Protein transition: focus on protein quality in sustainable alternative sources

Figures & data

Figure 1. Representatives DIAAS values (panel a), PDCAAS values (panel b) and digestibility values (panel c) for the protein sources discussed in the text. From left to right: meat, soy, pea, other legumes, insects, microalgae, fungi, plant-based meat analogues. All the data are taken from Tables 1–3. DIAAS values reported for the age group older children and adults; PDCAAS values reported for children >3 years; digestibility values only include true or standardized ileal digestibility.

Table 1. Digestible indispensable amino acid score (DIAAS) values for animal proteins.

Type	Processing method	DIAAS (%)	Scoring pattern (the age group DIAAS refers to)	First limiting amino acid	Protein digestibility %	Animal model	Reference
Dairy proteins
Casein		145	>3 years		94 (real ileal digestibility of N)^a	Human volunteers with naso-ileal intubation	(Guillin et al. 2022)
Whey protein isolate		67	0–6 months	Aromatic AA	101 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Mathai, Liu, and Stein 2017)
		125	>3 years
Whey protein concentrate		71	0–6 months	Aromatic AA	101 (standardized ileal digestibility of crude proteins)
		133	>3 years
Milk protein concentrate		85	0–6 months	Tryptophan	101 (standardized ileal digestibility of crude proteins)
		141	>3 years
Meat proteins
Beef	Ribeye roasted at an internal temperature of 56 °C	104	0–6 months		105 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Bailey et al. 2020)
		111	>3 years
	Ribeye roasted at an internal temperature of 64 °C	122	0–6 months		103 (standardized ileal digestibility of crude proteins)
		130	>3 years
	Ribeye roasted at an internal temperature of 72 °C	99	0–6 months	Leucine	105 (standardized ileal digestibility of crude proteins)
		107	>3 years
Beef	93% lean beef burger cooked at 157 °C and 20% humidity to an internal temperature of 71 °C	111	0.5-3 years		100 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing gilts	(Fanelli et al. 2022)
		119	>3 years				(Fanelli et al. 2022)
Beef	Beef topside steak, taken from the semitendinosus muscle of the hind leg, raw	97	>3 years	Valine	97 (true ileal digestibility of amino acids)	Pigs. Samples collected after euthanasia	(Hodgkinson et al. 2018)
	Beef topside steak, taken from the semitendinosus muscle of the hind leg, boiled at 80 °C	99			98 (true ileal digestibility of amino acids)
	Beef topside steak, taken from the semitendinosus muscle of the hind leg, grilled at 225 °C	80			96 (true ileal digestibility of amino acids)
	Beef topside steak, taken from the semitendinosus muscle of the hind leg, roasted in an oven at 160 °C	91			97 (true ileal digestibility of amino acids)
Pork	80% lean pork burger cooked at 157 °C and 20% humidity to an internal temperature of 71 °C	111	0.5-3 years		104 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing gilts	(Fanelli et al. 2022)
	Salami, cooked, cured and fermented	107	0–6 months		103 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Bailey et al. 2020)
		120	>3 years
		119	>3 years			Ileal-cannulated growing gilts	(Fanelli et al. 2022)
Eggs	Whole eggs	122	>3 years		104 (standardized ileal digestibility of crude proteins)	Ileal-cannulated pigs	(Heo et al. 2012)

Data of DIAAS and protein digestibility have been reported as integers, without decimal figures.

^a Determined with isotopically labeled material; equivalent to standard ileal digestibility.

Table 2. Digestible indispensable amino acid score (DIAAS), protein digestibility corrected amino acid score (PDCAAS) for grain legumes.

Type	Processing method	PDCAAS	Scoring pattern (the age group PDCAAS refers to)	DIAAS (%)	Scoring pattern (the age group DIAAS refers to)	First limiting amino acid (when DIAAS is <100)	Protein digestibility %	Animal model	Reference
Grain Legumes
Chickpeas (Cicer arietinum)	Soaking and cooking	–	–	67	0.5–3 years	Lysine	87 (true ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Han et al. 2020)
	Soaking and cooking	–	–	76	>3 years	Lysine		Ileal-cannulated growing pigs	(Han et al. 2020)
	Soaking and cooking	52	0.5–3 years	67	0.5–3 years	Tryptophan	85 (true protein digestibility of nitrogen)	Male weanling laboratory rats	(Nosworthy et al. 2017c)
Faba bean (Vicia faba)	–	–	–	55^a	0.5–3 years	Sulfur amino acids	NR	Ileal-cannulated growing pigs	(Herreman et al. 2020)
	Concentrate (58.15% crude protein)	43	–	–	–	Tryptophan	NA	–	(Nosworthy, Tulbek, and House 2017d)
	Isolate (85.77% crude protein)	56	–	–	–	Tryptophan	NA	–	(Nosworthy, Tulbek, and House 2017d)
	Soaking and cooking	–	–	53	0.5–3 years	Lysine	86 (true ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Han et al. 2020)
	Soaking and cooking	–	–	60	>3 years	Leucine		Ileal-cannulated growing pigs	(Han et al. 2020)
Lentil, whole green (Lens culinaris)	Soaking and cooking	63	0.5–3 years	58	0.5–3 years	Sulfur amino acids	88 (true protein digestibility of nitrogen)	Male weanling laboratory rats	(Nosworthy et al. 2017c)
Lentil, split red (Lens culinaris)	Soaking and cooking	54	0.5–3 years	50	0.5–3 years	Sulfur amino acids	91 (true protein digestibility of nitrogen)	Male weanling laboratory rats	(Nosworthy et al. 2017c)
Lentil (Lens culinaris)	Concentrate (46.28% crude protein)	68	–	–	–	Sulfur amino acids		–	(Nosworthy, Tulbek, and House 2017d)
	Isolate (78.29% crude protein)	50	–	–	–	Tryptophan		–	(Nosworthy, Tulbek, and House 2017d)
Lupin (Lupinus albus)	–	–	–	68^b	0.5–3 years	Sulfur amino acids		Ileal-cannulated growing pig	(Herreman et al. 2020)
	Flour	–	–	67	0–6 months	Valine	86 (standardized ileal digestibility of the limiting amino acid)	Ileal-cannulated growing pig	(Burgos-Díaz et al. 2019)
	Flour	–	–	71	0.5–3 years	Valine		Ileal-cannulated growing pigs	(Burgos-Díaz et al. 2019)
	Flour	–	–	72	>3 years	Valine		Ileal-cannulated growing pigs	(Burgos-Díaz et al. 2019)
	Concentrate	–	–	65	0–6 months	Valine	86 (standardized ileal digestibility of the limiting amino acid)	Ileal-cannulated growing pigs	(Burgos-Díaz et al. 2019)
	Concentrate	–	–	68	0.5–3 years	Valine		Ileal-cannulated growing pigs	(Burgos-Díaz et al. 2019)
	Concentrate	–	–	70	>3 years	Valine		Ileal-cannulated growing pigs	(Burgos-Díaz et al. 2019)
	Isolate	–	–	67	0–6 months	Valine	86 (standardized ileal digestibility of the limiting amino acid)	Ileal-cannulated growing pigs	(Burgos-Díaz et al. 2019)
	Isolate	–	–	71	0.5–3 years	Valine		Ileal-cannulated growing pigs	(Burgos-Díaz et al. 2019)
	Isolate	–	–	72	>3 years	Valine		Ileal-cannulated growing pigs	(Burgos-Díaz et al. 2019)
Pea (Pisum sativum)	Isolate, heat treated			100	>3 years	–	94 (real ileal digestibility of N)^c	Human volunteers with naso-ileal intubation	(Guillin et al. 2022)
	Soaking and cooking	–	–	57	0.5–3 years	Lysine	91 (true ileal digestibility of crude proteins)	ileal-cannulated growing pigs	(Han et al. 2020)
	Soaking and cooking	–	–	68	>3 years	Lysine		ileal-cannulated growing pig	(Han et al. 2020)
	Concentrate			73	>3 years	Sulfur amino acids	95 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Mathai, Liu, and Stein 2017)
	Concentrate (49.98% crude protein)	54	–	–	–	Tryptophan	NA	–	(Nosworthy, Tulbek, and House 2017d)
	Isolate (82.6% crude protein)	53	–	–	–	Tryptophan	NA	–	Nosworthy, Tulbek, and House (2017d)
	Boiling	60	0.5–3 years	58	0.5–3 years	Sulfur amino acids	92 (true ileal digestibility)	Male Sprague-Dawley rats	(Rutherfurd et al. 2015)
	Concentrate	89	0.5–3 years	82	0.5–3 years	Sulfur amino acids	98 (true ileal digestibility)	Male Sprague-Dawley rats	(Rutherfurd et al. 2015)
	Soaking and boiling	62	0.5–3 years	59	0.5–3 years	Sulfur amino acids		Male Sprague-Dawley rats	(Rutherfurd et al. 2015)
Pea, split yellow (Pisum sativum)	Soaking and cooking	64	0.5–3 years	73	0.5–3 years	Tryptophan (PDCAAS) Sulfur amino acids (DIAAS)	88 (true protein digestibility of nitrogen)	Male weanling laboratory rats	(Nosworthy et al. 2017c)
Pea, split green (Pisum sativum)	Soaking and cooking	50	0.5–3 years	46	0.5–3 years	Sulfur amino acids	85 (true protein digestibility of nitrogen)	Male weanling laboratory rats	(Nosworthy et al. 2017c)
Soybean (Glycine max)	Boiling	99 (97–101) ^d (n = 4)	2–5 years	–	0.5–3 years	Lysine (PDCAAS)	NR	Growing/weanling pig (DIAAS) Adult/weanling rat (PDCAAS)	(van den Berg et al. 2022)
	Protein concentrate	103 (101–106)^d^e (n = 2)	2–5 years	88 (75–110) ^d (n = 9)	0.5–3 years	Tryptophan (PDCAAS) Sulfur amino acids (DIAAS)	NR	Growing/weanling pig (DIAAS) Adult/weanling rat (PDCAAS)	(van den Berg et al. 2022)
	Isolate			98	>3 years	Sulfur amino acids	94 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Mathai, Liu, and Stein 2017)
	Isolate	94–97	0.5–3 years	90–91	0.5–3 years	Sulfur amino acids	96–97 (true ileal digestibility)	Male Sprague-Dawley rats	(Rutherfurd et al. 2015)
	Isolate	96 (80–102) ^d (n = 14)	2–5 years	85 (69–90) ^d (n = 5)	0.5–3 years	Sulfur amino acids (PDCAAS)	NR	Growing/weanling pig (DIAAS) Adult/weanling rat (PDCAAS)	(van den Berg et al. 2022)
	Isolate, alkaline-heat-treated	58 (35–101) ^d (n = 4)	2–5 years	–	–	–	NR	Adult/weanling rat (PDCAAS)	(van den Berg et al. 2022)
	Dry heating (89 °C)	59 (54–64) ^d (n = 2)	2–5 years	–	–	–	NR	Adult/weanling rat (PDCAAS)	(van den Berg et al. 2022)
Soybean, meal (Glycine max)	–	80 (74–85) ^d (n = 6)	2–5 years	89 (57–104) ^d (n = 41)	0.5–3 years	Sulfur amino acids (DIAAS)	NR	Growing/weanling pig (DIAAS) Adult/weanling rat (PDCAAS)	(van den Berg et al. 2022)
Soybean, flour (Glycine max)				105	>3 years	–	92 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Mathai, Liu, and Stein 2017)
	–	98	2–5 years	89	0.5–3 years	Sulfur amino acids (PDCAAS) Lysine (DIAAS)	NR	Growing/weanling pig (DIAAS) Adult/weanling rat (PDCAAS)	(van den Berg et al. 2022)
Black beans (Phaseolus vulgaris)	Soaking and cooking	53	0.5–3 years	49	0.5–3 years	Sulfur amino acids	70 (true protein digestibility of nitrogen)	Male weanling laboratory rats	(Nosworthy et al. 2017c)
Pinto beans (Phaseolus vulgaris)	Soaking and cooking	59	0.5–3 years	60	0.5–3 years	Tryptophan (PDCAAS) Sulfur amino acids (DIAAS)	76 (true protein digestibility of nitrogen)	Male weanling laboratory rats	(Nosworthy et al. 2017c)
Kidney bean, red (Phaseolus vulgaris)	Soaking and cooking	55	0.5–3 years	51	0.5–3 years	Sulfur amino acids	79 (true protein digestibility of nitrogen)	Male weanling laboratory rats	(Nosworthy et al. 2017c)
Kidney bean (Phaseolus vulgaris)	Soaking and cooking	–	–	77	0.5–3 years	Lysine	76 (true ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Han et al. 2020)
	Soaking and cooking	–	–	88	>3 years	Lysine		Ileal-cannulated growing pigs	(Han et al. 2020)
Navy beans (Phaseolus vulgaris)	Soaking and cooking	67	0.5–3 years	65	0.5–3 years	Tryptophan (PDCAAS) Sulfur amino acids (DIAAS)	80 (true protein digestibility of nitrogen)	Male weanling laboratory rats	(Nosworthy et al. 2017c)
Mung bean (Vigna radiata)	Soaking and cooking	–	–	68	0.5–3 years	Lysine	82 (true ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Han et al. 2020)
	Soaking and cooking	–	–	86	>3 years	Leucine		Ileal-cannulated growing pigs	(Han et al. 2020)
Adzuki bean (Vigna angularis)	Soaking and cooking	–	–	59	0.5–3 years	Leucine	80 (true ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Han et al. 2020)
	Soaking and cooking	–	–	64	>3 years	Leucine		Ileal-cannulated growing pigs	(Han et al. 2020)
Bambara groundnut, flour (Vigna subterranea (L.) Verdc.)	–	33	–	–	–	Sulfur amino acids	NA	–	(Mune et al. 2011)
	Concentrate	25	–	–	–	Sulfur amino acids	NA	–	(Mune et al. 2011)
Pigeon pea (Cajanus cajan)	Soaking and pressure-cooking	–	–	37	<0.5 years	Tryptophan	88 (standard ileal digestibility of amino acids)	ileal-cannulated gilts	(Mathai 2018)
Pigeon pea (Cajanus cajan)	Soaking and pressure-cooking	–	–	48	0.5–3 years	Sulfur amino acids		ileal-cannulated gilts	(Mathai 2018)
Pigeon pea (Cajanus cajan)	Soaking and pressure-cooking	–	–	57	>3 years	Sulfur amino acids		ileal-cannulated gilts	(Mathai 2018)
Cowpea (Vigna ungulata	Whole bean flour, autoclaved for 30’	38	Children (2–5 years)				87 (true fecal digestibility)	Golden Syrian Hamsters	(Frota et al. 2017)
Cowpea (Vigna ungulata	Protein isolate	58	Children (2–5 years)			Sulfur amino acids	97 (true fecal digestibility)	Golden Syrian Hamsters	(Frota et al. 2017)

Data of DIAAS and protein digestibility have been reported as integers, without decimal figures^a.

^a Mean value of 3 studies.

^b Mean value of 4 studies.

^c Determined with isotopically labeled material; equivalent to standard ileal digestibility.

^d Data expressed as mean (min-max) of n studies analyzed.

^e PDCAAS value was not truncated at 1 in the original paper.

NR = not reported; NA = not accessible.

Table 3. Digestible indispensable amino acid score (DIAAS), protein digestibility corrected amino acid score (PDCAAS) and in vitro DIAAS values for insect, microalgae, fungi and meat analogues.

Type	Processing method	PDCAAS (%)	Scoring pattern (the age group PDCAAS refers to)	DIAAS (%)	Scoring pattern (the age group DIAAS refers to)	First limiting amino acid	Protein digestibility (%)	Animal model	Reference
Insect
Lesser mealworm, (Alphitobius diaperinus)	Dried powder added to the basal diet	–	–	57	0–6 months	Tryptophan	78 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Malla et al. 2022)
		–	–	71	6 months–3 years	sulfur amino acids
		–	–	83	>3 years	sulfur amino acids
Yellow mealworm, (Tenebrio molitor)	Dried powder added to the basal diet	–	–	45	0–6 months	sulfur amino acids	72 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Malla et al. 2022)
		–	–	54	6 months–3 years	sulfur amino acids
		–	–	64	>3 years	sulfur amino acids
Banded cricket, (Gryllodes sigillatus)	Dried powder added to the basal diet	–	–	47	0–6 months	Tryptophan	64 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Malla et al. 2022)
		–	–	78	6 months–3 years	sulfur amino acids
		–	–	92	>3 years	sulfur amino acids
House cricket, (Acheta domesticus)	Dried powder added to the basal diet	–	–	45	0–6 months	Tryptophan	75 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Malla et al. 2022)
		–	–	76	6 months–3 years	sulfur amino acids
		–	–	89	>3 years	sulfur amino acids
Black soldier fly, (Hermetia illucens)	Dried powder added to the basal diet	–	–	47	0–6 months	Lysine	62 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing pigs	(Malla et al. 2022)
		–	–	57	6 months–3 years	Lysine
		–	–	68	>3 years	Lysine
Black soldier fly, (Hermetia illucens L.)	Dried low-fat larvae added to the basal diet	–	–	73	0–6 months	Lysine	85 (true protein digestibility)	Rat	(Traksele et al. 2021)
Termite (Macrotermes nigeriensis)	Dried powder added to the basal diet	42	preschool children (2–5 years)		–	sulfur amino acids	91 (true protein digestibility)	Young male weanling albino rats	(Oibiokpa et al. 2018)
Moth (Cirina forda)	Dried powder added to the basal diet	42	preschool children (2–5 years)		–	sulfur amino acids	82 (true protein digestibility)	Young male weanling albino rats	(Oibiokpa et al. 2018)
Grasshopper (Melanoplus foedus)	Dried powder added to the basal diet	46	preschool children (2–5 years)		–	Isoleucine	85 (true protein digestibility)	Young male weanling albino rats	(Oibiokpa et al. 2018)
Cricket (Gryllus assimilis)	Dried powder added to the basal diet	73	preschool children (2–5 years)		–	Threonine	81(true protein digestibility)	Young male weanling albino rats	(Oibiokpa et al. 2018)
Microalgae
Arthrospira sp.	NR	84	>3 years old	–	–	Histidine	90 (cecal digestibility of nitrogen)	Rats	(Tessier et al. 2021)
Chlorella sp.	NR	–	–	111	>3 years	Histidine	NR	Calculated from in vitro data	(Li et al. 2019)
Nannochloropsis sp.	NR	–	–	23	>3 years	Histidine	NR	Calculated from in vitro data	(Li et al. 2019)
Phaeodactylum tricornutum	NR	–	–	75	>3 years	Leucine	NR	Calculated from in vitro data	(Li et al. 2019)
Scenedesmus obliquus	NR	–	–	40	>3 years	Tryptophan	NR	Calculated from in vitro data	(Li et al. 2019)
Arthrospira platensis	NR	–	–	34	>3 years	Tryptophan	NR	Calculated from in vitro data	(Li et al. 2019)
Chlorella vulgaris	Undisrupted cell walls	63	Children 3–10 years old	–	–	Histidine	65 (true protein digestibility)	Male Sprague–Dawley rats	(Wang et al. 2020)
	Mechanically disrupted cell walls	77	Children 3–10 years old	–	–	sulfur amino acids	77
Chlorella sorokiniana	Undisrupted cell walls	64	Children 3–10 years old	–	–	Isoleucine	60 (true protein digestibility)	Male Sprague–Dawley rats	(Wang et al. 2020)
	Mechanically disrupted cell walls	81	Children 3–10 years old	–	–	Isoleucine	75
Acutodesmus obliquus	Undisrupted cell walls	29	Children 3–10 years old	–	–	Histidine	38 (true protein digestibility)	Male Sprague–Dawley rats	(Wang et al. 2020)
	Mechanically disrupted cell walls	46	Children 3–10 years old	–	–	Histidine	67
Proteins from fungi
Fusarium venenatum	Mycelium of Fusarium venenatum	–	–	34–42 ^a	6 months–3 years	sulfur amino acids	52	In vitro	(Ariëns et al. 2021)
Fusarium venenatum	Mycelium of Fusarium venenatum	–	–	40–50 ^a	>3 years	sulfur amino acids		In vitro	(Ariëns et al. 2021)
Fusarium venenatum		100		–	NR	sulfur amino acids	86 (true ileal digestibility)	Ileostomy patients	(Edwards and Cummings 2010)
Saccharomyces sp.	Yeast cell biomass (broken)	86	Children 2–5 years old	–	–	NR	83	In vitro	(Pacheco, Caballero-Córdoba, and Sgarbieri 1997)
Saccharomyces sp.	Isoelectrically precipitated protein concentrate	82	Children 2–5 years old	–	–	NR	92	In vitro	(Pacheco, Caballero-Córdoba, and Sgarbieri 1997)
Saccharomyces sp.	Sodium trimetaphosphate treated extract followed by isoelectrical precipitation	90	Children 2–5 years old	–	–	NR	90	In vitro	(Pacheco, Caballero-Córdoba, and Sgarbieri 1997)
Saccharomyces cerevisiae	Yeast protein concentrate	–	–	83–84	6 months–3 years	sulfur amino acids	83	In vitro	(Ariëns et al. 2021)
Saccharomyces cerevisiae	Yeast protein concentrate	–	–	97-99^a	>3 years	sulfur amino acids		In vitro	(Ariëns et al. 2021)
Plant-Based Meat Analogues
Beyond Burger	Ingredients: Water, pea protein isolate, expeller-pressed canola oil, and refined coconut oil 2% or less of: cellulose from bamboo, methylcellulose, potato starch, natural flavors, maltodextrin, yeast extract, salt, sunflower oil, vegetable glycerin, dried yeast, gum arabic, citrus extract, ascorbic acid, beet juice extract, acetic acid, succinic acid, modified food starch, annatto, and minerals (calcium, iron, salt, and potassium chloride) Preparation: Burgers were cooked at 157 °C and 20% humidity to an internal temperature of 71 °C	–	–	71	6 months–3 years	sulfur amino acids	90 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing gilts	(Fanelli et al. 2022)
		–	–	83	>3 years	sulfur amino acids
Impossible Burger	Ingredients: Water, soy protein concentrate, coconut oil, sunflower oil, and natural flavors 2% or less of: potato protein, methylcellulose, yeast extract, cultured dextrose, food starch modified, soy leghemoglobin, salt, mixed tocopherols, soy protein isolate, vitamins and minerals [zinc gluconate, thiamin hydrochloride (vitamin B1), niacin, pyridoxine hydrochloride (vitamin B6), riboflavin (vitamin B2), and vitamin B12] Preparation: Burgers were cooked at 157 °C and 20% humidity to an internal temperature of 71 °C	–	–	91	Young children (6 months to 3 years old)	sulfur amino acids	99 (standardized ileal digestibility of crude proteins)	Ileal-cannulated growing gilts	(Fanelli et al. 2022)
		–	–	107	>3 years	sulfur amino acids

Data of DIAAS, PDCAAS and protein digestibility have been reported as integers, without decimal figures.

^a Data reported as range for three different calculation methods.

NR = not reported.

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