Effect of Nutrient Intake, Nutritional Status, Physical Activity and Sunlight Exposure on Bone Mineral Density in Women: A Systematic Review

: Osteoporosis is a condition or disease that can cause bones to become brittle and break easily. The risk of osteoporosis in women is greater than in men, which is four times greater. Bone mineral density (BMD) or bone density is the total mineral present in bone. Measurement of BMD is important to show the degree of bone mineralization associated with osteoporosis. There are factors associated with reduced bone density. Thus, this systematic review aimed to analyze several factors related to BMD in women including nutrient intake, nutritional status, physical activity, and sunlight exposure. Studies in this systematic review were gathered by the (PRISMA) guidelines and identified through PubMed, Google Scholar, and ScienceDirect databases from 2017 until 2022. A total of 17 articles passed the eligibility and were analyzed in this systematic review. Studies found the effect of nutrient intake, BMI, physical activity, and sunlight exposure on BMD in women from different age groups. So it is necessary to make eating habits with good nutritional intake and have a lifestyle that routinely carries out sufficient physical activity and gets sufficient sunlight to improve and maintain bone health until old age.


INTRODUCTION
Bone mineral density (BMD) or bone density is the total mineral present in bone.Measurement of BMD is very important to determine the degree of bone mineralization.Osteoporosis requires attention because it can decrease the strength of the bones and increase major fracture risk [1].The decrease in density and quality of bone structure in osteoporosis is progressive.Osteoporosis is often called the "silent thief" stealing bone mass silently and also the "silent disease" because this disease comes on suddenly, has no obvious symptoms, and is not detected until it comes with fracture complication [2].
Osteoporosis occurs in approximately 200 million worldwide and osteoporosis is more common in postmenopausal women [3]. .The risk of osteoporosis in women is greater than in men, which is four times greater, the prevalence of osteoporosis in women in Indonesia is 23% in the old age group of 50-80 years and 53% in the 70-80 year age group [4].About 20% of osteoporosis-related fractures die within a year, one third of them must be bedridden, another third must be assisted to walk and only a third can recover and carry out normal activities [4].Fractures can cause physical, psychological, and social disorders that can affect the quality of life and increase the economic burden [5].
In women, a decrease in bone density occurs after menopause due to decreased levels of estrogen followed by an increase in calcium excretion from the body.Osteoporosis is more potential to occur in women because the protective effect of estrogen during the reproductive years prevents erosion of bone mass, and this protective effect ends in the menopausal period.[6].The estrogen reaches optimal levels in women of childbearing age.Women need to anticipate the menopausal conditions they will experience after passing reproductive age with an effort to maintain bone mass density.Around the age of 30-40 years, bone remodeling is in balance which in turn determines a person's bone mineral density [7].
Intake of nutrients is very important to increase the degree of bone mineralization.Protein and micronutrients in the form of calcium, vitamin D, potassium, and magnesium play an important role in maintaining bone health [8].Increasing protein intake can improve bone health which is related to increased BMD and bone turnover [9].Therefore, maintaining a healthy diet, especially dairy products, is very important for bone health.However, it's necessary to maintain normal nutritional status, because obesity is related to negative effects on BMD [10].
Calcium and vitamin D are important nutrients in the growth period.Vitamin D is needed in childhood and adulthood, since in the womb (utero), and during the growth period.Inadequate intake of calcium and vitamin D in addition to low physical activity can affect peak bone mass [11].A person who achieves a high peak bone mass will be able to reduce the risk of osteoporosis in the future [9].Vitamin D deficiency can cause growth retardation and bone deformity, which in old age will increase the risk of bone fracture.Vitamin D deficiency can disrupt calcium homeostasis and reduce bone mineralization [9], [12].Vitamin D activation can occur with the help of sunlight.Vitamin D deficiency generally occurs in four seasons of countries with less sunshine, but appropriate research shows that deficiency can also occur in tropical countries with two seasons [12].Based on the background described above, we conducted a systematic review of the published articles.This study aimed to analyze the effect of nutrient intake, nutritional status, physical activity, and sunlight exposure on BMD in women from observational studies.

METHOD
Studies in this systematic review were gathered by the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines.We conducted the literature search via PubMed, Google Scholar, and ScienceDirect databases from 2017 until 2022.The following search terms were used : ("bone mineral density" OR "bone density") AND ("nutrient intake" OR "nutrition" OR "nutritional status" OR "body mass index" OR "physical activity" OR "sunlight exposure") AND ("women" OR "female") to identify articles which were taken for further analysis.The inclusion criteria used for this study were: (1) articles were published in 2017-2022; (2) articles with observational study design; (3) articles had outcomes to women.Exclusion criteria included: (1) Articles were not in English or Indonesian language; (2) Articles were experimental studies or literature reviews; (3) no access to full-text articles.Women with a fracture had physical activity index lower than women without a fracture.Greater dietary calcium intake was related to higher BMD of the femoral neck, meanwhile, more cigarette intake was related to lower BMD of the femoral neck in men and women.

2.
Ménde For subjects with BMI< 50 kg/m 2 , an increase in BMI was related to higher BMD, however for subjects with BMI >50 kg/m 2 , an increase in BMI was related to lower BMD.

DISCUSSION
This study systematically reviewed 17 studies that used some observational study design including prospective longitudinal study, case-control, and cross-sectional study to see the effect of nutrients intake, nutritional status, physical activity and sunlight exposure on BMD focusing on women.The risk of osteoporosis in women is greater than in men [4].Osteoporosis is more common in women in old age because women after menopause experience increased bone resorption due to reduced levels of the hormone estrogen [29].Measurement of BMD is important to show the degree of bone mineralization associated with osteoporosis.Bone mineral density (BMD) or bone density is the total mineral present in bone.The World Health Organization (WHO) makes criteria for BMD based on a measurement, a T-score ≥ -1 SD is normal, a T-score between -1 SD and -2.5 SD is categorized as osteopenia, and a T-score ≤ -2.5 SD categorized osteoporosis [30].Nutritional intake is needed to optimize BMD and prevent osteoporosis.Pham et al [13] conducted a prospective longitudinal study and reported that higher dietary calcium intake was related to higher BMD and lower risk of fracture.Furthermore, the study conducted by Desrida et al [19] showed a positive relationship between calcium and vitamin D intake on BMD in adolescent girls.In addition, Kopiczko [22] suggested that sufficient dietary calcium and vitamin D intake was essential factor in bone tissue mineralization.Approximately 80-90% of bone contains minerals that are mainly filled with minerals calcium and phosphorus, so calcium had a major role in the occurrence of osteoporosis [31].The balance of calcium in the body is determined by the parathyroid hormone.If the calcium in the blood is normal, then the process of mineralization and demineralization takes place in balance.Low calcium intake accompanied by a decreased ability of the body to absorb calcium which generally occurs after menopause can cause a decrease in BMD [12].
Mineral Calcium is more contained in milk and dairy products.Cow's milk contains about 120 mg/100g of calcium [9].In addition, calcium is also found in non-dairy products such as fish, eggs, green vegetables, tofu, soybeans, and shellfish [32].Kim et al [20] conducted a study on South Korean adults, which showed that the frequency of milk consumption was related to high BMD and reduced risk of osteoporosis.Furthermore, Lee et al [21] examined the effect of both milk intake and physical activity in combination on BMD also in South Korean adults.The result was that medium to tough physical activity combined with the consumption of milk was related to BMD and supported bone health [21].Calcium intake will affect bone compression during the growth period and will affect the peak bone mass which can occur from the early age of 17-18 years to the end of the age of 35 years.Most of the bone mass will accumulate at the end of adolescence age both in men and women [12].
Additionally, not only calcium but other nutrients are also related to bone density.Al-Khammash et al [16] carried out a casecontrol study in postmenopausal women and showed that a poor diet that lacks carbohydrates, protein, fat, and water can reduce bone density, furthermore diet which is rich in ß-carotene, vitamin B6, C, E, Fe, Mg, Zn, Na, and phosphorus, had a preventive effect against osteoporosis.Groenendijk et al [17] found that great protein intake from animal sources was related to great BMD.Increasing protein intake by 0.8-0.9g/kg/day through the recommendation in certain conditions is beneficial for bone health because can increase BMD and bone turnover so which can lower the risk of fractures.Adequate protein is essential to maintain adequate BMD and strong muscle mass [9].
Vitamin D is very essential for maintaining bone health.Vitamin D regulates calcium and phosphorus to be available in the blood in the process of bone formation.Vitamin D in the body is mainly obtained from skin synthesis which begins with exposure to ultraviolet B, besides that vitamin D can also be obtained from foods but in a smaller amount [33].Lee et al [24] found an association between sunlight exposure with exposure duration ≥5 hours a day with a lower risk of fracture in patients with osteoporosis.Kopiczko [22] conducted a study on adult polish women and found that adequate past and present exposure to sunlight were the factors that significantly affect bone mineralization.Meanwhile, the study by Soomro et al [23] showed that osteopenia was quite common in the age group less than 25 years, with little exposure to sunlight, low physical activity, and inadequate dietary intake of calcium and vitamin D. Vitamin D was mainly obtained from sunlight, intake of food sources, supplementation and food intake fortification [12].
Vitamin D is often named the 'sun vitamin' in case it needs sunlight to metabolize it.Several recent studies have shown an increased vitamin D deficiency even in countries with sufficient sunshine.The cause of the deficiency is probably due to the influence of changes in lifestyle or food intake [12].Several factors affect the skin's ability to synthesize vitamin D from exposure to sunlight such as UV index, season, skin pigmentation, and age.Vitamin D formed in the skin can is better than vitamin D obtained from food because it lasts twice.Exposure to sunlight on the skin from the arms to the face for at least 30 minutes until the midday sun will suffice.Sun exposure of 10-15 minutes is sufficient for Asians at 11.5 LU whereas at 29 LU it takes 10-45 minutes with a longer duration in winter [34].Vitamin D in food is mainly in the shape of vitamin D3 and its metabolism is in the form of 25(OH)D3.Vitamin D from food is mainly found in animal sources in the form of cholecalciferol.The sources are fatty fish (such as salmon, tuna, and mackerel) and liver oils from fish.Little sources of vitamin D are in the liver, cheese, and egg yolks [9].
The way to determine a person's nutritional status is by anthropometric measurements, one of which is by assessing the body mass index (BMI).Some works of literature have studied the relationship between BMI and BMD.Méndez-Gallegos et al [14] conducted a prospective longitudinal study that found a relationship between BMI and BMD with a positive correlation in a group of first-time mothers 12 years ago.In addition, the study by Wang et al [25] showed an association between BMI and L1-4 BMD positively correlated.Several studies show obesity is a protective factor against osteoporosis.Hemmati et al [27] found that people with a high BMI will be at lower risk of osteoporosis.The prevalence of osteopenia and osteoporosis was lower in obese women [26] of Kim et al [28] in postmenopausal period Korean women had the result that in the women with a short menopausal period, the group with abdominal obesity has a lower risk of developing osteoporosis than those without abdominal obesity.However, Li et al [10] identified an inverted U-shaped relationship between BMI and BMD.For subjects with BMI< 50 kg/m 2 , an increase in BMI was related to an increase in BMD, however for subjects with BMI >50 kg/m 2 , an increase in BMI was related to a decrease in BMD [10].
An evaluation of the effect of obesity on BMD highlighted that increasing BMI helps support body weight [9].Excess body weight can cause metabolic changes in the form of insulin resistance and excessive production of androgen and estrogen hormones thereby reducing osteoblast action.Besides that, overproduction of adipokines or leptin levels due to high fat consumption may contribute to gained calcium absorption [35].However, excessive subcutaneous fat and visceral fat can increase systemic inflammation which can trigger bone loss, besides that it is associated with increased levels of proinflammatory cytokines such as TNF and IL-6 which can promote bone resorption and increase the risk of osteoporosis [26].
Physical activity has good benefits for individual health, including bone health.Desrida et al [19] had a study that resulted in an association between the level of physical activity and the bone density level of female adolescents.Young women with less active physical activity had a 36.64 times chance of having an abnormal bone density level compared to young women with active physical activity [19].Furthermore, in females, Lee et al [21] found that the group with milk intake and high-level physical activity had higher BMD.Meanwhile, Kopiczko [22] examined BMD and physical activity of women aged >40 years and the results showed the effects of past and present activity on BMD.Women with a fracture had physical activity index lower than women without a fracture [13].
The poorer the physical activity, the higher the risk of decreasing BMD.Lack of physical activity accelerates bone mass to be lost, while exercise bears the weight of the body and increases bone mass.For osteoporosis patients, the recommendations for an exercise program focused on maintaining a balance of posture, coordination, and stabilization of the hips and trunk.The recommended exercise for children and adolescents is at least 40 minutes of high-intensity, short-duration physical activity such as running or walking [9].Exercise can increase the peak bone mass in adolescent and prepubertal girls [36].High peak bone mass is essential for future bone health.The higher the peak bone mass gained, the lower the risk of osteoporosis.Sufficient physical activity will be very useful for lessening the risk of fractures by increasing BMD and reducing the risk of falling [9].
This review has the strength of focusing on women who are a group that is more susceptible to osteoporosis, as well as subjects from several age groups.This review also has limitations in the form of studies reviewed which are limited to observational studies and do not include experimental studies.Despite our limitations, this review provides useful knowledge regarding factors associated with BMD.

CONCLUSION
Bone mineral density (BMD) is important in relation to osteoporosis.Optimizing bone density from an early age can lessen the risk of osteoporosis and fractures in the future.Factors such as nutrient intake, nutritional status, physical activity, and sun exposure affect BMD.So it is necessary to make eating habits with good nutritional intake and have a lifestyle that routinely carries out sufficient physical activity and gets sufficient sunlight to improve and maintain bone health until old age.So we recommend further research in the future focusing on knowing more factors that affect BMD so that it can provide efforts to prevent osteoporosis.

Figure 1 .RESULT
Figure 1.Flow diagram of the studies included in the review.Adapted from PRISMA Flow Diagram.

Table 1 .
Elaboration of the articles analyzed