Table 2.
Animal-derived proteins: effects on bone in relation to age, exercise, energy restriction and source.
| Reference | Study Design | Protein Composition | Measurements | Key Outcomes |
|---|---|---|---|---|
| Hannan et al., 2000 [86] | 615 older adults (75 ± 4.4 years, 391 females (F), 224 males (M) (mean ± standard deviation (SD)) Relationship between dietary protein and subsequent 4-year change in bone health |
Protein type/intake determined through food frequency questionnaire | Protein intake, bone mineral density (BMD) | Lower protein intake associated with increased bone loss Higher intake of animal protein not associated with decrease in BMD |
| Roughead et al., 2003 [87] | Randomised crossover design Healthy postmenopausal F (n = 15, 60.5 ± 7.8 years) randomised to 8-week high-meat and 8-week low-meat diet (mean ± SD) |
High-meat diet: 20% of energy as protein Low-meat diet: 12% of energy as protein Calcium content similar (~600 mg) in both diets |
Calcium excretion, bone markers, dietary analysis | High-meat diet did not adversely affect urinary calcium excretion, calcium retention or markers of bone metabolism |
| Cao et al., 2011 [88] | Randomised crossover design Postmenopausal F (n = 16, 56.9 ± 3.2 years, mean ± SD) randomised to two diets: low protein, low potential renal acid load (PRAL) and high protein, high PRAL diet. |
Low protein, low PRAL diet: 10% of energy as protein High protein, high PRAL diet: 20% of energy as protein Each diet was 7 weeks separated by 1 week |
Calcium absorption, bone markers, dietary analysis | No effect of high meat/PRAL diet on markers of bone metabolism Increased fractional rate of calcium absorption and urinary calcium excretion |
| Durosier-Izart et al., 2017 [82] | Cross-sectional study design 746 F (65 ± 1.4 years, mean ± SD) Associations between animal (separated into non-dairy and dairy) and vegetable protein sources and bone health |
Protein type/intake determined through food frequency questionnaire | Areal BMD, distal radius and tibia bone microstructures, bone strength, protein intake | Predicted failure load and stiffness at distal radius and tibia positively associated with total, animal and dairy protein intake |
| Langsetmo et al., 2018 [25] | Cross-sectional study design Questionnaire data from 1016 M (84.3 ± 4 years, mean ± SD) Association of dairy, non-dairy and plant-derived protein intake on bone health |
Protein type/intake determined through food frequency questionnaire | Bone strength, BMD, protein intake | Higher dairy protein associated with higher estimated failure load at the distal radius and distal tibia Higher non-dairy animal protein associated with higher total BMD |
| Ballard et al., 2006 [89] | Randomised controlled trial 51 younger adults (18–25 years, 28 M, 23 F) were randomised to either protein (20.9 ± 2.4 years) or placebo (21.1 ± 2.2 years) supplementation during a 6-month training intervention of alternating resistance exercise training (RET) and aerobic exercise 5 ×/week (mean ± standard error of the mean (SEM)) |
Twice daily protein (42 g protein, 24 g carbohydrate (CHO), 2 g fat) Isocaloric CHO supplement (70 g CHO) |
Bone markers, protein intake | Increases in plasma insulin-like growth factor-I greater in protein group Serum bone alkaline phosphatase increased over time and tended to be higher in protein group N-terminal telopeptide concentrations greater in protein group |
| Mullins & Sinning, 2005 [90] | Randomised, double-blind, placebo-controlled design 24 healthy, untrained, young adult F (18–29 years) engaged in 12-week RET 3 d/week and were randomised to protein (22.8 ± 0.9 years) or placebo (22.7 ± 1.1 years) during the final 10 days (mean ± SEM) |
High-protein diet (during final 10 days): purified whey protein for daily protein intake of 2.4 g/kg/d Control: equivalent dose of isoenergetic CHO |
Bone markers, dietary analysis | High protein intake for final 10 days of RET had no effects on bone metabolism |
| Holm et al., 2008 [91] | Randomised, double-blind, placebo-controlled design Postmenopausal F were randomised to a protein-containing nutrient supplement (n = 13, 55 ± 1 years) or placebo (n = 16, 55 ± 1 years) in conjunction with 24-week RET (mean ± SEM) |
Nutrient supplement containing: 10 g whey protein, 31 g CHO, 1 g fat, 250 mg calcium and 5 µg vitamin D. 730 kJ in total. Placebo supplement containing: 6 g CHO and 12 mg calcium. 102 kJ in total. Supplements were consumed after each training session |
BMD, bone markers, dietary analysis | Nutrient group had greater increase in BMD at the femoral neck than controls Increased bone formation and osteocalcin following training in nutrient group |
| Wright et al., 2017 [92] | Randomised, double-blind, placebo-controlled design Obese/overweight adults were randomised to 0 g protein (n = 68, 50 ± 7 years) 20 g protein (n = 72, 48 ± 8 years) or ≥40 g protein (n = 46, 49 ± 8 years) combined with 36-week RET and aerobic exercise training 3 d/week for 36 weeks (mean ± SD) |
Unrestricted diet in combination with whey protein supplementation (0, 20, 40 or 60 g/d) (40 and 60 g group combined to form a ≥40 g group for analysis) |
BMD, bone mineral content (BMC), protein intake | Whey protein, regardless of dose, had no effect on BMD or BMC during training |
| Farnsworth et al., 2003 [93] | Parallel design 57 overweight adults randomised to either high protein (M n = 7 51.9 ± 3.3 years, F n = 21, 50.6 ± 2.7 years) or standard protein (M n = 7 48.6 ± 3.2 years, F n = 22, 50.6 ± 2.1 years) diet during 12 weeks of energy restriction and 4 weeks of energy balance (mean ± SEM) |
High-protein diet of meat, poultry and dairy foods (27% of energy as protein, 44% as CHO, and 29% as fat) Standard protein diet low in those foods (16% of energy as protein, 57% as CHO, and 27% as fat) Diets during 12 weeks of energy restriction (6–6.3 MJ/d) and 4 weeks of energy balance (≈8.2 MJ/d) |
Calcium excretion, bone markers, dietary analysis | Markers of bone turnover and calcium excretion unchanged between diet groups |
| Bowen et al., 2004 [3] | Randomised study design Overweight adults were randomly assigned to isoenergetic diets high in dairy protein (M 49.4 ± 3.2 years, F 46.5 ± 2.4 years) or mixed source protein (M 48.7 ± 4.2 years, F 46.1 ± 2.7 years) during 12 weeks of energy restriction and 4 weeks of energy balance (mean ± SEM) |
Isoenergetic diets (34% of energy as protein) high in either dairy protein (~2400 mg calcium/d) or mixed protein sources (~500 mg calcium/d) | Calcium excretion, bone markers, dietary analysis | Urinary calcium excretion decreased independently of diet Greater increase in bone resorption marker deoxypyridinoline with mixed protein Increased osteocalcin in mixed protein group |
| Josse et al., 2012 [94] | Randomised, controlled, parallel intervention design Premenopausal overweight and obese F were randomised into high protein/high dairy (30 ± 1 years), adequate protein/medium dairy (26 ± 1 years) or adequate protein/low dairy protein (28 ± 1 years) (mean ± SEM) |
High protein/high dairy: dietary protein (30% of energy), dairy foods (15% energy from protein) and dietary calcium (~1600 mg/d) Adequate protein/medium dairy: dietary protein (15% of energy), dairy foods (7.5% energy from protein) and dietary calcium (~1000 mg/d) Adequate protein/low dairy: dietary protein (15% of energy), dairy foods (<2% energy from protein) and dietary calcium (<500 mg/d) |
Bone markers | With low dairy, C-terminal telopeptide of collagen type-I, urinary deoxypyridinoline and osteocalcin increased With high dairy, osteocalcin, amino-terminal propeptide of collagen I increased with resorption markers unchanged |
Abbreviations: BMC, bone mineral content; BMD, bone mineral density; CHO, carbohydrate; F, females; M, males; PRAL, potential renal acid load; RET, resistance exercise training; SD, standard deviation; SEM, standard error of the mean.