Applied nutritional investigation
Prevalence of lifestyle practices that might affect bone health in relation to vitamin D status among female Saudi adolescents
Rajaa Al-Raddadi M.D.
a,*, Suhad Bahijri Ph.D.
b, Anwar Borai Ph.D.
c, Zeyad AlRaddadi Ph.D.
daSaudi Ministry of Health, Research Department, Jeddah, Saudi Arabia
bKing Abdul-Aziz University, Biochemistry Department, Jeddah, Saudi Arabia
cKing Abdullah International Medical Research Center, King Saud Bin Abdulaziz University for Health Sciences, Pathology, King Abdulaziz Medical City, Jeddah, Saudi Arabia
dKing Faisal Specialist Hospital and Research Center, Research Center, Jeddah, Saudi Arabia
a r t i c l e i n f o
Article history:
Received 18 April 2017 Accepted 23 July 2017
Keywords:
Prevalence Lifestyle Bone health Saudi Adolescents Vitamin D Risk factors Schools
a b s t r a c t
Background:Prevention of osteoporosis begins in childhood and adolescence, as most bone mass is accumulated during thefirst 2 decades of life, with 90% to 95% of an adult’s bone mineral content being achieved by the end of adolescence. Therefore, targeting modifiable behaviors among adolescents has an important effect on attaining adequate peak bone mass and minimizing risks for future fractures.
Objectives:The aims of this study were to estimate the prevalence of behaviors affecting bone health and vitamin D status and to identify factors associated with vitamin D deficiency among female Saudi adolescents.
Methods:Several modifiable risk factors that influence bone health include low consumption of dairy products, physical inactivity, insufficient sun exposure, smoking, excessive consumption of soft drinks and caffeine, and vitamin D deficiency. A cross-sectional analytical study was conducted in secondary schools in Jeddah City with 421 randomly selected female adolescents. A predesigned questionnaire was used for data collection, and blood samples were collected to measure levels of vitamin D. Ac2test and correlation coefficient were used to identify the association between vitamin D and the independent variables. Mean (SD) age was 17.2 y (þ1.2 y). Mean vitamin D level was 46 nmol/L (þ24.6 nmol/L), ranging from 10.8 to 150.8 nmol/L.
Results:The adolescents reported low consumption of dairy products, low prevalence of sun exposure, and low physical inactivity. Prevalence of vitamin D deficiency was 67.5%, and insufficiency was 21%.
There were no significant associations between vitamin D status and sociodemographic characteristics;
coffee and tea intake; anthropometric measurements; and calcium and/or vitamin D supplementation.
Intake of dairy products was significantly positively correlated with vitamin D levels.
Conclusions:This study indicated that female Saudi adolescents are at significant risk for devel- oping osteoporosis on the basis of the prevalence of risky behaviors, including low consumption of dairy products, high consumption of soft drinks, deficiency in physical exercise, low sun exposure, and high prevalence of vitamin D deficiency and insufficiency.
Ó2017 Elsevier Inc. All rights reserved.
Introduction
Peak bone mass (PBM) is an important determinant of osteoporotic fracture risk[1,2]. PBM is conditioned by extensive interactions among different factors including genetic, hormonal, and nutritional, as well as physical activity [3–5].
Building and maintaining healthy bones helps to reduce the risk for the most common bone disease: osteoporosis[6–9].
This study was funded by the King Abdulaziz City for Science and Technology (KACS) (grant number: LGP-33-11), Saudi Arabia. The authors have no conflicts of interest to declare.
*Corresponding author. Tel.:þ96-650-559-1381; fax:þ96-667-61604.
E-mail address:[email protected](R. Al-Raddadi).
http://dx.doi.org/10.1016/j.nut.2017.07.015 0899-9007/Ó2017 Elsevier Inc. All rights reserved.
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Nutrition
jo u rn a l h o m e p a g e :w w w . n u t r i t i o n j r n l . c o m
A study conducted in Jeddah reported that osteopenia affects about 50% of Saudis. The study also reported a high prevalence of osteoporosis among women at the age of 30 y, which is the age they are supposed to have reached their PBM.
Furthermore, vitamin D deficiency is common among females in Saudi Arabia [10–12]. Vitamin D deficiency among Saudi adolescents was reported in several studies, ranging from 50%
to 100%[10,13–16]. As vitamin D deficiency precipitates and exacerbates osteoporosis among adults and causes osteoma- lacia [17–20], the reported high prevalence of vitamin D deficiency in adolescents predicts an increased prevalence of osteoporosis and osteoporotic fractures.
Prevention of osteoporosis begins in childhood and adoles- cence because most bone mass is accumulated during thefirst 2 decades of life, with 90% to 95% of an adult’s bone mineral content being achieved by the end of adolescence[2,21]. Bone density in any part of adulthood is the result of peak bone density achieved at the end of adolescence and subsequent lifelong bone loss[22]. Targeting modifiable behaviors among adolescents has important consequences for the attainment of adequate PBM and future fracture risk[23–28].
Several modifiable behaviors that influence bone health include low consumption of dairy products, physical inactivity, lack of or low degree of sun exposure, smoking, and excessive consumption of carbonated beverages and caffeine [9,25–27,29–33]. Hence, osteoporosis may be prevented or delayed by maximizing PBM through lifestyle modification, including improved nutrition, increased physical activity, abstinence from smoking, and increased sun exposure during adolescence[2,34–37].
A better understanding of the negative behaviors that affect bone health is crucial to successfully minimize their effect on the bones, the development of osteoporosis and related fractures, and the cost of health care. Therefore, the present study aimed to investigate all possible lifestyle practices that have been reported to affect bone health among female Saudi adolescents and to study the relationship of these practices to vitamin D status.
Methods
This cross-sectional analytical study was conducted in Jeddah City on adolescent females attending secondary schools. A sample size of 421 was calculated using StatCalc in an Epi Info program, assuming population size to be 50 000, an expected frequency of 50%, and a confidence limit of 5%. A total of 152 secondary schools were distributed geographically into four sectors, with each sector including between 36 and 40 schools. A multistage sampling technique was adopted to select the adolescents. In stage 1, two schools were selected by simple random sampling from each sector, so that eight schools were included in the study. In stage 2, one to three classes were selected randomly from each selected school in proportion to the number of the registered students in each school and classes. Ethical approval for the study was obtained from MOH Ethical Committee, and legal guardians of all participants signed an informed consent form.
Main outcome measures
A questionnaire was designed and structured to include demographic information and dietary intake. The questionnaire included a short list of ques- tions on daily intake of all available forms of dairy products as well as daily intake of beverages reported to affect bone health (such as tea, coffee, carbonated beverages, and energy drinks) using easily understood serving sizes.
Assessment of the dietary intake included questions that asked the students to recall how often over the previous week they consumed any type the dairy food including skim/low-fat or whole milk and Laban, Labna, white, yellow cream cheese, other cheese, qishta, ice cream and Muhallabia, and other related sweets.
A commonly used portion size was specified for each food (e.g., glass of milk).
Total dairy food intake was calculated by summing the daily servings of all the foods in the dairy group.
The questionnaire also asked about soft and energy drinks, coffee, and tea, specifying quantity and frequency.
Assessment of the other behaviors included questions about lifestyle practices including those on smoking habits, exposure to sunlight (body parts
exposed, duration of exposure, and use of skin protection creams), physical activity, and use of calcium and vitamin D supplements.
After a brief explanation, all participants were asked to complete the questionnaire. Additionally, trained research assistants recorded the students’
anthropometric measurements (height, weight, waist circumference [WC], and hip circumference [HC]).
Weight was measured in kilograms (kg) to the nearest 0.5 kg without shoes using a lever balance scale. The scale was calibrated daily at the beginning of each workday using a known weight to ensure accuracy. Height was measured to the nearest 0.5 cm without shoes while standing upright in an erect position on the base of the balance. WC was measured at the level of the umbilicus, and HC at the maximal protrusion of the gluteal muscles, both to the nearest 0.5 cm.
Participants were categorized as underweight if body mass index (BMI) was
<18.5 kg/m2, overweight if BMI was in the range of 25 to 29.9 kg/m2, and obese
if BMI30 kg/m2[38].
A fasting blood sample was collected at the same time to measure the serum level of 25-hydroxyvitamin D or 25(OH)D.
Serum 25(OH)D was assayed in an accredited clinical chemistry laboratory at the National Guard Hospital, King Abdulaziz Medical City-Jeddah, Kingdom of Saudi Arabia, on Abbott Architect i2000 autoanalyzer by using a two-step sandwich chemiluminescent micro particle immunoassay technique (Abbott Laboratories, Wiesbaden, Germany). The test was performed following the manufacturer’s recommendation, giving an intraassay coefficient of variation (CV) of 3.7%, and interassay CV of 4.6%. The following levels of serum 25(OH)D were used to determine vitamin D status: deficiency<50 nmol/L, insufficiency 50
to<75 nmol/L, and sufficiency75 nmol/L[39,40].
Statistical analysis
Statistical Package for Social Science version 21 (IBM, Armonk, NY, USA) was used for data entry and analysis. Continuous variables are presented as mean and SD, and qualitative variables as frequency and percentages.
The relationship between vitamin D and the independent variables was analyzed using ac2test and Pearson correlation. Tests were considered significant atP<0.05.
Results
This study included 421 adolescents with a mean age of 17.2 y (SD 1.2).
Sociodemographic characteristics of the study participants are shown in Table 1. The majority of the adolescents were underweight or of normal BMI (67.5%). A small percentage was obese (13.1%). Almost half of the participants (46.1%) reported very low consumption of dairy products. Only 11.2% of these students reported that they eat two or more servings of dairy products per day. The most commonly consumed type of dairy product was cheese; 12.2% of the participants ate two or more cheese servings per day.
Table 1
Sociodemographic characteristics of the study participants
Characteristics Frequency (%)
High school level (n¼390)
First 79 (20.3)
Second 103 (26.4)
Third 208 (53.3)
Accommodation (n¼405)
Villa 127 (31.4)
Apartment 278 (68.6)
Father’s education (n¼414)
Below secondary 86 (20.8)
Secondary 159 (38.4)
University and postgraduate 169 (40.8)
Mother’s education (n¼413)
Below secondary 121 (29.3)
Secondary 139 (33.7)
University and postgraduate 153 (37)
Mother’s employment status (n¼408)
Employed 95 (23.3)
Not employed 313 (76.7)
The studied population reported that canned soft drinks were the most popular beverage consumed, with 62.9% drinking one to four cans per week, 2.2% drinking no more than one can per week, and 32.5% not drinking any soft drinks. Regular black tea was the second most consumed beverage, with 8.5% reporting daily intake, 36.1% drinking black tea more than one to four times per week, and 51.3% not drinking black tea on a regular basis.
On the other hand, green tea was ingested daily by 3.8% of the girls, and 77.7% reported complete avoidance. Additionally, 19.2%
of the sample reported drinking energy drinks one to six times per week, whereas not all types of coffee were popular among the sample; 94.1% did not drink American coffee compared with 85% for Turkish and 56.8% for Arabic coffee. Only 8.1% reported daily intake of Arabic coffee (Table 2).
Of the participants, only 12.4% were taking calcium and vitamin D supplements. Smoking, physical activity patterns, and period of sun exposure are presented inTable 3. Most of the participating adolescents reported avoidance of sun exposure.
More than 40% reported a complete lack of exercise, and 13.9%
reporting that they performed the recommended exercise per week. A very small percentage (4.1%) admitted to smoking, as shown inTable 3.
The mean vitamin D level was 46 nmol/L, SD24.6 ranging between 10.8 and 150.8. Using a cutoff value for serum 25(OH)D
levels of<50 nmol/L to define deficiency and 50 to<75 nmol/L to suspect insufficiency, 67.5% were found to be deficient and 21%
were suspected to have vitamin D insufficiency (Fig. 1).
Furthermore, no significant relationship was found between vitamin D status and lifestyle practices (sun exposure, exercise, and smoking), with P values ranging from 0.2 for exercise intensity and covering most of the body during sun exposure to 0.8 for smoking and duration of sun exposure, as seen inTable 4.
No significant association was found in the relationship between sociodemographic characteristics and vitamin D.
Similarly, no significant correlation was found between consumption of dairy products and vitamin D for any single dairy product; however, the overall consumption was significantly positively correlated with vitamin D level (P<0.001) (Table 5).
Moreover, no significant correlation was found between the consumption of various beverages and vitamin D status.
Discussion
Different stages of the life cycle dictate differing nutrient needs. Total nutrient needs are higher during adolescence than at any other time in the life cycle because of the phenomenal growth that occurs in adolescence, and optimal nutrition is a requisite for achieving full growth potential[41–43]. Indeed, studies reported that vitamin D deficiency is very prevalent among Saudi adoles- cents, ranging from about 50% to 100% [10,13–16]. This high prevalence of vitamin D deficiency during adolescence could increase the risk for osteomalacia, osteoporosis, and osteoporotic fractures later in life[17–20].
Choosing this particular age group, we aimed to investigate the prevalence of factors and behaviors previously reported to affect bone health and vitamin D status among Saudi females.
Additionally, we aimed to identify the factors associated with vitamin D deficiency. Because dietary studies on Saudis, and in particular on Saudi adolescents, are very limited, the present study provided baseline information for further epidemiologic studies and for planning appropriate prevention programs, which are recommended as the most powerful tool for reducing incidences of osteoporosis.
Physical activity provides the stimulus to build and retain bone in the body[24,44–49]. Therefore, exercise is essential for bone health. The present study revealed that 43.7% of the par- ticipants did not perform any exercise, and only 13.9% performed the recommended weekly amount of exercise.
Numerous studies have documented inverse relationships between smoking and both bone mass and fracture risk[50].
Only 4.1% of the studied adolescents admitted to smoking. This is Table 2
Participants’patterns of consumption of dairy products, coffee, tea, and soft and energy drinks
Dietary factors Serving Frequency %
Milk Never 380 90.3
1–2/d 33 7.8
2/d 8 1.9
Cheese Never 118 28.3
1–2/d 248 59.5
2/d 51 12.2
Laban Never 395 93.8
1–2/d 26 6.2
Other dairy products Never 335 80.3
1–2/d 82 19.7
All dairy product Never 194 46.1
1–2/d 180 42.8
2/d 47 11.2
Arabic coffee Never 239 56.8
1–4/wk 132 31.4
5–6/wk 16 3.8
1/d 34 8.1
Turkish coffee Never 358 85
1–4/wk 47 11.2
5–6/wk 7 1.7
1/d 9 2.1
American coffee Never 396 94.1
1–4/wk 21 5
5–6/wk 2 0.5
1/d 2 0.5
Black tea Never 216 51.3
1–4/wk 152 36.1
5–6/wk 17 4
1/d 36 8.5
Green tea Never 327 77.7
1–4/wk 68 16.2
5–6/wk 10 2.4
1/d 16 3.8
Soft drink Never 137 32.5
1–4/wk 265 62.9
5–6/wk 10 2.4
1/d 9 2.2
Energy drink Never 340 80.8
1–4/wk 78 18.5
5–6/wk 3 0.7
Table 3
Participants’smoking, physical activities, and sun exposure
Behaviors Frequency %
Sun exposure (n¼421)
Never 208 49.4
<15 min/d 160 38
15 to<30 min/d 29 6.9
30 min/d 24 5.7 Exercise (n¼410)
Never 179 43.7
<60 min 92 22.4
60 to<150 min 82 20
150 min 57 13.9 Smoking (n¼414)
No 393 94.9
Yes 17 4.1
Former smoker 4 1
a lower percentage than that reported in previous studies for adolescents in Madinah and Riyadh [51,52]. However, these studies included boys; hence, a higher prevalence was expected.
Furthermore, because smoking is frowned upon, smoking behavior could be underreported.
Calcium needs during adolescence are greater than in child- hood or adulthood because of the dramatic increase in skeletal growth. As w45% of PBM is attained during adolescence, adequate calcium intake is required for the development of dense bone mass and the reduction of the lifetime risk for frac- tures and osteoporosis [3,53]. The low dietary intake may include all macro- and micronutrients, including nutrients needed for bone health. Indeed, consumption of dairy products was generally very low among the participants; only 11.2%
consumed two or more servings of dairy products per day, and almost half of the students did not consume any kind of dairy product. This is in agreement with an earlier study reporting that 80% of Saudi adolescents fail to consume the currently recom- mended three daily servings of milk, cheese, or yogurt[54], thus raising alarm and emphasizing the need to try to increase consumption of dairy products among adolescents.
On the other hand, the participants consumed empty calories in soft drinks and sweetened tea. Studies indicate that high consumption of carbonated soft drinks, particularly colas, during the adolescent period may reduce bone mineral accrual and
increase fracture risk [55,56]. An earlier study reported that w30% of Saudi adolescents consumed carbonated soft drinks regularly[57]. We found that only 32.5% of our sample said they never drank soft drinks, whereas the remaining 67.5% consumed at least one to four cans on a weekly basis, with some partici- pants drinking even more. Almost 20% of the participants reported drinking energy drinks. Similar results were found for tea consumption (Table 4). Caffeine increases the urinary excretion of calcium. In contrast, intake of calcium and vitamin D supplements was reported by only 12.4% of the participants.
These and other factors, including low consumption of dairy products, increase the list of noted factors deleterious to bone health in the studied population.
Vitamin D is one of the factors reported to affect bone health, mainly through its effect on calcium and phosphate homeostasis.
In accordance with previous studies that reported a high prev- alence of vitamin D deficiency[10,13–16]: 67.5% of the partici- pants were found to be deficient, and 21% were suspected to have vitamin D insufficiency status on the basis of internationally suggested cutoff values[39,40]. This is not surprising in light of the reported avoidance of sun exposure by most of the partici- pating adolescents (89.3% reported<15 min/d), and only 3.8% of the participants had sun exposure of>30 min/d as well as a low intake of vitamin D-fortified dairy products and vitamin D sup- plements. The significant and positive correlation between intake of dairy products and vitamin D levels might be attributed to the most commonly used dairy products being enriched with vitamin D, even if not to the needed extent[58]. Similarfindings were indicated by Al-Daghri et al. who reported that“frequency of fresh milk consumption affected vitamin D levels in the overall population and more specifically in children and female sex,” and that“frequency of overall dairy product consumption was significantly associated with vitamin D status in women”[59].
However, no significant association was found between our estimated vitamin D levels and sociodemographic characteris- tics, consumption of various beverages, sun exposure, and smoking, although significant association was reported in earlier studies between sun exposure and dietary vitamin D. There could be a number of reasons that explain these contradicting results. They could be due to inherent self-reporting bias or the possibility that the cutoff used to define deficiency and insuffi- ciency in other populations is not applicable to Saudis.
Conclusion
Certain behaviors deleterious to bone health in the studied population are common, including lack of physical activity, avoidance of and low exposure to sunlight, and poor dietary Fig. 1.Prevalence of vitamin D deficiency and insufficiency among the participants
according to serum 25(OH)D level.
Table 4
Vitamin D status in relation to sun exposure, exercise, and smoking
Variables 25(OH)D nmol/L Pvalue
Deficiency n (%) Insufficient n (%) Normal n (%) Sun exposure, min/d
Never 129 (65.5) 74 (23.9) 21 (10.7) 0.8
<15 106 (69.7) 27 (17.8) 19 (12.5)
15 35 (68.6) 10 (19.6) 5 (11.8)
30 16 (72.7) 3 (13.6) 3 (13.6)
Covering most of the body during sun exposure
No 42 (64.6) 11 (16.9) 12 (18.5) 0.2
Yes 151 (76.1) 49 (21.8) 25 (11.1)
Applying sun protection agents
No 166 (65.4) 55 (21.7) 33 (13) 0.6
Yes 27 (73) 7 (18.9) 3 (8.1)
Exercise, min/wk
Never 107 (63.7) 33 (19.6) 28 (16.7) 0.2
<60 59 (67) 22 (25) 7 (8)
60 to<150 58 (71.6) 17 (21) 6 (7.4)
150 38 (73.1) 9 (17.3) 5 (9.6)
Smoking
No 255 (67.5) 80 (21.2) 43 (11.4) 0.8
Yes 11 (68.8) 4 (25) 1 (6.3)
Table 5
Correlation between lifestyle variables, anthropometric measurements, and vitamin D levels
Variables Correlation coefficient Pvalue
Milk, serving/d 0.1 0.8
Laban, serving/d 0.1 0.1
Cheese, serving/d 0.04 0.3
Other dairy products, serving/d 0.03 0.6
Total dairy products, serving/d 0.4 <0.001
Weight 0.05 0.3
BMI 0.05 0.3
Waist circumference 0.09 0.1
Hip circumferences 0.04 0.4
W/Hip 0.09 0.1
W/Height 0.09 0.1
BMI, body mass index; W, waist
practices such as low intake of dairy products and high consumption of soft drinks and caffeinated beverages.
These factors lead to deterioration in bone health and promote progression to osteoporosis and poor bone health consequences. Social factors, in particular insufficient exposure to sunlight, may play a role in the noted high prevalence of vitamin D deficiency.
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