Abstract
Background:
Three prospective studies have evaluated the association between dietary acrylamide intake and endometrial cancer (EC) risk with inconsistent results. The objective of this study was to evaluate the association between acrylamide intake and EC risk: for overall EC, for type-I EC, and in never smokers and never users of oral contraceptives (OCs). Smoking is a source of acrylamide, and OC use is a protective factor for EC risk.
Methods:
Cox regression was used to estimate hazard ratios (HRs) for the association between acrylamide intake and EC risk in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. Acrylamide intake was estimated from the EU acrylamide monitoring database, which was matched with EPIC questionnaire-based food consumption data. Acrylamide intake was energy adjusted using the residual method.
Results:
No associations were observed between acrylamide intake and overall EC (n=1382) or type-I EC risk (n=627). We observed increasing relative risks for type-I EC with increasing acrylamide intake among women who both never smoked and were non-users of OCs (HRQ5vsQ1: 1.97, 95% CI: 1.08–3.62; likelihood ratio test (LRT) P-value: 0.01, n=203).
Conclusions:
Dietary intake of acrylamide was not associated with overall or type-I EC risk; however, positive associations with type I were observed in women who were both non-users of OCs and never smokers.
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Main
Acrylamide is a known neurotoxin in humans, and a carcinogen in animals (Friedman, 2003; LoPachin and Gavin, 2008; Hogervorst et al, 2010). In 1994, based on animals studies, as well as evidence found in humans, the International Agency for Research on Cancer (IARC) classified acrylamide as ‘probably carcinogenic’ to humans (IARC group 2A; IARC, 1994). In 2002, Swedish researchers discovered acrylamide in some heat-treated carbohydrate-rich foods (Tareke et al, 2002), and further research concluded that acrylamide is formed during common cooking procedures (predominantly through the Maillard reaction), such as frying, grilling, and baking (Friedman, 2003). In the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort, the main determinants of estimated dietary intake of acrylamide based on 24-h dietary recall (DR) were bread, crisp bread, rusks, coffee, fried potatoes, cakes, biscuits, and cookies (Freisling et al, 2013). Acrylamide is also a component of cigarette smoke, thus, smoking is an important source of exposure (Boettcher et al, 2005; Vesper et al, 2008).
Acrylamide is metabolised via the Cyp2e1 enzyme system to glycidamide, a chemically reactive epoxide and mutagen in animals (Doroshyenko et al, 2009; Hogervorst et al, 2010). After acrylamide administration, hormone-related (including uterine tumours) and other tumours (e.g., oral tissues) have been observed in rats (Johnson et al, 1986).
Endometrial cancer (EC) is the fourth most common cancer diagnosed in European women, but mortality is relatively low with a 5-year survival rate varying from 65 to 85% (Cook et al, 2006; Ferlay et al, 2013). There is considerable international variation in incidence as well as mortality, and both rates increase dramatically with age (Cook et al, 2006; Ferlay et al, 2013; Jamison et al, 2013). Established risks factors for EC are obesity, low physical activity, history of polycystic ovary syndrome, and greater lifetime exposure to estrogens (Kaaks et al, 2002; Cook et al, 2006). The use of oral contraceptives (OCs, containing both oestrogen and progestin in the formula) is well established to lower the risk of develo** EC (Cook et al, 2006; Gierisch et al, 2013). There is evidence that tobacco smoking also reduces the risk of EC (Terry et al, 2004; Cook et al, 2006); however, an EPIC study reported an increased risk of EC in premenopausal women who smoked (Al-Zoughool et al, 2007). Endometrial cancer is generally classified into two types: type-I EC are mostly endometrioid adenocarcinomas and are associated with unopposed oestrogen exposure; and type-II EC tumours are mainly serous carcinomas, are believed to be oestrogen independent, and have poor prognosis (Amant et al, 2005; Table 4). Otherwise, associations between dietary acrylamide intake and type-I EC were below the null value in ever smokers (current and former smokers) and OC users (HR10 μg per day: 0.75, 95% CI: 0.60–0.94; Table 4). The LRT P-value of the contrast between ‘never smokers/non-OC users’, ‘ever smokers/non-OC users’, ‘never smokers/OC users’, and ‘ever smokers/OC users’ for the continuous acrylamide intake variable was 0.01 (Table 4).
Other effect-measure modifications in type-I EC
There was no evidence for effect-measure modification by BMI (Table 4), HRT use, or by geographical region (all LRT P-values >0.12, data not shown); however, evidence for effect-measure modification was found when the analyses were stratified by baseline menopausal status (LRT P-value: 0.01; Table 4), but none of the individual HRs were statistically significant. Likewise, effect-measure modification was observed by alcohol intake (LRT P-value: 0.01), but only the continuous variable in never drinkers showed a statistically significant positive association (HR10 μg per day: 1.23, 95% CI: 1.02–1.47; Table 4).
Discussion
No overall association was observed between dietary intake of acrylamide and overall EC or type-I EC risk; nevertheless, elevated relative risks, as well as P-values for linear trend were observed for the association between dietary intake of acrylamide and type-I EC among women who both never smoked and never used OCs. Statistically significant inverse associations between type-I EC risk and acrylamide intake were observed in OC users, and among OC users and ever smokers.
It is widely published that use of OCs (containing oestrogen and progestin) is protective against EC risk, and this effect is maintained for years (Amant et al, 2005; Cook et al, 2006; Cibula et al, 2010; Gierisch et al, 2013). Likewise, cigarette smoking tends to lower the risk of develo** EC, and it is thought to be more pronounced in recent smokers (Cook et al, 2006). All the relative risk estimates for type-I EC risk observed among OC users and ever smokers were below the null value; however, because OC use, duration of OC use, and smoking are associated with higher acrylamide intake in EPIC, and are also associated with lower EC risk, residual confounding by these variables may play a role in the observed inverse associations (in OC users and smokers). In addition, OC users, compared to non-OC users, tended to smoke more cigarettes per day and reported less time since having quit smoking. Thus, these baseline characteristics may have partially influenced the results obtained in this subgroup of women. Moreover, it has been hypothesised that acrylamide may have hormonal effects, and the results in non-OC users for type I are potentially compatible with this hypothesis, since type-I EC is considered to be oestrogen driven (Amant et al, 2005); nevertheless, this hypothesis has not been substantiated, and other mechanisms (i.e., genotoxicity caused by glycidamide) may be compatible with the results (Hogervorst et al, 2010, 2013).
The relation between dietary intake of acrylamide and EC risk has been previously published in three prospective cohort studies. Both the NLCS and NHS studies found statistically significantly increased relative risks: the NLCS among never-smoking women, and the NHS in the entire cohort (Hogervorst et al, 2007; Wilson et al, 2010). Although the NLCS and NHS studies did not evaluate the association between acrylamide intake and type-I EC specifically, about 80% of EC cases are thought to be type-I endometrioid tumours (Amant et al, 2005); thus, the majority of the cases in the previous publications were likely type-I EC cases. Only the SMC study observed no associations between acrylamide intake and EC risk (Larsson et al, 2009), and this could be due to the smaller baseline ranges of acrylamide intake in that study. The median acrylamide intake for the reference group in the SMC was 16.9 μg per day, and for the highest intake category was 32.5 μg per day, whereas in EPIC, the median for the reference group was 9.3 μg per day, and for the highest intake category was 44.0 μg per day. All three previous studies presented statistical models adjusted for OC use, but none reported analyses stratified by OC use.
Some evidence for an inverse association between the highest and lowest acrylamide quintiles and type-I EC risk was observed among women with a BMI <25 kg m−2; however, neither the continuous variable for acrylamide intake (per 10 μg per day) nor the LRT P-value were statistically significant. A suggestive increased risk for type-I EC was observed in women who reported never drinking alcohol at baseline when the continuous acrylamide variable was evaluated; nevertheless, this result was based on 103 type-I EC cases. Further, suggestive evidence for heterogeneity of the association between dietary acrylamide intake and type-I EC risk was also indicated by smoking status, and by menopausal status at baseline; nevertheless no dose-response trend was observed.
The strengths of our study are that EPIC is one of the largest prospective cohort studies on diet and cancer, and recall bias is unlikely because exposure and diet information were collected years before cancer diagnoses. The present study had more cases than the other three previously published studies (n=1382), and this allowed us to evaluate known type-I EC separately (n=627). The SMC study analysed 687 EC cases (Larsson et al, 2009), the NHS study analysed 484 EC cases (Wilson et al, 2010), and the NLCS study evaluated 221 (Hogervorst et al, 2007).
The present study had the following limitations: some food preparation techniques (e.g., cooking method) that could have contributed to the variability of total acrylamide intake were not assessed in all EPIC centres. In addition, the correlation coefficient between a single 24-h DR in EPIC, and acrylamide intake derived from food intake questionnaires was low: 0.17 (Ferrari et al, 2013). This could indicate that a single 24-h DR may not be enough to accurately estimate the average acrylamide intake. Further, the EPIC acrylamide estimates might have been influenced by measurement error; however, all the analyses were adjusted for energy intake since in EPIC and in other populations, it has been observed that the validity of acrylamide estimates improved after energy intake adjustment (Ferrari et al, 2013). Another limitation of our study is that 718 EC cases were not classified in any of the EC subtypes; however, as has been previously mentioned, a large proportion (≈80%) of endometrial carcinomas are thought to be type I (Amant et al, 2005). Finally, it should to be kept in mind that several subgroups have been examined in this study; thus, some of the observed results might be due to chance.
In conclusion, the results of the present study indicate that there were no associations between dietary intake of acrylamide and risk of overall EC or type-I EC; nevertheless, women with elevated acrylamide intake (upper quintile median, 44 μg per day) who both never smoked and never used OCs at baseline, were at higher risk of develo** type-I EC relative to women with the lowest intakes. Additional studies with biomarkers of internal dose of acrylamide exposure are needed in order to better understand the associations observed.
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Acknowledgements
The author’s responsibilities were as follows: ER, RK, NS, LL-B, HF, PF, LD, NC-B, LB, RTF, HB, A Tjønneland, AO, VM, EM-M, NL, M-DC, EA, K-TK, NW, RCT, YL, MAM, A Trichopoulou, VB, DT, CS, SS, RT, CS, RG, HBB-d-M, E Wirfält, UE, AI, NO, GS, ITG, E Weiderpass, and NCO-M: designed and conducted the multicenter EPIC cohort study. NS, EJD, RK, and MO-S: conducted the research. MO-S: analysed the data. MO-S and EJD: wrote the manuscript. MO-S and EJD: had primary responsibility for the final content. MO-S is affiliated with the University of Barcelona. All authors read and approved the final version of the manuscript. This work was partially supported by the Wereld Kanker Onderzoek Fonds (WCRF NL) (grant WCRF 2011/442) and by the Health Research Fund (FIS) of the Spanish Ministry of Health (Exp PI11/01473). The coordination of EPIC is financially supported by the European Commission (DG-SANCO) and the International Agency for Research on Cancer. The national cohorts are supported by the Health Research Fund (FIS) of the Spanish Ministry of Health, Regional Governments of Andalucía, Asturias, Basque Country, Murcia (no. 6236), Navarra and the Catalan Institute of Oncology, La Caixa (BM 06-130), Red Temática de Investigación Cooperativa en Cáncer (RD12/0036/0018; RD06/0020/0091) (Spain); Danish Cancer Society (Denmark); Ligue contre le Cancer, Institut Gustave Roussy, Mutuelle Générale de l’Education Nationale, Institut National de la Santé et de la Recherche Médicale (INSERM, France); Deutsche Krebshilfe, Deutsches Krebsforschungszentrum (DKFZ) and Federal Ministry of Education and Research (Germany); the Hellenic Health Foundation (Greece); Associazione Italiana per la Ricerca sul Cancro (AIRC) and National Research Council (Italy); Dutch Ministry of Public Health, Welfare and Sports (VWS), Netherlands Cancer Registry (NKR), LK Research Funds, Dutch Prevention Funds, Dutch ZON (Zorg Onderzoek Nederland), World Cancer Research Fund (WCRF) and Statistics Netherlands (The Netherlands); Nordic Center of Excellence in Food, Nutrition and Health-Helga (Norway); Swedish Cancer Society, Swedish Scientific Council and Regional Government of Skåne and Västerbotten (Sweden); Cancer Research UK, Medical Research Council (United Kingdom).
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Obón-Santacana, M., Kaaks, R., Slimani, N. et al. Dietary intake of acrylamide and endometrial cancer risk in the European Prospective Investigation into Cancer and Nutrition cohort. Br J Cancer 111, 987–997 (2014). https://doi.org/10.1038/bjc.2014.328
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