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International Journal of Food Sciences and Nutrition

ISSN: 0963-7486 (Print) 1465-3478 (Online) Journal homepage: http://www.tandfonline.com/loi/iijf20

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

To link to this article: http://dx.doi.org/10.1080/09637486.2016.1261087

Published online: 28 Nov 2016.

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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


content of processed fat foods, alcoholic beverages and
Cancer represents a group of more than a hundred of
sweets, are major source of trans-fatty acids, alcohol
conditions characterized by uncontrolled cell growth,
and refined carbohydrates, which may be related with
invasion in adjacent tissues and various grade of loss
increased risk of cancer (Wiseman 2008; Bagnardi et al.
of differentiation. The initiating process that result in
2015; Bouvard et al. 2015).
the alteration of the genetic information of the cells is,
Dietary patterns are able to capture various aspects
in most of cases, the result of damages accumulated
of diet adopted by a population and may provide
over time secondary to endogen or external stimula: insights on the synergistic effect of several components
the latter include smoking habits, infectious organisms, (Edefonti et al. 2009b). A number of observational
exposure to chemicals and diet composition, which in studies have been conducted on a posteriori empiric-
turn may affect cellular processes linked to cancer, such ally-derived dietary patterns: results were based on the
as DNA repair, cell proliferation and differentiation, association between the highest adherence to a dietary
cell cycle control, hormonal regulation, inflammation pattern compared with lowest, showing that higher
and immune function and carcinogen metabolism adherence to healthy and prudent dietary patterns
(Ogino et al. 2013; Kantor & Giovannucci 2015). were more likely to be associated with lower cancer
Among the others, diet has been considered the focus risk while higher adherence to so-called “Western”
of interest over the last 50 years for its potential role in and unhealthy dietary patterns was associated with
preventing cancer (Mourouti et al. 2015). Dietary pat- increased risk of cancer, especially gastrointestinal
terns with high content of fruit and vegetable are cancers (Magalhaes et al. 2012; Bertuccio et al. 2013).
important source of fiber and antioxidant compounds, However, no summary analysis of current evidence of
including polyphenolic compounds and healthy fatty studies directly comparing the association with cancer
acids [mono- and polyunsaturated fatty acids (MUFA risk between dietary patterns was performed. The aim
and PUFA, respectively)], which may have beneficial of the present study was to provide an overview and
effects toward cancer risk (Giacosa et al. 2013; 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 I2 statistic. The level of significance for the Q test was
cancer risk. 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-
Methods
eity. Sensitivity analyzes by excluding one study at the
Study search time were conducted. When data were sufficient to
A systematic search on PubMed (http://www.ncbi.nlm. perform subgroup analyses, we considered whether
nih.gov/pubmed/) and EMBASE (http://www.embase. differences by gender and cancer localization existed.
com/) databases of English language studies published Publication bias was evaluated by a visual investigation
up to March 2016 was performed. Search terms of funnel plots for potential asymmetry. All analyzes
included a combination of keywords, such as “dietary were performed with Review Manager (RevMan) soft-
pattern” and “cancer” and their variants. Inclusion cri- ware version 5.2 (The Nordic Cochrane Center, The
teria were the following: (i) having an observational Cochrane Collaboration).
(case-control or prospective) study design; (ii) evaluat-
ing the association with risk of cancer between a pos- Results
teriori derived dietary patterns based on principal
Study characteristics
component analysis (PCA) or cluster analysis; (iii)
assessed and reported a measure of association for the Out of the 219 unique citations, 71 were excluded
outcome considered as odds ratios (ORs) or hazard after abstract examination and 141 were excluded after
ratios (HRs) and the corresponding 95% confidence full-text reading for the following reasons: 35 studies
intervals (CIs). Reference lists of included studies were explored a priori dietary patterns; four studies explored
scrutinized for any article not previously identified. cancer survival; and 102 studies compared the level of
The article selection process was independently per- adherence within dietary patterns (Figure 1). This selec-
formed by two authors. 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.
Data extraction and study quality assessment
2009a; Wirfalt et al. 2009; Bastos et al. 2010; Magalhaes
Data were extracted from selected studies by using a et al. 2011). The main characteristics of the studies
standardized extraction form. The following informa- included are presented in Table 1: case–control studies
tion was collected: (i) author name; (ii) year of publi- (Chen et al. 2002; Rouillier et al. 2005; Austin et al.
cation; (iii) cohort name, length of follow-up, country; 2007; Edefonti et al. 2009a; Bastos et al. 2010;
(iv) number, gender, and age of participants and cases; Magalhaes et al. 2011) accounted for a total of 5042
(v) reference category and OR/HR and 95% CI for the cases and 5516 controls; the prospective study (Wirfalt
categories of exposure; and (vi) covariates used in et al. 2009) included 492,306 individuals and 3135 cases.
adjustments. Most of the studies were conducted on colorectal cancer
The Newcastle–Ottawa Quality Assessment Scale (Rouillier et al. 2005; Austin et al. 2007; Wirfalt et al.
was used to assess the quality of each study (Wells 2009; Magalhaes et al. 2011), two on gastric and esopha-
1999). The instrument consists of 3 domains indicat- geal cancers (Chen et al. 2002; Bastos et al. 2010), and
ing the study quality as follows: selection (4 points), one on breast and ovarian cancers (Edefonti et al.
comparability (2 points), and outcome (3 points) for a 2009a). All studies adjusted for variables potentially
total score of 9 points (9 representing the highest related with cancer incidence, including gender, body
quality). Studies scoring 7–9 points, 3–6 points and mass index, smoking status, physical activity, energy
0–3 points were identified as high, medium and low intake and hormonal and parity status in women. Study
quality, respectively. quality was high for most of the studies included in the
analyses.
Statistical analysis
Dietary patterns
Random-effects models were used to calculate risk
ratios (RRs) with 95% CIs for various categories of All studies used food frequency questionnaires to
exposure. The risk estimate from the most fully explore the dietary consumption of participants. In all
adjusted models in the analysis of the pooled RR was studies, dietary patterns were identified with PCA and
used. Heterogeneity was assessed using the Q test and cluster analysis: four studies compared dietary patterns
INTERNATIONAL JOURNAL OF FOOD SCIENCES AND NUTRITION 3

characterized by high meat intake with those high in heterogeneity was due to one study, after exclusion of
fruits and vegetables (Chen et al. 2002; Austin et al. which the summary risk estimates remained significant
2007; Bastos et al. 2010; Magalhaes et al. 2011); three with no evidence of heterogeneity (RR ¼1.88, 95% CI:
studies considered as category of reference dietary pat- 1.38, 2.58; I2 ¼ 0%, Pheterogeneity ¼ 0.59). A subgroup ana-
terns with no specific characterization or extreme con- lyzes based on cancer localization showed that the study
sumption of particular foods, which compared with conducted on upper digestive tract reported non-signifi-
patterns high in plant-foods and animal-foods cant summary risk estimates (RR ¼1.77, 95% CI: 0.59,
(Rouillier et al. 2005; Edefonti et al. 2009a; Wirfalt 5.33; I2 ¼ 76%, Pheterogeneity ¼ 0.02) while those conducted
et al. 2009) (Table 1). 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%,
High-meat versus plant-based dietary patterns Pheterogeneity ¼ 0.55).
and cancer risk
The association of high-meat compared to plant-based
Plant-based versus mixed food patterns and
dietary patterns and cancer risk was explored in four
cancer risk
studies (Chen et al. 2002; Austin et al. 2007; Bastos
et al. 2010; Magalhaes et al. 2011) including 1794 indi- Seven datasets from three studies (Rouillier et al. 2005;
viduals and 1271 cases (Figure 2a): the analysis based Edefonti et al. 2009a; Wirfalt et al. 2009) were ana-
on six datasets showed an increased risk of cancer for lyzed to test the association plant-based compared to
adoption of the former compared with the latter pattern dietary patterns with various foods and cancer risk
(RR ¼1.64, 95% CI: 1.02, 2.63) with significant evidence (Figure 2b). The studies comprised the cohort study
of heterogeneity (I2 ¼ 69%, Pheterogeneity ¼ 0.007) and and 3771 total cases and 3722 controls from case–con-
asymmetry of funnel plot (Figure 3a). A sensitivity ana- trol studies on colon, rectum, breast and ovarian can-
lysis by exclusion of one study at the time revealed that cers. The analysis showed a significant lower risk of

Figure 1. Study selection flow chart.


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 In the present study, unhealthy dietary patterns
of meat, and has been associated with decreased risk of characterized by red and, especially, processed meat,
cancer, including colorectal cancer (Grosso et al. 2014a; have been associated with increased risk of cancer.
Schwingshackl & Hoffmann 2015; D'Alessandro et al. Constituents of meat themselves, such as vitamin B,
2016). Plant-based dietary patterns are rich of several vitamin A, zinc and iron, as well as proteins provide
compounds that could play a role in the prevention of important nutritional benefits. In contrast, meat has a
cancer, for instance dietary fiber and antioxidants not negligible content in fat, including saturated fat
(Turati et al. 2015). Among antioxidants, vitamins, pol- and cholesterol, which may play a role in increasing
yphenols and omega-3 PUFA are the best candidates to the risk of certain cancers (Abid et al. 2014). Other
be responsible of anti-inflammatory effects, protective unhealthy factors have been hypothesized to be
action toward DNA damage (through prevention of responsible for the association between meat and can-
oxidation) and improving cell signaling and cell cycle cer, including (i) heterocyclic amines (HCAs) and
regulation, which are biological pathways related to polycyclic aromatic hydrocarbons (PAH) occurring
cancer initiation (Grosso et al. 2013a; Fantini et al. after cooking meat at high temperatures, and (ii) add-
2015). As most of the existing evidence on the role of ition of chemical preservatives such as sodium nitrite
nutrition and cancer risk is related to gastrointestinal (salt enriched with nitrates and nitrites) to increase its
cancers, dietary fiber may exert a key role through a durability, which leads to the formation of N-nitroso
direct action into the digestive tract by reducing transit compounds (NOC). From a mechanistic point of
time and contact of carcinogens with the colonic view, meat may exerts its effects (i) locally, with con-
mucosa, increasing binding of carcinogens and produc- tact with the lumen in the case of gastrointestinal can-
tion of short-chain fatty acids (Grosso et al. 2013b). cers; (ii) in target organs, through the hormone-like
INTERNATIONAL JOURNAL OF FOOD SCIENCES AND NUTRITION 7

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 limited to, better nutrition behaviors have been asso-
affect organ normal functioning and homeostasis; and ciated with higher diet quality and lower metabolic
(iii) at cellular level, activating/deactivating enzymes issues (De Vriendt et al. 2009; McLeod et al. 2011;
across organs and tissues, which may either promote Grosso et al. 2013c; Jones & Zidenberg-Cherr 2015).
or suppress carcinogenesis (Abid et al. 2014). Indeed, healthy and unhealthy dietary habits are pri-
However, despite low meat intake can be associated marily associated with body weight, which is an
with lower cancer risk, there is no evidence on vege- independent risk factor for cancer risk (Grosso et al.
tarian diets that total depletion of animal sources of 2014b; Godos et al. 2016b; Rodriguez-Monforte et al.
protein from the diet lead to further decreased risk 2016). Moreover, healthy and unhealthy lifestyle
(Godos et al. 2016 (ahead of print)). choices tend to cluster, and thus, dietary choices
Results of the present meta-analysis should be con- may be associated with smoking habit and physical
sidered in light of some limitations. The main issue activity (Alvarez-Cubero et al. 2015). Overall, it is
difficult to isolate the effect of one factor from
relied on the observational nature of the studies
another.
included, as most of them had a case-control design,
In conclusion, plant-based dietary patterns can be
which may be affected by recall bias and confounding.
considered a healthy choice over meat-based dietary
Moreover, heterogeneity in dietary patterns could lead
patterns. Future studies will provide additional evi-
to study bias. Regarding the latter, a limitation of
dence and better investigate the potential causative
exploring dietary habits and quality is the potential roles.
confounding effect of the overall lifestyle and back-
ground of a person, including higher socioeconomic
status and education, which may lead to better access Disclosure statement
to cure and health-related information (Rametta et al. The authors report no conflicts of interest. The authors
2013). Among the latter, higher nutrition knowledge alone are responsible for the content and writing of this
and health conscious choices, including, but not article.
8 F. BELLA ET AL.

ORCID Giacosa A, Barale R, Bavaresco L, Gatenby P, Gerbi V,


Janssens J, Johnston B, Kas K, La Vecchia C, Mainguet P,
Justyna Godos http://orcid.org/0000-0002-5809-5706 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.
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