Wo ld Jou nal o
Gas oen e ology
ISSN 1007-9327 (p in )
ISSN 2219-2840 (online)
Wo ld J Gas oen e ol 2020 July 28; 26(28): 3998-4181
Published by Baishideng Publishing G oup Inc
WJG h ps://www.wjgne .com IJuly 28, 2020 Volume 26 Issue 28
Wo ld Jou nal o
Gas oen e ology
W J G
Con en s Weekly Volume 26 Numbe 28 July 28, 2020
REVIEW
Seconda y causes o in lamma o y bowel diseases
3998
Ghou i YA, Tahan V, Shen B
Clinical conside a ions in he managemen o non-alcoholic s ea ohepa i is ci hosis p e- and pos -
ansplan : A mul i-sys em challenge
4018
S egge da JA, Mahend a aj K, Todo T, Nou eddin M
Panc ea ic neu oendoc ine umo s: The apeu ic challenges and esea ch limi a ions
4036
Mpilla GB, Philip PA, El-Rayes B, Azmi AS
Di e en ial egula ion o JAK/STAT-signaling in pa ien s wi h ulce a i e coli is and C ohn’s disease
4055
Co des F, Foell D, Ding JN, Va ga G, Be enwo h D
MINIREVIEWS
Helicobac e pylo i in ec ion: Beyond gas ic mani es a ions
4076
San os MLC, de B i o BB, da Sil a FAF, Sampaio MM, Ma ques HS, Oli ei a e Sil a N, de Magalhães Quei oz DM, de
Melo FF
ORIGINAL ARTICLE
Basic S udy
Celecoxib a enua es hepa ocy e apop osis by inhibi ing endoplasmic e iculum s ess in hioace amide-
induced ci ho ic a s
4094
Su W, Tai Y, Tang SH, Ye YT, Zhao C, Gao JH, Tuo BG, Tang CW
Case Con ol S udy
Food g oups, die quali y and colo ec al cance isk in he Basque Coun y
4108
Aleg ia-Le xundi I, Agui e C, Bujanda L, Fe nández FJ, Polo F, O do ás JM, E xeza aga MC, Zabalza I, La zabal M,
Po illo I, de Panco bo MM, Ga cia-E xeba ia K, Rocandio AM, A oyo-Izaga M
Re ospec i e S udy
P ima y scle osing cholangi is associa ed coli is: Cha ac e iza ion o clinical, his ologic ea u es, and hei
associa ions wi h li e ansplan a ion
4126
A anake-Ch isinge J, Dassopoulos T, Yan Y, Nalban oglu I
Insulin ecep o subs a e 1 may play di e gen oles in human colo ec al cance de elopmen and
p og ession
4140
Lompe a K, Jakubowska K, G udzinska M, Kanczuga-Koda L, Wincewicz A, Su macz E, Sulkowski S, Koda M
WJG h ps://www.wjgne .com II July 28, 2020 Volume 26 Issue 28
Wo ld Jou nal o Gas oen e ology
Con en s Weekly Volume 26 Numbe 28 July 28, 2020
Enhancemen pa ame e s o con as -enhanced compu ed omog aphy o panc ea ic duc al
adenoca cinoma: Co ela ion wi h pa hologic g ading
4151
Seo W, Kim YC, Min SJ, Lee SM
Obse a ional S udy
De ec ion o e lux-symp om associa ion in child en wi h esophageal a esia by ideo-pH-impedance
s udy
4159
Mahola nkij S, Sanpa a A, Decha un K, Dum isilp T, Tubja eon C, Kanghom B, Pa cha a akul T, Chaiji a uch N,
Chongs isawa V, Sin usek P
Randomized Con olled T ial
Epigas ic pain synd ome: Wha can adi ional Chinese medicine do? A andomized con olled ial o
Biling Wei ong G anules
4170
Wen YD, Lu F, Zhao YP, Wang P, Yang Q, Li JX, Li HZ, Chi LL, Zhou ZH, Tang YP, Xu JK, Zhao Y, Tang XD
WJG h ps://www.wjgne .com III July 28, 2020 Volume 26 Issue 28
Wo ld Jou nal o Gas oen e ology
Con en s Weekly Volume 26 Numbe 28 July 28, 2020
ABOUT COVER
Edi o ial boa d membe o Wo ld Jou nal o Gas oen e ology, D . Osamu Toyoshima is a Di ec o o Toyoshima
Endoscopy Clinic in Tokyo, Japan. D . Toyoshima g adua ed om he Uni e si y o Tokyo wi h his mas e ´s
deg ee in Medicine. A e g adua ing, he joined he Depa men o Gas oen e ology and Su gical Oncology a he
Uni e si y o Tokyo Hospi al and engaged in clinical p ac ice and medical esea ch. A e ha , he es ablished he
Toyoshima Endoscopy Clinic wi h his a he , D . Hi oshi Toyoshima. Toyoshima Endoscopy Clinic is an
endoscopy-specialized clinic, which pe o ms 10000 endoscopies annually. D . Osamu Toyoshima mainly conduc s
esea ch using clinical da a om Toyoshima Endoscopy Clinic. He is an expe in he ield o gas oen e ology,
especially o gas ic cance isk e alua ion based on he endoscopic gas i is and o quali y indica o s o
colonoscopy such as colo ec al polyp de ec ion.
AIMS AND SCOPE
The p ima y aim o Wo ld Jou nal o Gas oen e ology (WJG, Wo ld J Gas oen e ol) is o p o ide schola s and eade s
om a ious ields o gas oen e ology and hepa ology wi h a pla o m o publish high-quali y basic and clinical
esea ch a icles and communica e hei esea ch indings online. WJG mainly publishes a icles epo ing esea ch
esul s and indings ob ained in he ield o gas oen e ology and hepa ology and co e ing a wide ange o opics
including gas oen e ology, hepa ology, gas oin es inal endoscopy, gas oin es inal su ge y, gas oin es inal
oncology, and pedia ic gas oen e ology.
INDEXING/ABSTRACTING
The WJG is now indexed in Cu en Con en s®/Clinical Medicine, Science Ci a ion Index Expanded (also known as
SciSea ch®), Jou nal Ci a ion Repo s®, Index Medicus, MEDLINE, PubMed, PubMed Cen al, and Scopus. The 2020
edi ion o Jou nal Ci a ion Repo ® ci es he 2019 impac ac o (IF) o WJG as 3.665; IF wi hou jou nal sel ci es:
3.534; 5-yea IF: 4.048; Ranking: 35 among 88 jou nals in gas oen e ology and hepa ology; and Qua ile ca ego y:
Q2.
RESPONSIBLE EDITORS FOR THIS ISSUE
Elec onic Edi o : Yan-Liang Zhang; P oduc ion Depa men Di ec o : Yun-Xiaojian Wu; Edi o ial O ice Di ec o : Ze-Mao Gong.
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WJG h ps://www.wjgne .com 4108 July 28, 2020 Volume 26 Issue 28
Wo ld Jou nal o
Gas oen e ology
W J G
Submi a Manusc ip : h ps://www. 6publishing.com Wo ld J Gas oen e ol 2020 July 28; 26(28): 4108-4125
DOI: 10.3748/wjg. 26.i28.4108 ISSN 1007-9327 (p in ) ISSN 2219-2840 (online)
ORIGINAL ARTICLE
Case Con ol S udy
Food g oups, die quali y and colo ec al cance isk in he Basque
Coun y
Ike Aleg ia-Le xundi, Ca melo Agui e, Luis Bujanda, F ancisco J Fe nández, F ancisco Polo, José Mª
O do ás, Mª Ca men E xeza aga, Iñaki Zabalza, Mikel La zabal, Isabel Po illo, Ma ian M de Panco bo,
Koldo Ga cia-E xeba ia, Ana Mª Rocandio, Ma a A oyo-Izaga
ORCID numbe : Ike Aleg ia-
Le xundi 0000-0002-6702-9209;
Ca melo Agui e 0000-0003-3555-
1550; Luis Bujanda 0000-0002-4353-
9968; F ancisco J Fe nández 0000-
0002-2230-2806; F ancisco Polo
0000-0003-3305-1210; José Mª
O do ás 0000-0002-7581-5680; Mª
Ca men E xeza aga 0000-0002-4960-
9429; Iñaki Zabalza 0000-0001-7892-
4447; Isabel Po illo 0000-0002-3871-
3423; Ma ian M de Panco bo 0000-
0002-8081-0702; Koldo Ga cia-
E xeba ia 0000-0002-6107-9416; Ana
Mª Rocandio 0000-0002-7803-8039;
Ma a A oyo-Izaga 0000-0001-5592-
4241.
Au ho con ibu ions: A oyo-Izaga
M, de Panco bo MM, Agui e C,
Aleg ia-Le xundi I, Bujanda L,
Fe nández FJ, Polo F, E xeza aga
MC, Zabalza I, La zabal M,
Rocandio AM, Ga cia-E xeba ia K
and Po illo I con ibu ed o he
concep ion, design and da a
acquisi ion; A oyo-Izaga M,
Aleg ia-Le xundi I and O do ás
JM analysed he da a, in e p e ed
he esul s, and d a ed he
manusc ip ; and all he au ho s
c i ically e ised he pape and
app o ed he inal e sion o he
manusc ip .
Suppo ed by he Depa men o
Heal h and Consume A ai s,
Ike Aleg ia-Le xundi, Ma a A oyo-Izaga, Depa men o Pha macy and Food Sciences, Facul y
o Pha macy, Uni e si y o he Basque Coun y UPV/EHU, Vi o ia-Gas eiz 01006, Spain
Ca melo Agui e, Pha maco igilance Uni , Galdakao-Usansolo Uni e si y Hospi al, Osakide za,
Galdakao 48960, Spain
Luis Bujanda, Depa men o Gas oen e ology, Donos ia Uni e si y Hospi al / Biodonos ia,
Uni e si y o he Basque Coun y UPV/EHU, Cen o de In es igación Biomédica en Red de
En e medades Hepá icas y Diges i as (CIBERehd), San Sebas ian 20014, Spain
F ancisco J Fe nández, Depa men o Gas oen e ology, Galdakao-Usansolo Uni e si y
Hospi al, Osakide za, Galdakao 48960, Spain
F ancisco Polo, Depa men o Gas oen e ology, Basu o Uni e si y Hospi al, Osakide za,
Bilbao 48013, Spain
José Mª O do ás, Nu i ion and Genomics Labo a o y, Jean Maye Human Nu i ion Resea ch
Cen e on Aging, Tu s Uni e si y, Bos on, Massachuse s 02111, Uni ed S a es o Ame ica;
IMDEA Food, Mad id 28049, Spain
Mª Ca men E xeza aga, Depa men o Pa hology, Basu o Uni e si y Hospi al, Osakide za,
Bilbao 48013, Spain; Depa men o Physician and Su geon Speciali ies, Uni e si y o he
Basque Coun y UPV/EHU, Leioa 48940, Spain
Iñaki Zabalza, Depa men o Pa hology, Galdakao-Usansolo Uni e si y Hospi al, Osakide za,
Galdakao 48960, Spain
Mikel La zabal, Depa men o Pa hology, Donos ia Hospi al / Biodonos ia, Cen o de
In es igación Biomédica en Red de En e medades Hepá icas y Diges i as (CIBERehd), San
Sebas ian 20014, Spain
Isabel Po illo, Colo ec al cance sc eening p og amme, Osakide za, Bilbao 48011, Spain
Ma ian M de Panco bo, Ana Mª Rocandio, BIOMICs Resea ch G oup, Uni e si y o he Basque
Coun y UPV/EHU, Vi o ia-Gas eiz 01006, Spain
Koldo Ga cia-E xeba ia, Biodonos ia, Gas oin es inal gene ics g oup, Cen o de In es igación
Biomédica en Red de En e medades Hepá icas y Diges i as (CIBERehd), San Sebas ian 20014,
Aleg ia-Le xundi I e al. Die and colo ec al cance isk
WJG h ps://www.wjgne .com 4109 July 28, 2020 Volume 26 Issue 28
Basque Go e nmen , No.
2011111153; Saio ek, Basque
Go e nmen , No. S-PE12UN058;
P e-doc o al g an om he Basque
Go e nmen , No.
PRE_2015_2_0084; and Uni ed
S a es Depa men o Ag icul u e—
Ag icul u al Resea ch Se ice, No.
58-1950-4-003.
Ins i u ional e iew boa d
s a emen : This s udy was
app o ed by he Clinical Resea ch
E hics Commi ee o he Basque
Coun y ( e e ence numbe s
PI2011006 and PI2014042).
In o med consen s a emen :
W i en in o med consen was
ob ained om all he s udy
pa icipan s.
Con lic -o -in e es s a emen : No
bene i s in any o m ha e been
ecei ed o will be ecei ed om a
comme cial pa y ela ed di ec ly
o indi ec ly o he subjec o his
a icle.
Da a sha ing s a emen : Da ase
a ailable om he co esponding
au ho a [email p o ec ed].
STROBE s a emen : The au ho s
ha e ead he STROBE S a emen -
checklis o i ems, and he
manusc ip was p epa ed and
e ised acco ding o he STROBE
S a emen -checklis o i ems.
Open-Access: This a icle is an
open-access a icle ha was
selec ed by an in-house edi o and
ully pee - e iewed by ex e nal
e iewe s. I is dis ibu ed in
acco dance wi h he C ea i e
Commons A ibu ion
NonComme cial (CC BY-NC 4.0)
license, which pe mi s o he s o
dis ibu e, emix, adap , build
upon his wo k non-comme cially,
and license hei de i a i e wo ks
on di e en e ms, p o ided he
o iginal wo k is p ope ly ci ed and
he use is non-comme cial. See: h
p://c ea i ecommons.o g/licenses
/by-nc/4.0/
Manusc ip sou ce: In i ed
manusc ip
Recei ed: Feb ua y 28, 2020
Pee - e iew s a ed: Feb ua y 28,
Spain
Co esponding au ho : Ma a A oyo-Izaga, Pha mD, Depa men o Pha macy and Food
Sciences, Facul y o Pha macy, Uni e si y o he Basque Coun y UPV/EHU, Paseo de la
Uni e sidad, No. 7, Vi o ia-Gas eiz 01006, Spain. [email p o ec ed]
Abs ac
BACKGROUND
The esul s ob ained o da e conce ning ood g oups, die quali y and colo ec al
cance (CRC) isk a y acco ding o c i e ia used and he s udy popula ions.
AIM
To s udy he ela ionships be ween ood g oups, die quali y and CRC isk, in an
adul popula ion o he Basque Coun y (No h o Spain).
METHODS
This obse a ional s udy included 308 pa ien s diagnosed wi h CRC and 308 age-
and sex-ma ched subjec s as con ols. Du ing ec ui men , die a y,
an h opome ic, li es yle, socioeconomic, demog aphic and heal h s a us
in o ma ion was collec ed. Adhe ence o he die a y ecommenda ions was
e alua ed u ilizing he Heal hy Ea ing Index o he Spanish Die and he
MedDie Sco e. Condi ional logis ic eg essions we e used o e alua e he
associa ions o ood g oup in akes, die quali y sco es, ca ego ized in e iles, wi h
CRC isk.
RESULTS
The adjus ed models o po en ial con ounding ac o s showed a di ec associa ion
be ween milk and dai y p oduc s consump ion, in pa icula high- a cheeses
[odds a io (OR) hi d e ile s i s e ile = 1.87, 95% con idence in e als (CI):
1.11-3.16], and CRC isk. While he consump ion o ibe -con aining oods,
especially whole g ains (OR hi d e ile s i s e ile = 0.62, 95%CI: 0.39-0.98),
and a y ish (OR hi d e ile s i s e ile = 0.53, 95%CI: 0.27-0.99) was
associa ed wi h a lowe isk o CRC. Mo eo e , highe MD adhe ence was
associa ed wi h a educed CRC isk in adjus ed models (OR hi d e ile s i s
e ile = 0.40, 95%CI: 0.20-0.80).
CONCLUSION
Di ec associa ions we e ound o high- a cheese, whe eas an in e se ela ion
was epo ed o ibe -con aining oods and a y ish, as well as adhe ence o a
Medi e anean die a y pa e n.
Key wo ds: Colo ec al cance ; Food g oup; Die a y quali y; Medi e anean die ; Risk-
ac o s; Case-con ol s udy
©The Au ho (s) 2020. Published by Baishideng Publishing G oup Inc. All igh s ese ed.
Co e ip: This ma ched case-con ol s udy suppo s he ole o die in colo ec al cance
(CRC) isk. The esul s sugges ha high consump ion o high- a cheeses is associa ed
wi h CRC isk, whe eas, a high in ake o ibe -con aining oods, especially whole g ains,
and a y ish, as well as adhe ence o he Medi e anean die a y pa e n, was associa ed
wi h a lowe isk o CRC. Fu u e s udies a e needed o be e unde s and he in luence o
he die a y habi s on CRC p e en ion in his popula ion ha can p o ide leads o he
design and ailo ing o u u e in e en ions, and guide counselling s a egies o p omo ing
a heal hy li es yle.
Ci a ion: Aleg ia-Le xundi I, Agui e C, Bujanda L, Fe nández FJ, Polo F, O do ás JM,
E xeza aga MC, Zabalza I, La zabal M, Po illo I, de Panco bo MM, Ga cia-E xeba ia K,
Rocandio AM, A oyo-Izaga M. Food g oups, die quali y and colo ec al cance isk in he
Basque Coun y. Wo ld J Gas oen e ol 2020; 26(28): 4108-4125
Aleg ia-Le xundi I e al. Die and colo ec al cance isk
WJG h ps://www.wjgne .com 4110 July 28, 2020 Volume 26 Issue 28
2020
Fi s decision: Ma ch 21, 2020
Re ised: Ap il 3, 2020
Accep ed: July 16, 2020
A icle in p ess: July 16, 2020
Published online: July 28, 2020
P-Re iewe : Bo dona o M,
Khajehei M
S-Edi o : Zhang L
L-Edi o : A
E-Edi o : Zhang YL
URL: h ps://www.wjgne .com/1007-9327/ ull/ 26/i28/4108.h m
DOI: h ps://dx.doi.o g/10.3748/wjg. 26.i28.4108
INTRODUCTION
Colo ec al cance (CRC) is a majo public heal h challenge wo ldwide. CRC is he
hi d-mos commonly diagnosed malignancy and he ou h leading cause o cance
dea hs in he wo ld, accoun ing o app oxima ely 1.8 million new cases and almos
900000 dea hs in 2018[1]. In Eu ope, CRC is he leading malignancy in e ms o
incidence and he second in mo ali y in bo h sexes[2]. CRC is linked o wes e n
li es yles, in pa icula , o die , physical inac i i y, smoking, alcohol consump ion, and
body weigh [3,4].
Epidemiological e idence sugges s ha die a y ac o s may bo h p o ec agains and
p omo e he de elopmen o CRC. A comp ehensi e e iew[5] shows obus e idence
abou he p o ec i e ole o die a y ibe . O he oods, such as milk o ga lic, also may
be p o ec i e. Con e sely, ed mea and p ocessed mea in ake and alcoholic d inks
inc ease CRC isk. This ood g oup app oach has he ad an age o educing some o
he p oblems inhe en o analyses o nu ien in ake (e.g., inaccu acy and
incomple eness o ood-composi ion ables). Fu he mo e, i o e s an ad an age om
a p e en i e pe spec i e since ood g oup esul s a e easie o ans o m in o die a y
ecommenda ions han hose o nu ien s[6].
In his ega d, oods a e no consumed in isola ion bu as pa o a die a y pa e n;
he e o e, he ac ual e ec o die on disease isk may be obse ed only when all
componen s a e conside ed join ly[6]. Fo his pu pose, se e al die quali y indexes
ha e been de eloped using poin sys ems o measu e whole die quali y based on he
alignmen o ood choices wi h die a y ecommenda ions. Some o hese indices ha e
been used o begin assessing he ela ionships be ween o e all die quali y and CRC
isk, and he esul s show ha high sco es in hese indices a e associa ed wi h a lowe
CRC isk[7-10]. Howe e , he esul s a y conside ably acco ding o he index used and
o he ac o s such as sex and age. The e o e, he e is a need o u he examine hese
ela ionships in di e se popula ion s udies.
The cu en case-con ol s udy was unde aken in he No h o Spain o elucida e
he ela ionships be ween ood g oup consump ion, die quali y and CRC isk, and
iden i y possible di e ences in consump ion depending on umo loca ion, in an adul
popula ion ha pa icipa ed in a CRC sc eening p og amme (CRCSP) in he Basque
Coun y. To ou knowledge, his is he i s s udy in he Basque coun y popula ion, in
which bo h CRC incidence and mo ali y ha e inc eased in ecen yea s[11]. The e a e
ew s udies in his ega d in Spain[12,13]. And bo h in hese Spanish s udies and in o he s
ca ied ou in o he Medi e anean coun ies con ols we e appa en ly heal hy subjec s
wi hou clinical symp oms o signs o any ype o cance [14].
MATERIALS AND METHODS
S udy subjec s
This is an obse a ional, ma ched case-con ol s udy in a popula ion g oup esiding in
he Basque Coun y (No h o Spain). Pa icipan s in his s udy we e ec ui ed om
among pa ien s a ending any o he h ee hospi als o he Osakide za/Basque Heal h
Se ice (Basu o, Galdakao and Donos ia) membe s o he Basque Coun y CRCSP. To
be eligible o his CRCSP, he pa ien s had o be aged be ween 50 and 69,
asymp oma ic o colo ec al symp oms and egis e ed wi h he Osakide za/Basque
Heal h Se ice[11]. These inclusion c i e ia we e applied o bo h case and con ol g oup,
ha is, con ols ul illed he same eligibili y c i e ia de ined o he cases, wi h he
excep ion o he disease (ou come). Rec ui men and da a collec ion o he p esen
s udy we e conduc ed be ween 2014 and 2016.
All he pa ien s who we e newly diagnosed wi h CRC (n = 601) we e in i ed o
pa icipa e in his s udy. O hose, 283 e used o pa icipa e in he s udy, and 10 we e
excluded due o missing in o ma ion. Ul ima ely, 308 subjec s (66.2% men) consen ed
o pa icipa e in he su ey and comple ed all he ques ionnai es. In addi ion, o each
case, h ee age- (± 9.0 yea s) and sex-ma ched con ol pa ien s we e andomly sough
om he lis o CRC- ee subjec s (n = 1836) who pa icipa ed in he CRCSP du ing he
same pe iod as he cases. The ma ched con ols we e pa ien s wi h posi i e esul s
Aleg ia-Le xundi I e al. Die and colo ec al cance isk
WJG h ps://www.wjgne .com 4111 July 28, 2020 Volume 26 Issue 28
(abno mal) o immunochemical ecal occul blood es and nega i e colonoscopy
esul s (no mal). The pa icipa ion a e o he con ols was 37.6%, and 17 subjec s we e
excluded due o missing in o ma ion. Finally, he ma ched case- o-con ol a io was
1:1, and he inal da a se included 308 cases who we e diagnosed wi h CRC and 308
age- and sex-ma ched con ols. Fu he de ails on ec ui men and da a collec ion ha e
been desc ibed elsewhe e[15]. The main ad an age o he p esen s udy compa ed o
o he abo e-men ioned esea ches[12-14] is ha we con i med ha con ols we e ee o
he disease h ough colonoscopy. Colonoscopy was used as diagnos ic c i e ia o
iden i y he cases in o de o a oid alse posi i es and nega i es.
The pa hological s aging was based on he 7 h edi ion o he AJCC cance s aging
manual[16] as ollows: I (57.1%), IIA (13.6%), IIB (1.0%), IIC (0.3%), IIIA (7.5%), IIIB
(14.6%), IIIC (1.9%), IVA (2.9%), and IVB (1.0%). The loca ion o he cance was dis al
in 76% and p oximal ( o he splenic lexu e o he colon) in 24.0% o he samples.
Conce ning he umo g ade classi ica ion, we adop ed a wo-g ade classi ica ion ha
was di ided in o low g ade (well o mode a ely di e en ia ed) (80.5%) and high g ade
(poo ly di e en ia ed, anaplas ic, o undi e en ia ed) (4.5%); he pe cen age o
missing da a o his classi ica ion was 14.9%.
Some o he cases had unde gone su gical esec ion (73.7%) and/o adju an
ea men s, chemo he apy (34.1%), and chemo he apy and adia ion (6.8%). The
pe cen ages o subjec s acco ding o he ype o su gical p ocedu e we e as ollows:
26.3% sigmoidec omy, 17.5% igh hemicolec omy esec ion, 18.8% low an e io
esec ion, 6.5% le hemicolec omy esec ion, 2.3% ans e se colec omy, 1.0%
abdominope ineal esec ion, 1.0% o al colec omy, and 0.3% ansanal endoscopic
ope a ion. The cases we e in i ed o ake pa in his su ey a leas one mon h a e
inishing hei las ea men (su ge y, chemo he apy o adio he apy) (median, 1.3
yea s; ange, 0.1 o 4.2 yea s). All he clinical da a we e ob ained om he Basque
Coun y's popula ion-based CRCSP da abase, which links pa ien medical eco ds and
clinical da abases and e iewed by expe s a . This e iew allowed he
moni o iza ion o all cases om he submission o he sample h ough he analysis,
colonoscopy, pa hology and ollow-up.
This s udy was conduc ed acco ding o he guidelines laid down in he Decla a ion
o Helsinki, and all p ocedu es in ol ing pa ien s we e app o ed by he Clinical
Resea ch E hics Commi ee o he Basque Coun y ( e e ence numbe s PI2011006 and
PI2014042). W i en in o med consen was ob ained om all he s udy pa icipan s.
Consen ing pa icipan s sel -comple ed and e u ned a de ailed ood equency
ques ionnai e (FFQ) and one gene al ques ionnai e. The ques ions e e ed o he
beha io s be o e pa icipa ing in he CRCSP. Assis ance om he s udy s a was
a ailable o help he pa ien s o unde s and he i ems on he ques ionnai es. The
quali y managemen applied in he p esen s udy has been desc ibed in a p e ious
a icle[15].
Die a y assessmen
Die s we e assessed using a sho FFQ ha was a modi ied e sion o he Rod íguez
e al[17] (2008) ques ionnai e. This adap a ion was alida ed wi h mul iple 24-h ecalls in
he Basque gene al popula ion[18] and in CRC diagnosed pa ien s in a pilo o he
p esen s udy[19]. I consis s o 67 i ems and equi es he subjec s o ecall he numbe o
imes each ood i em was consumed ei he pe week o pe mon h. This FFQ included
speci ic ques ions abou he equency o in ake o alcoholic be e ages. Mo eo e , he
esponden s could also eco d he consump ion o o he oods ha we e no included
on he ood lis .
Consump ion equencies we e s anda dized o “pe day” and mul iplied by
s anda d se ing sizes (g ams)[20]. Fo i ems ha included se e al oods, each ood’s
con ibu ion was es ima ed wi h weigh ing coe icien s ha we e ob ained om he
usual consump ion da a[21]. Food i ems we e hen eg ouped acco ding o nu i ional
cha ac e is ics[22] and conside ing he po en ial con ibu ion o ood o he pa hogenesis
o CRC[23,24]. De ails on he i ems included in each ood g oup a e shown in Table 1. All
ood i ems ha we e consumed we e en e ed in o DIAL 2.12 (2011 ALCE
INGENIERIA)[25], a ype o die a y assessmen so wa e, o es ima e ene gy in ake (
kilocalo ies/day, kcal/d).
Adhe ence o he die a y ecommenda ions was e alua ed u ilizing he Heal hy
Ea ing Index o Spanish Die (HEISD)[26] and he MedDie Sco e (MDS)[27], as
p e iously desc ibed[19]. The heo e ical ange o he HEISD is 0-100 and o he MDS 0-
55, highe alues o hese sco es indica e g ea e adhe ence o he die a y
ecommenda ions o he Spanish popula ion and he Medi e anean die pa e n,
espec i ely. HEISD was di ided in o he ollowing ca ego ies: Poo die (< 50 poin s),
needs imp o emen (50-80 poin s) and p ope die (> 80 poin s)[26]; and he MDS in o
Aleg ia-Le xundi I e al. Die and colo ec al cance isk
WJG h ps://www.wjgne .com 4112 July 28, 2020 Volume 26 Issue 28
Table 1 Food g oup de ini ions
Food g oup Food i ems
Red and p ocessed mea
Red mea Bee , po k and lamb, minced mea , hambu ge s, mea balls
P ocessed mea Ham, sausage, salami, mo adella, black pudding o blood sausage
Egg Egg
Fish Whi e ish (hake, g oupe , sole, cod) and a y ish (sa dine, una, salmon, macke el)
Milk/dai y p oduc s
Non-cheese p oduc s Whole milk, semi-skimmed milk, skimmed milk, whole yogu , skimmed yogu and dai y desse s
Cheese Bu gos cheese, cu d, co age and cheeses low in calo ies, ma u e, semi-ma u e and c eamy cheese
Fibe -con aining oods
F ui s O ange, ange ine, apple, pea , banana, peach, aisins, p unes, d ied igs... na u al ui juices
Vege ables Salads, g een beans, cha d, spinach... ga nish ege ables (eggplan , mush ooms, peppe s...), ga lic, onion
Whole g ains Whole g ain pas a, b own ice, whole g ain cookies, whole b eak as ce eals (Muesli, All-B an)
Nu s Walnu s, almonds, hazelnu s, peanu s
Fa Vege able oils (oli e, sun lowe , co n, soy), bu e , ma ga ine, mayonnaise
Swee and added suga Chocola e, b eak as ce eals, cookies, mu ins, donu s, honey, suga , comme cial ui juice, so -d inks, cakes, pies
Alcoholic be e ages Bee , wine, ha d cide , e mou h, whiskey, um, gin, b andy, cock ails
he ollowing ones: Low adhe ence o MD (0-34 poin s) and high adhe ence (> 35
poin s). The cu -o poin o MDS was es ablished aking in o accoun ha sco es
below 34 poin s we e associa ed wi h a highe isk o co ona y hea disease, being he
ela i e odds ≥ 1.42[27].
Gene al ques ionnai e
A gene al ques ionnai e was used o ga he in o ma ion on weigh s a us (sel -
epo ed weigh and heigh ) and en i onmen al ac o s [demog aphic ac o s: Age and
sex; and li es yle in o ma ion: Physical exe cise (PE) and smoking consump ion]. These
ques ions we e aken om he Spanish Heal h Ques ionnai e[28]. Body mass index
(BMI) es ima ed om sel - epo ed heigh and weigh was classi ied acco ding o he
Wo ld Heal h O ganiza ion c i e ia o hose unde 65 yea s o age[29] and acco ding o
he c i e ia p oposed by Sil a Sil a Rod igues e al[30] o hose 65 yea s and olde .
Addi ionally, socioeconomic and heal h s a us da a we e assessed wi h wo indices
ha we e ob ained om he clinical da abases de eloped by he Heal h Depa men o
he Basque Go e nmen , namely he socioeconomic dep i a ion index (DI) and
p edic i e isk modelling (PRM), espec i ely. The i s one was es ima ed using he
MEDEA p ojec c i e ia[31], as has been desc ibed elsewhe e[12] and was di ided in o
quin iles (Q), wi h he i s being he leas disad an aged and he i h being he mos
disad an aged. The DI was success ully assigned o 80.2% o pa icipan s, while he
quali y o he egis e ed in o ma ion did no pe mi he linking o he emaining
19.8%.
The PRM is an index ha is based on Adjus ed Clinical G oups[32], Diagnos ic Cos
G oups/Hie a chical Condi ion Ca ego ies[33] and Clinical Risk G oups[34]. This index
combines in o ma ion abou diagnoses, p esc ip ions, p e ious cos s and he use o
speci ic p ocedu es. I is capable o p edic ing he use o heal h esou ces[35], and i was
s a i ied in o ou le els (L); he i s included pa icipan s wi h a isk o high heal h
esou ce consump ion and he ou h included hose wi h low heal h esou ce
consump ion. The PRM was success ully assigned o 95.1% o pa icipan s, while he
quali y o he egis e ed in o ma ion did no pe mi he linking o he emaining 4.9%.
S a is ical analysis
S a is ical analyses we e pe o med using IBM SPSS S a is ics o Windows, e sion
22.0 (IBM Co p., A monk, NY, Uni ed S a es) and STATA 13.0 (S a aCo p LP, TX,
Uni ed S a es). Ca ego ical a iables a e shown as a pe cen age, and con inuous
a iables a e shown as he means and s anda d de ia ions (SD). No mali y was
Aleg ia-Le xundi I e al. Die and colo ec al cance isk
WJG h ps://www.wjgne .com 4119 July 28, 2020 Volume 26 Issue 28
P0.789 < 0.001 -
Whole g ains
T1144/128 1.00 1.00 1.00
T283/77 0.92 (0.62-1.38) 0.86 (0.52-1.42) 0.98 (0.58-1.65)
T381/103 0.68 (0.46-1.01) 0.62 (0.37-1.06) 0.62 (0.39-0.98)
P0.135 < 0.001
1Food g oups consump ion was ca ego ized in o e iles acco ding o he dis ibu ion in con ols, and by sexes o ood g oups wi h signi ican di e ences
acco ding o sex; Te iles o ood g oups: Red mea , T1 < 33.5, T2 33.5-54.9, T3 > 54.9; P ocessed mea , T1 < 11.6, T2 11.6-22.8, T3 > 22.8; non-cheese dai y, T1 <
225.0, T2 225.0-325.0, T3 > 325.0; Cheese, T1 < 7.5, T2 7.5-20.0, T3 > 20.0; Vege ables, T1 < 152.9, T2 152.9-237.2, T3 > 237.2;Te iles o ood g oups o men:
F ui s, T1 < 207.5, T2 207.5-392.9, T3 > 392.9; Whole g ains, T1 < 1.0, T2 1.0-17.5, T3 > 17.5; Te iles o ood g oups o women: F ui s T1 < 242.9, T2 242.9-
425.0,: Whole g ains, T1 < 2.0, T2 2.0-30.0, T3 > 30.0.
2Model I, analyses we e pe o med using c ude condi ional logis ic eg ession, wi hou aking in o accoun con ounding ac o s.
3Model II, analyses we e pe o med using condi ional logis ic eg ession analysis adjus ed o age (50-59 yea s old, 60-69 yea s old), sex, body mass index
(unde weigh /no mal weigh , o e weigh /obesi y), ene gy in ake (kcal/d), physical exe cise le el (< 15 min/d o cycling/spo s, ≥ 15 min/d), smoking
s a us and in ensi y o smoking (ne e ; pas : qui smoking ≥ 11 yea s ago, qui < 11 yea s ago; Smoke : ≤ 15 ciga e es/d, > 15 ciga e es/d), Dep i a ion
Index (quin ile 1-3, quin ile 4-5) and P edic i e Risk Modelling (le el 1-2, le el 3-4), including ood g oups sepa a ely; Pa icipan s wi h missing da a o
he con ounding a iables we e included as a sepa a e ca ego y o hese a iables.
4Model III, model II including all he mean ood g oups. CI: Con idence in e al; OR: Odd a io; T: Te ile.
in e e ing abso p ion o hose, and lowe ing in es inal acidi y[51]. In addi ion,
e men a ion o ibe p oduced bu y a e. This sho -chain a y acid showed an i-
in lamma o y, an i-p oli e a ion and an ineoplas ic p ope ies in colonocy e cells
me abolism h ough mic obio a homeos asis and gene ic/epigene ic egula ion[52].
Fu he mo e, ou indings sugges ha high consump ion o whole g ains (highe
han 17.5 g/d in men and 30.0 g/d in women) may dec ease he isk o CRC, a e
con olling con ounding ac o s. The e is con incing e idence ha whole g ains help
o educe CRC isk[5,53]. The obse ed educ ion in CRC isk associa ed wi h high
consump ion o whole g ains may pa ly be a ibu ed o die a y ibe , esis an s a ch,
and oligosaccha ides ha can in luence he gu en i onmen . Insoluble ibe inc eases
he bulk o luminal con en s, dilu ing po en ial ca cinogens and p omo e s in he colon
and dec easing ansi ime, and, consequen ly, educes he exposu e o he colonic
epi helium o ha m ul compounds[54,55]. Addi ionally, o he componen s such as
i amins (especially B- i amins), mine als (e.g., magnesium and zinc), phenolic
compounds, an inu ien s (e.g., annins), and phy oes ogens may also con ibu e o
his p o ec ion[54].
On he o he hand, he consump ion o a y ish (highe han 42.8 g/d) was
associa ed wi h a dec eased isk in CRC by abou 50% (OR app oxima ely 0.5)
compa ed o lowe consump ion, a e adjus ing models o co a ia es. I should be
no ed ha he Basque Coun y popula ion has a highe consump ion o o al ish and
a y ish compa ed o o he Spanish au onomous communi ies[55,56]. Recen coho
s udies ha e obse ed ha a y ish was in e sely associa ed wi h CRC incidence[57,58]
and hey ha e ela ed his associa ion wi h exposu e o long-chain n-3
polyunsa u a ed a y acids[57]. E idence om animal and in i o s udies indica es ha
n-3 a y acids p esen in a y ish may inhibi ca cinogenesis[59]. High in ake o n-3
a y acids supp esses he p oduc ion o a achidonic acid-de i ed eicosanoids such as
p os aglandin E2 and leuko iene B431. N-3 a y acids could also supp ess he
exp ession o inducible ni ic oxide syn hase and nuclea ansc ip ion ac o κ B (NF-κ
B)[60].
In ela ion o he die quali y, ou indings on he MDS and CRC isk a e suppo ed
by hose o o he esea che s[13,61-63], who ound signi ican associa ions be ween lowe
isk o CRC and adhe ence o Medi e anean die a y pa e n. Howe e he HEISD was
no associa ed wi h CRC isk, disc epancies in esul s ob ained wi h he wo die a y
quali y indices analysed a e p obably due o di e ences in hei cons uc s and sco ing
c i e ia. The o e all MDS was in e sely associa ed wi h CRC isk, being highe he
o al sco e in cases wi h he p oximal loca ion o cance han o hose wi h he dis al
loca ion. These las esul s con as wi h p e ious indings, which showed ha he
p o ec i e e ec s o adhe ence o he MD we e mainly o dis al colon and ec al
cance and no o p oximal colon cance [64]. In he o al sample, in es iga ion o he
sepa a e sco e componen s showed ha whole g ain sco e was lowe o cases han o
con ols. This esul is consis en wi h ha ob ained o he associa ion be ween whole
g ains consump ion and CRC isk.
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Table 6 Die quali y indices in he sample s udied
Cases (n = 308) Con ols (n = 308)
mean SD mean SD P alue
HEISD componen s1
Mea s 3.1 1.7 3.1 1.7 0.811
P ocessed mea s 2.8 2.0 3.1 2.2 0.162
Legumes 8.6 2.1 8.5 2.3 0.716
Milk/Dai y 9.8 1.2 9.8 1.1 0.797
F ui s 9.1 1.8 9.1 1.9 0.464
Vege ables 8.9 1.7 8.9 1.6 0.816
G ains 9.9 0.9 9.9 1.9 0.862
Swee s 1.6 3.1 1.6 3.0 0.847
So -d ink 8.8 2.5 8.7 2.6 0.583
Va ie y 8.0 1.7 8.0 1.7 0.646
To al HEISD 70.7 7.2 70.8 7.9 0.906
MDS componen s2
Red mea s and p ocessed mea s 0.7 1.0 0.8 1.2 0.134
Poul y 2.9 1.2 2.9 1.2 0.335
Fish 3.8 1.1 3.8 1.2 0.771
Legumes 2.4 1.2 2.3 1.1 0.482
Full a dai y 2.0 1.8 2.0 1.9 0.618
Vege ables 4.9 0.6 4.9 0.5 0.599
F ui s 4.6 1.0 4.6 1.0 0.726
Po a oes 2.2 1.5 2.4 1.5 0.054
Whole g ains 2.0 2.2 2.3 2.3 0.044
Alcoholic be e ages 4.9 0.4 4.9 0.4 0.729
Oli e oil 4.9 0.6 4.8 0.8 0.446
To al MDS 35.3 4.5 36.0 4.3 0.027
1Each componen can con ibu e 10 poin s o he o al sco e and he heo e ical ange is 0–100.
2Each componen can con ibu e i e poin s o he o al sco e and he heo e ical ange is 0–55. HEISD: Heal hy Ea ing Index o Spanish Die ; MDS: Med
Die Sco e; SD: S anda d de ia ion.
Ou s udy has se e al limi a ions. Fi s , ecall bias inhe en in a case-con ol s udy
design canno be uled ou . The p ima y conce n o his s udy is he low pa icipa ion
a e, which may ha e limi ed he ep esen a i eness o s udy samples. The decision o
pa icipa e o no may be in luenced by se e al ac o s, including social, educa ional
and heal h condi ions, which may again co ela e wi h ou come isk ac o s. Second,
sel - epo ed da a could be subjec o measu emen e o s and he p oblem o ood
omissions due o memo y ailu e and unde epo ing o unheal hy habi s among
disease subjec s. Howe e , p e ious alida ion s udies indica e ha he sel - epo ed
die a y in o ma ion is epo ed wi h su icien accu acy o use in epidemiology
analyses[65]; and i should be no ed ha die a y changes a e usually modes a e
pa icipa ing in he CRCSP due o a lack o in o ma ion and pe sonalized ad ice[66,67].
Ano he limi a ion o his ype o s udy could be he selec ion o con ols (selec ion
bias). To a oid his ype o bias, we ob ained con ols om he same CRCSP and in he
same pe iod as cases, hus, i was con i med ha hey did no su e om CRC by
colonoscopy.
Despi e hese limi a ions, he esul s allow us o conclude ha high consump ion o
high- a cheeses is associa ed wi h CRC isk, whe eas, a high in ake o ibe -con aining
Aleg ia-Le xundi I e al. Die and colo ec al cance isk
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oods, especially whole g ains, and a y ish, and adhe ence o he Medi e anean
die a y pa e n was associa ed wi h a lowe isk o CRC. Fu u e s udies a e needed o
be e unde s and he in luence o he die a y habi s on CRC p e en ion in his
popula ion ha can p o ide leads o he design and ailo ing o u u e in e en ions,
and guide counselling s a egies o p omo ing a heal hy li es yle.
ARTICLE HIGHLIGHTS
Resea ch backg ound
Epidemiological e idence sugges s ha some oods may bo h p o ec agains and
p omo e he de elopmen o colo ec al cance (CRC). Howe e , oods a e no
consumed in isola ion bu as pa o a die a y pa e n; he e o e, he ac ual e ec o
die on disease isk may be obse ed only when all componen s a e conside ed join ly.
Fo his pu pose, se e al die quali y indexes ha e been de eloped using poin
sys ems o measu e whole die quali y based on he alignmen o ood choices wi h
die a y ecommenda ions.
Resea ch mo i a ion
Some die quali y indexes ha e been used o begin assessing he ela ionships be ween
o e all die quali y and CRC isk, and he esul s show ha high sco es in hese
indices a e associa ed wi h a lowe CRC isk. Howe e , he esul s a y conside ably
acco ding o he index used and o he ac o s such as sex and age. The e o e, he e is a
need o u he examine hese ela ionships in di e se popula ion s udies.
Resea ch objec i es
To s udy he ela ionships be ween ood g oups, die quali y and CRC isk, in an adul
popula ion o he Basque Coun y (No h o Spain).
Resea ch me hods
This obse a ional s udy included 308 pa ien s diagnosed wi h CRC and 308 age- and
sex-ma ched subjec s as con ols. Du ing ec ui men , die a y, an h opome ic,
li es yle, socioeconomic, demog aphic and heal h s a us in o ma ion was collec ed.
Die a y in ake was assessed using a sho ood equency ques ionnai e ha was
adap ed and alida ed o his popula ion. Adhe ence o he die a y ecommenda ions
was e alua ed u ilizing he Heal hy Ea ing Index o he Spanish Die and he
MedDie Sco e. S a is ical analyses we e pe o med using IBM SPSS S a is ics o
Windows, e sion 22.0 (IBM Co p., A monk, NY, Uni ed S a es) and STATA 13.0
(S a aCo p LP, TX, Uni ed S a es). Condi ional logis ic eg essions we e used o
e alua e he associa ions o ood g oup in akes, die quali y sco es, ca ego ized in
e iles, wi h CRC isk.
Resea ch esul s
The adjus ed models o po en ial con ounding ac o s showed a di ec associa ion
be ween milk/dai y p oduc s consump ion, in pa icula high- a cheeses [odds a io
(OR) hi d e ile s i s e ile = 1.87, 95% con idence in e als (CI): 1.11-3.16], and
CRC isk. While he consump ion o ibe -con aining oods, especially whole g ains
(OR hi d e ile s i s e ile = 0.62, 95%CI: 0.39-0.98), and a y ish (OR = 0.53,
95%CI: 0.27-0.99) was associa ed wi h a lowe isk o CRC. Mo eo e , highe MD
adhe ence was associa ed wi h a educed CRC isk in adjus ed models (OR = 0.40,
95%CI: 0.20-0.80).
Resea ch conclusions
Di ec associa ions we e ound o high- a cheese, whe eas an in e se ela ion was
epo ed o ibe -con aining oods and a y ish, as well as adhe ence o a
Medi e anean die a y pa e n.
Resea ch pe spec i es
Fu u e s udies a e needed o be e unde s and he in luence o he die a y habi s on
CRC p e en ion in his popula ion ha can p o ide leads o he design and ailo ing
o u u e in e en ions, and guide counselling s a egies o p omo ing a heal hy
li es yle.
Aleg ia-Le xundi I e al. Die and colo ec al cance isk
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