Sage Journals: Discover world-class research

Abstract

Osteoporosis affects one out of three postmenopausal women. Their remaining lifetime risk of fragility fractures exceeds that of breast cancer. The risk of osteoporosis and/or fragility fractures can be reduced through healthy lifestyle changes. These include adequate dietary intakes of calcium, vitamin D and protein, regular weight-bearing exercise, reduction in alcohol intake and smoking cessation. European guidance for the diagnosis and management of osteoporosis in postmenopausal women recommends a daily intake of at least 1000 mg/day for calcium, 800 IU/day for vitamin D and 1 g/kg body weight of protein for all women aged over 50 years. The development of programs that encourage lifestyle changes (in particular balanced nutrient intakes) are therefore essential for the reduction of osteoporosis risk.

Keywords

bone calcium dairy fracture menopause osteoporosis protein intake vitamin D

Osteoporosis is a progressive disease characterized by a decrease in bone mass and deterioration of bone structure leading to an increased risk of fragility fractures. Common osteoporotic fractures, such as those to the hip, spine, forearm and humerus, are often associated with debilitating pain that can lead to further physical disability, loss of independence, depression and premature death [1]. Using the WHO definition for osteoporosis (bone mineral density [BMD] ≥2.5 SD below the young adult mean), osteoporosis affected more than 22 million European women (22%) and 5.5 million men (7%) aged over 50 years in 2010 [1,2]. In 2010, the number of deaths due to fractures in Europe was 43,000 and the overall cost of osteoporosis to European healthcare systems was more than €37 billion [2]. Incident fractures accounted for 66% of this cost, long-term fracture care for 29% and pharmacological prevention for 5%. Given that the risk of osteoporosis significantly increases in people aged over 50 years, incidence is predicted to increase as the population ages and costs are expected to rise by 25% by 2025. Greater efforts are therefore required to prevent and manage this debilitating disease. The aim of this manuscript is to review the benefits of nutrition for the prevention of osteoporosis in postmenopausal women and to assess what can be done to increase osteoporosis awareness and encourage healthy lifestyle changes within this population.

Risk factors for osteoporosis

Bones start to grow before birth and continue to increase in size, strength and density until the end of the second decade of life, by which time more than 95% of maximum bone strength and density (peak bone mass) is acquired. After this, there is little change until menopause, when a rapid drop in estrogen production leads to an increase in bone turnover and accelerated bone loss, accompanied by microstructural alterations [3]. The overall effect of menopause is an average annual bone loss of 2–3% during the first few years and 0.5–1% thereafter [4]. Menopause is the biggest risk factor for osteoporosis in women.

Approximately 60–80% of peak bone mass variance is determined by genetics [5]. However, we can postulate that the risk of osteoporosis can be reduced by adopting healthy lifestyle choices that increase peak bone mass in children and adolescents, and reduce bone loss in adults [1,6 –8]. Factors that improve bone health include nutrition (particularly calcium and protein intake, but also vitamin D, potassium, phosphorus and other micronutrients and macronutrients), regular weight-bearing exercise, smoking cessation (where appropriate) and reduced alcohol intake [6,8].

The role of nutrition in the prevention & management of osteoporosis

Calcium

Calcium is embedded in collagen fibrils in the form of calcium phosphate (hydroxyapatite) and is essential for bone rigidity. Studies show that children whose mothers consume higher levels of calcium-rich foods during pregnancy (milk, milk products, pulses, nonvegetarian foods, green leafy vegetables and fruit) have a higher bone mineral content (BMC) and BMD at 6–9 years of age [9,10]. Similarly, daily calcium supplements are associated with significant increases in total body BMC and upper limb BMD in children aged 3–18 years, even after the supplement is discontinued [11 –14]. These studies suggest that increasing the level of calcium intake in children and adolescents has the potential to increase peak bone mass, thereby reducing the risk of osteoporosis later in life. In women who have already achieved their peak bone mass, increased calcium intake is associated with negligible bone loss (which means −0.014% per year vs −1% in control subjects) [15]. Moreover, high levels of dietary calcium intake and/or calcium supplements can significantly improve BMC and BMD, and reduce the risk of fractures during menopause [6–7,15 –27]. Notably, however, studies in postmenopausal women and older men suggest that calcium supplements alone may not be sufficient to reduce fracture risk and that additional vitamin D supplementation is required [28].

A meta-analysis has raised the concern that calcium supplements, particularly when administered without vitamin D, are associated with an increased risk of myocardial infarction [29]. Some epidemiological studies support this series of analyses. However, it appears this possible increased risk of cardiovascular events are not observed with food sources of calcium, despite similar benefits on bone density, and may be on fracture risk. Therefore food sources of calcium may be preferable.

Vitamin D

Calcium homeostasis is, to a significant extent, regulated by vitamin D. Vitamin D is obtained from cutaneous synthesis after sunlight exposure (80–90%) and from a limited number of foods, such as oily fish, mushrooms and some fortified dairy products (10–20%) [30]. Vitamin D deficiency decreases the amount of calcium absorbed from the intestine and increases levels of parathyroid hormone (PTH). This, in turn, rebalances the decrease in serum calcium by increasing calcium resorption from the bone [7,31 –34].

Serum levels of 25-hydroxyvitamin D [25(OH)D] lower than 50 nmol/l have a detrimental effect on bone health and may exacerbate osteoporosis in elderly or postmenopausal women by increasing the rate of bone turnover. Studies have shown that vitamin D supplementation is associated with a reduced risk of fragility fractures [35 –37] and survival [38,39] in elderly subjects. Moreover, vitamin D supplementation can reduce the risk of falls by improving muscle strength and physical stability [40 –42].

Protein

Protein accounts for approximately 50% of bone volume and about a third of its mass [43]. Cross-linking of collagen molecules in bone involves the modification of amino acids, and many of the collagen fragments released during the bone remodeling process cannot be reused to build new bone. As well as providing the structural matrix for bone, protein optimizes levels of IGF-I, a hormone that stimulates bone growth, increases calcium and phosphorus absorption in the gut, through the synthesis of calcitriol and increases the rate of phosphate reabsorption from the kidney [32]. Adequate supplies of dietary protein are therefore required for healthy bone maintenance.

Variations in protein intake within the ‘normal’ range (around 0.8–1.5 g/kg body weight/day) account for 3–4% of the variance in peak bone mass attainment in well-nourished children and adolescents [6,44]. A higher dietary protein intake is associated with greater muscle mass and strength, both in postmenopausal women [45 –49] and in young, healthy women following exercise [50]. In older people with osteoporosis, increased levels of protein intake (≥0.8 g/kg body weight/day or 24% of total energy intake) are associated with higher BMD [48,51 –53], a slower rate of bone loss [49,54] and a reduced risk of hip fracture [55,56]. In one study, low serum IGF-I concentrations predicted the risk of osteoporotic fractures in postmenopausal women independent of BMD [57]. This suggests that IGF-I concentrations may have an important role in maintaining bone and muscle strength.

Nutritional targets for the reduction of osteoporosis risk

Balanced nutritional intakes represent the first step in an effective preventive strategy. However, in the presence of increased risk of fracture and/or osteoporosis, this approach may not be sufficient and the management of those patients requires the administration of drugs whose antifracture efficacy has been demonstrated in well conducted clinical trials with fracture as the primary outcome. Regarding vitamin D, a meta-analysis of 17 studies including 52,625 subjects aged over 50 years showed that adequate levels of both vitamin D and calcium were associated with a 12% risk reduction in all types of fracture and a reduced rate of bone loss in studies reporting BMD [17]. These data are supported by a further meta-analysis in which high levels of calcium and vitamin D were associated with an 18% reduction in hip fracture risk compared with no treatment [18]. More recent studies support a target intake of 800 IU vitamin D per day with or without additional calcium supplementation with a documented significant 30% reduction of hip fractures and a 14% significant reduction of any nonvertebral fractures [35,37]. Based on these and similar studies, the Institute of Medicine suggests a recommended daily intake (RDI) of 800 mg/day for calcium and 400 IU for vitamin D throughout adult life and, for women aged over 50 years, a recommended daily allowance of 1000 mg/day for calcium (Table 1) [58]. Slightly higher RDIs for calcium and vitamin D, plus a new target for protein, are recommended by the European Guidance for the Diagnosis and Management of Osteoporosis in Postmenopausal Women (Table 1) [59]. Here, the RDIs for women aged over 50 years are ≥1000 mg/day for calcium and 800 IU for vitamin D (800–1000 IU/day for those with serum levels of 25-hydroxyvitamin D [25(OH)D] lower than 50 or 75 nmol/l in those with a high risk of falls and fractures) and 1 g/kg body weight for protein [59]. The best way to achieve these targets is though a healthy diet. As calcium is mainly provided in dairy products, dairies fortified with calcium and vitamin D that provide at least 40% of the RDI of calcium (400 mg) and 200 IU of vitamin D per portion are valuable options for the long-term attainment of these targets [59].

Table 1.

Dietary reference intakes for calcium, vitamin D and protein in women over the age of 50 years.

Age	IOM†		European Guidance for the Diagnosis and Management of Osteoporosis in Postmenopausal Women‡
	Calcium RDA (mg/day)	Vitamin D RDA (IU/day)	Calcium RDI (mg/day)	Vitamin D RDI (IU/day)	Protein RDI (g/kg body weight)
51–70 years	1000/1200	400/600	1000–1300	800	1
51–70 years with serum levels of vitamin D <50 nmol/l or <75 nmol/l in those with a high risk of falls and fractures	1000/1200	400/600	1000–1300	800–1000	1
70+ years	1000/1200	400/800	1000–1300	800–1000	1

†

Data taken from [58].

‡

Data taken from [1].

IOM: Institute of Medicine; RDA: Recommended daily allowance; RDI: Recommended daily intake.

Role of dairy products in the reduction of osteoporosis risk

Dairy products provide more calcium, protein, magnesium, potassium, zinc and phosphorus per calorie than any other food (Table 2) [32,60]. Approximately 250 mg of calcium can be obtained from a single 200 ml glass of milk, a 180 g serving of yoghurt or 30 g of hard cheese, which means the RDI for calcium can be obtained from only three to four portions of dairy. Up to 24 servings of green vegetables, or 48 servings of whole grain or refined grain foods would be required to have the same effect [61]. In addition to calcium, 1 l of milk provides around 32–35 g of protein [6]. Overall, dairy products may represent up to 52–65% of the RDI of calcium and 20–28% of the RDI of protein [6,14, 62]. Moreover, given the high prevalence of vitamin D insufficiency and the relatively low number of vitamin D rich foods (Table 3), a number of countries supplement certain foods (often milk, margarine, butter and yoghurt) with vitamin D [63]. The rationale for this is that vitamin D and calcium – both key elements for bone health – should be available in the same food products.

Table 2.

Nutrient content per 100 g (unless otherwise stated) of selected dairy food.

Source	Calcium (mg)	Potassium (mg)	Phosphorus (mg)	Protein (g)
Milk, fat 3.7%	119	151	93	3.3
Milk, skimmed	122	156	101	3.4
Cheese parmesan, grated	1,100	125	729	38
Swiss cheese	791	77	567	26.9
Cheddar cheese	721	98	512	24.9
Cottage cheese, nonfat	86	137	190	10.3
Cream cheese	98	138	106	5.9
Yoghurt, plain low fat†	183	234	144	5.3
Yoghurt, fruit low fat†	169	216	133	4.9
Egg, whole poached	56	138	197	12.5
Ice cream, vanilla	128	199	105	3.5

†

Depending on the preparation procedure, yoghurt may have calcium and protein contents similar to plain milk.

Data taken from [64].

Table 3.

Vitamin D content per 100 g (unless otherwise stated) of selected food.

Source	Vitamin D content (IU)
Farmed rainbow trout	759
Wild salmon	600–1000
Farmed salmon	100–250
Sardines (canned)	300–600
Mackerel (canned)	250
Tuna (canned)	236
Cod liver oil	400–1000 per tablespoon
Shiitake mushrooms (fresh)	100
Shiitake mushrooms (dried)	1600
Fresh mushrooms	76
Egg yolk	20 per yolk
Pork shoulder, roasted (lean and fat)	61
Butter	52
Orange juice (including concentrate), fortified with calcium and vitamin D	40
Cheese, cheddar	24
Cheese, Swiss	20

Data taken from [64].

Numerous randomized controlled trials and observational studies have examined the effects of dairy product consumption (including fortified dairy foods) on markers of bone activity and bone turnover in women [7,16,19,27,49,50,65]. In young, healthy women, consumption of fat-free milk versus an isoenergetic carbohydrate drink after resistance exercise promoted fat loss, lean mass gains or maintenance, improved BMD at clinically important sites and reduced bone resorption [50,65]. These studies suggest that the timing of milk protein intake after exercise is important for optimal bone health. In postmenopausal women of all ages, the consumption of soft cheese fortified with vitamin D and calcium increased protein intake and serum levels of IGF-I, and reduced levels of PTH, tartrate-resistant acid phosphatase isoform (TRAP) 5b and cross-linked teleopeptide of type 1 collagen (CTX) (biomarkers for bone resorption) [19,20]. Similar reductions in PTH levels and/or biomarkers of bone turnover were observed in premenopausal and postmenopausal women consuming milk or yoghurt fortified with vitamin D and/or calcium [21 –25]. However, the greatest improvements in biomarkers for bone turnover were observed in studies that ensured compliance with fortified dairy products using a long-term (12–30 months) intervention approach that combined dietary changes with lifestyle and nutrition counseling [26,27].

High protein diets are often criticized for their potentially harmful effects on bone health, in particular increased urinary calcium excretion. However, a study in 130 overweight middle-aged subjects (71 female) randomized to a weight loss diet providing 1.4 g/kg/day protein and three daily servings of dairy protein or 0.8 g/kg/day protein and two daily servings of dairy showed that, if the protein source includes dairy, bone health can be improved [49]. In this study, the high dairy protein diet increased urinary calcium excretion but improved calcium intake and increased whole body, lumbar spine, hip and total BMD. Further studies are required to fully understand the effects of dairy versus nondairy protein on bone health.

Although BMD or BMC changes provide useful information about the impact of nutrition on bone strength, age and extraskeletal factors must be taken into account when determining fracture risk [66]. Data on the relationship between dairy food intake and fracture risk are limited. A meta-analysis data from six studies in 195,102 women found no overall association between total milk intake and hip fracture risk [67]. However, a 12-year follow-up of the Framingham Offspring Study showed that dairy intake was related to hip but not spine BMD, and that yoghurt intake was related to hip (trochanter) BMD alone [68]. Yoghurt intake also showed a weak positive protective trend for hip fracture, while no other dairy groups showed a significant association. This suggests that not all dairy products are equally beneficial for bone health and that further studies are needed to assess the impact of various dairy products on bone turnover, BMC/BMD and fracture risk.

Calcium, vitamin D & protein insufficiency is common among postmenopausal women

Calcium and vitamin D intakes for postmenopausal women in Europe typically fall well below the RDIs (Figure 1). Mean calcium intakes for women aged over 50 years across five European countries range from just over 600 mg/day in Bulgaria to 900 mg/day in Portugal (Figure 1A) [7]. Although calcium levels tend to decrease in older women, a survey of girls and young women (aged 11–23 years) from six European countries showed that mean calcium intake is also inadequate in younger populations [69]. In France, 63–73% of girls aged 11–17 years consumed less than two-thirds of their RDI for calcium [70]. This suggests that calcium insufficiency is common throughout life.

Figure 1.

Calcium intakes and prevalence of vitamin D insufficiency. (A) Calcium intakes among women aged over 50 years from selected European countries. Mean calcium intakes range from approximately 600 (dashed area) to 800 mg/day by country. (B) Prevalence of vitamin D insufficiency among postmenopausal women from selected European countries.

Assessment of vitamin D levels in 8532 post-menopausal women with osteoporosis or osteopenia in nine European countries showed that serum 25-hydroxyvitamin D [25(OH)D] levels ranged from 51.5 nmol/l in France to 85.2 nmol/l in Spain (Figure 1B) [71]. Overall, 79.6% of women had levels lower than 80 nmol/l and 32.1% had lower than 50 nmol/l. A further study carried out in 11 European countries showed that vitamin D levels are considerably lower in winter, when almost 50% of women have 25-hydroxyvitamin D [25(OH)D] lower than 30 nmol/l [77]. Unlike calcium and vitamin D intakes, protein insufficiency is generally not a problem among younger European adults [78]. However, approximately 27–41% of older women (aged over 80 years) ingest less than their RDI of protein [79].

What can be done to improve nutritional target attainment?

A survey carried out by the International Osteoporosis Foundation (IOF) (n = 1200) found that 60% of women know they are likely to develop osteoporosis at some point in their lives and that 99% of respondents (men and women) understand the importance of calcium (in particular dairy products) for maintaining bone health [80]. However, fewer respondents (65 and 59%, respectively) are aware of the benefits of vitamin D and protein intake, 60% are unaware of dietary sources of vitamin D and only a small proportion of respondents engage in preventive health behaviors. Frequently reported barriers to obtaining adequate calcium intake include uncertainty regarding nondairy calcium food sources and supplements, and concerns that the high fat/cholesterol content of calcium-rich foods might cause weight gain and cardiovascular disease [81]. Together, these studies highlight the need to educate patients about the importance and potential sources of calcium, vitamin D and protein, and suggest that patients need to be reassured that their increased consumption of milk fat is unlikely to increase their risk of cardiovascular disease [82].

A number of different approaches are used to increase bone health awareness and encourage lifestyle changes. These include public health education programs, community projects, websites and nutritional and fitness guidelines [7]. The overall goal of health education is to ensure that individuals have an understanding of their current health status in order to make informed decisions about lifestyle changes and treatment. If a patient is aware they have a low BMD, they are more likely to increase their knowledge of osteoporosis and take appropriate steps to reduce their fracture risk. In one study, providing healthy postmenopausal women with their bone scan results increased perceived susceptibility to fracture and led to significant increases in calcium intake over the next 6 months [83]. However, many individuals do not undergo appropriate osteoporosis screening and are unaware of their fracture risk [84]. Educating physicians about the use of the Fracture Risk Assessment (FRAX) tool will encourage them to determine their patients’ 10-year probability of hip fracture or a major osteoporotic fracture, and will most likely lead to greater patient awareness and improved lifestyle [66].

Recently, the scorecard for osteoporosis in Europe (SCOPE) project reviewed all information available on osteoporosis across the 27 countries in the European Union and developed color-coded scorecards that highlight differences between countries in the burden of osteoporosis and fractures, policy framework and treatment provision and uptake [1]. It is hoped that the scorecard will enable healthcare professionals and policy makers to assess their country's general approach to the disease, thereby improving the management of bone health throughout Europe.

Conclusion

Osteoporosis is a debilitating disease that leads to fragility fractures, high morbidity and mortality and high healthcare costs. The greatest risk factor for osteoporosis in women aged over 50 years is the menopause. However, risk can be reduced by adopting a healthy lifestyle that includes adequate levels of dietary calcium, vitamin D and protein, regular weight-bearing exercise, smoking cessation and limited alcohol intake. European Guidance for the Diagnosis and Management of Osteoporosis in Postmenopausal Women recommends an RDI ≥1000 mg/day for calcium, 800 IU for vitamin D and 1 g/kg body weight for protein for all women aged over 50 years. An easy way to achieve these targets is though a healthy dairy-rich diet, including dairy products fortified with calcium and vitamin D, such as yoghurt and milk. Despite this, calcium and vitamin D insufficiency in postmenopausal women is common across Europe.

Future perspective

Primary prevention should be implemented as early as during childhood and adolescence, and after the menopause. Further development of educational initiatives and behavioral change programs designed to increase osteoporosis awareness and improve dietary nutrient intakes are therefore essential if the prevention and management of osteoporosis are to be improved. The efficacy of these measures should be verified with appropriate indicators.

Executive summary

Factors that maintain bone health include nutrition, weight-bearing exercises and avoidance of deleterious influences.

Calcium and vitamin D reduce fall and fracture risk.

Adequate dietary protein intakes are required for healthy bone maintenance.

Dairy products provide more calcium, protein, phosphorus, potassium, zinc and magnesium per calorie than any other food.

There is a need to educate subjects about the importance and potential sources of calcium, vitamin D and protein.

Footnotes

R Rizzoli is part of the advisory board and speaker bureau for Amgen, Danone, GSK, MSD and Servier. The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed.

Writing and editorial assistance was provided by J Read and L Buttle of Chill Pill Media, LLP, thanks to a grant from the Danone company.

References

Kanis

Borgstrom

Compston

SCOPE: a scorecard for osteoporosis in Europe. Arch. Osteoporos. 8, 144 (2013).

Hernlund

Svedbom

Ivergard

Osteoporosis in the European Union: medical management, epidemiology and economic burden. A report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA). Arch. Osteoporos. 8, 136 (2013).

Gallagher

Riggs

DeLuca

. Effect of estrogen on calcium absorption and serum vitamin D metabolites in postmenopausal osteoporosis. J. Clin. Endocrinol. Metab. 51, 1359–1364 (1980).

Burger

Boulet

. A Portrait of the Menopause. The Parthenon Publishing Group Ltd, Casterton Hall, Carnforth, Lancashire, UK (1991).

Ferrari

Rizzoli

Bonjour

. Genetic aspects of osteoporosis. Curr. Opin. Rheumatol. 11, 294–300 (1991).

Rizzoli

. Nutrition: its role in bone health. Best Pract. Res. Clin. Endocrinol. Metab. 22, 813–829 (2008).

Rizzoli

Abraham

Brandi

. Nutrition and bone health: turning knowledge and beliefs into healthy behaviour. Curr. Med. Res. Opin. 30, 131–141 (2014).

Rizzoli

Bianchi

Garabedian

McKay

Moreno

. Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone 46, 294–305 (2010).

Ganpule

Yajnik

Fall

Bone mass in Indian children - relationships to maternal nutritional status and diet during pregnancy: the Pune Maternal Nutrition Study. J. Clin. Endocrinol. Metab. 91, 2994–3001 (2006).

10.

Cole

Gale

Javaid

Maternal dietary patterns during pregnancy and childhood bone mass: a longitudinal study. J. Bone Miner. Res. 24, 663–668 (2009).

11.

Winzenberg

Shaw

Fryer

Jones

. Effects of calcium supplementation on bone density in healthy children: meta-analysis of randomised controlled trials. BMJ 333, 775 (2006).

12.

Huncharek

Muscat

Kupelnick

. Impact of dairy products and dietary calcium on bone-mineral content in children: results of a meta-analysis. Bone 43, 312–321 (2008).

13.

Bonjour

Chevalley

Ammann

Slosman

Rizzoli

. Gain in bone mineral mass in prepubertal girls 3.5 years after discontinuation of calcium supplementation: a follow-up study. Lancet 358, 1208–1212 (2001).

14.

Chevalley

Hoffmeyer

Bonjour

Rizzoli

. Early serum IGF-I response to oral protein supplements in elderly women with a recent hip fracture. Clin. Nutr. 29, 78–83 (2010).

15.

Nordin

. Calcium and osteoporosis. Nutrition 13, 664–686 (1997).

16.

Rizzoli

. Dairy products, yoghurts, and bone health. Am. J. Clin. Nutr. 99(5 Suppl.), S1256–S1262 (2014).

17.

Tang

Eslick

Nowson

Smith

Bensoussan

. Use of calcium or calcium in combination with vitamin D supplementation to prevent fractures. and bone loss in people aged 50 years and older: a meta-analysis. Lancet 370, 657–666 (2007).

18.

Boonen

Lips

Bouillon

Need for additional calcium to reduce the risk of hip fracture with vitamin D supplementation: evidence from a comparative meta-analysis of randomized controlled trials. J. Clin. Endocrinol. Metab. 92, 1415–1423 (2007).

19.

Bonjour

Benoit

Rousseau

Souberbielle

. Consumption of vitamin D- and calcium-fortified soft white cheese lowers the biochemical marker of bone resorption TRAP 5b in postmenopausal women at moderate risk of osteoporosis fracture. J. Nutr. 142, 698–703 (2012).

20.

Bonjour

Benoit

Pourchaire

Ferry

Rousseau

Souberbielle

. Inhibition of markers of bone resorption by consumption of vitamin D and calcium-fortified soft plain cheese by institutionalised elderly women. Br. J. Nutr. 102, 962–966 (2009).

21.

Kruger

Booth

Coad

Schollum

Kuhn-Sherlock

Shearer

. Effect of calcium fortified milk Suppl. ementation with or without vitamin K on biochemical markers of bone turnover in premenopausal women. Nutrition 22, 1120–1128 (2006).

22.

Bonjour

Brandolini-Bunlon

Boirie

Inhibition of bone turnover by milk intake in postmenopausal women. Br. J. Nutr. 100, 866–874 (2008).

23.

Kruger

Todd

High-calcium, vitamin D fortified milk is effective in improving bone turnover markers and vitamin D status in healthy postmenopausal Chinese women. Eur. J. Clin. Nutr. 66, 856–861 (2012).

24.

Kruger

Schollum

Kuhn-Sherlock

The effect of a fortified milk drink on vitamin D status and bone turnover in post-menopausal women from South East Asia. Bone 46, 759–767 (2010).

25.

Bonjour

Benoit

Payen

Kraenzlin

. Consumption of yoghurts fortified in vitamin D and calcium reduces serum parathyroid hormone and markers of bone resorption: a double-blind randomized controlled trial in institutionalized elderly women. J. Clin. Endocrinol. Metab. 98, 2915–2921 (2013).

26.

Manios

Moschonis

Trovas

Lyritis

. Changes in biochemical indexes of bone metabolism and bone mineral density after a 12-mo dietary intervention program: the Postmenopausal Health Study. Am. J. Clin. Nutr. 86, 781–789 (2007).

27.

Moschonis

Katsaroli

Lyritis

Manios

. The effects of a 30-month dietary intervention on bone mineral density: the Postmenopausal Health Study. Br. J. Nutr. 104, 100–107 (2010).

28.

Bischoff-Ferrari

Dawson-Hughes

Baron

Calcium intake and hip fracture risk in men and women: a meta-analysis of prospective cohort studies and randomized controlled trials. Am. J. Clin. Nutr. 86, 1780–1790 (2007).

29.

Bolland

Avenell

Baron

Effect of calcium supplements on risk of myocardial infarction and cardiovascular events: meta-analysis. BMJ 341, c3691 (2010).

30.

Mithal

Wahl

Bonjour

. Global vitamin D status and determinants of hypovitaminosis D. Osteoporos. Int. 20, 1807–1820 (2009).

31.

Holick

. Vitamin D deficiency. N. Engl. J. Med. 357, 266–281 (2007).

32.

Heaney

. Dairy and bone health. J. Am. Coll. Nutr. 28(Suppl. 1), S82–S90 (2009).

33.

Haines

Park

. Vitamin D Suppl. ementation: what's known, what to do, and what's needed. Pharmacotherapy 32, 354–382 (2012).

34.

Rizzoli

Boonen

Brandi

Vitamin D supplementation in elderly or postmenopausal women: a 2013 update of the 2008 recommendations from the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO). Curr. Med. Res. Opin. 29, 305–313 (2013).

35.

Bischoff-Ferrari

Willett

Wong

Prevention of nonvertebral fractures with oral vitamin D and dose dependency: a meta-analysis of randomized controlled trials. Arch. Intern. Med. 169, 551–561 (2009).

36.

Bergman

Fan

McFetridge

Sen

. Efficacy of vitamin D3 supplementation in preventing fractures in elderly women: a meta-analysis. Curr. Med. Res. Opin. 26, 1193–1201 (2010).

37.

Bischoff-Ferrari

Willett

Orav

A pooled analysis of vitamin D dose requirements for fracture prevention. N. Engl. J. Med. 367, 40–49 (2012).

38.

Autier

Gandini

. Vitamin D Suppl. ementation and total mortality: a meta-analysis of randomized controlled trials. Arch. Intern. Med. 167, 1730–1737 (2007).

39.

Zittermann

Iodice

Pilz

Grant

Bagnardi

Gandini

Vitamin D deficiency and mortality risk in the general population: a meta-analysis of prospective cohort studies. Am. J. Clin. Nutr. 95, 91–100 (2012).

40.

Bischoff-Ferrari

Dawson-Hughes

Staehelin

Fall prevention with supplemental and active forms of vitamin D: a meta-analysis of randomised controlled trials. BMJ 339, b3692 (2009).

41.

Murad

Elamin

Elnour

Abu NO

Clinical review: The effect of vitamin D on falls: a systematic review and meta-analysis. J. Clin. Endocrinol. Metab. 96, 2997–3006 (2011).

42.

Snijder

van Schoor

Pluijm

van Dam

Visser

Lips

Vitamin D status in relation to one-year risk of recurrent falling in older men and women. J. Clin. Endocrinol. Metab. 91, 2980–2985 (2006).

43.

Heaney

. Amount and type of protein influences bone health. Am. J. Clin. Nutr. 87(Suppl.), S1567–S1570 (2008).

44.

Alexy

Remer

Manz

Neu

Schoenau

. Long-term protein intake and dietary potential renal acid load are associated with bone modeling and remodeling at the proximal radius in healthy children. Am. J. Clin. Nutr. 82, 1107–1114 (2005).

45.

Scott

Blizzard

Fell

Giles

Jones

. Associations between dietary nutrient intake and muscle mass and strength in community-dwelling older adults: the Tasmanian Older Adult Cohort Study. J. Am. Geriatr. Soc. 58, 2129–2134 (2010).

46.

Gaillard

Alix

Boirie

Berrut

Ritz

. Are elderly hospitalized patients getting enough protein? J. Am. Geriatr. Soc. 56, 1045–1049 (2008).

47.

Houston

Nicklas

Ding

Dietary protein intake is associated with lean mass change in older, community-dwelling adults: the Health, Aging, and Body Composition (Health ABC) Study. Am. J. Clin. Nutr. 87, 150–155 (2008).

48.

Darling

Millward

Torgerson

Hewitt

Lanham-New

. Dietary protein and bone health: a systematic review and meta-analysis. Am. J. Clin. Nutr. 90, 1674–1692 (2009).

49.

Thorpe

Jacobson

Layman

Kris-Etherton

Evans

. A diet high in protein, dairy, and calcium attenuates bone loss over twelve months of weight loss and maintenance relative to a conventional high-carbohydrate diet in adults. J. Nutr. 138, 1096–1100 (2008).

50.

Josse

and Phillips

. Impact of milk consumption and resistance training on body composition of female athletes. Med. Sport Sci. 59, 94–103 (2012).

51.

Devine

Dick

Islam

Dhaliwal

Prince

. Protein consumption is an important predictor of lower limb bone mass in elderly women. Am. J. Clin. Nutr. 81, 1423–1428 (2005).

52.

Meng

Zhu

Devine

Kerr

Binns

Prince

. A 5-year cohort study of the effects of high protein intake won lean mass and BMC in elderly postmenopausal women. J. Bone Miner Res. 24, 1827–1834 (2009).

53.

Dawson-Hughes

Harris

Rasmussen

Song

Dallal

. Effect of dietary protein Suppl. ements on calcium excretion in healthy older men and women. J. Clin. Endocrinol. Metab. 89, 1169–1173 (2004).

54.

Hannan

Tucker

Dawson-Hughes

Cupples

Felson

Kiel

. Effect of dietary protein on bone loss in elderly men and women: the Framingham Osteoporosis Study. J. Bone Miner. Res. 15, 2504–2512 (2000).

55.

Munger

Cerhan

Chiu

. Prospective study of dietary protein intake and risk of hip fracture in postmenopausal women. Am. J. Clin. Nutr. 69, 147–152 (1999).

56.

Wengreen

Munger

West

Dietary protein intake and risk of osteoporotic hip fracture in elderly residents of Utah. J. Bone Miner. Res. 19, 537–545 (2004).

57.

Garnero

Sornay-Rendu

Delmas

. Low serum IGF-1 and occurrence of osteoporotic fractures. in postmenopausal women. Lancet 355, 898–899 (2000).

58.

Ross

Manson

Abrams

The 2011 report on dietary reference intakes for calcium and vitamin D from the Institute of Medicine: what clinicians need to know. J. Clin. Endocrinol. Metab. 96, 53–58 (2011).

59.

Kanis

McCloskey

Johansson

European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos. Int. 24, 23–57 (2013).

60.

Caroli

Poli

Ricotta

Banf

Cocchi

. Invited review: dairy intake and bone health: a viewpoint from the state of the art. J. Dairy Sci. 94, 5249–5262 (2011).

61.

Fulgoni

III Huth

DiRienzo

Miller

. Determination of the optimal number of dairy servings to ensure a low prevalence of inadequate calcium intake in Americans. J. Am. Coll. Nutr. 23, 651–659 (2004).

62.

Vissers

Streppel

Feskens

de Groot

. The contribution of dairy products to micronutrient intake in the Netherlands. J. Am. Coll. Nutr. 30, S415–S421 (2011).

63.

Scientific Committee on Food EC. Opinion of the Scientific Committee on Food on the tolerable upper intake level of vitamin D (2014). www.ewg.org/research/how-much-is-too-much

64.

USDA National Nutrient Database for Standard Reference. Release 26. 2013 http://ndb.nal.usda.gov/ndb/nutrients/index

65.

Josse

Tang

Tarnopolsky

Phillips

. Body composition and strength changes in women with milk and resistance exercise. Med. Sci. Sports Exerc. 42, 1122–1130 (2010).

66.

Kanis JA on behalf of the World Health Organization Scientific Group. Assessment of Osteoporosis at the Primary Healthcare Level. Technical Report WHO Collaborating Centre, University of Sheffield, UK (2008). www.who.int/chp/topics/Osteoporosis.pdf

67.

Bischoff-Ferrari

Dawson-Hughes

Baron

Milk intake and risk of hip fracture in men and women: a meta-analysis of prospective cohort studies. J. Bone Miner. Res. 26, 833–839 (2011).

68.

Sahni

Tucker

Kiel

Quach

Casey

Hannan

. Milk and yoghurt consumption are linked with higher bone mineral density but not with hip fracture: the Framingham Offspring Study. Arch. Osteoporos. 8, 119 (2013).

69.

Kardinaal

Ando

Charles

Dietary calcium and bone density in adolescent girls and young women in Europe. J. Bone Miner. Res. 14, 583–592 (1999).

70.

Castetbon

Vernay

Malon

Dietary intake, physical activity and nutritional status in adults: the French nutrition and health survey (ENNS, 2006–2007). Br. J. Nutr. 102, 733–743 (2009).

71.

Bruyere

Malaise

Neuprez

Collette

Reginster

. Prevalence of vitamin D inadequacy in European postmenopausal women. Curr. Med. Res. Opin. 23, 1939–1944(2007).

72.

Majem

Serra L

Barba

Ribas L

Castell

Salvador G

. Avaluacio de l'estat nutricional de la poblacio catalana 2002–2003. Departament de Salut, Generalitat de Catalunya, Barcelona. (2006) (Article in Catalan). www.gencat.net

73.

National Research Institute for Food and Nutrition Via Ardeatina 546, IRI. The Italian National Food Consumption Survey INRAN-SCAI 2005–2006 INRAN (2014). Hébel

Comportements et consommations alimentaires. en France. CCAF 2007 Survey-CREDOC Lavoisier (2014) (Article in French). http://www.pubfacts.com/detail/23865755

74.

Graca

Lino

Dias

. Instituto Nacional de Saude (INSA). Inquerito Nacional de Saude: Dados gerais, Continente 1998–1999 (2001) (Article in Portugeuse).

75.

Bajkova

Jordanov

Petrova

National survey of dietary intake and nutrition status of the Bulgarian population (2004).

76.

van der Wielen

Lowik

van den Berg

Serum vitamin D concentrations among elderly people in Europe. Lancet 346, 207–210 (1995).

77.

Bauer

Biolo

Cederholm

Evidence-based recommendations for optimal dietary protein intake in older people: a position paper from the PROT-AGE Study Group. J. Am. Med. Dir. Assoc. 14, 542–559 (2013).

78.

Morely

Argiles

Evans

Nutritional recommendations for the management of sarcopenia. J. Am. Med. Dir. Assoc. 11, 391–396 (2010).

79.

International Osteoporosis Foundation. IOF Osteoporosis Risk and Nutrition Awareness Survey (2006). www.iofbonehealth.org

80.

French

Vernace-Inserra

Hawker

. A prospective study to identify factors affecting adherence to recommended daily calcium intake in women with low bone mineral den sit y. J. Am. Coll. Nutr. 27, 88–95 (2008).

81.

Rice

Quann

Miller

. Meeting and exceeding dairy recommendations: effects of dairy consumption on nutrient intakes and risk of chronic disease. Nutr. Rev. 71, 209–223 (2013).

82.

Estok

Sedlak

Doheny

. Structural model for osteoporosis preventing behavior in postmenopausal women. Nurs. Res. 56, 148–158 (2007).

83.

McLeod

Johnson

. A systematic review of osteoporosis health beliefs in adult men and women. J. Osteoporos. 2011, 197454 (2011).

Nutrition and Bone Health in Women after the Menopause

Abstract

Keywords

Risk factors for osteoporosis

The role of nutrition in the prevention & management of osteoporosis

Calcium

Vitamin D

Protein

Nutritional targets for the reduction of osteoporosis risk

Role of dairy products in the reduction of osteoporosis risk

Calcium, vitamin D & protein insufficiency is common among postmenopausal women

What can be done to improve nutritional target attainment?

Conclusion

Future perspective

Footnotes

References