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REVIEW
Prevalence of Helicobacter pylori Infection Worldwide:A Systematic Review of Studies with National Coverage
Barbara Peleteiro • Ana Bastos • Ana Ferro •
Nuno Lunet
Received: 27 November 2013 / Accepted: 5 February 2014
� Springer Science+Business Media New York 2014
Abstract The systematic assessment of large population-
based surveys addressing the prevalence of Helicobacter
pylori infection may provide robust evidence for under-
standing the trends in the exposure to this major risk factor
across settings with distinct patterns of gastric cancer
variation. Our aim was to describe the prevalence of H.
pylori infection in different countries and periods, through
systematic review of the literature. We searched PubMed
from inception up to September 2013 to identify original
studies reporting on the prevalence of H. pylori, and only
those evaluating samples with national coverage were
included. We identified 37 eligible studies including data
for 22 countries. The prevalences were higher in Central/
South America and Asia, and at least two-fold higher in
countries with high gastric cancer incidence. In most
countries presenting data for different time periods, the
prevalences were usually lower in the most recent surveys.
However, there was little variation in settings where
prevalences were already low. Among countries with high
prevalence of H. pylori infection there is an ample scope
for reducing its burden in the next decades, whereas further
declines in settings with already low prevalences will
require more intensive efforts.
Keywords Helicobacter pylori � Prevalence � Trends �Systematic review � Epidemiology
Introduction
A continued decline in gastric cancer incidence and mor-
tality has been observed worldwide for several decades,
though the trends differ between [1–3] and within countries
[4–8]. The decrease in gastric cancer rates was primarily
attributed to a set of factors related to the improvement of
the populations’ living conditions, including the increase in
fruits and vegetables consumption and the decrease in salt
intake [9]. The recognition of Helicobacter pylori as a
human carcinogen [10, 11] brought a new paradigm to
interpret gastric carcinogenesis and temporal/geographical
variation in gastric cancer frequency [12].
It is estimated that H. pylori infection affects more than
half of the adult population worldwide [13] and is
responsible for 75 % of all gastric cancer cases [14]. The
systematic assessment of large population-based surveys
addressing the prevalence of infection may provide robust
evidence for understanding the trends in the exposure to
this major risk factor across settings with distinct patterns
of variation in gastric cancer mortality [2].
We aimed to describe the prevalence of H. pylori
infection in different countries and periods, through sys-
tematic review of studies with national coverage.
Methods
We searched PubMed from inception up to September
2013, to identify original studies reporting H. pylori
prevalence. The references retrieved were analyzed inde-
pendently by two reviewers (AB and AF), following pre-
defined criteria, to determine the eligibility of each report
(Fig. 1).
B. Peleteiro (&) � N. Lunet
Department of Clinical Epidemiology, Predictive Medicine and
Public Health, University of Porto Medical School, Al. Prof.
Hernani Monteiro, 4200-319 Porto, Portugal
e-mail: [email protected]
B. Peleteiro � A. Bastos � A. Ferro � N. Lunet
Institute of Public Health of the University of Porto (ISPUP),
Porto, Portugal
123
Dig Dis Sci
DOI 10.1007/s10620-014-3063-0
Fig. 1 Systematic review flowchart
Dig Dis Sci
123
The criteria for exclusion of studies were the following:
(1) reports not written in English, Portuguese, Spanish,
French, Italian or Polish, (2) studies not involving humans
(e.g., in vitro or animal research), (3) non-eligible publi-
cation types, such as review articles (except systematic
reviews), editorials, comments, guidelines or case reports,
(4) studies specifically evaluating samples expected to
yield biased estimates of the prevalence of H. pylori
infection in the general population (e.g., subjects under-
going endoscopy for purposes other than screening), (5)
studies including only H. pylori-positive subjects (e.g., H.
pylori eradication trials), (6) studies with data not related to
H. pylori prevalence or addressing other outcomes (e.g.,
mathematical models), (7) studies with non-systematic
assessment of H. pylori infection status in biological
samples (e.g., self-reported information, secondary data on
infection status retrieved from databases), (8) duplicate
studies or evaluating the same sample, and (9) studies
evaluating samples with no national coverage.
The references’ lists of the systematic reviews of studies
addressing the frequency of infection or its association with
other outcomes were also screened to further identify
potentially eligible original reports.
When more than one report referred to the same study,
we considered the one presenting the results with more
detail (e.g., regarding the prevalence according to age
strata), or providing data for the largest sample, although
any of the reports could be used to obtain information on
the study characteristics.
The disagreements between the independent assess-
ments of the reviewers were resolved by consensus or after
discussion with a third researcher (BP).
Two investigators (AB and AF) evaluated independently
the selected studies to extract the data regarding sampling
procedures, sample characteristics and assessment of H.
pylori infection status. Age-specific prevalence estimates
of H. pylori infection were extracted whenever available,
and sex-specific estimates were extracted only when no
estimates were provided for both sexes combined. Differ-
ences in the data extracted by the two investigators were
discussed until consensus, and involving a third researcher
(BP) whenever necessary.
Results were summarized in charts depicting age-spe-
cific prevalence of infection in different periods of data
collection for countries providing these data. Additionally,
age-specific prevalence estimates obtained from surveys
conducted mostly in the late 1990s/early 2000s were
plotted against the estimated gastric cancer incidence in the
corresponding countries [15]. To characterize each strata
regarding age of the participants, the median or the mean
age of participants in each age group were used, whenever
available. Alternatively, we assumed the mid-point of the
age interval; for the open age intervals at the extremes, we
estimated the mid-point by adding and subtracting the
width of the closest class to the upper and to the lower
limits, respectively (e.g., for surveys reporting data in
participants aged \ 30, 30–39, 40–49, and C50 years, 20
and 59 were the midpoints assigned to the lowest and
highest age groups, respectively).
Results
We identified 37 studies addressing the prevalence of H.
pylori infection [16–52] (Table 1) in 22 countries: five
American (one from North, one from Central and three
from South America), six Asian (three from East, one from
Southeast and two from Western Asia), ten European (five
from North, one from South, one from Western and three
from Central/Eastern Europe) and one from Oceania
(Australia).
The reports were published between 1995 and 2013, and
referred to data collected between 1968 and 2011. Most
studies had a cross-sectional design, except nine case–
control studies (data extracted referred to the control
groups) and three cohort studies (data extracted referred to
the baseline assessment).
Regarding the characteristics of the populations evalu-
ated, 12 studies were national surveys with random sam-
ples of the population obtained by stratified sampling of
households, eight studies used random samples of sera
from several serum banks (including samples of pregnant
women and blood donors), seven studies evaluated indi-
viduals undergoing routine health check-ups, four studies
used random samples of subjects included in governmental
public health databases, three studies evaluated random
samples of subjects selected from national registries of
residents, two studies were performed in military recruits,
and one study included randomly selected individuals from
electoral rolls. The studies covered a wide age range,
between\1 and 101 years, with sample sizes ranging from
96 to 25,536 subjects. The assessment of H. pylori status
was done mainly through ELISA tests to determine IgG
antibody titers in serum (n = 23), urine (n = 1) or saliva
(n = 1). One study used joint information of blood and
biopsy specimens. Two studies assessed current infection
status using a urea breath test.
Although the studies reviewed covered different age
ranges, overall, the prevalence of H. pylori increased with
age, decreasing in the older age groups in some countries
(Chile, Ecuador, Japan, Mexico, Latvia and Republic of
Korea) (Fig. 2). Most reports provided prevalence esti-
mates for strata with median age around 20 and 60 years.
Considering the data from samples evaluated mostly in the
late 1990s/early 2000s, the prevalence estimates were
generally higher among countries in Central/South
Dig Dis Sci
123
Ta
ble
1M
ain
char
acte
rist
ics
of
the
stu
die
sin
clu
ded
inth
esy
stem
atic
rev
iew
Cou
ntr
yP
erio
do
f
dat
a
coll
ecti
on
Fir
st
auth
or,
yea
r
of
pu
bli
cati
on
Ty
pe
of
stu
dy
Sam
ple
Ass
essm
ent
of
H.
pyl
ori
infe
ctio
n
stat
us
Pre
val
ence
of
H.
pyl
ori
infe
ctio
n,
wh
ole
sam
ple
(%)
Sel
ecti
on
Ag
e(y
ears
)
rang
e
mea
n±
SD
Siz
e
Arg
enti
na
1996
Olm
os,
20
00
[16]
Cro
ss-
sect
ion
al
Asa
mple
fro
mg
ener
alp
op
ula
tio
nw
asre
cru
ited
afte
rst
rati
fica
tio
no
f
the
countr
yac
cord
ing
tocl
imat
ean
daf
ter
sele
ctio
nof
the
mai
nci
ties
wit
hin
each
stra
tum
.F
rom
each
cho
sen
city
,p
ub
lic
and
pri
vat
eh
ealt
h
cen
ters
atte
nd
edb
yin
div
idu
als
of
dif
fere
nt
soci
alcl
asse
sw
ere
sele
cted
.A
mong
those
,outp
atie
nts
wit
hro
uti
ne
scre
enin
gblo
od
anal
yse
sw
ere
con
secu
tiv
ely
enro
lled
,if
bo
thth
eyan
dth
eir
par
ents
wer
eb
orn
inA
rgen
tin
aan
dh
adb
een
liv
ing
inth
eg
eog
rap
hic
area
they
repre
sente
dfo
rth
ela
st4
yea
rs.
They
wer
ere
cruit
edfr
om
32
pri
vat
ean
dp
ub
lic
hea
lth
cen
ters
from
all
geo
gra
phic
area
s
0–
80
ND
±N
D
N=
75
4
Chil
dre
n:
N=
26
1
Ad
ult
s:
N=
49
3
(17
8m
enan
d
31
5w
om
en)
Ser
um
IgG
(no
t
furt
her
spec
ified
)
Cru
de—
37
.5
Ad
just
ed—
35.7
Au
stra
lia
20
02
Mo
uja
ber
20
08
[17]
Cro
ss-
sect
ion
al
H.
pyl
ori
sero
pre
val
ence
was
det
erm
ined
usi
ng
ara
nd
om
sam
ple
of
2,4
13
sera
(sel
ecte
dra
nd
om
lyaf
ter
age-
stra
tifi
cati
on
)fr
om
ab
ank
of
app
roxim
atel
y8
,00
0co
llec
ted
fro
mp
eop
leag
ed1
–5
9y
ears
fro
m3
7
maj
or
dia
gnost
icla
bora
tori
esar
ound
Aust
rali
a.T
his
was
a
con
ven
ien
cesa
mp
leo
fse
rasu
bm
itte
dfo
rd
iagn
ost
icte
stin
gin
20
02
that
wo
uld
oth
erw
ise
hav
eb
een
dis
card
ed.
Ser
afr
om
sub
ject
sw
ho
wer
eim
munoco
mpro
mis
ed,
had
rece
ived
mult
iple
tran
sfusi
ons
inth
e
pas
t3
mon
ths,
or
had
sub
mit
ted
sam
ple
sfo
rte
stin
gfo
rH
IVw
ere
excl
ud
ed
1–
59
ND
±N
D
N=
2,4
13
(1,2
10
men
and
1,2
03
wo
men
)
Ser
um
IgG
(EL
ISA
)
15
.4
20
02
–2
00
5P
and
eya,
20
11
[18]
Cas
e–
con
tro
l
Par
tici
pan
ts(a
ge
18–79
yea
rs)
wer
era
ndom
lyse
lect
edfr
om
the
Au
stra
lian
Ele
cto
ral
Roll
(en
rolm
ent
isco
mp
uls
ory
)m
atch
edto
the
eso
phag
eal
can
cer
case
sw
ith
inst
rata
of
age
(in
5-y
ear-
age
gro
ups)
,
sex
and
stat
eo
fre
sid
ence
18
-79
ND
±N
D
N=
1,4
00
Ser
um
IgG
(EL
ISA
)
15
.5
Ch
ile
20
03
Fer
recc
io,
20
07
[19]
Cro
ss-
sect
ion
al
The
2003
Nat
ional
Hea
lth
Surv
eyw
asa
nat
ional
cross
-sec
tional
ho
use
ho
ldsu
rvey
of
3,6
19
peo
ple
bas
edo
na
mult
ista
ge
stra
tifi
ed
rand
om
sam
ple
of
the
Ch
ilea
np
op
ula
tio
no
ver
17
yea
rso
fag
e.O
nly
one
par
tici
pan
tw
asse
lect
edper
house
hold
,usi
ng
the
Kis
hm
ethod
to
cho
ose
the
resp
on
din
gin
div
idual
17
–84
ND
±N
D
N=
3,6
19
Ser
um
IgG
(EL
ISA
)
Cru
de—
73
.0
Ad
just
ed—
73.4
Ch
ina
19
89
Wan
g,
20
08
[20]
Cro
ss-
sect
ion
al
Fro
m1986
to1988,
anat
ional
stom
ach
cance
rm
ort
alit
ysu
rvey
was
per
form
edin
69
cou
nti
esra
nd
om
lych
ose
nfr
om
the
tota
lo
fab
ou
t
2,4
00
larg
ely
rura
lco
un
ties
inC
hin
a.T
he
cou
nti
esar
ere
pre
sen
tati
ve
of
rura
lm
ain
lan
dC
hin
aas
aw
ho
le.
H.
pyl
ori
pre
val
ence
,uri
nar
y
sodiu
mex
cret
ion
and
uri
nar
ynit
rate
excr
etio
nw
ere
der
ived
from
a
sub
sequ
ent
die
tary
surv
eyco
nd
uct
edin
19
89
inth
esa
me
69
cou
nti
es
35
–64
ND
±N
D
N=
8,2
80
On
lym
en
H.
pyl
ori
anti
bo
dy
in
uri
ne
(EL
ISA
)
71
.4
Dig Dis Sci
123
Ta
ble
1co
nti
nu
ed
Cou
ntr
yP
erio
do
f
dat
a
coll
ecti
on
Fir
st
auth
or,
yea
r
of
pu
bli
cati
on
Ty
pe
of
stu
dy
Sam
ple
Ass
essm
ent
of
H.
pyl
ori
infe
ctio
n
stat
us
Pre
val
ence
of
H.
pyl
ori
infe
ctio
n,
wh
ole
sam
ple
(%)
Sel
ecti
on
Ag
e(y
ears
)
rang
e
mea
n±
SD
Siz
e
Cze
ch
Rep
ub
lic
20
01
Bu
res,
20
06
[49]
Cro
ss-
sect
ion
al
Nin
etee
nce
nte
rso
fg
ener
alp
ract
itio
ner
s(G
Ps)
(7fo
rch
ild
ren
and
ado
lesc
ents
and
12
for
adu
lts)
wit
hca
tch
men
tar
eas
cov
erin
gci
ties
and
tow
ns
wit
hm
ore
than
20
,00
0in
hab
itan
ts(8
GP
s),
smal
ler
tow
ns
(B2
0,0
00
inh
abit
ants
)w
ith
surr
ou
nd
ing
vil
lag
es(8
GP
s)an
dru
ral
area
s(3
GP
s),
and
corr
esp
on
din
gto
the
dis
trib
uti
on
of
Cze
ch
popula
tion,w
ere
enro
lled
.In
atw
o-s
tep,ra
ndom
sele
ctio
nca
rrie
dout
centr
ally
,in
div
idual
sold
erth
an4
yea
rsw
ere
chose
nfo
rth
est
udy
and
invit
ed(i
nw
ritt
enfo
rm)
top
arti
cip
ate.
Th
ere
wer
en
o
pre
lim
inar
yex
clusi
on
crit
eria
5–
100
ND
±N
D
N=
2,5
09
(1,2
34
men
and
1,2
75
wo
men
)
13C
Ex
pir
edai
r
(UB
T)
41
.7
20
11
Bu
res,
20
12
[48]
Cro
ss-
sect
ion
al
Ato
tal
of
22
cen
ters
,in
clu
din
g1
5ce
nte
rso
fg
ener
alp
ract
itio
ner
sfo
r
adult
san
d7
for
chil
dre
nan
dad
ole
scen
ts,
ente
red
the
study.
Thes
e
cen
ters
cov
ered
citi
esan
dto
wn
sw
ith
mo
reth
an2
0,0
00
inhab
itan
ts
(10
centr
es),
smal
ler
tow
ns
(B2
0,0
00
inh
abit
ants
)w
ith
surr
ou
nd
ing
vil
lages
(nin
ece
ntr
es)
and
rura
lar
eas
(th
ree
centr
es),
and
wer
e
spre
ado
ver
the
wh
ole
cou
ntr
y,
corr
esp
on
din
gw
ell
toth
e
geo
gra
ph
ical
dis
trib
uti
on
of
the
Cze
chp
op
ula
tio
n.
Ato
tal
of
1,8
37
subje
cts
(aged
5–98
yea
rs)
took
par
tin
the
study,
random
lyse
lect
ed
out
of
38,1
47
regis
tere
dm
ales
and
fem
ales
inth
isag
era
nge
5–
98
ND
±N
D
N=
1,8
37
(85
7m
enan
d
96
9w
om
en)
13C
Ex
pir
edai
r
(UB
T)
23
.5
Ger
man
y1
98
7–
198
8B
ren
ner
,
19
99
[21]
Cro
ss-
sect
ion
al
Am
ult
i-st
age,
stra
tifi
edp
rob
abil
ity
sam
ple
was
dra
wn
fro
mth
en
on
-
inst
itu
tio
nal
ized
po
pu
lati
on
of
Ger
man
nat
ion
alit
yag
ed1
8–
89
yea
rs
18
–88
43
.3±
0.4
a
N=
18
34
Ser
um
IgG
(EL
ISA
)
39
.3
19
97
–1
99
9K
uep
per
-
Ny
bel
en,
20
05
[22]
Cro
ss-
sect
ion
al
Atw
o-s
tag
est
rati
fied
pro
bab
ilit
ysa
mp
le(c
om
mun
itie
s,in
div
idu
als)
was
dra
wn
fro
mth
en
on
-in
stit
uti
onal
ized
resi
den
tial
po
pula
tio
nag
ed
18
–79
yea
rsw
ith
suffi
cien
tk
no
wle
dg
eo
fth
eG
erm
anla
ngu
age
18
–79
45
.5±
ND
N=
6,5
45
Ser
um
IgG
(EL
ISA
)
40
.7
Ecu
ador
20
01
–2
00
2G
om
ez,
20
04
[23]
Cro
ss-
sect
ion
al
Ran
do
mly
ped
iatr
icp
atie
nts
(un
der
16
yea
rs)
from
the
fou
r
geo
gra
ph
ical
reg
ions
of
Ecu
ador
wer
eev
aluat
ed:
coas
t(c
oas
to
f
Pac
ific)
,m
ou
nta
inra
ng
e(A
nd
esm
ou
nta
inra
ng
e),
east
(Am
azo
n
rain
fore
st)
and
insu
lar
reg
ion
(Gal
apag
os
Isla
nds)
,b
etw
een
July
20
01
and
July
20
02
0–
16
ND
±N
D
N=
25
7S
eru
mIg
G(n
ot
furt
her
spec
ified
)
63
.0
Fin
lan
d1
99
1R
ehn
ber
g-
Lai
ho
,
19
99
[24]
Cro
ss-
sect
ion
al
All
Fin
ns
old
erth
an1
00
yea
rsp
arti
cip
ated
ina
Fin
nis
hh
ealt
h
eval
uat
ion
stud
yin
19
91
C1
00
10
1±
0.8
N=
17
3S
eru
mIg
G(E
IA)
61
.0
19
83
,1
99
5R
ehn
ber
g-
Lai
ho
,
20
01
[25]
Cohort
Inal
lm
ater
nit
ycl
inic
sam
ple
sse
lect
edfr
om
nin
edif
fere
nt
loca
liti
es
and
repre
sen
tin
gn
ort
her
n,
east
ern
,so
uth
ern
and
wes
tern
Fin
lan
d,
blo
od
sam
ple
sfr
om
pre
gn
ant
wo
men
wer
eco
llec
ted
20
–34
ND
±N
D
N=
73
0
(19
83)
N=
68
1
(19
95)
On
lyw
om
en
Ser
um
IgG
(EIA
)3
0.1
(19
83
)
13
.1(1
99
5)
Dig Dis Sci
123
Ta
ble
1co
nti
nu
ed
Cou
ntr
yP
erio
do
f
dat
a
coll
ecti
on
Fir
st
auth
or,
yea
r
of
pu
bli
cati
on
Ty
pe
of
stu
dy
Sam
ple
Ass
essm
ent
of
H.
pyl
ori
infe
ctio
n
stat
us
Pre
val
ence
of
H.
pyl
ori
infe
ctio
n,
wh
ole
sam
ple
(%)
Sel
ecti
on
Ag
e(y
ears
)
rang
e
mea
n±
SD
Siz
e
19
77
–1
98
0;
19
97–
19
98
Sal
om
aa-
Ras
anen
,
20
06
[26]
Coh
ort
Th
eS
oci
alIn
sura
nce
Inst
ituti
on
org
anis
eda
com
pre
hen
siv
e
popula
tion-b
ased
hea
lth
surv
eyin
Fin
land
(Min
i-F
inla
nd
Hea
lth
Su
rvey
)d
uri
ng
19
78–
19
80
,fo
llo
win
gp
ilo
tst
ud
ies
carr
ied
ou
tin
19
77,
sam
ple
du
sin
ga
two
-sta
ge
stra
tifi
edcl
ust
erd
esig
nan
d
repre
sen
tin
gal
lF
inn
sag
edC
30
yea
rs
30
–58
ND
±N
D
N=
33
6S
eru
mIg
G(n
ot
furt
her
spec
ified
)
65
.0(1
97
7–
19
80
)
59
.0(1
99
7–
19
98
)
19
83
,1
98
9,
19
95,2
00
1
Sei
skar
i,
20
09
[27]
Cro
ss-
sect
ion
al
Co
ded
(ano
ny
mou
s)se
rum
sam
ple
sfr
om
pre
gn
ant
Fin
nis
hw
om
en
wer
eo
bta
ined
fro
mth
eF
MC
-ser
um
ban
ko
fth
eF
inn
ish
Nat
ion
al
Publi
cH
ealt
hIn
stit
ute
(KT
L)
16
–49
ND
±N
D
N=
95
8
On
lyw
om
en
Ser
um
IgG
(EIA
)3
1.0
(19
83
)
21
.0(1
98
9)
24
.0(1
99
5)
19
.0(2
00
1)
Fra
nce
19
95
–1
99
7B
rou
tet,
19
99
[28]
Cro
ss-
sect
ion
al
Th
est
ud
yp
op
ula
tio
nco
nce
rned
pat
ien
tsco
nsu
ltin
gg
astr
oen
tero
log
ists
inF
ran
cefr
om
19
95
to1
99
7.
Th
ep
hy
sici
ans
wer
ech
ose
nfr
om
ali
st
of
the
most
acti
ve
gas
troen
tero
logis
ts.
Eac
hgas
troen
tero
logis
thad
to
succ
essi
vel
yin
clu
de
fou
rp
atie
nts
wit
hu
pp
erd
iges
tiv
etr
act
(UD
T)
sym
pto
ms
and
fou
rp
atie
nts
wit
han
yo
ther
sym
pto
ms
15
–92
47
±1
5.6
N=
15
97
IgG
insa
liv
a
(EL
ISA
)
25
.4
Hu
ng
ary
19
99
-20
00
Fu
resz
,
20
04
[29]
Coh
ort
Yo
un
gm
ale
do
nors
(aged
19
–23
yea
rs)
wer
ete
sted
for
H.
pyl
ori
sero
po
siti
vit
yat
the
star
to
fth
eir
com
pu
lso
rym
ilit
ary
serv
ice
19
–23
ND
±N
D
N=
2,4
57
On
lym
en
Ser
um
IgG
(EL
ISA
)
23
.0
Icel
and
19
75
–1
99
7L
ehti
nen
,
20
05
[30]
Nes
ted
case
–
con
tro
l
Mo
ther
so
fal
lch
ild
ren
wh
od
evel
op
edle
ukem
iab
efo
re1
5y
ears
of
age
wer
eid
enti
fied
thro
ug
hth
eIc
elan
dic
nat
ion
alp
op
ula
tio
nre
gis
trie
s,
and
fou
rco
ntr
ol
moth
ers
wit
hto
tall
yca
nce
r-fr
eeo
ffsp
ring
atth
eti
me
of
chil
dh
oo
dle
ukem
iad
iag
no
sis
wer
em
atch
edw
ith
the
ind
ex
moth
erac
cord
ing
toag
eat
seru
msa
mp
lin
g,
dat
eo
fsp
ecim
en
coll
ecti
on,
and
off
spri
ng
char
acte
rist
ics:
dat
eof
bir
than
dse
xo
fth
e
chil
d
ND
–N
D
27
.0±
0.3
b
N=
96
On
lyw
om
en
Ser
um
IgG
(EL
ISA
)
33
.0
Isra
el1
98
6–
199
5G
dal
evic
h,
20
00
[31]
Cas
e–
con
tro
l
Ser
um
from
case
so
fd
uo
den
alp
epti
cd
isea
sew
ere
ind
ivid
ual
ly
mat
ched
tofi
ve
con
tro
lsfr
om
the
Isra
elD
efen
seF
orc
eM
edic
al
Corp
s’se
rum
ban
k,es
tabli
shed
from
are
pre
senta
tive
sam
ple
of
mal
e
and
fem
ale
recr
uit
so
nth
eir
firs
td
ayo
fse
rvic
e
ND
–N
D
18
.73
±0
.74
N=
14
4S
eru
mIg
G
(EL
ISA
)
46
.5c
Jap
an1
98
8–
199
0K
iku
chi,
20
05
[32]
Nes
ted
case
–
con
tro
l
Hea
lth
yre
sid
ents
aged
40
–79
yea
rsw
ere
enro
lled
asa
bas
icco
ho
rt
po
pula
tio
nfr
om
45
area
sth
rou
gh
ou
tJa
pan
and
pro
vid
edth
eir
sera
wh
enth
eyat
ten
ded
gen
eral
hea
lth
chec
kp
rog
ram
s
40
–79
ND
±N
D
N=
63
3
(34
9m
enan
d
28
4w
om
en)
H.
pyl
ori
anti
bo
dy
in
seru
m(n
ot
furt
her
spec
ified
)
70
.0
1990–1993
Sas
azuki,
20
06
[33]
Nes
ted
case
–
con
tro
l
All
case
sw
ere
gen
der
and
age
mat
ched
toco
ntr
ols
repre
senti
ng
all
inhab
itan
tsin
the
stud
yar
eas
(27
citi
es,
tow
ns,
or
vil
lages
inn
ine
Publi
cH
ealt
hC
ente
rs)
and
ages
40–59
yea
rsin
aco
hort
esta
bli
shed
in1
99
0an
d4
0–
69
yea
rsin
aco
ho
rtes
tab
lish
edin
19
93
40
–69
57
.4±
0.3
2a
N=
51
1
(34
2m
enan
d
16
9w
om
en)
Ser
um
IgG
(EL
ISA
)
75
.0c
Lat
via
20
08
-20
09
Lej
a,2
01
2
[50
]
Cro
ss-
sect
ion
al
Par
tici
pan
ts,
aged
24–74
yea
rs,
wer
era
ndom
lyse
lect
edfr
om
the
nat
ion
alp
op
ula
tio
nre
gis
try
cov
erin
gth
een
tire
cou
ntr
y,
insu
cha
man
ner
that
ther
ew
asan
equ
alg
rou
psi
zefo
rev
ery
10
-yea
rco
ho
rt,
wit
han
equ
alsp
lit
bet
wee
nth
ese
xes
17
-99
54
±N
D
N=
35
64
(12
18
men
and
23
46
wo
men
)
Ser
um
IgG
(EL
ISA
)
79
.21
Dig Dis Sci
123
Ta
ble
1co
nti
nu
ed
Cou
ntr
yP
erio
do
f
dat
a
coll
ecti
on
Fir
st
auth
or,
yea
r
of
pu
bli
cati
on
Ty
pe
of
stu
dy
Sam
ple
Ass
essm
ent
of
H.
pyl
ori
infe
ctio
n
stat
us
Pre
val
ence
of
H.
pyl
ori
infe
ctio
n,
wh
ole
sam
ple
(%)
Sel
ecti
on
Ag
e(y
ears
)
rang
e
mea
n±
SD
Siz
e
Leb
anon
20
08
–2
00
9N
aja,
20
12
[52
]
Cro
ss-
sect
ion
al
Par
tici
pan
tsold
erth
an18
yea
rsan
dw
ith
no
chro
nic
dis
ease
s,se
lect
ed
from
the
nat
ion
wid
eN
utr
itio
nan
dN
on
-Co
mm
un
icab
leD
isea
ses
Ris
kF
acto
rcr
oss
-sec
tional
surv
eyw
ere
random
lych
ose
n,
bas
edon
the
age-
sex
dis
trib
uti
on
of
the
Leb
anes
epopula
tion
18
-ND
40
.97
±1
5.5
N=
30
8
(14
4m
enan
d
16
4w
om
en)
Ser
um
IgG
(EL
ISA
)
52
.0
Mex
ico
19
87
–1
98
8T
orr
es,
19
98
[38]
Cro
ss-
sect
ion
al
Ser
um
sam
ple
sw
ere
retr
ieved
from
the
Nat
ional
Ser
um
Ban
k,
whic
h
con
tain
sse
rum
sam
ple
sfr
om
all
32
stat
eso
fM
exic
ore
pre
sen
tin
g
ages
1–
90
yea
rsfr
om
all
soci
oec
on
om
icle
vel
san
dal
lg
eog
rap
hic
area
s
1–
90
ND
±N
D
N=
11
,60
5S
eru
mIg
G
(EL
ISA
)
66
.0
Rep
ub
lic
of
Ko
rea
19
93
–1
99
9S
hin
,2
00
5
[36
]
Nes
ted
case
–
con
tro
l
The
Kore
anM
ult
i-ce
nte
rC
ance
rC
ohort
(KM
CC
)co
nsi
sted
of
mal
e
and
fem
ale
sub
ject
sag
edo
ver
30
yea
rs,
wh
ow
ere
vo
lun
tary
par
tici
pan
tsin
aca
nce
r-sc
reen
ing
surv
eyin
fou
rg
eog
rap
hic
ally
defi
ned
area
so
fK
ore
a
40
-82
ND
±N
D
N=
34
4
(22
8m
enan
d
11
6w
om
en)
Ser
um
IgG
(EL
ISA
)
80
.8
19
98
Kim
,2
00
1
[34
]
Cro
ss-
sect
ion
al
Asy
mp
tom
atic
hea
lth
yin
div
idu
als
wh
ov
isit
edth
eh
ealt
h-c
are
cen
ters
for
rou
tin
eh
ealt
hsc
reen
ing
or
ano
utp
atie
nt
med
ical
clin
icw
ere
enro
lled
.T
he
crit
eria
for
enro
lmen
tin
cluded
no
his
tory
of
pep
tic
ulc
erdis
ease
,no
abdom
inal
surg
ery,
no
his
tory
of
erad
icat
ion
ther
apy
for
H.
py
lori
infe
ctio
n,
and
no
sym
pto
ms
of
up
per
gas
troin
test
inal
dis
ease
such
asin
dig
esti
on
,n
ause
a,v
om
itin
g,
hea
rtb
urn
and
epig
astr
icb
urn
ing
pai
n
0–
79
ND
±N
D
N=
5,7
32
Ser
um
IgG
(EL
ISA
)
46
.6
20
05
Yim
,2
00
7
[37
]
Cro
ss-
sect
ion
al
Ad
ult
sub
ject
sag
edC
16
yea
rsw
ho
vis
ited
the
hea
lth
-car
ece
nte
rsfo
r
rou
tin
eh
ealt
hch
eck
-up
pro
gra
min
on
eo
ffo
ur
hea
lth
care
cen
ters
loca
ted
inS
eoul
and
inth
eo
ther
thre
ed
iffe
ren
tp
rov
ince
so
fS
ou
th
Ko
rea
16
–79
ND
±N
D
N=
15
,91
6
(8,6
16
men
and
7,3
00
wo
men
)
Ser
um
IgG
(EIA
)5
6.0
20
06
Kim
,2
00
8
[35
]
Cro
ss-
sect
ion
al
Subje
cts
who
vis
ited
40
Hea
lthca
reC
ente
rsin
South
Kore
afo
ra
rou
tin
eh
ealt
hch
eck
-up
16
–79
46
.7±
11
.1
N=
25
,53
6S
eru
mIg
G(n
ot
furt
her
spec
ified
)
Ure
ase
enzy
me
in
bio
psi
es(R
UT
)
H.
pyl
ori
pre
sen
cein
his
tolo
gic
al
exam
inat
ion
59
.2c
20
11
Lim
,2
01
3
[51
]
Cro
ss-
sect
ion
al
Ad
ult
sub
ject
sag
ed1
6y
ears
or
old
erw
ho
vis
ited
hea
lth
care
cen
ters
for
routi
ne
hea
lth
chec
k-u
pbet
wee
nJa
nuar
yan
dD
ecem
ber
2011
in
So
uth
Ko
rea
16
–79
ND
±N
D
N=
10
,79
6
(6,0
85
men
and
4,7
11
wo
men
)
Ser
um
IgG
(EL
ISA
and
EIA
)
54
.4
Rep
ub
lic
of
San
Mar
ino
19
90
–1
99
1G
asb
arri
ni,
19
95
[40]
Cro
ss-
sect
ion
al
Ad
ult
po
pula
tio
n(C
18
yea
rs)
liv
ing
inth
en
ine
dis
tric
tso
fth
e
Rep
ubli
cof
San
Mar
ino
(17,0
00
inhab
itan
ts)
and
sele
cted
from
the
Nat
ion
alR
egis
ter
of
resi
den
tsin
San
Mar
ino
atJa
nu
ary
19
90,
afte
ra
rand
om
stra
tifi
edsa
mpli
ng
wit
hp
rop
ort
ion
alal
loca
tio
nb
yag
e,se
x,
and
dis
tric
t
20
–79
ND
±N
D
N=
2,2
37
(1,0
48
men
and
1,1
89
wo
men
)
Ser
um
IgG
(EL
ISA
)
51
.0
Dig Dis Sci
123
Ta
ble
1co
nti
nu
ed
Cou
ntr
yP
erio
do
f
dat
a
coll
ecti
on
Fir
st
auth
or,
yea
r
of
pu
bli
cati
on
Ty
pe
of
stu
dy
Sam
ple
Ass
essm
ent
of
H.
pyl
ori
infe
ctio
n
stat
us
Pre
val
ence
of
H.
pyl
ori
infe
ctio
n,
wh
ole
sam
ple
(%)
Sel
ecti
on
Ag
e(y
ears
)
rang
e
mea
n±
SD
Siz
e
Sin
gap
ore
19
98
Ch
ua,
20
02
[39
]
Cas
e–
con
tro
l
Contr
ols
wer
ere
cruit
edfr
om
the
par
tici
pan
tsin
ara
ndom
ized
hea
lth
surv
eyo
f1
1,0
00
Sin
gap
ore
anh
ou
seh
old
.T
hes
ein
div
idu
als
wer
en
ot
kn
ow
nto
be
suff
erin
gfr
om
any
gas
troin
test
inal
dis
ease
55
–69
61
.5±
4.1
N=
26
1
(13
0m
enan
d
13
1w
om
en)
Ser
um
IgG
(EL
ISA
)
50
.2
Sw
eden
19
95
So
rber
g,
20
03
[42]
Cro
ss-
sect
ion
al
Ser
um
fro
ma
larg
en
atio
nw
ide
sam
ple
of
blo
od
do
nors
,p
resu
min
gth
at
they
wer
ere
pre
sen
tati
ve
for
the
gen
eral
po
pula
tio
n,
dra
wn
for
the
purp
ose
of
inves
tigat
ing
the
sero
pre
val
ence
of
Bo
rrel
iab
urg
do
rfer
i
infe
ctio
nin
dif
fere
nt
par
tso
fS
wed
en
17
–79
50
.5±
12
.9
N=
3,5
02
Ser
um
IgG
(EL
ISA
)
18
.0
19
95
–1
99
7Y
e,2
00
4
[43
]
Cas
e–
con
tro
l
Contr
ol
subje
cts
wer
era
ndom
lyse
lect
edfr
om
the
conti
nuousl
y
up
dat
edS
wed
ish
Po
pu
lati
on
Reg
iste
ran
dfr
equen
cy-m
atch
edto
rese
mb
leth
eag
e(i
n1
0-y
ear
stra
ta)
and
sex
dis
trib
uti
on
so
fca
se
pat
ien
tsw
ith
eso
phag
eal
aden
oca
rcin
om
a
51
–79
69
±N
D
N=
49
9
(41
4m
enan
d
85
wo
men
)
Ser
um
IgG
(EL
ISA
)
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Dig Dis Sci
123
America (&20 years: ranging from 30 % in Argentina to
70 % in Mexico; &60 years: ranging from 70 % in Chile
to 90 % in Mexico) and Asia (in 1998 the prevalence was
50 % at &20 years and 70 % at &60 years in Republic of
Korea). Studies conducted in the United States of America
yielded prevalences around 20 and 40 % among young
adults and at older ages, respectively, in 1999–2000. In
general, the prevalences of infection were at least two-fold
higher in countries with high gastric cancer incidence, both
in young adults and in older subjects (Fig. 3).
In most countries presenting data for different time
periods, surveys conducted more recently yielded lower
prevalence estimates, though only small variations were
observed when prevalences were already low (Fig. 2). In
Finland, the proportion of pregnant women infected declined
to nearly half between 1983 and 2001. In the Czech
Republic, between 2001 and 2011, the prevalence decreased
from 30 to 10 % in young adults and from 60 to 40 % in
older subjects. In the Republic of Korea, the prevalences
decreased between 1998 and 2005, from 50 to 20 % at
20 years and from 70 to 60 % at 60 years; in 2011 the
prevalences were similar to the observed in 2005. Small
declines were also observed in the United States of America
between 1988–1991 and 1999–2000 at &60 years. In Japan,
H. pylori prevalence was similar in the late 1980s and early
1990s among the older subjects.
Some studies reported prevalence estimates only for the
whole sample, not allowing a direct comparison with data
from other countries. The prevalences were: 71.4 % in
China (35–64 years, 1989); 23 % in Hungary (19–23 years,
1999–2000); 33 % in Iceland [median age ± standard
deviation (SD): 27 ± 0.3 years, 1975–1997]; 46.5 % in
Israel (mean age ± SD: 18.73 ± 0.74 years, 1986–1995);
52.0 % in Lebanon (mean age ± SD: 40.97 ± 15 years,
2008–2009); 50.2 % in Singapore (55–69 years, 1998);
51 % in San Marino (20–79 years, 1990–1991); and 13.4 %
in the United Kingdom (1–84 years, 1986–1996) (Table 1).
Discussion
This study provides an overview of the best available
evidence on the prevalence of H. pylori infection obtained
from studies with national coverage. It shows the expected
020
4060
8010
0
Hel
icob
acte
r py
lori
prev
alen
ce (
%)
0 20 40 60 80
Argentina, 1996
Ecuador, 2001-2002Chile, 2003
Mexico, 1987-1988
Argentina, Chile, Ecuador, Mexico
020
4060
8010
0
Hel
icob
acte
r py
lori
prev
alen
ce (
%)
0 20 40 60 80
20022002-2005
Australia
020
4060
8010
0
Hel
icob
acte
r py
lori
prev
alen
ce (
%)
0 20 40 60 80
20012011
Czech Republic0
2040
6080
100
Hel
icob
acte
r py
lori
prev
alen
ce (
%)
0 20 40 60 80
Age (years)
1983, women
1995, women1989, women
2001, women
Finland
020
4060
8010
0
Hel
icob
acte
r py
lori
prev
alen
ce (
%)
0 20 40 60 80
France, 1995-1997
Latvia, 2008-2009Germany, 1998
France, Germany, Latvia
020
4060
8010
0
Hel
icob
acte
r py
lori
prev
alen
ce (
%)
0 20 40 60 80
1988-1990, men
1990-19941988-1990, women
Japan
020
4060
8010
0
Hel
icob
acte
r py
lori
prev
alen
ce (
%)
0 20 40 60 80
Age (years)
1993-1999
20051998
2011
Republic of Korea
020
4060
8010
0
Hel
icob
acte
r py
lori
prev
alen
ce (
%)
0 20 40 60 80
19951995-1997
Sweden
020
4060
8010
0
Hel
icob
acte
r py
lori
prev
alen
ce (
%)
0 20 40 60 80
Age (years) Age (years) Age (years)
Age (years) Age (years)
Age (years) Age (years)
1988-1991, children1988-1991, adults1999-2000, children1999-2000, adults, men1999-2000, adults, women
United States of America
Fig. 2 Prevalence of Helicobacter pylori infection in different
countries, according to age groups (the median or the mean age of
participants in each age-group were used, whenever available, or,
alternatively, we assumed the mid-point of the age interval) and year
of survey (countries with studies for a single period of data collection
were grouped together)
Dig Dis Sci
123
variation across countries with different gastric cancer
incidence rates; in general, the prevalences of infection
were at least two-fold higher in countries with high risk of
gastric cancer, both in young adults and in older subjects.
Changes leading to a higher socioeconomic status, better
hygiene practices and less household overcrowding may
have had an important contribution to the decrease in the
prevalence of H. pylori infection. However, the cohort
effect associated with these changes has become gradually
less important in some countries, with consequent stabil-
ization of the prevalences [53, 54].
The guidelines for management of H. pylori infection
that have been adopted since the 1990s, targeting subjects
with specific clinical conditions or broader segments of the
population [55–57], may have also contributed to the
observed declines [58].
In the Republic of Korea, which is among the countries
with highest gastric cancer incidence and mortality rates [1,
2], there was a substantial decline in the prevalence of
infection from 1998 to 2005, reaching figures as low as
those observed in settings with already low gastric cancer
risk. Declines to similarly low prevalences were also
observed in the Czech Republic during the last decade.
Conversely, there was little variation when the prevalences
were already low [1, 2], such as in the United States of
America, suggesting that further reductions may require
more intensive prevention (e.g., specific interventions in
child day-care facilities [59] and initiatives to promote
breastfeeding practices [60] may contribute to a lower
frequency of infection in early life) and control efforts.
The evidence generated by the present review is natu-
rally limited by the quality and homogeneity of the original
reports regarding the methods used and the presentation of
results. Most studies evaluated samples from the general
population and relied on the assessment of serum IgG
antibodies to define infection status, which contributes to
the comparability of the studies considered for the review.
However, this method reflects lifetime prevalence of H.
pylori infection, leading to an overestimation of the prev-
alence of current infection. On the other hand, an under-
estimation of the lifetime prevalence may also occur in
older subjects, as infection tends to disappear with the
progression of gastric lesions caused by the bacteria,
leading to a decrease in the circulating IgG titers [61].
This systematic review could also be limited by the fact
that it was based in only one electronic database. However,
publication bias is unlikely, since most large studies with
national coverage are probably published in PubMed
indexed journals, and we do not expect that the magnitude
of the prevalence of H. pylori infection influences the
decision to publish the results. On the other hand, our
database search relied on a comprehensive search expres-
sion, and was complemented by backward citation track-
ing. Nevertheless, the number of studies eligible for this
review was relatively small, and only a few countries had
national data from investigations conducted in different
MEX
AUSFRA
KOR
USA
ARG
CHL
CZE
LTV
SWE
MEX
AUSFRA
KOR
USA
CHL
CZE
JPN
DEU
LTV
SWE
1020
3040
Age
-sta
ndar
dize
d in
cide
nce
rate
/100
.000
(Lo
g sc
ale)
0 20 40 60 80 100
Prevalence of Helicobacter pylori infection (%)
Age 20 years
Age 60 years
Fig. 3 Gastric cancer incidence (retrieved from GLOBOCAN, 2008
[15]) as a function of the prevalence of Helicobacter pylori infection
in different countries (considering the data from samples evaluated
mostly in the late 1990s/early 2000s, according to age groups (strata
with median age closest to 20 and 60 years). ARG Argentina, AUS
Australia, CHL Chile, CZE Czech Republic, DEU Germany, FRA
France, JPN Japan, KOR Republic of Korea, LTV Latvia, MEX
Mexico, SWE Sweden, USA United States of America
Dig Dis Sci
123
years, limiting the assessment of trends in the prevalence of
H. pylori infection. A systematic assessment of high
quality studies with subnational coverage may further
contribute to improve our understanding of the worldwide
trends in the frequency of H. pylori infection.
Among countries with high prevalence of H. pylori
infection there is an ample scope for reducing its burden in
the next decades, through prevention and control. In set-
tings with already low prevalences, further declines will
require a more intensive effort to reduce the frequency of
H. pylori infection.
Acknowledgments The authors gratefully acknowledge the col-
laboration of Bruno Barroso and Helena Carreira for the participation
in the screening of reference lists and data extraction. This work was
supported by ‘‘Fundacao para a Ciencia e a Tecnologia’’ (PTDC/
SAU-EPI/122460/2010 and SFRH/BPD/75918/2011).
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