Annals of Oncology Advance Access originally published online on October 3, 2006
Annals of Oncology 2007 18(1):36-39; doi:10.1093/annonc/mdl328
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© 2006 European Society for Medical Oncology
epidemiology |
Fried foods, olive oil and colorectal cancer
1 Istituto di Ricerche Farmacologiche ‘Mario Negri’, Milan
2 Servizio di Epidemiologia e Biostatistica, Centro di Riferimento Oncologico, Aviano, Pordenone, Italy
3 Unité d'épidémiologie du cancer, Institut universitarie de médicine sociale et préventive, Lausanne, Switzerland
4 Policlinico di Monza, Via Amati, Monza, Milan
5 Servizio di Epidemiologia, Istituto Tumori ‘Fondazione Pascale’, Naples, Italy
6 International Agency for Research on Cancer, Lyon, France
7 Istituto di Statistica Medica e Biometria, Università degli Studi di Milano, Italy
* Correspondence to: Dr C. Galeone, Istituto di Ricerche Farmacologiche "Mario Negri", Via Eritrea 62, 20157 Milan, Italy. Tel: +39-02-39014-577; Fax: +39-02-33200-231; E-mail: galeone{at}marionegri.it
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Abstract |
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 Top Abstract introductionpatients and methodsresultsdiscussionAcknowledgementsReferences |
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Background: The epidemiologic evidence for an etiologic role of fried foods and heterocyclic amines in colorectal carcinogenesis is inconsistent.
Patients and methods: We have investigated the relation between fried foods and colorectal cancer risk using data from a large, multicentric case–control study conducted in Italy and Switzerland between 1992 and 2000, with 1394 cases of colon cancer, 886 cases of rectal cancer and 4765 controls.
Results: After allowing for major relevant covariates, the multivariate odds ratios (ORs) for an increment of one portion per week of fried foods were 0.97 [95% confidence interval (CI) = 0.93–1.01] for colon cancer and 1.04 (95% CI = 1.00–1.09) for rectal cancer. When we analyzed the type of fats mainly used for frying, we found that olive oil, but not other types of oils, appeared to protect from colon cancer risk (OR = 0.89, 95% CI = 0.82–0.98).
Conclusions: Our results do not indicate a relevant role of fried foods on colorectal cancer risk. We found a possible favorable effect of (fried) olive oil on colon cancer risk but not on rectal cancer risk.
Key words: acrylamide, case–control study, colorectal cancer, fried foods, heterocyclic amines, olive oil
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introduction |
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TopAbstractintroductionpatients and methodsresultsdiscussionAcknowledgementsReferences |
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Heterocyclic amines (HCAs), compounds formed in the cooking of certain foods, especially during the frying of protein-rich food such as meat, eggs and fish, have been shown to be bacterial mutagens and animal carcinogens [1]. In rats, these amines induce cancer specifically in organs such as breast, colon or pancreas, which are associated with Western-type diet [2]. Further, fried potatoes are an important dietary source of acrylamide, a substance that the International Agency for Research on Cancer classified in 1994 as ‘probably carcinogenic to humans’ (Group 2A), on the basis of sufficient evidence for carcinogenicity in experimental animals and mechanistic considerations [3].
It is therefore important to investigate whether fried foods are related to digestive tract cancers in humans, but the epidemiologic evidence for an etiologic role of fried foods and HCAs in colorectal carcinogenesis is inconsistent [4], whereas there is no evidence of a role of acrylamide from dietary sources [5, 6]. A Swedish case–control study found no association between total HCAs intake and colorectal cancer risk [7] and other studies found no relation between fried meat and colorectal cancer [8–11]. However, an American case–control study found a positive association between pan-fried red meat intake [odds ratio (OR) = 2.0, for the highest level of intake] and colon cancer risk [12], and other epidemiological studies found a direct relation with colorectal adenomas and cancer [13, 14]. In a cohort study on Swedish women, including 741 cases of colorectal cancer [15], there was no association between estimates of acrylamide intake and colorectal cancer. The OR was 0.90 for the highest quintile of intake [95% confidence interval (CI) = 0.6–1.4].
We have therefore investigated the possible relation between fried foods and colorectal cancer risk using data from a large, multicentric case–control study.
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patients and methods |
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TopAbstractintroductionpatients and methodsresultsdiscussionAcknowledgementsReferences |
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Data were derived from a multicentric case–control study of colorectal cancer conducted in Italy and Switzerland between 1992 and 2000. The study included 1394 cases of colon cancer (median age 62 years), 1225 from Italy and 169 from Switzerland; 886 cases of rectal cancer (median age 63 years), 728 from Italy and 158 from Switzerland and 4765 controls, 4154 from Italy and 611 from Switzerland (median age 58 years) [16, 17]. All cancer cases were incident and histologically confirmed. Controls were patients admitted to the same hospitals for acute, non-neoplastic conditions unrelated to digestive tract diseases (22% had non-alcohol-related traumas, mostly fractures and sprains; 28% non-traumatic orthopedic disorders; 24% acute surgical conditions and 26% miscellaneous other illnesses such as eye, ear or skin diseases). Trained interviewers questioned cases and controls during their hospital stay; the proportion of refusals was <5% for both cases and controls in all Italian centers and about 15% in Switzerland. The design was the same for the Italian and Swiss studies. Information was collected on sociodemographic factors, anthropometric variables, smoking, alcohol and other lifestyle habits, a problem-oriented medical history, physical activity and history of cancer in relatives. Information on diet referred to the previous 2 years and was based on a validated and reproducible food frequency questionnaire (FFQ) [18, 19] comprising 78 foods, food groups or recipes, and allowing the estimation of total energy intake. The FFQ was divided into six sections: (i) bread, cereals, first courses; (ii) second courses (i.e. meat, fish and other main dishes); (iii) side dishes (i.e. vegetables, fried/baked potatoes); (iv) fruits; (v) sweets, desserts and soft drinks and (vi) milk, hot beverages and sweeteners. At the end of each section, one or two open questions were used to include foods that were not in the questionnaire, but were eaten at least once per week. There were a few differences in the dietary items listed in the Italian and Swiss versions of the questionnaire, to account for different eating and drinking patterns, but these differences did not concern the fried food items and types of fat used to fry. Among the items in the FFQ, some questions referred specifically to consumption of fried foods, such as beef, fish, eggs and omelets and potatoes. The weekly frequency of consumption of fried foods, as well as their usual portion size, was investigated. An additional question aimed at assessing the type of fat used to fry (i.e. olive oil; specific-seed oils such as sunflowers, maize, peanut and soya; mixed-seed oils and butter and margarine) was included.
data analysis
ORs and the corresponding 95% CIs were derived from unconditional multiple logistic regression models, including terms for age, study center, sex, education (<7, 7 to <12 and 
12 years), body mass index (in quartiles), tobacco smoking (never, ex, current smokers of <15, 15 to <25 and 25 cigarettes per day), alcohol drinking (
1, >1 to 3 and >3 glasses per day, plus a term for non-drinkers and ex-drinkers), non-alcohol energy intake (in quintiles), family history of colorectal cancer, physical activity and red meat intake.
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results |
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Table 1 reports the ORs of colorectal cancer according to levels of intake of various fried foods and, separately for colon and rectum, of total fried foods, after adjustment for several potential confounding factors. The ORs of colorectal cancer for the highest level of intake (
1 portion per week) were 0.93 (95% CI = 0.79–1.07) for fried beef, 0.87 (95% CI = 0.75–1.01) for fried fish, 0.98 (95% CI = 0.86–1.11) for fried eggs and 0.95 (95% CI = 0.83–1.08) for fried/baked potatoes. Corresponding values for total fried foods were 0.83 (95% CI = 0.70–0.98) for colon, 0.91 (95% CI = 0.74–1.12) for rectum and 0.86 (95% CI = 0.74–0.98) for colorectum. When we restricted the analysis to the Italian data set, the OR for colorectal cancer for the highest tertile of total fried food intake was 0.84 (95% CI = 0.72–0.97), whereas in the Swiss data set the corresponding value was 1.22 (95% CI = 0.75–3.05). The ORs were borderline heterogeneous across strata of country (P = 0.047). The ORs for an increment of one portion of fried foods per week were 0.97 (95% CI = 0.93–1.01) for colon cancer, 1.04 (95% CI = 1.00–1.09) for rectal cancer and 1.00 (95% CI = 0.97–1.03) for both cancers together.
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Table 2 gives the continuous ORs for colon, rectal and colorectal cancers according to the type of oil mainly used for frying. The ORs for an increment of one portion of fried foods per week for colon, rectal and both cancers together were, respectively, 0.89 (95% CI = 0.82–0.98), 0.97 and 0.93 for use of olive oil; 1.00, 1.06 and 1.02 for specific-seed oils and 0.98, 1.03 and 1.00 for mixed-seed oils used.
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discussion |
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TopAbstractintroductionpatients and methodsresultsdiscussionAcknowledgementsReferences |
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Our results do not indicate a relevant role of fried foods on colorectal cancer risk. These inconsistent findings may be explained by a relatively moderate consumption of fried foods in Italy (median value in our study: 1.8 portions per week) and/or by the large intake of vegetables, fruits and fiber-containing foods, typical of Mediterranean populations, which could be responsible for their comparably lower incidence of colorectal cancer. When we evaluated the fat used for frying, we found that olive oil, but not other types of oils, appeared to protect from colon cancer, confirming its possible favorable effect on colorectal and other cancers [20–24]. However, previous studies considered the overall dietary consumption of olive and other oils, whereas this investigation provided indications that fried olive oil may also reduce the risk for colon cancer.
The favorable effect of olive oil has been proposed on the basis of animal experiments and of its fatty acid composition (mainly oleic acid, a monounsaturated fatty acid) or of the content of specific micronutrients and antioxidants (including vitamin E) [20, 25]. Further, previous studies found that the formation of HCAs during cooking is decreased by the addition of pure antioxidants or food containing antioxidants [26, 27]. As in our population >24% of the subjects interviewed declared they used olive oil for frying, this may be another interpretation for the null relation found between fried foods and colorectal cancer. This was further supported by the higher risks observed in the Swiss than in the Italian data set, as use of olive oil for frying was uncommon (3%) in Switzerland as compared with 27% in Italy. The behavior of virgin olive oil, that presents a lower degree of unsaturation than vegetable shortening [28] during repeated frying operations, indicates that this oil is more stable in comparison with other vegetable oils and also for this reason the use of olive oil is suggested for deep-frying [29, 30].
In order to reduce potential information bias, in this study the questionnaire was administered by the same interviewers, under similar conditions, to both cases and controls, and controls were selected among patients with admission diagnoses not related to diet modifications. Bias in the recall of consumption of fried foods should be limited in this population, also given the satisfactory validity and reproducibility of the FFQ [18, 19] and the comparability between cases and controls in hospital-based settings [31]. Findings from companion case–control studies of the upper aero-digestive tract, where a positive association with fried foods was observed [32, 33], provide indirect evidence that the absence of association appears to be real, since both the upper and lower digestive tract cancer studies were conducted on similar populations and using similar study designs.
Other main strengths of this case–control study are its large size and the low percentage of refusals of the subjects contacted. With reference to confounding, the findings were consistent after inclusion in the regression models of several lifestyle and dietary covariates such as physical activity, energy, fruit and vegetable intake and red meat intake.
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Acknowledgements |
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This work was conducted with the contribution of the Italian Association for Cancer Research, the Italian and Swiss Leagues against Cancer the Swiss Research against Cancer/Oncosuisse (KFS 700 and OCS-1633). The authors thank Mrs C. Pasche and F. Lucchini for Swiss data collection and validation and Mrs I. Garimoldi for editorial assistance.
Received for publication May 9, 2006. Revision received July 24, 2006. Accepted for publication August 8, 2006.
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References |
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1. Pfau W and Marquardt H. (2001) Cell transformation in vitro by food-derived heterocyclic amines Trp-P-1, Trp-P-2 and N(2)-OH-PhIP. Toxicology 166:25–30.[CrossRef][ISI][Medline]
2. Weisburger JH and Jones RC. (1990) Prevention of formation of important mutagens/carcinogens in the human food chain. Basic Life Sci 52:105–118.[Medline]
3. International Agency for Research on Cancer. (1994) Monographs on the Evaluation of Carcinogenic Risks to Humans. Volume 60. Some Industrial Chemicals(IARC, Lyon, France).
4. International Agency for Research on Cancer. (1993) Monographs on the Evaluation of Carcinogenic Risks to Humans. Volume 56. Some Naturally Occurring Substances: Food Items and Constituents, Heterocyclic Aromatics Amines and Mycotoxins(IARC, Lyon, France).
5. Mucci LA, Dickman PW, Steineck G, et al. (2003) Dietary acrylamide and cancer of the large bowel, kidney, and bladder: absence of an association in a population-based study in Sweden. Br J Cancer 88:84–89.[CrossRef][ISI][Medline]
6. Pelucchi C, Galeone C, Levi F, et al. (2006) Dietary acrylamide and human cancer. Int J Cancer 118:467–471.[CrossRef][ISI][Medline]
7. Augustsson K, Skog K, Jagerstad M, et al. (1999) Dietary heterocyclic amines and cancer of the colon, rectum, bladder, and kidney: a population-based study. Lancet 353:703–707.[CrossRef][ISI][Medline]
8. Lyon JL and Mahoney AW. (1988) Fried foods and the risk of colon cancer. Am J Epidemiol 1128:1000–1006.
9. Gerhardsson de Verdier M, Hagman U, Peters RK. (1991) Meat, cooking methods and colorectal cancer: a case-referent study in Stockholm. Int J Cancer 49:520–525.[ISI][Medline]
10. Knekt P, Steineck G, Jarvinen R, et al. (1994) Intake of fried meat and risk of cancer: a follow-up study in Finland. Int J Cancer 59:756–760.[ISI][Medline]
11. Pietinen P, Malila N, Virtanen M, et al. (1999) Diet and risk of colorectal cancer in a cohort of Finnish men. Cancer Causes Control 10:387–396.[CrossRef][ISI][Medline]
12. Butler LM, Sinha R, Millikan RC, et al. (2003) Heterocyclic amines, meat intake, and association with colon cancer in a population-based study. Am J Epidemiol 157:434–445.
13. Sinha R, Kulldorff M, Chow WH, et al. (2001) Dietary intake of heterocyclic amines, meat-derived mutagenic activity, and risk of colorectal adenomas. Cancer Epidemiol Biomarkers Prev 10:559–562.
14. Navarro A, Munoz SE, Lantieri MJ, et al. (2004) Meat cooking habits and risk of colorectal cancer in Cordoba, Argentina. Nutrition 20:873–877.[CrossRef][ISI][Medline]
15. Mucci LA, Adami HO, Wolk A. (2006) Prospective study of dietary acrylamide and risk of colorectal cancer among women. Int J Cancer 118:169–173.[CrossRef][ISI][Medline]
16. Franceschi S, La Vecchia C, Russo A, et al. (1998) Macronutrient intake and risk of colorectal cancer in Italy. Int J Cancer 76:321–324.[CrossRef][ISI][Medline]
17. Levi F, Pasche C, La Vecchia C, et al. (1999) Food groups and colorectal cancer risk. Br J Cancer 79:1283–1287.[CrossRef][ISI][Medline]
18. Franceschi S, Barbone F, Negri E, et al. (1993) Reproducibility of an Italian food frequency questionnaire for cancer studies: results for specific food items. Eur J Cancer 29:2298–2305.
19. Decarli A, Franceschi S, Ferraroni M, et al. (1996) Validation of a food-frequency questionnaire to assess dietary intakes in cancer studies in Italy. Results for specific nutrients. Ann Epidemiol 6:110–118.[CrossRef][ISI][Medline]
20. Braga C, La Vecchia C, Franceschi S, et al. (1998) Olive oil, other seasoning fats, and the risk of colorectal carcinoma. Cancer 82:448–453.[CrossRef][ISI][Medline]
21. Lipworth L, Martinez ME, Angell J, et al. (1997) Olive oil and human cancer: an assessment of the evidence. Prev Med 26:181–190.[CrossRef][ISI][Medline]
22. Bosetti C, La Vecchia C, Talamini R, et al. (2000) Food groups and risk of squamous cell esophageal cancer in northern Italy. Int J Cancer 87:289–294.[CrossRef][ISI][Medline]
23. Franceschi S, Favero A, Conti E, et al. (1999) Food groups, oils and butter, and cancer of the oral cavity and pharynx. Br J Cancer 80:614–620.[CrossRef][ISI][Medline]
24. Bosetti C, La Vecchia C, Talamini R, et al. (2002) Food groups and laryngeal cancer risk: a case-control study from Italy and Switzerland. Int J Cancer 100:355–360.[CrossRef][ISI][Medline]
25. Giacosa A. (2004) The Mediterranean diet and its protective role against cancer. Eur J Cancer Prev 13:155–157.[CrossRef][ISI][Medline]
26. Purcaro G, Navas JA, Guardiola F, et al. (2006) Polycyclic aromatic hydrocarbons in frying oils and snacks. J Food Prot 69:199–204.[ISI][Medline]
27. Weisburger JH. (1999) Antimutagens, anticarcinogens, and effective worldwide cancer prevention. J Environ Pathol Toxicol Oncol 18:85–93.[Medline]
28. Andrikopoulos NK, Kalogeropoulos K, Falirea A, Barbagianni N. (2002) Performance of virgin olive oil and vegetable shortening during deep-frying and pan-frying of potatoes. Int J Food Sci Technol 37:177–190.
29. Fedeli E. (1988) The behaviour of olive oil during cooking and frying. In Varela G, Bender AE, Morton IA (Eds.). Frying of Food: Principles, Changes, New Approaches(Ellis Horwood, Chichester, UK) pp. 52–81.
30. Quiles JL, Huertas JR, Battino M, et al. (2002) The intake of fried virgin olive or sunflower oils differentially induces oxidative stress in rat liver microsomes. Br J Nutr 88:57–65.[ISI][Medline]
31. D'Avanzo B, La Vecchia C, Katsouyanni K, et al. (1997) An assessment, and reproducibility of food frequency data provided by hospital controls. Eur J Cancer Prev 6:288–293.[CrossRef][ISI][Medline]
32. Bosetti C, Talamini R, Levi F, et al. (2002) Fried foods: a risk factor for laryngeal cancer? Br J Cancer 87:1230–1233.[CrossRef][ISI][Medline]
33. Galeone C, Pelucchi C, Talamini R, et al. (2005) Role of fried foods and oral/pharyngeal and oesophageal cancers. Br J Cancer 92:2065–2069.[CrossRef][ISI][Medline]
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