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Breast cancer and its association with alcohol Worldwide, more than a million women are However, while the association is consistent and diagnosed with breast cancer every year, considered confirmed for consumers of three accounting for 10% of all new cancers and 23% or more drinks per day (Rosenberg et al. 1993, of all female cancer cases. Breast cancer incidence Longnecker 1994, van den Brandt et al. 1995, rates vary considerably, with the highest rates in Swanson et al. 1997, Suzuki et al. 2010, Zhang and the developed countries and the lowest rates in Holman 2011), for consumers of one to two drinks developing countries (Cancer Research UK 2008). per day, the data is less consistent or erratic (Flatt Breast cancer is the most common cancer in et al. 2010). Indeed, it has been suggested that women in Australia, UK and the USA, where one in the relationship between alcohol consumption eight women will be diagnosed with breast cancer and breast cancer is linear (Bowlin et al. 1997, in Australia before the age of 85 (AIHW 2008), one Smith-Warner et al. 1998, Hamajima et al. 2003, in nine will be diagnosed at some stage in their life Thygesen et al. 2008, Chen et al. 2011) or increases in the UK (UK Office for National Statistics 2007), monotonically (Ellison et al. 2001, Tjonneland et al. and one in four will be diagnosed at some stage 2003, Thygesen et al. 2008) for the average daily in their life in the USA (CDC 2007). Breast cancer amount of alcohol consumed. The highest risk incidence rates continue to increase with age, with has been associated with consumption of six or the greatest rate of increase immediately prior to more drinks per day (Chen et al. 2011). It has also been suggested that consumption patterns may modify risk (Morch et al. 2007, Chen et al. 2011), An association between alcohol consumption of such that the consumption of four to five drinks
breast cancer
consumed per session may increase/double risk The first purported positive association between by 50% compared to only one drink consumed per alcohol consumption and breast cancer was session. Paradoxically, alcohol dependence does reported in 1977 (Williams and Horm 1977), and not increase the risk of breast cancer (Kuper 2000).
since then approximately 100 epidemiological studies have been published, which consistently It has also been suggested, but not substantiated, support such as association (Longnecker 1994, Key that there is a positive relationship between the et al. 2006). This association has been observed for duration (and hence accumulated amount) of both pre- and post-menopausal women of all ages, alcohol consumption over the lifespan of a woman and is observed to be independent of the type of and her risk of breast cancer, although age at alcoholic beverage consumed (Rosenberg et al. commencement of alcohol consumption appears 1993, Longnecker 1994, Bowlin et al. 1997, Hamajima to be irrelevant (Longnecker et al. 1995a, 1995b, et al. 2003, Petri et al. 2004, Key et al. 2006). The Bowlin et al. 1997, Swanson et al. 1997, Terry et association may also be more significant for certain al. 2006, Chen et al. 2011). For example, the risk of subtypes of breast cancer for example, hormone- breast cancer appears similar for cumulative alcohol sensitive rather than hormone-insensitive subtypes consumption prior to 40 years of age and after 40 (Millikan et al. 2008, Dolle et al. 2009, Kwan et al. years of age (Chen et al. 2011). Again it has been 2009, Li et al. 2010, Kabat et al. 2011).
suggested but not substantiated that there is long latency between onset of alcohol consumption and onset of breast cancer of approximately 20 has been proposed that alcohol may modify the years (Willett and Stampfer 1997, Thygesen et al. significance of these risk factors, and in particular, 2008), although some studies conversely suggest act additively with those risk factors that influence that recent consumption is a better predictor the concentration of hormones in plasma. It has of risk compared to retrospective consumption also been proposed that the factors other than due to confounders such as aging, hormonal/ family history, may act additively with the family menopausal status and body mass index (Ellison history risk factor, and also, that some of these risk et al. 2001, Horn-Ross et al. 2004, McDonald et al. factors may be limited to those women who have 2004, Tjonneland et al. 2004, 2007).
a positive family history of breast cancer (Gapstur et al. 1992, Horn-Ross et al. 2004). Consequently, it In addition, light to moderate alcohol consumption has been proposed but not proven that the positive after diagnosis of breast cancer generally does association between alcohol and breast cancer not appear to be associated with a recurrence of may be restricted primarily to women who have a breast cancer (Reding et al. 2008, Flatt et al. 2010), positive family history of breast cancer (Vachon et although increased body mass index may influence al. 2001). any association (Homes et al. 1999, Kwan et al. 2010). Further, light to moderate alcohol consumption Potential interaction between steroid hormones
after diagnosis of breast cancer also appears also and alcohol
not be associated with overall mortality (Holmes et Concerning the plasma concentration of the sex al. 1999, Dal Maso et al. 2008, Franceschi et al. 2009, or steroid hormones as a risk factor for breast Kwan et al. 2010), or it may actually reduce the risk cancer, there is a positive association between of overall mortality (Reding et al. 2008, Barnett et al. the risk of development of breast cancer and the 2008). There may, however, be an association with concentration of these hormones for both pre- and heavier consumption in developing, for example, post-menopausal women; the steroid hormones estrogen receptor positive breast cancer in the include androgens, such as testosterone, and contralateral breast (Li et al. 2009).
estrogens, such as estradiol, estrone and estriol Risk factors for breast cancer and alcohol
(Brinton et al. 1986, Bergkvist et al. 1989, Colditz et al. 1990, Steinberg et al. 1991, Colditz et al. 1995, The errancy of the data suggests that causation of Dorgan et al. 2001, The Endogenous Hormones breast cancer may be multi-factorial. The primary and Breast Cancer Collaborative Group 2002, Kaaks risk factors for breast cancer are purported to be: et al. 2005a,b, Eliassen et al. 2006). One source of lifestyle; inherited gene mutations and hence family endogenous estrogens is the aromatization of history; medical history; reproductive history (such androgens to estrogens, and alcohol has been as early menarche, nulliparity and late menopause); observed to increase this aromatization; the endogenous/exogenous hormones (such as conversion occurs primarily in the ovary for pre- hormone replacement therapy); body mass index; menopausal women and peripherally for post- and environmental exposure to carcinogens. It menopausal women (Figure 1). Figure 1. Primary mechanisms for the production of estrogens In pre-menopausal women:
dehydroepiandrosterone (DHEA) ——> androgens (testosterone) ———> estrogens (estradiol)
In post-menopausal women:
androgens (androdstenedione) ———> estrogens (estrone)
Breast cancer and its association with alcohol - 2 An elevated concentration of testosterone or in plasma which is positively associated with a estradiol may increase the risk of breast cancer decreased risk of mortality from cardiovascular approximately six- and five-fold, respectively disease. For example, from a meta-analysis of 38 (Dorgan 1994, 1996), where the risk may be epidemiological studies by Longnecker in 1994, proportional to concentration (The Endogenous daily consumption of one alcoholic drink was Hormones and Breast Cancer Collaborative Group associated with an 11% (7 to 16%) increased risk 2002). Indeed, Reichman et al. (1993) observed in of breast cancer compared with abstainers while pre-menopausal women that the concentration from a subsequent meta-analysis of 53 studies by of DHEA sulfate, testosterone and estradiol Clavel-Chapelom in 2002, daily consumption of one increased across the menstrual cycle following the alcoholic drink was associated with only a 7.1% (5.5 consumption of alcohol as did Muti et al. (1997) to 8.7%) increased risk. Furthermore, the pattern of and Rinaldi et al. (2006). The increase in sulfated alcohol consumption influences the concentration DHEA implies that alcohol may also increase the of the steroid hormones circulating in plasma, such production of DHEA sulfate in the adrenal cortex that chronic and heavy intake of alcohol is observed through its effect on the hypothalamic-pituitary- to lead to early menopause, a lower concentration adrenal axis (Rivier 1996, Dorgan 2001). Gavaler of gonadotrophins post-menopausally and an and van Thiel (1992) and Rinaldi et al. 2006 reported increased concentration of the steroid hormones similar observations in post-menopausal women post-menopausally (Gavaler and van Thiel 1987).
and Hankinson et al. (1995, 1998) also reported an increase in the plasma concentration of estrone, Potential
interaction
which is purported to be a primary source of replacement therapy and alcohol
estradiol in breast cancer cells, following the Post-menopausal women on estrogen replacement consumption of alcohol. Furthermore, the effect therapy (ERT) who consume alcohol are generally of alcohol on the sex hormones is both acute and observed to have a significantly elevated plasma concentration of estradiol as compared with women not using ERT (Ginsberg et al. 1996 and Gavalar The data shows also that there is a dose dependent 1998). Ginsberg et al. (1996) observed an increase response to alcohol on the aromatization of of approximately 300%, which corresponds to the testosterone and on the subsequent concentration preovulatory peak in the menstrual cycle, where the of estradiol in plasma, which then peaked and changes in the circulating concentration of estradiol plateaued (Longnecker et al. 1995); this was significantly correlated with changes in the blood consistent with the risk of breast cancer in concentration of alcohol on both the ascending consumers of alcohol compared to abstainers and descending limbs of the blood alcohol curve. (Longnecker et al. 1988). Purported mechanisms The plasma concentration of this steroid hormone, by which alcohol may increase the concentration which correlated with the plasma concentration of steroid hormones include: stimulation of of follicle stimulating hormone (FSH), is correlated ovarian theca cells to produce androgens through with total amount of alcohol consumed per week increased pituitary luteinizing hormone secretion; (Gavalar 1998); interesting Gavalar also observed an induction of androgen catabolism in the liver; and/ increase in the concentration of estrone. However, or increased liver aromatase activity leading to an the interaction of alcohol and ERT is not simple as the increased conversion of androgens to estrogens.
dose-response relationship of ERT is inverse when a The question remaining is at what level of moderate amount of alcohol is consumed (Gavaler moderate consumption the elevation of risk 1998). occurs, and then relative risk (risk benefit ratio) Consequently, accumulating data suggests that when compared with other causes of death, such alcohol consumption is most strongly associated as cardiovascular disease, which increases in post- with the risk of breast cancers that are hormonally menopausal women as a consequence of a reduced responsive, such as lobular (5-10% of all cancers) concentration of estradiol in plasma; estrogens and hormone receptor positive tumors (estrogen significantly lower the concentration of cholesterol receptor positive (ER+), such as ER+PR+ and ER+PR- Breast cancer and its association with alcohol - 3 subtypes) (66%) (Enger et al. 1999, Li et al. 2003, cancer, the gene has been observed to be mutated Terry et al. 2006, Suzuki et al. 2008, Li et al. 2010, in 15 to 50% of tumors (Olivier and Hainaut 2001). Kabat et al. 2011) as well as with the risk of tubular (2%) (Rosenberg et al. 2006); this is consistent with The concurrent consumption of alcohol and folate data suggesting that ERT is most strongly associated (at least 300 mg/day) has been observed to reduce with lobular cancers (Li et al. 2000, 2008, 2010, the relative risk of alcohol-induced breast cancer Zanetti-Dallenbach et al. 2008). Data also suggests to 1.05 for women consuming greater than 15 that no or a negative association observed for triple g alcohol/day or one and a half standard drinks, negative breast cancer (ER-/PR- or ER-/PR) or basal- but was only 0.55 for women consuming greater like breast cancer (Millikan et al. 2008, Dolle et al. than 600 mg/day of folate. Indeed, the concurrent 2009, Kwan et al. 2009, Trivers et al. 2009, Kabat et supplements reduces the relative risk to 0.74 for women consuming greater than 15 g alcohol/day The suggestion of a further increased risk of breast compared to those not using vitamins (Zhang et al. cancer by post-menopausal woman who use ERT 1999). The interaction between alcohol and folate and who are also light to moderate consumers has been observed to be primarily limited to estrogen of alcohol remains controversial (Suzuki et al. receptor negative (ER-) breast cancer tumors (Zhu 2005, Nielsen and Gronbaek 2008), in particular and Williams 1998, Sellers et al. 2002, Zhang et al as ERT decreases the risk of other diseases such 2005), which is consistent with an interaction of as cardiovascular disease (Ross et al. 1981, Szklo alcohol and folate on breast tissue tumors being et al. 1984, Stampfer et al. 1985), osteoporosis mainly through the primary metabolite of alcohol, (Hutchinson et al 1979, Weiss et al. 1980, Paganini- acetaldehyde, which is directly carcinogenic as Hill et al. 1981), and dementias such as Alzheimer’s well as indirectly carcinogenic via folate depletion, disease (Tang et al. 1996, Zuccala et al. 2001, Ganguli, independent of circulating estrogens and estrogen et al. 2005, Stampfer et al. 2005, McDougall et al. 2006, Reid et al. 2006, Wright et al. 2006) and hence decreases the risk of death from all causes (Bush et Potential interaction between inherited gene
al. 1983, Criqui et al. 1988, Thun et al. 1997).
mutations and alcohol
Inherited mutations in the BRCA-1 and BRC-2
Potential interaction between folate and alcohol
genes confer significantly increased lifetime risks An adequate consumption of folate, however, may of breast cancer, in particular for BRCA-1 mutation reduce the increased risk of breast cancer associated carriers less than 50 years of age (Wooster et al. with alcohol consumption (Zhang et al. 1999, 2005, 1995; Tavtigian et al. 1996, Antoniou et al. 2003). Rohan et al. 2000, Sellers et al. 2001, Baglietto et al In contrast to the general population, light to 2005, Stolzenberg-Solomon et al. 2006, Tjonneland moderate alcohol consumption does not appear et al. 2005, 2006). For example, while alcohol to increase the risk of breast cancer in women interferes with DNA synthesis and repair, folate is carrying a BRCA-1 gene mutation although higher involved in DNA synthesis, repair and methylation. amounts may be multiplicative (McGuire et al. 2006, In animal models, folate supplementation reduces Dennis et al. 2010, Dennis et al. 2011), which may DNA strand breaks in the p53 gene (Kim et al. 2000); reflect hormone receptor status; estrogen receptor the P53 protein regulates the cell cycle to prevent negative tumors account of 80% of tumors in BRCA- genome mutation, and hence functions to suppress 1 mutation carriers (Foulkes et al. 2004, McDonald et tumors. It can activate DNA repair proteins when it al. 2004, Zhang et al l 2007). Risk appears increased in recognizes damaged DNA, hold the cell cycle at the women carrying a BRC-2 gene mutation and appears G1/S regulation point on DNA damage recognition additive with increased body mass index (Dennis to prevent uncontrolled cell division and can et al, 2011). Light to moderate wine consumption, initiate apoptosis, the programmed cell death, if however, actually may be protective for BRCA-1 but the DNA damage proves to be irreparable. Cancer not BRCA-2 mutation carriers (Dennis et al. 2010, occurs when the rate of proliferation of mutated cells greatly exceeds the rate of apotosis. In breast Breast cancer and its association with alcohol - 4 Other potential mechanisms of action for alcohol activation of these enyzmes (Anderson et al. 1995).
in breast cancer
While these observations are yet to be confirmed in Concerning biological or environmental exposure, human breast tissue, the induction of cytochrome alcohol is purported to influence the local and P4502E1 is associated with an increased production systemic metabolism of mammary carcinogens. Risk of reactive oxygen species that are associated with is the sum of numerous factors, each with a small DNA damage including single and double strand risk, such that the summed risk is high from the breakage (Wright et al. 1999, Koch et al. 2004), enhancing or synergistic effects or influences of the where breast tissue tumors contain an approximate risk factors. It is suggested that approximately 50% nine-fold higher concentration of these DNA of breast cancer is not related to genetic/hormonal modifications (Li et al. 1999). risk factors, but is related to the environment as Alcohol may additionally influence alterations in cell observed from cultural/geographic correlations cycle behaviour such as cell cycle duration leading for risk. With respect to environmental exposure to to the hyperproliferation of mutated cells, that is, carcinogens, metabolism in the body may either uncontrolled cell division; nutritional deficiencies, activate or detoxify the carcinogen. For example: such as methyl-, vitamin E-, folate- pyridoxal carcinogen —> toxic intermediates —> detoxified —>excreted phosphate-, zinc- and selenium-deficiencies; and alterations of the immune system eventually resulting in an increased susceptibility to certain virus infections such as hepatitis B virus and hepatitis whereby, a decrease in or inhibition of metabolism, There is also accumulating data that the primary increases the exposure of the circulating carcinogen metabolite of alcohol, acetaldehyde, is partly in the blood to organs/tissues, such as the breast.
responsible for alcohol-associated carcinogenesis. Because alcohol is not itself genotoxic and nor Acetaldehyde is directly carcinogenic and tumorigenic in animals, potential mechanisms mutagenic interfering with both DNA synthesis for the positive association between alcohol and repair. It also binds to cellular proteins and DNA and breast cancer include the facilitation of forming stable protein and DNA adducts, which carcinogens into cells, the induction of carcinogen result in physical and functional impairment of the activating enzymes, the inhibition of DNA repair cell and consequently in an immunological cascade and the promotion of tumors. Potential ubiquitous reaction, and in the occurrence of replication carcinogens include N-nitrosamines, to which errors and/or mutations in oncogenes or tumor people are exposed from sources such as tobacco suppressor genes (Dellarco 1988, Fang and Vaca and N-nitrosodimethylylamine (NDMA). The former 1995, Nakamura et al. 2003). Acetaldehyde also carcinogen is metabolized by cytochrome P4502E1 degrades folate in the colon, where a folate dietary enzymes in the liver, such that in the presence deficiency has been associated with an increased of alcohol, this metabolism is inhibited and the risk of breast, pancreatic and colon cancer (Gloria et unmetabolized carcinogen circulates in the blood al. 1997, Duthie et al. 2000, Hussien et al. 2005). together with the alcohol. The coexposure of the Alcohol is metabolised to acetaldehyde by the carcinogen and alcohol to tissues has been observed enzyme alcohol dehydrogenase (ADH), where approximately 96-98% of ADH activity occurs in the In addition, cytochrome P4502E1 enzymes have liver but it also expressed and regulated by other been observed in animal breast tissue and there tissues including breast tissue (Seitz et al. 1998, is greater expression of these enzymes in breast Wright et al. 1998, Triano et al. 2003). Individuals tissue tumors compared to normal breast tissue, differ in their ability to metabolise alcohol because such that high concentration of circulating of genetic differences in ADH; ADH is encoded by carcinogen may be activated by the cytochrome at least five different genes that result in enzyme P4502E1 enzymes and/or alcohol may induce the classes of different metabolic activity for alcohol and Breast cancer and its association with alcohol - 5 hence concentration of circulating acetaldehyde Although animal studies show that alcohol does (Bosron and Li 1986). For example, Class 1 ADH not initiate or promote tumorogenesis and may polypeptide subunits are encoded by three specific actually decrease the incidence of tumors, some gene loci, ADH1A (_ ), ADH1B (_ ) and ADH1C studies also show that alcohol may effect or enhance ( ) where, in vitro, the (_ )-a polypeptide subunit metastasising tumors (Weiss et al. 1995, Swanson et encoded by the ADH1C*1 variant metabolises al. 1997), and that this effect is dependent on the alcohol to acetaldehyde 2.5-times faster than stage of alcohol consumption, that is, pre- or post- the ADH1C*2 variant (Lee et al. 2006), and the - treatment with a carcinogen, and on the amount of 1 polypeptide subunit encoded by the ADH1B*2 alcohol consumed. While it is unknown what stage variant metabolises alcohol to acetaldehyde 100- of carcinogenesis is affected by alcohol, recent times faster than the subunits encoded by the research implies that alcohol acts at a late stage of ADH1B*1 variant, but has a lower affinity for alcohol carcinogenesis (Weiss et al. 1995, Swanson et al. (Hurley et al, 1990). Several studies have examined 1997). an association between the different polypeptide subunits and risk of breast cancer with conflicting Conclusions
and hence inconclusive results (Freudenheim et al. While there is an indisputable association between 1999, Hines et al. 2000, Lilla et al. 2005, Sturmer et alcohol consumption and the risk of breast cancer, al. 2005, Terry et al, 2006, Visvanathan et al. 2007, the mechanisms behind the association require Kawase et al. 2009, Larsen et al. 2010). Results further elucidation. This risk of breast cancer from one recent study supports an association should not, however, be considered in isolation between ‘fast’ metabolisers of alcohol per se and from the risk of other factors for mortality, such as hence the ‘fast’ appearance of acetaldehyde and an cardiovascular disease, whereby cardiovascular increased risk of breast cancer (Terry et al. 2006), disease is the primary cause of mortality in the where women with the fast metabolising ADH1C*1 industrialised or westernised world. Indeed, the light variant and hence ADH1C*1,1 genotype have been to moderate consumption of alcohol is associated observed to be 1.8-times more at risk for breast with a significantly reduced risk of mortality from cancer than women with other genotypes (Coutelle cardiovascular disease and from all causes, for et al. 2004). Intriguingly, the expression of ADH1 is both men and women, irrespective of age and breast tissue is decreased in invasive breast cancers ethnicity (Boffetta and Garfinkel 1990, Marmot (Triano et al. 2003). The results of another recent and Brunner 1991). Thus, it may be advisable for study, however, also suggests that slow converters women to enumerate and evaluate their risk factors of alcohol to acetaldehyde may also be at increased for cardiovascular disease and for breast cancer, in risk of developing breast cancer, which implies that addition to the amount and pattern of their alcohol both alcohol and its primary breakdown product consumption, before considering abstaining from acetaldehyde could be contributing compounds alcohol.
Creina Stockley MSc Clinical Pharmacology, MBA; is Health and Regulatory Information Manager,
AWRI and a member of AIM’s Social Scientific and Medical Council.
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