International Journal of Food Sciences and Nutrition

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Differences in the association between empirically

derived dietary patterns and cancer: a meta-
analysis

Francesca Bella, Justyna Godos, Antonella Ippolito, Alessia Di Prima &

Salvatore Sciacca

To cite this article: Francesca Bella, Justyna Godos, Antonella Ippolito, Alessia Di Prima &
Salvatore Sciacca (2016): Differences in the association between empirically derived dietary
patterns and cancer: a meta-analysis, International Journal of Food Sciences and Nutrition,
DOI: 10.1080/09637486.2016.1261087

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INTERNATIONAL JOURNAL OF FOOD SCIENCES AND NUTRITION, 2016
http://dx.doi.org/10.1080/09637486.2016.1261087

RESEARCH ARTICLE

Differences in the association between empirically derived dietary patterns

and cancer: a meta-analysis
Francesca Bella, Justyna Godos , Antonella Ippolito, Alessia Di Prima and Salvatore Sciacca
Integrated Cancer Registry of Catania-Messina-Siracusa-Enna, Azienda Universitario Ospedaliera Policlinico “Vittorio Emanuale:,
Catania, Italy

ABSTRACT ARTICLE HISTORY

Plant-based dietary patterns have been associated with decreased cancer risk. The aim of the pre- Received 15 September 2016
sent study was to perform a meta-analysis of studies comparing empirically derived dietary pat- Revised 7 November 2016
terns in relation to cancer risk. A systematic search of PubMed and EMBASE electronic databases Accepted 8 November 2016
was conducted. Eligible studies had an observational design and evaluated the association with
cancer risk between a posteriori derived dietary patterns. Random-effects models were applied to KEYWORDS
calculate relative risks (RRs) of cancer between diets. Statistical heterogeneity and publication Plant based; meat based;
bias were explored. An increased risk of cancer for the adoption of high-meat compared to mixed foods; dietary
plant-based dietary patterns was found (RR ¼1.64, 95% CI: 1.02, 2.63). Lower risk of cancer for patterns; cancer; meta-
individuals adopting a plant-based dietary pattern over a mixed one was found (RR ¼0.88, 95% analysis
CI: 0.82, 0.95). In conclusion, plant-based dietary patterns can be considered a healthy choice
over meat-based dietary patterns.

Introduction Marventano et al. 2015). In contrast, diets with high

Cancer represents a group of more than a hundred of
conditions characterized by uncontrolled cell growth,
invasion in adjacent tissues and various grade of loss
of differentiation. The initiating process that result in
the alteration of the genetic information of the cells is,
in most of cases, the result of damages accumulated
over time secondary to endogen or external stimula:
the latter include smoking habits, infectious organisms,
exposure to chemicals and diet composition, which in
turn may affect cellular processes linked to cancer, such
as DNA repair, cell proliferation and differentiation,
cell cycle control, hormonal regulation, inflammation
and immune function and carcinogen metabolism
(Ogino et al. 2013; Kantor & Giovannucci 2015).
Among the others, diet has been considered the focus
of interest over the last 50 years for its potential role in
preventing cancer (Mourouti et al. 2015). Dietary pat-
terns with high content of fruit and vegetable are
important source of fiber and antioxidant compounds,
including polyphenolic compounds and healthy fatty
acids [mono- and polyunsaturated fatty acids (MUFA
and PUFA, respectively)], which may have beneficial
effects toward cancer risk (Giacosa et al. 2013;
content of processed fat foods, alcoholic beverages and
sweets, are major source of trans-fatty acids, alcohol
and refined carbohydrates, which may be related with
increased risk of cancer (Wiseman 2008; Bagnardi et al.
2015; Bouvard et al. 2015).
Dietary patterns are able to capture various aspects
of diet adopted by a population and may provide
insights on the synergistic effect of several components
(Edefonti et al. 2009b). A number of observational
studies have been conducted on a posteriori empiric-
ally-derived dietary patterns: results were based on the
association between the highest adherence to a dietary
pattern compared with lowest, showing that higher
adherence to healthy and prudent dietary patterns
were more likely to be associated with lower cancer
risk while higher adherence to so-called “Western”
and unhealthy dietary patterns was associated with
increased risk of cancer, especially gastrointestinal
cancers (Magalhaes et al. 2012; Bertuccio et al. 2013).
However, no summary analysis of current evidence of
studies directly comparing the association with cancer
risk between dietary patterns was performed. The aim
of the present study was to provide an overview and
perform a meta-analysis of studies comparing

CONTACT Justyna Godos justyna.godos@student.uj.edu.pl Integrated Cancer Registry of Catania-Messina-Siracusa-Enna, Azienda Universitario
Ospedaliera Policlinico "Vittorio Emanuale", Catania, Italy
ß 2016 Informa UK Limited, trading as Taylor & Francis Group
2 F. BELLA ET AL.
empirically derived dietary patterns in relation with
cancer risk.
Methods
Study search
A systematic search on PubMed (http://www.ncbi.nlm.
nih.gov/pubmed/) and EMBASE (http://www.embase.
com/) databases of English language studies published
up to March 2016 was performed. Search terms
included a combination of keywords, such as “dietary
pattern” and “cancer” and their variants. Inclusion cri-
teria were the following: (i) having an observational
(case-control or prospective) study design; (ii) evaluat-
ing the association with risk of cancer between a pos-
teriori derived dietary patterns based on principal
component analysis (PCA) or cluster analysis; (iii)
assessed and reported a measure of association for the
outcome considered as odds ratios (ORs) or hazard
ratios (HRs) and the corresponding 95% confidence
intervals (CIs). Reference lists of included studies were
scrutinized for any article not previously identified.
The article selection process was independently per-
formed by two authors.
Data extraction and study quality assessment
Data were extracted from selected studies by using a
standardized extraction form. The following informa-
tion was collected: (i) author name; (ii) year of publi-
cation; (iii) cohort name, length of follow-up, country;
(iv) number, gender, and age of participants and cases;
(v) reference category and OR/HR and 95% CI for the
categories of exposure; and (vi) covariates used in
adjustments.
The Newcastle–Ottawa Quality Assessment Scale
was used to assess the quality of each study (Wells
1999). The instrument consists of 3 domains indicat-
ing the study quality as follows: selection (4 points),
comparability (2 points), and outcome (3 points) for a
total score of 9 points (9 representing the highest
quality). Studies scoring 7–9 points, 3–6 points and
0–3 points were identified as high, medium and low
quality, respectively.
Statistical analysis
Random-effects models were used to calculate risk
ratios (RRs) with 95% CIs for various categories of
exposure. The risk estimate from the most fully
adjusted models in the analysis of the pooled RR was
used. Heterogeneity was assessed using the Q test and
I2 statistic. The level of significance for the Q test was
defined as p < .10. The I2 statistic represented the
amount of total variation that could be attributed to
heterogeneity. I2 values >50 indicated high heterogen-
eity. Sensitivity analyzes by excluding one study at the
time were conducted. When data were sufficient to
perform subgroup analyses, we considered whether
differences by gender and cancer localization existed.
Publication bias was evaluated by a visual investigation
of funnel plots for potential asymmetry. All analyzes
were performed with Review Manager (RevMan) soft-
ware version 5.2 (The Nordic Cochrane Center, The
Cochrane Collaboration).
Results
Study characteristics
Out of the 219 unique citations, 71 were excluded
after abstract examination and 141 were excluded after
full-text reading for the following reasons: 35 studies
explored a priori dietary patterns; four studies explored
cancer survival; and 102 studies compared the level of
adherence within dietary patterns (Figure 1). This selec-
tion process led to the consideration of seven studies to
be included in this meta-analysis (Chen et al. 2002;
Rouillier et al. 2005; Austin et al. 2007; Edefonti et al.
2009a; Wirfalt et al. 2009; Bastos et al. 2010; Magalhaes
et al. 2011). The main characteristics of the studies
included are presented in Table 1: case–control studies
(Chen et al. 2002; Rouillier et al. 2005; Austin et al.
2007; Edefonti et al. 2009a; Bastos et al. 2010;
Magalhaes et al. 2011) accounted for a total of 5042
cases and 5516 controls; the prospective study (Wirfalt
et al. 2009) included 492,306 individuals and 3135 cases.
Most of the studies were conducted on colorectal cancer
(Rouillier et al. 2005; Austin et al. 2007; Wirfalt et al.
2009; Magalhaes et al. 2011), two on gastric and esopha-
geal cancers (Chen et al. 2002; Bastos et al. 2010), and
one on breast and ovarian cancers (Edefonti et al.
2009a). All studies adjusted for variables potentially
related with cancer incidence, including gender, body
mass index, smoking status, physical activity, energy
intake and hormonal and parity status in women. Study
quality was high for most of the studies included in the
analyses.
Dietary patterns
All studies used food frequency questionnaires to
explore the dietary consumption of participants. In all
studies, dietary patterns were identified with PCA and
cluster analysis: four studies compared dietary patterns

characterized by high meat intake with those high in
fruits and vegetables (Chen et al. 2002; Austin et al.
2007; Bastos et al. 2010; Magalhaes et al. 2011); three
studies considered as category of reference dietary pat-
terns with no specific characterization or extreme con-
sumption of particular foods, which compared with
patterns high in plant-foods and animal-foods
(Rouillier et al. 2005; Edefonti et al. 2009a; Wirfalt
et al. 2009) (Table 1).
High-meat versus plant-based dietary patterns
and cancer risk
The association of high-meat compared to plant-based
dietary patterns and cancer risk was explored in four
studies (Chen et al. 2002; Austin et al. 2007; Bastos
et al. 2010; Magalhaes et al. 2011) including 1794 indi-
viduals and 1271 cases (Figure 2a): the analysis based
on six datasets showed an increased risk of cancer for
adoption of the former compared with the latter pattern
(RR ¼1.64, 95% CI: 1.02, 2.63) with significant evidence
of heterogeneity (I2 ¼ 69%, Pheterogeneity ¼ 0.007) and
asymmetry of funnel plot (Figure 3a). A sensitivity ana-
lysis by exclusion of one study at the time revealed that
Figure 1. Study selection flow chart.
INTERNATIONAL JOURNAL OF FOOD SCIENCES AND NUTRITION 3
heterogeneity was due to one study, after exclusion of
which the summary risk estimates remained significant
with no evidence of heterogeneity (RR ¼1.88, 95% CI:
1.38, 2.58; I2 ¼ 0%, Pheterogeneity ¼ 0.59). A subgroup ana-
lyzes based on cancer localization showed that the study
conducted on upper digestive tract reported non-signifi-
cant summary risk estimates (RR ¼1.77, 95% CI: 0.59,
5.33; I2 ¼ 76%, Pheterogeneity ¼ 0.02) while those conducted
on colorectal cancer showed a significant risk related to
adoption of high-meat compared to plant-based dietary
patterns (RR ¼1.74, 95% CI: 1.25, 2.44; I2 ¼ 0%,
Pheterogeneity ¼ 0.55).
Plant-based versus mixed food patterns and
cancer risk
Seven datasets from three studies (Rouillier et al. 2005;
Edefonti et al. 2009a; Wirfalt et al. 2009) were ana-
lyzed to test the association plant-based compared to
dietary patterns with various foods and cancer risk
(Figure 2b). The studies comprised the cohort study
and 3771 total cases and 3722 controls from case–con-
trol studies on colon, rectum, breast and ovarian can-
cers. The analysis showed a significant lower risk of
 4

Table 1. Main characteristics of the studies included in the meta-analysis.

Study cohort, No. of indi- Method of
follow-up viduals/No. Dietary pattern Dietary pattern included in the Study
Author, year Cancer site Study design (country) of controls No. of cases Age range assessment identification analysis Covariates adjustment quality
Chen, 2002 Esophageal, Case–control USA 449 124 esopha- 21 year FFQ, 54 Cluster (I) higher energy contributions from Age, sex, energy Medium
gastric geal, 124 items analysis fish, poultry, fruit and vegetables, intake, respondent
distal dark bread and cereals and lower type, BMI, alcohol
F. BELLA ET AL.

stomach energy contributions from red meat, use, tobacco use,

processed meat and gravy; (II) high education, family his-
in red meat, processed meat, and tory, vitamin supple-
beans and the low in fruit, cereals ment use.
and salty snacks.
Rouillier, Colorectal Case–control France 309 171 30–79 years FFQ, NA Cluster (I) low intake of mixed foods; (II) Age, gender, energy, Medium
2005 analysis high intake of whole-meal cereal BMI, exercise, tobacco
products, fish, honey, chicory drink, and alcohol.
olive oil, vegetables and fruit; (III)
high intake of bread, pork, oils other
than olive oil, wine, starchy foods
and high-fat processed meat.
Austin, 2007 Colorectal Case–control USA 466 179 30–80 years FFQ, Cluster (I) high consumption of total fruits Age, race, sex, BMI, Medium
adenomas 124 items analysis (including citrus/melon/berry fruits) NSAID use, smoking
and whole grain products with and alcohol
slightly below-average vegetable con- consumption.
sumption and significantly lower con-
sumption of all animal meats
(chicken/fish, beef/pork/lamb, and
franks/luncheon meats); (II) below-
average consumption of whole grain
products, all vegetables (except pota-
toes), and fruits and above-average
consumption of all the major meat
categories, discretionary fat and
added sugar.
Edefonti, Breast, Case–control Italy 3413 2569 breast, 23–74 years FFQ, 78 PCA (I) mixed foods; (II) vitamins and Age, education, parity, High
2009 ovarian 1031 ovarian breast cases, items fiber; (III) animal products menopausal status,
18–79 years geographic area, BMI,
ovarian history of digestive
cases, 17–79 cancers, history of
years female cancers and
controls energy intake.
Bastos, 2010 Gastric Case–control Portugal 1463 591 18 y FFQ, 82 PCA (I) high consumption of dairy prod- Age, gender, educa- High
items ucts, fruits, salads and vegetables and tion and total energy
low consumption of meat and alco- intake (by location
holic beverages; (II) high consump- and histological type,
tions of most food groups and lowest according to
vegetable soup intake. Helicobacter pylori
infection status).
Magalheas, Colorectal Case–control Portugal 151879
rectum, 102 18 years FFQ, 82 PCA (I) high consumption of dairy prod- Age, sex, education Medium
2011 colon items ucts, fish and seafood, wholegrain level, total energy
cereals, vegetables and salads, intake and physical
legumes, fruits and vegetable soup activity.
and low intake of wine; (II) high con-
sumption of red meat, processed
(continued)
 INTERNATIONAL JOURNAL OF FOOD SCIENCES AND NUTRITION 5

cancer for individuals adopting a plant-based dietary

quality
pattern over a mixed one (RR ¼0.88, 95% CI: 0.82,
Study 0.95) with no evidence of heterogeneity (I2 ¼ 6%,

High
Covariates adjustment Pheterogeneity ¼ 0.38) or asymmetry of funnel plot

also adjusted for hor-

(Figure 3b). Sensitivity analysis by excluding one study

Age, BMI, education,

leisure time physical

ethnicity, smoking,

energy. In women
at the time did not change summary results (data not

activity and total

mone therapy.
shown). Subgroup analysis to explore potential con-
founding factors showed no variations of previous
findings: the results remained significant when consid-
ering women (RR ¼0.91, 95% CI: 0.83, 0.99; I2 ¼ 0%,
Pheterogeneity ¼ 0.54) and gastrointestinal cancer (RR
sweets, potatoes, wine and alcoholic
beverages, and low intake of whole-

like fish and lean chicken; (III) regu-

vegetables, fruits, and low-fat foods
(I) mixed foods; (II) high intakes of
Dietary pattern included in the

¼0.87, 95% CI: 0.80, 0.95; I2 ¼ 1%, Pheterogeneity ¼ 0.40),

grain cereals and vegetable soup.
meat, refined cereals, sugar and

but not female cancers (RR ¼0.89, 95% CI: 0.76, 1,05;
I2 ¼ 51%, Pheterogeneity ¼ 0.15).
analysis

Meat-based dietary versus mixed foods patterns

lar-fat meats.

and cancer risk

The association of meat-based compared to mixed
foods dietary patterns and cancer risk was explored in
identification
Method of

five datasets from three studies (Rouillier et al. 2005;

pattern

analysis

Edefonti et al. 2009a; Wirfalt et al. 2009) and showed

Cluster

no significant results (Figure 2c), with no evidence of

heterogeneity and asymmetry of funnel plot (Figure 3c).
assessment
Dietary

A sensitivity analysis with exclusion of one study at the

FFQ, 181

time and based on cancer localization did not change

items

the summary results.

In men, 631 50–71 years
Age range

Discussion
BMI: body mass index; FFQ: food frequency questionnaire; PCA: principal component analysis.

The summary of evidence on the association between

rectal cancer

rectal cancer
colon cancer

colon cancer
No. of cases

women, 258

empirically derived healthy and unhealthy dietary pat-

and 1539

cases; in

and 707

terns and risk of cancer showed consistent results with

cases

existing literature. Results from this meta-analysis

showed an inverse association between adoption of
No. of indi-
viduals/No.
of controls

men and
(293,576

women)
492,306

198,730

mainly plant-based dietary pattern compared to meat-

based one and cancer risk as well as a positive associ-
ation between adoption of a dietary pattern character-
ized by high meat consumption compared to a
NIH-AARP Diet
Study cohort,

5-year follow-
follow-up
(country)

1995–2000,
and Health

vegetable-based and risk of cancer. These findings

up; USA

confirm the corroborated hypothesis that dietary pat-

Study

terns rich in fruit and vegetables may exert benefits

toward cancer risk, while high consumption of red/
Study design

processed meat may increase the risk of cancer.

Cohort

There is evidence from epidemiological studies on

dietary patterns that higher adherence to healthy diet-
Cancer site

ary patterns is associated with decreased risk of certain

Wirfalt, 2009 Colon/rectal
Table 1. Continued

cancers, especially gastrointestinal cancers and colorec-

tal adenoma (Magalhaes et al. 2012; Chen et al. 2016;
Godos et al. 2016a). Among popular dietary patterns,
Author, year

the Mediterranean diet is considered as a model of

healthy dietary pattern because of its peculiar characteris-
tics, including high consumption of plant-derived foods,
6 F. BELLA ET AL.
Figure 2. Forest plots of studies evaluating summary risk ratios for cancer between (a) high-meat versus plant-based, (b) plant-
based versus mixed foods, and (c) meat-based dietary versus mixed foods dietary patterns.
olive oil and fish as main source of fats and low intake
of meat, and has been associated with decreased risk of
cancer, including colorectal cancer (Grosso et al. 2014a;
Schwingshackl & Hoffmann 2015; D'Alessandro et al.
2016). Plant-based dietary patterns are rich of several
compounds that could play a role in the prevention of
cancer, for instance dietary fiber and antioxidants
(Turati et al. 2015). Among antioxidants, vitamins, pol-
yphenols and omega-3 PUFA are the best candidates to
be responsible of anti-inflammatory effects, protective
action toward DNA damage (through prevention of
oxidation) and improving cell signaling and cell cycle
regulation, which are biological pathways related to
cancer initiation (Grosso et al. 2013a; Fantini et al.
2015). As most of the existing evidence on the role of
nutrition and cancer risk is related to gastrointestinal
cancers, dietary fiber may exert a key role through a
direct action into the digestive tract by reducing transit
time and contact of carcinogens with the colonic
mucosa, increasing binding of carcinogens and produc-
tion of short-chain fatty acids (Grosso et al. 2013b).
In the present study, unhealthy dietary patterns
characterized by red and, especially, processed meat,
have been associated with increased risk of cancer.
Constituents of meat themselves, such as vitamin B,
vitamin A, zinc and iron, as well as proteins provide
important nutritional benefits. In contrast, meat has a
not negligible content in fat, including saturated fat
and cholesterol, which may play a role in increasing
the risk of certain cancers (Abid et al. 2014). Other
unhealthy factors have been hypothesized to be
responsible for the association between meat and can-
cer, including (i) heterocyclic amines (HCAs) and
polycyclic aromatic hydrocarbons (PAH) occurring
after cooking meat at high temperatures, and (ii) add-
ition of chemical preservatives such as sodium nitrite
(salt enriched with nitrates and nitrites) to increase its
durability, which leads to the formation of N-nitroso
compounds (NOC). From a mechanistic point of
view, meat may exerts its effects (i) locally, with con-
tact with the lumen in the case of gastrointestinal can-
cers; (ii) in target organs, through the hormone-like

Figure 3. Funnel plots of the analyses comparing high-meat versus plant-based, (b) plant-based versus mixed foods, and (c) meat-
based dietary versus mixed foods dietary patterns and risk of cancer.
properties of certain HCAs, which may differentially
affect organ normal functioning and homeostasis; and
(iii) at cellular level, activating/deactivating enzymes
across organs and tissues, which may either promote
or suppress carcinogenesis (Abid et al. 2014).
However, despite low meat intake can be associated
with lower cancer risk, there is no evidence on vege-
tarian diets that total depletion of animal sources of
protein from the diet lead to further decreased risk
(Godos et al. 2016 (ahead of print)).
Results of the present meta-analysis should be con-
sidered in light of some limitations. The main issue
relied on the observational nature of the studies
included, as most of them had a case-control design,
which may be affected by recall bias and confounding.
Moreover, heterogeneity in dietary patterns could lead
to study bias. Regarding the latter, a limitation of
exploring dietary habits and quality is the potential
confounding effect of the overall lifestyle and back-
ground of a person, including higher socioeconomic
status and education, which may lead to better access
to cure and health-related information (Rametta et al.
2013). Among the latter, higher nutrition knowledge
and health conscious choices, including, but not
INTERNATIONAL JOURNAL OF FOOD SCIENCES AND NUTRITION 7
limited to, better nutrition behaviors have been asso-
ciated with higher diet quality and lower metabolic
issues (De Vriendt et al. 2009; McLeod et al. 2011;
Grosso et al. 2013c; Jones & Zidenberg-Cherr 2015).
Indeed, healthy and unhealthy dietary habits are pri-
marily associated with body weight, which is an
independent risk factor for cancer risk (Grosso et al.
2014b; Godos et al. 2016b; Rodriguez-Monforte et al.
2016). Moreover, healthy and unhealthy lifestyle
choices tend to cluster, and thus, dietary choices
may be associated with smoking habit and physical
activity (Alvarez-Cubero et al. 2015). Overall, it is
difficult to isolate the effect of one factor from
another.
In conclusion, plant-based dietary patterns can be
considered a healthy choice over meat-based dietary
patterns. Future studies will provide additional evi-
dence and better investigate the potential causative
roles.
Disclosure statement
The authors report no conflicts of interest. The authors
alone are responsible for the content and writing of this
article.
8 F. BELLA ET AL.
ORCID
Justyna Godos http://orcid.org/0000-0002-5809-5706
References
Abid Z, Cross AJ, Sinha R. 2014. Meat, dairy, and cancer.
Am J Clin Nutr. 100:386S–393S.
Alvarez-Cubero MJ, Pascual-Geler M, Rivas A, Martinez-
Gonzalez LJ, Saiz M, Lorente JA, Cozar JM. 2015.
Lifestyle and dietary factors in relation to prostate cancer
risk. Int J Food Sci Nutr. 66:805–810.
Austin GL, Adair LS, Galanko JA, Martin CF, Satia JA,
Sandler RS. 2007. A diet high in fruits and low in meats
reduces the risk of colorectal adenomas. J Nutr. 137:
999–1004.
Bagnardi V, Rota M, Botteri E, Tramacere I, Islami F,
Fedirko V, Scotti L, Jenab M, Turati F, Pasquali E, et al.
2015. Alcohol consumption and site-specific cancer risk:
a comprehensive dose-response meta-analysis. Br J
Cancer. 112:580–593.
Bastos J, Lunet N, Peleteiro B, Lopes C, Barros H. 2010.
Dietary patterns and gastric cancer in a Portuguese urban
population. Int J Cancer. 127:433–441.
Bertuccio P, Rosato V, Andreano A, Ferraroni M, Decarli A,
Edefonti V, La Vecchia C. 2013. Dietary patterns and gas-
tric cancer risk: a systematic review and meta-analysis.
Ann Oncol. 24:1450–1458.
Bouvard V, Loomis D, Guyton KZ, Grosse Y, Ghissassi FE,
Benbrahim-Tallaa L, Guha N, Mattock H, Straif K,
International Agency for Research on Cancer Monograph
Working Group. 2015. Carcinogenicity of consumption of
red and processed meat. Lancet Oncol. 16:1599–1600.
Chen H, Ward MH, Graubard BI, Heineman EF, Markin
RM, Potischman NA, Russell RM, Weisenburger DD,
Tucker KL. 2002. Dietary patterns and adenocarcinoma
of the esophagus and distal stomach. Am J Clin Nutr.
75:137–144.
Chen J, Jiang W, Shao L, Zhong D, Wu Y, Cai J. 2016.
Association between intake of antioxidants and pancreatic
cancer risk: a meta-analysis. Int J Food Sci Nutr.
67:744–753.
D’Alessandro A, De Pergola G, Silvestris F. 2016.
Mediterranean diet and cancer risk: an open issue. Int J
Food Sci Nutr. 67:593–605.
De Vriendt T, Matthys C, Verbeke W, Pynaert I, De
Henauw S. 2009. Determinants of nutrition knowledge in
young and middle-aged Belgian women and the associ-
ation with their dietary behaviour. Appetite. 52:788–792.
Edefonti V, Randi G, Decarli A, La Vecchia C, Bosetti C,
Franceschi S, Dal Maso L, Ferraroni M. 2009a. Clustering
dietary habits and the risk of breast and ovarian cancers.
Ann Oncol. 20:581–590.
Edefonti V, Randi G, La Vecchia C, Ferraroni M, Decarli A.
2009b. Dietary patterns and breast cancer: a review with
focus on methodological issues. Nutr Rev. 67:297–314.
Fantini M, Benvenuto M, Masuelli L, Frajese GV, Tresoldi I,
Modesti A, Bei R. 2015. In vitro and in vivo antitumoral
effects of combinations of polyphenols, or polyphenols
and anticancer drugs: perspectives on cancer treatment.
Int J Mol Sci. 16:9236–9282.
Giacosa A, Barale R, Bavaresco L, Gatenby P, Gerbi V,
Janssens J, Johnston B, Kas K, La Vecchia C, Mainguet P,
et al. 2013. Cancer prevention in Europe: the
Mediterranean diet as a protective choice. Eur J Cancer
Prev. 22:90–95.
Godos J, Bella F, Sciacca S, Galvano F, Grosso G. 2016.
Vegetarianism and breast, colorectal, and prostate cancer
risk: an overview and meta-analysis of cohort studies. J
Hum Nutr Diet. [Epub ahead of print]. doi: 10.1111/
jhn.12426.
Godos J, Bella F, Torrisi A, Sciacca S, Galvano F, Grosso G.
2016a. Dietary patterns and risk of colorectal adenoma: a
systematic review and meta-analysis of observational
studies. J Hum Nutr Diet. 29:757–767.
Godos J, Zappala G, Bernardini S, Giambini I, Bes-
Rastrollo M, Martinez-Gonzalez M. 2016b. Adherence to
the Mediterranean diet is inversely associated with meta-
bolic syndrome occurrence: a meta-analysis of observa-
tional studies. Int J Food Sci Nutr. [Epub ahead of print].
doi: 10.1080/09637486.2016.1221900.
Grosso G, Bei R, Mistretta A, Marventano S, Calabrese G,
Masuelli L, Giganti MG, Modesti A, Galvano F, Gazzolo D.
2013a. Effects of vitamin C on health: a review of evidence.
Front Biosci (Landmark Ed). 18:1017–1029.
Grosso G, Biondi A, Galvano F, Mistretta A, Marventano S,
Buscemi S, Drago F, Basile F. 2014a. Factors associated
with colorectal cancer in the context of the
Mediterranean diet: a case-control study. Nutr Cancer.
66:558–565.
Grosso G, Buscemi S, Galvano F, Mistretta A, Marventano S,
La Vela V, Drago F, Gangi S, Basile F, Biondi A.
2013b. Mediterranean diet and cancer: epidemiological evi-
dence and mechanism of selected aspects. BMC Surg.
13:S14.
Grosso G, Mistretta A, Marventano S, Purrello A, Vitaglione P,
Calabrese G, Drago F, Galvano F. 2014b. Beneficial effects
of the Mediterranean diet on metabolic syndrome. Curr
Pharm Des. 20:5039–5044.
Grosso G, Mistretta A, Turconi G, Cena H, Roggi C,
Galvano F. 2013c. Nutrition knowledge and other deter-
minants of food intake and lifestyle habits in children
and young adolescents living in a rural area of Sicily,
South Italy. Public Health Nutr. 16:1827–1836.
Jones AM, Zidenberg-Cherr S. 2015. Exploring nutrition
education resources and barriers, and nutrition know-
ledge in teachers in California. J Nutr Educ Behav. 47:
162–169.
Kantor ED, Giovannucci EL. 2015. Gene-diet interactions
and their impact on colorectal cancer risk. Curr Nutr
Rep. 4:13–21.
Magalhaes B, Bastos J, Lunet N. 2011. Dietary patterns and
colorectal cancer: a case-control study from Portugal. Eur
J Cancer Prev. 20:389–395.
Magalhaes B, Peleteiro B, Lunet N. 2012. Dietary patterns
and colorectal cancer: systematic review and meta-ana-
lysis. Eur J Cancer Prev. 21:15–23.
Marventano S, Kolacz P, Castellano S, Galvano F, Buscemi S,
Mistretta A, Grosso G. 2015. A review of recent
evidence in human studies of n-3 and n-6 PUFA intake
on cardiovascular disease, cancer, and depressive disor-
ders: does the ratio really matter? Int J Food Sci Nutr. 66:
611–622.

McLeod ER, Campbell KJ, Hesketh KD. 2011. Nutrition
knowledge: a mediator between socioeconomic position
and diet quality in Australian first-time mothers. J Am
Diet Assoc. 111:696–704.
Mourouti N, Kontogianni MD, Papavagelis C, Panagiotakos
DB. 2015. Diet and breast cancer: a systematic review. Int
J Food Sci Nutr. 66:1–42.
Ogino S, Lochhead P, Chan AT, Nishihara R, Cho E,
Wolpin BM, Meyerhardt JA, Meissner A, Schernhammer
ES, Fuchs CS, Giovannucci E. 2013. Molecular patho-
logical epidemiology of epigenetics: emerging integrative
science to analyze environment, host, and disease. Mod
Pathol. 26:465–484.
Rametta S, Grosso G, Galvano F, Mistretta A, Marventano S,
Nolfo F, Buscemi S, Gangi S, Basile F, Biondi A. 2013.
Social disparities, health risk behaviors, and cancer. BMC
Surg. 13:S17.
Rodriguez-Monforte M, Sanchez E, Barrio F, Costa B,
Flores-Mateo G. 2016. Metabolic syndrome and dietary
patterns: a systematic review and meta-analysis of obser-
vational studies. Eur J Nutr. [Epub ahead of print]. doi:
10.1007/s00394-016-1305-y.
Rouillier P, Senesse P, Cottet V, Valleau A, Faivre J,
Boutron-Ruault MC. 2005. Dietary patterns and the
INTERNATIONAL JOURNAL OF FOOD SCIENCES AND NUTRITION 9
adenomacarcinoma sequence of colorectal cancer. Eur J
Nutr. 44:311–318.
Schwingshackl L, Hoffmann G. 2015. Adherence to
Mediterranean diet and risk of cancer: an updated sys-
tematic review and meta-analysis of observational studies.
Cancer Med. 4:1933–1947.
Turati F, Rossi M, Pelucchi C, Levi F, La Vecchia C. 2015.
Fruit and vegetables and cancer risk: a review of southern
European studies. Br J Nutr. 2:S102–S110.
Wells GASB, O’connell D, Peterson J, Welch V, Losos M,
Tugwell P. The Newcastle-Ottawa Scale (NOS) for assess-
ing the quality of nonrandomised studies in meta-analy-
ses. Proceedings of the Ottawa (Canada): Ottawa Health
Research Institute; 1999.
Wirfalt E, Midthune D, Reedy J, Mitrou P, Flood A, Subar
AF, Leitzmann M, Mouw T, Hollenbeck AR, Schatzkin A,
Kipnis V. 2009. Associations between food patterns
defined by cluster analysis and colorectal cancer incidence
in the NIH-AARP diet and health study. Eur J Clin Nutr.
63:707–717.
Wiseman M. 2008. The second World Cancer Research Fund/
American Institute for Cancer Research expert report.
Food, nutrition, physical activity, and the prevention of
cancer: a global perspective. Proc Nutr Soc. 67:253–256.