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Dietary Recommendations in the Prevention and Treatment of
Osteoporosis
Emmanuel Biver Julia Herrou Guillaume Larid M′elanie A Legrand
Sara Gonnelli C′edric Annweiler Roland Chapurlat V′eronique
Coxam Patrice Fardellone Thierry Thomas Jean-Michel Lecerf
Bernard Cortet Julien Paccou
PII: S1297-319X(22)00181-6
DOI: https://doi.org/doi:10.1016/j.jbspin.2022.105521
Reference: BONSOI 105521
To appear in: Joint Bone Spine
Received Date: 23 September 2022
Revised Date: 1 December 2022
Accepted Date: 9 December 2022
Please cite this article as: Biver E, Herrou J, Larid G, Legrand MA, Gonnelli S, Annweiler C,
Chapurlat R, Coxam V, Fardellone P, Thomas T, Lecerf J-Michel, Cortet B, Paccou J, Dietary
Recommendations in the Prevention and Treatment of Osteoporosis, Joint Bone Spine
(2022), doi: https://doi.org/10.1016/j.jbspin.2022.105521
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? 2022 Published by Elsevier.
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Dietary Recommendations in the Prevention and Treatment of
Osteoporosis
Emmanuel Biver?, Julia Herrou?, Guillaume Larid?, Mélanie A Legrand?, Sara
Gonnelli?, Cédric Annweiler?, Roland Chapurlat?, Véronique Coxam?, Patrice
Fardellone?, Thierry Thomas?, Jean-Michel Lecerf?, Bernard Cortet?, Julien Paccou?
? Service of Bone Diseases, Geneva University Hospitals and Faculty of Medicine, Geneva,
Switzerland.
? Inserm U 1153, Université de Paris, AP-HP Centre, H?pital Cochin, Service de
rhumatologie, Paris, France.
? Rheumatology Department, University Hospital of Poitiers, CHU de Poitiers, 2 Rue de la
Milétrie, 86021, Poitiers, France.
? Department of Rheumatology, Edouard Herriot University Hospital, 5, Place d''Arsonval,
69003 Lyon, France; INSERM UMR 1033, Université de Lyon, Lyon, France.
? Department of Rheumatology, Cochin Hospital, Assistance Publique - H?pitaux de Paris
Centre, Institut National de la Santé et de la Recherche Médicale (INSERM) Unités Mixtes de
Recherche (UMR) 1153, Université de Paris, Paris, France.
? Department of Geriatric Medicine and Memory Clinic, Research Center on Autonomy and
Longevity, University Hospital, Angers, France.
? Unité de Nutrition Humaine (UNH), INRA/Université Clermont Auvergne, 63009
Clermont-Ferrand, France.
? Department of Rheumatology, CHU Amiens, Unité EA MP3CV, Amiens, France.
? Department of Rheumatology, H?pital Nord, Centre Hospitalier Universitaire (CHU) Saint-
Etienne, INSERM U1059, Lyon University, Saint-Etienne, France.
? Department of Nutrition and Physical Activity, Institut Pasteur de Lille, Lille, France.
? Univ. Lille, CHU Lille, MABlab ULR 4490, Department of Rheumatology, F-59000 Lille,
France.
Corresponding author:
Julien Paccou, Department of Rheumatology, Lille University Hospital, Lille, France
Email: julien.paccou@chru-lille.fr
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Highlights
? This is the first set of dietary recommendations in the prevention and treatment of
Osteoporosis.
? These recommendations were established by a multidisciplinary working group and
resulted in 15 questions and recommendations pertaining to "daily practices".
? A Mediterranean-type diet and the daily consumption of 2 to 3 dairy products are
recommended.
? Conversely, unbalanced Western diets, vegan diets, weight-loss diets in non-
overweight individuals, alcohol consumption and daily consumption of sodas are
advised against.
Abstract
Introduction: This article presents the initial recommendations of the French Rheumatology
Society (Société Fran?aise de Rhumatologie – SFR) and the Osteoporosis Research and
Information Group (Groupe de Recherche et d’Informations sur les Ostéoporoses – GRIO) on
the role of diet in the prevention and treatment of osteoporosis.
Methods: The recommendations were produced by a working group composed of
rheumatologists, physician nutrition specialists and a geriatrician. Fifteen (15) questions
pertaining to "daily practices" were preselected by the working group. For the literature
review, the working group focussed mainly on the effects of diet on bone mineral density
(BMD) and fractures, and primarily on meta-analyses of longitudinal studies and dietary
intervention studies.
Results: A Mediterranean-type diet and the daily consumption of 2 to 3 dairy products are
recommended. Together, these provide the calcium and "high quality" protein required to
maintain a normal calcium-phosphorus balance and bone metabolism, and are associated with
lower fracture risk. Conversely, unbalanced Western diets, vegan diets, weight-loss diets in
non-overweight individuals, alcohol consumption and daily consumption of sodas are advised
against. In terms of the beneficial effects on bone mineral density and fracture risk, current
scientific data are either insufficient or too divergent to recommend increasing or restricting
the consumption of tea or coffee, vitamins other than vitamin D, vitamin D-enriched or
phytoestrogen-rich foods, calcium-enriched plant-based beverages, oral nutritional
supplements, or dietary sources of prebiotics and probiotics.
Conclusions: These are the first set of recommendations addressing the role of diet in the
prevention and treatment of osteoporosis. More research is necessary to direct and support
guidelines.
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Keywords: Nutrition, diet, bone mineral density, osteoporosis, fractures
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1. Introduction
Dietary considerations are common among patients with osteoporosis. Additionally, a
balanced diet is a major determinant of bone health. With the progress of scientific knowledge
and changes in dietary habits – often influenced by contradictory messages that are a mixed
bag of myths and actual scientific data –, new questions are emerging.
Nowadays, patients want more detailed information on the role of diet and diet regimens in
the prevention and management of osteoporosis.
We have therefore drawn up a list of recommendations for healthcare professionals,
addressing the role of diet in the prevention and treatment of osteoporosis. The proposed
recommendations were produced with the support of the French Rheumatology Society
(SFR), the Osteoporosis Research and Information Group (GRIO) and experts in nutrition.
2. Objectives and methods
This initial set of recommendations is intended for healthcare professionals who see patients
with queries on the role of nutrition in the prevention and treatment of osteoporosis. The
recommendations were drawn up by a working group set up by the SFR and the GRIO,
comprising 6 senior rheumatologists, 4 junior rheumatologists, 2 experts in nutrition and 1
geriatrician, who met on several occasions for that specific purpose. The recommendations
are based on a shortlist of 15 practical questions selected by the working group and a partner
patient from among those that are most frequently raised by patients. Four (4) groups were
formed to respond to the 15 questions (3 or 4 questions per group), and a junior
rheumatologist, acting under the supervision of 2 or 3 senior rheumatologists, was assigned to
each group. Two (2) Study Coordinators (EB and JP) coordinated the groups'' work and
drafted the final version of the recommendations. The bibliographic research was conducted
by the 4 junior rheumatologists and the articles they compiled were reviewed with their senior
counterparts with a view to selecting the most relevant literature addressing the questions
raised. The literature review focussed primarily on the body of meta-analyses of observational
studies, and the rare intervention studies with BMD or fracture data addressing the questions
of interest. Several joint meetings were then organised with the groups to discuss and validate
the selected literature. Each group then drafted the questions before submitting them to the
working group for review. When several meta-analyses on the same topic were found, all of
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them were taken into account in the recommendations and/or summarised in a table showing
the fracture data. When the data in the literature were found to be lacking, the
recommendations were based on the level of professional consensus, considering current
practices and experts’ opinions. The recommendations were graded based on the level of
evidence of the literature, in accordance with the methodology proposed by the French
National Authority for Health (Haute Autorité de Santé - HAS) [1].
The recommendations were then reviewed by a multidisciplinary reading committee
composed of rheumatologists, experts in nutrition, a dietician and a geriatrician. Their
comments were taken into account in drafting the final version of the recommendations. The
members of the working group then voted on each recommendation in the final version, using
a scale ranging from 0 (totally disagree) to 10 (fully agree).
These recommendations are not meant to cover all specific cases, or to relieve physicians of
their responsibility to their patients.
3. Results
3.1. What are the expected benefits of the Mediterranean diet for
bone health?
Traditionally, the Mediterranean diet is composed mainly of fruit and vegetables, legumes,
cereals and olive oil. Dairy products – mainly fermented – are consumed daily (once or twice
a day), fish at least twice a week, and meat only occasionally. The Mediterranean diet is rich
in antioxidant micronutrients, vitamins C and E, carotenoids and polyphenols, and sometimes
Omega-3 fatty acids. This diet has been associated with a wide range of benefits for
cardiovascular health and its related risk factors, including obesity, hypertension, metabolic
syndrome, dyslipidaemia and diabetes. It is also associated with less age-related cognitive
dysfunction and lower incidence of neurodegenerative disorders [2]. Regarding bone health, a
meta-analysis reported a positive association between high adherence to the Mediterranean
diet (vs. low adherence) and BMD at the lumbar spine (mean difference (MD=0.12 g/cm2,
CI95%=0.06–0.19), femoral neck (MD=0.10 g/cm2, CI95%=0.06–0.15) and total hip
(MD=0.11 g/cm2, CI95%=0.09–0.14) in men and women aged 20 to 79 years [3]. Recent
publications have all reported a positive association between Mediterranean diet adherence
scores and lower risk of hip fractures in men and women (Table 1) [3-10].
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Conversely, in another meta-analysis, a Western-type diet – which is rich in red meat, refined
foods, sugar-sweetened drinks and processed foods – was found to be associated with lower
BMD and higher fracture risk compared to the Mediterranean diet (Table 1) [7].
Recommendation [B – scientific assumption]
A Mediterranean-type diet is associated with better bone health. It is therefore
recommended for patients with osteoporosis, or in the prevention of osteoporosis.
3.2. Are vegetarian and vegan diets harmful to bone health?
Restrictive diets are, by definition, diets that exclude certain types of food. Currently, the
most popular restrictive diets are vegetarian diets – which exclude all animal products – and
vegan diets – which exclude all animal products, plus honey, as well as the use of non-dietary
animal products (e.g., leather, wool, and silk). Vegan diets are poor in calcium, proteins and
micronutrients, such as vitamins B2, B3, B12 and D, iodine, zinc, potassium and selenium
[11]. Vegetarian diets exclude all animal flesh (meat, fish), but not eggs and dairy products.
In a meta-analysis, lower lumbar spine and femoral neck BMD values were reported in
vegetarians and vegans compared to omnivores (e.g., at the lumbar spine, in vegans, MD=-
0.070 g/cm2, CI95%=-0.116, -0.025, and in vegetarians, MD=-0.023 g/cm2, CI95=-0.035, -
0.010 [8]. In that same study, lumbar spine and femoral neck BMDs were found to be lower
in vegans than in vegetarians. Lastly, fracture risk was 44% higher in vegans than in
omnivores. A 25% increase in fracture risk was also observed in vegetarians, but the
association was not statistically significant (Table 1) [8]. It is important to point out that, in
that meta-analysis, no adjustments were made for weight, or calcium or protein intake.
In the EPIC-Oxford cohort, after adjusting for calcium and protein intake, only vegans
exhibited an increase in fracture risk – especially at the hip – compared to omnivores (fracture
risk multiplied by 2.31) [9]. In the Adventist Health 2 cohort, only vegan women exhibited a
55% increase in fracture risk at the hip, but this heightened risk was not observed in vegan
women on calcium supplementation alone or combined with vitamin D (Table 1) [10].
Recommendation [B – scientific assumption]
Vegan diets, and to a lesser extent, vegetarian diets, are associated with poorer bone health.
Vegan diets should therefore be avoided in patients with osteoporosis, or in the prevention
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of osteoporosis. In vegans, an adjustment of calcium intake should be systematically
proposed.
3.3. How do voluntary weight-loss diets affect bone health?
The purpose of weight-loss diets is to induce weight loss by restricting daily calorie intake
(CR, calorie restriction).
The main studies on the topic investigated weight loss and BMD in overweight or obese
individuals. Roughly speaking, a 10% loss in weight leads to a 2% loss in bone mass. In a
meta-analysis including both overweight and obese individuals, moderate bone loss was
found at the total hip, but not at the lumbar spine [12]. In overweight or obese individuals,
physical activity or calcium supplementation combined with a weight-loss diet seems to curb
bone loss [13, 14].
In a randomised trial investigating the effect on bone health of prolonged CR (-25% over 24
months) compared to unrestricted calorie intake in young, non-obese individuals (mean age:
37.9 years; mean BMI: 25.1 kg/m2), significant bone loss was found in the CR group at the
lumbar spine (–0.013 ± 0.003 vs. 0.007 ± 0.004 g/cm2; p<0.001), femoral neck (–0.015 ±
0.003 vs. 0.005 ± 0.004 g/cm2; p=0.03) and total hip (–0.017 ± 0.002 vs. 0.001 ± 0.003 g/cm2;
p<0.001) [15]. Physical activity was identical in both groups at the outset but, at 12 and 24
months, the reduction in physical activity was significantly greater in the CR group than in the
unrestricted group.
Literature investigating fracture risk is less abundant. The impact of CR on fracture risk seems
to vary according to age, other factors affecting bone health, BMI and the characteristics of
the diet being followed (most notably deficiencies in calcium and protein intake).
Nevertheless, the risk of hip fractures may be higher in patients who lost weight than in those
whose initial weight remained unchanged. In a meta-analysis involving 85,592 overweight,
obese and non-obese individuals (1,374 hip fractures), the risk of hip fractures increased by
84% in those who lost the most weight compared to those in the reference group whose
weight remained stable [16].
Recommendation [B – scientific assumption]
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In overweight and obese patients, weight loss is recommended on account of the beneficial
effect on a number of clinical and biological parameters. For this population, we
recommend regular, suitably adapted, weight-bearing physical activity, combined with
sufficient levels of vitamin D and calcium intake, to limit the bone loss induced by
restricted calorie intake. On the other hand, for normal-weight individuals, weight-loss diets
are advised against owing to their adverse effects on bone mass, and possibly fracture risk.
3.4. Are all dairy products equivalent in terms of their benefits for bone
health?
Recommended daily calcium intakes (Table 2) can be achieved by ingesting 3 dairy products
a day (which provide approximately 150 to 200 mg of calcium per portion) [17, 18]. Dairy
products are high in calcium and have good bioavailability compared to other sources of
calcium, such as plant-based sources [19, 20]. Dairy products are also a source of protein,
other nutrients that contribute to good bone health (e.g., phosphorus and vitamins) and, in the
case of fermented dairy products, probiotics.
In a recent meta-analysis of randomised control trials, dairy consumption was found to have a
beneficial effect on BMD at all sites (lumbar spine: standardised mean difference
(SMD)=0.21 g/cm2, CI95%=0.05-0.37, p=0.009; femoral neck: SMD=0.36 g/cm2,
CI95%=0.19-0.53, p<0.001; total hip: SMD=0.37 g/cm2, CI95%=0.20-0.55, p<0.001) [21]. In
a prospective, randomised intervention study conducted in retirement homes, a 33% reduction
in the incidence of fractures, a 46% reduction in hip fractures and an 11% reduction in falls
was found in homes in which the number of dairy products in residents'' diets was increased
from 2 to 3.5 a day on average, compared to homes in which residents'' diets remained
unchanged [22].
Regardless of the type of dairy product, all of the meta-analyses with fracture-risk data
reported either beneficial associations or no association with fracture risk, and possibly
stronger associations in the case of fermented dairy products (Table 3) [23-28]. No studies
investigating the effects of sheep- or goat-milk dairy products on BMD or fracture risk were
found in the literature.
Recommendation [B – scientific assumption]
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The literature shows that the consumption of dairy products has a beneficial effect on BMD
at all sites, and beneficial or neutral associations with fracture risk. The beneficial effect on
fracture risk seems to be more pronounced with fermented dairy products (yoghurt, cheese).
In patients with osteoporosis or in the prevention of osteoporosis, we recommend the
consumption of 2 to 3 different dairy products a day.
3.5. Does excessive intake of dietary calcium and dairy products pose a
health risk?
Contrary to conventional wisdom, which holds that dairy products'' high saturated fatty acid
content could adversely affect the lipid profile and increase the risk of cardiovascular
diseases, the consumption of dairy products – except butter, which is a fatty substance – is
associated with a favourable lipid profile and a reduction in the risk of cardiovascular disease
and type-2 diabetes [29-31]. The ''matrix'' effect of dairy products – i.e., the interaction
between the various nutrients they contain – affects their physiological effects. As such, the
adverse effect of dairy products on the lipid profile is less pronounced with the consumption
of cheese than with other high-fat dairy products, such as butter or cream [32]. Increasing the
intake of dairy products in general is not associated with a worsening of the lipid profile
(triglycerides, total cholesterol, and LDL and HDL cholesterol), or even with an improvement
in the lipid profile in the case of low-fat dairy products [33].
Furthermore, the dietary intake of calcium in the same recommended amounts is associated
with either no increase in cardiovascular risk [34], or a reduction in cardiovascular risk [35],
especially with fermented dairy products [36]. However, cheese should be consumed only in
moderate amounts because of its high energy density – due to its lipid content – and the
amount of salt it contains.
Patients with a history of urinary lithiasis often restrict their calcium intake. Yet low calcium
intake is detrimental in that it promotes the onset of oxalate lithiasis by increasing the
digestive absorption of oxalates in response to the reduction in calcium-oxalate complexes in
the intestine [37]. No heightened risk of lithiasis has been reported with recommended
calcium intake levels by age, i.e., between 800 and 1200 mg/day [38].
Recommendation [B – scientific assumption]
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Dietary calcium intake should be evaluated before prescribing supplementation. Neither a
heightened cardiovascular or lithiasis risk, nor a negative association with the lipid profile,
has been found with recommended levels of dietary calcium intake (approximately 1g/day).
The consumption of dairy products can be encouraged as this is associated with favourable
lipid profiles and a reduction in cardiovascular risk.
3.6. Is the calcium from plant-based beverages and mineral waters as
beneficial for bone health as the calcium from dairy products?
Some mineral waters are a good dietary source of calcium as the bioavailability of the calcium
in them is equivalent to the bioavailability of calcium in dairy products [39]. Calcium-rich
mineral waters may contribute to maintaining BMD and reducing hip fracture risk, as reported
in the only available observational study [40, 41]. When waters with the same calcium content
were compared, bicarbonate-rich waters were found to reduce bone remodelling more than
sulphate-rich waters. However, for some of bicarbonate-rich waters, the possible intake of salt
should also be considered as salt induces calciuria [42].
Plant-based beverages should be enriched to levels approaching the calcium content of milk.
Moreover, with the exception of soy-based beverages, plant-based beverages contain very
little protein [43]. To the best of our knowledge, no BMD or fracture data are available in
connection with the consumption of plant-based beverages, other than an intervention study,
which found that cow''s milk had a more favourable effect on the prevention of post-
menopausal bone loss than a soy-based drink [44]. Additionally, dairy products provide a
wide range of nutrients that are beneficial to bone health, including proteins, which are found
only in small quantities or not at all in plant-based drinks and mineral waters.
Recommendation [C – low level of evidence]
Mineral waters are a source of dietary calcium, whose bioavailability is equivalent to that of
calcium in dairy products. Calcium- and bicarbonate-rich waters that are poor in sulphates
should be preferred. In patients with osteoporosis or in the prevention of osteoporosis, we
recommend the consumption of calcium-rich mineral waters (>250-300 mg Ca/L) if the
daily consumption of dairy products is not enough to attain optimal calcium intake levels.
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There is no data suggesting that plant-based beverages are equivalent to animal milks as a
source of calcium. As such, there are no arguments in favour of recommending their
consumption for bone health.
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3.7. Does protein intake (quality and quantity) affect bone health?
Approximately one-third of bone mass is composed of proteins. Proteins form the structure of
the organic matrix of bone (collagen) and contribute to bone-tissue function (non-collagen
proteins).
During bone remodelling, the amino acids released as a result of proteolysis cannot be reused
in situ. Furthermore, some amino acids – the essential amino acids – can only be obtained
through diet. In addition to their structural role, dietary proteins stimulate the release of IGF1
(Insulin-like growth factor 1), a hormone that has an anabolic effect on musculoskeletal tissue
[45]. Optimal protein intake is therefore essential for acquiring and maintaining bone mass. A
distinction should also be made between animal protein and plant protein. To attain
recommended daily protein intake levels (Table 2), diets should include "high-quality"
proteins – i.e., proteins that are easily digested, rich in essential amino acids, and available for
protein synthesis – the sources of which are primarily animal (meat, fish, dairy products and
eggs), but also include soybean.
Two (2) meta-analyses reported a protective effect of protein on lumbar spine BMD [46, 47].
On the other hand, no effect was found at the hip. Where fracture data is concerned, the
literature is limited to cohort observational studies [48]. In elderly individuals with
osteoporosis, optimal protein intake levels are associated with an 11-16% reduction in hip
fracture risk (Table 4) [46, 49-52]. However, the beneficial effect of protein intake on bone
health is only observed if calcium and vitamin D intake levels are optimal (1g/day and 800
IU/day, respectively) as part of a balanced diet with suitable calorie intake levels [53, 54].
In menopausal women, individuals with osteoporosis and the elderly, the recommended daily
protein intake is at least 1-1.2 g/kg/day, with at least 20 to 30 g of "high quality" protein per
meal (Table 5). In the most fragile elderly individuals, or in those with a chronic illness,
because of anabolic resistance to dietary protein and splanchnic sequestration, increasing
these intake levels to 1.2-1.5 g/kg/day is recommended (in the absence of severe renal
impairment) [55].
It is generally accepted that "high quality" dietary proteins induce a better anabolic response
since they are rich in essential amino acids, and particularly leucine. However, in the meta-
analyses investigating associations between protein intake and BMD or fracture risk, no
significant differences were found between animal and plant proteins [46, 52, 56].
Nonetheless, partially replacing animal protein with plant protein may be associated with an
increase in bone remodelling markers and parathyroid hormone [57]. Some cohort studies
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suggest more favourable associations between calculated bone strength and animal protein
intake compared to plant protein intake [58, 59]. Apart from being a source of calcium, dairy
products, especially whey, which is rich in leucine, are a source of "high quality" protein [28].
Recommendation [B – scientific assumption]
In patients with osteoporosis or in the prevention of osteoporosis, we recommend a protein
intake of at least 1-1.2 g/kg/day as part of a balanced diet with suitably adapted calorie,
calcium and vitamin D intakes. Protein intakes should include "high quality" animal
proteins. Dairy products that are rich in "high quality" protein and calcium are
recommended.
3.8. Are high-protein, high-calorie oral nutritional supplements good for
bone health?
The prevalence of undernutrition is high in the elderly, especially after hip fractures. It is
estimated that between 18.7 and 45.7% of older people are undernourished [60].
Undernutrition in older people is associated with an increase in overall fragility, sarcopenia
and falls [55].
Currently, data on the efficacy of high-protein, high-calorie oral nutritional supplements
(ONSs) on bone health are lacking. After a hip fracture, ONSs could help prevent
postoperative complications, improve functional recovery, reduce length of stay and, possibly,
reduce mortality. However, the methodological quality of the available trials is poor [60-62].
Recommendation [C – low level of evidence]
In patients with osteoporosis, protein intake should be adapted in line with nutritional status
(dietary advice; increase in dietary intake and/or ONSs, such as high-protein drinks). The
use of ONSs should not be systematic: they should be reserved for undernourished patients
only, or when it is difficult to change the patient''s diet. In patients with osteoporosis who
are not undernourished, we do not recommend the systematic use of high-protein, high-
calorie ONSs on account of the lack of scientific data demonstrating a beneficial effect on
bone health.
3.9. Do acid-producing diets adversely affect bone health?
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The "dietary acid load hypothesis as the cause of osteoporosis" emerged in the 1960s.
According to this hypothesis, animal protein, and to a lesser extent cereals – both endogenous
sources of acids (sulphur-containing amino acids and phosphoproteins) – caused metabolic
acidosis and a reduction in urinary pH, leading to excessive bone resorption as a
compensatory response inducing the release of cations (calcium, calcium bicarbonate) from
bone, thereby disrupting bone and calcium homeostasis, and ultimately leading to
hypercalciuria. The acid-producing potential of a food item is calculated using indices such as
the PRAL (potential renal net acid load) index or the NEAP (net endogenous acid
production) index.
This hypothesis has since been invalidated as, in the absence of renal impairment and calcium
and vitamin D deficiencies:
- diet, whether acid or alkaline, does not modify systemic pH [63]
- no association has been found between endogenous acid production and BMD,
fracture risk or osteoporosis [64-66]
- high protein intake does not affect the calcium balance. Dietary protein-induced
hypercalciuria is due to an increase in concomitant calcium intake and the intestinal
absorption of calcium (mediated by IGF-1), and not the release of calcium from bone
[45].
Recommendation [B – scientific assumption]
In the absence of chronic renal impairment and calcium and vitamin D deficiency, there is
no scientific evidence to suggest that acid-producing diets have an adverse effect on bone
health.
3.10. Are vitamin D-enriched foods an alternative to supplementation as
a means of optimising vitamin D status?
Vitamin D synthesis in the skin depends on exposure to sunlight and accounts for at least 70%
of vitamin D status (serum 25-OH-D values). It is however limited by a number of
environmental factors (climate, latitude, pollution, etc.) and cultural factors (lifestyle,
clothing, sunscreens, etc.). Furthermore, dietary vitamin D intake is generally very moderate
(mainly through oil-rich fish and cod liver oil). Food enrichment is the process of adding
bioactive compounds to food to prevent/treat nutrient deficiencies. Several clinical trials
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investigating the efficacy of vitamin D-enriched foods versus placebo have been conducted in
adults and have reported an increase in serum 25-OH-D values [67].
In the only meta-analysis that has been conducted – covering 6 intervention studies –, the
consumption of vitamin D-enriched foods was found to have a moderate beneficial effect on
BMD compared to placebo [68]. The literature on the effect of vitamin D-enriched foods on
fracture risk is scarce, and all the more so as most of the studies considered medically
prescribed supplementation at the same time. A study covering the French population, based
on a simulation model including three age groups – 60-69 years, 70-79 years and 80-89 years
– suggested that the regular consumption of vitamin D-enriched dairy products could
significantly reduce the number of fractures – especially at the hip – and could be an
inexpensive strategy, especially for persons aged over 70 years [69].
Very few studies have compared the efficacy of medically prescribed supplementation versus
enriched foods in optimising vitamin D status. Although, theoretically, vitamin D-enriched
foods could be an alternative to supplementation, evidence of a beneficial effect of vitamin D
on bone health has only been demonstrated with supplementation.
Recommendation [C – low level of evidence]
In cases of vitamin D deficiency, vitamin D-enriched foods could be an alternative to
supplementation as a means of optimising vitamin D status, but there is not enough
scientific evidence to assert that they are comparable to medically prescribed
supplementation in terms of their effect on bone health.
3.11. To what extent do other vitamins affect bone health?
The relationship between vitamin intake and bone health can be considered from different
angles, e.g., by referring to preclinical studies on the known effects of specific vitamins on
bone cells or calcium and phosphorus metabolism, studies on the prevalence of vitamin
deficiencies and high-risk situations, epidemiological studies investigating dietary intake or
circulating levels of specific vitamins, and intervention studies investigating the effect of
increasing vitamin intake (in most cases using supplements) (Table 6) [18].
The vitamins whose effect on bone metabolism and calcium and phosphorus metabolism has
been clearly established are vitamins D and K. In the absence of undernutrition or chronic
diseases of the digestive tract, vitamin insufficiencies/deficiencies in adults mainly concern
vitamins D, B9 (folates) and B12. Deficiencies in vitamins A, B1, B2, B3, B5, B6, B8, C, E
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and K are very rare. Deficiencies in vitamin B12 – sourced from animal-derived foods only –
are most notably observed in vegans and individuals who have undergone bariatric surgery.
Vitamin A, B6, C, D and E supplementation in excess of recommended doses is not without
health risks [18].
Favourable associations have been reported between bone health and an increase in dietary
intake of vitamins D, K, B9 (folates), B6 (if intake is not too high), C and E. Where vitamin A
is concerned, the data are conflicting, with provitamin carotenoids showing a probable
beneficial effect, and retinol an adverse effect. High intake levels of vitamins B6 and B12
have been reported to be associated with an increase in risk fracture.
In studies investigating bone health in connection with circulating vitamin levels,
insufficiencies/deficiencies in vitamin D, K and B9 (folates) were associated with lower BMD
and even an increase in fracture risk.
The findings in the 2 types of studies mentioned above are difficult to interpret in terms of
causality as many confounding factors related to dietary habits, lifestyle and even genetic
background can affect bone parameters and fracture risk.
Intervention studies – which offer the highest level of evidence – were very rare and often
suffered from many potential biases. They were often of low statistical power, in some cases
testing combinations of vitamin supplements, and control groups were not adequate for
detecting the effect of a specific vitamin. The reported beneficial associations between
fracture risk and dietary intake or plasma concentration of vitamin K were not confirmed in
meta-analyses of the intervention studies, which suggest a beneficial effect of vitamin K
(menaquinone) on BMD only [70-76].
Recommendation [C – low level of evidence]
Except in the case of vitamin D, there is not enough scientific evidence to recommend
supplementation with other vitamins to improve bone health.
3.12. What effects does soda, tea and coffee consumption have on bone
health?
Studies investigating the effect of sodas on bone health are scarce and also consider other
non-alcoholic drinks, such as tea and coffee. A recent meta-analysis suggests that an
association exists between lower BMD and high sodas consumption in young, healthy adults
[77]. However, the findings reported in that meta-analysis are difficult to extrapolate to
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clinical practice since most of the bone mineral density analyses were performed for the entire
body and, in most cases, the subjects were young, healthy adults. In that meta-analysis, three
cohort studies found that fracture risk started to increase with the consumption of 1 to 2 sodas
a day. Moreover, high soda consumption was voluntarily associated with insufficient intake of
dairy products, or other dietary or lifestyle practices that are less beneficial to bone health.
The association between tea consumption and bone health has been the subject of
investigation since the 1990s, with conflicting results. However, in the most recent studies,
higher hip and lumbar spine BMDs have been reported in tea drinkers compared to non-tea
drinkers [78]. This may be due to the effects of the polyphenolic compounds (catechins) in
tea. In most of the publications, tea consumption is also associated with a reduction in fracture
risk [79].
Due to the negative effect of caffeine on calcium metabolism – i.e., an increase in the
excretion and a reduction in the absorption of calcium – many studies have attempted to
investigate the effect of coffee on bone metabolism. They suggest a moderate negative
association between high coffee consumption (> 400 mg/day of caffeine, or approximately 3
cups of coffee) and BMD, compared to low coffee consumption [80]. Regarding coffee
consumption and fracture risk, a meta-analysis reported an association between coffee
consumption and an increase in fracture risk in women (RR (CI95%)=1.14 (1.05–1.24)), and
a reduction in fracture risk in men (RR=0.76 (0.62–0.94)) [81]. Another recent meta-analysis
suggested an association between lower incidence of hip fractures and moderate coffee
consumption (up to 3 cups a day) compared to low coffee consumption (RR(CI95%)=0.86
(0.67–1.05)), regardless of sex. However, the association disappeared after adjusting for
potential confounding factors, such as calorie and calcium intake, and tea consumption [82].
Recommendation [B – scientific assumption]
Daily soda consumption seems to have a negative effect on bone health. As such, it is
recommended to restrict soda consumption, especially since this is often associated with a
reduction in the intake of dairy products. High tea consumption seems to have a beneficial
effect on bone health. However, the benefits are not well enough established to recommend
increasing tea consumption. The consumption of up to 3 cups of coffee a day seems to have
no adverse effects on bone health.
3.13. Does alcohol consumption adversely affect bone health?
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Several studies have investigated the association between alcohol consumption (drinking) and
bone health. The results are variable, reflecting the complexity of the association, which
depends on age, sex, menopause status, mode of consumption – regular or acute (binge
drinking), type of alcohol, and other confounding factors associated with drinking (smoking,
comorbidities, etc.), whether excessive or not [83, 84]. An additional difficulty lies in the lack
of consensus on what constitutes light, moderate and heavy drinking. Gaddini et al propose
the following definitions: light (occasional consumption of small amounts); moderate (regular
consumption – i.e., ≥ 3 days a week, with ≤ 1 glass a day for women, and ≤ 2 glasses a day for
men); and heavy (consumption exceeding the thresholds defined for moderate consumption,
either regularly (most days of the week) or occasionally (≥ 5 glasses, i.e. binge drinking) [85].
Moderate drinking is more often associated with higher BMD values and lower hip fracture
risk than light drinking. This has been demonstrated especially in menopausal women who
drink small amounts of red wine [86]. This finding in menopausal women could be due to the
protective effect of the polyphenols and terpenes (resveratrol) in wine. On the other hand,
heavy drinking is associated with lower BMD values and higher hip fracture risk [85, 87].
Furthermore, regardless of its effects on bone health, drinking increases the risk of falls and,
consequently, fractures.
Recommendation [B – scientific assumption]
Light to moderate alcohol consumption seems to have no adverse effect on bone health in
women. On the other hand, heavy consumption is associated with lower BMD values and
higher fracture risk. However, since alcohol is addictive and detrimental to health in
general, alcohol consumption, even in moderation, is not recommended.
3.14. What are the expected benefits of phytoestrogens for bone health?
Phytoestrogens are plant-based compounds that are similar in structure to estradiol. Families
of molecules that are classified as phytoestrogens include lignans, isoflavones and some
flavonoids. Dietary sources of lignans include flaxseed and whole-grain cereals. Soybean is a
major source of isoflavones. A distinction should be made between (i) studies on dietary soy
intake, and (ii) intervention studies on soy-based dietary supplements.
In Asian menopausal women, high dietary soy intake is associated with higher BMD values
[88]. It is worth noting that soy is also a source of "high-quality" protein. However, it is
difficult to extrapolate this finding to Western populations due to differences in exposure and
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genetic background. A beneficial effect of isoflavone-rich dietary supplements (genistein and
daidzein) has been demonstrated in menopausal women in some of the intervention studies
that have been published to date. In 2 recently published meta-analyses (2017 and 2020) of
randomised controlled trials in premenopausal and menopausal women, improvements in
BMD were reported at the lumbar spine and femoral neck [89, 90], but this was not found in
the meta-analysis published in 2010 by Ricci et al [91].
Fracture risk has been investigated mainly in Asian populations. High dietary intakes of tofu,
soy protein and isoflavone equivalents are associated with a 21 to 36% reduction in hip
fracture risk in women, but not in men [92].
Recommendation [B – scientific assumption]
Phytoestrogens seem to have a beneficial effect on bone health in Asian women, in dietary
conditions consistent with practices in those populations. As far as Western women are
concerned, there is not enough data in the literature to recommend a soy-based diet or soy-
based dietary supplements in patients with osteoporosis or in the prevention of
osteoporosis.
3.15. What are the expected benefits of pre- and probiotics for bone
health?
Prebiotics are short-chain carbohydrates (oligosaccharides) that cannot be digested by human
digestive enzymes, but which selectively improve the activity of specific groups of beneficial
bacteria in the colon. The fermentation of prebiotics as a result of the activity of these bacteria
leads to the production of short-chain fatty acids and various metabolites (postbiotics).
Probiotics are living microorganisms which, in controlled quantities, are beneficial to their
hosts. A systematic literature review of control studies on the effects of pre- and probiotics
has recently been published [93]. Owing to the diversity of pre- and probiotics, the literature
is scarce. It is highly probable that the microbiota plays a role in bone health.
As far as prebiotics are concerned, several studies, investigating mainly calcium absorption,
have been conducted in children and adolescents, but only a few have been conducted in
adults. No studies investigating the role of prebiotics on fracture risk have been published. In
summary, prebiotics have only modest, short-term effects on calcium absorption. In the 3
studies investigating the effect of prebiotics on BMD, the results were negative [93].
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Of the 5 controlled studies investigating the effect of probiotics on bone loss, 4 reported a
significant reduction in bone loss. The magnitude of the beneficial effect on BMD is
comparable to that observed with vitamin D and calcium supplements [93].
Recommendation [B – scientific assumption]
Prebiotics, which form the substrate for our bacterial microflora, have a modest beneficial
effect on intestinal calcium absorption. Although some probiotic strains have been reported
to be associated with a modest reduction in bone loss, target populations, optimal bacterial
strains and conditions of intake are not sufficiently well defined to recommend their
specific use in patients with osteoporosis or in the prevention of osteoporosis.
4. Discussion
Nutritional care is an integral part of osteoporosis prevention and treatment. These
recommendations are based on 15 questions in connection with daily practices (Table 7) that
address, in very pragmatic terms, various aspects of nutritional care in patients seen for
osteoporosis, as well as topics other than calcium and vitamin D supplementation. To the best
of our knowledge, they are the first set of recommendations of this type, addressing globally
the effect of diet on bone health. Producing these recommendations also provided an
opportunity to dispel certain misconceptions about the role of diet in bone health by referring
to scientific data. An example of this is the supposedly negative effect of acid-producing diets
on bone health (recommendation 9). On the contrary, at recommended levels of dietary
calcium intake, neither an increase in cardiovascular or lithiasis risk, nor a negative
association with the lipid profile, has ever been reported (recommendation 5).
The recommendations are divided into three categories, namely, positive recommendations
(what we recommend), neutral recommendations (what we do not recommend), and negative
recommendations (what we advise against).
The positive recommendations apply to Mediterranean-type diets and the consumption of
dairy products (2 to 3 a day) in combination with "high quality protein" and calcium, and
especially fermented dairy products (yoghurt, cheese). Considering the most recently
published data, the consumption of at least 3 dairy products a day may be envisaged for
institutionalised, dependent elderly individuals [22]. Lastly, calcium-rich mineral waters are
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also a good source of calcium, if daily consumption of dairy products is not enough to attain
optimal calcium intake levels (recommendations 1, 4, 6, 7).
The neutral recommendations apply to pre- and probiotics, phytoestrogens, tea and coffee
consumption, and vitamins other than vitamin D (recommendations 11, 12, 14, 15). Currently,
there is not enough scientific data to specifically recommend their use in patients with
osteoporosis or in the prevention of osteoporosis. The same is true of vitamin D-enriched
foods and calcium-enriched plant-based beverages as replacements for vitamin D
supplementation and dairy products, respectively (recommendations 6, 10). Lastly, the
systematic use of high-protein, high-calorie ONSs cannot be recommended owing to a lack of
scientific data demonstrating a beneficial effect on bone health (recommendation 8).
The negative recommendations apply to unbalanced Western diets, vegetarian and especially
vegan diets, weight-loss diets in normal-weight individuals, alcohol consumption, even in
moderation, and excessive soda consumption (recommendations 1, 2, 3, 12, 13).
In conclusion, these are the first set of recommendations addressing the role of diet in the
prevention and treatment of osteoporosis. Updating them is essential, given the pace at which
literature on the subject is being produced.
Acknowledgements
We are thankful to the review board who reviewed and commented on these
recommendations: Yves Boirie (Endocrinologist, Clermont-Ferrand), Francoise Debiais
(Rheumatologist, Poitiers), Pascal Guggenbuhl (Rheumatologist, Rennes), Rose-Marie Javier
(Rheumatologist, Strasbourg), Eric Lespessailles (Rheumatologist, Orléans), Maria
Papageorgiou (Endocrinologist, Geneva), Christian Roux (Rheumatologist, Paris), and
Achille Tchalla (Geriatric Medicine, Limoges). We also thank the partner patient for taking
part to the discussion for selecting the practical questions.
Conflicts of interest
EB occasional work (advisory boards): Nestlé
JH, GL, MAL, SG, CA, RC, VC, PF, TT, JML, BC, JP declare that they have no competing
interest.
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[92] Koh WP, Wu AH, Wang R, Ang LW, Heng D, Yuan JM, et al. Gender-specific associations
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Table 1: Fracture risk by main types of diet
Diet Study Population Hip fractures All fractures
Mediterranean diet
(MD)
Meta-analysis,
Malmir et al. [3]
EPIC cohort [4]
CHANCES study
[6]
351,625 participants,
Aged 13 to 80 years
188,795 participants
(139,981 women), Mean
age 48.6 years
140,775 participants
(116,176 women), Aged
≥ 60 years
↘ by 21% with high adhesion to the MD: RR
(CI95%)=0.79 (0.72, 0.87)
↘ by 7% per 1-point ↗ (0-10) in MD adhesion
score: HR (CI95%)=0.93 (0.89, 0.98)
↘ by 4% per 2-point ↗ (0-10) in MD adhesion
score: HR (CI95%)=0.96 (0.92, 0.99)
Western diet (WD) Meta-analysis,
Denova-Gutiérrez et
al. [7]
122,061 participants,
Aged > 50 years
↗ by 10% in men with unbalanced (vs. balanced) WD:
(M) OR (CI95%)=1.10 (1.02, 1.19)
(W) OR (CI95%)=1.08 (1.00- 1.17)
Vegetarian diet Meta-analysis,
Iguacel et al. [8]
EPIC-Oxford cohort
[9]
Adventist Health
Study 2 [10]
37,134 participants,
Aged 25 to 80 years
34,696 participants,
Aged 20 to 89 years
34,542 participants
(18,712 women), Aged >
45 years
↗ by 25% (versus omnivores): HR
(CI95%)=1.25 (1.04, 1.50)
No significant ↗ in risk (versus omnivores) in
women and men:
- Semi-vegetarians: HR (CI95%) (W)=0.99
(0.64, 1.53); (M)=0.79 (0.42, 1.48)
- Pescetarians: HR (CI95%) (W)= 1.20 (0.81,
1.78); (M)=0.81 (0.50, 1.32)
- Lacto-ovo vegetarians: HR (CI95%) (W)=1.17
(0.91, 1.50); (M)=1.11 (0.81, 1.51)
No ↗ in risk (versus omnivores): RR (CI95%)= 1.25
(0.92, 1.71)
↗ by 9% (versus omnivores): HR (CI95%)=1.09 (1.00,
1.19)
Vegan diet Meta-analysis,
Iguacel et al. [8]
EPIC-Oxford cohort
[9]
37,134 participants,
Aged 25 to 80 years
34,696 participants,
Aged 20 to 89 years
Risk multiplied by 2: HR (CI95%)=2.31 (1.66,
3.22)
↗ by 44% (versus omnivores): RR (CI95%)=1.44
(1.05, 1.98)
↗ by 43% (versus omnivores): HR (CI95%)=1.09
(1.20, 1.70)
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Adventist Health
Study 2 [10]
34,542 participants
(18,712 women), Aged >
45 years
↗ by 55% in women: HR (CI95%)=1.55 (1.06,
2.26)
No ↗ in risk in M: HR (CI95%)=1.01 (0.61,
1.68)
Semi-vegetarians: consume meat and fish <1x/week; Pescetarians: include dairy products, eggs and fish in an otherwise vegetarian diet; Lacto-ovo vegetarians: include
dairy products and eggs in an otherwise vegetarian diet
(M) Men; (W) Women
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Table 2: Calcium and proteins intakes recommended by the French Agence nationale de
sécurité sanitaire de l’alimentation, de l’environnement, et du travail (ANSES) [17, 18].
Calcium - Average nutritional requirement: 750 mg/day
- Satisfactory intake: 950 mg/day
- Upper safety limit: 2500 mg/day
Proteins - Nutritional reference for the population: 0.83 g/kg/day, 10-20% of total energy
intake for adults <60 years; elderly: 1g/kg/day
- Upper safety limit: 2.2g/kg/day (27% of total energy intake)
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Table 3: Fracture risk according to consumption of dairy products (higher vs. highest)
in recent meta-analyses (According to [18])
Milk Yoghurt Cheese Any dairy product
Numbe
r of
studies
Risk
(CI95%
)
Numbe
r of
studies
Risk
(CI95%
)
Numbe
r of
studies
Risk
(CI95%
)
Numbe
r of
studies
Risk
(CI95%
)
Bian et
al
(2018)
[23]
Hip
fracture 10
RR=0.9
1 (0.74,
1.12)
3
RR=0.7
5 (0.66,
0.86)
3
RR=0.6
8 (0.61,
0.77)
2
RR=1.0
2 (0.93,
1.12)
Hip
fracture 7
OR=0.7
1 (0.55,
0.91)
1
OR=0.7
7 (0.39,
1.52)
3
OR=0.7
7 (0.53,
1.11)
1
OR=1.7
0 (0.52,
5.59)
Matia-
Martin
et al
(2019)
[24]
All
fractures 3
HR=1.0
5 (0.94,
1.18)
2
HR=0.9
2 (0.87,
0.98)
2
HR=0.8
9 (0.81,
0.98)
Hip
fracture 5
HR=0.9
1 (0.69,
1.21)
5
HR=0.8
7 (0.71,
1.05)
4
HR=0.8
0 (0.62,
1.03)
Vertebra
l
fracture
3
HR=0.8
1 (0.66,
1.00)
1
HR=1.1
8 (0.59,
2.39)
1
HR=0.6
5 (0.33,
1.27)
Malmi
r et al
(2020)
[25]
Hip
fracture 10
RR=0.9
3 (0.75,
1.15)
- - 6
RR=0.9
0 (0.73,
1.11)
Hip
fracture 9
OR=0.7
5 (0.57,
0.99)
- - 3
OR=0.8
6 (0.53,
1.38)
Hidaya
t et al
(2020)
[26]
Hip
fracture 9
RR=0.8
6 (0.73,
1.02)
4
RR=0.7
8 (0.68,
0.90)
4
RR=0.8
5 (0.66,
1.08)
-
Ong et
al
(2020)
[27]
Hip
fracture - 3
RR=0.7
6 (0.63,
0.80)
2
RR=0.8
9 (0.73,
1.10)
-
RR: Relative Risk (cohort studies); HR: Hazard Ratio (cohort studies); OR; Odds Ratio (case-control studies)
statistically significant
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Table 4: Meta-analyses comparing fracture risk between highest versus lowest level of
protein consumption
Meta-
analysis Population
Fracture
site
Total protein Animal protein Plant-based protein
Numbe
r of
studies
Risk (CI95%)
Numbe
r of
studies
Risk (CI95%)
Numbe
r of
studies
Risk (CI95%)
Darling, 2009
[46]
Adults ≥ 18
years
Hip
fractures 3
RR=0.75 (0.47,
1.21) 3
RR=0.83 (0.54,
1.30) 2
RR=1.21 (0.82,
1.79)
Wu, 2015
[49]
Adults ≥ 18
years
All
fractures 3
RR=0.99 (0.97,
1.02) 2
RR=0.79 (0.32,
1.96)
Hip
fractures 6
RR=0.89 (0.82,
0.97) 4
RR=1.04 (0.70,
1.54)
Wallace,
2017 [50]
Adults ≥ 18
years
Hip
fractures 5
RR=0.84 (0.73,
0.95)
Groenendijk,
2019 [51]
Adults > 65
years
Hip
fractures 4
HR=0.89 (0.84,
0.94)
Darling, 2019
[52]
Adults ≥ 18
years
All
fractures
4
3
3
RR=0.94 (0.72,
1.23)
HR=0.82 (0.59,
1.14); 0.79#
(0.64, 0.97)
OR=0.69 (0.30,
1.68)
4 RR=0.98 (0.76, 1.27) 3 RR=0.97 (0.89, 1.09)
RR: Relative Risk (cohort studies); HR: Hazard Ratio (cohort studies); OR; Odds Ratio (case-control studies)
Statistically significant
# If removal the study with low calcium intake.
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Table 5: Mean calcium and protein content by food.
Class of food Food
Calcium Protein
Content per 100 g Portion equivalent to 300 mg of calcium Content per 100 g Portion (g) equivalent to 20 g of protein
Meat, fish
and eggs, or
equivalent
Cooked meat (average
quality) 10.4 mg 2.9 kg 27.2 g 75 g
Chicken fillet 6.3 mg 4.8 kg 20.7 g 100 g
Cooked fish 29.9 mg 1 kg 23.5 g 85 g
Hard-boiled eggs 41 mg 732 (14 eggs) 13.5 g 150 g (3 eggs)
Plain tofu 100 mg 300 g 14.7 g 140 g
Dairy products
Cheese 626 mg 48 g (1 portion) 21.3 g 90 g (2 portions)
Fromage blanc 122 mg 246 g (2 small containers) 7 g 300 g (3 small containers)
Yoghurt 121 mg 248 g (2 yoghurts) 3.6 g 500 g (4 yoghurts)
Milk 117 mg 0.25 litres 3.3 g 0.5 litres
Nuts, cereals
and legumes
Walnuts 75 mg 400 g 15.7 g 130 g
Almonds (with skin) 260 mg 115 g 22.6 g 90 g
Soybean 220 mg 136 g 37.8 g 50 g
White rice (cooked) 14 mg 2.1 kg 3.1 g 650 g
Pasta (cooked) 17 mg 1.8 kg 4.4 g 450 g
Whole-wheat pasta (cooked) 22 mg 1.4 kg 4.9 g 410 g
Lentils (cooked) 40 mg 750 g 10.1 g 200 g
Chickpeas (cooked) 72 mg 417 g 8.3 g 240 g
Bread 31 mg 968 g (4 baguettes) 9.0 g 220 g (1 baguette)
Soy drink, plain, not enriched
with calcium 12 mg 2500 g (approx. 2.5 litres) 3.6 g 555 g (approx. 0.5 litres)
Soy drink, plain, calcium-
enriched 98 mg 306 g (approx. 0.3 litres) 3.7 g 540 g (approx. 0.5 litres)
Oat milk, plain 1 mg Not applicable <0.5 g > 4 litres
Fruit and vegetables Green beans (cooked) 55 mg 545 g 2 g 1 kg Green peas (cooked) 33 mg 909 g 5.8 g 340 g
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Spinach (cooked) 140 mg 214 g 3.2 g 625 g
Quinoa (cooked) 23 mg 1.3 kg 5 g 400 g
Apple (raw) 5 mg 6 kg 0.3 g 6.6 kg
Orange 66 mg 0.5 kg 0.8 g 2.5 kg
Other Spirulina 120 mg 250 g 57.5 g 35 g
At equal calcium intakes, calcium absorption varies depending on bioavailability.
Source: Ciqual food composition Table 2020 (ANSES) http://ciqual.anses.fr/
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Table 6: Vitamins and bone health (adapted from reference [18])
Vitamins
Demonstrated effect on
bone and calcium and
phosphorus metabolism
Insufficiency/deficiency
in adults
Potential health
risks when
recommended
doses exceeded
Associations
between
increase in
dietary
vitamin
intake and
bone health
Associations between
circulating vitamin
levels and bone health
Beneficial effects of
supplementation on bone
health in intervention
study
D
? (Calcium and
phosphorus metabolism,
bone remodelling)
Frequent ? (hypercalcemia) Favourable Insufficiency/deficiency is deleterious Demonstrated for insufficiency/deficiency
K ? (activation of osteocalcin) Very rare Not demonstrated Favourable Insufficiency/deficiency is deleterious
No demonstrated
beneficial effect on
fracture risk. Beneficial
effect on BMD with
vitamin K2 only
A
± (increase in bone
formation and reduction
in bone resorption;
inhibits mineralisation)
Very rare
? (hepatotoxic
and teratogenic
effects; increase
in mortality)
Favourable
for
provitamin
carotenoids;
deleterious
for retinol
Deleterious with retinol;
favourable with
provitamin carotenoids.
Not enough data to draw
conclusions (1 study with
retinol reporting no effect
on BRMs)
B6 (pyridoxine)
Not demonstrated.
Substrate for alkaline
phosphatase
Very rare
? (reversible
peripheral
neuropathies)
Favourable
without the
need for high
intakes;
unfavourable
with high
intakes
Uncertain
- B6 supplementation has
no effect on fracture risk,
but high doses associated
with increase in hip
fracture risk.
- Folate-B12
supplementation has no
effect on fracture risk,
except in individuals > 80
years, but increase in
cases of cancer; reduces
homocysteine but no
effect on BRMs.
B9 (folic acid or
folate)
± (increase in bone
resorption and decrease in
bone formation; in the
case of
hyperhomocysteinemia,
alteration of bone matrix
Possible Not demonstrated Favourable Insufficiency/deficiency is deleterious
B12 (cobalamin
or
cyanocobalamin).
Possible (vegans) Not demonstrated
Deleterious
with high
intake
No association
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induced by folate and B12
deficiency)
- B6-folates-B12
supplementation: no effect
on fracture risk
B1 (thiamine) ± Very rare Not demonstrated No data No data No studies
B2 (riboflavin) Not demonstrated Very rare Not demonstrated No data No data No studies
B3 (niacin) Not demonstrated Very rare Not demonstrated No data No data No studies
B5 (pantothenic
acid) ± Very rare Not demonstrated No data No data No studies
B8 (biotin) Not demonstrated Very rare Not demonstrated No data No data No studies
C (ascorbic acid) ± (antioxidant properties) Very rare
? (pro-oxidant
effect with high-
dose vitamin C
and iron
supplementation;
increase in
mortality)
Favourable Conflicting data No studies
E
± (due to anti-
inflammatory and
immumodulatory effects)
Very rare ? (increase in mortality) Favourable No data
Not enough data to draw
conclusions (1 study
reporting a favourable
effect on BRMs)
BRMs: bone remodelling markers
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Table 7: Questions on diet and dietary recommendations in the prevention and treatment of osteoporosis
Question Recommendation HAS grade [1]
Level of
agreement
of working
group
1 - What are the expected benefits of the
Mediterranean diet for bone health?
A Mediterranean-type diet is associated with better bone health. It is therefore
recommended for patients with osteoporosis, or in the prevention of osteoporosis.
B – scientific
assumption 9.3 (1.1)
2 - Are vegetarian and vegan diets
harmful to bone health?
Vegan diets, and to a lesser extent, vegetarian diets, are associated with poorer bone
health. Vegan diets should therefore be avoided in patients with osteoporosis, or in the
prevention of osteoporosis. In vegans, an adjustment of calcium intake should be
systematically proposed.
B – scientific
assumption 9.5 (1.0)
3 - How do voluntary weight-loss diets
affect bone health?
In overweight and obese patients, weight loss is recommended on account of the
beneficial effect on a number of clinical and biological parameters. For this population,
we recommend regular, suitably adapted, weight-bearing physical activity, combined
with sufficient levels of vitamin D and calcium intake, to limit the bone loss induced by
restricted calorie intake. On the other hand, for normal-weight individuals, weight-loss
diets are advised against owing to their adverse effects on bone mass, and possibly
fracture risk.
B – scientific
assumption 9.5 (0.9)
4 - Are all dairy products equivalent in
terms of their benefits for bone health?
The literature shows that the consumption of dairy products has a beneficial effect on
BMD at all sites, and beneficial or neutral associations with fracture risk. The beneficial
effect on fracture risk seems to be more pronounced with fermented dairy products
(yoghurt, cheese). In patients with osteoporosis or in the prevention of osteoporosis, we
recommend the consumption of 2 to 3 different dairy products a day.
B – scientific
assumption 9.5 (1.0)
5 - Does excessive intake of dietary
calcium and dairy products pose a health
risk?
Dietary calcium intake should be evaluated before prescribing supplementation. Neither
a heightened cardiovascular or lithiasis risk, nor a negative association with the lipid
profile, has been found with recommended levels of dietary calcium intake
(approximately 1g/day). The consumption of dairy products can be encouraged as this is
associated with favourable lipid profiles and a reduction in cardiovascular risk.
B – scientific
assumption 9.3 (1.0)
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6 - Is the calcium from plant-based
beverages and mineral waters as
beneficial for bone health as the calcium
from dairy products?
Mineral waters are a source of dietary calcium, whose bioavailability is equivalent to
that of calcium in dairy products. Calcium- and bicarbonate-rich waters that are poor in
sulphates should be preferred. In patients with osteoporosis or in the prevention of
osteoporosis, we recommend the consumption of calcium-rich mineral waters (>250-300
mg Ca/L) if the daily consumption of dairy products is not enough to attain optimal
calcium intake levels. There is no data suggesting that plant-based beverages are
equivalent to animal milks as a source of calcium. As such, there are no arguments in
favour of recommending their consumption for bone health.
C – low level of
evidence 9.1 (1.2)
7- Does protein intake (quality and
quantity) affect bone health?
In patients with osteoporosis or in the prevention of osteoporosis, we recommend a
protein intake of at least 1-1.2 g/kg/day as part of a balanced diet with suitably adapted
calorie, calcium and vitamin D intakes. Protein intakes should include "high quality"
animal proteins. Dairy products that are rich in "high quality" protein and calcium are
recommended.
B – scientific
assumption 9.2 (1.3)
8 - Are high-protein, high-calorie oral
nutritional supplements good for bone
health?
In patients with osteoporosis, protein intake should be adapted in line with nutritional
status (dietary advice; increase in dietary intake and/or ONSs, such as high-protein
drinks). The use of ONSs should not be systematic: they should be reserved for
undernourished patients only, or when it is difficult to change the patient''s diet. In
patients with osteoporosis who are not undernourished, we do not recommend the
systematic use of high-protein, high-calorie ONSs on account of the lack of scientific
data demonstrating a beneficial effect on bone health.
C – low level of
evidence 9.3 (1.1)
9 - Do acid-producing diets adversely
affect bone health?
In the absence of chronic renal impairment and calcium and vitamin D deficiency, there
is no scientific evidence to suggest that acid-producing diets have an adverse effect on
bone health.
B – scientific
assumption 9.4 (1.1)
10 - Are vitamin D-enriched foods an
alternative to supplementation as a means
of optimising vitamin D status?
In cases of vitamin D insufficiency, vitamin D-enriched foods could be an alternative to
supplementation as a means of optimising vitamin D status, but there is not enough
scientific evidence to assert that they are comparable to medically prescribed
supplementation in terms of their effect on bone health.
C – low level of
evidence 9.2 (1.5)
11 - To what extent do other vitamins
affect bone health?
Except in the case of vitamin D, there is not enough scientific evidence to recommend
supplementation with other vitamins to improve bone health.
C – low level of
evidence 9.5 (0.7)
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12 - What effects does soda, tea and
coffee consumption have on bone health?
Daily soda consumption seems to have a negative effect on bone health. As such, it is
recommended to restrict soda consumption, especially since this is often associated with
a reduction in the intake of dairy products. High tea consumption seems to have a
beneficial effect on bone health. However, the benefits are not well enough established
to recommend increasing tea consumption. The consumption of up to 3 cups of coffee a
day seems to have no adverse effects on bone health.
B – scientific
assumption 9.3 (1.1)
13 - Does alcohol consumption adversely
affect bone health?
Light to moderate alcohol consumption seems to have no adverse effect on bone health
in women. On the other hand, heavy consumption is associated with lower BMD values
and higher fracture risk. However, since alcohol is addictive and detrimental to health in
general, alcohol consumption, even at moderate levels, is not recommended.
B – scientific
assumption 9.4 (0.9)
14 - What are the expected benefits of
phytoestrogens for bone health?
Phytoestrogens seem to have a beneficial effect on bone health in Asian women, in
dietary conditions consistent with practices in those populations. As far as Western
women are concerned, there is not enough data in the literature to recommend a soy-
based diet or soy-based dietary supplements in patients with osteoporosis or in the
prevention of osteoporosis.
B – scientific
assumption 9.6 (0.8)
15 - What are the expected benefits of
pre- and probiotics for bone health?
Prebiotics, which form the substrate for our bacterial microflora, have a modest
beneficial effect on intestinal calcium absorption. Although some probiotic strains have
been reported to be associated with a modest reduction in bone loss, target populations,
optimal bacterial strains and conditions of intake are not sufficiently well defined to
specifically recommend their use in patients with osteoporosis or in the prevention of
osteoporosis.
B – scientific
assumption 9.5 (0.8)
Agreement score between 0 and 10 where 10 is complete agreement.
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