Fruit and vegetable consumption in relation to hepatocellular carcinoma in a multi-centre, European cohort study

doi:10.1038/bjc.2014.654

Multicenter Study

. 2015 Mar 31;112(7):1273-82.

doi: 10.1038/bjc.2014.654.

Fruit and vegetable consumption in relation to hepatocellular carcinoma in a multi-centre, European cohort study

C Bamia¹, P Lagiou², M Jenab³, K Aleksandrova⁴, V Fedirko⁵, D Trichopoulos⁶, K Overvad⁷, A Tjønneland⁸, A Olsen⁸, F Clavel-Chapelon⁹, M-C Boutron-Ruault⁹, M Kvaskoff⁹, V A Katzke¹⁰, T Kühn¹⁰, H Boeing⁴, U Nöthlings¹¹, D Palli¹², S Sieri¹³, S Panico¹⁴, R Tumino¹⁵, A Naccarati¹⁶, H B Bueno-de-Mesquita¹⁷, P H M Peeters¹⁸, E Weiderpass¹⁹, G Skeie²⁰, J R Quirós²¹, A Agudo²², M-D Chirlaque²³, M-J Sanchez²⁴, E Ardanaz²⁵, M Dorronsoro²⁶, U Ericson²⁷, L M Nilsson²⁸, M Wennberg²⁹, K-T Khaw³⁰, N Wareham³¹, T J Key³², R C Travis³², P Ferrari³, M Stepien³, T Duarte-Salles³, T Norat³³, N Murphy³³, E Riboli³³, A Trichopoulou³⁴

Affiliations

¹ Department of Hygiene, Epidemiology and Medical Statistics, University of Athens Medical School, Athens 115 27, Greece.
² 1] Department of Hygiene, Epidemiology and Medical Statistics, University of Athens Medical School, Athens 115 27, Greece [2] Department of Epidemiology, Harvard School of Public Health, 02115 Boston, MA, USA [3] Bureau of Epidemiologic Research, Academy of Athens, Athens 106 79, Greece.
³ International Agency for Research on Cancer (IARC-WHO), 69372 Lyon, France.
⁴ Department of Epidemiology, German Institute of Human Nutrition Potsdam-Rehbruecke, Nuthetal 14558, Germany.
⁵ Department of Epidemiology, Rollins School of Public Health, Winship Cancer Institute, Emory University, Atlanta 30322, GA, USA.
⁶ 1] Department of Epidemiology, Harvard School of Public Health, 02115 Boston, MA, USA [2] Bureau of Epidemiologic Research, Academy of Athens, Athens 106 79, Greece [3] Hellenic Health Foundation, Athens 115 27, Greece.
⁷ Department of Public Health, Section for Epidemiology, Aarhus University, DK-8000 Aarhus C, Denmark.
⁸ Danish Cancer Society Research Center, DK-2100 Copenhagen, Denmark.
⁹ 1] Inserm, Centre for Research in Epidemiology and Population Health (CESP), U1018, Nutrition, Hormones and Women's Health Team, Villejuif, F-94805 Paris, France [2] Paris South University, UMRS 1018, Villejuif, F-94805 Paris, France [3] IGR, Villejuif, F-94805 Paris, France.
¹⁰ Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany.
¹¹ Department of Nutrition and Food Sciences, University of Bonn, 53111 Bonn, Germany.
¹² Molecular and Nutritional Epidemiology Unit, Cancer Research and Prevention Institute-ISPO, 50139 Florence, Italy.
¹³ Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, 20133 Milan, Italy.
¹⁴ Dipartimento di Medicina Clinica e Chirurgia Federico II University, 80131 Naples, Italy.
¹⁵ Cancer Registry and Histopathology Unit, 'Civic-M.P. Arezzo' Hospital, ASP 97100 Ragusa, Italy.
¹⁶ HuGeF-Human Genetics Foundation-Torino Molecular and Genetic Epidemiology Unit, 10126 Torino, Italy.
¹⁷ 1] Department for Determinants of Chronic Diseases (DCD), National Institute for Public Health and the Environment (RIVM), 3720 BA Bilthoven, The Netherlands [2] Department of Gastroenterology and Hepatology, University Medical Centre Utrecht, 3508 GA Utrecht, The Netherlands [3] Department of Social and Preventive Medicine, Faculty of Medicine, University of Malaya, 50603 Kuala Lumpur, Malaysia [4] Department of Epidemiology and Biostatistics, School of Public Health, Faculty of Medicine, Imperial College, W2 1NY UK London, UK.
¹⁸ 1] Department of Epidemiology and Biostatistics, School of Public Health, Faculty of Medicine, Imperial College, W2 1NY UK London, UK [2] Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, 3508 GA Utrecht, The Netherlands.
¹⁹ 1] Department of Community Medicine, Faculty of Health Sciences, UiT The Arctic University of Norway, N-9037 Tromsø, Norway [2] Cancer Registry of Norway, NO-0304 Oslo, Norway [3] Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, SE-171 Stockholm, Sweden [4] Department of Genetic Epidemiology, Folkhälsan Research Center, 00250 Helsinki, Finland.
²⁰ Department of Community Medicine, Faculty of Health Sciences, UiT The Arctic University of Norway, N-9037 Tromsø, Norway.
²¹ Public Health Directorate, CP 33006 Oviedo, Asturias, Spain.
²² Unit of Nutrition, Environment and Cancer, Cancer Epidemiology Research Program, Catalan Institute of Oncology (ICO), 08908 Barcelona, Spain.
²³ 1] Epidemiology Department, Murcia Regional Health Council, E-30008 Murcia, Spain [2] CIBER Epidemiology and Public Health CIBERESP, 28029 Madrid, Spain.
²⁴ 1] CIBER Epidemiology and Public Health CIBERESP, 28029 Madrid, Spain [2] Escuela Andaluza de Salud Pública, Instituto de Investigación Biosanitaria ibs, GRANADA, Hospitales Universitarios de Granada/Universidad de Granada, 18080 Granada, Spain.
²⁵ 1] CIBER Epidemiology and Public Health CIBERESP, 28029 Madrid, Spain [2] Navarre Public Health Institute, 31003 Pamplona, Spain.
²⁶ 1] Basque Regional Health Department, Public Health Direction, 4-20013 Donostia, San Sebastian, Spain [2] Biodonostia Research Institute CIBER Epidemiology and Public Health CIBERESP, s/n 20014 San Sebastian, Spain.
²⁷ Diabetes and Cardiovascular disease, Genetic Epidemiology Department of Clinical Sciences in Malmö Lund University, SE-205 92 Malmo, Sweden.
²⁸ 1] Department of Nutritional Research, Public Health and Clinical Medicine, Umeå University, SE-901 85 Umeå, Sweden [2] Arcum, Arctic Research Centre at Umeå University, SE-901 85 Umeå, Sweden.
²⁹ Department of Nutritional Research, Public Health and Clinical Medicine, Umeå University, SE-901 85 Umeå, Sweden.
³⁰ University of Cambridge, CB2 0SR Cambridge, UK.
³¹ 1] University of Cambridge, CB2 0SR Cambridge, UK [2] MRC Epidemiology Unit, CB2 0QQ Cambridge, UK.
³² Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, OX3 7LF Oxford, UK.
³³ Department of Epidemiology and Biostatistics, School of Public Health, Faculty of Medicine, Imperial College, W2 1NY UK London, UK.
³⁴ 1] Department of Hygiene, Epidemiology and Medical Statistics, University of Athens Medical School, Athens 115 27, Greece [2] Hellenic Health Foundation, Athens 115 27, Greece.

PMID: 25742480
PMCID: PMC4385950
DOI: 10.1038/bjc.2014.654

Multicenter Study

Fruit and vegetable consumption in relation to hepatocellular carcinoma in a multi-centre, European cohort study

C Bamia et al. Br J Cancer. 2015.

. 2015 Mar 31;112(7):1273-82.

doi: 10.1038/bjc.2014.654.

Authors

Affiliations

¹ Department of Hygiene, Epidemiology and Medical Statistics, University of Athens Medical School, Athens 115 27, Greece.
² 1] Department of Hygiene, Epidemiology and Medical Statistics, University of Athens Medical School, Athens 115 27, Greece [2] Department of Epidemiology, Harvard School of Public Health, 02115 Boston, MA, USA [3] Bureau of Epidemiologic Research, Academy of Athens, Athens 106 79, Greece.
³ International Agency for Research on Cancer (IARC-WHO), 69372 Lyon, France.
⁴ Department of Epidemiology, German Institute of Human Nutrition Potsdam-Rehbruecke, Nuthetal 14558, Germany.
⁵ Department of Epidemiology, Rollins School of Public Health, Winship Cancer Institute, Emory University, Atlanta 30322, GA, USA.
⁶ 1] Department of Epidemiology, Harvard School of Public Health, 02115 Boston, MA, USA [2] Bureau of Epidemiologic Research, Academy of Athens, Athens 106 79, Greece [3] Hellenic Health Foundation, Athens 115 27, Greece.
⁷ Department of Public Health, Section for Epidemiology, Aarhus University, DK-8000 Aarhus C, Denmark.
⁸ Danish Cancer Society Research Center, DK-2100 Copenhagen, Denmark.
⁹ 1] Inserm, Centre for Research in Epidemiology and Population Health (CESP), U1018, Nutrition, Hormones and Women's Health Team, Villejuif, F-94805 Paris, France [2] Paris South University, UMRS 1018, Villejuif, F-94805 Paris, France [3] IGR, Villejuif, F-94805 Paris, France.
¹⁰ Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany.
¹¹ Department of Nutrition and Food Sciences, University of Bonn, 53111 Bonn, Germany.
¹² Molecular and Nutritional Epidemiology Unit, Cancer Research and Prevention Institute-ISPO, 50139 Florence, Italy.
¹³ Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, 20133 Milan, Italy.
¹⁴ Dipartimento di Medicina Clinica e Chirurgia Federico II University, 80131 Naples, Italy.
¹⁵ Cancer Registry and Histopathology Unit, 'Civic-M.P. Arezzo' Hospital, ASP 97100 Ragusa, Italy.
¹⁶ HuGeF-Human Genetics Foundation-Torino Molecular and Genetic Epidemiology Unit, 10126 Torino, Italy.
¹⁷ 1] Department for Determinants of Chronic Diseases (DCD), National Institute for Public Health and the Environment (RIVM), 3720 BA Bilthoven, The Netherlands [2] Department of Gastroenterology and Hepatology, University Medical Centre Utrecht, 3508 GA Utrecht, The Netherlands [3] Department of Social and Preventive Medicine, Faculty of Medicine, University of Malaya, 50603 Kuala Lumpur, Malaysia [4] Department of Epidemiology and Biostatistics, School of Public Health, Faculty of Medicine, Imperial College, W2 1NY UK London, UK.
¹⁸ 1] Department of Epidemiology and Biostatistics, School of Public Health, Faculty of Medicine, Imperial College, W2 1NY UK London, UK [2] Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, 3508 GA Utrecht, The Netherlands.
¹⁹ 1] Department of Community Medicine, Faculty of Health Sciences, UiT The Arctic University of Norway, N-9037 Tromsø, Norway [2] Cancer Registry of Norway, NO-0304 Oslo, Norway [3] Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, SE-171 Stockholm, Sweden [4] Department of Genetic Epidemiology, Folkhälsan Research Center, 00250 Helsinki, Finland.
²⁰ Department of Community Medicine, Faculty of Health Sciences, UiT The Arctic University of Norway, N-9037 Tromsø, Norway.
²¹ Public Health Directorate, CP 33006 Oviedo, Asturias, Spain.
²² Unit of Nutrition, Environment and Cancer, Cancer Epidemiology Research Program, Catalan Institute of Oncology (ICO), 08908 Barcelona, Spain.
²³ 1] Epidemiology Department, Murcia Regional Health Council, E-30008 Murcia, Spain [2] CIBER Epidemiology and Public Health CIBERESP, 28029 Madrid, Spain.
²⁴ 1] CIBER Epidemiology and Public Health CIBERESP, 28029 Madrid, Spain [2] Escuela Andaluza de Salud Pública, Instituto de Investigación Biosanitaria ibs, GRANADA, Hospitales Universitarios de Granada/Universidad de Granada, 18080 Granada, Spain.
²⁵ 1] CIBER Epidemiology and Public Health CIBERESP, 28029 Madrid, Spain [2] Navarre Public Health Institute, 31003 Pamplona, Spain.
²⁶ 1] Basque Regional Health Department, Public Health Direction, 4-20013 Donostia, San Sebastian, Spain [2] Biodonostia Research Institute CIBER Epidemiology and Public Health CIBERESP, s/n 20014 San Sebastian, Spain.
²⁷ Diabetes and Cardiovascular disease, Genetic Epidemiology Department of Clinical Sciences in Malmö Lund University, SE-205 92 Malmo, Sweden.
²⁸ 1] Department of Nutritional Research, Public Health and Clinical Medicine, Umeå University, SE-901 85 Umeå, Sweden [2] Arcum, Arctic Research Centre at Umeå University, SE-901 85 Umeå, Sweden.
²⁹ Department of Nutritional Research, Public Health and Clinical Medicine, Umeå University, SE-901 85 Umeå, Sweden.
³⁰ University of Cambridge, CB2 0SR Cambridge, UK.
³¹ 1] University of Cambridge, CB2 0SR Cambridge, UK [2] MRC Epidemiology Unit, CB2 0QQ Cambridge, UK.
³² Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, OX3 7LF Oxford, UK.
³³ Department of Epidemiology and Biostatistics, School of Public Health, Faculty of Medicine, Imperial College, W2 1NY UK London, UK.
³⁴ 1] Department of Hygiene, Epidemiology and Medical Statistics, University of Athens Medical School, Athens 115 27, Greece [2] Hellenic Health Foundation, Athens 115 27, Greece.

PMID: 25742480
PMCID: PMC4385950
DOI: 10.1038/bjc.2014.654

Abstract

Background: Vegetable and/or fruit intakes in association with hepatocellular carcinoma (HCC) risk have been investigated in case-control studies conducted in specific European countries and cohort studies conducted in Asia, with inconclusive results. No multi-centre European cohort has investigated the indicated associations.

Methods: In 486,799 men/women from the European Prospective Investigation into Cancer and nutrition, we identified 201 HCC cases after 11 years median follow-up. We calculated adjusted hazard ratios (HRs) for HCC incidence for sex-specific quintiles and per 100 g d(-1) increments of vegetable/fruit intakes.

Results: Higher vegetable intake was associated with a statistically significant, monotonic reduction of HCC risk: HR (100 g d(-1) increment): 0.83; 95% CI: 0.71-0.98. This association was consistent in sensitivity analyses with no apparent heterogeneity across strata of HCC risk factors. Fruit intake was not associated with HCC incidence: HR (100 g d(-1) increment): 1.01; 95% CI: 0.92-1.11.

Conclusions: Vegetable, but not fruit, intake is associated with lower HCC risk with no evidence for heterogeneity of this association in strata of important HCC risk factors. Mechanistic studies should clarify pathways underlying this association. Given that HCC prognosis is poor and that vegetables are practically universally accessible, our results may be important, especially for those at high risk for the disease.

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References

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[1] Agudo A, Slimani N, Ocké MC, Naska A, Miller AB, Kroke A, Bamia C, Karalis D, Vineis P, Palli D, Bueno-de-Mesquita HB, Peeters PH, Engeset D, Hjartåker A, Navarro C, Martínez Garcia C, Wallström P, Zhang JX, Welch AA, Spencer E, Stripp C, Overvad K, Clavel-Chapelon F, Casagrande C, Riboli E. Consumption of vegetables, fruit and other plant foods in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohorts from 10 European countries. Public Health Nutr. 2002;5:1179–1196. - PubMed

[2] Agudo A, Slimani N, Ocké MC, Naska A, Miller AB, Kroke A, Bamia C, Karalis D, Vineis P, Palli D, Bueno-de-Mesquita HB, Peeters PH, Engeset D, Hjartåker A, Navarro C, Martínez Garcia C, Wallström P, Zhang JX, Welch AA, Spencer E, Stripp C, Overvad K, Clavel-Chapelon F, Casagrande C, Riboli E. Consumption of vegetables, fruit and other plant foods in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohorts from 10 European countries. Public Health Nutr. 2002;5:1179–1196. - PubMed

[3] Braga C, La Vecchia C, Negri E, Franceschi S. Attributable risks for hepatocellular carcinoma in northern Italy. Eur J Cancer. 1997;33:629–634. - PubMed

[4] Braga C, La Vecchia C, Negri E, Franceschi S. Attributable risks for hepatocellular carcinoma in northern Italy. Eur J Cancer. 1997;33:629–634. - PubMed

[5] Chuang SC, La Vecchia C, Boffetta P. Liver cancer: descriptive epidemiology and risk factors other than HBV and HCV infection. Cancer Lett. 2009;286:9–14. - PubMed

[6] Chuang SC, La Vecchia C, Boffetta P. Liver cancer: descriptive epidemiology and risk factors other than HBV and HCV infection. Cancer Lett. 2009;286:9–14. - PubMed

[7] Clifton PM, Petersen KS, Blanch N, Keogh JB. How do fruit and vegetables prevent heart disease and type 2 diabetes. Curr Opin Lipidol. 2014;25:155–156. - PubMed

[8] Clifton PM, Petersen KS, Blanch N, Keogh JB. How do fruit and vegetables prevent heart disease and type 2 diabetes. Curr Opin Lipidol. 2014;25:155–156. - PubMed

[9] Cook LT, O'Reilly GA, Goran MI, Weigensberg MJ, Spruijt-Metz D, Davis JN. Vegetable consumption is linked to decreased visceral and liver fat and improved insulin resistance in overweight Latino youth. J Acad Nutr Diet. 2014;114:1776–1783. - PMC - PubMed

[10] Cook LT, O'Reilly GA, Goran MI, Weigensberg MJ, Spruijt-Metz D, Davis JN. Vegetable consumption is linked to decreased visceral and liver fat and improved insulin resistance in overweight Latino youth. J Acad Nutr Diet. 2014;114:1776–1783. - PMC - PubMed

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Fruit and vegetable consumption in relation to hepatocellular carcinoma in a multi-centre, European cohort study

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Fruit and vegetable consumption in relation to hepatocellular carcinoma in a multi-centre, European cohort study

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