Critique 270 – Alcohol consumption and prognosis and survival in breast cancer survivors: the Pathways Study

Title

Alcohol consumption and prognosis and survival in breast cancer survivors: the Pathways Study

Authors

Kwan ML; Valice E; Ergas IJ; Roh JM; Caan BJ; Cespedes Feliciano EM; Kolevska T; Hartman TJ; Quesenberry CP; Ambrosone CB; Kushi LH

Citation

Cancer (2023) https://doi.org/10.1002/cncr.34972

Author’s Abstract

Background The impact of alcohol consumption on breast cancer (BC) prognosis remains unclear.

Methods The authors examined short-term alcohol intake in relation to recurrence and mortality in 3659 women who were diagnosed with stage I-IV BC from 2003 to 2015 in the Pathways Study. Alcohol drinking in the past 6 months was assessed at cohort entry (mean, 2 months postdiagnosis) and 6 months later using a food-frequency questionnaire. Study end points were recurrence and death from BC, cardiovascular disease, and all causes. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using multivariable Cox proportional hazards models.

Results Over an average follow-up of 11.2 years, 524 recurrences and 834 deaths (369 BC-specific and 314 cardiovascular disease-specific) occurred. Compared with non-drinkers (36.9%), drinkers were more likely younger, more educated, and current or past smokers. Overall, alcohol consumption was not associated with recurrence or mortality. However, women with higher body mass index (BMI ≥ 30 kg/m²) had lower risk of overall mortality with increasing alcohol consumption for occasional drinking (HR, 0.71; 95% CI, 0.54-0.94) and regular drinking (HR, 0.77; 95% CI, 0.56-1.08) around the time of diagnosis, along with 6 months later, in a dose-response manner (p < .05). Women with lower BMI (<30 kg/m²) were not at higher risk of mortality but were at possibly higher, yet nonsignificant, risk of recurrence for occasional drinking (HR, 1.29; 95% CI, 0.97-1.71) and regular drinking (HR, 1.19; 95% CI, 0.88-1.62).

Conclusions Alcohol drinking around the time of and up to 6 months after BC diagnosis was associated with lower risk of all-cause mortality in obese women. A possible higher risk of recurrence was observed in nonobese women.

Forum comments

Background including previous results

In the USA, approximately one in eight women, and in the European Union and Australia one in seven, respectively, will be diagnosed with breast cancer in their lifetime. The aetiology of breast cancer is attributed to a complex interaction between various modifiable and non-modifiable factors. Breast cancer aetiology is determined by an interaction of genetics, environmental, nutritional and hormonal elements. Risk factors include age, prior history of breast cancer, positive family history, obesity, smoking, alcohol consumption, early menarche, late menopause, sedentary lifestyle, nulliparity and hormone replacement therapy (Fakhri et al., 2022). Certain inherited high penetrance gene mutations greatly increase breast cancer risk, the most dominant being mutations in the genes BRCA1, BRCA2 and PALB-2 (Shiovitz & Korde 2015). Factors associated with decreased risk of breast cancer include multiparity, history of breastfeeding, physical activity and weight loss (Admoun & Mayrovitz, 2022). Risk increases with older age with about 80% of breast cancer patients being older than 50 years.

Whereas US breast cancer incidence rates have increased by 0.5% per year in recent years, for example, potentially due to improved screening and awareness, breast cancer death rates have been decreasing steadily since 1989, for an overall decline of 43% through 2020. This decline has been similarly observed in the EU and Australia. Breast cancer, however, remains the second leading cause of cancer death in women, second only to lung cancer each year in these countries (ACS, 2023). For all stages of breast cancer combined, Western European countries have all attained a five-year net survival of at least 80%, while Australia has attained a five-year net survival of 92% and a 10-year relative survival of 86.8%.

The association between alcohol consumption and breast cancer incidence has been established since 1998. Smith-Warner et al. (1998) performed a pooled analysis on six cohort studies showing a linear increase in breast cancer incidence in women over the range of consumption reported by most women. Similarly, other more recent meta-analyses have confirmed the association between alcohol consumption and breast cancer incidence (Bagnardi et al., 2001, Ellison et al., 2001). With the possibility that some overdiagnosis may exist (Mu & Mukamal, 2016) and with the possibility that the increased risk of any cancer among light-moderate drinkers may be substantially due to underreporting of intake (Klatsky et al., 2014), it is well-accepted that a woman’s risk of breast cancer will increase. Increase estimates range from 4% (Seitz et al., 2012; Zhou et al., 2022) to about 10% (Smith-Warner et al., 1998) with each 10 g of daily alcohol consumption. This means that a consumption of 10-12 g alcohol per day (one glass) will increase a woman’s risk for breast cancer from approximately 12.5% to about 13-13.75%.

It has been proposed that factors other than genetic factors, may act additively with this family history risk factor and even that some of these risk factors may be limited to those women who have a positive family history of breast cancer (Gapstur et al. 1992). A similar conclusion was drawn from a recent meta-analysis showing that the effect of alcohol consumption on the incidence of breast cancer is mainly manifested in oestrogen receptor (ER) positive breast cancer (Sun et al., 2020).

The mechanisms underlying the alcohol-breast cancer association are less well established. Based on the strong ER-positive breast cancer association, alcohol consumption may increase steroid hormones and oestrogen receptors (Oyesanmi et al., 2010). Alcohol consumption does not seem to increase mammographic density (McDonald et al., 2016) as a way to increase breast cancer risk.

Lifestyle in general appears to be very important in reducing the risk for breast cancer. In a recent observational study of patients with high-risk breast cancer, strongest collective adherence to cancer prevention lifestyle recommendations including drinking up to one alcoholic beverage daily, was associated with significant reductions in disease recurrence and mortality (Cannioto et al., 2023). In this study with most patients being diagnosed with ER-positive breast cancer, patients with highest versus lowest lifestyle index scores experienced a 37% reduction in disease recurrence and a 58% reduction in mortality.

One of the positive lifestyle factors in the Cannioto et al. (2023) study was also eating a colourful variety of vegetables, fruits, and plenty of whole grains. This may have contributed to a higher folate intake, whereas a higher folate intake is associated with a decreased risk of breast cancer among Japanese women (Islam et al., 2013) and younger American women (Ja Kim et al., 2017). Also, fibre intake may have been higher, where low fibre intake (<18.5 g/day) was associated with an increased risk for breast cancer (Romieu et al., 2017).

Prognosis and survival in individuals with breast cancer in relation to alcohol consumption is a topic that has been researched before. Various cohort studies indicated no association between pre- and post-diagnosis alcohol consumption and breast cancer recurrence or breast cancer specific mortality.  A recent population-based cohort study including 1926 Black or African American breast cancer survivors also studied the association between pre-diagnostic alcohol consumption with all-cause mortality and breast cancer-specific mortality. No statistically significant association was found between alcohol consumption and all-cause mortality or breast cancer-specific mortality (Zeinomar et al., 2023).

A meta-analysis by Ali et al. (2014) based on 11 cohort studies also showed that there was little evidence that pre- or post-diagnosis alcohol consumption was associated with breast cancer-specific mortality for women with ER-positive disease. There was weak evidence that moderate post-diagnosis alcohol consumption was associated with a small reduction in breast cancer-specific mortality in ER-negative disease.

Another recent systematic review and meta-analysis was performed by the Japanese Breast Cancer Society to assess breast cancer recurrence associated with alcohol consumption. This study also showed that no significant increase or decrease in risk associated with alcohol consumption. Concerning breast cancer-related mortality, similarly no significant increase or decrease in risk associated with alcohol consumption was observed (Nomura et al., 2023).

Thus, whereas the positive association between alcohol consumption and breast cancer incidence is well-established, so is the absence of a positive association between pre-diagnosis and post-diagnosis alcohol consumption and breast cancer recurrence and breast cancer specific mortality.

Design and main outcomes

The Pathways Study is a prospective cohort study of 3659 female breast cancer survivors who were diagnosed with invasive breast cancer from 2005 to 2013 at Kaiser Permanente Northern California (KPNC). Alcohol consumption was collected from participants at enrolment into the cohort and six months later using a Food Frequency Questionnaire. Women reported their average frequency of consumption over the past 6 months for wine, beer, and liquor. Baseline assessment captured the period just before and around the time of breast cancer diagnosis (peri‐diagnosis), whereas the 6‐month assessment captured the early period after breast cancer diagnosis (post-diagnosis). Study outcomes included breast cancer recurrence, breast cancer mortality, cardiovascular disease (CVD) mortality, and all‐cause mortality. Recurrences were ascertained during follow‐up interviews at 6, 12, 24, 48, 72, and 96 months.

For peri-diagnosis consumption, compared with no consumption, occasional consumption (0.36 to <0.6 g/day) and regular consumption (≥6.0 g/day) of alcohol were not associated with any outcomes. No significant dose‐response effect for increasing consumption was observed. For alcohol drinking post-diagnosis, all associations were nonsignificant, including for all‐cause mortality, with no significant dose‐response effects observed. Across all models, the type of alcohol, including wine, beer, and liquor, was not associated with any outcome, except for beer consumed at follow‐up, which was associated with a higher risk of breast cancer mortality (HR, 1.47; 95% CI, 1.06–2.03).

Risk associations varied by BMI. Specifically, in obese women, compared with no drinking, occasional consumption of two or more drinks per week was associated with a decreased risk of overall death, contributed in part by decreased risk of CVD death. Also, occasional consumption was possibly associated with an increased risk of recurrence in nonobese women.

Comments on outcomes and methodology

This study further adds to the existing evidence that pre- or post-diagnostic alcohol consumption is not positively associated with breast cancer occurrence. Although the authors claim that this is the largest prospective cohort study of breast cancer survivors, the overall number of person-years in this study was relatively small (some 40,000). Whereas the results are consistent with previous meta-analyses, a meta-analytical approach would provide stronger results on the various interesting sub-questions addressed in this study.

One of the interesting sub-questions addressed in this study was a possible beverage specific effect. The data indicated that no such beverage specific effects exist, such that across all models the type of alcohol was not associated with any outcome, except for beer consumption at follow-up; this was associated with a considerably higher risk of breast cancer mortality. The authors do not explain how this beverage specific effect may have occurred in the analysis, since the association was only observed with beer consumption at follow-up. Possibly, the authors considered this observation of less importance since no statement was made on beverage-specific effects in their conclusions.

Another recent meta-analysis specifically on breast cancer incidence from 22 cohort studies and 45,350 breast cancer cases, showed that current drinkers had an increased risk compared with never drinkers for ER-positive cancers mainly. In a dose-response analysis, there was a statistically significant linear trend with breast cancer risk increasing gradually by total amount of alcohol and wine, but not amount of beer and spirits (Sun et al., 2020).

One possible explanation may lie in the lack of data on the pattern of alcohol consumption or even the lack of data on the change in the pattern of alcohol consumption. It may be that women drink less after their breast cancer diagnosis and concomitantly change their beverage preferences. The authors indicate, however, that the majority of women stay in the same or in the adjacent category of alcohol consumption from pre-diagnosis to early post-diagnosis exposure. It may be interesting to analyse these data in more detail, not only to describe these changes but also to investigate the effects of changes in the amount of alcohol drunk on study outcomes and to study the effects of changes in alcoholic beverage preference after breast cancer diagnosis.

Specific Comments from Forum Members

Forum member Ellison stated: “The authors have done as good a job as possible given the number of cases in their cohort but unfortunately, by having to do separate analyses for the subjects with alcohol consumption estimates pre- and post- diagnosis, there were limitations due to small numbers in some subgroups.  Further, while there were tendencies for an increase or decrease in risk associated with alcohol in some comparisons, it is noted that the continuous alcohol estimates were almost always either 1.0 (the same as that of non-drinkers) or very close to 1.0 when comparing effects of alcohol intake on outcomes.  This does not support large or meaningful health effects (either beneficial or adverse) associated with alcohol consumption in women with breast cancer.  Also, it would have been interesting to see the alcohol effects for ‘normal’ weight subjects (BMI < 25), ‘overweight’ subjects (BMI values between 25 and 30), rather than having only one BMI cut-point of 30 for assessing obesity.   

A key weakness of this study is that data were not available on the pattern of drinking, not even whether or not there was reported binge drinking. Also, the characterization of being an ‘occasional’ or ‘regular’ drinker based only on the average amount of alcohol reported is not considered a useful separation of subjects; the amount consumed per occasion (which may be important for a relation with cancer) cannot be assessed with such a classification.  It is stated that there was skewness in the upper group, and it would have been helpful to know the effects of regular moderate versus regular heavy drinkers. Most previous studies indicate that regular (even daily) moderate alcohol consumption, especially when consumed with food, is associated with the healthiest outcomes (Tricholpoulou et al., 2009, Hellmann et al., 2010, Barberia-Latasa et al., 2022)”

Forum member Mattivi adds that “it would have been interesting to validate the consumption deduced from the food frequency questionnaire with biomarkers by collecting non-invasive biofluid samples (e.g. urine), especially to identify possible misclassifications due to unreported consumption.”

Forum member de Gaetano considers: “This study supports the importance of including all-cause mortality as an outcome in alcohol consumption studies. When I read that alcohol is a risk for cancer, I would always read at the same time data on all-cause mortality. As an example, in post-menopausal, likely overweight or obese women, the risk of cardiovascular morbidity/mortality is high, which is different from the relative low risk of pre-menopausal, normal weight women. Thus, I am not surprised that in this paper moderate alcohol consumption is reducing total mortality in obese but not in non-obese women.”

Forum member Skovenborg follows on that “the Pathways Study have assessed alcohol consumption at baseline (on average 2.3 months postdiagnosis) and at 6-month follow-up (on average 8.4 months postdiagnosis.) Little is known about whether survivors of breast cancer do make more health behaviour changes than other women. To my knowledge, only two prospective studies have addressed changes in the post-diagnosis alcohol consumption of breast cancer survivors. The study from Norway (Skeie et al., 2009) found no differences in change of alcohol consumption or BMI in breast cancer survivors before and after breast cancer diagnosis. In the study from Denmark (Bidstrup et al., 2013.), women with breast cancer did not reduce their BMI, or modify their alcohol use compared with cancer-free women. Both studies found a small increase in alcohol consumption in both groups of women and the results suggest that the pre-diagnosis alcohol consumption of the breast cancer survivors in the Pathways Study might be similar to their post-diagnosis consumption. Neither study had information about the drinking pattern.

According to Jones (2019), ethanol distributes into the total body water (TBW) compartment, which represents between 50 and 60% of body weight or 43–51 L for a person weighing 85 kg. Women are generally smaller than men, are shorter and have lower body weight, as well as more fatty tissue. For a water-soluble drug like ethanol, its distribution volume (Vd) is influenced by a person’s age and gender, with lower values observed in women and in elderly men. Table #3 makes a comparison of ethanol Vd determined for healthy male and female subjects in controlled drinking experiments.

The average Vd was 0.69 L/kg for men compared with 0.60 L/kg for women, which suggests that after drinking the same dose/kg of ethanol females achieve a roughly 15% higher peak BAC than males. The Vd in obese people suggests that after drinking the same dose/kg of ethanol obese people will achieve a higher peak BAC than non-obese people. As a result, the same dose of alcohol per kg bodyweight and the higher peak BAC would be expected to increase the adverse health effects of alcohol and not decrease the effects as the authors write. According to Maudens et al. (2014), the Vd of ethanol varied between 0.40 and 0.68 L/kg for women, and between 0.43 and 0.73 L/kg for men. For both sexes, the Vd decreased with increasing BMI with an increasing peak BAC as result of a similar alcohol dose (g alcohol/kg) in obese women”.

Forum member Lanzmann-Petithory further explained that “many of the studies of the Danish Centre for Alcohol Research (e.g., Petri et al., 2006, Hellmann et al., 2010) suggested that there was a difference in risk of breast cancer before and after menopause with alcohol consumption. After menopause, the risk of breast cancer increased with the first glass of wine, whereas before menopause, it was 2 or 3 glasses of wine. This could potentially be due to the estrogen-like polyphenol stilbenoids found in wine that may increase levels of estrogen and other hormones associated with hormone-receptor-positive breast cancer. In France, Bougnoux et al. (2005) carried out a number of studies on the role of the omega-6 to omega-3 ratio in the risk of breast cancer recurrence, in particular the protective role of omega-3 alpha-linolenic acid and DHA (Liu & Ma, 2014)”. [Other polyphenol components of wine, however, may stimulate the synthesis of EPA and DHA from the precursor alpha-linolenic acid to prevent the ethanol-induced oxidation of long chain fatty acids, thus delaying their breakdown, and potentially reducing the risk of breast cancer (Di Giuseppe et al., 2009)]; “further research has been published on this subject quite recently.”

In addition, Forum member Boban shared that “the most recent systematic review observed no association between wine consumption specifically and breast/gynaecological cancers (Lucerón-Lucas-Torres et al. 2023)”, while Forum member Waterhouse reminds that “we have another demonstration that alcohol reduces cardiovascular disease mortality, and Rimm et al. (1998) published another study showing a strong interaction between folate and alcohol consumption” allied to a reduced risk of cardiovascular disease. Furthermore, Baglietto et al. (2005) subsequently suggested that women who had high alcohol consumption and low intake of folate had an increased risk of breast cancer, but those women who had high alcohol consumption and moderate to high levels of folate intake had no increased risk.

Concluding comments

As previously mentioned, practicing certain healthy behaviours such as a healthy diet, physical activity, maintaining optimal weight, and avoiding excessive alcohol consumption and total tobacco use, is known to improve quality of life and/or be associated with survival among individuals diagnosed with early-stage cancer (Hanna et al., 2013, Palesh et al., 2014, LoConte et al., 2018, Scott et al., 2018, Campbell et al., 2019, Boyd et al., 2020). An evidence gap is that despite this knowledge, it is not clear whether individuals living with advanced or metastatic cancer receive the same benefits from these healthy behaviours (Mollica, 2022). In addition, there is a lack of evidence regarding the effectiveness of existing recommendations for healthy behaviours such as physical exercise, alcohol consumption and weight management for individuals living with advanced or metastatic cancer (Piercy et al., 2018). An overall goal of further research would be to determine the optimal type, amount, and frequency of positive health behaviours including alcohol consumption necessary to maintain or improve health outcomes for these populations; determine their acceptability and feasibility for patients; and determine how health-care providers and health systems can support healthy behaviours throughout the care trajectory.

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Comments on this critique by the International Scientific Forum on Alcohol Research were provided by the following members:

Henk Hendriks, PhD, Netherlands

Creina Stockley, PhD, MBA, Independent consultant and Adjunct Senior Lecturer in the School of Agriculture, Food and Wine at the University of Adelaide, Australia

R Curtis Ellison, MD, Section of Preventive Medicine/Epidemiology, Boston University School of Medicine, Boston, MA, USA

Giovanni de Gaetano, MD, PhD, Department of Epidemiology and Prevention, IRCCS Istituto Neurologico Mediterraneo NEUROMED, Pozzilli, Italy

Fulvio Ursini, MD, Dept. of Biological Chemistry, University of Padova, Padova, Italy

Erik Skovenborg, MD, specialized in family medicine, member of the Scandinavian Medical Alcohol Board, Aarhus, Denmark

Dominique Lanzmann-Petithory, MD, PhD, Nutrition/Cardiology, Praticien Hospitalier Hôpital Emile Roux, Paris, France

Harvey Finkel, MD, Hematology/Oncology, Retired (Formerly, Clinical Professor of Medicine, Boston University Medical Center, Boston, MA, USA)

Mladen Boban, MD, PhD, Professor and Head of the Department of Pharmacology, University of Split School of Medicine, Croatia

Ramon Estruch, MD, PhD.  Associate Professor of Medicine, University of Barcelona, Spain

Pierre-Louis Teissedre, PhD, Faculty of Oenology–ISVV, University Victor Segalen Bordeaux 2, Bordeaux, France

Andrzej Pająk, MD, PhD, Professor Epidemiology and Population Studies, Jagiellonian University Medical College, Kraków, Poland

Andrew L. Waterhouse, PhD, Department of Viticulture and Enology, University of California, Davis

Luc Djoussé, MD, DSc, Dept. of Medicine, Division of Aging, Brigham & Women’s Hospital and Harvard Medical School, Boston, MA, USA

Fulvio Mattivi, MSc, Head of the Department Food Quality and Nutrition, Research and Innovation Centre, Fondazione Edmund Mach, in San Michele all’Adige, Italy