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American Journal of Clinical Nutrition, Vol. 88, No. 5, 1297-1303, November 2008
© 2008 American Society for Nutrition

ORIGINAL RESEARCH COMMUNICATION

A 22-y prospective study of fish intake in relation to prostate cancer incidence and mortality1,2,3

Jorge E Chavarro, Meir J Stampfer, Megan N Hall, Howard D Sesso and Jing Ma

1 From the Departments of Nutrition (JEC and MJS) and Epidemiology (MJS), Harvard School of Public Health, Boston, MA; the Channing Laboratory (JEC, MJS, and JM) and Divisions of Aging and Preventive Medicine (HDS), Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA; and the Department of Epidemiology (MNH), Mailman School of Public Health, Columbia University, New York, NY

2 Supported by research grants CA42182, CA58684, and CA90598 and the Yerby Postdoctoral Fellowship Program.

3 Reprints not available. Address correspondence to JE Chavarro, Department of Nutrition, Harvard School of Public Health, 665 Huntington Avenue, Boston, MA 02115. E-mail: jchavarr{at}hsph.harvard.edu.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Fish and seafood n–3 fatty acids may prevent or delay the progression of prostate cancer, but epidemiologic studies do not uniformly support this hypothesis.

Objective: We examined the relation of fish and seafood n–3 fatty acid intakes with prostate cancer incidence and mortality.

Design: We conducted a prospective cohort study among 20 167 men participating in the Physician's Health Study who were free of cancer in 1983.

Results: During 382 144 person-years of follow-up, 2161 men were diagnosed with prostate cancer and 230 died of prostate cancer. Fish intake was unrelated to prostate cancer incidence. Survival analysis among the men diagnosed with prostate cancer revealed that those consuming fish ≥5 times/wk had a 48% lower risk of prostate cancer death than did men consuming fish less than once weekly [relative risk (RR) = 0.52; 95% CI: 0.30, 0.91; P for trend = 0.05]. A similar association was found between seafood n–3 fatty acid intake and prostate cancer mortality (RRQ5 versus Q1 = 0.64; 95% CI: 0.42, 0.99; P for trend = 0.02). These associations became stronger when the analyses were restricted to clinically detected cases.

Conclusion: These results suggest that fish intake is unrelated to prostate cancer incidence but may improve prostate cancer survival.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
More than 180 000 men in the United States are expected to be newly diagnosed with prostate cancer and 28 660 are expected to die of this disease in 2008 (1). Several aspects of diet may be important in preventing or slowing the progression of prostate cancer (2, 3). In vitro and animal studies suggest that long-chain n–3 fatty acids may inhibit prostate cancer growth (4, 5). However, epidemiologic studies examining the association between intake of these fatty acids or fish, their main dietary source (6), and the incidence of prostate cancer are inconsistent (7). In addition, data relating fish or long-chain n–3 fatty acid intake to prostate cancer progression or survival are sparse but encouraging (3).

We previously reported an inverse association, in a subsample of this cohort, between whole blood levels of long-chain n–3 fatty acids, a biomarker of intake, and prostate cancer risk (8). This association was particularly strong for clinically aggressive tumors, which suggests that these nutrients may either reduce the incidence of lethal disease or improve prostate cancer survival. To follow-up on these findings, we investigated whether fish intake was related to prostate cancer incidence and mortality among all men in the Physician's Health Study who reported their fish intake in 1983.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study population
This study is based in the Physician's Health Study (9, 10), a randomized trial of aspirin and β-carotene in the prevention of heart disease and cancer among 22 071 male physicians, aged 40–84 y in 1982. The aspirin component of the trial was terminated early in 1988 because of the benefits of aspirin on myocardial infraction (9). The β-carotene component of the trial was terminated in 1995 (10). At baseline, participants completed 2 mailed questionnaires, in which they provided information on medical history and several lifestyle factors. Follow-up questionnaires were mailed at 6 and 12 mo after randomization and yearly thereafter. Participants were asked to report newly diagnosed diseases of interest, including prostate cancer, in the yearly follow-up questionnaires.

Whenever a participant reported a diagnosis of prostate cancer, we requested hospital records and pathology reports to confirm the diagnosis and determine tumor stage, grade, and other clinical characteristics at diagnosis. Histologic grade was recorded as well, moderately, or poorly differentiated tumors, or following the Gleason scoring system, depending on the information available in the pathology reports. Low-grade tumors were defined as Gleason <7 or well or moderately differentiated. High-grade tumors were defined as Gleason ≥7 or poorly differentiated. Stage was recorded according to the modified Whitemore-Jewett classification scheme (11). Localized disease was defined as stages A and B, and advanced disease was defined as stages C and D. Cases without pathologic staging were classified as undetermined stage unless there was clinical evidence of distant metastases. Cases were divided according to the clinical presentation as prostate-specific antigen (PSA)-screening detected, clinical symptoms, metastatic symptoms, abnormal digital rectal exam (DRE), or other form of presentation by use of the clinical information available in the medical records. We were notified of deaths by family members and postal authorities and through periodic systematic searches of the National Death Index. We obtained death certificates and detailed medical records to determine cause of death, which was assigned by the End Point Committee of 3 physicians. Follow-up for this cohort is >99% complete for morbidity and mortality.

Dietary assessment
On the 12-mo questionnaire, the participants completed an abbreviated food-frequency questionnaire that did not allow the estimation of total energy intake. This questionnaire asked about the average intake during the previous year of 1) canned tuna fish, 2) dark meat fish (eg, mackerel, salmon, sardines, bluefish, and swordfish), 3) other fish, and 4) shrimp, lobster, or scallops as a main dish. For each food, the questionnaire offered 7 options for frequency of intake ranging from rarely/never to 2 or more times per day. The reproducibility and validity of these questions has not been assessed in this cohort but is available from a similar population of male health professionals (12). As a measure of reproducibility, the correlations between 2 food-frequency questionnaires completed 1 y apart were 0.54 for canned tuna fish, 0.63 for dark meat fish, 0.48 for other fish, and 0.67 for shrimp, lobster, and scallops (12). As a measure of validity, the correlations between prospectively collected diet records and intakes from the food-frequency questionnaire were 0.56 for canned tuna fish, 0.42 for dark meat fish, 0.39 for other fish, and 0.23 for shrimp, lobster, and scallops (12). As an additional measure of validity, we calculated the correlations between fish and seafood n–3 fatty acid intakes and whole blood levels of eicosapentaenoic acid and docosahexaenoic acid among 436 members of this cohort who had complete data on fish intake and served as controls in a previous case-control study of prostate cancer (Table 1Go; 8). These correlations were generally high and higher for types of fish known to have higher eicosapentaenoic acid and docosahexaenoic acid content, which suggests reasonable validity of fish and seafood n–3 fatty acid intakes among these men.


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  		TABLE 1.. Spearman correlation coefficients between whole blood levels of long-chain n–3 fatty acids and intakes of fish and n–3 fatty acids from seafood (n = 436)1

 
Intakes of the 4 fish items were summed to obtain average daily fish intake. We estimated the average daily intake of n–3 fatty acids from fish by multiplying the n–3 fatty acid content per serving of each item (0.69 g for canned tuna fish, 1.37 g for dark meat fish, 0.17 g for other fish, and 0.46 g for shellfish) by the frequency of intake. The n–3 fatty acid content for the specified portion sizes was obtained from the US Department of Agriculture (13). Men were divided into groups according to their intakes of total fish and specific fish intake, as well as into quintiles according to their intake of n–3 fatty acids from fish.

Statistical analyses
Men who died or reported a cancer diagnosis before the 12-mo follow-up questionnaire and men who did not report fish intake in this questionnaire were excluded, leaving 20 167 men for analyses. For the prostate cancer incidence analyses, men were followed from the date of return of the 12-mo questionnaire until the date of prostate cancer diagnosis, the date of death, or the end of follow-up (1 March 2006), whichever came first. We also analyzed prostate cancer mortality among the 2161 men diagnosed with prostate cancer during the follow-up. For the mortality analyses, men were followed from the date of prostate cancer diagnosis until the date of death or the end of follow-up, whichever came first.

The relative risks of prostate cancer and death from prostate cancer were estimated by using Cox proportional-hazards regression models, with the lowest intake category as the reference group. Tests for linear trend were performed using the median intake values in each category as a continuous variable. Multivariate models included terms for body mass index (BMI), physical activity, smoking status, race, use of multivitamins and vitamin E supplements, random assignment to aspirin or β-carotene, and intakes of dairy foods, meat, alcohol, and tomato products. Separate multivariate models for prostate cancer incidence were fit for cases according to grade at diagnosis, stage at diagnosis, lethality, diagnosis before or after the widespread use of PSA for prostate cancer screening (cutoff date: 31 December 1990), and clinical presentation of the case. Multivariate models for death from prostate cancer had additional terms for age at diagnosis, tumor stage and grade at diagnosis, and whether the tumor was detected through PSA screening. Additional mortality analyses were performed after excluding cases detected by PSA screening and by limiting the analysis to cases detected by an abnormal DRE or clinical manifestations. All analyses were performed in SAS version 9.1 (SAS Institute, Cary, NC). All P values are two-sided.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
We confirmed 2161 incident cases of prostate cancer diagnosed among 20 167 men followed for 382 144 person-years accrued through 2006. The mean follow-up time was 19 y. At baseline, fish intake was positively related to the intake of tomato products and alcohol, the use of multivitamin and vitamin E supplements, and vigorous physical activity and was inversely related to the intake of whole milk and meats. Men with a high fish intake were more likely to be white and were less likely to be smokers. Fish intake was unrelated to age at enrollment, height, BMI, intake of reduced-fat milk, and randomization group (Table 2Go). Most prostate cancer cases presented as localized (71.6%), low-grade (62.3%) disease and were diagnosed during the era of widespread PSA screening (84.3%). PSA screening was the most common presentation mode (61.9%), followed by clinical or metastatic symptoms (19.8%) and abnormal DRE findings (16.9%). The median age at diagnosis was 70 y.


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  		TABLE 2.. Baseline characteristics by category of baseline fish intake (n = 20 167)

 
Total fish intake was unrelated to prostate cancer risk. Most specific fish types were also unrelated to prostate cancer with the exception of "other" unspecified fish, which was positively related to this malignancy (Table 3Go). Fish intake remained unrelated to prostate cancer risk when this association was examined separately according to different tumor characteristics (stage, grade, lethality, date of diagnosis; data not shown). The positive association between "other" fish intake and prostate cancer was stronger among cases detected through PSA screening (as reported from medical records) and cases diagnosed after the widespread use of PSA screening for prostate cancer. The multivariate-adjusted relative risk for PSA-screening-detected prostate cancer comparing men in the highest with those in the lowest category of "other" fish intake was 1.37 (95% CI: 1.05, 1.79; P for trend = 0.01). The corresponding relative risk for cases detected during the PSA-screening era was 1.37 (95% CI: 1.15, 1.65; P for trend < 0.001). The associations of fish and seafood n–3 fatty acid intakes with prostate cancer incidence were not modified by baseline BMI or random assignment to aspirin or β-carotene in the trial (range of P for interaction = 0.27–0.75) .


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  		TABLE 3.. Relative risk (95% CI) for prostate cancer by intake of fish and seafood n–3 fatty acids (n = 20 167)

 
Next, we examined the association between baseline fish intake and prostate cancer mortality among the 2161 men diagnosed with prostate cancer. Baseline fish intake was inversely related to prostate cancer death (Table 4Go). The association was similar for most types of fish and for n–3 fatty acids from seafood, apart from the category of shrimp, scallops, and lobster, and was not modified by BMI or assignment to aspirin or β-carotene (range of P for interaction = 0.36–0.99)


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  		TABLE 4.. Relative risk (95% CI) for prostate cancer death by fish and seafood n–3 fatty acid intakes (n = 2 161 230 deaths)

 
We considered the possibility that these inverse associations were due to early detection or treatment of cases detected through increased PSA screening among health-conscious men who ate more fish. We therefore repeated the analyses after excluding all PSA-detected cases and by limiting the analyses to cases presenting by clinical symptoms or abnormal DRE. In the analyses excluding PSA-detected cases, intakes of fish and n–3 fatty acids from seafood remained strongly inversely related to prostate cancer mortality. The multivariate-adjusted prostate cancer mortality ratios for increasing intake of total fish were 0.82 (95% CI: 0.54, 1.24) for once a week, 0.85 (95% CI: 0.57, 1.25) for 2 to 4 times per week, and 0.51 (95% CI: 0.27, 0.95) for 5 or more times weekly, compared with men consuming fish less than once per week (P for trend = 0.08). The corresponding mortality ratios for increasing quintiles of n–3 fatty acid intake were 0.88 (95% CI: 0.57, 1.36), 0.83 (95% CI: 0.54, 1.27), 0.73 (95% CI: 0.44, 1.18), and 0.55 (95% CI: 0.34, 0.91), compared with men in the lowest quintile of intake (P for trend = 0.01). These associations became stronger when the analyses were restricted to men presenting with clinical symptoms or abnormal DRE (Figure 1Go). The multivariate-adjusted prostate cancer mortality ratio was 0.39 (95% CI: 0.17, 0.88; P for trend = 0.01) comparing men consuming fish 5 or more times weekly with men consuming fish less than once per week and 0.39 (95% CI: 0.21, 0.71; P for trend = 0.004) comparing the top with the bottom quintile of n–3 fatty acid intake from seafood.


Figure 1
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  		FIGURE 1.. Multivariate-adjusted cumulative prostate cancer mortality rates by a) fish and b) seafood n–3 fatty acid intake among digital rectal exam or clinically detected prostate cancer cases (n = 478 122 deaths). Adjusted for age at prostate cancer diagnosis; BMI; physical activity; intakes of alcohol, tomato products, and dairy products; smoking; race; use of multivitamins; use of vitamin E supplements; random assignment to aspirin or β-carotene; and tumor stage and grade at diagnosis.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In this prospective study, we found that fish intake was unrelated to prostate cancer incidence. Furthermore, we found that prediagnostic fish intake was inversely related to prostate cancer mortality. This inverse association between fish intake and prostate cancer mortality did not appear to be the result of earlier detection or treatment of PSA-detected cases and was not changed after we accounted for potential confounding factors.

Multiple animal and in vitro studies have shown that long-chain n–3 fatty acids inhibit prostate cancer growth (4, 5, 14, 15). These findings suggest that a higher intake of fish, in which these fatty acids are particularly concentrated (6), might have a role in the primary prevention of prostate cancer. However, most epidemiologic studies have not found an association between fish or long-chain n–3 fatty acid intake and prostate cancer risk (16–30). These null findings include most prospective cohort studies (16–18, 24–26, 30), most case-control studies (19–23, 27–29), and most studies with questionnaire-based diet assessment (16–18, 23–25, 28, 30) and biomarker assessment of fatty acids (19, 21, 22, 26, 27, 29). In contrast with our previous report (8), these findings do not support the hypothesis that fish or long-chain n–3 fatty acid intake decreases prostate cancer incidence and are consistent with the results of most of the epidemiologic studies.

We found a positive association between intake of "other" unspecified fish and prostate cancer risk that was restricted to PSA-detected tumors. It is likely that the observed association did not represent a deleterious effect of fish but rather was a spurious association arising from higher prostate cancer detection through PSA screening among health-conscious individuals. Fish intake was related to several healthy behaviors in this cohort. Although we did not collect data on PSA screening habits in the entire cohort, others have reported that PSA screening is more common among men who have other health-conscious behaviors (31, 32). Because PSA screening markedly increases detection of prostate cancer, not accounting for it will likely overestimate the association between healthy lifestyle habits, such as fish consumption, and prostate cancer risk. This possibility is consistent with our results.

Higher intakes of fish, particularly dark meat fish, and seafood n–3 fatty acids were related to lower prostate cancer mortality among the men diagnosed with prostate cancer. This association did not appear to be the result of earlier diagnosis or treatment of PSA-detected cases because it became stronger when these men were excluded from the analyses and when the analyses were restricted to cases known to be detected by abnormal DRE or clinical symptoms, which suggests that fish intake itself could be beneficial in delaying tumor progression. Few epidemiologic studies have examined whether fish or long-chain n–3 fatty acid intake influences prostate cancer progression or mortality. Chan et al (3) found that fish intake after prostate cancer diagnosis was inversely related to a composite outcome of prostate cancer progression, recurrence, or death. Also, Freeman et al (33) found that long-chain n–3 fatty acid levels in noncancerous prostate tissue of men undergoing radical prostatectomy for clinically localized prostate cancer were lower among men who later experienced biochemical recurrence of the disease than among those without recurrence. In a recent small pilot randomized trial, men assigned to a study diet that emphasized, among other changes, increased intake of n–3 fatty acid–rich fish, had an increase in PSA doubling time (34). Similarly, the studies that previously reported fish or long-chain n–3 fatty acid intake to decrease prostate cancer risk, including our previous work (8), have generally reported stronger associations with advanced stage (35–37), clinically aggressive (8), metastatic (38), or lethal (39) disease, which suggests that these dietary factors may have a role in reducing disease progression or mortality.

Laboratory data also suggest a role of marine n–3 fatty acids in reducing prostate cancer progression and mortality. Eicosapentaenoic acid, and to a greater extent its 15-LOX metabolite 15-HEPE, suppress the proliferation of multiple prostate cancer lines and the generation of COX-2 and 5-LOX metabolites of arachidonic acid (40) that are known to increase proliferation, tumor cell survival, and angiogenesis (41–44). Moreover, in a mouse model simulating prostate cancer recurrence after radical prostatectomy, mice fed an eicosapentaenoic acid precursor had reduced tumor recurrence, increased PSA doubling time, and decreased proliferation and increased apoptosis in recurrent tumor cells (14) Likewise, mice fed eicosapentaenoic acid in a model of hormone ablation therapy showed improved response to therapy (higher tumor apoptosis-to-mitosis ratios) and decreased progression into androgen independence (45).

Our study has several limitations. First, we had only a single assessment of fish intake at baseline. Although this certainly misclassifies the true exposure information over time, the effect of this misclassification would be to attenuate the true association between fish intake and our outcomes of interest. Second, the dietary information collected was insufficient to estimate total energy intake and thus we were unable to adjust our models for energy intake. However, all our models were adjusted for body size (expressed as BMI), one of the primary determinants of total energy intake, and for physical activity, the most important determinant of between-person variation in total energy intake (46). These adjustments may indirectly account for total energy intake to some extent. In a similar cohort of male health professionals, the correlations of fish and seafood n–3 fatty acids with total energy intake were low (0.16 and 0.17, respectively) compared with other nutrients (47) and the n–3 fatty acids were not important sources of energy (0.14% of calories; range: 0–2.96%), which further suggests that the inability to control for total energy intake may not have been an important source of bias, as previous analyses of dietary factors in this cohort also suggest (48). Third, we did not collect information on screening practices among the entire cohort. However, we had data available on the clinical presentation of cases. Last, because all the cohort members were physicians, some results from this study may not be directly generalizable. However, it is unlikely that the underlying biology of prostate cancer differs between physicians and nonphysicians, because previous findings from this and other cohorts of health professionals have been replicated in other populations (48–51). The strengths of our study include its prospective design and high follow-up rates for morbidity and mortality. Also, the large number of cases allowed us to examine the associations separately according to several tumor characteristics and to examine the relation of fish and long-chain n–3 fatty acid intake with prostate cancer mortality.

In summary, our findings suggest that fish intake may not affect the risk of developing prostate cancer, in agreement with most of the epidemiologic evidence to date. In addition, our survival data suggest that fish intake may reduce prostate cancer mortality.


   ACKNOWLEDGMENTS
 
The authors thank Weiliang Qiu for his assistance preparing the cumulative mortality figures.

The contributions of the authors were as follows—JEC, MJS, and JM were responsible for the study concept and design. JEC analyzed the data and drafted the manuscript. JM obtained funding. MJS, HDS, and JM contributed to the collection and assembly of the data. All authors critically reviewed the manuscript and provided important intellectual content and approved the final version of the manuscript. None of the authors had personal or financial conflicts of interest.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Received for publication May 14, 2008. Accepted for publication July 24, 2008.





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