This rating was double-checked by a staff member of the German Nutrition Society NK and thereafter reviewed by all co-authors. The final ratings of the overall certainty of evidence were approved by all authors. In total, records were initially identified by literature search.

After the removal of duplicates, records were screened based on title and abstract. We identified potentially eligible records, and eleven SRs were finally considered to be eligible with respect to inclusion and exclusion criteria [ 18 , 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 , 27 , 28 ].

The literature selection process is outlined in the flow diagram shown in Fig. A list of the excluded studies after full-text assessment, including justifications for exclusion, is provided in Supplementary Material S 6. The reason for exclusion was that Wallace et al. Tsagari et al. Table 2 shows the characteristics of the eleven included SRs.

Three were SRs with MA of RCTs [ 21 , 23 , 27 ], two were SRs with MA of cohort studies [ 20 , 24 ], two were SRs of RCTs without MA [ 18 , 22 ], and one was an SR of cohort studies without MA [ 26 ].

One SR with MA [ 28 ] and one without MA [ 25 ] included both RCTs and cohort studies. A further SR with MA included RCTs, cohort, and cross-sectional studies [ 19 ].

The included SRs investigated the following outcomes: fractures [ 19 , 20 , 24 , 25 , 26 , 28 ], BMD [ 18 , 19 , 20 , 21 , 22 , 23 , 25 , 27 , 28 ], bone mineral content BMC [ 20 , 21 ], bone metabolism markers [ 18 , 19 , 20 , 22 , 23 , 26 ], falls [ 25 ], and bone loss [ 25 , 26 ].

animal protein intake [ 22 ]. The intervention period of included RCTs ranged from 38 days to 3 years and follow-up of included cohort studies from 1 to 32 years.

One SR provided no information on follow-up [ 24 ]. One SR was restricted to peri- or postmenopausal women [ 22 ], whereas the other ten SRs included data of both sexes.

Four SRs focused on older adults [ 18 , 20 , 22 , 25 ]. Six SRs were based on adults over 18 years [ 19 , 21 , 23 , 24 , 27 , 28 ] and one on participants aged 14 years or older [ 26 ].

In one SR, health status was not reported [ 24 ]. The other ten SRs were primarily based on a healthy adult population [ 18 , 19 , 20 , 21 , 22 , 23 , 25 , 26 , 27 , 28 ], but some included additionally studies with subjects suffering from sarcopenia, frailty, overweight, obesity, prehypertension, hypertension, hyperlipidemia, or metabolic syndrome.

One SR included exclusively RCTs on participants actively losing weight [ 21 ]. Overall scores of AMSTAR 2 for each included SR are reported in Table 2. Supplementary Material S 7 provides a more detailed overview showing the assessments of each individual item.

Methodological quality was rated as high for five SRs [ 18 , 20 , 24 , 25 , 27 ], moderate for two SRs [ 26 , 28 ], and low for four SRs [ 19 , 21 , 22 , 23 ]. Overall scores of NutriGrade for each SR are summarized in Table 2. Briefly, out of the 57 NutriGrade ratings, 28 were very low, 24 were low, and five were moderate.

Supplementary Material S 8 provides a more detailed account showing the assessments of each individual NutriGrade item.

In SRs of RCTs Table 2 , protein intake ranged from 1. Total protein intake varied largely between single SRs in intervention groups and control groups One SR with MA [ 22 ] compared animal protein vs. Although protein intake between the included SRs varied strongly, even within groups of high and low intakes cohort studies or intervention and control groups RCTs , we tried to answer our research question by comparing high vs.

low protein intake and intervention vs. control groups. All SRs regarding fracture risk were exclusively based on data from observational studies. Four SRs with MA [ 19 , 20 , 24 , 28 ] and two SRs without MA [ 25 , 26 ] reported data on protein intake and total fracture risk.

The vast majority of SRs did not observe an association of high protein intake vs. low protein intake on total fracture risk, neither for total protein intake three out of four SRs nor for plant protein intake three out of three SRs [ 19 , 24 , 26 ]. Two SRs [ 19 , 24 ] observed no association between high vs.

low animal protein intake on total fracture risk, whereas two SRs [ 25 , 26 ] observed a positive association. The two SRs without MA that reported an association between total fracture risk and higher animal protein intake were of high [ 25 ] and moderate [ 26 ] methodological quality; however, both of them included a single cohort study.

With respect to hip fracture risk, three SRs with MA were available [ 20 , 24 , 28 ]. Two of them observed an inverse association between higher protein intake and hip fracture risk [ 20 , 24 ]. Both SRs were of high methodological quality and were based on a higher number of individual studies than the SR by Darling et al.

Groenendijk et al. The SR by Wu et al. In addition, Wu et al. explored a possible dose-response relationship between the amount of daily protein intake within a daily range of 45 to g protein and hip fracture risk, using data of three sub-studies which met dose-response meta-analysis criteria.

Although statistically non-significant, results were generally consistent with their data on low vs. high protein intake. Neither higher intakes of plant nor of animal protein were associated with hip fracture risk in two SRs [ 24 , 28 ].

Altogether, two out of three SRs reported consistently an inverse association between total protein intake and the risk of hip fractures. Thus, there is possible evidence for a decrease in hip fracture risk for higher vs. lower total protein intake. None of the SRs observed an association between animal or plant protein intake and hip fracture risk.

One SR with MA reported data on protein intake and limb fracture risk in two cohort studies [ 24 ]. Wu et al. Five SRs with MA [ 19 , 21 , 23 , 27 , 28 ] and four SRs without MA [ 18 , 20 , 22 , 25 ] reported data on BMD at different skeletal sites Table 2.

None of the SRs that examined the relations between total protein intake and total body BMD [ 20 , 21 , 25 , 27 ] or total hip BMD [ 20 , 21 , 23 , 27 ], respectively, found an association cohort studies [ 20 ] or effect intervention studies [ 21 , 25 , 27 ].

Regarding lumbar spine BMD, three out of six SRs including in total seven RCTs reported null effects of higher protein intake [ 19 , 27 , 28 ]. One SR of cohorts did not show any consistent results [ 20 ], and the other two SRs reported a statistically significant higher lumbar spine BMD by a higher protein intake [ 21 , 23 ].

Wright et al. normal protein diet [ 21 ]. Lumbar spine BMD was statistically significant and consistently, yet modest, increased by high protein diet. The SR by Shams-White et al. summarized the effect of high vs. Higher protein intake statistically significantly increased lumbar spine BMD without evidence for heterogeneity.

With respect to femoral neck BMD, the vast majority of SRs three out of four reported null effects of high vs. One SR of six cohort studies did not observe consistent results [ 20 ]. Regarding specific protein sources, Blair et al.

None of the included RCTs found statistically significant differences between both protein sources in the net changes in lumbar spine, femoral neck, or total body BMD.

There was one SR with MA of RCTs [ 21 ] and one SR without MA of cohort studies [ 20 ] on protein intake and total body BMC. One cohort study observed no association of high vs.

low total protein intake with total body BMC, whereas the other cohort study observed a positive association. The SR by Wright et al. The majority of included SRs reached neither a moderate methodological quality nor a low certainty of evidence.

Due to the low methodological quality, the overall certainty of evidence that the amount of protein intake does influence femoral neck and lumbar spine BMC was considered to be insufficient. Markers of bone formation, such as serum osteocalcin and bone-specific alkaline phosphatase BAP , as well as markers of bone resorption, such as N-terminal telopeptide NTX and C-terminal telopeptide CTX , were investigated in five SRs of RCTs, two of them with MA [ 19 , 23 ] and three without MA [ 18 , 20 , 22 ].

did not demonstrate a statistically significant effect of total protein supplementation on serum osteocalcin [ 23 ].

Furthermore, both cohort studies included in the SR by Groenendijk et al. showed no association between total protein intake and osteocalcin [ 20 ]. Blair et al. Changes in BAP were investigated in two SRs [ 19 , 22 ].

Darling et al. compared the effect of soy vs. animal protein on BAP in peri- and postmenopausal women, but did not find statistically significant treatment effects [ 22 ]. Furthermore, Shams-White et al.

examined the effect of soy vs. animal protein on NTX two RCTs with 91 participants [ 22 ]. Due to the low methodological quality of the SR by Shams-White et al. The reason for this rating was the high methodological quality of the SR by Groenendijk et al.

Single SRs without MA reported data on bone loss [ 25 , 26 ] or falls [ 25 ]. None of the two SRs found consistent results on the relationship between protein intake and bone loss, either for total [ 25 , 26 ], animal [ 25 ], or plant protein [ 25 ].

Pedersen et al. included a single cohort study of older adults to examine the association between protein intake and risk of falls [ 25 ]. This cohort study did not report any statistically significant associations between total, animal, or plant protein and the risk of falls.

This umbrella review summarizes the results of several SRs on various parameters of bone health such as biomarkers of bone metabolism, total and site-specific BMD, and fracture risk. To the best of our knowledge, this umbrella review is the first to provide a summary evidence assessment of previous SRs.

Osteoporotic fractures are the most important outcomes of impaired bone metabolism. Our results indicate that a beneficial effect of a protein intake above the recommendation 1.

The SRs on hip fracture risk included a substantial percentage of elderly people, an age group that is known for an exponential increase in the risk of fractures [ 31 ], particularly in nursing home residents [ 32 ].

As a higher protein intake may have beneficial effects on skeletal muscle [ 14 ], we cannot exclude the possibility that the beneficial effect of a higher protein intake on hip fracture risk reduction supported by three SRs with MA identified here may be explained by beneficial effects on skeletal muscle [ 33 ].

The results on hip fracture risk obtained from SRs of observational studies are in line with the results of a secondary prevention trial in older patients with recent osteoporotic hip fracture [ 34 ]. This study could demonstrate that a daily protein supplementation of 20 g vs.

an isoenergetic placebo attenuates proximal femur bone loss and reduces in-hospital stay in rehabilitation care facilities. At baseline, the protein-supplemented group of that RCT had a daily protein intake of 45 g on average, corresponding to 0.

In this context, it is notable that in community-dwelling older adults, the prevalence of a protein intake below 0. The situation seems to be even worse in nursing home residents, where a mean daily protein intake of only 0. Thus, the high risk of hip fractures in older adults, and particularly in nursing home residents, may, at least in part, be increased by a protein intake below the current recommendation.

Since guidelines from expert consensus groups, such as the European Society on Parenteral and Enteral Nutrition ESPEN , already advocate a higher intake of protein than currently recommended 1. Generally, the evaluation of the effect of protein intake on the risk of fractures is challenging for several reasons: First, it may take years or even decades until a nutrition-related fracture occurs, but it is nearly impossible to perform long-term RCTs regarding the effect of different intakes of a macronutrient like protein on bone health.

This explains why only data of observational studies are available regarding protein intake and fracture risk, where under- and overreporting of specific foods has to be considered as this may affect dose-response analysis on protein intake and fracture risk.

Second, there may be interactions between protein intake, calcium intake, and physical activity [ 3 , 39 , 40 ], and protein-rich foods, such as meat, milk, or soy, contain many other nutrients, which makes it difficult to separate a potential protein-related effect from the effect of other nutrients.

Third, even multivariable-adjusted prospective cohort studies may be biased by unexplained confounding factors not related to nutrition. Finally, low-trauma fractures, which are typical in osteoporotic individuals, are rarely seen in young and middle-aged adults, who were important target populations of this umbrella review.

SRs on BMD are at the interface between studies on fracture as outcome and studies on bone turnover markers, since BMD is linked to bone strength [ 1 ] and thus to fracture risk [ 41 ]. Studies on BMD have the advantage that substantial effects can be demonstrated already after several months or 1 or 2 years, making even RCTs possible.

Nevertheless, evidence from available SRs for an effect of the amount of protein intake on BMD remains insufficient. Results on biochemical parameters of bone formation and resorption reflect short- to mid-term bone health.

Theoretically, dietary protein may have anabolic effects on skeletal muscle or bone protein synthesis, but it may also adversely increase bone resorption by its calciuretic effect [ 42 , 43 ], particularly if animal protein with its relatively high content of sulfur-containing amino acids is ingested.

With respect to the type of protein intake, a large prospective study in elderly women showed that a higher intake of animal vs. plant protein was associated with a more rapid femoral neck bone loss and a higher risk of hip fracture [ 44 ]. According to the acid-base hypothesis, skeletal salts are mobilized from bone to balance acids endogenously generated from sulfur-containing, acid-forming amino acid, which are more prevalent in animal than in plant protein [ 45 ].

However, this hypothesis was challenged by the results of a recently published RCT, demonstrating an increased bone turnover among healthy adults by partial replacement of animal by plant protein [ 46 ].

Our umbrella review does neither reveal beneficial nor adverse effects on bone turnover markers by protein supplementation. In this regard, soy and animal protein did not differ substantially.

In line with these findings, some have argued that the calciuretic effect of protein may be compensated by increased intestinal calcium absorption rather than bone loss [ 42 , 43 ]. We need to point out that the quality of SRs available to date has been limited, especially at the RCT level.

Particularly, the quality of the SRs with MA on protein intake and BMD was only low to very low [ 22 , 28 ], with the exception of the SR with MA on high protein weight loss diets [ 21 ], which was of moderate quality. A further major limitation is that most SRs with MA were not restricted to specific risk groups, such as older adults whose risk of fracture and of inadequate energy and protein intake is high, and whose requirement on daily protein intake is probably higher than currently assumed.

In addition, there was a wide and overlapping range of protein intake between groups with low and high protein intakes in different SRs and its underlying cohorts or RCTs, thus hampering the detection of clear dose-response relationships.

Finally, it may be not clear why a classical GRADE assessment instead of NutriGrade was not performed. We are aware that in the meantime, the GRADE approach was amended in a way that cohort studies can now also be assigned an initially high score, when risk of bias tools such as ROBINS-I are used [ 47 ].

However, the adjustments were not published until , whereas the guideline methodology for our umbrella review was established in Overall, available data regarding the impact of protein intake on bone health from SRs are insufficient to draw reliable conclusions for the general adult population.

Since osteoporotic fractures increase exponentially with higher age [ 31 ], and guidelines from expert consensus groups, such as the European Society on Parenteral and Enteral Nutrition ESPEN , already advocate a higher intake of protein than currently recommended 1.

In addition, more high-quality research regarding the effect of dose and type of protein on bone health in the entire adult population is needed. Turner CH Bone strength: current concepts. Ann N Y Acad Sci — Article PubMed Google Scholar.

Hillier TA, Stone KL, Bauer DC et al Evaluating the value of repeat bone mineral density measurement and prediction of fractures in older women: the study of osteoporotic fractures.

Arch Intern Med — Chevalley T, Bonjour JP, Ferrari S et al High-protein intake enhances the positive impact of physical activity on BMC in prepubertal boys. J Bone Miner Res — Article CAS PubMed Google Scholar. Olaniyan ET, O'Halloran F, McCarthy AL Dietary protein considerations for muscle protein synthesis and muscle mass preservation in older adults.

Nutr Res Rev — Bischoff-Ferrari HA Chapter Prevention of falls. In: Bilezikian JP, Bouillon R, Clemens T et al eds Primer on the metabolic bone diseases and disorders of mineral metabolism. Wiley, pp — Chapter Google Scholar. Schiessl H, Frost HM, Jee WS Estrogen and bone-muscle strength and mass relationships.

Bone —6. Scheld K, Zittermann A, Heer M et al Nitrogen metabolism and bone metabolism markers in healthy adults during 16 weeks of bed rest. Clin Chem — Bonjour J-P The dietary protein, IGF-I, skeletal health axis. Horm Mol Biol Clin Investig — Bonjour JP, Ammann P, Chevalley T et al Protein intake and bone growth.

Can J Appl Physiol 26 Suppl :S—S Sugawara K, Takahashi H, Kashiwagura T et al Effect of anti-inflammatory supplementation with whey peptide and exercise therapy in patients with COPD. Respir Med — Takeda S, Kobayashi Y, Park J-H et al Effect of different intake levels of dietary protein and physical exercise on bone mineral density and bone strength in growing male rats.

J Nutr Sci Vitaminol — Chevalley T, Bonjour J-P, Audet M-C et al Prepubertal impact of protein intake and physical activity on weight-bearing peak bone mass and strength in males. J Clin Endocrinol Metab — Richter M, Baerlocher K, Bauer JM et al Revised reference values for the intake of protein.

Ann Nutr Metab — Kirk B, Prokopidis K, Duque G Nutrients to mitigate osteosarcopenia: the role of protein, vitamin D and calcium. Curr Opin Clin Nutr Metab Care — Kroke A, Schmidt A, Amini AM et al Dietary protein intake and health-related outcomes: a methodological protocol for the evidence evaluation and the outline of an evidence to decision framework underlying the evidence-based guideline of the German Nutrition Society.

Eur J Nutr — Article CAS PubMed PubMed Central Google Scholar. Shea BJ, Reeves BC, Wells G et al AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both.

BMJ j Article PubMed PubMed Central Google Scholar. Schwingshackl L, Knüppel S, Schwedhelm C et al Perspective: NutriGrade: a scoring system to assess and judge the meta-evidence of randomized controlled trials and cohort studies in nutrition research.

Adv Nutr — Nutrients Darling AL, Manders RJF, Sahni S et al Dietary protein and bone health across the life-course: an updated systematic review and meta-analysis over 40 years. Osteoporos Int — Groenendijk I, den Boeft L, van Loon LJ et al High versus low dietary protein intake and bone health in older adults: a systematic review and meta-analysis.

Comput Struct Biotechnol J — Wright CS, Li J, Campbell WW Effects of dietary protein quantity on bone quantity following weight loss: a systematic review and meta-analysis.

Shams-White MM, Chung M, Fu Z et al Animal versus plant protein and adult bone health: a systematic review and meta-analysis from the National Osteoporosis Foundation. PLoS One e Shams-White MM, Chung M, Du M et al Dietary protein and bone health: a systematic review and meta-analysis from the National Osteoporosis Foundation.

Am J Clin Nutr — Wu A-M, Sun X-L, Lv Q-B et al The relationship between dietary protein consumption and risk of fracture: a subgroup and dose-response meta-analysis of prospective cohort studies.

Sci Rep Pedersen AN, Cederholm T Health effects of protein intake in healthy elderly populations: a systematic literature review. Food Nutr Res Pedersen AN, Kondrup J, Børsheim E Health effects of protein intake in healthy adults: a systematic literature review.

Santesso N, Akl EA, Bianchi M et al Effects of higher- versus lower-protein diets on health outcomes: a systematic review and meta-analysis. Eur J Clin Nutr — Darling AL, Millward DJ, Torgerson DJ et al Dietary protein and bone health: a systematic review and meta-analysis.

Wallace TC, Frankenfeld CL Dietary protein intake above the current RDA and bone health: a systematic review and meta-analysis. J Am Coll Nutr — Tsagari A Dietary protein intake and bone health. J Frailty Sarcopenia Falls —5.

Hadji P, Klein S, Gothe H et al The epidemiology of osteoporosis--bone evaluation study BEST : an analysis of routine health insurance data. Dtsch Arztebl Int — Sawka AM, Ismaila N, Cranney A et al A scoping review of strategies for the prevention of hip fracture in elderly nursing home residents.

PLoS One 5:e Sahni S, Cupples LA, McLean R et al Protective effect of high protein and calcium intake on the risk of hip fracture in the Framingham offspring cohort. J Bone Miner Res, Wiley, New Jersey, USA.

But did you know protein is an essential building block of healthy bones, too? On the contrary, a diet rich in protein is a powerful weapon for strengthening bones. A growing body of research proposes older women, in particular, experience improved bone density when they consume higher quantities of protein i.

Similar findings were made in a six-year observational study where , postmenopausal women were assessed ii. Scientists concluded higher protein intake was associated with significantly better bone density in the hip, spine, and total body, and a decreased risk of fractures in the forearm.

Learn more about how to maintain bone health after the menopause here. Diets that receive more calories from protein are also thought to preserve and protect bone mass during weight loss. This can be seen in one randomised, controlled trial in which women who ate 86 grams protein every day on a calorie-restricted regimen lost less bone mass from their spine, arm, hip and leg areas than their female counterparts who consumed 60 grams of protein each day iii.

Convinced yet? Thought so. Proponents of this theory believe protein spikes the acid load of your body, thereby inciting the body to leach calcium from the bones in order to neutralise it iv. And though, admittedly, there are some studies substantiating this claim, they reveal high-protein consumption only triggers short-term calcium excretion — not long term v.

In actuality, longer-term studies are wholly against this idea. Indeed, a systematic review and meta-analysis published in established that high protein intake is not a detriment to bone health. If anything, a raft of data points to increased protein consumption supporting bones vii. In the UK, adults are advised to eat 0.

Generally speaking, men should aim for 55 grams and women 45 grams of protein daily. That translates to two palm-sized servings of fish, meat, tofu, pulses, or nuts. Where possible, try to include protein with every meal.

Lean meat, poultry, fish, milk, yoghurt, and eggs are all rich sources of animal-based protein. In particular, back off the bacon. Processed meats are crammed with preservatives and salt, which conspire to hijack your bone health and your overall wellbeing. Plus, cutting down on your animal protein consumption means you can do your bit for the environment every little counts, right?

Roasted chicken breast: 53 grams of protein 1 can of tuna: 39 grams of protein grams of cottage cheese: 27 grams of protein 85g of cooked beef: 22 gram of protein g of Greek yoghurt: 17 grams of protein 1 large egg: 6 grams of protein. Tempeh, tofu, lentils, quinoa, beans, oats, and chia seeds are also brimming with bone-supporting protein.

If you eat an array of protein sources every day, you should, theoretically, get your dose of all the amino acids. But if you want to fast track your amino acid intake, it can be helpful to combine whole grains with legumes because they complement each other and deliver all of the essential amino acids.

Black beans and rice or whole wheat bread and peanut butter are great examples. Amaranth, quinoa, chia seeds , hempseed, and soya are the exceptions to the rule, containing all the essential amino acids. Pack these into your diet and your amino acid needs will be met every day.