Journal List > Nutr Res Pract > v.16(Suppl 1) > 1162209

Park, Chung, Hwang, Shon, and Kim: A review of recent evidence of dietary protein intake and health

Abstract

The Korea National Health and Nutrition Examination Survey of 2013 to 2017 reported that the average protein consumption of the Korean population is above the current recommended nutrient intake of protein proposed by the Dietary Reference Intakes for Koreans. Some health professionals and the media often advise consuming diets high in protein for promoting metabolic regulation, weight control, and muscle synthesis. However, due to lack of scientific evidence, the validity and safety of high protein consumption are yet to be fully ascertained. The present review assesses recent evidence published in 2014–2020 from human studies, focusing on adequate protein intake and protein sources for the prevention of chronic diseases, particularly metabolic disorders and sarcopenia.

INTRODUCTION

Proteins are essential macronutrients for the human body, allowing both growth and maintenance. They provide amino acids to construct not only approximately 25,000 proteins encoded within the human genome, but also other nitrogen compounds required for the structural and functional system of the human body. The dietary requirement of proteins is based on the amount of protein and/or the constituent amino acids that need to be provided through the diet, to satisfy the metabolic demand and nitrogen equilibrium [1]. The current estimated average requirement (EAR) of protein as proposed in the Dietary Reference Intakes for Koreans (KDRIs) is based on the nitrogen balance approach as well as the factorial method for special needs for growth, pregnancy, and lactation [2].
The last two decades have seen a gradual increase in the average protein consumption in the Korean population [3]. According to the Korea National Health and Nutrition Examination Survey of 2013 to 2017, the average protein consumption of the Korean population is above the current EAR of protein, and even above the recommended nutrient intake in KDRIs for all age groups, except among the over 75 years elderly [2] (Table 1). Intriguingly, similar to increasing protein intake, there has also been an increase in the consumption of animal foods rich in proteins [4].
Table 1

Comparison of the 2020 Dietary Reference Intakes for Koreans of protein with the average daily protein intake estimated by the 2013–2017 Korea National Health and Nutrition Examination Survey by age group

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Life stage Age (yrs) Average protein intake (g/day) EAR %EAR RNI %RNI
Children 1–2 38.1 ± 1.1 15 254.0 20 190.5
3–5 46.3 ± 1.1 20 231.7 25 185.3
Adults (males) 6–8 62.9 ± 1.6 30 209.5 35 179.6
9–11 74.8 ± 2.4 40 187.0 50 149.6
12–14 89.1 ± 3.0 50 178.2 60 148.5
15–18 96.4 ± 3.7 55 175.2 65 148.2
19–29 88.3 ± 2.4 50 176.7 65 135.9
30–49 88.8 ± 1.3 50 177.6 65 136.6
50–64 82.5 ± 3.5 50 165.1 60 137.6
65–74 69.2 ± 2.2 50 138.5 60 115.4
≥ 75 58.0 ± 2.4 50 116.1 60 96.7
Adults (females) 6–8 52.3 ± 1.5 30 174.4 35 149.5
9–11 65.2 ± 2.0 40 163.0 45 144.9
12–14 66.4 ± 2.2 45 147.6 55 120.7
15–18 63.5 ± 2.5 45 141.1 55 115.5
19–29 64.3 ± 1.6 45 142.8 55 116.9
30–49 63.0 ± 0.9 40 157.5 50 126.0
50–64 57.8 ± 1.0 40 144.5 50 115.6
65–74 49.6 ± 1.8 40 124.0 50 99.2
≥ 75 37.7 ± 1.5 40 94.2 50 75.3
EAR, estimated average requirement; RNI, recommended nutrient intake.
Due to insufficient evidence based on scientific data, there has been substantial discussion about the validity and safety of high protein consumption. This study aims to review recent evidence published in 2014–2020 from human studies, focusing on adequate protein intake for the prevention of chronic diseases throughout the life cycle.

HIGH PROTEIN INTAKE IN EARLY LIFE AND OBESITY RISK

Protein intake in early life is critical for adequate development and growth. It has been established the adequate intake level of protein for infants in KDRIs based on the assumption that breastfeeding milk supplies enough protein for an infant’s adequate growth [2]. While clinical outcomes from protein deficiency have been well studied, the effects of early exposure to high protein diet during infancy have not been fully explored. Recent evidence indicates that infants on a high protein formula-fed diet in the first two years of life show greater weight gains and weight/length-for-age, as compared to breastmilk-fed infants (Table 2) [5678910]. Rapid weight gain during infancy is known to be a risk factor for obesity in later life [1112]. A European multicenter, double-blind, randomized controlled trial (RCT) study reported that high protein formula-fed infants in the first year of life showed higher body mass index (BMI) at 6 years of age than breastmilk-fed infants [9]. The results suggest that a lower protein formula reduces BMI and childhood obesity risk, potentially leading to reduced risks for adulthood obesity. This requires further investigations with long-term follow-ups.
Table 2

Associations of development and growth with high protein formula intake in early life

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Author, country (study) Year Study design Age (mean ± SD or range) Subject No. Background nutrient intake Comparison groups Duration Outcomes
Collell et al. [5], European-Childhood Obesity Program randomized trial 2016 RCT 0–2 yrs 47 Breast feeding or formula Breast feeding vs. LP formula1) vs. HP formula1) 2 yrs BMI was higher in HP formula group compared to LP formula and breast feeding group.
Cardiac function parameters were increased in HP formula group compared to LP formula group.
Liotto et al. [6], Italy 2018 RCT 5.3 ± 3.5 days 50 Breast feeding or formula Breast feeding vs. LP formula2) vs. HP formula2) 4 mon No difference in weight gain among formula groups.
Fat-free mass increase in LP formula group was similar to that of breast feeding group.
Oropeza-Ceja et al. [7], Mexico 2018 RCT ≤ 40 days 17 Breast feeding or formula Breast feeding vs. LP formula3) vs. MP formula3) vs. HP formula3) 4 mon Weight gain was greater in MP and HP formula compared to breast feeding.
Tang and Krebs [8], USA 2014 RCT 5–6 mon (exclusively breastfed) 18 Exclusive breast feeding (no formula use) Cereal group4) vs. Meat group4) (1–2 servings/day until 9–10 mon of age) 5 mon Weight-for-age z score and length-for-age z score in Meat group increased.
Weber et al. [9], European Childhood Obesity Project 2014 RCT 5.3 ± 3.5 days 24 Breast feeding or formula Breast feeding vs. HP formula5) vs. LP formula5) 6 yrs BMI increased in HP formula group.
Ziegler et al. [10], USA 2015 RCT ≤ 3 mon 82 Breast feeding or formula at age 3 mon Breast feeding vs. LP formula6) vs. HP formula6) 9 mon Weight gain from 3 to 6 mon was similar between LP and HP formula groups, but faster than breast feeding group. Odds ratios from 4 to 12 mon indicated fewer infants with weight > 85th percentile in LP formular group than in HP formular group.
*Complementary foods were allowed in small amounts from 4 to 6 mon and in unrestricted amounts after 6 mon
RCT, randomized controlled trial; BMI, body mass index; LP, low protein; MP, middle protein; HP, high protein.
1)LP formula: 1.25–1.6 g/100 mL; HP formula: 2.05–3.2 g/100 mL.
2)LP formula: 1.2 g/100 mL; HP formula: 1.7 g/100 mL.
3)LP formula: 1 g protein/dL with bovine alpha-lactalbumin, 26% of total protein; MP formula: 1.3 g/dL with bovine lactalbumin; HP formula: 1.5 g/dL with standard infant formula, which is based on cow’s milk proteins, adjusted by the addition of whey protein concentrates to more closely resemble the whey protein-to-casein ratio of human milk of proximately 65:35.
4)Cereal group: fortified infant cereals as the first complementary food; meat group: commercially prepared pureed meats.
5)LP formula: 1.25 g/dL and 1.6 g/dL protein for follow-up; HP formula: 2.05 g/dL and 3.2 g/dL protein for follow-up.
6)LP formula: 1.61 g/100 kcal (modified bovine whey proteins with caseinoglycomacropeptide removed); HP formula: 2.15 g/100 kcal (unmodified bovine milk protein with a whey/casein ratio of 60/40).

HIGH PROTEIN INTAKE AND CARDIOVASCULAR DISEASE (CVD) IN ADULTHOOD

Metabolic outcomes of high protein consumption have been repeatedly reported [1314]. Excess protein intake is associated with an increased risk of metabolic disorders such as obesity and associated CVD. These associations are often, but not exclusively, speculated from indirect consequences of high protein consumption accompanied by high energy and animal fat intake. Recent RCTs have reported that high protein intake effectively reduces the biomarkers for CVD risk in healthy and obese adults [15161718]. It is noteworthy that these results are limited to either young healthy individuals with iso- or hypercaloric diets, or overweight and obese adults with hypocaloric diets [15161718]. Moreover, prospective cohorts and cross-sectional studies have shown inconsistent results associating protein intake as grams per day or energy percentage and CVD [192021222324]; this could probably be due to the varying ranges of cutoff for the level of intake or the percentage of energy. Further investigations are needed to fully understand the effect of protein intake on CVD risks with respect to the level of energy consumption and the protein proportion of total energy.

ASSOCIATIONS OF PROTEIN SOURCES AND CVD

It was further observed that intake of animal and plant protein is associated with metabolic disease risk factors (Table 3). In general, the quality of protein varies depending on the composition of amino acids such as indispensable amino acid ratio and animal or plant food sources [25]. However, there is limited evidence to establish dietary reference intake of animal and plant protein for Koreans. The associations of animal and plant protein intake with metabolic diseases, such as CVD, were inconsistent. In several Western studies, plant protein intake had a beneficial effect on blood pressure, whereas animal protein intake had no significant effect on blood pressure [2627]. Conversely, in Japanese adults, animal protein intake had a stronger preventive effect on high blood pressure than plant protein intake [28].
Table 3

Associations of animal and plant protein intake with cardiovascular disease

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Author, country Year Study design Age (mean ± SD or range) Subject No. Background nutrient intake Comparison groups Duration Outcomes
van Nielen et al. [29], Netherlands 2014 RCT 61 ± 5 yrs 15 Background diet: 18%, 45%, and 34% energy from protein, carbohydrate, and fat, respectively HP1) diet vs. HS1) diet 12 wks Total and LDL cholesterol were lower after HS diet
Tielemans et al. [30], Netherlands 2014 Prospective cohort 70.1 ± 4.6 yrs 272 Baseline median intake: 4.1%, 4.9%, and 5.9% energy intake from plant protein in lowest, middle, and highest tertile group, respectively T1 of plant protein intake2) vs. T2 and T2 of plant protein intake2) 5 yrs T2 and T3 of plant protein intake were related to change in SBP and DBP
Liu et al. [23], China 2013 Cross sectional 18–80 yrs 2,241 Not available Q1 of animal protein intake3) vs. Q4 of animal protein intake3) (female) Not available Hypertension risk was inversely associated with animal protein intake
Chung et al. [31], Korea 2020 Cross sectional 30–64 yrs 13,485 Not available Q1 of animal protein intake4) vs. Q4 of animal protein intake4) (male) Not available Reduced HDL cholesterol risk was positively associated with animal intake
Q1 of plant protein intake5) vs. Q4 of plant protein intake5) (male) High blood pressure risk was inversely associated with plant protein intake
RCT, randomized controlled trial; HP, high mixed protein; HS, high soy protein; LDL, low-density lipoprotein; SBP, systolic blood pressure; DBP, diastolic blood pressure; HDL, high-density lipoprotein.
1)HP diet: high protein diet of mixed, not soy sources (high protein mix, 1.6 g protein/kg/day); HS diet: high protein diet replacing meat with soy (high protein soy, 1.7 g protein/kg/day, 30 g/day soy).
2)T1: lowest tertile group, energy intake from plant protein 4.1%/day; T2 and T3: middle and highest tertile groups, energy intake from plant protein 4.9% and 5.9%/day, respectively (baseline median intake).
3)Q1: lowest quartile group, animal protein intake < 3.4 g/day; Q4: highest quartile group, animal protein intake > 11.3 g/day.
4)Q1: lowest quartile group, animal protein intake 11.4 ± 0.3 g/day; Q4: highest quartile group, animal protein intake 88.4 ± 1.3 g/day.
5)Q1: lowest quartile group, plant protein intake 22.2 ± 0.2 g/day; Q4: highest quartile group, plant protein intake 62.5 ± 0.4 g/day.
Contradictory results from recent studies have established that the association of animal protein and plant protein intake with cardiovascular risk factors remains controversial. For example, in an RCT of postmenopausal women with abdominal obesity, soy protein diet showed 4% and 9% reduction in the total and low-density lipoprotein cholesterol plasma levels, compared to a mixed protein diet which mainly consisted of meat, dairy, and bread [29]. In addition, in a cohort study of male elderly, high plant protein intake was associated with reduced 5-year change in blood pressure as compared to low plant protein intake, while animal protein intake showed no significant association [30]. However, according to a cross-sectional study, high animal protein intake was inversely related to the prevalence of hypertension, as compared to low animal protein intake among female adults [23]. Another study reported that higher animal protein intake was associated with higher prevalence of reduced high-density lipoprotein cholesterol, while higher plant protein intake was associated with lower prevalence of high blood pressure in Korean male adults [31]. Thus, more evidence and sensitive analysis are required to establish dietary reference intake of animal and plant protein intake in a large population, by conducting further clinical studies. In addition, specific populations, such as vegetarians whose food protein sources are relatively clear, should be considered in future studies for establishing dietary reference intake of animal and plant protein.

HIGH PROTEIN INTAKE AND SARCOPENIA IN ELDERLY

Sarcopenia is defined as an abnormal loss of muscle mass and muscle strength [32]. In the elderly, sarcopenia results in frailty, which is characterized by unintentional weight loss, weakness, exhaustion, reduced physical activity, and falls [33], thereby reducing the quality of life and shortening the lifespan. Physical inactivity and low protein intake are suggested risk factors for sarcopenia [34] and frailty [35]. Therefore, to prevent sarcopenia, the need to adjust and increase the protein intake standards for elderly individuals over 65 years of age has been suggested. Moreover, older people who want to maintain muscle mass and optimal body function require higher amounts of dietary protein than younger individuals to overcome age-related anabolic resistance [36373839]. Summarizing the results of literature analysis on frailty/sarcopenia since 2014, research results have consistently reported that protein supplementation or high-protein diet in elderly subjects suppresses the sarcopenia/frailty indicators (muscle mass and muscle strength loss) and increases muscle fiber production (Table 4).
Table 4

Associations of protein intake with sarcopenia in elderly

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Author, country Year Study design Age (range) Subject No. Background nutrient intake Comparison groups Duration Outcomes
Kerstetter et al. [40], USA 2015 RCT > 60 yrs women 208 Dietary protein: 1.07 g/kg (protein group), 1.06 g/kg (carbohydrate group) Carbohydrate group1) vs. protein group1) 18 mon Total and truncal lean mass was higher in the protein group
>70 yrs men
Kim et al. [41], USA 2015 RCT 52–75 yrs 20 No information 1RDA2) vs. 2RDA2) 4 days Rates of protein synthesis of whole body and muscle were higher in the 2RDA group than 1RDA group, regardless of protein intake pattern
Mitchell et al. [42], Australia, New Zealand 2017 RCT > 70 yrs 29 RDA group: 3,132 kcal, protein 101, carbohydrate 288, fat 161 g/day Complete diet containing current RDA3) vs. 2RDA3) for protein 10 wks Whole body lean mass, trunk lean mass, and knee-extension peak power increased in 2RDA group
2RDA group: 2,224 kcal, protein 88, carbohydrate 264, fat 75 g/day
Park et al. [43], Korea 2018 RCT 70–85 yrs 120 Protein intake at baseline: 0.84 g/kg, 0.77 g/kg, and 0.8 g/kg for 0.8 g, 1.2 g, and 1.5 g protein/kg/day groups, respectively 0.8 g vs. 1.2 g vs. 1.5 g protein/kg/day fulfilled with placebo and protein powder supplements 12 wks Appendicular skeletal muscle mass, skeletal muscle mass index, and gait speed were higher in the 1.5 g protein/kg/day group
Houston et al. [36], USA 2017 Prospective cohort 70–79 yrs 1,998 Baseline intake: 13.4%, 14.4%, and 15.6% energy intake from protein for < 0.7 g, 0.7–< 1.0 g, and ≥ 1.0 g protein/kg/day groups, respectively < 0.7 g vs. 0.7–< 1.0 g vs. ≥ 1.0 g protein/kg/day 6 yrs Risk of mobility limitation in < 0.7 g and 0.7–< 1.0 g protein/kg/day group was higher than ≥ 1.0 g protein/kg/day group
Mendonça et al. [47], UK 2019 Cohort ≥ 85 yrs 722 Not available Protein (g/kg/day) 5 yrs Better disability trajectories were associated with ≥ 1.0 g protein/kg/day
Mustafa et al. [48], USA 2018 Prospective cohort ≥ 50 yrs 1,779 Baseline intake: 15.9%, 17.1%, and 18.1% energy intake from protein for < 0.8 g, 0.8–1.1 g, and ≥ 1.2 g protein/kg/day groups, respectively < 0.8 g vs. 0.8–1.1 g vs. ≥ 1.2 g protein/kg/day 12 yrs Functional decline was slower in ≥ 0.8 g protein/kg/day group
Granic et al. [49], UK 2018 Cohort ≥ 85 yrs 722 No information < 1 g vs. ≥ 1 g protein/kg/day 5 yrs Grip strength and physical performance were higher in ≥ 1 g protein/kg/day group
McLean et al. [50], USA 2015 Prospective cohort ≥ 60 yrs 646 No information Total, animal, and plant protein intake group 6 yrs Higher grip strength was associated with greater total and animal protein intake
Bradlee et al. [44], USA 2017 Prospective cohort ≥ 40 yrs 685 Baseline intake: 1.04 and 1.01 g/day for 6 to < 8 total animal protein food servings per day in men, and women, respectively Protein source foods (servings/day, varies depends on foods) 16 yrs Skeletal muscle mass was higher and functional decline was lower in higher protein (animal source) food intake group
Gray-Donald et al. [51], Canada 2014 Nested case control 68–82 yrs 422 Not available < 0.8 g vs. 0.8–< 1.0 g vs. 1.0–< 1.2 g vs. ≥ 1.2 g protein/kg/day 1 yr Protection against weight loss was better in ≥ 1 g protein/kg/day groups
Huang et al. [45], Taiwan 2016 Cross sectional 65–85 yrs 327 Not available Q1 of total and vegetable protein density4) vs. Q4 of total and vegetable protein density4) Not available Risk for low muscle mass was higher in the Q1 of total and vegetable protein density
Kobayashi et al. [52], Japan 2013 Cross sectional 65–94 yrs 2,108 Not available Q1 of total protein intake5) vs. Q5 of total protein intake5) (women) Not available Frailty was negatively related to total protein intake
Nilsson et al. [46], Sweden 2018 Cross sectional 65–70 yrs 106 Not available 0.8 g vs. 1.1 g protein/kg/day Not available Muscle mass and physical function were higher in 1.1 g protein/kg/day group
Oh et al. [24], Korea 2017 Cross sectional ≥ 60 yrs 4,452 Not available < 0.8 g vs. 0.8–1.2 g vs. > 1.2 g protein/kg/day Not available Risk of sarcopenia was higher in < 0.8 g and 0.8–1.2 g protein/kg/day group
RCT, randomized controlled trial; RDA, recommended dietary allowance.
1)Carbohydrate group: carbohydrate (isocaloric maltodextrin) supplement group; Protein group: 45 g whey protein (40 g protein, 1.3 g protein/kg) group.
2)1RDA (0.8 g/kg/day), 2RDA (1.5 g/kg/day) with uneven (15/20/65% total protein amount at breakfast/lunch/dinner) or even (33/33/33% total protein amount at breakfast/lunch/dinner) intake of protein in the context of mixed meals.
3)RDA: 0.8 g/kg/day; 2RDA: 1.6 g/kg/day.
4)Q1: lowest quartile group, < 13.2% and < 5.8% for total and vegetable protein density, respectively; Q4: highest quartile group, ≥ 17.2% and ≥ 9.4% for total and vegetable protein density, respectively.
5)Q1: lowest quintile group, total protein intake ≤ 62.9 g/day; Q5: highest quintile group, total protein intake ≥ 84.3 g/day.
In a study providing 40 g protein supplement (1.3 g protein/kg/day) for 18 month to male and female senior citizens with no difference in daily protein intake, there was a significant increase in the amount of lean body mass [40]. In the context of mixed meals, whole body and muscle protein synthesis rate and net protein balance were significantly higher in the 1.5 g protein/kg/day intake group than in the 0.8 g protein/kg/day group [41]. Even or uneven distribution of protein intake across the three meals had no effect on these results. Consumption of a well-controlled complete diet containing twice the Recommended Dietary Allowance (RDA) (1.6 g/kg/day) of protein for 10 weeks in over 70-year-old men resulted in increased whole-body mass, trunk lean mass, and physical function manifested by knee-extension peak power and grip strength, as compared to intake of RDA (0.8 g/kg/day) group [42]. As shown in the protein dose-response study of Park et al. [43], the beneficial effects targeted towards the prevention of sarcopenia and frailty appear to be manifested by a protein intake of 1.5 g/kg/day. Prospective cohort and cross-sectional studies reported the beneficial effect of high-protein (≥ 0.8–1.0 g/kg/day vs < 0.8 g/kg/day) diet on preventing loss of skeletal muscle mass and physical function in the elderly (Table 4). However, there has been no consistent research demonstrating the effect of dietary protein sources. Increased skeletal muscle mass and lower functional decline were reported in the group consuming maximum animal protein foods [44], whereas the group with the least amount of plant protein intake was at a higher risk [45].
Conversely, blood urea nitrogen was significantly increased with protein intake of 1.2–1.6 g/kg/day, as compared to protein intake of 0.8 g/kg/day, within the normal range [4143]. Given the decline in kidney function with age, concerns are frequently raised about the effect of a high-protein diet on kidney function in the elderly. Additionally, since body mass of the elderly is lower than the general adult, there is an opinion that the intake of low protein is not consequential. Further quantitative studies to define optimal protein intake in old age are therefore required in the future.

CONCLUSION

Accruing studies have reported the correlation between protein intake and chronic diseases. However, insufficient scientific evidence fails to establish the protein intake standards for the prevention of obesity, CVD, and sarcopenia. These standards need to be determined by considering the characteristics based on the life cycle and health status. High protein intake in early childhood may be a risk factor for obesity, but may help prevent frailty and sarcopenia in the elderly. In the future, measures, such as reducing protein in infant formula and increasing protein intake in the elderly, are expected to be prepared. In particular, it should be considered that compared to other age groups, lack of protein intake in the elderly may be higher due to the inability to eat good quality meals due to loss of appetite, weakness, and difficulty in eating due to disease. The correlation between the protein source and the risk of chronic disease also remains inconsistent, and most reports are based on observational studies or a small number of subjects, thereby limiting interpretation. It is believed that more clinical intervention studies are required in the future to prepare more sophisticated protein intake standards based on scientific evidence.

Notes

Funding: This research was supported by Policy Research Program for (project No. 20180415A13-00, 25193068200, 25203084501) from the Ministry of Health and Welfare in 2018–2020.

Conflict of Interest: The authors declare no potential conflicts of interests.

Author Contributions:

  • Project administration: Hwang JT, Kim E.

  • Writing - review & editing: Park YJ, Chung S, Shon J, Hwang JT, Kim E.

References

1. World Health Organization/Food and Agriculture Organization of the United Nations/United Nations University (WHO/FAO/UNU). Protein and Amino Acid Requirements in Human Nutrition. Report of a Joint WHO/FAO/UNU Expert Consultation. Geneva: World Health Organization;2007.
2. Ministry of Health and Welfare, The Korean Nutrition Society. 2020 Dietary Reference Intakes for Koreans: Energy and Macronutrients. Seoul: Ministry of Health and Welfare, The Korean Nutrition Society;2020.
3. Kim JG, Kim JS, Kim JG. Trends of food supply and nutrient intake in South Korea over the past 30 years. Curr Res Nutr Food Sci. 2019; 7:85–95.
4. Yun S, Kim HJ, Oh K. Trends in energy intake among Korean adults, 1998-2015: results from the Korea National Health and Nutrition Examination Survey. Nutr Res Pract. 2017; 11:147–154. PMID: 28386388.
5. Collell R, Closa-Monasterolo R, Ferré N, Luque V, Koletzko B, Grote V, Janas R, Verduci E, Escribano J. Higher protein intake increases cardiac function parameters in healthy children: metabolic programming by infant nutrition-secondary analysis from a clinical trial. Pediatr Res. 2016; 79:880–888. PMID: 26882370.
6. Liotto N, Orsi A, Menis C, Piemontese P, Morlacchi L, Condello CC, Giannì ML, Roggero P, Mosca F. Clinical evaluation of two different protein content formulas fed to full-term healthy infants: a randomized controlled trial. BMC Pediatr. 2018; 18:59. PMID: 29439736.
7. Oropeza-Ceja LG, Rosado JL, Ronquillo D, García OP, Caamaño MDC, García-Ugalde C, Viveros-Contreras R, Duarte-Vázquez MÁ. Lower protein intake supports normal growth of full-term infants fed formula: a randomized controlled trial. Nutrients. 2018; 10:10.
8. Tang M, Krebs NF. High protein intake from meat as complementary food increases growth but not adiposity in breastfed infants: a randomized trial. Am J Clin Nutr. 2014; 100:1322–1328. PMID: 25332329.
9. Weber M, Grote V, Closa-Monasterolo R, Escribano J, Langhendries JP, Dain E, Giovannini M, Verduci E, Gruszfeld D, Socha P, et al. Lower protein content in infant formula reduces BMI and obesity risk at school age: follow-up of a randomized trial. Am J Clin Nutr. 2014; 99:1041–1051. PMID: 24622805.
10. Ziegler EE, Fields DA, Chernausek SD, Steenhout P, Grathwohl D, Jeter JM, Nelson SE, Haschke F. Adequacy of infant formula with protein content of 1.6 g/100 kcal for infants between 3 and 12 months. J Pediatr Gastroenterol Nutr. 2015; 61:596–603. PMID: 26154030.
11. Monasta L, Batty GD, Cattaneo A, Lutje V, Ronfani L, Van Lenthe FJ, Brug J. Early-life determinants of overweight and obesity: a review of systematic reviews. Obes Rev. 2010; 11:695–708. PMID: 20331509.
12. Koletzko B, von Kries R, Closa R, Escribano J, Scaglioni S, Giovannini M, Beyer J, Demmelmair H, Anton B, Gruszfeld D, et al. Can infant feeding choices modulate later obesity risk? Am J Clin Nutr. 2009; 89:1502S–1508S. PMID: 19321574.
13. Metges CC, Barth CA. Metabolic consequences of a high dietary-protein intake in adulthood: assessment of the available evidence. J Nutr. 2000; 130:886–889. PMID: 10736347.
14. Pedersen AN, Kondrup J, Børsheim E. Health effects of protein intake in healthy adults: a systematic literature review. Food Nutr Res. 2013; 57:23364.
15. Kim HH, Kim YJ, Lee SY, Jeong DW, Lee JG, Yi YH, Cho YH, Choi EJ, Kim HJ. Interactive effects of an isocaloric high-protein diet and resistance exercise on body composition, ghrelin, and metabolic and hormonal parameters in untrained young men: a randomized clinical trial. J Diabetes Investig. 2014; 5:242–247.
16. Gulati S, Misra A, Tiwari R, Sharma M, Pandey RM, Yadav CP. Effect of high-protein meal replacement on weight and cardiometabolic profile in overweight/obese Asian Indians in North India. Br J Nutr. 2017; 117:1531–1540. PMID: 28653586.
17. Rietman A, Schwarz J, Blokker BA, Siebelink E, Kok FJ, Afman LA, Tomé D, Mensink M. Increasing protein intake modulates lipid metabolism in healthy young men and women consuming a high-fat hypercaloric diet. J Nutr. 2014; 144:1174–1180. PMID: 24899158.
18. Campos-Nonato I, Hernandez L, Barquera S. Effect of a high-protein diet versus standard-protein diet on weight loss and biomarkers of metabolic syndrome: a randomized clinical trial. Obes Facts. 2017; 10:238–251. PMID: 28601864.
19. Preis SR, Stampfer MJ, Spiegelman D, Willett WC, Rimm EB. Dietary protein and risk of ischemic heart disease in middle-aged men. Am J Clin Nutr. 2010; 92:1265–1272. PMID: 20881068.
20. Prentice RL, Huang Y, Kuller LH, Tinker LF, Horn LV, Stefanick ML, Sarto G, Ockene J, Johnson KC. Biomarker-calibrated energy and protein consumption and cardiovascular disease risk among postmenopausal women. Epidemiology. 2011; 22:170–179. PMID: 21206366.
21. Halton TL, Willett WC, Liu S, Manson JE, Albert CM, Rexrode K, Hu FB. Low-carbohydrate-diet score and the risk of coronary heart disease in women. N Engl J Med. 2006; 355:1991–2002. PMID: 17093250.
22. Assmann KE, Joslowski G, Buyken AE, Cheng G, Remer T, Kroke A, Günther AL. Prospective association of protein intake during puberty with body composition in young adulthood. Obesity (Silver Spring). 2013; 21:E782–E789. PMID: 23788493.
23. Liu R, Dang S, Yan H, Wang D, Zhao Y, Li Q, Liu X. Association between dietary protein intake and the risk of hypertension: a cross-sectional study from rural western China. Hypertens Res. 2013; 36:972–979. PMID: 23842622.
24. Oh C, No JK. Appropriate protein intake is one strategy in the management of metabolic syndrome in Korean elderly to mitigate changes in body composition. Nutr Res. 2018; 51:21–28. PMID: 29673541.
25. Friedman M. Nutritional value of proteins from different food sources. J Agric Food Chem. 1996; 44:6–29.
26. Altorf-van der Kuil W, Engberink MF, Vedder MM, Boer JM, Verschuren WM, Geleijnse JM. Sources of dietary protein in relation to blood pressure in a general Dutch population. PLoS One. 2012; 7:e30582. PMID: 22347387.
27. Wang YF, Yancy WS Jr, Yu D, Champagne C, Appel LJ, Lin PH. The relationship between dietary protein intake and blood pressure: results from the PREMIER study. J Hum Hypertens. 2008; 22:745–754. PMID: 18580887.
28. Umesawa M, Sato S, Imano H, Kitamura A, Shimamoto T, Yamagishi K, Tanigawa T, Iso H. Relations between protein intake and blood pressure in Japanese men and women: the Circulatory Risk in Communities Study (CIRCS). Am J Clin Nutr. 2009; 90:377–384. PMID: 19515740.
29. van Nielen M, Feskens EJ, Rietman A, Siebelink E, Mensink M. Partly replacing meat protein with soy protein alters insulin resistance and blood lipids in postmenopausal women with abdominal obesity. J Nutr. 2014; 144:1423–1429. PMID: 25008579.
30. Tielemans SM, Kromhout D, Altorf-van der Kuil W, Geleijnse JM. Associations of plant and animal protein intake with 5-year changes in blood pressure: the Zutphen Elderly Study. Nutr Metab Cardiovasc Dis. 2014; 24:1228–1233. PMID: 24998077.
31. Chung S, Chung MY, Choi HK, Park JH, Hwang JT, Joung H. Animal protein intake is positively associated with metabolic syndrome risk factors in middle-aged Korean men. Nutrients. 2020; 12:3415.
32. Roubenoff R. Sarcopenia: a major modifiable cause of frailty in the elderly. J Nutr Health Aging. 2000; 4:140–142. PMID: 10936900.
33. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001; 56:M146–M156. PMID: 11253156.
34. Dennison EM, Sayer AA, Cooper C. Epidemiology of sarcopenia and insight into possible therapeutic targets. Nat Rev Rheumatol. 2017; 13:340–347. PMID: 28469267.
35. Rolland Y, Abellan van Kan G, Bénétos A, Blain H, Bonnefoy M, Chassagne P, Jeandel C, Laroche M, Nourhashémi F, Orcel P, et al. Frailty, osteoporosis and hip fracture: causes, consequences and therapeutic perspectives. J Nutr Health Aging. 2008; 12:335–346. PMID: 18443717.
36. Houston DK, Tooze JA, Garcia K, Visser M, Rubin S, Harris TB, Newman AB, Kritchevsky SB. Health ABC Study. Protein intake and mobility limitation in community-dwelling older adults: the health ABC study. J Am Geriatr Soc. 2017; 65:1705–1711. PMID: 28306154.
37. Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor PM, Rennie MJ. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J. 2005; 19:422–424. PMID: 15596483.
38. Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, Williams J, Smith K, Seynnes O, Hiscock N, et al. Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol. 2009; 587:211–217. PMID: 19001042.
39. Volpi E, Campbell WW, Dwyer JT, Johnson MA, Jensen GL, Morley JE, Wolfe RR. Is the optimal level of protein intake for older adults greater than the recommended dietary allowance? J Gerontol A Biol Sci Med Sci. 2013; 68:677–681. PMID: 23183903.
40. Kerstetter JE, Bihuniak JD, Brindisi J, Sullivan RR, Mangano KM, Larocque S, Kotler BM, Simpson CA, Cusano AM, Gaffney-Stomberg E, et al. The effect of a whey protein supplement on bone mass in older Caucasian adults. J Clin Endocrinol Metab. 2015; 100:2214–2222. PMID: 25844619.
41. Kim IY, Schutzler S, Schrader A, Spencer H, Kortebein P, Deutz NE, Wolfe RR, Ferrando AA. Quantity of dietary protein intake, but not pattern of intake, affects net protein balance primarily through differences in protein synthesis in older adults. Am J Physiol Endocrinol Metab. 2015; 308:E21–E28. PMID: 25352437.
42. Mitchell CJ, Milan AM, Mitchell SM, Zeng N, Ramzan F, Sharma P, Knowles SO, Roy NC, Sjödin A, Wagner KH, et al. The effects of dietary protein intake on appendicular lean mass and muscle function in elderly men: a 10-wk randomized controlled trial. Am J Clin Nutr. 2017; 106:1375–1383. PMID: 29092886.
43. Park Y, Choi JE, Hwang HS. Protein supplementation improves muscle mass and physical performance in undernourished prefrail and frail elderly subjects: a randomized, double-blind, placebo-controlled trial. Am J Clin Nutr. 2018; 108:1026–1033. PMID: 30475969.
44. Bradlee ML, Mustafa J, Singer MR, Moore LL. High-protein foods and physical activity protect against age-related muscle loss and functional decline. J Gerontol A Biol Sci Med Sci. 2017; 73:88–94. PMID: 28549098.
45. Huang RY, Yang KC, Chang HH, Lee LT, Lu CW, Huang KC. The association between total protein and vegetable protein intake and low muscle mass among the community-dwelling elderly population in Northern Taiwan. Nutrients. 2016; 8:8.
46. Nilsson A, Montiel Rojas D, Kadi F. Impact of meeting different guidelines for protein intake on muscle mass and physical function in physically active older women. Nutrients. 2018; 10:1156.
47. Mendonça N, Granic A, Hill TR, Siervo M, Mathers JC, Kingston A, Jagger C. Protein intake and disability trajectories in very old adults: the newcastle 85+ study. J Am Geriatr Soc. 2019; 67:50–56. PMID: 30382594.
48. Mustafa J, Ellison RC, Singer MR, Bradlee ML, Kalesan B, Holick MF, Moore LL. Dietary protein and preservation of physical functioning among middle-aged and older adults in the Framingham offspring study. Am J Epidemiol. 2018; 187:1411–1419. PMID: 29590270.
49. Granic A, Mendonça N, Sayer AA, Hill TR, Davies K, Adamson A, Siervo M, Mathers JC, Jagger C. Low protein intake, muscle strength and physical performance in the very old: the newcastle 85+ study. Clin Nutr. 2018; 37:2260–2270. PMID: 29191494.
50. McLean RR, Mangano KM, Hannan MT, Kiel DP, Sahni S. Dietary protein intake is protective against loss of grip strength among older adults in the Framingham offspring cohort. J Gerontol A Biol Sci Med Sci. 2016; 71:356–361. PMID: 26525088.
51. Gray-Donald K, St-Arnaud-McKenzie D, Gaudreau P, Morais JA, Shatenstein B, Payette H. Protein intake protects against weight loss in healthy community-dwelling older adults. J Nutr. 2014; 144:321–326. PMID: 24357473.
52. Kobayashi S, Asakura K, Suga H, Sasaki S. Three-generation Study of Women on Diets and Health Study Group. High protein intake is associated with low prevalence of frailty among old Japanese women: a multicenter cross-sectional study. Nutr J. 2013; 12:164. PMID: 24350714.
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