DOI: 10.1111/hel.

12403

REVIEW ARTICLE

Epidemiology of Helicobacter pylori infection

Christophe Burucoa1 | Anthony Axon2

1
EA 4331 LITEC, University of Poitiers, CHU
Poitiers, Poitiers, France
2
University of Leeds, Leeds, UK
Correspondence
Christophe Burucoa, Laboratoire de
Bactériologie, University of Poitiers, CHU de
Poitiers, Poitiers, France.
Email: Christophe.burucoa@univ-poitiers.fr
Abstract
The study of Helicobacter pylori genetic variability brought us interesting data on the
history of mankind. Based on multilocus sequence typing and more recently on whole-­
genome sequencing, paleomicrobiology still attracts the attention of global research-
ers in relation to its ancestor roots and coexistence with humans. Three studies
determining the prevalence of virulence factors illustrates the controversial results
obtained since 30 years by studies trying to associate prevalence of different virulence
markers and clinical outcomes of H. pylori infection. Three articles analyzed the preva-
lence and risk of multiple (genetically distinct isolates) and mixed (susceptible and re-
sistant isolates) infections. A number of studies confirm that H. pylori prevalence is
falling worldwide especially in the developed world and in children but that the level
of infection is higher in certain ethnic minorities and in Migrants. There is little new in
identifying the mode of H. pylori transmission though intrafamilial spread appears to
be important. There have, however, been some interesting papers on the presence of
the organism in food, water, and the oral cavity.

KEYWORDS
human migration, multiple infection, transmission, virulence factors

1 |  ANCESTOR ROOTS OF H. PYLORI AND
THEIR RELATION TO HUMAN POPULATIONS
Helicobacter pylori was dispersed globally with its human host resulting
in distinct phylogeographic patterns that can be used to reconstruct
both recent and ancient human migrations. Mark Achtman in a recent
paper reviewed the 20 last year researches on this exciting topic.1 A
striking number of parallels were made between the genetic patterns
and sources of native human populations and their associations with
population of H. pylori. But not all geographical patterns are concor-
dant between H. pylori and humans. Some ancestral variants have likely
been lost through the lineage extinction that would be associated with
human population sizes that are too small to stably maintain infection.
A similar pattern was observed in Amerindian in the America, who
were predominantly infected with hpEurope and hpAfrica1 strains that
were imported after 1492.
A recent Latin American (LA) study analyzed the genome of
107 H. pylori strains from Mexico, Nicaragua, and Colombia, and
compared with 59 publicly available worldwide genomes using
a new phylogenetic virtual genome fingerprinting method.2 This
analysis resulted in increased resolution of populations individualiz-
ing a large Latin American cluster of strains distinct from European,
Amerindian, and African clusters already 500 years after the Spanish
colonization.
Another study by analyzing the genome sequence of H. pylori iso-
lated in North, Central, and South America found the evidence for ad-
mixture between H. pylori of European and African origin throughout
the Americas, without substantial input from Amerindian bacteria.3
In the US, strains of African and European origin have remained ge-
netically distinct, while in Colombia and Nicaragua, bottlenecks and
rampant genetic exchange among isolates have led to the formation
of national gene pools. Bacterial populations evolve quickly and can
spread rapidly to people of different ethnicities.
Study by Oleastro et al.4 typed strains isolated in Portugal from
Portuguese and from former Portuguese colonies by multilocus se-
quence typing (MLST) and showed that strains from Portuguese
belong to hpEurope and that the introgression of hpEurope in non-­
European countries that speak Portuguese is low, except for Brazil and
Cape Verde, where hpEurope accounted for one-­quarter and one-­half
of the population, respectively.

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Possibly the most dramatic apparent discrepancy between human
population structure and that of H. pylori is represented by the hpEu-
rope bacterial population. Similar to Europeans, hpEurope is predom-
inant from Western Asia throughout Europe. However, hpEurope is
a hybrid population, representing the descendents of admixture be-
tween the ancestor of hpNEAfrica, now largely restricted to north-­
eastern Africa, and hpAsia2, which is found throughout central and
northern Asia. This admixture event seems to have occurred long after
humans and H. pylori left Africa. Indeed, analyzes of ancient H. pylori
DNA from the Iceman, a 5300-­year-­old copper age mummy from the
Italian Alps, showed that its genomic structure predates that admixture
5
event and its ancestry was almost exclusively from hpAsia2. Finding
pure hpAsia2 in the Italian Alps 5000 years ago suggests that the ad-
mixture that led to hpEurope was even more recent than 5000 years.
However, the human migrations that are known to have occurred
since the Bronze Age do not include a potential wave of migrants who
might have introduced hpNEAfrica strain throughout Western Eurasia.
2 |  PREVALENCE OF VIRULENCE
FACTORS AND ASSOCIATIONS WITH
CLINICAL OUTCOMES
Different studies addressing the prevalence of virulence factor genes
(vacA, cagA, cagE, oipA, babA2, babB, and iceA…) were conducted
over the world trying to associate these virulence factors to clinical
outcomes.
Pinto Ribeiro et al.6 investigated this relationship in 290 patients
from Macau, China. vacAi1 and vacAm1 were detected in 85.2% and
53.6% of the patients that were infected with single genotypes. The
prevalence of cagA-­positive strains was 87.5%. No significant asso-
ciation was observed between vacA genotypes or cagA and gastric
carcinoma. 37.5% of the infected patients had coexistence of H. pylori
strains with different vacA genotypes.
Dabiri et al.7 in 160 H. pylori isolated from Tehran patients, Iran,
detected cagA, cagE, oipA, iceA1, babA2, and babB in 69%, 51%, 55%,
26%, 78%, and 28%. There was no association between the cagA,
vacA, cagE, or iceA status and clinical outcome in patients. Only babB
and iceA1 were significantly associated with higher risk of gastric
­cancer (GC).
A similar study conducted by Safaralizadeh et al.8 in Tabriz, Iran,
only 630 km from Tehran where the previous reported study was con-
ducted, found contradictory results. In Tabriz patients, a significant cor-
relation was found between the presence of cagA and GC.
This discrepancy illustrates the controversial results obtained since
30 years by studies trying to associate prevalence of different genes
supposed or confirmed to be virulence markers and clinical outcomes
of H. pylori infection. Mechanistic experiments have already assessed
or denied such role. Indeed, the clinical outcome of H. pylori infection
toward severe diseases (ulcers, GC) is the result of a complex inter-
play between bacterial virulence factors, host immune response and
alimentary factors. Studying virulence factors only may sometime be
insufficient.
3 | MULTIPLE AND MIXED
H. PYLORI INFECTIONS
Individuals can be infected by either a single or multiple strains of
H. pylori. Multiple infection indicates genetically distinct strains and
mixed infection presence of both antibiotic-­susceptible and resistant
isolates of the same strain. They are difficult to detect but should im-
pact the effectiveness of eradication treatment. Multiple infections
are very often suspected when virulence genes are characterized.6-9
Three articles focused on multiple infections this year.
Ben Mansour et al.9 compared the prevalence of multiple and mixed
H. pylori infection in a developing country, Tunisia, and in a developed
country, France, including 42 H. pylori-­culture positive-­infected pa-
tients (21 Tunisian and 21 French). Three to eleven (mean=9) colonies
were isolated from each antrum biopsy. A total of 375 different iso-
lates were typed using Random Amplified Polymorphic DNA (RAPD)
fingerprinting, and antimicrobial susceptibility testing was performed.
Multiple H. pylori infections were more prevalent in Tunisia (48%)
than in France (5%, P<.001). Mixed infection was common (24%), it
occurred in 19% of Tunisian patients and in 29% of French patients
(P=.46) and was mainly (8/10) due to genetically related clones of the
same strain.
Lai et al.10 used six distinct colonies from each culture plate for
genotyping of the cagA, cagE, cagT, cagM, and vacA s-­or m-­regions.
They evaluated 420 colonies isolated from 70 Taiwanese patients. The
prevalence of multiple infections of all H. pylori-­infected patients was
28.6% (20/70), much higher in patients with duodenal ulcer (47.6%)
than in patients with other gastroduodenal diseases (20%, P<.05).
Mixed infections (metronidazole susceptible and resistant) were ex-
tremely frequent (77%).
Matta et al.11 compared the genomic variability and the rate of
multiple H. pylori infection in patients with chronic gastritis from two
Colombian populations with contrasting GC risks: Túquerres-­Nariño
(high risk) and Tumaco-­Nariño (low risk). Multiple infections were 1.7
times more frequent in Túquerres (55.3%) than in Tumaco (44.7%,
P=.027). Using RAPD fingerprinting, a higher genetic variability was
found in the H. pylori isolates from the population with higher risk of
GC.
4 | RESERVOIRS OF H. PYLORI AND
ITS TRANSMISSION
In spite of the fact that H. pylori is a serious and common infection re-
sponsible for most cases of peptic ulcer and GC, we are still not certain
how the infection is usually transmitted. Epidemics have been caused
iatrogenically by gastric intubation, but the debate continues with ei-
ther the faeco-­oral, oro-­oral, or gastro-­oral routes being the most likely
explanation. However, food and water are also possibilities, and each
of these mechanisms has been addressed in the literature this year.
Intrafamilial transmission is common especially from mother to
child and a study from Iran investigated children aged under 15 years.12
The parents of those with positive urea breath test provided fecal and
BURUCOA and AXON
blood samples. Of 30 families, 10 children had H. pylori genotypes re-
lated to their mothers but only two to their fathers. They concluded
that mother-­to-­child transmission is the main route of intrafamilial
transmission of H. pylori in Iranian families.
Evidence favoring the faeco-­oral route came from a study com-
paring serology for hepatitis A virus (HAV) and H. pylori that found the
adjusted odds of H. pylori seropositivity to be over two times higher
after adjusting for confounders suggesting that H. pylori is transmitted
in the same way as HAV infection.13
14
The oro-­oral route was considered in a review of oral H. pylori.
Helicobacter pylori has been detected in dental plaque, saliva, tongue,
tonsil tissue, root canals, and oral mucosa usually by PCR. However,
the reviewers consider that H. pylori can be identified unequivocally
only through culture because erroneous PCR results can result from
transient H. pylori in the mouth or from food or DNA via reflux from
the stomach, and also from misclassification of other urease-­producing
microorganisms. Therefore, it remains unclear whether H. pylori can
survive in the oral environment. On the other hand, an original arti-
cle this year studied the prevalence of oral H. pylori in asymptomatic
Mexican children under five and reported it to be 13% by PCR, the
results being confirmed by sequencing and showing more than 97%
identity with H. pylori.15
Transmission by infected water has long been a concern and has
been extensively reviewed this year.16 An American article17 studied
the survival of H. pylori through a tertiary wastewater treatment process
using plate cultivation, regular PCR assays and quantitative real-­time
PCR from DNA. Helicobacter pylori was viable in all processed waste-
water samples in the Ann Arbor treatment plant and could be found in
a higher concentration in the receiving Huron River. An Iranian article18
found eight of 450 samples from four separate brands of bottled min-
eral water to be contaminated by H. pylori on culture. Sensitivity test-
ing showed them to be highly resistant to a wide range of antibiotics.
Another study from Iran19 cultured ready to eat food, finding that 74 of
550 (13.4%) samples were positive for H. pylori. Olive salad, restaurant
salad, fruit salad, and soup were the most commonly contaminated.
A Norwegian group20 tested 1,416 subjects of all age groups in an
urban and a rural community in Northern Norway by stool detection
and found H. pylori infection in 0.6% of children, 20% of adolescents,
and rising to 45% in the highest age group. They concluded that trans-
mission might start not only in childhood, but also in adolescence,
where potential transmission routes could be outdoor toilet use, pri-
vate well water, and farm animals.
A Chinese article21 recorded a positive 13C-­urea breath test in 13 of
827 Chinese patients one year after H. pylori eradication (1.75%). A ques-
tionnaire showed peptic ulcer, close contact with infected individuals and
hospitalization to be independent risk factors for H. pylori recurrence.
5 | PREVALENCE OF H. PYLORI AND
RECENT CHANGES
Recent research has consistently shown that the prevalence of
H. pylori is declining in the developed world and especially so in
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children suggesting that the infection will die out in due course. This
is one reason put forward to suggest that population screen and treat
may be unnecessary in these countries. However, this argument takes
no account of ethnic groups, the effects of migration and those eco-
nomically disadvantaged communities where infection rates are often
much higher; therefore, a selective approach to screen and treat might
be considered. The importance of local differences in prevalence is,
therefore, important, and a number of interesting studies have been
reported this year. An excellent review relating to these issues is set
out by Mitchell and Katelaris.22
A number of original studies have focused on children. One study
from Iceland23 studied 205 children aged between 7 and 18 years and
found only 3.4% to be infected. However, the prevalence was 2.6%
among children where both parents were born in a low prevalence
country compared to 17% among those where at least one parent
had been born in a high prevalence area (P=.026). Seroprevalence in
Icelandic adults is 30%-­40%.
Studies from Japan have also shown a considerable fall of H. py-
lori prevalence in childhood. One study from a high GC incidence
area found only 85 of 1,765 (4.8%) students aged 13-­15 years to
be positive,24 and in another the prevalence in school children aged
12-­15  years was 3.1%.25 Inoue26 reported that Japanese gener-
ations born before 1950 have a high prevalence of around 80%-­
90%, decreasing with age to reach around 10% or less in those born
around the 1990s, and less than 2% for those born after year 2000.
Similar trends are seen in China where in Hangzhou27 the positivity
rates were 14.8%, 20.2%, and 25.8% in 3-­6, 7-­11, and 12-­17 years
age groups, respectively, with the overall prevalence decreasing
from 21.6% to 17.2% between 2007 and 2014. In adults undergoing
health checks in urban China,28 the prevalence fell from 31.9% in the
1950-­1959 birth cohort down to 20% in those born after 1990. This
decrease correlated with the increase in per capita gross domestic
product. The prevalence of H. pylori has also declined in Iran29 where
a meta-­analysis estimates an overall prevalence of 54%, with a prev-
alence of 42% in children and 62% in adults. Initial reports of H. py-
lori infection from Iran had earlier indicated a prevalence of more
than 85%. Prevalence continues to decline in Sweden.30 In Latvia on
the other hand there has been no evidence of a fall in prevalence in
children over the last 10 years.31
6 | PREVALENCE OF H. PYLORI
IN MIGRANTS
A systematic review involving 28 studies32 described the prevalence
of H. pylori among migrants. In all but two, the prevalence of H. pylori
was similar to or lower than that in their country of origin but higher
than that of their destination. Second and later generation migrants
had a lower prevalence than first-­generation migrants. An Australian
study33 reported the prevalence and demography of H. pylori in the
refugee population attending the Migrant Health Service in South
Australia, comparing them with the nonrefugee population. Within
the Australian community, estimates of H. pylori prevalence range
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from 15% to 38%, the prevalence in 198 migrants was 21.5%, which
is almost 1.5 times that of the Australian population’s estimate when
both adults and children are included. The likelihood of infection was
lower in females (OR 0.71, 95% CI 0.51-­0.98) than in males. Compared
to Middle Eastern migrants, the likelihood of infection was 1.75 times
higher in African and 1.90 times higher in Burmese migrants. Infection
was not associated with age. They concluded that the high infection
rate and long latency period between infection and the development
of complications, the ready availability of testing and relatively effec-
tive eradication available added weight to a decision to screen this
population.
7 |  PREVALENCE OF H. PYLORI IN
ETHNIC MINORITIES
Several articles this year have addressed the issue of H. pylori preva-
lence in ethnic minorities. These are often not immigrant communi-
ties but as with Australian Aboriginals and Native Americans may
have colonized the country earlier than the currently dominant
community. A total of 16,751 hospital patients in Sichuan province,
Western China were investigated.34 In addition, 18,703 patients from
nine hospital-­based cross-­sectional studies were included in a meta-­
analysis. Helicobacter pylori prevalence declined from 56.6% to 41.1%
between 2008 and 2014. Patients younger than 20 years had the low-
est prevalence (31.9%), while adults aged 40-­49 years had the highest
(42.5%). The ethnic minority population (predominantly Tibetan) had
a higher prevalence (58.9%) than the Han Chinese population (40.8%);
the meta-­analysis also found a higher risk among Tibetan people (OR
1.37, 95% CI 1.24-­1.52, P=.008).
The Tay is the second largest ethnic group in Vietnam. The sero-
prevalence in 1,094 subjects from 278 households was 51.4% in adults
and 41.4% in children. Regular hand washing after defecation and
breastfeeding were protective factors, while infected mothers, first
siblings, and grandparents were risk factors for infection in children.35
Helicobacter pylori prevalence in Indonesia is relatively low. One
study showed in 193 subjects from a low-­
income community in
Northern Jakarta an H. pylori prevalence of only 15%.36 In another
study, 267 patients in Java, Papua, Sulawesi, Borneo, and Sumatra
Islands were examined.37 The overall prevalence was 22.1%, and
Papuan, Batak, and Buginese ethnics had a higher prevalence than
Jacvanese, Dayak and Chinese though numbers were small.
A fascinating paper has investigated H. pylori prevalence in ancient
Malaysian tribes.38 The main subpopulations In Malaysia are Malays,
Chinese, and Indians who have a H. pylori prevalence of 16.4%, 48.1%,
and 61.8%, respectively. However, three Aboriginal tribes (the Orang
Asli) comprise 1% of the Malaysian population and are divided into
three separate tribes (the Negrito, Senoi, and Proto-­Malay) and live
in seven isolated settlements. A total of 275 subjects were studied,
115 (44.7%) were H. pylori positive, the highest seroprevalence being
among Negrito (65.7%), details of their living conditions are given in
detail and prevalence appeared to be related to age, gender, tribe, and
house materials.
D I S C LO S U R ES O F I NT ER ES TS
The authors declare no conflict of interest.
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How to cite this article: Burucoa C, Axon A. Epidemiology of
Helicobacter pylori infection. Helicobacter. 2017;22(Suppl. 1):
e12403. https://doi.org/10.1111/hel.12403