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Departments of Epidemiology and Nutrition, Harvard School of Public Health, and the Channing Laboratory, Department of Medicine, Harvard Medical School and Brigham and Women's Hospital, Boston, MA 02115
ABSTRACT
INTRODUCTION
CASE CONTROL STUDIES
COHORT STUDIES
DIFFERENT TYPES OF FAT
FAT, ENERGY BALANCE AND
AGE AT PUBERTY
ENERGY INTAKE AND BREAST CANCER
SUMMARY
FOOTNOTES
LITERATURE CITED
ABSTRACT 
Rates of breast cancer vary approximately fivefold among countries and are strongly correlated with national per capita availability of dietary fat. However, this relation may be substantially confounded by many other factors associated with affluent lifestyles, such as reduced parity and physical activity. In large prospective epidemiologic studies, little evidence has been seen to support any major positive association between dietary fat and risk of breast cancer over the range of 15-45% or more of energy from fat. The observation that women in counties in China consuming approximately 25% of energy from fat have much lower rates of breast cancer than U.S. women with similar fat intakes provides additional evidence that factors other than dietary fat account for the large international differences. Some epidemiologic evidence suggests that monounsaturated fat and olive oil in particular may reduce risk of breast cancer when substituted for other types of fat. In contrast to findings for dietary total fat, most types of epidemiologic studies provide indirect support for a protective effect of energy restriction and reduced growth rates against breast cancer, which is consistently observed in animal studies of mammary carcinogenesis.
KEY WORDS: breast cancer · fat · energy · energy · dietINTRODUCTION
Dietary fat as a possible cause of cancer became of interest in the first half of the 20th century when studies by Tannenbaum and colleagues (Tannenbaum and Silverstone 1953
) indicated that diets high in fat could promote tumor growth in animal models. In this early work, energy (caloric) restriction also profoundly reduced the incidence of tumors. Dietary fat has a clear effect on tumor incidence in many models (Birt 1986, Freedman et al. 1990, Welsch 1992), although not in all (Appleton and Landers 1986, Sonnenschein et al. 1991); however, a central issue has been whether this is independent of the effect of energy intake. An independent effect of fat has been seen in some animal models (Birt 1986, Freedman et al. 1990, Welsch 1992), but this effect has been either weak (Ip 1990) or nonexistent (Boissonneault et al. 1986) in some studies designed specifically to address this issue.
Breast cancer is the most frequent malignancy among women in Western countries, and the disease still continues to show a steady increase (Sondik 1994). Rates in most parts of Asia, South America and Africa have been only about one fifth as high as in the United States (Aoki et al. 1992), but in almost all these areas rates of breast cancer are also increasing. Populations that migrate from low to high incidence countries develop breast cancer rates that approximate those in the new host country (Adelstein et al. 1979). However, among Japanese immigrants to the United States, not until the second or third generation do rates approach those of the general U.S. population (Buell 1973). This slower rate of change for Japanese immigrants may indicate delayed acculturation, although a similar delay in increase is not observed for colon cancer.
A major rationale for the dietary fat hypothesis has been the international correlation between fat consumption and national breast cancer mortality (Armstrong and Doll 1975). A principal limitation of both the international correlational and migrant studies is the potential for confounding; many other differences besides dietary fat exist between the low fat-consuming (less affluent) and high fat-consuming (more affluent) countries. Indeed, the correlations with gross national product are similar to those for fat intake (Armstrong and Doll 1975). Among the many factors that differ between low and high fat-consuming countries, reproductive behaviors, physical activity level and body fatness are particularly notable and are strongly associated with specific cancers. In a study of 65 Chinese counties (Marshall et al. 1992) in which both dietary assessment and mortality rates were measured using standardized methods and per capita fat intake varied from 6 to 25% of energy, only a weak positive association was seen between fat intake and breast cancer mortality. Notably, women in four counties consumed approximately 25% of energy from fat, yet experienced rates of breast cancer far below those of U.S. women with similar fat intake (Willett et al. 1992), thus providing strong evidence that factors other than fat intake account for the large international differences.
Breast cancer incidence rates have increased substantially in the United States during this century, as have the estimates of per capita fat consumption based on food disappearance data. However, surveys based on reports of individual actual intake, rather than food disappearance, indicate that consumption of energy from fat, either as absolute intake or as a percentage of energy, has actually declined in the last several decades (Stephan and Wald 1990), a time during which breast cancer incidence has increased (Sondik 1994).
CASE CONTROL STUDIES
), dietary fat was unrelated to risk of breast cancer. The results from 12 smaller case control studies were summarized in a meta-analysis by Howe et al. (1990), which included 4312 cases and 5978 controls. The pooled relative risk was 1.35 (P < 0.0001) for a 100 g increase in daily total fat intake, although the risk was somewhat stronger for postmenopausal women (relative risk = 1.48, P < 0.001). This magnitude of association, however, could potentially be compatible with biases due to recall of diet or the selection of controls (Giovannucci et al. 1993).
COHORT STUDIES
), no association was seen for overall fat intake over the range of <20 to >45% of energy from fat (Fig. 1). A similar lack of association was seen among postmenopausal women only and for specific types of fat. Only among the small number of women consuming less than 15% of energy from fat was a significant association seen; breast cancer risk was elevated more than twofold in this group. These cohort findings therefore do not support the results of the case control studies cited above.
by permission of The New England Journal of Medicine, copyright (1996), Massachusetts Medical Society. All rights reserved.
DIFFERENT TYPES OF FAT
). However, in a meta-analysis of case control studies (Howe et al. 1990), increased risk of breast cancer was somewhat greater for saturated (relative risk = 1.46) and monounsaturated fats (relative risk = 1.41) than for polyunsaturated fats (relative risk = 1.25).
). This is an intriguing observation given the relatively low rates of breast cancer in southern European countries, which have high average intakes of monounsaturated fats due to the use of olive oil as the primary fat. In two recent case control studies in Spain and Greece, women who used more olive oil had reduced risks of breast cancer (Martin-Moreno et al. 1994, Trichopoulou et al. 1995). Furthermore, olive oil has been shown to be protective relative to other sources of fats in some animal studies (Welsch 1992).
FAT, ENERGY BALANCE AND
AGE AT PUBERTY
), but in rural China the typical age is ~17-18 y (Chen et al. 1987). Further, the average age at menarche has been declining worldwide for the last 200 y (Wyshak and Frisch 1982), thus suggesting that increasing breast cancer rates that occur with increasing industrialization have been associated with decreasing average age at menarche.
, Merzenich et al. 1993, Moisan et al. 1990). In two cohorts (Maclure et al. 1991, Moisan et al. 1990), no association was found between the fat composition of the diet and occurrence of menarche, but a suggestion of earlier onset with higher fat intake was seen in one study (Merzenich et al. 1993). Collectively, these studies provide strong evidence that rapid growth rates prior to puberty play an important role in determining future risk of breast cancer, but that overall energy balance rather than the fat composition of the diet is most important.
ENERGY INTAKE AND BREAST CANCER
). The overall lack of association between energy intake and risk of breast cancer in prospective studies of breast cancer thus provides some evidence against an important protective effect of physical activity (Hunter et al. 1996) but does not exclude an effect of energy balance, because small differences between energy intake and expenditure that could not be detected epidemiologically could translate into important gains or losses of weight over a period of years. The most informative indication of energy balance in epidemiological studies will thus be anthropometric measurements: height as a reflection of childhood growth and weight and weight change in adults. These are discussed elsewhere (Hunter and Willett 1996, Ziegler 1997). In general, these studies do indicate positive associations between height and breast cancer incidence and associations between weight gain and risk of breast cancer in postmenopausal women, thus indicating adverse effects on breast cancer risk of positive energy balance and more rapid growth throughout life.
SUMMARY
, Potter 1996). Such a dietary pattern is also likely to be beneficial from the standpoint of cardiovascular disease. On the other hand, unsaturated fats (with the exception of trans fatty acids) are likely to be beneficial with regard to cardiovascular disease, and little evidence suggests that they adversely affect cancer risk; thus, efforts to reduce their intake do not seem to be warranted at this time. Because excess adiposity adversely affects risks of several cancers and cardiovascular disease, balancing energy from any source with adequate physical activity is extremely important.
FOOTNOTES
LITERATURE CITED
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