The health impact of osteoporosis on individuals and the population at large is huge and its effect on national economies is negative. The aim of this study was to investigate the association between coffee consumption and osteopenia/osteoporosis in premenopausal and postmenopausal women in Taiwan. Data of 2929 women who completed a questionnaire about their weekly coffee consumption and bone health were retrieved from the Li-Shin Hospital (2006-2011). Coffee consumption was classified into 0, 1-4 and 5-7 cups per week (1 cup was equivalent to 400 mL). Osteoporosis and osteopenia were defined using bone mineral densities measured by quantitative ultrasound (QUS). Multiple logistic regression was used to determine the association between coffee drinking and osteopenia/osteoporosis. After exclusions were made, a total of 2533 participants were included in the final analysis. Adjusted confounders included age, hepatitis B surface antigen (HBsAg), anti-Hepatitis C virus (HCV), waist-hip ratio (WHR), body mass index (BMI), smoking, alcohol, tea, exercise, vegetarian diet, supplements, yogurt, education, and blood type. There were 1336 premenopausal and 1593 postmenopausal women at baseline. Among the premenopausal women, an increase in the weekly coffee consumption significantly decreased the odds for osteoporosis (P-trend = 0.0179). The consumption of 1-4 and 5-7 cups of coffee per week significantly reduced the risk of osteoporosis/osteopenia (OR = 0.677; 95% C.I. = 0.469-0.978) and (OR = 0.607; 95% C.I. = 0.400-0.923), respectively. Among postmenopausal women, however, there was no significant relationship between weekly coffee consumption and osteoporosis/osteopenia. It was concluded that coffee drinking might likely minimize the risk of osteoporosis/osteopenia in premenopausal Taiwanese women.
Osteoporosis is defined as a progressive systemic skeletal disease characterized by reduced quantity and quality of bones. In this condition, the quantity of bone (bone mineral density) is >2.5 standard deviations below the young adult’s race/gender-adjusted mean. Osteopenia, on the other hand, is a condition where the bone mineral density is between -1 and -2.5 standard deviations below the young adult’s race/gender-adjusted mean. Osteopenia can lead to osteoporosis which in turn can increase the risk of fractures. Most patients are often diagnosed with osteoporosis following bone fractures. In such cases, osteopenia might have become more severe thereby leading to more bone quality deterioration and loss.
Osteopenia and osteoporosis are associated with several modifiable/non-modifiable risk factors 1, 2. Generally, both conditions are more common in the elderly 3, 4, 5, 6, especially in females 7, 8, 9. Some preventive modifiable factors for osteoporosis and osteopenia include higher BMI 10, 11, 12, 13, 14, calcium and vitamin D intake 15, 16, among others. Currently, coffee is among the most consumed beverages and its consumption is global. Several studies have been carried out to assess the relationship between coffee drinking and osteopenia or osteoporosis. Nonetheless, the results have been inconsistent 17, 18, 19, 20. For instance, the consumption of 600 mL or more of coffee per day was associated with an increased osteoporotic fracture risk in Swedish women 19. However, higher amounts of coffee were not associated with increased risk of fractures in Swedish women 18. Moreover, coffee drinking was shown to be preventive against osteoporosis in postmenopausal women 21. Most previous studies did not stratify their participants by menopausal status. This study therefore aimed at investigating the association between coffee consumption and osteopenia or osteoporosis in premenopausal and postmenopausal women in Taiwan.
A total of 2929 participants consisting of 1336 premenopausal and 1593 postmenopausal women aged 30 years and above who lived in the Pingzhen District of Taoyuan city from 2006 to 2011 were enrolled in the study. Their information was retrieved from the Li-Shin Hospital, a regional hospital in Northern Taiwan. They responded to a questionnaire about their weekly coffee consumption and other factors including age, smoking, alcohol, tea, exercise, diet, disease history, educational level, and blood type. The BMI and WHR were also determined. Coffee consumption was classified into 0, 1-4 and 5-7 cups per week. A cup of coffee was equivalent to 400 mL. Bone mineral density was measured by quantitative ultrasound (QUS). Osteopenia and osteoporosis were defined as -2.5<T-score<-1 and T-score≤-2.5, respectively. Multiple logistic regression analysis was used to determine the relationship between coffee drinking and osteopenia/osteoporosis. The analysis included 2533 participants comprising 1198 premenopausal and 1335 postmenopausal women after those with missing data (n = 396) were excluded. Osteopenia and osteoporosis (i.e. all T-scores<-1) were considered as a single outcome and odds ratios with their 95% confidence intervals were computed. Multivariate adjustments were performed for confounders including age, hepatitis B surface antigen (HBsAg), anti-Hepatitis C virus (HCV), waist-hip ratio (WHR), body mass index (BMI), smoking, alcohol, tea, exercise, vegetarian diet, supplements (vitamins A, B, C, D, E and calcium), yogurt, education and blood type. The study was approved by the Antai Medical Care Cooperation Antai Tian-Sheng Memorial Hospital Institutional Review Board (No. 15-018-B1).
Table 1 shows the baseline data of the study participants. There were 1336 premenopausal and 1593 postmenopausal women with mean ages of 43.161 and 58.878 years, respectively. Table 2 presents the odds ratios for osteoporosis/osteopenia in premenopausal women. After multivariate adjustments, the consumption of 1-4 and 5-7 cups of coffee per week significantly decreased the risk of osteoporosis/osteopenia (OR = 0.677; 95% C.I. = 0.469-0.978) and (OR = 0.607; 95% C.I. = 0.400-0.923), respectively (P-trend = 0.0179). Moreover, higher BMI and education above college level also significantly decreased the risk (OR = 0.906; 95% C.I. = 0.863-0.951) and (OR = 0.487; 95% C.I. = 0.273-0.867), respectively.
However, increasing age was a significant risk factor of osteoporosis (OR = 1.046; 95% C.I. = 1.022-1.072). The odds ratios for osteoporosis/osteopenia in postmenopausal women are shown in Table 3. After adjusting for covariates, there was no significant association between coffee consumption and osteoporosis/osteopenia. Higher BMI significantly reduced the risk of osteoporosis/osteopenia (OR = 0.954; 95% C.I. = 0.923-0.987). However, high vitamin C and increasing age were significant risk factors of osteoporosis/osteopenia (OR = 2.022; 95% C.I. = 1.093-3.741) and (OR = 1.079; 95% C.I. = 1.059-1.099), respectively. Surprisingly, calcium and vitamin D had no significant effects on osteoporosis/osteopenia in both premenopausal and postmenopausal women.
To our knowledge, this is the first study to demonstrate that coffee consumption might prevent osteoporosis/osteopenia in premenopausal Taiwanese women. Osteoporosis is common in women 7, 8, 9 even though the risk is lower in premenopausal than postmenopausal women 22. While more attention has been paid to postmenopausal osteoporosis, premenopausal osteoporosis, on the other hand, has not been equally explored probably due to its low incidence. Notwithstanding, preventive factors of premenopausal osteoporosis should be identified to avoid damages that might occur later in life. There are controversies regarding the effects of coffee consumption on osteoporosis 17, 18, 19, 20, 23. In a recent study, coffee consumption was protective against osteoporosis in postmenopausal Korean women 17. However, premenopausal women were excluded from the study. Another study showed no significant association between coffee consumption and bone mineral density of either the femoral neck or lumbar spine among Korean premenopausal women 16, 17. Similarly, a study exploring how someone’s smoking and coffee consumption habits in the premenopausal stage could affect the postmenopausal bone mineral density showed no significant effect 24. Discrepancies between our study and previous studies may be due to different volumes of weekly coffee intake 18, 19, 23. Furthermore, differences in sample sizes, study designs, ethnicities, among others might have contributed to these discrepancies. The preventive effect of coffee on osteoporosis has been attributed to some of its biochemical components other than caffeine. For instance, Choi and colleagues 21 explained it based on chlorogenic acids and kahweol which have antioxidant and anti-inflammatory properties, respectively. Higher BMI significantly reduced the risk of osteoporosis in both premenopausal and postmenopausal women. Similar results have previously been shown in women 10, 11, 12, 13, 14. Increase in age is a potential non-modifiable risk factor for osteopenia and osteoporosis 1, 4, 5, 10. This was evident among both the premenopausal and postmenopausal women included in our study. Over time, both the quantity and quality of bone continue to deteriorate, increasing the chances of developing osteoporotic fractures. Intervention with calcium and vitamin D supplements could help to reduce osteoporosis at old age 15, 16. Nonetheless, both calcium and vitamin D had no significant influence on osteoporosis/osteopenia in the present study. Education above college level was shown to be preventive against osteoporosis/osteopenia among the premenopausal women involved in the current study. This was consistent with some previous studies where higher educational level had a protective role on osteoporosis 25, 26, 27, 28. Education plays a good role in bringing awareness to individuals about most diseases and their risk factors. This could help these individuals in preventing the diseases by modifying their lifestyles like physical activities and nutritional intake. Osteoclastogenesis and osteoblastogenesis are some potential protective mechanisms of Vitamin C’s role on bone health 29, 30, 31, 32. Previous cross-sectional studies have shown positive though inconsistent effects of Vitamin C on osteoporosis 33, 34, 35, 36. However, this study negatively associated high vitamin C with the risk of osteoporosis among postmenopausal women. The reason for such an observation cannot be clearly explained.
As a limitation, bone mineral density was measured using quantitative ultrasound (QUS) instead of the recommended dual-energy x-ray absorptiometry (DXA). However, a high precision and reliability have been demonstrated when QUS was used to measure BMD and strong correlations were found between T-scores measured by QUS and those measured by DXA 37, 38. This demonstrates the potential of QUS in osteoporosis and fracture risk screening 39. Moreover, its use is convenient due to its cost-effectiveness, non-ionizing nature, and portability. Even though QUS is not a recommended diagnostic test for osteoporosis, the guidelines for the diagnosis and management of osteoporosis does not prevent its use in fracture risk assessment especially in the absence of DXA 40. Another limitation of this study is its cross-sectional nature which could not be used to make causal inferences. However, coffee drinking is a habit and its impact on bone health cannot be rolled out.
This study concludes that coffee drinking might be preventive against osteoporosis/osteopenia in premenopausal women. However, there is no significant effect in postmenopausal women. In order to curtail premenopausal osteoporosis/osteopenia, coffee drinking should, therefore, be encouraged. Further studies are warranted to fully confirm the preventive effect of coffee drinking on premenopausal osteoporosis/osteopenia.
This study was partly funded by grants from the Landseed Hospital (CSMU-LSH-103-02, CSMU-LSH-104-01, CSMU-LSH-105-01, and CSMU-LSH-106-01).
The authors have no competing interests.
[1] | Abrahamsen B, Brask-Lindemann D, Rubin KH, Schwarz P. A review of lifestyle, smoking and other modifiable risk factors for osteoporotic fractures. Bonekey reports. 2014;3. | ||
In article | View Article | ||
[2] | Snelling AM, Crespo CJ, Schaeffer M, Smith S, Walbourn L. Modifiable and nonmodifiable factors associated with osteoporosis in postmenopausal women: results from the Third National Health and Nutrition Examination Survey, 1988-1994. Journal of women's health & gender-based medicine. 2001; 10(1): 57-65. | ||
In article | View Article PubMed | ||
[3] | Compston JE, Papapoulos S, Blanchard F. Report on osteoporosis in the European community: current status and recommendations for the future. Osteoporosis international. 1998; 8(6): 531-4. | ||
In article | View Article PubMed | ||
[4] | Guggenbuhl P. Osteoporosis in males and females: Is there really a difference? Joint Bone Spine. 2009; 76(6): 595-601. | ||
In article | View Article PubMed | ||
[5] | Woolf AD, Pfleger B. Burden of major musculoskeletal conditions. Bulletin of the World Health Organization. 2003; 81(9): 646-56. | ||
In article | PubMed PubMed | ||
[6] | MacLaughlin EJ, Sleeper RB, McNatty D, Raehl CL. Management of age-related osteoporosis and prevention of associated fractures. Therapeutics and clinical risk management. 2006; 2(3): 281. | ||
In article | View Article PubMed | ||
[7] | Cawthon PM. Gender differences in osteoporosis and fractures. Clinical Orthopaedics and Related Research®. 2011; 469(7): 1900-5. | ||
In article | View Article PubMed | ||
[8] | Melton LJ, Chrischilles EA, Cooper C, Lane AW, Riggs BL. How many women have osteoporosis? Journal of bone and mineral research. 2005; 20(5): 886-92. | ||
In article | View Article PubMed | ||
[9] | Pietschmann P, Rauner M, Sipos W, Kerschan-Schindl K. Osteoporosis: an age-related and gender-specific disease–a mini-review. Gerontology. 2009; 55(1): 3-12. | ||
In article | View Article PubMed | ||
[10] | Aggarwal N, Raveendran A, Khandelwal N, Sen RK, Thakur J, Dhaliwal LK, et al. Prevalence and related risk factors of osteoporosis in peri-and postmenopausal Indian women. Journal of mid-life health. 2011; 2(2): 81. | ||
In article | View Article PubMed | ||
[11] | Asomaning K, Bertone-Johnson ER, Nasca PC, Hooven F, Pekow PS. The association between body mass index and osteoporosis in patients referred for a bone mineral density examination. Journal of Women's Health. 2006; 15(9): 1028-34. | ||
In article | View Article PubMed | ||
[12] | De Laet C, Kanis J, Odén A, Johanson H, Johnell O, Delmas P, et al. Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporosis international. 2005; 16(11): 1330-8. | ||
In article | View Article PubMed | ||
[13] | Jain V, Agrawal B, Varshney A, Biswas S. Prediction of bone mineral density by age, body mass index and menopausal status in middle socioeconomic status women of urban Kolar region of Bhopal. IOSR Journal of Dental and Medical Sciences. 2013; 12(3): 17-21. | ||
In article | View Article | ||
[14] | Oldroyd A, Mitchell K, Bukhari M. The prevalence of osteoporosis in an older population with very high body mass index: evidence for an association. International journal of clinical practice. 2014; 68(6): 771-4. | ||
In article | View Article PubMed | ||
[15] | Chapuy M, Schott A, Garnero P, Hans D, Delmas P, Meunier P. Healthy elderly French women living at home have secondary hyperparathyroidism and high bone turnover in winter. EPIDOS Study Group. The Journal of Clinical Endocrinology & Metabolism. 1996; 81(3):1129-33. | ||
In article | PubMed | ||
[16] | Kim SY. Coffee consumption and risk of osteoporosis. Korean journal of family medicine. 2014; 35(1): 1. | ||
In article | View Article PubMed | ||
[17] | Choi E-J, Kim K-H, Koh Y-J, Lee J-S, Lee D-R, Park SM. Coffee consumption and bone mineral density in Korean premenopausal women. Korean journal of family medicine. 2014; 35(1): 11-8. | ||
In article | View Article PubMed | ||
[18] | Hallström H, Byberg L, Glynn A, Lemming EW, Wolk A, Michaëlsson K. Long-term coffee consumption in relation to fracture risk and bone mineral density in women. American journal of epidemiology. 2013:kwt062. | ||
In article | View Article PubMed | ||
[19] | Hallström H, Wolk A, Glynn A, Michaëlsson K. Coffee, tea and caffeine consumption in relation to osteoporotic fracture risk in a cohort of Swedish women. Osteoporosis international. 2006; 17(7): 1055-64. | ||
In article | View Article PubMed | ||
[20] | Lacerda SA, Matuoka RI, Macedo RM, Petenusci SO, Campos AA, Brentegani LG. Bone quality associated with daily intake of coffee: a biochemical, radiographic and histometric study. Brazilian dental journal. 2010; 21(3):199-204. | ||
In article | View Article PubMed | ||
[21] | Choi E, Choi K-H, Park SM, Shin D, Joh H-K, Cho E. The Benefit of Bone Health by Drinking Coffee among Korean Postmenopausal Women: A Cross-Sectional Analysis of the Fourth & Fifth Korea National Health and Nutrition Examination Surveys. PloS one. 2016; 11(1): e0147762. | ||
In article | View Article PubMed | ||
[22] | Cheng ML, Gupta V. Premenopausal osteoporosis. Indian journal of endocrinology and metabolism. 2013; 17(2): 240. | ||
In article | View Article PubMed | ||
[23] | Kapetanovic A, Avdic D. Influence of coffee consumption on bone mineral density in postmenopausal women with estrogen deficiency in menstrual history. Journal of Health Sciences. 2014; 4(2). | ||
In article | View Article | ||
[24] | Demirbag D, Ozdemir F, Ture M. Effects of coffee consumption and smoking habit on bone mineral density. Rheumatology international. 2006; 26(6): 530-5. | ||
In article | View Article PubMed | ||
[25] | Akkus Z, Camdeviren H, Celik F, Gur A, Nas K. Determination of osteoporosis risk factors using a multiple logistic regression model in postmenopausal Turkish women. Saudi medical journal. 2005; 26(9): 1351-9. | ||
In article | PubMed | ||
[26] | Bener A, Hammoudeh M, Zirie M. Prevalence and predictors of osteoporosis and the impact of life style factors on bone mineral density. APLAR Journal of Rheumatology. 2007; 10(3): 227-33. | ||
In article | View Article | ||
[27] | Ho SC, Chen Y-m, Woo JL. Educational level and osteoporosis risk in postmenopausal Chinese women. American journal of epidemiology. 2005; 161(7): 680-90. | ||
In article | View Article PubMed | ||
[28] | Varenna M, Binelli L, Zucchi F, Ghiringhelli D, Gallazzi M, Sinigaglia L. Prevalence of osteoporosis by educational level in a cohort of postmenopausal women. Osteoporosis International. 1999; 9(3): 236-41. | ||
In article | View Article PubMed | ||
[29] | Hie M, Tsukamoto I. Vitamin C-deficiency stimulates osteoclastogenesis with an increase in RANK expression. The Journal of nutritional biochemistry. 2011; 22(2): 164-71. | ||
In article | View Article PubMed | ||
[30] | Park JK, Lee EM, Kim AY, Lee EJ, Min CW, Kang KK, et al. Vitamin C deficiency accelerates bone loss inducing an increase in PPAR-γ expression in SMP30 knockout mice. International journal of experimental pathology. 2012; 93(5): 332-40. | ||
In article | View Article PubMed | ||
[31] | Pradel W, Mai R, Gedrange T, Lauer G. Cell passage and composition of culture medium effects proliferation and differentiation of human osteoblast-like cells from facial bone. J Physiol Pharmacol. 2008; 59(Suppl 5): 47-58. | ||
In article | PubMed | ||
[32] | Urban K, Höhling HJ, Lüttenberg B, Szuwart T, Plate U. An in vitro study of osteoblast vitality influenced by the vitamins C and E. Head Face Med. 2012; 8(25): 10.1186. | ||
In article | View Article | ||
[33] | Pasco JA, Henry MJ, Wilkinson LK, Nicholson GC, Schneider HG, Kotowicz MA. Antioxidant vitamin supplements and markers of bone turnover in a community sample of nonsmoking women. Journal of women's health. 2006; 15(3): 295-300. | ||
In article | View Article PubMed | ||
[34] | Prynne CJ, Mishra GD, O'Connell MA, Muniz G, Laskey MA, Yan L, et al. Fruit and vegetable intakes and bone mineral status: a cross-sectional study in 5 age and sex cohorts. The American journal of clinical nutrition. 2006; 83(6): 1420-8. | ||
In article | PubMed | ||
[35] | Sahni S, Hannan MT, Gagnon D, Blumberg J, Cupples LA, Kiel DP, et al. High vitamin C intake is associated with lower 4-year bone loss in elderly men. The Journal of nutrition. 2008; 138(10): 1931-8. | ||
In article | PubMed PubMed | ||
[36] | Sowers M, Wallace RB, Lemke JH. Correlates of mid-radius bone density among postmenopausal women: a community study. The American journal of clinical nutrition. 1985; 41(5): 1045-53. | ||
In article | PubMed | ||
[37] | Hammad LF. Measurements of bone mineral density and stiffness index in young Saudi females. Pakistan journal of medical sciences. 2016; 32(2): 399. | ||
In article | PubMed PubMed | ||
[38] | Kang C, Speller R. Comparison of ultrasound and dual-energy X-ray absorptiometry measurements in the calcaneus. The British journal of radiology. 1998; 71(848): 861-7. | ||
In article | View Article PubMed | ||
[39] | Chin K-Y, Ima-Nirwana S. Calcaneal quantitative ultrasound as a determinant of bone health status: what properties of bone does it reflect. Int J Med Sci. 2013; 10(12): 1778-83. | ||
In article | View Article PubMed | ||
[40] | Hough S, Ascott-Evans BH, Brown SL, Cassim B, De Villiers TJ, Lipschitz S, et al. NOFSA guideline for the diagnosis and management of osteoporosis. Journal of Endocrinology, Metabolism and Diabetes of South Africa. 2010; 15(3): 107-8. | ||
In article | View Article | ||
Published with license by Science and Education Publishing, Copyright © 2017 Huan-Cheng Chang, Chuan-Fa Hsieh, Yi-Chin Lin, Disline Manli Tantoh, Ya-Yu Kung, Mei-Chi Lin, Yi-Ching Liaw and Yung-Po Liaw
This work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit https://creativecommons.org/licenses/by/4.0/
[1] | Abrahamsen B, Brask-Lindemann D, Rubin KH, Schwarz P. A review of lifestyle, smoking and other modifiable risk factors for osteoporotic fractures. Bonekey reports. 2014;3. | ||
In article | View Article | ||
[2] | Snelling AM, Crespo CJ, Schaeffer M, Smith S, Walbourn L. Modifiable and nonmodifiable factors associated with osteoporosis in postmenopausal women: results from the Third National Health and Nutrition Examination Survey, 1988-1994. Journal of women's health & gender-based medicine. 2001; 10(1): 57-65. | ||
In article | View Article PubMed | ||
[3] | Compston JE, Papapoulos S, Blanchard F. Report on osteoporosis in the European community: current status and recommendations for the future. Osteoporosis international. 1998; 8(6): 531-4. | ||
In article | View Article PubMed | ||
[4] | Guggenbuhl P. Osteoporosis in males and females: Is there really a difference? Joint Bone Spine. 2009; 76(6): 595-601. | ||
In article | View Article PubMed | ||
[5] | Woolf AD, Pfleger B. Burden of major musculoskeletal conditions. Bulletin of the World Health Organization. 2003; 81(9): 646-56. | ||
In article | PubMed PubMed | ||
[6] | MacLaughlin EJ, Sleeper RB, McNatty D, Raehl CL. Management of age-related osteoporosis and prevention of associated fractures. Therapeutics and clinical risk management. 2006; 2(3): 281. | ||
In article | View Article PubMed | ||
[7] | Cawthon PM. Gender differences in osteoporosis and fractures. Clinical Orthopaedics and Related Research®. 2011; 469(7): 1900-5. | ||
In article | View Article PubMed | ||
[8] | Melton LJ, Chrischilles EA, Cooper C, Lane AW, Riggs BL. How many women have osteoporosis? Journal of bone and mineral research. 2005; 20(5): 886-92. | ||
In article | View Article PubMed | ||
[9] | Pietschmann P, Rauner M, Sipos W, Kerschan-Schindl K. Osteoporosis: an age-related and gender-specific disease–a mini-review. Gerontology. 2009; 55(1): 3-12. | ||
In article | View Article PubMed | ||
[10] | Aggarwal N, Raveendran A, Khandelwal N, Sen RK, Thakur J, Dhaliwal LK, et al. Prevalence and related risk factors of osteoporosis in peri-and postmenopausal Indian women. Journal of mid-life health. 2011; 2(2): 81. | ||
In article | View Article PubMed | ||
[11] | Asomaning K, Bertone-Johnson ER, Nasca PC, Hooven F, Pekow PS. The association between body mass index and osteoporosis in patients referred for a bone mineral density examination. Journal of Women's Health. 2006; 15(9): 1028-34. | ||
In article | View Article PubMed | ||
[12] | De Laet C, Kanis J, Odén A, Johanson H, Johnell O, Delmas P, et al. Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporosis international. 2005; 16(11): 1330-8. | ||
In article | View Article PubMed | ||
[13] | Jain V, Agrawal B, Varshney A, Biswas S. Prediction of bone mineral density by age, body mass index and menopausal status in middle socioeconomic status women of urban Kolar region of Bhopal. IOSR Journal of Dental and Medical Sciences. 2013; 12(3): 17-21. | ||
In article | View Article | ||
[14] | Oldroyd A, Mitchell K, Bukhari M. The prevalence of osteoporosis in an older population with very high body mass index: evidence for an association. International journal of clinical practice. 2014; 68(6): 771-4. | ||
In article | View Article PubMed | ||
[15] | Chapuy M, Schott A, Garnero P, Hans D, Delmas P, Meunier P. Healthy elderly French women living at home have secondary hyperparathyroidism and high bone turnover in winter. EPIDOS Study Group. The Journal of Clinical Endocrinology & Metabolism. 1996; 81(3):1129-33. | ||
In article | PubMed | ||
[16] | Kim SY. Coffee consumption and risk of osteoporosis. Korean journal of family medicine. 2014; 35(1): 1. | ||
In article | View Article PubMed | ||
[17] | Choi E-J, Kim K-H, Koh Y-J, Lee J-S, Lee D-R, Park SM. Coffee consumption and bone mineral density in Korean premenopausal women. Korean journal of family medicine. 2014; 35(1): 11-8. | ||
In article | View Article PubMed | ||
[18] | Hallström H, Byberg L, Glynn A, Lemming EW, Wolk A, Michaëlsson K. Long-term coffee consumption in relation to fracture risk and bone mineral density in women. American journal of epidemiology. 2013:kwt062. | ||
In article | View Article PubMed | ||
[19] | Hallström H, Wolk A, Glynn A, Michaëlsson K. Coffee, tea and caffeine consumption in relation to osteoporotic fracture risk in a cohort of Swedish women. Osteoporosis international. 2006; 17(7): 1055-64. | ||
In article | View Article PubMed | ||
[20] | Lacerda SA, Matuoka RI, Macedo RM, Petenusci SO, Campos AA, Brentegani LG. Bone quality associated with daily intake of coffee: a biochemical, radiographic and histometric study. Brazilian dental journal. 2010; 21(3):199-204. | ||
In article | View Article PubMed | ||
[21] | Choi E, Choi K-H, Park SM, Shin D, Joh H-K, Cho E. The Benefit of Bone Health by Drinking Coffee among Korean Postmenopausal Women: A Cross-Sectional Analysis of the Fourth & Fifth Korea National Health and Nutrition Examination Surveys. PloS one. 2016; 11(1): e0147762. | ||
In article | View Article PubMed | ||
[22] | Cheng ML, Gupta V. Premenopausal osteoporosis. Indian journal of endocrinology and metabolism. 2013; 17(2): 240. | ||
In article | View Article PubMed | ||
[23] | Kapetanovic A, Avdic D. Influence of coffee consumption on bone mineral density in postmenopausal women with estrogen deficiency in menstrual history. Journal of Health Sciences. 2014; 4(2). | ||
In article | View Article | ||
[24] | Demirbag D, Ozdemir F, Ture M. Effects of coffee consumption and smoking habit on bone mineral density. Rheumatology international. 2006; 26(6): 530-5. | ||
In article | View Article PubMed | ||
[25] | Akkus Z, Camdeviren H, Celik F, Gur A, Nas K. Determination of osteoporosis risk factors using a multiple logistic regression model in postmenopausal Turkish women. Saudi medical journal. 2005; 26(9): 1351-9. | ||
In article | PubMed | ||
[26] | Bener A, Hammoudeh M, Zirie M. Prevalence and predictors of osteoporosis and the impact of life style factors on bone mineral density. APLAR Journal of Rheumatology. 2007; 10(3): 227-33. | ||
In article | View Article | ||
[27] | Ho SC, Chen Y-m, Woo JL. Educational level and osteoporosis risk in postmenopausal Chinese women. American journal of epidemiology. 2005; 161(7): 680-90. | ||
In article | View Article PubMed | ||
[28] | Varenna M, Binelli L, Zucchi F, Ghiringhelli D, Gallazzi M, Sinigaglia L. Prevalence of osteoporosis by educational level in a cohort of postmenopausal women. Osteoporosis International. 1999; 9(3): 236-41. | ||
In article | View Article PubMed | ||
[29] | Hie M, Tsukamoto I. Vitamin C-deficiency stimulates osteoclastogenesis with an increase in RANK expression. The Journal of nutritional biochemistry. 2011; 22(2): 164-71. | ||
In article | View Article PubMed | ||
[30] | Park JK, Lee EM, Kim AY, Lee EJ, Min CW, Kang KK, et al. Vitamin C deficiency accelerates bone loss inducing an increase in PPAR-γ expression in SMP30 knockout mice. International journal of experimental pathology. 2012; 93(5): 332-40. | ||
In article | View Article PubMed | ||
[31] | Pradel W, Mai R, Gedrange T, Lauer G. Cell passage and composition of culture medium effects proliferation and differentiation of human osteoblast-like cells from facial bone. J Physiol Pharmacol. 2008; 59(Suppl 5): 47-58. | ||
In article | PubMed | ||
[32] | Urban K, Höhling HJ, Lüttenberg B, Szuwart T, Plate U. An in vitro study of osteoblast vitality influenced by the vitamins C and E. Head Face Med. 2012; 8(25): 10.1186. | ||
In article | View Article | ||
[33] | Pasco JA, Henry MJ, Wilkinson LK, Nicholson GC, Schneider HG, Kotowicz MA. Antioxidant vitamin supplements and markers of bone turnover in a community sample of nonsmoking women. Journal of women's health. 2006; 15(3): 295-300. | ||
In article | View Article PubMed | ||
[34] | Prynne CJ, Mishra GD, O'Connell MA, Muniz G, Laskey MA, Yan L, et al. Fruit and vegetable intakes and bone mineral status: a cross-sectional study in 5 age and sex cohorts. The American journal of clinical nutrition. 2006; 83(6): 1420-8. | ||
In article | PubMed | ||
[35] | Sahni S, Hannan MT, Gagnon D, Blumberg J, Cupples LA, Kiel DP, et al. High vitamin C intake is associated with lower 4-year bone loss in elderly men. The Journal of nutrition. 2008; 138(10): 1931-8. | ||
In article | PubMed PubMed | ||
[36] | Sowers M, Wallace RB, Lemke JH. Correlates of mid-radius bone density among postmenopausal women: a community study. The American journal of clinical nutrition. 1985; 41(5): 1045-53. | ||
In article | PubMed | ||
[37] | Hammad LF. Measurements of bone mineral density and stiffness index in young Saudi females. Pakistan journal of medical sciences. 2016; 32(2): 399. | ||
In article | PubMed PubMed | ||
[38] | Kang C, Speller R. Comparison of ultrasound and dual-energy X-ray absorptiometry measurements in the calcaneus. The British journal of radiology. 1998; 71(848): 861-7. | ||
In article | View Article PubMed | ||
[39] | Chin K-Y, Ima-Nirwana S. Calcaneal quantitative ultrasound as a determinant of bone health status: what properties of bone does it reflect. Int J Med Sci. 2013; 10(12): 1778-83. | ||
In article | View Article PubMed | ||
[40] | Hough S, Ascott-Evans BH, Brown SL, Cassim B, De Villiers TJ, Lipschitz S, et al. NOFSA guideline for the diagnosis and management of osteoporosis. Journal of Endocrinology, Metabolism and Diabetes of South Africa. 2010; 15(3): 107-8. | ||
In article | View Article | ||