Association Between Diet During Preadolescence and Adolescence and Risk for Breast Cancer During Adulthood

Journal of Adolescent Health 52 (2013) S30eS35

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Review article Association Between Diet During Preadolescence and Adolescence and Risk for Breast Cancer During Adulthood

Somdat Mahabir, Ph.D., M.P.H. * Modiﬁable Risk Factors Branch, Epidemiology and Genomics Research Program, Division of Cancer Control and Population Sciences, National Cancer Institute, Bethesda, Maryland

Article history: Received May 3, 2012; Accepted August 31, 2012 Keywords: Preadolescent diet; Adolescent diet; Adult breast cancer

ABSTRACT IMPLICATIONS AND It is increasingly evident that diet during preadolescence and adolescence has important conse- CONTRIBUTION quences for breast cancer during adulthood. However, only a few epidemiologic studies have been Current evidence points to conducted on the relationship between diet during preadolescence and adolescence, and cancer a trend in which aspects of during adulthood. This situation is partly because of methodological challenges such as the long diet during preadolescence latency period, the complexity of breast cancer, the lack of validated diet assessment tools, and the and adolescence either large number of subjects that must be followed, all of which increase costs. In addition, funding increases or decreases risk opportunities are few for such studies. Results from the small number of epidemiologic studies are for adult breast cancer. inconsistent, but evidence is emerging that specific aspects of the diet during preadolescence and Several methodological iss- adolescence are important. For example, during preadolescence and adolescence, severe calorie uessuchasdietaryrecall restriction with poor food quality, high total fat intake, and alcohol intake tend to increase risk, bias may affect the validity whereas high soy intake decreases risk. Research on preadolescent and adolescent diet is a para- of the current evidence. digm shift in breast cancer investigations. This research paradigm has the potential to produce Therefore, it is crucial that transformative knowledge to inform breast cancer prevention strategies through dietary inter- research opportunities tar- vention during preadolescence and adolescence, rather than later in life, as is current practice, get the development of when it is perhaps less effective. Methodological challenges that have plagued the field might now tools that would accurately be overcome by leveraging several existing large-scale cohort studies in the U.S. and around the aidinboththeprospective world to investigate the role of diet during preadolescence and adolescence in risk for adult breast and retrospective collection cancer. of dietary data in early life Published by Elsevier Inc on behalf of Society for Adolescent Health and Medicine. such as in preadolescence and adolescence. However, because of the emerging evidence, it is not too early to consider issuing voluntary advice to adolescents regarding risk and potential benefits in preventing later breast cancer development.

Publication of this article was supported by the Centers for Disease Control and Prevention. Breast cancer results from the interaction of multiple deter- The author reports no potential conflicts of interest. minants, including genetic susceptibility and exposure to * Address correspondence to: Somdat Mahabir, Ph.D., M.P.H., Modifiable Risk modifiable risk factors. In addition, breast cancer diagnosis is Factors Branch, Epidemiology and Genomics Research Program, Division of age-related, with a marked increase in cancer incidence after the Cancer Control and Population Sciences, National Cancer Institute, Executive Plaza North, Room 5138, Bethesda, MD 20892. reproductive years. Most research on breast cancer focuses on E-mail address: [email protected]. risk factors during adulthood, but awareness is growing that

1054-139X/$ e see front matter Published by Elsevier Inc on behalf of Society for Adolescent Health and Medicine. http://dx.doi.org/10.1016/j.jadohealth.2012.08.008 S. Mahabir / Journal of Adolescent Health 52 (2013) S30eS35 S31 early-life exposures and events, including during preadolescence Preadolescent and Adolescent Diet and adolescence, can affect breast cancer risk. Clues from epidemiologic studies of cardiovascular disease Calories (CVD) indicate that early-life diet affects later risk for CVD. In 1989, Barker and colleagues [1] published data showing that In 1988, deWaard and Trichopoulos [19] proposed that an men with the lowest weights at birth and at 1 year of age had energy-rich diet during puberty and adolescence stimulates the the highest death rates from ischemic heart disease, and that growth of mammary glands and increases the occurrence of increasing weight was associated with a graded decrease in precancerous lesions in the breast. It is well established that risk. Barker et al proposed that an environment that induces energy restriction in animal models leads to reduced cancer poor fetal and infant growth will be followed by high risk of incidence. Prospective data from the Boyd Orr cohort study ischemic heart disease during adulthood. This idea has been (3,834 people took part in a family diet and health survey validated by several prospective cohort studies. For example, between 1937 and 1939) reported significant positive association studies in Sweden [2],Finland[3], Denmark [4], Norway [5], between childhood energy intake and all-cause cancer mortality, England [6], and Scotland [7] found that mortality from which included breast cancer [20]. Retrospective analysis of data ischemic heart disease was inversely associated with birth from the Nurses’ Health Study II (NHS II) cohort study of weight. In the U.S. [8,9] and India [10], a strong inverse asso- adolescent total caloric intake and breast cancer risk showed ciation between birth weight and nonfatal coronary heart a significant trend for increased risk with increased levels of total disease was reported. A recent systematic review of 17 pub- calories consumed [21]. A retrospective cohort study using the lished studies concluded that low birth weight increases risk Swedish Cancer Registry found that younger women with for ischemic heart disease [11]. If indeed early-life exposures anorexia nervosa (before age 40 years) have lower risk of breast affect CVD risk, by logical extension and because of similar cancer compared with women in the Swedish general population pathways, such exposures may also affect risk for breast [22]. Anorexia nervosa, an illness that occurs generally during cancer. For example, a single acute exposure to radiation to adolescence or early adulthood, is an indicator of caloric those who were in utero or in early childhood at the time of the restriction. On the contrary, early-life caloric restriction coupled atomic bombings of Hiroshima and Nagasaki resulted in with malnutrition or famine increases risk for breast cancer significantly elevated risk of malignancies decades later [12].In development. For example, women who were in the pubertal addition, studies of migrant populations show that rates of phase of life during World War II and exposed to calorie breast cancer change after migration and primarily affect the restriction without substantially poor diets had decreased risk of next generation [13,14], which supports the idea that early-life subsequent breast cancer compared with women exposed to exposures have a role. In Asia, breast cancer incidence rates are severe calorie restriction and poor food quality [23]. Birth much lower than in the U.S., but when Asian women migrate cohorts of subjects exposed to severe calorie restriction and poor to the U.S., their breast cancer risk increases gradually over diet quality such as experienced by European Jews who had several generations and eventually approaches that of U.S. potentially been exposed to the Holocaust and then migrated to white women [13]. Early studies suggest that the increased Israel had substantially increased breast cancer risk [24]. The breast cancer risk among Asians did not appear until the strongest increased breast cancer risk occurred in the youngest second generation was born in the U.S. [15]. These studies birth cohort of European Jews, which suggests that early-life [13,15] and other early studies [16,17] prompted the hypothesis exposure had a major role [24], and affirms that timing of the that exposure to western diet and lifestyle at an early age was exposure is clearly important. The Netherlands Cohort Study, in critical to breast cancer development. which a proxy was used to assess adolescent energy restriction In 2006, a review was published on early-life diet and the during the Hunger Winter (1944e1945), found evidence that risk for adult breast cancer [18]. The focus was not on the severe food restriction during the Hunger Winter significantly epidemiological evidence, but on postulated mechanistic links increased risk for adult breast cancer in the western rural areas, between early-life diet and breast cancer development. For but not in the western city areas [25]. Thus, the Netherlands this review, we used Pub Med to search for all published Cohort Study data did not provide clear evidence to support the epidemiologic studies of preadolescent and adolescent diet hypothesis that energy restriction resulting from severe famine in relation to adult breast cancer risk, and reviewed the leads to significantly increased breast cancer risk. evidence. In this article, we discuss a possible mechanistic Surrogate indicators of caloric consumption and, more link, and the challenges to and opportunities for elucidating generally, energy balance such as childhood growth, body fatness the role of preadolescent and adolescent diet and adult breast at young age, and adolescent body size all point to a role in breast cancer. cancer development. An advantage of presenting data on anthropometry is that it is a time-integrated measure of energy balance, whereas variability in total caloric intake may represent Definition of Preadolescence and Adolescence variability in physical activity, which makes it difficult to inter- pret some of the findings presented. Prospective data from For the purposes of this review, preadolescence is defined as a British cohort in which 2,547 girls were observed from birth in the period of childhood growth before the onset of puberty. 1966 to the end of 1999 showed that adult height was positively Adolescence is that phase after which a girl or boy has undergone associated with age at menarche and breast cancer. Overall, the puberty, but has not yet attained full growth. Adolescence can be breast cancer cases were taller and slimmer throughout child- considered as a preadult phase. Preadolescent and adolescent hood. Women who grew faster in childhood and reached adult dietary exposures are considered to be early-life exposures. In height above the average for their menarche category were at the terms of age, the preadolescence to adolescence spectrum is highest risk for breast cancer [26]. In a prospective analysis of from age 8 to18 years. NHS (1988e2004) and NHS II (1989e2005) among 188,860 S32 S. Mahabir / Journal of Adolescent Health 52 (2013) S30eS35 women (7,582 breast cancer cases) who recalled their body Red meat fatness at ages 5, 10, and 20 years, it was reported that body fatness at young ages had a strong and independent inverse An analysis of NHS II data showed that increasing adolescent association with both premenopausal and postmenopausal consumption of red meat was associated with a nonsignificant breast cancer [27]. Several studies have found that childhood and trend toward increased breast cancer risk [21]. However, a more adolescent body size is inversely associated with both premen- recent analysis of premenopausal women in NHS II showed that opausal and postmenopausal breast cancer risk [28e32]. increased levels of red meat consumed during adolescence was associated with a significant linear trend for increased premen- Fat opausal breast cancer risk [39]. A recent case-control study of Chinese immigrant women A recent analysis from the NHS II, based on 39,268 premen- reported that high consumption of red meat during adolescence, opausal women who completed a 124-item food frequency but not during adulthood, was associated with significantly questionnaire about their diet during high school (participants higher adult mammographic breast density [40]. This finding is were 34e53 years of age at the time they were surveyed in 1998) important despite the low level of red meat consumed by found that the highest intake of total fat compared with the Chinese immigrants compared with western populations. Data lowest during adolescence was associated with significantly from another case-control study found that frequent intake of increased risk for premenopausal breast cancer (relative ratio ¼ ground beef during preadolescence was associated with a 1.35; 95% confidence interval [CI], 1.00e1.81; p trend ¼ .05). nonsignificant 44% increased risk of adult breast cancer [41]. However, when data on consumption of saturated, monounsaturated, polyunsaturated, trans, animal, and vegetable fat French fries were analyzed separately, the associations were null [33].Inan earlier retrospective analysis of 47,355 participants in the NHS II, A nested case-control study of 582 women with breast cancer no association was found between adult breast cancer risk and and 1,569 control subjects, all selected from participants in the adolescent intake of total, animal, saturated, monounsaturated NHS and NHS II, assessed the preschool diet of nurses at ages 3e5 and polyunsaturated fats, although a significantly reduced risk years by collecting information from the mothers of the partici- was observed for the highest intake of vegetable fat [21]. Case- pants. Results showed that frequent consumption of french fries controls studies show inconsistent results [34,35]. In a nested during the preschool age was associated with significantly case-control study of participants within the NHS II cohort, increased risk for breast cancer later in life. For every one addi- women who consumed a high level of vegetable fat during tional serving of french fries per week during their preschool adolescence had a lower risk of breast cancer [34]. A small Utah years, adult breast cancer risk increased by 27% [41]. No other case-control study found that adolescent consumption of total data on preadolescent or adolescent french fry consumption and fat (or fat from milk, cheese, and yogurt) was not associated with adult breast cancer have been published. adult breast cancer risk [35]. The effect of adolescent fat consumption on adult mammo- Vegetables, fruit, and fiber graphic breast density, a marker of breast cancer risk, was also studied. In that study, women (1,142 postmenopausal women Prospective data from the Boyd Orr cohort of 4,999 men and and 451 premenopausal women) in the Minnesota Breast Cancer women who had been children in the households participating Family cohort who had mammograms but had no breast cancer in a survey of family diet and health, after 60 years of follow-up were asked to report on diet consumption during their adoles- (483 incident malignant neoplasms; 82 incident breast cancers), cence (age 12e13 years). Fat consumption was not associated reported that increased childhood fruit consumption but not with mammographic breast density among the women [36]. vegetable intake was associated with significantly reduced risk of Whether the women later developed breast cancer was not incident cancer [42]. A nested case-control analysis of partici- assessed. pants in the NHS to assess diet during high school and breast An intervention study that randomly assigned 8- 10-year-olds cancer, in which 843 eligible cases were diagnosed between the (n ¼ 286) to one of two groupsd(1) usual care or (2) a behavioral start of the study (1976) and before the return of the high school intervention that promoted a reduced fat dietdreported that diet questionnaire (1986), reported that women who consumed modest reductions in fat intake lowered serum concentrations of a higher level of dietary fiber during adolescence had a lower risk estradiol (29.8%; 95% CI, 5.4%e47.9%), nonesex hormone-binding for breast cancer than those who consumed a low level of fiber globulinebound estradiol (30.2%; 95% CI, 7.0%e47.7%), estrone [34]. Similarly, in an analysis of the NHS II, the highest quintile of (20.7%; 95% CI, 4.7%e34.0%), and estrone sulfate (28.7%; 95% CI, adolescent dietary fiber intake was associated with a significant 5.1%e46.5%) in the follicular phase and increased testosterone 25% lower risk of adult proliferative benign breast disease (BBD) (27.2%; 95% CI, 5.7%e53.1%) in the luteal phase of the menstrual (n ¼ 682 cases) than was those in the lowest quintile. High cycle in blood samples at the Year 5 visit [37]. During this time, intakes of nuts and apples during adolescence also were associ- girls in the intervention group consumed significantly less total ated with significantly reduced risk for BBD. Adolescents who and saturated fat. These results indicate that modest reductions consumed less than two servings of nuts per week had a 36% in adolescent fat intake reduce hormone concentrations consis- lower risk for BBD than adolescents who ate more than one tent with reductions in breast cancer risk. However, a follow-up serving per month [43]. However, an analysis of participants in of the participants at age 25e29 years found that serum estradiol the NHS II of diet during high school in 1998, at which time the concentrations were significantly higher in the behavioral participants were 34e53 years of age and observed for 7 years intervention group, which indicates that modest reductions in (1998e2005), during which time 455 invasive premenopausal adolescent fat consumption is unlikely to lower breast cancer breast cancer cases were diagnosed, showed that dietary fiber risk [38]. intake during adolescence was not significantly associated with S. Mahabir / Journal of Adolescent Health 52 (2013) S30eS35 S33

Table 1 Breast cancer risk in women and dietary soy consumption in childhood and adolescence

Authors Study design Sample size Childhood soy Adolescence soy Ethnicity

Shu et al, 200148 Case-control 1,459 cases and 1,556 controls .51 (.40e.65); p trend ¼ .001 Chinese Wu et al, 200246 Case-control 501 cases and 594 controls .51 (.31e.84); p trend ¼ .002 Asian-Americans (Chinese, Japanese, or Filipino) Thanos et al, 200647 Case-control 3,024 cases and 3,420 controls .81 (.71e.94); p trend < .01 Whites (Canadians) Korde et al, 200945 Case-control 597 cases and 966 controls .42 (.20e.90); .77 (.57e1.04); p trend ¼ .08) Asian-Americans (Chinese, p trend¼.02 Japanese, or Filipino) Lee et al, 200949 Prospective 73,223 (592 incident cases All women: .97 (.76e1.27); p trend ¼ .97 Chinese cohort after 7.4 years’ follow-up) Premenopausal: .57 (.34e.97); p trend ¼ .06 Postmenopausal: 1.20 (.87e1.65); p trend ¼ .20

premenopausal breast cancer development [33]. Similarly, in and 1,569 controls) [41] also found that consuming whole milk at a previous analysis of NHS II data, adolescent intake of total age 3e5 years was associated with a significant 10% decreased vegetables or total fruit did not affect breast cancer development risk for adult breast cancer. However, the Boyd Orr prospective [21]. A nested case-control analysis of NHS and NHS II data re- cohort study found that milk, total dairy and cream intake during ported null findings for the association between high school childhood were not associated with breast cancer risk after 65 dietary intakes of vegetable, fruit, and fiber and breast cancer years of follow-up [50]. In contrast, the Norwegian Women and development [41]. A population-based case-control study (1,647 Cancer prospective cohort study reported that childhood milk cases and 1,501 controls) of diet during adolescence and breast consumption was protective against breast cancer [51], but cancer in which participants were identified by random-digit a subsequent analysis with longer follow-up showed no associ- dialing reported that high versus low consumption of fruits ation between childhood milk consumption and breast cancer and vegetables during adolescence was associated with a [52]. Similarly, other large studies in North America found no nonsignificantly reduced risk of breast cancer [44]. In a much significant association between childhood dairy consumption smaller case-control (172 cases and 190 controls) study of and risk for breast cancer [21,44]. adolescent diet and breast cancer in Utah, the higher quartile of fiber intake produced a significantly elevated odds ratio for Adolescent Drinking increased postmenopausal breast cancer risk [35]. Good evidence suggests that high alcohol consumption Bean (soy) during late adolescence continues into adulthood [53]. Because adult alcohol consumption is a known risk factor for breast Evidence from in vitro animal studies and a few epidemio- cancer, it seems logical that adolescent alcohol consumption logical studies has been accumulating to suggest that would have similar effects. However, results of only one consumption of soy foods contributes to reductions in breast prospective study of alcohol intake assessed during adolescence, cancer risk. Table 1 shows the results of studies that investigated rather than retrospectively recalled years later, and risk of benign the association between childhood or adolescent dietary soy breast disease, a risk factor for breast cancer development, have intake and risk for adult breast cancer. A recent population-based been published [54]. The study found that the risk of biopsy- case-control study [45] of 579 first primary breast cancer cases confirmed benign breast disease increased with the amount of and 966 matched control subjects reported that increasing alcohol consumed among girls at ages 9e15 years. Girls who childhood (12 years old or younger) and adolescent (12e19 years drank 6 or 7 days per week had a 5.5 times higher risk of having old) soy intakes were associated with substantial reductions in benign breast disease compared with those who did not drink or risk for later breast cancer among Asian-American women. Adult had less than one drink per week [54]. These results are soy intake was also associated with reduced breast cancer risk in consistent with those of a retrospective study in which adults this population, but the strongest and most consistent associa- recalled alcohol consumption at age 18e22 years. Alcohol tion was with childhood intake [45]. Soy intake was associated consumption of 15 g/day or more at age 18e22 years, but not at with significantly reduced breast cancer risk among women who 15e17 years, was associated with significant increased risk for consumed the highest level of soy during either childhood (odds benign breast disease [55]. In the NHS I and II cohorts, high ratio [OR] ¼ .42; 95% CI, .20e.90; p trend ¼ .02) or adolescence alcohol consumption during adolescence was associated with (OR ¼ .77; 95% CI, .57e1.04; p trend ¼ .08) [45]. Four other a nonsignificant increased risk for adult breast cancer [30,56].To studies (Table 1)done of Asian-American women [46]; one of date, results from case-control studies of adolescent alcohol non-Asians, mostly white Canadian women [47]; and the other consumption and breast cancer risk have been inconsistent two of Chinese women [48,49]dreported that increased soy [57e60]. intake during adolescence reduced risk for adult breast cancer. In general, when soy consumption in these studies is compared, the daily median intake of soy is lower among Asian-Americans and Discussion whites than Asians or Chinese women in Shanghai. Limited research has been done on the role of preadolescent Whole milk and dairy and adolescent diet in risk for adult breast cancer. This situation is partly because of methodological challenges such as the long In addition to their findings on french fries, data from the NHS latency period for breast cancer development, which requires II (a nested case-control study of 582 women with breast cancer epidemiologic studies of preadolescent and adolescent dietary S34 S. Mahabir / Journal of Adolescent Health 52 (2013) S30eS35 exposures to have a long follow-up and be large and expensive. cancer earlier (during preadolescence and adolescence) rather Other challenges include the lack of validation of most of the than later in life. Research must also address the interactions diet, currently used dietary assessment tools for pre-adolescence and adiposity, inflammation, and immunity during preadolescence adolescence dietary consumption and the fact that dietary recall and adolescence, and breast cancer development during adult- is prone to bias. Most studies have used questionnaires devel- hood. The ideal epidemiologic study design would be prospective oped for dietary exposure assessment in adults. Errors in studies starting from the in utero period, with long follow-up for assessing diet during preadolescence and adolescence because of breast cancer outcomes. These types of prospective studies would the lack of valid measurement tools, lack of adequate dietary be costly, but the impact could be substantial. Several birth range of intake, and the unique characteristics of study pop- cohorts around the world could be collectively harnessed to ulations in different geographic locations contribute to the answer important questions regarding the role of preadolescence inconsistent results from prospective, retrospective, and case- and adolescence diet and adult breast cancer risk [66]. control studies, although few studies have been conducted Current evidence points to a trend in which aspects of diet overall. There is a need to validate the questionnaires used in the during preadolescence and adolescence either increase or existing cohort studies that have engaged in the retrospective decrease risk for adult breast cancer. Several methodological collection of early-life dietary data as a scientific building up of issues such as dietary recall bias may affect the validity of the research resources. Although some effort at validation has been current evidence. Therefore, it is crucial that research opportu- undertaken, it is inadequate and inconsistent in its implications. nities target the development of tools that would accurately aid in For example, in the data from the Fels Study established in 1929, both the prospective and retrospective collection of dietary data although some individual dietary factor were reasonably recal- in early life, such as in preadolescence and adolescence. However, led, it was found that the food frequency questionnaire did not because of the emerging evidence, it is not too early to consider validly measure overall preschool diet when completed by issuing voluntary advice to adolescents regarding risk and mothers 4 decades later [61], or overall adolescent diet when potential benefits in preventing later breast cancer development. completed by middle-aged and older adults 48 years after Such advice regarding healthier diet would be useful, not harmful, adolescence [62]. However, validation studies using the NHS II to good health in general and might potentially offset a percentage suggest that the food frequency questionnaire can reasonably of the breast cancer risk attributable to dietary exposures at the capture diet recalled by mothers [63] and by young adults [64]. age 8e18 range. 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