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Vegetarian diets and cancer risk
BMC Medicine ( IF 7.0 ) Pub Date : 2022-02-24 , DOI: 10.1186/s12916-022-02282-8
Mathias Weller ₁

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Vegetarian diets contain vegetables, fruits, whole grains, legumes, nuts, and seeds [1]. They are devoid of flesh foods (such as meat, poultry, wild game and their products) and may or may not include eggs and dairy products (vegan diet) [1]. A pescatarian diet is a vegetarian diet that includes fish and is devoid of flesh foods [1]. In many countries, the number of people who adopt a vegetarian diet is increasing, and there are several main reasons for this [2]. Ethical concerns about animal welfare and environmental sustainability motivate the adoption of a vegetarian diet [3]. Vegetarian diets are associated with increased environmental sustainability through reduced greenhouse gas emissions, deforestation and water use [4]. Health improvements and weight loss are other strong motivators for the adoption of a vegetarian diet [3]. According to the Academy of Nutrition and Dietetics of the USA, vegetarian diets are associated with better health outcomes, an increased life expectancy, and a reduced risk of coronary heart disease, type 2 diabetes, hypertension and obesity [1]. Furthermore, vegetarian diets are also considered to reduce the risk of certain types of cancer [1].

Previous studies on the association of dietary patterns and specific types of cancer led to partially conflicting results. The pooled analysis of data obtained from the Oxford Vegetarian Study and the EPIC-Oxford cohort, including 61,647 participants, revealed that vegetarians and pescatarians have an overall reduced risk of developing cancer compared to meat eaters [5]. Additionally, the database study also identified a reduced risk of stomach cancer, cancers of the lymphatic and haematopoietic tissue and multiple myeloma among vegetarians and pescatarians and a reduced risk of colorectal cancer among pescatarians [5]. Based on 69,120 participants, the Adventist Health Study-2 revealed that vegetarians were protected from cancers of the gastrointestinal tract compared to nonvegetarians [6]. A vegan diet reduced the overall cancer incidence and the risk of female-specific cancers [6]. In contrast, a recent meta-analysis that included nine studies did not identify any benefit of a vegetarian diet on the risk of breast, colorectal or prostate cancer [7]. Another recent meta-analysis attributed a reduced risk of cancer mortality to a vegetarian diet without showing any association between diet and a specific type of cancer [8].

The reports presented by Parra-Soto et al. [9] and Watling et al. [10] are based on 409,110 and 472,377 UK Biobank participants, respectively, recruited between 2006 and 2010. The mean follow-up was 10.6 and 11.4 years [9, 10], respectively. To date, both papers represent the largest database studies ever to address the question of vegetarian and pescatarian diets and the risk of cancer. The design and results differ substantially in some aspects between both studies. In contrast to Parra-Soto et al. [9], Watling et al. [10] distinguished between regular and low meat eaters as those who consume processed, red meat (beef, pork, lamb) or poultry >5 or ≤5 times a week, respectively. Low meat eaters had a reduced risk of colorectal cancer compared to regular meat eaters [10]. Vegetarians had a lower risk of all cancers, prostate cancer and postmenopausal breast cancer, and pescatarians had a lower risk of all cancers than regular meat eaters [10]. The authors indicated that the reduced risk of postmenopausal breast cancer may be largely attributed to the lower mean body mass index (BMI) of vegetarian women. The authors also performed subgroup analysis for sex and smoking. After removing lung cancer cases from the analysis, the reduced risk of all cancers for vegetarians, pescatarians and low meat eaters was only found among ever-smokers [10]. Furthermore, a reduced risk of colorectal cancer among dietary groups compared to regular meat eaters was only found among men [10].

Due to the exclusion of all participants with cancer at baseline and those with missing data about diet and important covariates, the study group of Parra-Soto et al. [9] was smaller. Meat eaters form a single group, and the results are also represented for a separate dietary group of fish-poultry eaters [9]. In their maximally adjusted model, vegetarians had a lower risk of all cancers, and prostate cancer and pescatarians had a lower risk of all cancers than regular meat eaters [9]. In contrast to the study of Watling et al. [10], vegetarians did not have a reduced risk of breast cancer but did have a reduced risk of colorectal cancer [9]. Furthermore, pescatarians also had a reduced risk of melanoma [9]. Additionally, in a meta-analysis, authors pooled their UK Biobank data with eight prospective cohort studies [9]. In the pooled analysis, vegetarians and pescatarians had a reduced risk of all cancers and a borderline reduced risk of colorectal cancer [9].

The different outcomes of the two studies are explained by varying sample sizes, categories of diet groups and distinct modelling strategies. The subgroup analysis in one study indicated that important additional variables, such as smoking, can modulate the risk of cancers and can confound the results of dietary cancer associations. Both papers are based on large datasets and undoubtedly reveal that vegetarian diets can indeed decrease the risk of specific types of cancer. The risks of prostate cancer and colorectal cancer among men are decreased by a vegetarian diet. In the case of postmenopausal breast cancer, the protective effect may be an indirect one that acts through the modification of the BMI. The diet may only have an impact on certain types of cancer, as neither study detected any effect of the vegetarian diet on the risk of lung cancer. However, the protective effects of vegetarian diets on rare types of cancer may not have been detected in these studies because the numbers of affected patients were low. It is predictable that future studies will probably reveal further associations between vegetarian diets and risk reduction in other cancer types.

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Melina V, Craig W, Levin S. Position of the Academy of Nutrition and Dietetics: Vegetarian Diets. J Acad Nutr Diet. 2016;116(12):1970–80. https://doi.org/10.1016/j.jand.2016.09.025.
Article PubMed Google Scholar
How many adults in the U.S. are vegetarian and vegan? How many adults eat vegetarian and vegan meals when eating out? [https://www.vrg.org/nutshell/Polls/2019_adults_veg.htm]
Hagmann D, Sigrist M, Hartmann C. Meat avoidance: motives, alternative proteins and diet quality in a sample of Swiss consumers. Public Health Nutr. 2019;22(13):2448–59. https://doi.org/10.1017/S1368980019001277.
Article PubMed Google Scholar
Fresán U, Sabaté J. Vegetarian Diets: Planetary Health and Its Alignment with Human Health. Adv Nutr. 2019;10(Suppl_4):S380–8. https://doi.org/10.1093/advances/nmz019.
Article PubMed PubMed Central Google Scholar
Key TJ, Appleby PN, Crowe FL, Bradbury KE, Schmidt JA, Travis RC. Cancer in British vegetarians: updated analyses of 4998 incident cancers in a cohort of 32,491 meat eaters, 8612 fish eaters, 18,298 vegetarians, and 2246 vegans. Am J Clin Nutr. 2014;100(Suppl 1):378S–85S.
CAS Article Google Scholar
Tantamango-Bartley Y, Jaceldo-Siegl K, Fan J, Fraser G. Vegetarian diets and the incidence of cancer in a low-risk population. Cancer Epidemiol Biomarkers Prev. 2013;22(2):286–94. https://doi.org/10.1158/1055-9965.EPI-12-1060.
Article PubMed Google Scholar
Godos J, Bella F, Sciacca S, Galvano F, Grosso G. Vegetarianism and breast, colorectal and prostate cancer risk: an overview and meta-analysis of cohort studies. J Hum Nutr Diet. 2017;30(3):349–59.
CAS Article Google Scholar
Dinu M, Abbate R, Gensini GF, Casini A, Sofi F. Vegetarian, vegan diets and multiple health outcomes: A systematic review with meta-analysis of observational studies. Crit Rev Food Sci. 2017;57(17):3640–9.
Article Google Scholar
Parra-Soto S, et al. Association of meat, vegetarian, pescatarian, and fish-poultry diets with risk of 19 cancer sites and all cancer: Findings from the UK Biobank prospective cohort study and meta-analysis. BMC Med. 2022. https://doi.org/10.1186/s12916-022-02257-9.
Watling CZ, et al. Risk of cancer in regular and low meat-eaters, fish-eaters, and vegetarians: a prospective analysis of UK Biobank participants. BMC Med. 2022. https://doi.org/10.1186/s12916-022-02256-w.

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Post Graduate Program in Public Health, State University of Paraíba (UEPB), Campina Grande, Paraíba, Brazil
Mathias Weller

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Weller, M. Vegetarian diets and cancer risk. BMC Med 20, 81 (2022). https://doi.org/10.1186/s12916-022-02282-8

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Received: 31 January 2022
Accepted: 02 February 2022
Published: 24 February 2022
DOI: https://doi.org/10.1186/s12916-022-02282-8

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Keywords

Diet
Vegetarian
Pescatarian
Meat
Colorectal cancer
Breast cancer
Prostate cancer
Cohort studies

中文翻译：

素食与癌症风险

素食饮食包括蔬菜、水果、全谷物、豆类、坚果和种子 [1]。它们不含肉食（如肉类、家禽、野味及其制品），可能包括也可能不包括鸡蛋和奶制品（纯素饮食）[1]。pescatarian 饮食是一种素食饮食，包括鱼，不含肉食 [1]。在许多国家，采用素食的人数正在增加，这有几个主要原因 [2]。对动物福利和环境可持续性的伦理担忧促使人们采用素食[3]。素食通过减少温室气体排放、森林砍伐和用水量来提高环境可持续性[4]。健康改善和体重减轻是采用素食的其他强大动力 [3]。根据美国营养与饮食学会的数据，素食与更好的健康结果、延长预期寿命以及降低患冠心病、2 型糖尿病、高血压和肥胖症的风险有关 [1]。此外，素食也被认为可以降低某些类型癌症的风险[1]。

先前关于饮食模式与特定癌症类型之间关联的研究导致部分相互矛盾的结果。对来自牛津素食研究和 EPIC-Oxford 队列（包括 61,647 名参与者）的数据进行汇总分析后发现，与肉食者相比，素食者和鱼素者患癌症的风险总体降低 [5]。此外，该数据库研究还发现素食者和鱼素人患胃癌、淋巴和造血组织癌症和多发性骨髓瘤的风险降低，鱼素人患结肠直肠癌的风险降低 [5]。基于 69,120 名参与者的 Adventist Health Study-2 显示，与非素食者相比，素食者免受胃肠道癌症的侵害 [6]。纯素饮食降低了整体癌症发病率和女性特定癌症的风险[6]。相比之下，最近一项包含 9 项研究的荟萃分析并未发现素食对乳腺癌、结直肠癌或前列腺癌的风险有任何益处 [7]。最近的另一项荟萃分析将降低癌症死亡率的风险归因于素食，但没有显示饮食与特定类型的癌症之间存在任何关联[8]。

Parra-Soto 等人提出的报告。[9] 和 Watling 等人。[10] 分别基于 2006 年至 2010 年间招募的 409,110 和 472,377 名英国生物银行参与者。平均随访时间分别为 10.6 年和 11.4 年 [9, 10]。迄今为止，这两篇论文代表了有史以来解决素食和鱼素饮食问题以及癌症风险的最大数据库研究。两项研究的设计和结果在某些方面存在很大差异。与 Parra-Soto 等人相反。[9]，Watling 等人。[10] 将常规肉食者和低肉食者区别为每周食用加工过的红肉（牛肉、猪肉、羊肉）或家禽 > 5 次或≤5 次的人。与常规肉食者相比，低肉食者患结直肠癌的风险降低 [10]。素食者患所有癌症的风险较低，前列腺癌和绝经后乳腺癌，鱼素人患所有癌症的风险低于普通肉食者 [10]。作者指出，绝经后乳腺癌风险的降低可能很大程度上归因于素食女性的平均体重指数 (BMI) 较低。作者还对性别和吸烟进行了亚组分析。从分析中剔除肺癌病例后，素食者、鱼素者和低肉食者患所有癌症的风险仅在经常吸烟的人中发现[10]。此外，与常规肉食者相比，饮食组的结直肠癌风险降低仅在男性中发现 [10]。作者指出，绝经后乳腺癌风险的降低可能很大程度上归因于素食女性的平均体重指数 (BMI) 较低。作者还对性别和吸烟进行了亚组分析。从分析中剔除肺癌病例后，素食者、鱼素者和低肉食者患所有癌症的风险仅在经常吸烟的人中发现[10]。此外，与常规肉食者相比，饮食组的结直肠癌风险降低仅在男性中发现 [10]。作者指出，绝经后乳腺癌风险的降低可能很大程度上归因于素食女性的平均体重指数 (BMI) 较低。作者还对性别和吸烟进行了亚组分析。从分析中剔除肺癌病例后，素食者、鱼素者和低肉食者患所有癌症的风险仅在经常吸烟的人中发现[10]。此外，与常规肉食者相比，饮食组的结直肠癌风险降低仅在男性中发现 [10]。

由于排除了所有基线癌症参与者以及缺少饮食和重要协变量数据的参与者，Parra-Soto 等人的研究小组。[9] 更小。肉食者形成一个单一的群体，结果也代表了一个单独的鱼禽饮食群体[9]。在他们的最大调整模型中，素食者患所有癌症的风险较低，而前列腺癌和鱼素人患所有癌症的风险低于普通肉食者 [9]。与 Watling 等人的研究相反。[10]，素食者患乳腺癌的风险并未降低，但患结直肠癌的风险确实降低了 [9]。此外，鱼素人患黑色素瘤的风险也降低了 [9]。此外，在一项荟萃分析中，作者将他们的英国生物银行数据与八项前瞻性队列研究进行了汇总 [9]。在汇总分析中，

这两项研究的不同结果可以通过不同的样本量、饮食组的类别和不同的建模策略来解释。一项研究中的亚组分析表明，重要的附加变量，例如吸烟，可以调节癌症的风险，并且可以混淆饮食癌症关联的结果。这两篇论文都基于大型数据集，毫无疑问地揭示了素食确实可以降低特定类型癌症的风险。素食可以降低男性患前列腺癌和结直肠癌的风险。在绝经后乳腺癌的情况下，保护作用可能是通过改变 BMI 发挥作用的间接保护作用。饮食可能只对某些类型的癌症有影响，因为两项研究都没有发现素食对肺癌风险有任何影响。然而，在这些研究中可能没有发现素食对罕见癌症的保护作用，因为受影响的患者人数很少。可以预见的是，未来的研究可能会进一步揭示素食与其他癌症类型风险降低之间的关联。

不适用

Melina V、Craig W、Levin S. 营养与营养学学院的职位：素食。J Acad 营养饮食。2016;116(12):1970-80。https://doi.org/10.1016/j.jand.2016.09.025。
文章 PubMed 谷歌学术
美国有多少成年人是素食主义者？有多少成年人在外出就餐时吃素食和纯素餐？[https://www.vrg.org/nutshell/Polls/2019_adults_veg.htm]
Hagmann D、Sigrist M、Hartmann C. 肉类回避：瑞士消费者样本中的动机、替代蛋白质和饮食质量。公共卫生营养学。2019;22(13):2448-59。https://doi.org/10.1017/S1368980019001277。
文章 PubMed 谷歌学术
Fresán U, Sabaté J. 素食：行星健康及其与人类健康的一致性。进阶营养。2019；10（增刊 4）：S380–8。https://doi.org/10.1093/advances/nmz019。
文章 PubMed PubMed Central Google Scholar
Key TJ、Appleby PN、Crowe FL、Bradbury KE、Schmidt JA、Travis RC。英国素食者的癌症：对 32,491 名肉食者、8612 名鱼食者、18,298 名素食者和 2246 名素食者组成的队列中 4998 例癌症的最新分析。Am J Clin Nutr。2014；100（增刊 1）：378S–85S。
CAS 文章谷歌学术
Tantamango-Bartley Y、Jaceldo-Siegl K、Fan J、Fraser G. 素食和低风险人群的癌症发病率。癌症流行病学生物标志物 2013;22(2):286-94。https://doi.org/10.1158/1055-9965.EPI-12-1060。
文章 PubMed 谷歌学术
Godos J、Bella F、Sciacca S、Galvano F、Grosso G. 素食主义与乳腺癌、结直肠癌和前列腺癌风险：队列研究的概述和荟萃分析。J Hum Nutr 饮食。2017;30(3):349-59。
CAS 文章谷歌学术
Dinu M、Abbate R、Gensini GF、Casini A、Sofi F. 素食、纯素饮食和多种健康结果：对观察性研究进行荟萃分析的系统评价。Crit Rev 食品科学。2017;57(17):3640-9。
文章谷歌学术
Parra-Soto S 等人。肉类、素食、鱼素和鱼禽饮食与 19 个癌症部位和所有癌症风险的关联：来自英国生物银行前瞻性队列研究和荟萃分析的结果。BMC医学。2022. https://doi.org/10.1186/s12916-022-02257-9。
Watling CZ 等人。经常和低肉食者、鱼食者和素食者患癌症的风险：对英国生物银行参与者的前瞻性分析。BMC医学。2022. https://doi.org/10.1186/s12916-022-02256-w。

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