Affiliations of authors: Jean Mayer USDA Human Nutrition Research Center on Aging, Tufts University, Boston, MA (XG, KLT); Boston University School of Public Health, Boston, MA (MPL)
Correspondence to: Katherine L. Tucker, PhD, Jean Mayer USDA Human Nutrition Research Center on Aging, Tufts University, 711 Washington St., Boston, MA 02111 (e-mail: Katherine.tucker{at}tufts.edu).
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ABSTRACT |
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INTRODUCTION |
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The inverse associations between dairy product and calcium intakes and the risks of some chronic diseases have been well documented. Intake of dairy products has been associated with reduced risks of osteoporosis (1517) and, possibly, of insulin resistance syndrome (18). These effects are thought to be due mainly to the high calcium content of dairy foods. On the basis of these observations, the Dietary Guidelines for Americans 2005 recommends that all Americans increase their daily intakes of nonfat or low-fat milk and milk products (19).
It is important to weigh potential benefits of such a recommendation against the potential risks. For example, results of a recent meta-analysis of casecontrol studies suggested that men with the highest milk consumption have a 68% higher risk of prostate cancer than men with the lowest intakes (20). However, casecontrol studies are prone to recall and selection bias, which may have resulted in an overestimation of the association. We hypothesized that high intakes of dairy foods and calcium are associated with an increased risk of prostate cancer and examined this hypothesis by performing a meta-analysis of prospective studies.
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METHODS |
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We used guidelines established for including nonrandomized studies in Cochrane reviews (21) to select the publications to be included in this meta-analysis and to extract data. We conducted a comprehensive search of Medline (PubMed and OVID) English-language literature published from 1966 through May 2005, using the following search algorithm: (dairy OR milk OR calcium) AND (prostate cancer OR prostatic neoplasm). We also manually searched the reference lists of relevant publications to identify additional studies. To be included in our meta-analysis, studies had to 1) be conducted in adult men, 2) use an observational prospective study design, 3) present data on incident cases of prostate cancer or advanced prostate cancer or on mortality from prostate cancer, and 4) report associations in the form of relative risks (RRs) or odds ratios by categories of dairy product or calcium intake. We identified 13 publications that reported results from prospective studies: 10 publications (8,9,14,2228) were identified by searching Medline and three publications were identified by the manual search (10,29,30). One publication (30) was excluded from the meta-analysis because milk intake had been treated as a continuous variable, not discrete categories. The remaining 12 publications (810,14,2229) were included in the meta-analysis. Two publications (8,27) examined associations among participants in the Health Professionals Follow-up Study, and two publications (22,29) examined associations among California members of the Seventh-day Adventist Church. The two publications from each study population examined different exposures (i.e., dairy and calcium intake) or outcomes (i.e., total and advanced prostate cancer). We therefore used one of each set of publications in separate analyses of different exposures and outcomes. We also identified a randomized clinical trial that examined prostate cancer risk after 10.3 years of follow up among men who were randomly assigned to receive calcium supplementation (1,200 mg/d) or placebo (31). Although this study did not meet the inclusion criteria for the meta-analysis, we included it in the sensitivity analyses.
Data Extraction
We used a standardized protocol and reporting form to abstract the following data from each publication: the first author's name, the year of publication, the country in which the study was performed, the study design, the sample size, the mean age or age range of study subjects, the duration of follow-up, the method of assessment of dairy product or calcium intake, the categories of dairy product or calcium intake, whether prostate cancer was the primary end point, the covariates for adjustments in multivariable models, and the relative risks and 95% confidence intervals (CIs) for prostate cancer associated with dairy product or calcium intake.
Statistical Analysis
We used the reported relative risk as the measure of the association between dairy product or calcium intake and the risk of prostate cancer. We used the reported relative risks for total dairy product intake when they were provided. Two publications (24,26) reported separate relative risks for several dairy items (e.g., for milk or for cheese). In this situation, we pooled the relative risk estimates for the different dairy items, weighted by inverse of the variance, within each study. We used the reported relative risks for total prostate cancer, when they were provided, to examine the association between dairy product or calcium intake and the risk of prostate cancer. When the relative risks for total prostate cancer were not provided, we used the reported relative risks for clinical (stage 24) (9) or fatal (10) prostate cancer in our analyses. When both crude and adjusted relative risks were provided, we used the most fully adjusted relative risks for all studies except for the study by Michaud et al. (27); for that study, we used the reported relative risk without calcium adjustment in our main analysis to avoid overadjustment. Reported relative risks were transformed to their natural logarithms to normalize the distributions. Standard errors (SEs) were calculated from the following equation (32):
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The inverse of the variance (i.e., the square of the SE) was used to weight each relative risk estimate for calculations of the pooled relative risks.
To examine associations between the risk of prostate cancer and dairy product or calcium intake, we pooled the relative risk estimates for the highest intake category versus the lowest intake category from each study, weighted by the inverse of their variances. Random-effects models were used for the primary analysis of the association between prostate cancer risk and dairy product or calcium intake, and fixed-effects models were used for the sensitivity analysis. Because the two models produced identical results, we present only the results from the random-effects models, which consider both within- and between-study variation (33). We used the meta-regression method (34,35) to examine associations between study characteristics, including the subjects' ages (60 years versus <60 years) at baseline (i.e., at enrollment or at first exposure assessment), the duration of follow-up (
10 years versus <10 years), the location of study (United States versus elsewhere), and publication year (after 1998 versus before), on the pooled relative risks. We selected 1998 as a cutoff point because studies published after that year began to examine calcium and vitamin D hypotheses in relation to prostate cancer; 60 years of age and 10 years of follow up were selected as cutoff points because they were the approximate median values. Location was used to differentiate exposure to vitamin Dfortified liquid milk; vitamin D is added in the United States, but not generally in Europe (36).
We examined doseresponse relationships for dairy product and calcium intake and the risk of prostate cancer. Because the studies included in our meta-analysis used different units to report dairy product intake (e.g., servings, grams, grams of dry weight, frequencies, and glasses), we transformed all reported dairy intakes into servings per day. On the basis of the U.S. Food Guide Pyramid, we assumed that one serving of milk or yogurt was equivalent to 244 g, cheese to 43 g, ice cream to 132 g, and butter to 5 g (37). We assumed that 1 glass of milk, as reported, was 1 serving. On the basis of the average dairy intake distribution in the United States (38), we calculated the following intake ratios for milk, cheese, yogurt, ice cream, and butter as 7.5 : 1.0 : 0.4 : 1.0 : 0.1 for regular weight and 4.0 : 3.1 : 0.2 : 2.0 : 0.7 for dry weight, respectively. For studies that reported grams of total dairy item weight (9,26) or grams of dry weight (27), we distributed the total grams to this set of dairy items, based on these intake ratios. We converted dry weight to regular weight based on the water content of each food, obtained from the Nutrient Data System, version 4.06 (NDS, University of Minnesota, Minneapolis, MN). We then converted regular weight (g) to number of servings for each dairy item separately.
Because the most recent dietary guidelines recommend increased intakes of milk, cheese, and yogurt, we used intake servings of these dairy items per day in our doseresponse analysis (19). However, the specific dairy items reported varied by study. Some studies (25,29) reported only milk intake, whereas other studies (10,14,27,28) included butter or ice cream in their total dairy intakes. Tseng et al. (23) provided separate data on the servings of milk, cheese, and yogurt. For the remaining studies, we assumed intake proportions (by servings) of milk, cheese, yogurt, ice cream, and butter as 0.32 : 0.24 : 0.02 : 0.08 : 0.34, based on average dairy intake proportions in the United States (38). We then computed the number of intake servings of milk, cheese, and yogurt based on the dairy items that were reported by each study and on the intake ratio. For example, if a study reported only total intake from all of these five foods, we obtained milk, cheese, and yogurt intake servings by multiplying the total servings by 0.58 (the sum of 0.32, 0.24, and 0.02).
When median intakes per category were not presented in the publications, we estimated the mean intake of dairy item (milk, cheese, and yogurt) and calcium in each category by calculating the midpoint of the upper and lower boundaries. When the upper boundary of the highest intake category was not reported, we assumed that it had the same amplitude of intake as the preceding intake category (39,40). For example, if the highest calcium intake category was reported as greater than 2000 mg/d and the preceding category was reported as 15002000 mg/d, we would assign the average intake of the highest calcium intake category a value of 2250 mg/d. When studies in doseresponse analyses are combined, the reference group must be comparable across studies (39,40). Therefore, we eliminated from the doseresponse analyses two studies (9,10) in which the reference groups (lowest intake category) for dairy intake had considerably higher intakes than those in the other studies. For the same reason, we excluded one study (9) that had a high calcium intake in the reference group. Another study (14) was excluded from the doseresponse analysis of calcium intake and prostate cancer risk because it did not report total calcium intake. Thus, eight studies (14,2329) were included in our doseresponse analysis of intake of dairy products (i.e., milk, cheese, and yogurt) and prostate cancer risk, and four studies (8,23,26,28) were included in our doseresponse analysis of calcium intake and risk of prostate cancer. However, we also performed sensitivity analyses in which all studies were included.
To examine doseresponse relationships, we performed weighted regression analyses by regressing the natural log of the relative risk of prostate cancer for intakes of dairy products (milk, cheese, and yogurt) or calcium. All regression models were fit with no intercept term because all data points were derived from comparisons with reference groups (32,39,41). However, for completeness, we repeated the analyses with inclusion of intercept terms. We used the PROC MIXED procedure in SAS software with a repeated statement to allow estimates of log relative risks from the same study to be correlated. Random-effects models were used because they consider both within- and between-study variation. Because the relationships between dairy and calcium intakes and risk of prostate cancer may not be linear, we introduced quadratic terms and the natural logs of intakes (dairy or calcium) into the models. Because quadratic and natural log terms were not statistically significant (P>.05 for all), we used simpler models with original scales for dairy product or calcium intakes in our analyses.
We conducted sensitivity analyses for pooled estimates by the stepwise introduction of stricter criteria for inclusion of studies. We first limited the analysis to studies that had used validated food frequency questionnaires, and we computed the pooled relative risks for dairy products and for calcium intake separately for these studies. Only four of the 10 studies that examined dairy product intake and four of the six studies that examined calcium intake met this criterion. We then computed the pooled relative risks after excluding studies that had not adjusted for total energy intake. We also performed a sensitivity analysis for calcium intake by including the study by Baron et al. (31). We conducted sensitivity analyses for doseresponse relationships between dairy product intake and risk of prostate cancer. We repeated each of the simpler doseresponse analyses, described above, by including ice cream in total dairy intake. We also repeated these analyses by including only the studies that were conducted in the United States (14,2325,2729).
We used the Q, H, and I2 statistics (42) to examine heterogeneity among the studies included in this meta-analysis. For the Q statistic, a P value of less than .1 indicated statistically significant heterogeneity, an H statistic of less than 1.2 suggested no heterogeneity among studies, and I2 was the proportion of total variation contributed by between-study variation (42). Publication bias was examined with the use of funnel plots and with the Begg and Egger tests (4345). Relative risks of prostate cancer for men in the highest versus the lowest calcium or dairy product intake categories were used to examine publication bias. For the Begg and Egger tests, statistical significances were set at P<.1. Statistical analyses were performed with SAS statistical software (version 8.2, SAS, Inc., Cary, NC). All statistical tests were two-sided.
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RESULTS |
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DISCUSSION |
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In a recent meta-analysis of casecontrol studies, Qin et al. (20) reported a combined odds ratio of prostate cancer of 1.68 for men in the highest milk intake category versus men in the lowest intake category, which is greater than the pooled relative risk of prostate cancer (1.11) for subjects in the highest dairy intake category compared with those in the lowest category that we report here. This difference in risk estimates may, in part, reflect recall bias, a common problem in casecontrol studies that can lead to an overestimation of the association between a dietary variable and the risk of cancer (49). Furthermore, eight of the 11 studies in the meta-analysis by Qin et al. (20) used hospital-based control subjects; casecontrol studies that use hospital-based control subjects have been shown to report greater odds ratios than either casecontrol studies using population-based control subjects or prospective studies (50,51). Another possible reason for the difference in risk estimates is that the prospective and casecontrol studies had different exposure levels for the highest intake categories.
The recently released Dietary Guidelines for Americans 2005 recommends that Americans increase their intake of milk and milk products (19). The new goal for people who require 6.72 MJ/d (1600 kcal/d) or more (including all adult men and women) is 3 servings/d of low-fat or fat-free milk or milk products. Given the recent release of these new dietary guidelines and the prevalence of prostate cancer among adult men in the United States, our findings are timely and have important public health implications. The United States has the highest prostate cancer incidence in the world (46). Prostate cancer is the most common cancer among men in the United States (177 cases per 100 000 persons) (1), and the number of incident cases is expected to increase substantially as the population ages (2). Specifically, there were approximately 220 900 incident cases of prostate cancer in the United States in 2003 (52), and this number is projected to increase to 452 000 by 2045 (1). Prostate cancer currently ranks sixth among all specific causes of death in the United States (1). Doseresponse analyses suggested that, among male adults, intakes of 3 servings/d of dairy products were associated with an approximately 9% greater risk of prostate cancer, compared with the current average intake of 1.8 servings/d (53) (RR with and without intercept term = 1.1 and 1.09, respectively). In the United States, this would be associated with approximately 20 000 more incident cases per year. Approximately 35 000 and 99 000 Americans are projected to die of prostate cancer in 2005 and 2045, respectively (1).
There are several limitations that should be considered when interpreting our results. First, only four of the 10 studies used validated food frequency questionnaires to assess exposures. Misclassification of exposure may have occurred due to inaccurate dietary assessment in studies using unvalidated questionnaires. In addition, because total energy intake is associated with both dairy and calcium intakes as well as with risk of prostate cancer (12), it may be a confounder of these associations. Adjustment for total energy intake was done in only three studies that analyzed dairy product intakes and in only four studies that analyzed calcium intakes. However, results of our sensitivity analysis showed that excluding studies that had not adjusted for energy or that had not used a validated food frequency questionnaire did not greatly change the pooled relative risk. These results suggest that our findings are not substantially confounded by a lack of energy adjustment or the lack of validated food frequency questionnaires. Although we cannot distinguish between the effects of calcium from food sources and calcium from supplements on the risk of prostate cancer from the information provided by the articles, Giovannucci et al. (8) showed that dietary and supplemental calcium intakes were each associated with an increased risk of prostate cancer.
A second limitation of these analyses is that all studies assessed dietary intake based on responses to a single questionnaire that was administered only once. Thus, misclassification of exposures may have been introduced, which could lead to an underestimation of the risk of prostate cancer. Several studies have examined the stability of dietary intakes over time. Correlations generally showed good stability of reported dairy intake (r = .45 over 610 years) (54), of whole milk intake (r = .58 over 1525 years) (55), and of calcium intake (r = .63 over 3 years) over time (56).
A third limitation is that heterogeneity may be introduced by methodologic differences among studies, including different measurements of intake and outcomes used. In addition, intake levels ranged widely across the studies included in our meta-analysis. For example, the lowest intake categories ranged from 0 to 1.5 servings/d for dairy products and from 228 to 802 mg/d for calcium. Although statistical tests did not suggest heterogeneity among the studies, we used random-effects models, which consider both within- and between-study variation (32), for the pooled relative risk estimates and the doseresponse analyses.
A fourth limitation is that measurement units for dairy intake and reported dairy items varied across studies. To account for this variation, we converted the different units of measurement to number of servings per day, and computed the amount of milk, cheese, and yogurt intake for each study based on intake distributions determined from the U.S. national data. Such conversions inevitably introduce misclassification, which may lead to an underestimation of the associations. Moreover, the proportions of dairy intake may also vary across ethnicities and regions, thereby introducing errors. Because our dairy intake distribution categories were based on the U.S. dietary pattern, we conducted a sensitivity study to examine the doseresponse relationship between dairy intake and prostate cancer risk among the studies conducted in the United States. The estimated coefficients decreased only slightly from those obtained in our analyses of all studies. Therefore, the contribution of U.S. and non-U.S. studies did not produce errors in our analysis.
Fifth, our results are also limited because we were not able to examine the effect of prostate-specific antigen (PSA) screening on associations between dairy product and calcium intakes and the risk of prostate cancer. Only one study (28) conducted a subgroup analysis for men who had a PSA screening versus those who did not. However, Etzioni et al. (57) reported that PSA screening, which has been used widely in the United States after 1991, leads to overdiagnosis of prostate cancer (56). Detection bias, therefore, may be introduced to our study, which may lead to an underestimate of the associations, as suggested by Rodriguez et al. (28). They found a statistically significant relationship between calcium intake and prostate cancer among men who reported not having had PSA screening before 1992 (Ptrend<.01) but not among men who had a PSA screening test (Ptrend = .93) (28).
Sixth, our study is limited by the inclusion of only those studies that were published in English, although we did include two studies that were conducted outside of the United States. Results of the meta-regression analysis suggested that study location did not have a statistically significant effect on the pooled relative risks for dairy or calcium intake. We repeated a Medline literature search for nonEnglish-language studies, using the same search terms. Fourteen additional articles were found, but none met our inclusion criteria, based on a examination of their abstracts and titles.
Finally, our study is limited because of the small sample size. Only 10 publications examined associations with dairy intake, and only six publications examined associations with calcium intake. Thus, further sensitivity analysis restriction led to loss of statistical significance for pooled relative risks, although the risk estimates changed only slightly. Because of the small sample size, we had limited power to conclusively reject the null hypothesis of no publication bias. Therefore, we set statistical significance for publication bias at P<.1. We also presented funnel plots, which suggested consistent results for dairy product intake but not for calcium intake. The presence of possible publication bias could have led to an overestimate of the risk for calcium intake.
Several hypotheses have been proposed to explain the relationship between dairy product or calcium intakes and the increased risk of prostate cancer. Suppression of the production of plasma 1,25-dihydroxyvitamin D3 by plasma calcium is one possible mechanism underlying the association between dairy product and calcium intakes and the risk of prostate cancer (3,7). High 1,25-dihydroxyvitamin D3 concentrations may inhibit cellular proliferation and induce differentiation of normal and neoplastic prostate cells (8). Alternatively, higher intakes of milk and calcium have been associated with increased plasma levels of insulin-like growth factor-I (58,59). Results of a recent meta-analysis showed that high plasma concentrations of insulin-like growth factor-I were associated with a 49% increased risk of prostate cancer (60). Finally, it is possible that estrogen in milk may be another mechanism through which dairy intake may contribute to the etiology of prostate cancer (61).
Calcium is an important nutrient, and dairy products are the major source of calcium in most Western countries. It is well documented that increased calcium intakes are associated with reduced risks of osteoporosis, hypertension, and colorectal cancer (17,6265). On the other hand, two cohort studies have found positive associations between the risk of Parkinson's disease and greater dairy intake in men (66,67). In addition, high intakes of cow's milk have been hypothesized to contribute to male reproductive disorders because of its high estrogen content (68). Several prospective studies have found that higher milk intake was also associated with an increased risk of ovarian cancer (6971). Given the high prevalence of prostate cancer in American men, these findings, together with our findings, suggest caution before one embraces the new recommendations to increase dairy intake, especially among older men. More research, both population based and mechanistic, is needed to carefully examine both the potential benefits and risks of increasing intakes of dairy foods.
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Manuscript received April 20, 2005; revised September 22, 2005; accepted October 11, 2005.
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