Dairy Products for Preventing Osteoporosis

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This entry is adapted from the peer-reviewed paper 10.3390/nu13041329

Breast milk is the best infant food, but milk should not be avoided later in life to prevent losing bone mass. On the other hand, more and more people limit their milk consumption and consume other dairy or non-dairy products. For example, they are usually replaced with plant beverages, which should be consumed carefully in several age groups. Additionally, an important element of milk and dairy products, as well as plant beverages, are probiotics and prebiotics, which may modulate bone turnover. Dietary recommendations focused on milk, and dairy products are an important element for the prevention of osteoporosis.

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1. Osteoporosis

Osteoporosis is a skeletal disorder with decreased bone mineral density (BMD) and bone strength, leading to increased risk of fractures. Osteoporosis may be divided into primary and secondary (70% and 30% of all cases, respectively). Secondary osteoporosis can be caused by several diseases, e.g., inflammatory bowel diseases, celiac disease, or endocrinology disorders ^[1]. Risk factors of osteoporosis are, among others, malabsorption, cigarette smoking, stress, air pollution, older age, low physical activity, and co-occurring diseases (Figure 1) ^[2]^[3]. Osteoporosis affects women twice as often as men. Additionally, it is estimated that 0.3 million and 1.7 million people have hip fractures in the USA and Europe, respectively ^[4]. Having a proper peak bone mass and maintaining it as long as possible is especially important for osteoporosis prevention.

Figure 1. Risk factors of osteoporosis.

It is vital to note that 1/3 adult people achieve their total bone mass between 2 and 4 Tanner stages, and 95% of peak bone mass is reached before the age of 16. For this reason, puberty is a key time for bone mass formation ^[5]^[6]. Data about the age of peak bone mass are inconsistent, and it is suggested that a peak bone mass is reached at around 18 years of age for women and 20 years of age for men ^[7]. However, other authors suggest peak bone mass is reached between 20 and 30 years of age ^[8].

Additionally, peak bone mass is influenced by genetic and environmental factors, including diet ^[9]. Therefore, proper intake of minerals and vitamins, especially vitamin D and calcium, is essential, especially in a period of rapid growth, such as childhood and adolescence. The next stage is bone remodeling, which leads to total rebuilding of the skeleton—once every ten years with no change in bone net weight. Proper intake of calcium and vitamin D helps maintain peak bone mass. The next stage is bone resorption, associated with higher activity of osteoclasts than osteoblasts, which results in a decreased bone mass and increased risk of fracture ^[5].

It is vital to notice that low vitamin D concentration causes hyperparathyroidism and decreases intestinal absorption of calcium, leading to bone resorption ^[10]^[11]. Vitamin D deficiency is associated with osteoporosis ^[12]. Moreover, women with fractures presented higher prevalence of vitamin D deficiency ^[13].

An important element of osteoporosis prevention is physical activity ^[14]. Physical activity increases BMD ^[15]. Additionally, regular exercise increases muscle strength, decreasing risk of fall and fracture ^[16].

Table 1 and Table 2 show calcium content in selected products and the Recommended Daily Intake of calcium for various age groups.

Table 1. Calcium content in selected products ^[17].

Products.	Portion	Calcium Content (mg)
Whole milk	200 mL	236
Semi-skimmed milk	200 mL	240
Skimmed milk	200 mL	244
Sheep milk	200 mL	380
Soy dring (non-enriched)	200 mL	26
Soy drink (calcium-enriched)	200 mL	240
Rice drink	200 mL	22
Almond milk	200 mL	90
Flavoured yoghurt	150 g	197
Natural yoghurt	150 g	207
Hard cheese (e.g., Parmesan, Cheddar)	30 g	240
Fresh cheese (e.g., Ricotta, cottage cheese)	200	138
Mozzarella	60	242

Table 2. Recommended Daily Intake of calcium for various age groups ^[18].

Age	RDI (mg)
0–6 months	200
7–12 months	260
1–3 years	700
4–8 years	1000
9–13 years	1300
14–18 years	1300
19–50 years	1000
51–70 years
Women	1200
Men	1000
71 years and older	1200
Pregnant and breastfeeding
Teenagers	1300
Adults	1000

RDI-Recommended Daily Intake.

2. Breast Milk

Compounds of breast milk may come from three sources: the diet of the mother, stocks storage by mother, and lactocytes ^[19]. The amount of produced milk was negatively correlated with maternal age and weight gained during pregnancy, but these factors did not affect the content of fat in milk. Diet also did not influence the amount and compounds of milk, especially the content of protein, fat, carbohydrates, iron, and calcium. Additionally, fat-soluble vitamins content depended on a mother’s diet to a smaller extent and water-soluble vitamins to a significant one ^[20]^[21].

Lactose is the main carbohydrate of human milk. It is made up of glucose and especially important galactose, which supports the development of the central nervous system. Additionally, breast milk contains oligosaccharides (about 15–23 g/L in colostrum and 1–10 g/L in mature milk) ^[22].

Supplementation of protein in the mother’s diet did not affect milk composition ^[23]. The main proteins in breast milk are casein, whey protein and mucin; however, protein content decreases with the child’s age ^[22].

Fats—mostly triacylglycerols (98%)—are a source of about 44% of total breast milk energy. Additionally, breast milk contains more than 200 various fatty acids (FA). The breast milk of European women contains 35–40% of saturated FA, 45–50% mono-unsaturated FA and 15% poly-unsaturated FA ^[22]. Moreover, the amount of long-chain FA and free FA is greater in human milk than cow’s milk ^[21]. Fat in human milk is absorbed at around 92%. It is vital to notice that the amount of cholesterol was lower in breast milk than in cow’s or sheep milk ^[24]. The composition of FA is dependent on the mother’s diet. Patin et al. have shown that, after consumption of 100g of fish (sardines) three times a week by breastfeeding women, the amount of omega-3 FA in breast milk was raised ^[25].

The optimum calcium:phosphorus (Ca:P) ratio is between 1:1 and 1:2 ^[26]. Furthermore, the Ca:P ratio is better in breast milk than cow’s milk (1.4–1.7:1 and 1.24:1, respectively) ^[27]. Additionally, the Ca:P ratio in cow’s milk is dependent on fat content and is higher in whole milk than skimmed ^[28].

Breast milk is also a source of immune factors, including Il2 (Interleukin 2), Il4, Il10, IgA (immunoglobulin A) total IgG, or macrophages. There were no significant differences in the amount of immune factors in breast milk from women after exposure to stress. However, two weeks after the stressful situation, the level of cortisol in milk was significantly higher. Moreover, breast milk also contains growth hormones ^[19]^[29].

3. Lactation and BMD

Breastfeeding may affect the BMD of both mother and child. Children who were initially (first six months of life) breastfed and later fed milk formula (up to 2 years old) had higher BMD than children only breastfed or only fed with milk formula (for the first two years of life) ^[30]. According to Blanco et al., exclusive breastfeeding for the first six months of life was associated with higher BMD in adolescents, when compared with mixed feeding ^[31]. Additionally, 6-year-old children who were breastfed presented higher BMD than children who were never breastfed. Among breastfed children, the group that was exclusively breastfed for minimum the first four months presented lower BMD and higher bone area (BA) than children who were not breastfed for the first four months ^[32].

On the other hand, among mothers, a breastfeeding period was negatively correlated with BMD of the lumbar spine. Additionally, the frequency of osteoporosis was higher among women who were breastfeeding for a minimum of 37 months than women who were breastfeeding for a shorter period. However, the age of the mother and number of deliveries did not correlate with BMD ^[33]. According to Tsvetov et al., a negative correlation between the number of deliveries and BMD was reported ^[34]. Moreover, breastfeeding for more than 18 months increased vertebral fracture risk more than twice in postmenopausal women ^[35]. In turn, Cooke-Hubley et al. reported that parity and lactation are not associated with higher risk of decreased BMD, clinical fragility or radiographic vertebral fractures over 10 years ^[36]. It is vital to notice that absorption of calcium during pregnancy increases, but this does not occur during lactation, and calcium is resorbed from the mother’s bones ^[37].

4. Cow’s Milk and Dairy Products and BMD

Milk and dairy products contain protein, minerals and vitamins (Figure 2), which may be beneficial for bone health ^[38]. Cultured dairy products (e.g., yoghurt and kefir) are formed by adding starter cultures, which convert the lactose in milk to lactic acid. For this reason, fermented dairy products may also contain bacteria, which are beneficial for human health ^[39].

Figure 2. The effect of cow’s milk on bone.

Studies have confirmed that dairy product consumption is essential for human health, especially in the pediatric group. Bone mineral content (BMC) was lower by about 5.6% in women aged 20–49 years who had consumed less than one portion of milk weekly during childhood, when compared with women who had consumed more than one portion. Additionally, low milk consumption during adolescence was associated with a 3% reduction in the BMD and BMC of the hip in adulthood. Among women over 50 years old, there was a non-linear association between milk consumption in childhood and adolescence and BMD and BMC of the hip. Moreover, low milk intake in childhood was linked with two times higher fracture risk ^[40]. For this reason, osteoporosis is called pediatric disease with geriatric consequences ^[41]. It is vital to note that children who had avoided milk and had not eaten food fortified with calcium reported fracture before puberty more frequently than children who had consumed cow’s milk ^[42]. Adults’ height correlated positively with the amount of milk consumed between the ages of 5–12 and 13–17 ^[43]. Higher consumption of dairy products was associated with higher total BMD among 6-year-old girls and boys. Additionally, positive association occurred between total BMD and intake of a minimum one portion of dairy products daily ^[44]. Sioen et al. have reported that consumption of dairy products by children (6–12 years old) positively affected total BMC and areal bone mineral density (aBMD) after adjusting for confounding factors ^[45]. Among young people (18–30 years old), total BMD was lower among people with lower dairy product consumption than subjects with proper intake. There was no significant difference in lumbar spine BMD among groups. It is vital to note that lower intake of dairy products was associated with higher BMI (Body Mass Index) and adipose tissue percentage ^[46]. On the other hand, as van Dongen et al. have shown, higher intake of milk, milk + yoghurt, and milk + yogurt + cheese was associated with higher trabecular and integral vBMD and VCS among men but not women ^[47]. Additionally, the positive impact of dairy products on BMD may depend on serum vitamin D levels. Intake of dairy products, fluid dairy and milk was associated with higher BMD of the femoral neck and lumbar spine among subjects with normal 25(OH)D concentration but not in a group with vitamin D deficiency ^[48]. Among 70-year-old women and men, total dairy product intake was positively associated with trabecular and cortical cross-sectional areas in the tibia and the areal bone mineral density of the radius ^[49].

On the other hand, as Michaëlsson et al. have reported, dairy product intake was linked with higher mortality in women and men and a higher risk of fracture among women in Sweden ^[50]. However, it should be mentioned that in Sweden, milk was fortified with vitamin A in the years 1987–1990 and 1997, which may influence the abovementioned results ^[51]. About 60% of dietary calcium should come from dairy products. Meeting dairy calcium requirements correlated positively with children’s BMD ^[52]. Meta-analysis has not shown a clear association between the group with an enormous amount of milk intake and risk of osteoporotic fracture and hip fracture. Additionally, results were heterogeneous and did not allow for clear conclusions ^[53].

5. Plant Milk (Plant Beverages) and BMD

In the last years, the market availability of plant products, substitutes for cow’s milk, has increased. These products are made from, among others, soybeans, rice, oats, almonds, coconut and are called plant milk or plant beverages. The most similar protein content to cow’s milk occurs in soya beverages. In turn, the content of protein in rice, oats and almond milk is very low. Plant beverages contain a lower amount of saturated fatty acids and do not contain cholesterol. However, producers frequently add fat and sugar to these products, which may increase the risk of metabolic disorders. Moreover, plant beverages contain a lower amount of iodine, potassium, phosphorus and selenium compared with semi-skimmed milk ^[41].

Data about the differences between the absorption of calcium from dairy and soy products are unclear ^[54]^[55]. It is vital to note that the Ca:P ratio in unfortified soya milk is lower than in cow’s milk (2:1 and 1.3:1, respectively). However, calcium fortification changes this ratio for the better (1.8:1) ^[56]. Nevertheless, calcium and vitamin D fortification of plant beverages is not obligatory in every country ^[57].

Soy products contain isoflavones, which show an affinity with the estrogen receptor and protects from loss of bone mass. 18-months of intake of cow’s milk fortified with calcium by postmenopausal women increased the BMD of the femoral neck significantly. However, consumption of soy-fortified milk decreased (not significantly) femoral neck BMD ^[58]. Additionally, intake of cow’s milk with soy isoflavones led to an increase in the level of 25OHD and a decrease in the concentration of bone turnover markers (osteoprotegerin and tartrate-resistant acid phosphatase) ^[59]. As Lydeking-Olsen et al. have reported among women divided into four groups—consuming soy products, treated with transdermal progesterone (TDP), combined group (consuming soy products and treated with TDP) and control group—BMD and BMC decreased significantly in combined and control groups. BMD and BMC increased in the soy group only, but differences were not significant ^[60]. An animal study has shown that isoflavones inhibited bone loss in mature female rats with a decreased level of estradiol ^[61].

An in vitro study has shown that germinated soy germ extracts increased expression of osteocalcin and alkaline phosphatase ^[62].

Among individuals who weekly drink 1.3 cups of soy milk fortified with calcium, decreased low T-score risk was decreased by 57% when compared with individuals who did not drink soy milk, even if they consumed dairy products ^[63]. Children are the group who are particularly vulnerable to nutrients deficiencies. Children that consumed plant beverages presented lower serum concentration of vitamin D than children who drank cow’s milk ^[57].

Cow’s milk is often replaced with plant milk by vegans. According to Ambroszkiewicz et al., people on a vegan diet consume an insufficient amount of calcium and vitamin D, which may lead to osteoporosis ^[64].

Consumption of unfortified beverages instead of breast milk, cow’s or modified milk may be especially harmful to children in the first year of life because it could lead to the development of rickets, failure in thrive, kwashiorkor, anaemia, metabolic alkalosis, scurvy and hyperoxaluria ^[65].

Table 3 and Table 4 present the content of nutrients in dairy products and various milks.

Table 3. Content of nutrients in 100 g of human, cow and plant milk.

	Human ^[66]	Cow’s ^[67]	Plant ^[68]
Fat (g)	3.8	3.7–3.9	0.66–49.2
Proteins (g)	1.0	3.2–3.5	0.59–19.00
Casein (g)	0.3	2.8	0
Carbohydrates (g)	7.0	7.0	27.3–50.0
Lactose (g)	7.0	0.9–4.9	0
Calcium (mg)	34	118	4.0–180.0
Phosphorus (mg)	15	89.6	49.0–1000.0
Sodium (mg)	15	44.5	2.2–140.01
Potassium (mg)	58	150	65.00–2000.0

Table 4. Content of macronutrients, calcium, phosphorus and vitamin D in milk and dairy products ^[69].

	Protein (g)	Fat (g)	Carbohydrates (g)	Calcium (mg)	Phosphorus (mg)	Ca:P Ratio	Wit.D (μg)
Milk, 3.5% fat	3.3	3.5	4.8	118	85	1.38	0.03
Milk, 2% fat	3.4	2.0	4.9	120	86	1.40	0.02
Cream, 18%	2.5	18.0	3.6	99	71	1.39	0.14
Natural yoghurt, 2%	4.3	2.0	6.2	170	122	1.39	0.03
Berries yoghurt	3.7	1.5	8.8	134	96	1.40	0.02
Cheddar cheese	27.1	31.7	0.1	703	487	1.44	0.26
Cottage cheese	12.3	4.3	3.3	80	140	0.57	0.09

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