations projected in June 2013 that the world pop-ulation will reach from the current 7.2 billion to 8.2billion by 2025 and to 9.6 billion by 2050.4 Thesenutritional deficiencies highlight an urgent need tofind sustainable solutions to food insecurity, par-ticularly the availability of high-quality food pro-teins for human consumption. Towards this goal,on December 12, 2013, the New York Academy of

doi: 10.1111/nyas.12500

1Ann. N.Y. Acad. Sci. 1321 (2014) 1–19 C© 2014 New York Academy of Sciences.

Sustainability, challenge and innovations Wu et al.

Sciences convened the conference “Frontiers inAgricultural Sustainability: Studying the ProteinSupply Chain to Improve Dietary Quality” featuringexpert discussions on the science of protein nutri-tion, challenges and obstacles in achieving a sus-tainable protein supply; new technologies for theproduction of protein-rich foods; and dietary in-terventions at the levels of the farm, community,nation, and globe.

Mandana Arabi (executive director, the SacklerInstitute for Nutrition Science) introduced the con-ference by highlighting the importance of integrat-ing scientific, agricultural, health, and environmen-tal sectors to build better systems for food-proteinproduction. Speakers were Barbara Burlingame(Food and Agriculture Organization of the UnitedNations), Jessica Fanzo (Columbia University), Ga-bor Forgacs (University of Missouri–Columbia),Geoffrey von Maltzahn (Flagship Ventures), DennisMiller (Cornell University), Prabhu Pingali (Cor-nell University), Mark Post (Maastricht University,the Netherlands), Charles Schasteen (DuPont Nu-trition & Health Protein Solutions), Josip Simunovic(North Carolina State University), Jean Steiner (U.S.Department of Agriculture), Anna E. Thalacker-Mercer (Cornell University), Irvin Widders (Michi-gan State University), and Guoyao Wu (Texas A&MUniversity). Topics presented at the meeting in-cluded (1) the role of agriculture in providing di-etary protein for human consumption; (2) proteinfoods as sources of amino acids and micronutri-ents; (3) the function of dietary protein in humanhealth; (4) challenges to the sustainability of proteinproduction by animal agriculture; (5) approachesto solving sustainability problems; and (6) innova-tions in the protein supply chain. These topics arediscussed in the following sections.

The role of agriculture in providing dietaryprotein for human consumption

Agriculture dates back thousands of years. The pri-mary role of agriculture is to grow crops and raiselivestock and poultry to provide food for humanpopulations. Plant production takes advantage ofthe natural sunlight as the sole energy source whilerequiring fertilization and water. In contrast, do-mestic animals (e.g., ruminants, pigs and poultry)are raised in both extensive (e.g., grassland-based)and intensive (e.g., housing) systems, with foods ofplant origin as their primary energy sources.5 Agri-

Figure 1. Digestion of dietary protein in the gastrointestinaltract of humans and animals. Proteases in the stomach andthe small intestine hydrolyze dietary protein into large peptidesand then to small peptides and free amino acids. Products ofprotein digestion in the lumen of the small intestine consist ofapproximately 20% free amino acids and 80% of dipeptides plustripeptides. In the lumen of the small intestine, all dietary aminoacids undergo various degrees of catabolism by luminal bacteriaand some of them are oxidized by enterocytes. Uptake of �60%and �40% of free amino acids from the lumen of the small intes-tine into enterocytes is performed by Na+-dependent and Na+-independent amino acid transport systems, respectively. AA =amino acids; GSH = glutathione; NT = nucleotides; PepT1 =H+ gradient-driven peptide transporter 1; SI = small intestine.

cultural production is key to supplying food proteinand, therefore, to developing and sustaining humancivilization.6

Needs for protein in human dietsThere is a myth among lay individuals that humanscan make proteins (e.g., insulin and growth hor-mone) without a need to consume dietary protein.Guoyao Wu explained that without the provisionof dietary protein, which is the ultimate source ofamino acids in the blood and cells, proteins cannotbe synthesized in the body.7 This myth likely resultedfrom a lack of understanding of protein nutrition inmammals. It should be borne in mind that utiliza-tion of dietary proteins by the body requires theirdigestion in the gastrointestinal tract; the absorptionof digestion products (amino acids, dipeptides, andtripeptides) through enterocytes (absorptive epithe-lial cells of the small intestine) into the portal vein;metabolic transformation of amino acids and smallpeptides in a cell- and tissue-specific manner; andsynthesis of tissue proteins from amino acids inthe blood and cells (Fig. 1). Currently, it is very

2 Ann. N.Y. Acad. Sci. 1321 (2014) 1–19 C© 2014 New York Academy of Sciences.

Wu et al. Sustainability, challenge and innovations

expensive to produce large amounts of crystallineamino acids, and yet humans need food proteinsas major sources of these nitrogenous nutrients tosupport growth, development, reproduction, lacta-tion, and health. Thus, plant and animal agricultureis crucial to providing dietary protein for humanconsumption.8–15

Plant- and animal-source foods for proteinprovisionHumans consume proteins in foods consisting ofanimal- (e.g., dairy products, eggs, fish, and meats)and plant- (e.g., cereals, beans, potatoes, cassava,vegetables, and fruits) based agricultural products.6

Dennis Miller indicated that plant-based foods (pri-marily cereals and legumes) have been a majorsource of protein for humans for millennia. Cur-rently, plant- and animal-based foods contribute�65% and �35%, respectively, of protein in hu-man diets on a worldwide basis. In contrast, in NorthAmerica, plant and animal foods provide �32% and�68% of total protein, respectively. With increasesin population and per capita income, demand foranimal-source foods is expected to increase sub-stantially. This is particularly evident given that thepopulation of the world is projected to reach 9.6 bil-lion in 2050, as noted previously. As people becomewealthier, average meat consumption per capita isexpected to increase by 29% from 40.0 kg in 2013to 51.5 kg in 2050.5 Accordingly, global meat pro-duction will need to increase from 288 million tonsin 2013 to 494 million tons in 2050. Because animaldiets may include grains (e.g., corn and soybean)whose global supply is estimated to be relativelystagnant over the next 40 years,5 animal produc-tion is perceived to compete with humans for food.However, it should be recognized that ruminantscan consume human inedible plants (e.g., pasturegrasses, alfalfa, and hay) and/or their byproducts(e.g., soybean hulls, beet pulp, brewers dried grains,and distillers dried grains), thereby converting low-quality materials to high-quality animal products(Fig. 2). Most of these ingredients are also fed topigs. Guoyao Wu emphasized that this is indeed aunique advantage of livestock production to society.

Food insecurity and protein deficienciesThe need to substantially increase agricultural pro-duction of protein also lies in the current sta-tus of food insecurity. In October 2013, the FAOreported that 843 million people worldwide (in-

Figure 2. Nutritional perspectives of land-based productionof animal proteins. Livestock and poultry convert low-qualityforages or ingredients into high-quality proteins for human con-sumption.

cluding children and adults) suffered from hunger,nearly all of whom reside in low- and middle-income countries.1 Deficiencies of protein and mi-cronutrients (including vitamin A, iron, zinc, andfolate) remain major nutritional problems in poorregions of the world.1,2 Of note, deficiencies of vi-tamin A, iron, zinc, and other micronutrients canresult from deficiencies of dietary proteins.3 Ap-proximately one billion people worldwide havechronically inadequate protein intake or protein-energy malnutrition.1–3 Partly due to protein de-ficiencies, vitamin and mineral deficiencies (alsoknown as hidden hunger) affect an estimated 2 bil-lion people worldwide with the highest prevalencebeing in sub-Saharan Africa and South Asia.16 Pro-tein deficiencies also occur in subpopulations indeveloped nations. For example, Dasgupta et al.17

have reported that 51% of home-bound elderly sub-jects receiving home-delivered meals in the UnitedStates have protein intakes below the recommendeddietary allowance (RDA) of 0.8 g protein/kg bodyweight/day.

United Nations Secretary-General Ban Ki-moon’sZero Hunger Challenge, announced in 2013,presents his vision for global food security: 100%access to adequate food throughout the year, 100%growth in smallholder productivity and income, 0%stunted children under age 2, and 0% food loss orwaste.8 Barbara Burlingame, deputy director of theFAO’s Nutrition Division, explained that these goalsare arrayed around a central aim: sustainable foodsystems.

Additionally, Jessica Fanzo suggested that be-sides agricultural sustainability, biodiversity is es-sential to the prevention of human hunger and the



improvement of food’s nutritional quality. How-ever, the sole cultivation of plant species with a highcontent of specific nutrients has caused a tremen-dous erosion of biodiversity.6 The recognition ofvarietal differences in nutrient content promptedthe International Rice Commission to recommendin 2013 that rice biodiversity and nutritional com-position be analyzed before genetic modification isbegun. Accordingly, Burlingame discussed notablerecommendations made in 2013 by the Commissionon Genetic Resources for Food and Agriculture tothe FAO, which are intended to promote collabora-tion among government sectors focused on biodi-versity and environment and among academic de-partments and nonprofits focused on human nutri-tion. She pointed out that African nutrition expertshave long argued that agrobiodiversity determinesdietary quality and is, therefore, central to food se-curity; but this idea is only now finding broaderacceptance.

Protein foods as sources of amino acidsand micronutrients

Amino acids are building blocks of protein in bothplants and animals. Protein foods consist of eggs,meat, dairy products, poultry, seafood, beans, peas,processed soy products, nuts, and seeds. All of thesefoods contain relatively high levels of protein (e.g.,> 40% on dry matter basis). In contrast, most sta-ple foods of plant origin (except for legumes) haveprotein content < 15% (dry matter basis). Miner-als (e.g., iron and zinc) and vitamins (e.g., vitaminsB6 and B12, and vitamin A) are essential nutrientsfor animals and humans, and must be present in thediet. With the exception of vitamin C, animal tissuesare good sources of most micronutrients. In contrastto animals, plants can synthesize all vitamins and/orvitamin precursors (�-carotene, a precursor of vi-tamin A) with the exception of vitamin B12, whichis present in only animal-source foods. While pro-tein is relatively stable during post-harvest storage,processing of plant- and animal-source foods canreduce their vitamin content to various degrees, de-pending on storage conditions, the stability of thevitamin, and time.

Plant- and animal-source foods for provisionof amino acidsThe quantity and quality of protein are both deter-minants of the adequacy of diets for meeting pro-

tein requirements.7 Protein content in most plantsis relatively low. Additionally, most plant proteinsare “incomplete” in that they are deficient in one ormore of the nutritionally indispensable (essential)amino acids.7 However, proper combinations of dif-ferent plant protein sources may be complementary,with one source providing the amino acid that islimiting in another source and vice versa, therebypossibly making the mixture of plant proteins “com-plete” sources of amino acids. In many societies, tra-ditional diets contain both cereals (e.g., maize andwheat) and legumes (e.g., peas and beans), whichare complementary for most but not all amino acidsand, therefore, may meet protein requirements foradults but not for optimal growth in children.9

In his presentation, Irvin Widders reported thatthe protein quality and crop yield of legume vari-eties have been improved in rural Guatemala, alongwith their enhanced consumption by humans. Al-though some plant-based foods contain inhibitorsthat reduce protein digestibility, these inhibitors canbe inactivated by adequate heat processing priorto consumption. In addition, cereals and legumescontain phytates and other factors that may inhibitthe absorption of trace minerals such as iron andzinc. Diets high in these foods may increase the riskfor certain micronutrient deficiencies. Guoyao Wuadded that animal proteins contain adequate andbalanced amounts of all amino acids for humanconsumption to promote optimal growth, develop-ment, and health. For example, meat and white ricecontain 2.98 and 0.27 g sulfur amino acids (methio-nine plus cysteine) per 100 g dry matter, respec-tively (Table 1). To meet the Institute of Medicine–recommended dietary allowance of these two aminoacids by the 70-kg adult human,10 daily intakes ofmeat and white rice would be 45 and 493 g drymatter, respectively. Thus, consumption of meatcan substantially reduce the need for plant-basedfoods to meet adequate protein requirements of hu-mans, particularly children. While there is a com-mon belief that there are virtually no nutrients inanimal-based foods that are not better provided byplants, it is animal-source, but not plant-source,products that supply taurine (a sulfur-containingamino acid) that is essential for protecting the eyes,heart, skeletal muscle, and other tissues of hu-mans from oxidative damage and degeneration.11

Furthermore, animal-source, but not plant-source,foods are dietary sources of carnosine (a key



Table 1. Composition of amino acids in meat and plant-source foodsa

Food Protein and amino acid content (%, g/100 g DM)

Protein Lysine SAA Threonine Tryptophan

Meatb 66.7 4.89 2.98 3.56 0.93

Soybeanc 42.0 2.69 1.05 1.60 0.50

Wheatc 11.8 0.34 0.47 0.34 0.11

Cornc 10.8 0.28 0.44 0.35 0.08

White ricec 8.2 0.19 0.27 0.18 0.07

aAdopted from Li et al.49 and Young and Pellett.50

bDry matter (DM) content = 30%cDM content = 87%SAA = sulfur-containing amino acids (methionine + cysteine)

antioxidative dipeptide) for humans to maintainneurological and muscular functions.7 These factshighlight the importance of animal agriculture forthe benefit of humankind.

Plant- and animal-source foods for provisionof vitamins and mineralsFoods of plant origin are excellent sources of manyvitamins (particularly vitamins of the B complexexcept for vitamin B12 that is biosynthesized onlyby microorganisms), but have low contents of traceminerals (Table 2). In contrast, meats, egg and milkare excellent sources of most of these micronutri-ents. Of note, iron in animal-source foods is ab-sorbed by the human small intestine more effi-ciently than iron in plant-source foods.12 Milk isan abundant source of calcium for bone growth.Moreover, animal-source foods are the only re-liable source of vitamin B12, a nutrient that isdeficient in the diets for up to 86% of childrenin some developing countries.12 This presents adilemma. Namely, low intakes of animal-sourcefoods increase risks for protein and micronutri-ent deficiencies, especially in children and the el-derly, but these foods are expensive and their pro-duction at a low efficiency may be environmentallyunsustainable.

In her presentation, Barbara Burlingame indi-cated that fortified foods, as well as the supplementsand therapeutic products that consist of either singlenutrients or a combination of nutrients, are not theonly solutions to malnutrition and that improvingwhole dietary patterns should be seriously consid-ered. This further underscores important roles forprotein foods (particularly foods of animal origin)

as excellent sources of amino acids and micronutri-ents for humans.

There are metabolic interactions among proteins,vitamins, and minerals. Thus, efficient utilizationof dietary protein depends on the availability of notonly water- and lipid-soluble vitamins but also traceelements, and vice versa. However, as noted previ-ously, most of trace elements and many of the lipid-soluble vitamins are deficient in plant-source foods.Thus, micronutrient fortification of staple foods hasbeen successfully used to prevent micronutrient de-ficiencies in populations. Food fortification beganin the 1920s with the production of iodized salt.This was followed by fortification of milk with vi-tamin D in the 1930s, the enrichment of flour andother cereal products with iron, niacin, riboflavin,and thiamin in the 1940s, fortification of margarinesand low fat milk with vitamin A in the 1950s, forti-fication of infant cereals and infant formulas in the1960s, and enrichment of flour with folic acid in the1990s. Food fortification interventions in the UnitedStates and other industrialized countries have beencredited with dramatically reducing the prevalencesof goiter (iodine deficiency), rickets (vitamin D de-ficiency), pellagra (niacin deficiency), and iron de-ficiency. These deficiencies were widespread in theUnited States and elsewhere in the early part of the20th century and continue to be major problems inmany developing countries around the world.

Miller described his own work undertaken withHarvestPlus,18 a global alliance of research insti-tutions that uses plant breeding to enhance theconcentrations of iron, zinc, and/or beta-carotenein staple food crops. One of his projects aimedto determine whether iron in a newly developed



Table 2. Micronutrients from plant- and animal-source foods

Micronutrient Plant-source foods Animal-source foods

Thiamin (vitamin B1) Peas and other legumes, nuts, whole

grains, and wheat germ

Meat, liver, milk, eggs, and other animal

products

Riboflavin (vitamin B2) Wheat germ, whole grains, nuts,

legumes, and green vegetables


products

Niacin (vitamin B3) Whole grains, wheat germ, nuts,

legumes, and vegetables


products

Vitamin B6 Nuts, legumes, whole grains, vegetables,

and bananas


products

Pantothenic acid Whole grains, legumes, nuts, and

vegetables


products

Biotin Whole grains, legumes, nuts, and

vegetables


products

Folic acid Peas and other legumes, nuts, juice,

whole grains, and leafy vegetables

Liver, milk, eggs, meat, and other

animal products

Vitamin B12 Absent from plants Meat, liver, milk, eggs, and other animal

products

Vitamin C Abundant in fresh vegetables, juice,

tomatoes, green tea, and potatoes, but

virtually absent from whole grains

Liver, milk, eggs, meat, and other

animal products contain some

vitamin C

Vitamin A Absent from plants; however, dark,

green, orange, or yellow vegetables

are good sources of provitamin A

Liver, milk, eggs, meat, and butter are

good sources of vitamin A

Vitamin D Absent from plants; however, sun-dried

vegetables contain vitamin D2

Milk, eggs, and liver are good sources of

vitamin D3

Vitamin E Vegetable oils and wheat germ oil Meat, liver, milk, eggs, fat, and other

animal products

Vitamin K Alfalfa, pepper, whole grains and

vegetables


products

Iron Limited in plants, but beans and dark

green leafy vegetables provide some

Meat, liver, blood, milk, and other

animal products

Zinc Limited in plants, but legumes, nuts,

wheat germ, and seeds provide some


animal products

Copper Whole grains, legumes, nuts, green leafy

vegetables, wheat germ, and seeds


animal products

Selenium Whole grains, legumes, nuts, green leafy

vegetables, wheat germ, seeds; very

limited in certain regions


animal products

Molybdenum Whole grains, legumes, nuts, green leafy

vegetables, wheat germ, and seeds


animal products

biofortified variant of the common bean is bioavail-able for hemoglobin synthesis in animals. In onestudy, pigs fed diets containing beans biofortifiedin iron had a significantly increased total bodyhemoglobin iron content over those fed a dietcontaining a conventional variety of the common

bean, suggesting that biofortified beans could in-crease the intake of bioavailable iron in humanpopulations that consume beans as a dietarystaple.19 While acknowledging that micronutrientbiofortification might not be a silver bullet, Millerargued for its promise as an approach to prevent



micronutrient deficiencies in populations in devel-oping countries.20

The function of dietary protein in humanhealth

As noted previously, dietary protein is the ultimatesource of the amino acids used to make proteinin humans. In the body, proteins play importantroles in (1) cell and extracellular structures; (2)enzyme-catalyzed reactions; (3) gene expression; (4)hormone-mediated actions; (5) muscle contraction;(6) osmotic regulation; (7) protection against oxida-tive stress, infection, and bleeding; (8) regulation ofmetabolism; and (9) storage and transport of nutri-ents (including long-chain fatty acids, iron, vitaminA, and zinc) and oxygen.7 Therefore, dietary pro-tein intake has an important influence on the statusof other nutrients in the body and adequate proteinnutrition is essential for optimal human growth andhealth.

Protein nutrition and children: growth andhealthDeposition of protein in tissues, particularly skele-tal muscle, is required for the growth of children.They are more sensitive to protein malnutritionthan adults. Available evidence shows that pro-tein deficiency is a major factor causing impairedgrowth in millions of children worldwide.1–3 Us-ing results from previously published studies, Wureiterated that isocaloric supplementation (1050 –1255 kJ/day) with meat to basal diets (7300 kJ/day)consisting almost exclusively of staple crops (cornand beans) could increase upper arm muscle areaby 80% in 7-year-old children in Kenya, comparedwith the control group.9 These findings indicate thatplant proteins alone may not be adequate to supportmaximal growth in humans. Furthermore, infantsand children with a deficiency of dietary proteinexhibit impaired immune function and increasedsusceptibility to infectious disease.7

Protein nutrition and agingDietary requirements of protein by humans differthroughout the life span. While it was previouslythought that adults need less dietary protein as theyage, results of recent studies indicate that increasedintake of high-quality protein can alleviate muscleloss in elderly subjects.

Indeed, Anna E. Thalacker-Mercer reported thatsome populations, such as older adults, are particu-

larly vulnerable to the adverse effects of inadequatedietary protein. Her research has focused on pro-tein metabolism in skeletal muscle, which accountsfor 40–45% of body weight in healthy nonobese in-dividuals and is the major reservoir of protein inhumans.7 When dietary protein intake is reduced,as it often is in the elderly, the body breaks downskeletal muscle protein to generate the amino acidsit needs for the provision of energy, immune re-sponse and other physiological processes. Underconditions of protein malnutrition, skeletal musclealso becomes less able to synthesize protein, lead-ing to muscle atrophy. Using advanced molecular-biology techniques, Thalacker-Mercer has furtheridentified a crucial clue to the impact of aging onmuscle metabolism from her studies of transcip-tome (gene expression) profiles.

Protein nutrition is a major factor affectinghealthy aging in humans.13 Globally, the aging pop-ulation is growing, and in most countries life ex-pectancy is increasing. However, this could meanadditional years of impaired living from chronicdisease and disability. The mass and function ofskeletal muscle is a significant factor affecting thequality of life in the elderly, and this tissue is im-pacted by nutrition, particularly dietary protein.21

Acute studies demonstrate that old (compared toyoung) adult skeletal muscle has impaired anabolicresponses when the quantity of amino acids avail-able for protein synthesis is low; responses im-proved with higher quantities.14 The skeletal mus-cle transcriptome further supports the view thatolder adults have an impaired anabolic responseto habitual protein consumption between 0.75–1.00 g/kg body mass per day and an augmentedcatabolic response when protein intakes are belowthe RDA values (Fig. 3).15 Recent studies demon-strate enhanced mixed muscle protein synthesis inadults consuming �30 g of dietary protein at eachmeal throughout the day compared to a skeweddietary protein intake (i.e. the majority of pro-tein is consumed at the evening meal).22 Furtherresearch is necessary to determine the benefits ofbalancing the composition and amounts of aminoacids in dietary protein throughout the day forolder adults. Defining an optimum amount of di-etary protein that is appropriate to maintain theavailability of amino acids for biological needsis necessary, but has not been achieved in olderindividuals.



Figure 3. Representative clusters (C0, C3, and C6) from aself-organizing map showing the patterns of differentially ex-pressed transcripts resulting from the diet-by-age interaction.Each point within a cluster is equal to the mean transcript levelfor the younger (dashed line) or older (solid line) males at eachof three dietary protein intakes (indicated at the bottom of thegraph; LPro (lower protein, 0.50 g/kg body weight per day),MPro (medium protein, 0.75 g/kg body weight per day), andHPro (higher protein, 1.00 g/kg body weight per day)). Num-bers in the top center within each cluster are the number oftranscripts that had the specified expression pattern. Functionalcategorization for differentially expressed genes within a clusterare indicated on top of the cluster. Adapted from Thalacker-Mercer et al.15

Amino acids and insulin sensitivity in humansAside from the biological use of dietary amino acidsfor protein metabolism in skeletal muscle, recent re-search suggests a role for amino acids in insulin sen-sitivity. With the emergence of metabolomics, ele-vated concentrations of branched chain amino acids(BCAA) have been identified as possibly an earlypredictor for the future development of diabetes inadults,23 children and adolescents.24 These findingsare supported by earlier studies that demonstratedhigher levels of BCAA, primarily leucine, in theplasma of obese and insulin-resistant individuals.25

Leucine and other amino acids are also prog-nostic for improved insulin sensitivity followinglifestyle interventions and bariatric surgery.26 In ad-dition to leucine, Thalacker-Mercer et al.27 recentlyidentified the amino acid glycine as being tightlycorrelated with insulin action; leucine/isoleucineand glycine were the strongest predictors for in-sulin action in nonobese individuals, while glycinealone is the only predictor of insulin action inobese individuals.27 Intriguingly, they found thatthe relationship between leucine and insulin ac-tion was influenced by the body’s preference forfat utilization. Together with data from Newgard

et al.,28 there is evidence that insulin sensitivity,particularly that of the skeletal muscle, is relatedto BCAA under conditions of high fat feeding. It isunclear whether amino acids play a causal role inmetabolic dysfunction or are just a biomarker, butfuture studies are warranted.

There are many unanswered questions aboutthe biological need and role of dietary protein foroverall human health. Much research is still neededto address whether the RDA for dietary protein isadequate for older adults. Establishing an optimumprotein intake for older adults, to improve musclemaintenance while aging, may address some ofthe problems/concerns identified with the RDA.Additionally, changes in meal patterns for olderadults might improve protein and/or amino acidefficiency for stimulating skeletal muscle anabolism.While only briefly discussed, increasing physicalactivity and exercise might be the best stimulationfor improving the nutritional efficiency of dietaryprotein and and overall skeletal muscle health.Physical activity and exercise patterns could also un-derlie the relationships between BCAA and insulinsensitivity.

Challenges to the sustainability of proteinproduction by animal agriculture

Globally, natural resources for feedstuff provisionare becoming increasingly limited. The conversionof dietary proteins to tissue proteins in animals,which requires complex physiological and biochem-ical processes, occurs at suboptimal rates. Thisnecessitates the development of effective means toimprove the efficiency of livestock and poultry pro-duction. Specifically, microbial fermentation of pro-tein in the rumen of ruminants (e.g., cows, goats,buffalo, and sheep) produces ammonia and smallpeptides, with some of them being utilized for syn-thesis of amino acids and polypeptides in bacte-ria. Digestibility of dietary protein in post-weaningnon-ruminants (e.g., pigs and chickens) is at best75 to 92%, depending on ingredients. Irreversiblecatabolism of amino acids generates CO2, ammo-nia, H2S, methane, urea and uric acid, furtherresulting in suboptimal efficiency of animal pro-duction and potentially adverse effects on the en-vironment. Thus, there are sustainability challengesfor the production of high-quality protein by farmanimals.



Suboptimal efficiency of protein production byanimalsAn important concept emerging from the presen-tations is that efficiencies in the conversion of di-etary proteins into tissue or milk proteins in live-stock species and poultry remain suboptimal (e.g.,23.3% for pigs during a 25-week period of growthand 6.7% for grazing beef cattle during a 76-weekperiod of growth). Major reasons may be (a) thehistoric lack of consideration of so-called nutrition-ally nonessential amino acids (NEAA; e.g., arginine,glutamate, glutamine, glycine, and proline) in di-etary formulations; (b) high rates of amino acidcatabolism by bacteria in the small-intestinal lu-men; (c) high rates of amino acid catabolism byintestinal mucosa; (d) high rates of protein degra-dation in the intestinal mucosa; and (e) low ratesof protein synthesis in skeletal muscle.7 Promisingmeans to ameliorate these problems include dietarysupplementation with amino acids (e.g., glutamate,glutamine, glycine, and arginine) to inhibit intesti-nal amino acid catabolism, thereby enhancing theentry of dietary amino acids into the blood circu-lation; activating cell signaling pathways (e.g., themTOR pathway) through genetic and dietary meansto promote synthesis of amino acids and proteins inanimals; and formulation of low-protein diets byconsidering the needs for all amino acids, particu-larly those with regulatory functions (namely, func-tional amino acids), to optimize the proportion andamounts of dietary amino acids.29

Impacts of animal production on theenvironmentAs alluded to previously, animal production canhave potential impacts on the environment. Theseimpacts include (a) use of water, (b) contribution(14.5%) to human-caused greenhouse gas (GHG)emissions (carbon dioxide (CO2), nitrous oxide(N2O), and methane (CH4)) and thus global warm-ing, and (c) generation of NH3 and urea as sources ofenvironmental pollution, and (d) overgrazing caus-ing soil erosion.

These impacts were also highlighted by Jean L.Steiner, who explained that a major goal of herproject is to reduce the environmental footprint ofbeef-grazing systems by reducing the emissions ofpotent GHGs, such as nitrous oxide and methane.N2O is increased by the application of nitrogen fer-tilizer to crops on forage land. Steiner is building

Figure 4. Global distribution of grazing land in the year 2000.Adapted from Erb et al.29

a database to improve our knowledge of how tomanage agroecosystem fertilization and reduce N2Oemissions. Her team is analyzing fertilizer manage-ment practices to find ways to minimize N2O emis-sions through appropriate rate, timing, and type offertilization and collecting information about back-ground emissions from unfertilized prairie land. Inaddition, methane emissions from cattle depend onthe quality of forage (including the types of speciesconsumed) and the type of livestock (e.g., cow, calf,heifer, steer). The team is using grazing lands asopen laboratories, tagging cattle with GPS collarsto identify their grazing patterns and preferencesto develop emissions-reducing steps in the produc-tion cycle. Efforts are also underway to improve thequality of vegetation, increase soil carbon seques-tration, and understand how agronomic manage-ment strategies impact water quantity and quality,which is particularly important in regions prone todrought.

Rearing of ruminants on grasslands forprotein productionSteiner explained that improving the sustainabilityof forage-based animal productivity systems and re-ducing their environmental footprint can increaseresilience to vagaries of climate, market, and gov-ernment policy. An example is to build a robustcattle production system in grasslands to withstandclimate, resource, and market variability. The grass-lands constitute the largest global land use and arean important part of agricultural and ecological sys-tems across a wide range of potential productivityconditions on every continent (Fig. 4).30 Ruminant



livestock grazing is often the only viable form ofagricultural production on these lands.31 In mostregions of the world, lands suited to some levelof grazing (grasslands, woodlands, forestlands, andsparsely vegetated or barren lands) constitute themajority of the land use. In the world’s lower incomecountries, grassland and woodland that support ru-minant grazing are proportionally more importantthan other land uses, compared to middle- and high-income countries. Grazing lands provide a widerange of ecosystem services, including provision offood, livelihoods, biodiversity, habitat, carbon stor-age, and water filtration.32–34 The role of grasslandecosystems as net sinks or sources of GHGs is poorlyunderstood, limited by sparse data regarding man-agement impacts on the flux of nitrous oxide andmethane. In grazing lands, soil quality and integrityof the vegetative and faunal communities are intrin-sically intertwined and both are impacted by grazingsystems.33

In the southern Great Plains of the United States,beef cattle production is a dominant part of theagricultural sector. Beef cattle production is basedon mixed annual and perennial land uses, includingnative prairie, a variety of introduced pastures andhays, and grazing of winter wheat during the winter.Agriculture in this region is subject to a highly dy-namic climate with extremes of heat and cold as wellas drought and flooding.35 Because of the portionof land in this region that supports beef-grazing sys-tems, it has a large impact on carbon, nitrogen, andwater budgets of the system. Management practicesare critical to ensure efficient use of these resourcesto produce animal protein, but quantitative under-standing of environmental effects of beef grazingsystems is sparse.

Multidisciplinary efforts to reduce gaseousemissions from livestockBeef cattle enterprises include cow-calf produc-tion, weaned stocker grazing, and finishing opera-tions. Animal science research has focused predom-inantly on the finishing phases of beef production.However, addressing the system as a whole re-quires integrated, multidisciplinary research andextension involving soil and plant sciences, ecol-ogy, animal science, climatology, hydrology, sociol-ogy, economics, and other disciplines. Steiner de-scribed a multi-institutional, collaborative project“Resilience and Vulnerability of Beef Cattle Produc-

tion in the Southern Great Plains Under Chang-ing Climate, Land Use and Markets.” This “GrazingCAP” was established to better understand vulnera-bility and enhance resilience of beef-grazing systemsthrough diversified forages, improved management,strategic drought planning, and improved decisionsupport systems for evaluation of alternative op-tions and to safeguard and strengthen productionand ecosystem services while mitigating GHG emis-sions.

The research addresses how different manage-ment practices and systems affect the environmen-tal footprint of beef-grazing systems, particularlyhow rate, form, and timing of fertilization of wheatand perennial pastures affect soil nitrous oxideemissions; how forage and feed quality affect en-teric methane emissions for various livestock classes(cow, calf, stocker, heifer); and how agronomic man-agement of crops and pastures (tillage, rotation, fer-tilization, stocking density, duration, and timing)affect soil organic carbon, species diversity of pas-tures, water quality and water quantity.

Steiner shared with the audience that her collabo-rative team includes 34 coinvestigators and numer-ous students and postdoctoral research associateslocated at Oklahoma State University, Kansas StateUniversity, University of Oklahoma, Tarleton StateUniversity, and the Samuel Roberts Noble Founda-tion; and Agricultural Research Service researchersfrom El Reno, Oklahoma, and Bushland, Texas.Their research is structured around ongoing long-term research at the partner institutions to quan-tify seasonal and annual productivity and C, N,H2O, and energy budgets, along with new inten-sive field campaigns conducted to develop improvedunderstanding of interactive processes (Fig. 5). Re-search and extension efforts include on-farm re-search. A modeling team is developing a frameworkfor linking models to develop regional maps of theenvironmental footprint and life cycle analysis ofbeef-grazing systems (Fig. 6). Extension teams aredeveloping improved climate content for extensionprograms, decision support tools for beef cattle pro-ducers, and delivery of science-based information,including best management practices and technol-ogy for producers as well as for consumers.

Steiner’s project was developed to increaseresilience and sustained productivity of beefcattle systems, including mitigation of GHG emis-sions, through improved grazing management,



Figure 5. Grazing CAP research framework addressing multiple, interactive processes that interact at multiple scales to affectbeef-grazing impacts on the environmental footprints of C, N, H2O, and energy.

increased water use efficiency, diversified for-age sources, multiple marketing options, strategicdrought planning, and improved decision support.As the project progresses from its first year throughthe five-year plan, success will contribute to sustain-able rural economies under variable and changingclimate, market, and policy environments.

Approaches to solving sustainabilityproblems

Enhancing biodiversityThere is strong evidence linking biodiversity andnutritional quality.6 Fanzo explained that biodiver-sity in the ecosystem is an attractive way to sustainprotein production to improve nutritional qualityof food. Redirecting the global agricultural systemas the supplier of the world’s food to ensure betternutrition is crucial. Now more than ever, we needto better define new and sustainable approaches toimproving the quality and variety of food producedand consumed around the world to meet critical nu-trient gaps, such as protein, essential fatty acids andmicronutrients. One area that requires further un-derstanding is the role of biodiversity in improvingdietary diversity and quality. Biodiversity is poten-tially important to food systems because it provides

the basis of sustaining life. The diverse traits exhib-ited among crops, animals and other organisms usedfor food and agriculture, as well as the web of rela-tionships that bind these forms of life at ecosystem,species, and genetic levels all directly or indirectlyaffect the nutritional quality of foods. Agriculturalbiodiversity is the basis of the food and nutrientvalue chain. The sustainable conservation and useof biodiversity could be an important contributorto food security.

Varietal and species differences, which can be ex-ploited within more biodiverse environments, havedifferent protein content and quality. For example,animal source foods, mainly meat, milk and eggs,provide concentrated, high-quality sources of es-sential nutrients for optimal protein, energy andmicronutrient nutrition (especially iron, zinc, andvitamin B12). The diversity of breeds is closely re-lated to the diversity of production systems andcultures. Local breeds in regions are usually usedin grassland-based pastoral and small-scale mixedcrop–livestock systems with low to medium use ofexternal inputs. However, only about 40 of the al-most 50,000 known avian and mammalian specieshave been domesticated. On a global scale, cat-tle, sheep, chickens, goats and pigs are the major



Figure 6. A linked observation-modeling framework to assessvulnerability, risks, and resilience of beef grazing systems.

animals raised and consumed. Therefore, the ma-jority of products of animal origin are based onquite narrow species variability. There are also eth-ical considerations about the equitable distributionand access to these valuable sources of food acrosscountries. Other sources, such as insects, can makesignificant contributions to dietary protein quality.

A question remains of how to best promote theuse of biodiversity within food production systemsthat provide nutritionally rich protein sources, con-tribute to dietary diversity and quality and, poten-tially, promote better nutrition and health. Thereare also challenges on how to balance tradeoffs andavoid poverty traps while using and conserving bio-diversity. More research is needed on how biodiver-sity of animal, plant and forest species and varietiescontributes to dietary quality. There is a need formore guidance on what conservation and use ofbiodiversity would mean economically for all foodvalue chain actors. Last, we need more implementa-tion research to better understand how to measure,assess and evaluate the impact of biodiversity on di-ets, health and nutrition in the context of climatevariability and environmental degradation in low-and middle-income countries.

Aseptic methods for food processing andstorageJosip Simunovic proposed that improving tech-nologies for industrial muscle-food preservationis another approach to sustaining a protein sup-ply. One challenge faced by the industry that pro-cesses so-called muscle foods (i.e., hot dogs, salami,

and hams) is the limited shelf life and the poten-tial for spoilage during distribution and storage ofraw frozen and thermally processed “fully cooked”meats. Canned and sterilized muscle foods are shelfstable at ambient temperatures but are rapidly losingmarket share because of their low sensory quality:they “smell and taste bad.”

The sterilization process for canned solid food,namely, the time/temperature regimes required tokill pathogens, such as Salmonella and Escherichiacoli, in the whole product results in over-processingof everything surrounding the so-called cold spotat the center of the canned product. Overcookingresults in loss of sensory quality, destroys valuablenutrients, wastes energy, and limits the maximumpackage size (i.e., products in large cans are mostsusceptible to damage). To mitigate these problems,Simunovic has developed a new aseptic processingtechnique to more rapidly and uniformly heat meatproducts than conventional approaches. In contrastto canning in which products are sterilized withinthe package, his method sterilizes food products un-der continuous flow (as a continuously flowing liq-uid substance as opposed to a solid lump) and thencombines rapidly cooled products with separatelysterilized packaging under aseptic conditions. Thethermal technology used for food sterilization relieson a focused microwave energy that creates uniformheat distribution. This technology has been refinedin the last decade and can now be used on large, in-dustrial volumes and nonhomogeneous products,yielding different textures and consistent results.

Development and implementation ofsustainable agricultural policiesChanges in agricultural technologies and govern-ment policies are also needed to sustain productionof high-quality protein. On the basis of his observa-tions in rural India, Prabhu Pingali argued that anopportunity exists for an agricultural renaissance,based on government investment in agricultural in-frastructure, innovations in genomics and bioforti-fication, ease of information dissemination throughcellular technologies, and increased enrollment insafety-net programs to improve the nutrition andhealth of women of childbearing age. He stated thatthe past fifty years has been a period of extraordinarygrowth in food crop productivity, despite increasingland scarcity and rising land values.36 In India, pro-ductivity gains and food supply expansion through



the Green Revolution have provided tremendousopportunities for tackling nutrition and economicdevelopment challenges.37,38 Despite these promis-ing developments, India has remained an epicenterfor childhood stunting and malnutrition.39 Approx-imately 40% of the country’s children are stunted.40

In addition to reduced labor productivity and re-duced physical development, stunting (the resultof chronic malnutrition), causes lifelong reductionsin cognitive potential and ability. Identification ofpolicies and programs that can ensure that all house-holds are able to access and afford sufficient dietarydiversity, including access to iron and protein-richfoods, like milk, meat, and legumes, remains a chal-lenge.

The Tata-Cornell Agriculture and Nutrition Ini-tiative (TCi) is a long-term research initiative fo-cused on solving problems of poverty, malnutrition,and rural development in India, with a particularemphasis on reducing childhood stunting and im-proving the diets of women in their childbearingyears. Along with core TCi research and adminis-trative staff, the program comprises student scholars(Cornell graduate students), Cornell faculty and ex-ternal faculty fellows, and visiting researchers fromuniversities in India and around the globe. Together,the TCi team works alongside partner institutionsin India and worldwide to address the agriculture–nutrition nexus.

TCi research focuses on four pathways that linkagriculture to nutrition. The first area considersfood affordability, which includes household in-come and the impact of farm-level profitability andproductivity for expanding food budgets and culti-vating food for home consumption. TCi research inthis area focuses on agriculture-led growth strate-gies, including a current research effort to under-stand how changing cropping patterns are affectingwomen’s empowerment, women’s iron-deficiencyprevalences, and various anthropometric indicatorsof childhood growth. The TCi’s second area of re-search looks at the availability of micronutrient-rich foods, as well as the effectiveness of food andmicronutrient intervention programs. TCi scholarsand researchers in this area are currently engagedin work that is evaluating new methods of deliv-ering and fortifying the mid-day meals for Indianschoolchildren and testing for impacts in child nu-tritional status and cognitive ability.

The third and fourth areas of TCi research godeeper than evaluating a household’s ability to ac-

cess food. Even if a household is able to access food,the distribution of food and micronutrients withinthe household may not be equitable. TCi researchin this area highlights how behavior change canpositively influence the distribution of food so thatwomen, girls, and young children not only get thequantity of food they need, but also the diversity offood they require. TCi research underway in Orissais analyzing what types of iron-rich foods are tra-ditionally fed to infants and how campaigns aimingto bolster consumption of these foods can be deliv-ered in contextually appropriate ways. Similarly, afourth TCi research area evaluates the linkages be-tween nutrition and the rural health environment,including household and individual access to cleanwater, sanitation and toilets. TCi is partnering withAguaClara, a Cornell University–based engineeringfirm that has designed and developed clean waterpumps and filtration systems specifically designedfor the Indian context. TCi research is evaluatinghow the time saved by women (who would other-wise spend hours fetching water) might translate togreater nutritional impacts, including infant breast-feeding and early childhood care. A fifth area ofresearch has focused TCi researchers evaluating themetrics currently used and needed for linking agri-culture to nutritional outcomes.

Collectively, increasing protein and micronutri-ent consumption requires research and develop-ments of the policies and practices that can ensurethat these foods are affordable and available—andconsumed in a healthy environment—at both thehousehold and individual levels. The TCi program isan effort to focus researchers from multiple discipleson addressing the ever-complex and changing issuesaround maternal and child malnutrition, by honingin on the agricultural factors that determine relativefood affordability, availability of high-quality pro-tein and micronutrients, as well as intra-householddistribution of food and resources.

Optimizing dietary formulation for animalsLivestock and poultry convert low-quality foragesor ingredients into high-quality proteins (Fig. 2).Nutritional means can be developed to enhance theefficiency of animal growth and development. Forexample, Wu and coworkers have formulated anoptimal protein diet that contains adequate propor-tions and amounts of all amino acids to increasemilk production by 17%–26% in lactating sows.7

Thus, it is imperative to modify the long-standing



ideal protein concept, which ignored NEAA in thediet, to now include these amino acids in dietaryformulation, thereby improving the efficiency oflivestock production. In addition, dietary argininesupplementation can increase litter size by two ingestating sows. Besides nutritional approaches, an-imal breeding should also play an important rolein increasing protein deposition in skeletal mus-cle. Improvements in farm animal productivity willnot only reduce the contamination of soils, ground-water, and air by excessive excretion of animalwastes, but will also help sustain animal agricul-ture to produce high-quality proteins for the grow-ing population in the face of declining resourcesworldwide.

Improving plant breeding to enhance cropyield and protein qualityPlant physiologist Widders told the audience thatthe productivity of legume crops in many areas inthe developing world is pitifully low. This indicates aneed to close the yield gap—the difference betweenthe genetic yield potential of the crop and the actualyield on farms. The Widders team studies many as-pects of crop yield, from molecular genetics to cropmanagement strategies that aim to improve nutri-tional quality and marketing approaches. Throughthe United States Agency for International Develop-ment’s Feed the Future program, Widders is work-ing to reduce undernutrition in Guatemala, where80% of children in rural areas are stunted and amajority of the population live in poverty. Collab-orating with the country’s Ministries of Agricultureand Health, Widders aims to increase bean produc-tion on farms and consumption of beans by chil-dren and women of childbearing age. Interventionsaim to improve access to quality seeds of bean va-rieties with enhanced yield potential; to improveintegrated crop management practices, such as croprotation; to implement simple steps, such as dissem-inating sacks for long-term, non-wasteful storage;to promote seed exchanges; and to improve localunderstanding and appreciation of beans as a nutri-tious, ancestral crop. Another project is looking atthe impact on child health of regular consumptionof pulses by examining gut microbial flora, intestinalnutrient absorption, and immune function. It alsoexamines whether the benefits of pulse consumptionextend to better child growth and reduced incidenceof diarrheal disease.

Innovations in the protein supply chain

The end of the conference featured discussions ofnew methods for producing protein, which are in-tended to create sustainable alternatives to animalprotein in response to a scarcity of natural resourcesrequired for its production.

Reclaiming healthy, sustainable products fromsoy protein waste streamsCharles Schasteen explained that the production ofsoybeans is an energy-efficient process. He also indi-cated that soy protein is an accessible form of plant-based protein with relatively high quality and willplay an important role in regions with huge pro-jected population growth and limited infrastruc-ture to produce animal protein. When soybeans areprocessed to create protein ingredients, the startingmaterial used by the food industry to make com-mercial products is a form known as defatted soyflake. However, the process of producing isolatedsoy protein is wasteful and generates products thatcontain only 46% of the protein in the starting soyflake. Schasteen’s team has developed a new processto mitigate this waste. The feed material, raw soywhey, is formulated to contain 2% solids and 98%water. The technology concentrates and separatesthis starting material into individual components(e.g., soy whey protein, soy whey sugars, soy wheyminerals, and water), each of which is usable at theend of the process. Soy whey protein has severaltraits (e.g., unprecedented solubility across a rangeof pH, low viscosity, and high emulsification capac-ity) that make it a viable replacement for dairy pro-teins. Furthermore, soy whey protein forms a morestable foam than egg white and is a healthier al-ternative to chemical-based emulsifiers. These newprotein products for use as food ingredients and inbeauty and personal care products are targeted forprototype availability later in 2014.

Launching companies for innovation acrossthe nutrient supply chainNew technologies, combined with genome, pro-teome, and microbiome research, are catalyzingstartup companies focused on global problems innutrition and health. In this regard, Geoffrey vonMaltzahn presented innovative ideas and technolo-gies that have driven the launch of companies fo-cused on nutrition and health. In his view, agri-culture practiced in its current form is a wasteful



endeavor, using over 40% and 75%, respectively, ofarable land and fresh water while producing up to30% of GHG emissions, degrading land, depletingground water, and leading to habitat destructionand loss of biodiversity.

The startup company Essentient aims to stream-line food production by eliminating the need forarable land and wasteful intermediary steps in cul-tivation, harvesting, storage, and transportation,turning instead to single-celled photosynthetic or-ganisms that are engineered to produce and secretenutrients (including protein and amino acids) cur-rently derived from agriculture at supra-agriculturalefficiencies. Notably, early-stage nutrient factories,whose yield has far outstripped that of traditionalagriculture, are being pilot tested in nonarable re-gions. Another company, Pronutria, has built a pro-prietary library of more than a billion protein poly-mers (amino acid chains) found in the typical West-ern diet. By comparing clinically proven amino acidcombinations to the library, the company has de-signed proteins with desired characteristics to treatdisease. These proteins can be delivered orally asprodrugs, which are digested in the gastrointesti-nal tract to release a specific combination of aminoacids with unique functions. Some protein candi-dates are in clinical trials to prevent or amelioratethe loss of skeletal muscle in humans. Other candi-dates are scheduled to begin trials in 2014 for treat-ing metabolic disease. Von Maltzahn also describedefforts to pioneer a new type of medical treatmentinvolving the human microbiome at a startup calledSeres Health. The company designs Ecobiotics totherapeutically adjust microbial ecology for medi-cal benefits. A new startup, Symbiota, is exploitingnew knowledge of plant microbiota to improve cropyield, pathogen resistance, and stress resilience.

Laboratory-made animal protein to replacelivestock meatAn alternative to current non-sustainable proteinproduction practices is to produce beef meat in thelaboratory from stem cells via regenerative tech-niques. Conventional beef production in animalagriculture at a low efficiency is unlikely to besustainable. Beef cattle have a poor bioconversionrate—about 15%—from feed or grass input to edi-ble protein output and may be a huge environmentalburden. Nonetheless, meat production falls short ofdemand in many regions of the world. Mark Post

(a pioneer in tissue engineering using the stem celltechnology) and Gabor Forgacs made the case forlaboratory-derived meat products as an alternativeto livestock meat.

At the beginning of his talk, Post introduced tissueengineering for food as the next challenge in large-scale cell production. He stated that building theworld’s first hamburger from bovine skeletal mus-cle stem cells required 3 billion cells. The three mainreasons why this endeavor was undertaken are in-sufficient capacity of traditional livestock meat pro-duction to supply the projected doubling of demandin the coming decades, the need to mitigate climateeffects from livestock as a result of GHG emissions,and improving animal welfare.41 In order to succeed,a tissue engineering alternative to livestock beef pro-duction should be resource efficient and sustain-able, and the result should sufficiently mimic beef.The application of tissue engineering for food sharestechnological challenges with medical applicationsbut is different in scale, physiological requirementsand behavioral/ethical implications.42,43

After harvesting a small piece of skeletal mus-cle from a cow through biopsy and simultaneouslyextracting skeletal muscle stem cells, also knownas satellite cells (SATs), and adipose tissue–derivedstem cells (ADSCs), cells are expanded separatelythrough standard cell-culturing techniques. For theproof of concept hamburger, Post and coworkersused 10-layer cell factories; but in the near futurethey will move to micro-carrier or cell aggregate–based production. To sustainably produce the largenumber of cells needed for production of consump-tion meat, a serum-free medium is an absolute re-quirement. From hundreds of serum-free cultureconditions, Post’s group has identified some that arepromising for SATs and ADSCs. Further optimiza-tion of medium conditions for SATs is necessary, asthese cells require unusually high serum additionand therefore specialized serum replacement. Theorigin (e.g., algae lysates) and production of non-serum components of the medium also require at-tention to the development of a resource-efficientcell culture. Recycling of media will be an integralpart of the process.

Differentiation of SATs is performed by a com-bination of serum starvation and the supply of aprovisional matrix that allows self-organization ofthe cells into muscle fibers.44 For the fibers to fullyand stably mature, they need to develop tension



between anchor points. By laying down the cell-matrix gel in a donut shape encircling a centrallypositioned column, the cells anchor to themselvesin an elastic fashion that also allows scaling andeasy harvesting of tissues. With this technique, thePost team is able to reach more than 95% success inmuscle fiber formation. Part of the production pro-cess is conducted under low oxygen conditions thatenhance muscle differentiation and increase myo-globin expression 5-fold. The latter contributes tocolor, taste, and nutritional value of cultured beef.

Cultured beef will only be a solution for prob-lems with livestock meat production if the publicis willing to accept and consume it. The associ-ation with other artificial or modified foods hasbeen translated by investigators and media as the“yuck factor.”42,43 However, a survey among a cross-section of the Dutch population indicates that 63%of the 7700 respondents are in favor of the cul-tured beef development.45 Of the respondents whohad heard about cultured beef and know what it is,approximately 71% are willing, 14% are not sure,and 16% are not willing to try cultured beef. Sim-ilarly, a web-based poll issued by the United King-dom newspaper, The Guardian, immediately follow-ing the public presentation of the proof-of-conceptstem cell hamburger, indicated that 68% of the par-ticipants had a positive attitude towards culturedbeef. Considering the seriousness of the problemsfaced by livestock meat production and the promis-ing developments in culturing meat, forward effortsto bring cultured beef into larger scale practice arewarranted.

Like Post, Gabor Forgacs is keen to overcome thechallenges of pursuing sustainable sources of pro-tein for human consumption. To produce meat thatreflects the geometry and composition of an ani-mal tissue, Forgacs is using a bioprinting technol-ogy, which lays down bio-ink units—a preparationof multicellular aggregates—with support materialsalong an architectural template. Structural forma-tion, or “magic,” as he called it, occurs post-printing,in a process similar to embryonic development ofanimals. When the bioprinted material has reachedthe desired thickness and shape, cells assemble, fuse,and undergo morphogenetic changes to produce atissue that largely resembles animal meat. Severalchallenges remain to improve this tissue engineer-ing technology, most notably scaling up the process,reducing cost, and achieving consumer acceptance.

Nonetheless, both Post and Forgacs believed thatbecause of dwindling natural resources and globalpopulation growth, alternative protein sources, suchas those derived from their laboratories, might notbe a choice, but rather a necessity in the future.

Conclusion and perspectives

Human health depends on consumption of di-etary protein with adequate amounts and properratios of all amino acids. High nutritional quality ofanimal protein and the sole sources of physiolog-ically important amino acids (e.g., taurine) anddipeptides (e.g., carnosine) from animal productsnecessitate the continuation and extension of ani-mal agriculture. Production of animal-source foodsis more expensive and generates more GHG emis-sions than production of plant-based foods. There-fore, there is increasing pressure to reduce con-sumption of animal-source foods in global popula-tions. However, as noted previously, animal-sourcefoods are excellent sources of high-quality proteinand micronutrients that are often deficient in thediets (primarily based on plant-source foods) ofpopulations in developing countries. Low intakes ofanimal-source foods increase risks for protein andmicronutrient deficiencies, especially in children. Atpresent, there is concern that animal production ata low efficiency is environmentally unsustainable.46

So, what strategies can we use to enhance the nu-tritional quality of plant-based foods? Several ap-proaches have promise:

1. Select plants that have enhanced concen-trations of limiting essential amino acids.Considerable progress has been achieved inincreasing the levels of lysine in maize. Forexample, quality protein maize (QPM) hasnearly double the concentration of lysine asconventional maize.47 So far, however, QPMseeds are not available to farmers, in part, dueto poorer yields and undesirable changes inthe phenotype of the seeds.

2. Biofortify staple food crops with vitamins andminerals. Biofortification is the application ofplant breeding and agronomic practices to in-crease the concentrations of essential nutrientsin staple food crops.46 HarvestPlus is leadinga global effort to develop and distribute bio-fortified seeds to farmers in resource-poor ar-eas around the world.18 When farmers plant



these biofortified seeds and later harvest thecrops for consumption by their families andcommunity members, they will be helpingto increase the intakes of essential nutrientsin these communities. To date, HarvestPlushas released beans and millet biofortified withiron; cassava, maize, and sweet potato biofor-tified with vitamin A; and wheat biofortifiedwith zinc.

3. Commercially fortify foods. Commercial foodfortification is the addition of vitamins andminerals to foods during processing. It datesto the 1920s when iodine was added to saltin the United States and Europe to preventiodine deficiency. Fortification of milk withvitamin D began in the 1930s, and iron, thi-amin, riboflavin, and niacin were added to ce-real flours in the 1940s. Fortification has been asuccessful strategy for reducing micronutrientmalnutrition in developed countries, but onlyrecently has it been implemented in many de-veloping countries. Likewise, addition of oneor more limiting or functional amino acids(e.g., lysine, arginine, glycine, and taurine) tofood can improve human health and growth.

4. Balance the proportions of all amino acids inhuman diets by consumption of animal prod-ucts (e.g., meats, egg, and milk) containinghigh-quality protein.48–50

Recommendations:

1. Make enhancing nutritional quality of foodcrops an explicit goal for plant breeding pro-grams across the globe.47 The focus shouldbe on those nutrients that are limiting inthe diets of people in resource-poor areas.These nutrients include nutritionally essen-tial amino acids (especially lysine and the sul-fur amino acids), iron, zinc, and beta-carotene(pro-vitamin A).

2. Conserve and use sustainably agro-biodiversity to ensure sufficient productionof food proteins at low costs, particularly forsmallholder farmers.

3. Promote and support agricultural researchthat will help to develop food crops with en-hanced nutritional quality. Approaches shouldinclude both conventional plant breeding andgenetic engineering.

4. Expand commercial fortification and homefortification of foods to regions where proteinand micronutrient malnutrition is prevalent.

5. Encourage dietary diversity and consumptionof animal-source foods in regions where pro-tein and micronutrient malnutrition is preva-lent until nutritionally enhanced plant-basedfoods are more widely available.

6. Enhance the efficiency of livestock and poultryproduction through mechanism-based means(e.g., optimizing the proportion and amountsof both nutritionally essential and “nonessen-tial” amino acids in diets) to stimulate proteinsynthesis and inhibit protein degradation intissues.

7. Promote sustainable practices for ruminantgrazing on grasslands and rangelands. Exten-sive grazing is often the only viable agriculturalsystem for regions that have climate and soillimitations that preclude cropping. Properlymanaged grazing lands can sustain biodiver-sity and provide nutritious foods to the grow-ing global population, including the world’spoorest population.

8. Continue to explore radical innovations inthe production of animal proteins (e.g., insectprotein and cultured meat).

Acknowledgements

This article was based on presentations by the au-thors, as well as by Drs. Barbara Burlingame, GaborForgacs, Geoffrey von Maltzahn, Charles Schasteen,Josip Simunovic, and Irvin Widders at the Decem-ber 12, 2013 conference “Frontiers in AgriculturalSustainability: Studying the Protein Supply Chainto Improve Dietary Quality” held at the New YorkAcademy of Sciences. This conference was orga-nized by Drs. Nelson G. Almeida (Kellogg Com-pany), Mandana Arabi (the Sackler Institute forNutrition Science), Amy Beaudreault (the SacklerInstitute for Nutrition Science), Norberto Chaclin(PepsiCo), Bruce Cogill (Bioversity International),Girish Ganjyal (Washington State University), andMichael Morrissey (Oregon State University). P.L.Pingali thanks K.D. Ricketts for help in preparingthe summary of his talk. Constructive comments ofDrs. Douglas Braaten, H. Russell Cross, and ShaleneMcNeill are gratefully appreciated.



Conflicts of interest

The authors declare no conflicts of interest.

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