Table 3.
Characteristics of 14 studies describing long-term effects of protein intake in healthy children and adolescents.
| Observational Studies | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Source | Age (Years) | No. of Individuals | % of Boys | Age of Outcomes |
Total Protein Intake |
Animal Protein Intake | Dairy Protein Intake | Plant Protein Intake | Main Outcomes | Observations |
| Günther et al., 2007 [21], the DONALD Study, Germany | 1; 5–6 | 203 | 50.25 | 7 | 1 y: 13.3 (11.7, 14.8) (%E) |
1 y: 8.4 (7.1, 9.8) (%E) |
1 y: 4.4 (2.5, 6.3) (%E) |
1 y: 4.8 (4.0, 5.7) (%E) |
BMI-SDS at 7 y: positive association; a higher animal (p for trend = 0.03) and dairy (p for trend = 0.02) protein intake (%E) was associated with a higher BMI-SDS at 7 y. BF% at 7 y: positive association; a higher animal (p for trend = 0.008) and dairy (p for trend = 0.07) protein intake (%E) was associated with a higher BMI-SDS at 7 y. |
In the fully adjusted models, the results for protein intake at 5–6 years were overall less convincing than those for 1 years. |
| 5–6 y: 12.4 (11.2, 13.7) (%E) | 5–6 y: 7.8 (6.7, 8.8) (%E) |
5–6 y: 3.5 (2.6, 4.5) (%E) |
5–6 y: 4.5 (4.0, 5.1) (%E) |
BMI-SDS at 7 y: positive tendency; a higher animal protein intake (%E) (p for trend = 0.07) was associated with a higher BMI-SDS at 7 y. BF% at 7 y: positive association; a higher animal protein intake (%E) (p for trend = 0.01) was associated with a higher BF% at 7 y. Inverse association: a higher vegetable protein intake (%E) (p for trend = 0.05) was associated with a lower BF% at 7 y. |
||||||
| Magarey et al., 2001 [52], South Australia | 2; 4; 6; 8; 11; 13; 15 |
143–243 | 51.1–59.0 | 4; 6; 8; 11; 13; 15 |
6 y boys: 54.7 ± 12.3 (g/d) 14.0 ± 2.1 (%E) 6 y girls: 51.1 ± 12.3 (g/d) 14.6 ± 2.0 (%E) |
NA | NA | NA | BMI-SDS at 8 y: negative association; only protein intake at 6 years was negatively associated with BMI-SDS score at 8 y. Triceps measurement: no association; neither protein intake nor any nutrient was a significant predictor of the triceps-SD score for any time interval. |
For most ages, energy-adjusted macronutrient intakes at previous age were not significant predictors of BMI-SDS at subsequent ages. None of the nutrients at 2 years were a significant predictor of BMI at 8 years. |
| Hermanussen 2008 [49], the DONALD Study, Germany | 2–18 | 1028 | 48.7 | -------- | NA | NA | NA | NA | BMI-SDS: positive association; significant interaction with the mean absolute daily intake of all protein (r = 0.143, p < 0.0001) and animal protein (r = 0.151, p < 0.0001). Significant interaction with protein intake (%E) of all protein (r = 0.203, p < 0.0001) and animal protein (r = 0.163, p < 0.0001). |
The correlation depended on age: maxima in the group of 10–12 years in both genders (boys: r = 0.31, p < 0.0001; girls: r = 0.36, p < 0.0001). |
| Skinner et al., 2004 [57], United States | 2–8 | 70 | 52.86 | 8 | Boys: 56.89 ± 15.11 (g/d) 1 Girls: 53.44 ± 16.33 (g/d) 1 Both: 14 (%E) |
NA | NA | NA | BMI at 8 y: positive association; mean longitudinal (2–8 years of age) dietary protein intake (g/d) was positively related to BMI. | |
| Switkowski et al., 2019 [53], Project Viva Cohort (NCT02820402), US | 3.2 | 1165 | 50 | 7.7 y 13 y |
Boys: 58.2 ± 8.20 (g/d) Girls: 58.4 ± 8.48 (g/d) |
NA | NA | NA | BMI z-scores at 13 y: positive association; a 10 g/d increase in total protein intake at 3.2 years was associated with 0.12 (95% CI: 0.01, 0.23) unit greater BMI z-scores only in boys. Positive association with animal protein intake only in boys (13 y). DXA lean mass index at 13 y: positive association; there was a trend towards a higher DXA lean mass index (p = 0.06) only in boys (13 y). Positive association with animal protein intake only in boys (13 y). Free IGF-I concentrations at 13 y: positive association; only in boys did a 10 g/d increase in total protein intake at 3.2 years correspond to a 5.67% higher total IGF-I (95% CI: 0.30%, 11.3%) and a 6.10% higher free IGF-I (95% CI: 1.19%, 11.3%). |
Outcomes evaluated: height, IGF-I, measures of adiposity and lean mass. There were no associations of protein intake in early childhood with any of the mild-childhood (7.7 years) and adolescent girls (13 years) outcomes. There were no associations of protein intake in early childhood with either SS + TR skinfolds or DXA fat mass among boys at 13 years. |
| Durao et al., 2017 [58], Generation XXI, Portugal | 4 | 1999 | 51.3 | 7 | Boys: 77.5 ± 16.00 (g/d) 18.6 ± 2.58 (%E) Girls: 73.8 ± 14.33 (g/d) 18.8 ± 2.54 (%E) |
NA | NA | NA | BMI z-scores at 7 y: positive association; higher protein intake in both boys (T3 vs. T1: p for trend = 0.045) and girls (T2 vs. T1: p for trend = 0.266) was positively associated with BMI z-scores. FSI at 7 y: positive association; higher protein intake was positively associated with FSI only in boys (T3 vs. T1: p for trend = 0.035). When compared to boys in the first tertile, boys in the highest tertile of protein intake at 4 years of age showed a statistically significant increase in FSI of 0.207 z-score units, at 7 years. |
Boys: T1 (≤72.7 g/d) T2 (72.8–81.0 g/d) T3 (≥81.0 g/d) Girls: T1 (≤69.7 g/d) T2 (69.8–77.5 g/d) T3 (≥77.5 g/d) |
| van Vught et al., 2010 [55], CoSCIS, Denmark | 6 | 203 | 46.31 | 9 | Boys: 69.90 ± 17.33 (g/d) Girls: 62.72 ± 14.92 (g/d) Total: 66.05 ± 16.04 (g/d) |
NA | NA | NA | Height at 9 y: positive association; high intake of ARG (p = 0.05) was associated with increased height among girls. Intake of protein or LYS was not associated with changes in linear growth either in boys or girls. FMI at 9 y: inverse association; high protein (p = 0.01), ARG (p = 0.01), and LYS (p = 0.01) intake was associated with a decrease in body fat gain in girls with a BMI in the 5th percentile. Inverse association between the intake of LYS and change in FMI, only among boys with a BMI in the 5th percentile (p = 0.01). FFMI at 9 y: no significant associations were found between habitual protein intake, ARG or LYS intake, and change in FFMI either in boys or girls. |
Boys: ARG intake: 2.8 ± 0.9 (g/d) LYS intake: 4.5 ± 1.3 (g/d) Girls: ARG intake: 2.4 ± 0.6 (g/d) LYS intake: 4.0 ± 1.1 (g/d) |
| Jen et al., 2018 [33], Generation R Study, The Netherlands | 8 | 3991 | 49.3 | 10 | 61.4 ± 17.1 (g/d) 16.5 ± 2.3 (%E) |
38.1 ± 14.1 (g/d) | NA | 23.3 ± 7.1 (g/d) | BMI at 10 y: positive association; a higher protein intake was associated with a higher BMI (model 3: 0.05 SDS, 95% CI 0.01, 0.09). Weight at 10 y: positive association; a higher protein intake was associated with a higher weight (model 3: 0.08 SDS, 95% CI 0.02, 0.13). Association mainly explained by a higher FFMI (model 3: 0.07 SDS per 5 %E, 95% CI 0.02, 0.11) and not FMI (model 3: 0.03 SDS, 95% CI −0.01, 0.07). |
Both plant and animal proteins were associated with a higher FFMI, but the association was stronger for plant protein (model 3: 0.11 SDS, 95% CI 0.02, 0.21) They observed a trend between higher plant protein intake and lower FMI, which was significant when it was consumed at the expense of animal protein. |
| Maffeis et al., 1998 [56], Italy | 8 | 112 | 51.79 | 12 | 73 ± 16 (g/d) 14.7 ± 1.7 (%E) |
NA | NA | NA | BMI at 12 y: not significant association with protein intake (%E) (p = NS). | |
| van Vught et al., 2009 [54], EYHS, Denmark | 9 | 364 | 44.27 | 14–16 | Boys: 71.7 ± 21.4 (g/d) Girls: 67.8 ± 19.0 (g/d) Total: 70 ± 21 (g/d) |
NA | NA | NA | FMI at 14–16 y: inverse association; high protein (p = 0.03), ARG (p = 0.04), and LYS (p = 0.03) intake was associated with a decrease in body fat gain only in girls with a BMI in the 1–4th (leaner girls). FFMI at 14–16 y: positive association; high protein intake was positively associated with an increase in FFMI gain only among girls with a BMI in the 5th quintile (p = 0.04). Boys: no significant associations were found for protein or for ARG or LYS and FMI or FFMI. |
Boys: ARG intake: 3.0 ± 1.2 (g/d) LYS intake: 4.4 ± 1.8 (g/d) Girls: ARG intake: 2.8 ± 1.0 (g/d) LYS intake: 4.1 ± 1.5 (g/d) |
| Assmann et al., 2013 [50], the DONALD Study, Germany | Boys: 10–15 Girls: 9–14 |
262 | 46.56 | 18–25 | Boys: T1 12.0 (11.3, 12.6) (%E) T2 13.3 (12.7, 13.7) (%E) T3 14.6 (14.0, 15.4) (%E) Girls: T1 11.2 (10.9, 11.8) (%E) T2 12.8 (12.2, 13.4) (%E) T3 14.4 (13.4, 15.2) (%E) |
Boys: T1 7.0 (6.6, 7.5) (%E) T2 8.4 (8.1, 8.8) (%E) T3 10.0 (9.5, 10.6) (%E) Girls: T1 6.4 (5.9, 6.6) (%E) T2 7.9 (7.7, 8.2) (%E) T3 9.6 (9.0, 10.4) (%E) |
Boys: T1 3.4 (2.5, 4.3) (%E) T2 4.2 (3.7, 4.7) (%E) T3 4.8 (3.8, 5.8) (%E) Girls: T1 3.4 (3.0, 3.9) (%E) T2 3.8 (3.1, 4.5) (%E) T3 4.6 (3.6, 5.3) (%E) |
Boys: T1 5.1 (4.6, 5.5) (%E) T2 4.8 (4.2, 5.2) (%E) T3 4.6 (4.1, 4.9) (%E) Girls: T1 5.0 (4.5, 5.5) (%E) T2 4.8 (4.2, 5.3) (%E) T3 4.6 (4.2, 5.1) (%E) |
FMI at 18–25 y: inverse association; a higher animal protein intake during puberty was associated with a lower FMI only in men (p for trend = 0.001). FFMI at 18–25 y: positive association; a higher animal protein intake was associated with a higher FFMI, primarily among women (p for trend = 0.001). Slightly positive association with a higher animal protein in young adult men (p for trend = 0.04). |
There was no significant relationship between dairy protein intake during puberty and FFMI in young adulthood (p for trend = 0.17). Plant protein was not associated with body composition among either sex. Even in the highest energy-adjusted tertile of animal protein intake, protein accounted for less than 15% of energy intake. |
| Joslowski et al., 2013 [51], the DONALD Study, Germany | Boys: 10–15 Girls: 9–14 |
213 | 44.6 | 18–36 | Boys: T1 11.8 ± 1.1 (%E) T2 13.2 ± 0.8 (%E) T3 14.5 ± 0.9 (%E) Girls: T1 11.2 ± 0.9 (%E) T2 12.8 ± 0.8 (%E) T3 14.5 ± 1.2 (%E) |
Boys: T1 7.0 ± 0.9 (%E) 38.4 (g/d) T2 8.3 ± 0.4 (%E) 42.9 (g/d) T3 9.8 ± 0.9 (%E) 49.8 (g/d) Girls: T1 6.2 ± 0.9 (%E) 26.2 (g/d) T2 7.9 ± 0.4 (%E) 32.8 (g/d) T3 9.8 ± 1.0 (%E) 41.6 (g/d) |
Boys: T1 3.5 ± 1.2 (%E) T2 4.4 ± 0.7 (%E) T3 4.6 ± 1.3 (%E) Girls: T1 3.5 ± 0.9 (%E) T2 3.7 ± 1.1 (%E) T3 4.6 ± 1.4 (%E) |
Boys: T1 4.9 ± 0.8 (%E) T2 4.8 ± 0.8 (%E) T3 4.6 ± 0.7 (%E) Girls: T1 5.0 ± 0.7 (%E) T2 4.9 ± 0.7 (%E) T3 4.7 ± 0.7 (%E) |
IGF-I and IGFBP-3 at 18–36 y: positive association; habitually higher animal protein intakes in females during puberty were related to higher IGF-I (p for trend = 0.005) and IGFBP-3 (p for trend = 0.01). IGFBP-2 at 18–36 y: inverse association; habitually higher animal protein intakes in females during puberty were related to lower IGFBP-2 (p for trend = 0.04). |
Animal protein intake in puberty was not related to IGF-I, IGFBP-3, IGFBP-1, or IGFBP-2 in males. In contrast, among males, a habitually higher animal protein intake in early life (0.5–2 years) was associated with lower concentrations of IGF-I in young adulthood. Among females, animal protein intake in early life was not related to IGF-I. Data suggests that, among females, a habitually higher animal protein intake during puberty may precipitate an upregulation of the GH–IGF-I axis. By contrast, higher animal protein intakes in early life may yield a long-term downregulation of the GH–IGF-I axis in males. |
| Koppes et al., 2009 [63], AGAHLS, The Netherlands | 13 | 350 | 48 | 36 | NA | NA | NA | NA | Body fatness at 36 y: positive association; women with high body fatness at the age of 36 years had a significantly higher relative protein intake at ages 13 (p < 0.001), 32 (p < 0.05) and 36 years (p < 0.05). Men with high body fatness at the age of 36 years had a significantly higher relative protein intake at ages 32 (p < 0.05) and 36 years (p < 0.01). |
Inter-period Pearson correlation coefficients are used to express the relative contribution to total energy intake of the four macronutrients. Throughout the 23-year period of follow-up, the relative protein intake in women with high body fatness at the age of 36 years was about 1% higher than in women without high body fatness. |
| Interventional Studies | ||||||||||
| Source |
Study
Design |
Age
(Years) |
Sample Size |
% of
Boys |
Intervention |
Duration of
Intervention |
Baseline Total Protein
Intake |
Final Total Protein
Intake |
Main Outcomes | Observations |
| Thams et al., 2022 [48], NCT03956732 | 2 × 2-factorial randomized controlled trial | 6–8 | 184 | 45.11 | Substitution of 260 g/d milk or yogurt in their diet with: (1) High-protein (HP) yogurt: 10 g protein/100 g (2) Normal-protein (NP) yogurt: 3.5 g protein/100 g |
24 weeks (range: 21–26 weeks) | 15.4 ± 2.4 (%E) |
HP: 18.3 ± 3.4 (%E) NP: 15.9 ± 2.5 (%E) |
The yogurt intervention per se resulted in a lower FMI increase with HP than with NP (p = 0.037). Regression analyses showed a negative dose–response association between changes in dairy protein intake (g/kg body weight/d) and changes in FMI (β: –0.19; 95% CI: –0.33, −0.041 kg/cm2; p = 0.012). |
The expected intake of protein from the yogurts was around 17 g/d higher in HP than NP varieties, corresponding to an ∼25% increase in total protein intake for Danish children. |
Values are means ± SD or median (25th and 75th percentiles). 1 Mean of protein intake values at age 2.3 to 8 y. AGAHLS, Amsterdam Growth and Health Longitudinal Study; ARG, arginine; BF%, Body Fat Percentage; BMI, Body Mass Index; BMI-SDS, Body Mass Index-Standard Deviation Score; CLHNS, The Cebu Longitudinal Health and Nutrition Survey; CoSCIS, Copenhagen School Child Intervention Study; DONALD Study, Dortmund Nutritional and Anthropometrical Longitudinally Designed Study; EYHS, European Youth Heart Study; FSI, Fasting Serum Insulin; HP, High protein; IGFBP, Insulin Growth Factor-Binding Proteins; Insulin-Growth-Factor I; LYS, lysine; NA, Not Available; NP, Normal protein; NS, No Significance; Q, Quartile; SCCNG, Southwest China Childhood Nutrition and Growth; T, Tertile.