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Cancer Causes Control (2013) 24:11571165

DOI 10.1007/s10552-013-0195-z

ORIGINAL PAPER

Consumption of fruit, vegetables, and


other food groups and the risk of
nasopharyngeal carcinoma
Jerry Polesel Diego Serraino Eva Negri Luigi Barzan Emanuela
Vaccher Maurizio Montella Antonella Zucchetto Werner Garavello
Silvia Franceschi Carlo
La Vecchia Renato Talamini

Received: 11 October 2012 / Accepted: 20 March 2013 / Published online: 28 March 2013
Springer Science+Business Media Dordrecht 2013

Abstract
Purpose The role of dietary habits in the etiology of
nasopharyngeal carcinoma (NPC) has been extensively
investigated in high-incidence areas, but evidence is scanty
in low-incidence populations. This study aimed to investigate the relationship between NPC risk and a wide range
of food groups in the Italian population.
Methods We conducted a hospital-based casecontrol
study in Italy on 198, histologically confirmed, NPC cases
of Caucasian ethnicity, aged 1876 years. Controls were
594 Caucasian cancer-free patients admitted to general
hospitals for acute conditions. Odds ratios (ORs) and the
corresponding confidence intervals (CIs) were estimated
through logistic regression, adjusting for socio-demographic characteristics, tobacco smoking, alcohol drinking,
and energy intake.

Results Elevated vegetable consumption was inversely


related to NPC risk (OR for highest vs. lower quartile = 0.51; 95 % CI 0.290.90). The association was
particularly strong for yellow- or red-pigmented vegetables
(OR = 0.31; 95 % CI 0.180.54), and this effect was
stronger among never smokers (OR = 0.18; 95 % CI
0.060.55) than among ever smokers (OR = 0.37; 95 %
CI 0.190.71). Increased NPC risk emerged for elevated
eggs consumption (OR = 2.50; 95 % CI 1.444.32; ptrend
\0.01). No significant associations emerged between NPC
risk and consumption of cereals, meat, fish, dairy products,
and sweets.
Conclusions The study findings show that, also in lowrisk populations, vegetable consumption is a protective
factor against NPC. The stronger effect for yellow- or redpigmented vegetables is in agreement with the inverse
association reported for carotenoids intake.

J. Polesel (&) D. Serraino A. Zucchetto R. Talamini


Unit of Epidemiology and Biostatistics, Centro di Riferimento
OncologicoI, IRCCS, Via Franco Gallini, 2, 33081 Aviano, PN,
Italy
e-mail: polesel@cro.it

A. Zucchetto C. La Vecchia
Department of Clinical Sciences and Community Health,
Universita` degli Studi di Milano, Milan, Italy

E. Negri C. La Vecchia
Istituto di Ricerche Farmacologiche Mario Negri,
IRCCS, Milan, Italy
L. Barzan
Department of Head and Neck Surgery, Azienda Ospedaliera
Santa Maria degli Angeli, Pordenone, Italy

W. Garavello
Clinica Otorinolaringoiatrica DNTB, Universita` degli Studi di
Milano Bicocca, 20126 Milan, Italy
S. Franceschi
International Agency for Research on Cancer, Lyon, France

E. Vaccher
Division of Medical Oncology A, Centro di Riferimento
Oncologico, IRCCS, Aviano, Italy
M. Montella
Unit of Epidemiology, Istituto Tumori Fondazione Pascale,
IRCCS, 80125 Naples, Italy

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Keywords
Nasopharyngeal carcinoma Dietary habits

Food groups Vegetables Fruit


Introduction
Nasopharyngeal carcinoma (NPC) is rare in Europe and
North America, accounting for less than one percent of all
cancer cases [1]. In Europe, age-adjusted incidence rates
are generally below two cases/100,000 person-years
among men and below one case/100,000 among women
[1]. Conversely, it is frequent in China, in Southeastern
Asia, and in the Arctic region [2], as well as in migrants
from those areas [3], with incidence rates peaking at 30
cases/ 100,000 in men and at ten cases in women [1].
This peculiar geographic distribution reflects differences
in NPC pathology and epidemiology. In high-incidence
areas, undifferentiated carcinoma is by far the most
frequent NPC histological subtype [4], which has been
strongly associated to infection with EpsteinBarr virus
(EBV) [5]. Conversely, in low-incidence populations,
differentiated NPC represents an up to 25 % proportion of
all NPCs [4]. Well-established risk factors for head and
neck carcinomas (i.e., tobacco smoking and alcohol
drinking) appear to have a stronger effect on differentiated
NPC rather than undifferentiated ones [6, 7].
Evidence for the relationship between NPC risk and diet
is sparse, though generally consistent in showing a protective effect of non-starchy vegetables, fresh fruit [811],
red/yellow fruit, and vegetables [1215]. NPC risk was
also related to high consumption of preserved vegetables,
especially pickled ones [8, 11].
Although the role of dietary habits on NPC etiology has
been extensively investigated in high-incidence areas, the
peculiarity in these areas of some foods and of the methods
for cooking and preserving food hinders the broadening of
results to low-incidence countries [9, 16]. Only two U.S.
studies were conducted in low-incidence populations [14,
17], mainly focusing on fruit and vegetables. To provide
additional evidence for the relation between NPC and a
wide series of food groups in southern Europe, we
analyzed data from a casecontrol study conducted in
Italy.

Materials and methods


Between 1992 and 2008, we conducted a casecontrol
study on NPC within an established network of
collaborating cen- ters, including Aviano and Milan in
northern Italy and Naples and Catania in southern Italy [7,
18]. Overall, cases were 198 Caucasian patients aged 18
76 years (median age 52 years) with incident NPC,
admitted to major general hospitals in the study areas. All
198 NPC cases were histologically confirmed.

Cancer Causes Control (2013) 24:11571165

They included 137 (68.5 %) undifferentiated NPCs (WHO


type 3) [19], 23 (11.5 %) keratinizing squamous cell carcinomas (WHO type 1), and 40 (20.0 %) not otherwise
specified NPCs. EBV status was available for 61 NPC
cases based on the detection of EBV nuclear antigen
(EBNA) in tissue sam- ples. All 57 undifferentiated NPCs
and two out of four dif- ferentiated NPCs were EBVpositive.
Three controls were frequency-matched to each case,
according to sex, age, and place of living. The control
group included 594 Caucasian patients (aged 1976 years;
median age 52 years) admitted for a wide spectrum of
acute conditions to the same hospitals where cases had
been interviewed. Subjects admitted for malignant neoplasms, conditions related to tobacco smoking or alcohol
consumption, or any disorder that might have induced
long-term modification of diet were excluded from the
control group. Controls were admitted for traumas (34 %),
other orthopedic disorders (32 %), acute surgical conditions (22 %), and miscellaneous other illnesses, including
eye, nose, ear, skin, or dental disorders (12 %). All study
participants signed an informed consent, according to the
recommendations of the boards of ethics of the study
hospitals.
Trained interviewers administered a structured questionnaire to cases and controls during their hospital stays,
thus keeping refusal below 3 %. The questionnaire collected information on socio-demographic factors, lifestyle
habits, smoking and drinking habits, a problem-oriented
medical history, and family history of cancer.
The subjects usual diet during the 2 years prior to
cancer diagnosis (or hospital admission for controls) was
investigated through a food-frequency
questionnaire
(FFQ), which included 78 foods or recipes, structured into
six sections: (1) milk, yoghurt, coffee, tea, sugar, and
artificial sweeteners; (2) bread and cereals (first courses);
(3) meat and foods used as meat substitutes (second
courses); (4) vegetables (side dishes); (5) fruit; and (6)
chocolate and candies, desserts, and soft drinks. An additional section assessed lifelong use of alcoholic beverages.
Patients were asked to indicate the average weekly consumption of several dietary items; intakes lower than once
a week, but at least once a month, were coded as 0.5 per
week. Serving size was defined either in natural units
(e.g., one apple, one orange) or as an average serving in the
Italian diet (e.g., 100 g of salad; 150 g of tomatoes; 125 g
of boiled potatoes). Food items were grouped into food
groups according to similarities of nutritional properties
[20]. For fruit and vegetables subject to seasonal variation,
consumption in season and the corresponding duration
were elicited. The questionnaire was successfully tested for
reproducibility [21] and validity [22]. The FFQ did not
include specific items for preserved fruit, preserved vegetables, salted meat, and salted fish, but their consumption is

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