Helicobacter. 2018;23(Suppl. 1):e12514. wileyonlinelibrary.com/journal/hel
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https://doi.org/10.1111/hel.12514
© 2018 John Wiley & Sons Ltd
1 | GLOBAL PREVALENCE OF
HELICOBACTER PYLORI INFECTION
Two independent systematic reviews and meta- analyses on
Helicobacter pylori global prevalence in the general population were
published recently.1,2 The meta- analysis by Hooi et al1 included
studies published between 1970 and 2016; 183 papers from 62
countries were in the final analysis (11 from Africa, 75 from Asia, 66
from Europe, 13 from Latin America and Caribbean, 13 from North
America, and 5 from Oceania) with a total population of 531 880 in-
dividuals. The meta- analysis by Zamani et al2 included studies from
a more recent time period (from 2000 to 2017); 183 studies from 73
countries in six continents included 410 879 participants.
In the study by Hooi et al,1 the highest prevalence of H. pylori was
found in Africa (79.1%), Latin America and the Caribbean (63.4%),
and Asia (54.7%), and the lowest prevalence in Northern America
(37.1%) and Oceania (24.4%). The authors suggested that approxi-
mately 4.4 billion individuals were infected globally in 2015 which
would account for 60.3% of the global population. At the turn of the
21st century, in highly industrialized countries the prevalence had
decreased, while in developing and newly industrialized countries
it plateaued.1 However, the data on Asia were criticized by Sugano
et al3 who claimed that older data on the prevalence of H. pylori can-
not be used to describe the current situation, in particular, for Japan.
A lower prevalence was suggested by the second meta- analysis2
reporting an overall global H. pylori prevalence of 44.3%, ranging
from 50.8% in developing countries to 34.7% in developed coun-
tries; the prevalence of H. pylori was similar between males (46.3%)
and females (42.7%). Inclusion of publications from different time
periods should not be the cause of differences in the suggested
prevalence since the publication by Hooi et al1 considered the time-
trends. Use of serology may result in an over- estimation of the cur-
rent prevalence; however, this was the predominant test employed
in both analyses. Although the distribution patterns are globally
similar, substantial differences in the prevalences in several areas of
the world were reported in the two studies (eg, in Russia, Portugal,
the Baltic States, Brazil). A possible explanation is the proportion of
studies on children and adults included in the analysis, eg, in Russia,
DOI: 10.1111/hel.12514
REVIEW ARTICLE
Epidemiology of Helicobacter pylori infection
Olga Sjomina1,2 | Jelizaveta Pavlova1 | Yaron Niv3 | Marcis Leja1,2,4
1Institute of Clinical and Preventive
Medicine, Faculty of Medicine, University of
Latvia, Riga, Latvia
2Riga East University Hospital, Riga, Latvia
3Department of Gastroenterology, Rabin
Medical Center, Tel Aviv University, Tel Aviv,
Israel
4Digestive Diseases Centre GASTRO, Riga,
Latvia
Correspondence
Marcis Leja, Institute of Clinical and
Preventive Medicine, 2 Hipokrata iela,
LV1038 Riga, Latvia.
Email: [email protected]
Abstract
This review provides the most recent data concerning the epidemiology of
Helicobacter pylori infection. Overall, the trend of declining prevalence of H. pylori
infection is continuing, with major evidence available from studies in Europe.
However, in some parts of the world, for example, in some countries in the Middle
East, the prevalence has remained relatively stable. A number of systematic reviews
and meta- analyses have been published during the past year indicating the lowest
prevalence rates of the infection in Oceania (24.4%), the highest in Africa (79.1%), and
the global annual recurrence rate of H. pylori (4.3%). The recurrence rates were found
to be directly related to the human development index and prevalence of infection.
Several studies have addressed the correlation between H. pylori infection and socio-
demographic conditions, source of drinking water and dietary factors. A hypothesis
on the role of insects and yeasts in transmitting H. pylori has been suggested and
addressed. Helicobacter sp. have been found in flow flies in Brazil. So far there is no
evidence available that H. pylori may survive and persist on the outer body of the fly.
KEYWORDS
prevalence, recurrence, reservoirs, transmission
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studies on children were predominantly included resulting in a lower
prevalence, while in Latvia only one study on children was included
with a prevalence <20%, and furthermore, the only population-
based study on adults indicated 79.2% prevalence.4 Therefore, ide-
ally, a standardized prevalence study should be performed at the
same time point in different parts of the world; such efforts are cur-
rently being carried out by the International Agency for Research on
Cancer (the ENIGMA study).
Venneman et al5 published another systematic review by ad-
dressing H. pylori prevalence in European countries. A total of 52
studies from 19 countries published until October 2015 were in-
cluded. The lowest H. pylori prevalence was reported in Northern
Europe, while the highest was in Eastern and Southern Europe with
up to 84% in Portugal and Poland. Over time, a decrease in the prev-
alence of H. pylori infection by 19%- 28% throughout the period of
10- 21 years was found.
A systematic review with meta- analysis by Ibrahim et al6 ad-
dressed gender differences in the prevalence of H. pylori infection
in either pediatric populations or adults; the male gender was as-
sociated with a higher prevalence. Recent knowledge concerning
H. pylori virulence factors was reviewed by Kabamba et al7 including
information on population- genetics and human migrations. Several
geographical regions are underrepresented in the human migration
studies performed so far, in particular Central Africa, Northeast
Africa, Central Asia and Siberia.
The key results of selected individual studies and reviews are
briefly summarized below.
1.1 | Europe
A large multicentre study in the Czech Republic8 demonstrated
the decrease in H. pylori prevalence from 41.7% in 2001 to 23.5%
in 2011, with no significant changes in the prevalence of uninvesti-
gated dyspepsia; the authors considered this to be an indirect argu-
ment against any causal role of H. pylori in uninvestigated dyspepsia.
An H. pylori prevalence of 49.8% was found among dyspeptic pa-
tients in Spain.9
Helicobacter pylori seropositivity was reported in 28.9% of
German blood donors from Magdeburg (44.4% CagA positivity
among the H. pylori- positives)10 and in 35.8% of dyspeptic patients
in Poland, marking a substantial decrease from ~75% 10 years
beforehand.11
In Denmark, a population- based cohort study enrolled 3365
healthy subjects in 1982- 1983 to evaluate possible risk factors of
incidental peptic ulcers. Overall, 42.9% were borderline or positive
for H. pylori IgG antibodies.12
1.2 | Near and Middle East
The results of a cross- sectional study in Northeast Iran conducted
from 2010 to 2015, and involving 11 596 participants were reported
by Salehi et al.13 The H. pylori IgG antibody positivity was 72.8%; no
change in the seroprevalence was observed during the study period.
In the same country, Dabiri et al14 studied H. pylori genotype preva-
lence in 160 dyspeptic H. pylori positive patients; vacA, cagA, cagE,
oipA, iceA1, babA2 and babB genes were positive in 100%, 69%,
51%, 55%, 26%,78% and 28% of 160 strains, respectively. The pres-
ence of babB and iceA1 significantly correlated with a higher risk of
gastric cancer (GC) development.
A report from Afghanistan indicated a 75.7% H. pylori positivity
in a dyspeptic patient population.15
1.3 | Africa
Several studies originated from Africa.
The prevalence of H. pylori in dyspeptic patients in Northwest
Ethiopia was 43% in males and 32% in females,16 and higher in
Ghana: 71.1%.17 In the latter study population, vacAs1 was pres-
ent in 69.2%, vacAm1 in 44.7%, vacAm2 in 22.0%, and cagA in
74.8%; but vacAs1/cagA+ was found in 72.6% of the H. pylori pos-
itive individuals.17
A potentially declining prevalence was reported among Algerian
patients; the recent report indicated a 57% prevalence while in the
1980s, it was >80%. Among the 42 bacterial strains isolated from 38
patients, the proportion of haplotypes was: 33 hpEurope and nine
hpNEAfrica.18
Finally, an extensive review of H. pylori epidemiology, haplo-
types, management and resistance in Africa was published by Smith
et al.19 Studies published between 1965 and 2017 were included. In
many African countries, the prevalence among healthy individuals
exceeds 50%, while in dyspeptic patients the prevalence is 90%.
Studies from several countries identified the correlation between
low socioeconomic status and H. pylori prevalence, however, such a
correlation has not been found in Zambia. The devastating poverty
in many parts of the continent did not allow the elimination of risk
factors for H. pylori infection which also includes behavioral prac-
tices, such as premastication of food. The authors concluded that,
although GC incidence is not high in Africa, H. pylori infection is a
major public health challenge. Data on prevalence are not available
from all the countries on the continent.
1.4 | Asia
A meta- analysis involving 170 752 Japanese inhabitants showed that
the prevalence of H. pylori decreased steadily in those born from
1948 to 2003, with a predicted prevalence of infection of 60.9% in
those born in 1910 and 6.6% in those born in 2000. In individuals
born after 1998, H. pylori prevalence was lower than 10%.20
A hospital- based study in southwest China that investigated
H. pylori infection in 10 912 subjects by urea breath test (UBT)
reported a prevalence of 34.4%,21 whereas a multicentre, na-
tionwide prospective study enrolling 4734 asymptomatic Korean
adults in seven geographic areas22 showed a seropositivity in
51.0% of the cases. A higher H. pylori prevalence (80.0%) was
found among Mongolian dyspeptic patients.23 Higher babA-
positivity rates were found in high GC risk countries, Bhutan and
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Myanmar (91.8% and 90.7%, respectively), when compared to
Nepal and Bangladesh.24
Other studies addressed the prevalence of H. pylori genotypes
in Nepal,25 Thailand,26 India,27 and Vietnam.28 In Thailand, the East
Asian type cagA was the predominant genotype among strains from
Hmong, Thai- Chinese and Thai (96.0%, 85.7% and 62.7%, respec-
tively), whilst the Karen had mostly Western- type cagA (73.3%). In
Vietnam, the cagA positivity was 99.4%, and of those, 57.1% were of
East Asian type.28
1.5 | North America
A cross- sectional study, based on the Cernter Health Facts data-
base in the United States and aiming at addressing racial/ethnic
differences in gastrointestinal symptoms and diseases associated
with H. pylori infection, was performed by Huerta- Franco et al.29
The analysis concerned the time period from 2000 to 2015, in-
cluding 11 130 663 patients, among whom 152 086 were positive
for H. pylori. The highest prevalence of the infection was found
in Hispanic and Native American/Alaskan populations. Blacks
and Asian Pacific/Islanders presented the highest relative risk of
dyspepsia, peptic ulcer and atrophic gastritis associated with the
bacteria. Among Korean Americans, the H. pylori prevalence was
found to be 25.3%.30
Another H. pylori prevalence study was reported from Alaska.31
Altogether 710 participants from six communities and one urban city
to represent four geographical regions in Alaska were recruited from
1996 to 1997. The prevalence of the infection was 68%- 69% (de-
pending on the test used). The factors associated with H. pylori pos-
itivitywere:AlaskaNativeracialstatus,age≥20years,ruralregion
of residence, living in a crowded home, and drinking water that was
not piped or delivered.31
A couple of studies addressed H. pylori epidemiology in Hispanic
populations. In Texas, an overall 20% seropositivity in men was
reported based on biorepository samples collected to study pros-
tate cancer. Hispanic origin participants had a significantly higher
prevalence.32
In the Guerrero State of Mexico (southwestern part of the coun-
try), the prevalence of H. pylori among the endoscopy referrals was
30.5%.33 A total of 80% of the strains were vacA s1m1, and the cagA
and babA2 genes were detected in 74% and 32% of the strains, re-
spectively. The most frequent genotypes were vacA s1m1/cagA(+)/
babA2(−) and vacA s1m1/cagA(+)/babA2(+), with a prevalence of
40% (20/50) and 28% (14/50), respectively.
1.6 | Central and South America
A biorepository- based cross- sectional population study (528 sam-
ples) from Puerto Rico reported a 33% prevalence of H. pylori in this
population34; interestingly, the infection was less common among
never- married subjects. Another cross- sectional study in Bolivia
(263 asymptomatic volunteers) found 59% of subjects infected by
H. pylori.35
1.7 | Australia and Oceania
Newly arrived refugees in Australia were found to have a nearly 1.5
times higher prevalence of H. pylori than the Australian population.36
However, in absolute figures, the prevalence of the infection (21.5%)
is generally lower than in most of the previously reported studies on
migrating populations in other parts of the world.37
2 | FACTORS ASSOCIATED WITH
HELICOBACTER PYLORI INFECTION
2.1 | Demographic and socioeconomic factors
Demographic and socioeconomic factors were assessed in a study
by Genta et al38 on 487 587 U.S. residents who underwent upper
endoscopy with biopsy. Increasing levels of income and college edu-
cation were associated with decreasing prevalence of H. pylori gas-
tritis, as well as intestinal metaplasia and gastric atrophy.
Wen et al39 addressed the rural- urban disparity by comparing
the populations in the urban city of Shijiazhuang and rural Shexian
County. Substantially higher rates of GC, as well as H. pylori prev-
alence (75% vs 50%), were found in the rural area. The two popu-
lations (urban vs rural) were characterized by a difference in gross
domestic product (GDP) per capita (US$2700 vs US$6965) and ur-
banization rate (48% vs 100%). Increasing urbanization in the rural
area was associated with a lower prevalence of H. pylori infection
and a decrease in GC.
2.2 | Diet and lifestyle
An observational cross- sectional study on 166 adults in Portugal5
found a higher prevalence of H. pylori in adults with a lower con-
sumption of vegetables and fruit and higher consumption of fried
food; in addition, lower frequency of handwashing before going to
the bathroom and well water consumption was also found to be risk
factors, whereas no association was demonstrated with tobacco, al-
cohol, coffee or other dietary factors.40
The relationship of H. pylori seroprevalence and CagA seropreva-
lence to a number of dietary factors was addressed in a study of 294
adult asymptomatic blood donors in Bulgaria.41 Frequent (>5 days
per week) honey consumption was associated with both reduced
H. pylori seroprevalence (OR, 0.68; 95% CI, 0.473- 0.967) and re-
duced CagA IgG seroprevalence (OR, 0.65; 95% CI, 0.486- 0859).
Frequent (>5 days per week) yoghurt consumption was also asso-
ciated with lower CagA positivity (OR, 0.56; 95% CI, 0.341- 0.921).
2.3 | Reservoirs and transmission
A study from Peru42 added to the previously available evidence that
H. pylori DNA can be identified in drinking water samples; 20.3% of
drinking water samples were found to be contaminated in the Lince
district of Lima. Links were found between lower temperatures and
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a lower likelihood of the presence of H. pylori, as well as between
higher pH and higher quantities of H. pylori.
An interesting hypothesis of H. pylori transmission was sug-
gested by Junqueira et al43 in Brazil. The authors hypothesized that
insects, in particular blowflies and houseflies, might be responsible
for the transmission as they feed with and breed in fecal material.
In their study, 116 individual houseflies and blowflies from varying
habitats on three continents were sampled. Helicobacter sp. reads
were found in 15 blowflies; all were collected in Brazil. The question
whether H. pylori may survive and persist on the outer body of the
fly, remains unanswered.
Another study related to environmental H. pylori reservoirs
was reported from Iran. Siavoshi et al44 studied yeast isolates for
the intracellular occurrence of H. pylori. Yeasts were isolated from
29 samples, including oral swabs from villagers (n = 7), flowers and
fruits (n = 6), honey and honeybees (n = 12) and miscellaneous sam-
ples (n = 4). Amplification products of H. pylori- specific 16S rDNA
(521 bp) were detected in 65% of yeasts. The highest frequency of
H. pylori was found in the honey and bee group (83.3%), as well as
flower and fruit group (83.3%).
3 | HELICOBACTER PYLORI ACQUISITION
A birth cohort of 105 newborns was prospectively studied in
Bangladesh45 from birth up to 24 months of age; 92.8% of the
mothers were carriers of H. pylori, and of these, 93.4% were CagA
positive. Blood samples at birth (cord blood), and at 6, 12, 18, and
24 months of life, and breast milk samples, were analyzed. At the
end of the 2- year follow- up period, 47.6% were positive for H. pylori,
of those 78.0% were CagA positive. A substantial proportion of the
children (58) underwent seroconversion. In addition, this study did
not support previous suggestions that breastfeeding could protect
against H. pylori colonization in breast- fed infants until the age of
~1 year due to the antibody levels in breast milk.45
4 | RECURRENCE OF HELICOBACTER
PYLORI
Recurrence (either by recrudescence or reinfection) is defined as
evidence of an active H. pylori infection in a patient with previously
confirmed H. pylori eradication: recrudescence is the reappearance
of the original infection following an initially false- negative poster-
adication test result, and reinfection can be an infection with a new
strain.46
Hu et al46 performed a systematic review with meta- analysis of
H. pylori recurrence rates worldwide. A total of 132 studies (53 934
patient- years) were analyzed. The global annual recurrence rate of
H. pylori was 4.3%. It was inversely related to the human develop-
ment index (HDI) (3.1%, 6.2% and 10.9% in countries with a very
high, high and medium or low HDI, respectively) and was directly re-
lated to H. pylori prevalence (10.9% 3.7%, 3.4% and 1.6% in countries
with a very high, high, medium or low local H. pylori prevalence).
Rates varied widely among countries from 21.3% in Turkey to a low
of 0.2% in the Netherlands.46,47 Reinfection and recrudescence were
also addressed in 39 studies (16 111 patient- years): the mean annual
reinfection and recrudescence rates were 3.1% and 2.2%, respec-
tively. Globally, there was disappointingly no change in recurrence
rates over the past 27 years, but the rates remained varied across
different regions.46,47
5 | PUBLIC AWARENESS
Driscoll et al48 performed a literature review to assess knowl-
edge, attitudes, and practices of patients or community popula-
tions related to H. pylori transmission, prevention, and associated
morbidity. Of the nine studies published between 1997 and
2014 and included in this review, two were conducted in Eastern
China, two in South Korea, two in North America, and one each
in Ethiopia, India and Malaysia. Generally, the knowledge related
to H. pylori was poor across all studies, even in high GC risk areas.
Only 22%- 35% of the responders had ever heard about H. pylori.
ACKNOWLEDGEMENTS
The work of the team in Latvia was supported in part by a grant from
the Latvian Research Council.
DISCLOSURES OF INTERESTS
The authors have declared no disclosures of interests related to this
work.
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