JACN Did you know that you can get alerts when a new issue is online?
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Lloyd, T.
Right arrow Articles by Cusatis, D. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lloyd, T.
Right arrow Articles by Cusatis, D. C.
Journal of the American College of Nutrition, Vol. 19, No. 2, 256-261 (2000)
Published by the American College of Nutrition

Original Research

Bone Status among Postmenopausal Women with Different Habitual Caffeine Intakes: A Longitudinal Investigation

Tom Lloyd, PhD, Nan Johnson-Rollings, RN, MEd, Douglas F. Eggli, MD, Kessey Kieselhorst, RD, MPA, Elizabeth A. Mauger, PhD and Deborah Cardamone Cusatis, MD, PhD

Departments of Health Evaluation Sciences (T.L., N.J.-R., E.A.M., D.C.C.), Pennsylvania State College of Medicine and University Hospitals, Pennsylvania State Geisinger Health System, Milton S. Hershey Medical Center, Hershey, Pennsylvania
Radiology (D.F.E.), Pennsylvania State College of Medicine and University Hospitals, Pennsylvania State Geisinger Health System, Milton S. Hershey Medical Center, Hershey, Pennsylvania
Clinical Nutrition (K.K.), Pennsylvania State College of Medicine and University Hospitals, Pennsylvania State Geisinger Health System, Milton S. Hershey Medical Center, Hershey, Pennsylvania


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Objective: Caffeine consumption has been proposed as a risk factor for bone loss in postmenopausal women. Past epidemiologic studies on caffeine and bone have been confounded by covariates including cigarette and alcohol use, differing levels of physical activity and hormone replacement therapy. The purpose of the study was to use a longitudinal design to determine the relationship between habitual dietary caffeine intake and postmenopausal bone status.

Methods: Data were collected at two time points separated by two years; 138 women with little or no exposure to tobacco or to drugs known to affect bone status were seen at Visit 1, and 112 returned for Visit 2. Ninety-two of these subjects had received no drugs known to affect bone status over the two-year interval and were kept in the sample. Nutrient and caffeine intake were assessed from three-day diet records. Bone measurements were made by dual energy x-ray absorptiometry (DXA).

Results: Correlation analyses indicated no association between dietary caffeine intake and total body or femoral neck bone density or bone mass. Similarly, no associations were found between caffeine consumption and longitudinal changes in total body or femoral neck bone measurements. These results held true both with and without statistical adjustment for calcium intake.

Conclusions: This study does not support the idea that caffeine is a risk factor for bone loss in healthy postmenopausal women.

Key words: caffeine, calcium, bone loss, postmenopausal women, longitudinal studies


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Caffeine consumption is the subject of extensive research due to its wide use and acknowledged psychoactive effects [1]. Daily per capita caffeine intake in the United States is about 2.0 mg/kg, with coffee supplying over 80 percent of caffeine consumed by adults [2]. In recent years, many epidemiologic studies have addressed the question of whether caffeine is a risk factor for bone loss in adult women [3–12]. Comparison of past studies has been limited by variations in study design, age of subjects studied, techniques for bone measurements and methods for estimation of caffeine intake. Further, in all of these studies, variables known to affect bone loss (e.g., smoking, alcohol use, body weight, physical activity, and hormone replacement therapy or HRT) were controlled for statistically rather than by experimental design. Statistical methods, however, cannot always fully control for the complex relationships that exist among these variables. For example, it is recognized that cigarette smokers tend to consume more caffeine than non-smokers [13–18]. However, smoking cessation among caffeine consumers is followed by an increase in serum caffeine levels [19], indicating enhanced caffeine catabolism and, possibly, dampened caffeine effects among smokers. Therefore, fair evaluation of caffeine’s effects on bone requires controlling for the effects of smoking through study design.

The present investigation was designed specifically to minimize the effects of such confounding variables. The purpose of the study was to use longitudinal data to build on our previous cross-sectional examination of the relationships between caffeine and bone [20]. Because smoking, exogenous sex steroids and body weight are known to affect bone status of women [21], healthy postmenopausal women aged 55 to 70 who were between 70 percent and 130 percent of ideal body weight and had minimal or no exposure to tobacco or to HRT were recruited in 1993. The subjects were studied at two time points, with a 24-month interval between clinic visits. The objectives of this longitudinal investigation were to determine the relationship of subjects’ average caffeine use to bone measurements and to the change in these measurements over the 2-year study interval.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
All procedures involving human subjects were reviewed and approved by the Institutional Review Board at the Pennsylvania State University College of Medicine and University Hospital. Volunteers for this study were recruited by local newspaper advertisements from a pool of more than 75,000 women in this age group within 25 miles of the Hershey Medical Center. Only individuals responsible for their own care and food preparation were studied. Initial screening of potential applicants was made by telephone interview.

Subject Population: Inclusion and Exclusion Criteria
Postmenopausal, Caucasian women between the ages of 55 and 70 at entry and between 70 and 130 percent of ideal body weight for height were studied. At the time of entry subjects were asked to classify their usual caffeine use as low (equivalent to 0–2 cups caffeinated coffee per day), moderate (equivalent to 3–4 cups caffeinated coffee per day) or high (equivalent to >=5 cups caffeinated coffee per day). Approximately equal numbers of subjects (33, 30 and 29, respectively, from the final cohort of 92 subjects) reported usual intakes in each of these three categories during recruitment. To control for the potentially confounding effects of exercise, we recruited within each of the three self-reported caffeine use groups subgroups of low (no regular exercise program), moderate (1–3 times per week of at least 30 minutes/time), and high (more than three times per week of at least 30 minutes/time) exercise patterns. Approximately equal numbers of subjects in the three caffeine groups reported exercise levels in each of the three activity categories.

Applicants were excluded during the initial interview with the project coordinator for any of the following reasons: 1) use of postmenopausal HRT for >=1 year, 2) clinically-expressed osteoporosis, as evidenced by previously-detected osteoporosis-related fractures (e.g., of the hip, wrist or spine) or by use of bisphosphonates, calcitonin or sodium fluoride, 3) use of thiazides or other diuretics, 4) use of corticosteroids for >3 months, 5) current smoking or a history of >5 packs a year, 6) chemotherapy for cancer, 7) rheumatoid arthritis, 8) history of any endocrine disease known to affect mineral metabolism (of the parathyroid, thyroid, adrenal gland or ovary), 9) current or past consumption of more than one alcoholic drink per day and 10) current participation in a resistive or load-bearing aerobic exercise program for more than 5 hours a week. Subjects with any of the following were not excluded: heart disease being treated with nitroglycerin, calcium channel blockers or beta blockers, diabetes being treated with insulin, arthritis of <5 years duration being treated with nonsteroidal antiinflammatory drugs, depression being treated with antidepressant or psychotropic drugs for <5 years. Of the entry cohort of 138 subjects, 112 returned for the second clinic visit approximately two years later (mean±SD, 2.1±0.3 years). Ninety-two of the subjects had not received any drug therapy with possible bone effects over the two-year interval. Only data from these 92 subjects were used for the current investigation.

Clinic Visits and Data Collection
At each clinic visit, the following data were collected from each subject: 1) medical history, anthropometric measurements, and occupational and recreational activity history, 2) three days of diet records and 3) total body bone measurements. The research coordinator (NR) collected all histories and anthropometric data. Bone measurements, including total body bone mineral content (TBBMC) and density (TBBMD) and femoral neck bone mineral density measurements, were made with a Hologic QDR 2000 dual energy x-ray absorptiometer (DXA). Details of this method and its reproducibility have been reported [22,23].

Nutritional Analysis
The subjects completed three-day food records, including two weekdays and one weekend day, prior to each study visit. Subjects reported all food, drink and vitamin and mineral supplements they consumed over the three days, estimating serving sizes using common household measures. Detailed instructions concerning the completion of the records were provided to the subjects by a registered dietitian (KK). The same dietitian reviewed the diet records, discussed any ambiguities in the records with the subjects and entered the food items into a computer nutrient analysis program (Nutritionist IV, FirstDataBank, San Bruno, California 94066). In addition to obtaining data on caffeine intake from major sources, such as coffee, tea and soft drinks, this program collects caffeine content data from minor sources, such as chocolate-containing products. Nutrient intake has been expressed as per day values.

Statistical Analysis
Descriptive statistics in the form of means and standard deviations of anthropometric and bone measurements as well as caffeine and other dietary measurements were calculated. Paired t tests were used to detect differences in these variables between Visits 1 and 2. Dietary caffeine intake was averaged for the two study visits, and linear relationships between average caffeine intake and bone measurements were assessed using Pearson correlation analyses. Partial correlation analyses were then conducted to investigate these same relationships while keeping dietary calcium constant, thus controlling for its possible confounding effects. In our final analysis, the cohort was divided into halves, according to level of calcium intake averaged over the two study visits. Within each of these halves, the subjects were divided into tertiles according to dietary caffeine intake (again, averaged over the two study visits), and mean bone and bone change values for the subjects in the tertiles were compared using t tests. All analyses were conducted using SAS statistical package (SAS version 6.12, SAS Institute, Cary, North Carolina).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The overall descriptive statistics for the 92 participants for Visit 1 and Visit 2 are presented in Table 1. The following significant changes between the visits were observed: The participants, on average, 1) were two years older, 2) lost 1 cm in height, 3) gained 1.2 kg in weight, 4) had a gain in BMI from 25.0 to 25.7 kg/m2, 5) had a decrease in total body bone mineral density (TBBMD) from 0.98 to 0.97 g/cm2, 6) decreased their percent energy from fat from 29.0 percent to 27.0 percent, 7) decreased their fat intake from 57 to 50 g/d, 8) decreased their consumption of protein from 71 to 67 g/d, 9) increased their calcium intake from 776 to 848 mg/d, 10) increased their bread intake from 8.9 to 9.7 serv/d and 11) decreased their meat intake from 5.0 to 4.3 serv/d.


View this table:
[in this window]
[in a new window]
  		Table 1. Descriptive Statistics of the Subjects Remaining in the Sample at Visit 2 (n=92)

 
As shown in Fig. 1, the subjects’ daily caffeine intake averaged for Visits 1 and 2 was broadly distributed, with 32 subjects consuming between zero and 150 mg/d, 14 subjects consuming 151 to 300 mg/d and 46 subjects consuming more than 300 mg/d. When this group was originally studied (Visit 1), no association was observed between habitual caffeine intake and bone measurements [20]. Similarly, the correlation analyses shown in Table 2 indicate no significant associations between dietary caffeine intake and any of the bone measurements at Visit 2 or any changes in these measurements between Visits 1 and 2. This was the case both with and without statistical adjustment for dietary calcium, as indicated by the partial and Pearson correlation coefficients, respectively. Table 3 displays the mean bone measurements at Visit 2 and the changes in these values between the two study visits for both high- and low-calcium-consumers in each tertile of caffeine intake. No significant differences emerged in any of the bone-change variables according to caffeine tertile for subjects in either the high or low calcium group.



View larger version (44K):
[in this window]
[in a new window]
  		Fig. 1. Distribution of subjects’ daily caffeine intake, averaged for Visits 1 and 2.

 

View this table:
[in this window]
[in a new window]
  		Table 2. Correlation Analyses Relating Dietary Caffeine to Bone Measurements (n=92)1

 

View this table:
[in this window]
[in a new window]
  		Table 3. Bone Measurements1 by Caffeine Intake Tertile (Low, Medium and High) in Subjects with Below- and Above-Median Calcium Intakes (n=92)2

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
It is estimated that osteoporosis will affect one in three United States women [27]. Although some studies have suggested an association between caffeine intake and bone density [5,28,29], several others have not [6,9,11]. In view of these conflicting reports, improving our understanding of the effects of dietary caffeine on bone status is of great importance. Because a randomized clinical trial of the long-term effects of caffeine is not possible, we must recognize and address study limitations in three areas. First, determining daily caffeine intake is problematic, as caffeinated products of the same type (e.g., coffees, teas, colas) vary tremendously in their caffeine content [30]. Second, measurement of habitual caffeine intake patterns of free living populations is difficult [31]. Recall of caffeinated beverage use has been studied and found to be poor [32]. At a minimum, more than one assessment is needed. Third, there is co-occurrence of such possibly confounding variables as consumption of cigarettes and alcohol and low levels of physical activity with caffeine consumption among many adult populations [14–16].

The objective of the present study was to use a longitudinal research plan, control for major potential confounders by inclusion/exclusion criteria and then evaluate the relationship between long-term caffeine intake and bone status among postmenopausal women. While a limitation of the study is the moderately small sample size, the recruitment strategy allows for clear interpretation of the results. Healthy postmenopausal, white women who had used little or no tobacco or HRT were enrolled in the study. They were recruited to obtain a broad distribution of caffeine intake and exercise levels. The subjects in the study cohort were 62.5±4.6 years old at their first visit. Results of the initial study and nutrient intake assessments and physical activity profiles showed that dietary caffeine intake of the original cohort of 138 postmenopausal women ranged from 0–1400 mg/d and was not associated with total body or femoral neck bone mineral density measurements [20]. The 92 subjects who returned for a second visit two years later and remained in the sample lost, on average, 1 cm in height and gained 1.2 kg in weight, resulting in a modest increase in their BMI. They lost one percent total body bone mass and one percent total body bone mineral density or about 0.5 percent per year. These age-dependent bone losses are consistent with those observed with other large data sets from postmenopausal women [33,34]. The nutrient intake profiles at Visits 1 and 2, summarized in Table 1, show that for both visits our subjects’ mean intake values were largely in agreement with age and race-matched data from the most recent National Health and Nutrition Examination Survey [35,36].

Previous studies have suggested that any existing relationships between caffeine intake and bone measurements may be impacted by dietary calcium. Using a sample of 980 postmenopausal women, Barrett-Connor and colleagues found increased lifetime intake of caffeinated coffee to be associated with decreased bone mineral density in subjects who did not consume milk on a daily basis, but failed to find such a relationship for subjects consuming one glass of milk per day [6]. Similarly, in their sample of 205 postmenopausal women, Harris and Dawson-Hughes found an increase in bone loss with increasing caffeine intake among subjects with lower consumption (below 744 mg/d) of calcium, but not among subjects with higher levels of calcium intake [8]. In view of the results of these studies, our correlation analysis examined the relationships between caffeine and bone measurements both with and without statistical adjustment for the effects of dietary calcium. As shown in Table 2, both the Pearson and the partial correlation coefficients regarding caffeine’s relationship with all of the measured bone variables were very small. Further, the differences between these values were negligible, and in no case did the use of partial correlation analysis increase the correlation coefficient to the point of statistical significance. Therefore, regardless of adjustment for dietary calcium, no significant linear relationships were observed between the subjects’ caffeine intake and their bone density or content measurements. Similarly, as shown in Table 3, we did not find any difference in bone loss according to caffeine intake in subjects with either higher (above 746 mg/d) or lower consumption of calcium.

By collecting two sets of caffeine intake and bone measurements separated in time by two years, we were able to assess whether habitual differences in dietary caffeine intake were related to age-dependent bone loss. As would be expected with aging, total body bone mineral content and density were lower at the second visit. Again, however, no significant correlations, with or without controlling for the possible effects of dietary calcium, were found between dietary caffeine and the change in the bone measurements between the two study visits. In response to our research question, then, we interpret our results to indicate that habitual differences in caffeine intake over the range achieved by our subjects are not associated with bone loss. Therefore, this study does not support the idea that caffeine is a risk factor for bone loss in healthy postmenopausal women.


   ACKNOWLEDGMENTS
 
This research was supported by a grant from the International Life Sciences Institute and The National Coffee Association.


   FOOTNOTES
 
Supported by a grant from the International Life Sciences Institute and The National Coffee Association.

Reprints will not be available from the author.

Received June 1, 1999. Accepted January 1, 2000.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Gilbert RM: Caffeine consumption. In Spiller GA (ed.): "The Methylxanthine Beverages and Foods: Chemistry, Consumption and Health Effects." New York: Alan R. Liss, pp 185–213, 1984.
  2. Barone JJ, Grice HC: Seventh International Caffeine Workshop. Food Chem Toxicol 32: 65–77, 1994.[Medline]
  3. Kiel DP, Felson DT, Hannan MT, Anderson JJ, Wilson PWF: Caffeine and the risk of hip fracture: The Framingham Study. Am J Epidemiol 132: 675–684, 1990.[Abstract/Free Full Text]
  4. Hernandez-Avila M, Colditz GA, Stampfer MJ, Rosner B, Speizer FE, Willett WC: Caffeine, moderate alcohol intake, and risk of fractures of the hip and forearm in middle-aged women. Am J Clin Nutr 54: 157–163, 1991.[Abstract/Free Full Text]
  5. Cooper C, Atkinson EJ, Wahner HW, O’Fallon WM, Riggs BL, Judd HL, Melton III LJ: Is caffeine consumption a risk factor for osteoporosis? J Bone Miner Res 7: 465–471, 1992.[Medline]
  6. Barrett-Connor E, Chang JC, Edelstein SL: Coffee-associated osteoporosis offset by daily milk consumption: The Rancho Bernardo Study. JAMA 271: 280–283, 1994.[Abstract/Free Full Text]
  7. Cumming RG, Klineberg RJ: Case-control study of risk factors for hip fractures in the elderly. Am J Epidemiol 139: 493–503, 1994.[Abstract/Free Full Text]
  8. Harris SS, Dawson-Hughes B: Caffeine and bone loss in healthy postmenopausal women. Am J Clin Nutr 60: 573–578, 1994.[Abstract/Free Full Text]
  9. Reid IR, Ames RW, Evans MC, Sharpe SJ, Gamble GD: Determinants of the rate of bone loss in normal postmenopausal women. J Clin Endocrinol Metab 79: 950–954, 1994.[Abstract]
  10. Cummings SR, Nevitt MC, Browner WS, Stone K, Fox KM, Ensrud KE, Cauley J, Black D, Vogt TM: Risk factors for hip fracture in white women: Study of Osteoporotic Fractures Research Group. N Engl J Med 332: 767–773, 1995.[Abstract/Free Full Text]
  11. Harris SS: Effects of caffeine consumption on hip fracture, bone density and calcium retention. In Burckhardt P, Dawson-Hughes B, Heaney RP (eds): "Nutritional Aspects of Osteoporosis." New York: Springer-Verlag, pp 163–171, 1998.
  12. Tavani A, Negri E, LaVecchia C: Coffee intake and risk of hip fracture in Northern Italy. Prev Med 24: 396–400, 1995.[Medline]
  13. Klesges RC, Ray JW, Klesges LM: Caffeinated coffee and tea intake and its relationship to cigarette smoking: An analysis of the Second National Health and Nutrition Examination Survey (NHANESII). J Subst Abuse 6: 407–418, 1994.[Medline]
  14. Schwarz B, Bischof H-P, Kunze M: Coffee, tea and lifestyle. Prev Med 23: 377–384, 1994.[Medline]
  15. Jacobsen BK, Thelle DS: The Tromso heart study: Is coffee drinking an indicator of a lifestyle with high risk for ischemic heart disease? Acta Med Scand 222: 215–221, 1987.[Medline]
  16. Puccio EM, McPhillips JB, Barrett-Connor E, Ganiats TG: Clustering of atherogenic behaviors in coffee drinkers. Am J Public Health 80: 1310–1313, 1990.[Abstract/Free Full Text]
  17. Leviton A, Pagano M, Allred EN, el Lozy M: Why those who drink the most coffee appear to be at increased risk of disease. A modest proposal. Ecol Food Nutr 31: 285–293, 1994.
  18. Talcott GW, Poston 2nd WS, Haddock CK. Co-occurrent use of cigarettes, alcohol, and caffeine in a retired military population. Mil Med 163: 133–138, 1998.[Medline]
  19. Benowitz NL, Hall SM, Modin G: Persistent increases in caffeine concentrations in people who stop smoking. Br Med J 298: 1075–1076, 1989.
  20. Lloyd T, Rollings N, Eggli DF, Kieselhorst K, Chinchilli VM: Dietary caffeine intake and bone status of postmenopausal women. Am J Clin Nutr 65: 1826–1830, 1997.[Abstract/Free Full Text]
  21. Ward JA, Lord SR, Williams P, Anstey K, Zivanovic E: Physiologic, health and lifestyle factors associated with femoral neck bone density in older women. Bone 3: 373S–378S, 1995.
  22. Nguyen TV, Sambrook PN, Eisman JA: Sources of variability in bone mineral density measurements: implications for study design and analysis of bone loss. J Bone Miner Res 12: 124–135, 1997.[Medline]
  23. Ellis KJ, Shypailo RJ: Bone mineral and body composition measurements: cross calibrations of pencil-beam and fan-beam dual-energy x-ray absorptiometers. J Bone Miner Res 13: 1613–1618, 1998.[Medline]
  24. Food and Nutrition Board, Institute of Medicine, National Academy of Sciences: "Dietary Reference Intakes (DRIs) for Calcium, Phosphorus, Magnesium, Vitamin D, and Fluoride." Washington, DC: National Academy Press, 1997.
  25. Food and Nutrition Board, National Research Council: "Recommended Dietary Allowances," 10th ed. Washington, DC: National Academy Press, 1989.
  26. Committee on Diet and Health, Food and Nutrition Board, National Research Council: "Diet and Health—Implications for Reducing Chronic Disease Risk." Washington, DC: National Academy Press, 1989.
  27. Melton JL: Epidemiology of spinal osteoporosis. Spine 22: 2S–11S, 1997.[Medline]
  28. Bauer DC, Genant KH, Cauley JA, Orwoll S, Scott JC, Tao JL, Cummings SR and the Study of Osteoporotic Fractures Research Group: Determinants of bone density in elderly women. Clin Res 39: 571A, 1991.
  29. Yano K, Heilbrun LK, Wasnich RD, Hankin JH, Vogel JM: The relationship between diet and bone mineral content of multiple skeletal sites in elderly Japanese-American men and women living in Hawaii. Am J Clin Nutr 42: 877–888, 1985.[Abstract/Free Full Text]
  30. Pennington JAT: "Bowes and Church’s Food Values of Portions Commonly Used," 16th ed. Philadelphia: JB Lippincott, pp 381–383, 1994.
  31. Kennedy JS, von Moltke LL, Harmatz JS, Engelhardt N, Greenblatt DJ: Validity of self-reports of caffeine use. J Clin Pharmacol 31: 677–680, 1991.[Abstract]
  32. Hughes JR, Oliveto AH: A systematic survey of caffeine intake in Vermont. Exp Clin Psychopharmacol 5: 393–398, 1997.[Medline]
  33. Ryan PJ, Spector TP, Blake GM, Doyle DV, Fogelman L: A comparison of reference bone mineral density measurements derived from two sources: Referred and population based. Br J Radiol 66: 1138–1141, 1993.[Abstract/Free Full Text]
  34. Gotfredsen A, Hadberg A, Nilas L, Christiansen C: Total body bone mineral in healthy adults. J Lab Clin Med 110: 362–368, 1987.[Medline]
  35. Center for Disease Control and Prevention: Energy and macronutrient intakes of persons ages two months and over in the United States: Third National Health and Nutrition Examination Survey, Phase I, 1988–91. National Center for Health Statistics, Advance Data 1994, No. 255: 1–24. DHHS Pub. No. (PHS) 95-1250.
  36. Center for Disease Control and Prevention: Dietary intake of vitamins, minerals, and fiber of persons ages 2 months and over in the United States: Third National Health and Nutrition Examination Survey, Phase I, 1988–91. National Center for Health Statistics, Advance Data 1994, No. 258: 1–28. DHHS Pub. No. (PHS) 95-1250.



This article has been cited by other articles:


Home page
 Am. J. Clin. Nutr.Home page
A. Devine, J. M Hodgson, I. M Dick, and R. L Prince
Tea drinking is associated with benefits on bone density in older women
Am. J. Clinical Nutrition, October 1, 2007; 86(4): 1243 - 1247.
[Abstract] [Full Text] [PDF]

Home page
 Am J EpidemiolHome page
Z. Chen, M. B. Pettinger, C. Ritenbaugh, A. Z. LaCroix, J. Robbins, B. J. Caan, D. H. Barad, and I. A. Hakim
Habitual Tea Consumption and Risk of Osteoporosis: A Prospective Study in the Women's Health Initiative Observational Cohort
Am. J. Epidemiol., October 15, 2003; 158(8): 772 - 781.
[Abstract] [Full Text] [PDF]

Home page
 J. Am. Coll. Nutr.Home page
J. Z. Ilich, R. A. Brownbill, L. Tamborini, and Z. Crncevic-Orlic
To Drink or Not to Drink: How Are Alcohol, Caffeine and Past Smoking Related to Bone Mineral Density in Elderly Women?
J. Am. Coll. Nutr., December 1, 2002; 21(6): 536 - 544.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Clin. Nutr.Home page
L. K Massey
Is caffeine a risk factor for bone loss in the elderly?
Am. J. Clinical Nutrition, November 1, 2001; 74(5): 569 - 570.
[Full Text] [PDF]

Home page
 J. Am. Coll. Nutr.Home page
J. Z. Ilich and J. E. Kerstetter
Nutrition in Bone Health Revisited: A Story Beyond Calcium
J. Am. Coll. Nutr., June 1, 2000; 19(6): 715 - 737.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Lloyd, T.
Right arrow Articles by Cusatis, D. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lloyd, T.
Right arrow Articles by Cusatis, D. C.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS