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12514
REVIEW ARTICLE
1
Institute of Clinical and Preventive
Medicine, Faculty of Medicine, University of Abstract
Latvia, Riga, Latvia
This review provides the most recent data concerning the epidemiology of
2
Riga East University Hospital, Riga, Latvia
Helicobacter pylori infection. Overall, the trend of declining prevalence of H. pylori
3
Department of Gastroenterology, Rabin
Medical Center, Tel Aviv University, Tel Aviv, infection is continuing, with major evidence available from studies in Europe.
Israel However, in some parts of the world, for example, in some countries in the Middle
4
Digestive Diseases Centre GASTRO, Riga,
East, the prevalence has remained relatively stable. A number of systematic reviews
Latvia
and meta-analyses have been published during the past year indicating the lowest
Correspondence
prevalence rates of the infection in Oceania (24.4%), the highest in Africa (79.1%), and
Marcis Leja, Institute of Clinical and
Preventive Medicine, 2 Hipokrata iela, the global annual recurrence rate of H. pylori (4.3%). The recurrence rates were found
LV1038 Riga, Latvia.
to be directly related to the human development index and prevalence of infection.
Email: marcis.leja@lu.lv
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
Helicobacter. 2018;23(Suppl. 1):e12514. wileyonlinelibrary.com/journal/hel © 2018 John Wiley & Sons Ltd | 1 of 6
https://doi.org/10.1111/hel.12514
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2 of 6 SJOMINA et al.
studies on children were predominantly included resulting in a lower In the same country, Dabiri et al14 studied H. pylori genotype preva-
prevalence, while in Latvia only one study on children was included lence in 160 dyspeptic H. pylori positive patients; vacA, cagA, cagE,
with a prevalence <20%, and furthermore, the only population- oipA, iceA1, babA2 and babB genes were positive in 100%, 69%,
based study on adults indicated 79.2% prevalence.4 Therefore, ide- 51%, 55%, 26%,78% and 28% of 160 strains, respectively. The pres-
ally, a standardized prevalence study should be performed at the ence of babB and iceA1 significantly correlated with a higher risk of
same time point in different parts of the world; such efforts are cur- gastric cancer (GC) development.
rently being carried out by the International Agency for Research on A report from Afghanistan indicated a 75.7% H. pylori positivity
Cancer (the ENIGMA study). in a dyspeptic patient population.15
Venneman et al5 published another systematic review by ad-
dressing H. pylori prevalence in European countries. A total of 52
1.3 | Africa
studies from 19 countries published until October 2015 were in-
cluded. The lowest H. pylori prevalence was reported in Northern Several studies originated from Africa.
Europe, while the highest was in Eastern and Southern Europe with The prevalence of H. pylori in dyspeptic patients in Northwest
up to 84% in Portugal and Poland. Over time, a decrease in the prev- Ethiopia was 43% in males and 32% in females,16 and higher in
alence of H. pylori infection by 19%-28% throughout the period of Ghana: 71.1%.17 In the latter study population, vacAs1 was pres-
10-21 years was found. ent in 69.2%, vacAm1 in 44.7%, vacAm2 in 22.0%, and cagA in
A systematic review with meta-analysis by Ibrahim et al6 ad- 74.8%; but vacAs1/cagA+ was found in 72.6% of the H. pylori pos-
dressed gender differences in the prevalence of H. pylori infection itive individuals.17
in either pediatric populations or adults; the male gender was as- A potentially declining prevalence was reported among Algerian
sociated with a higher prevalence. Recent knowledge concerning patients; the recent report indicated a 57% prevalence while in the
H. pylori virulence factors was reviewed by Kabamba et al7 including 1980s, it was >80%. Among the 42 bacterial strains isolated from 38
information on population-genetics and human migrations. Several patients, the proportion of haplotypes was: 33 hpEurope and nine
geographical regions are underrepresented in the human migration hpNEAfrica.18
studies performed so far, in particular Central Africa, Northeast Finally, an extensive review of H. pylori epidemiology, haplo-
Africa, Central Asia and Siberia. types, management and resistance in Africa was published by Smith
The key results of selected individual studies and reviews are et al.19 Studies published between 1965 and 2017 were included. In
briefly summarized below. 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
1.1 | Europe
low socioeconomic status and H. pylori prevalence, however, such a
A large multicentre study in the Czech Republic8 demonstrated correlation has not been found in Zambia. The devastating poverty
the decrease in H. pylori prevalence from 41.7% in 2001 to 23.5% in many parts of the continent did not allow the elimination of risk
in 2011, with no significant changes in the prevalence of uninvesti- factors for H. pylori infection which also includes behavioral prac-
gated dyspepsia; the authors considered this to be an indirect argu- tices, such as premastication of food. The authors concluded that,
ment against any causal role of H. pylori in uninvestigated dyspepsia. although GC incidence is not high in Africa, H. pylori infection is a
An H. pylori prevalence of 49.8% was found among dyspeptic pa- major public health challenge. Data on prevalence are not available
tients in Spain.9 from all the countries on the continent.
Helicobacter pylori seropositivity was reported in 28.9% of
German blood donors from Magdeburg (44.4% CagA positivity
1.4 | Asia
among the H. pylori-positives)10 and in 35.8% of dyspeptic patients
in Poland, marking a substantial decrease from ~75% 10 years A meta-analysis involving 170 752 Japanese inhabitants showed that
11
beforehand. the prevalence of H. pylori decreased steadily in those born from
In Denmark, a population-
based cohort study enrolled 3365 1948 to 2003, with a predicted prevalence of infection of 60.9% in
healthy subjects in 1982-1983 to evaluate possible risk factors of those born in 1910 and 6.6% in those born in 2000. In individuals
incidental peptic ulcers. Overall, 42.9% were borderline or positive born after 1998, H. pylori prevalence was lower than 10%. 20
for H. pylori IgG antibodies.12 A hospital-b ased 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-
1.2 | Near and Middle East
tionwide prospective study enrolling 4734 asymptomatic Korean
The results of a cross-sectional study in Northeast Iran conducted adults in seven geographic areas22 showed a seropositivity in
from 2010 to 2015, and involving 11 596 participants were reported 51.0% of the cases. A higher H. pylori prevalence (80.0%) was
by Salehi et al.13 The H. pylori IgG antibody positivity was 72.8%; no found among Mongolian dyspeptic patients. 23 Higher babA-
change in the seroprevalence was observed during the study period. positivity rates were found in high GC risk countries, Bhutan and
SJOMINA et al. |
3 of 6
a lower likelihood of the presence of H. pylori, as well as between with a very high, high, medium or low local H. pylori prevalence).
higher pH and higher quantities of H. pylori. Rates varied widely among countries from 21.3% in Turkey to a low
An interesting hypothesis of H. pylori transmission was sug- of 0.2% in the Netherlands.46,47 Reinfection and recrudescence were
43
gested by Junqueira et al in Brazil. The authors hypothesized that also addressed in 39 studies (16 111 patient-years): the mean annual
insects, in particular blowflies and houseflies, might be responsible reinfection and recrudescence rates were 3.1% and 2.2%, respec-
for the transmission as they feed with and breed in fecal material. tively. Globally, there was disappointingly no change in recurrence
In their study, 116 individual houseflies and blowflies from varying rates over the past 27 years, but the rates remained varied across
habitats on three continents were sampled. Helicobacter sp. reads different regions.46,47
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. 5 | PU B LI C AWA R E N E S S
Another study related to environmental H. pylori reservoirs
was reported from Iran. Siavoshi et al44 studied yeast isolates for Driscoll et al 48 performed a literature review to assess knowl-
the intracellular occurrence of H. pylori. Yeasts were isolated from edge, attitudes, and practices of patients or community popula-
29 samples, including oral swabs from villagers (n = 7), flowers and tions related to H. pylori transmission, prevention, and associated
fruits (n = 6), honey and honeybees (n = 12) and miscellaneous sam- morbidity. Of the nine studies published between 1997 and
ples (n = 4). Amplification products of H. pylori-specific 16S rDNA 2014 and included in this review, two were conducted in Eastern
(521 bp) were detected in 65% of yeasts. The highest frequency of China, two in South Korea, two in North America, and one each
H. pylori was found in the honey and bee group (83.3%), as well as in Ethiopia, India and Malaysia. Generally, the knowledge related
flower and fruit group (83.3%). 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.
A birth cohort of 105 newborns was prospectively studied in The work of the team in Latvia was supported in part by a grant from
45
Bangladesh from birth up to 24 months of age; 92.8% of the the Latvian Research Council.
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
D I S C LO S U R E S O F I N T E R E S T S
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, The authors have declared no disclosures of interests related to this
of those 78.0% were CagA positive. A substantial proportion of the work.
children (58) underwent seroconversion. In addition, this study did
not support previous suggestions that breastfeeding could protect REFERENCES
against H. pylori colonization in breast-fed infants until the age of
1. Hooi JKY, Lai WY, Ng WK, et al. Global prevalence of
~1 year due to the antibody levels in breast milk.45 Helicobacter pylori infection: systematic review and meta-analysis.
Gastroenterology. 2017;153:420‐429.
2. Zamani M, Ebrahimtabar F, Zamani V, et al. Systematic review with
meta-analysis: the worldwide prevalence of Helicobacter pylori in-
4 | R ECU R R E N C E O F H ELI CO BAC TER
fection. Aliment Pharmacol Ther. 2018;47:868‐876.
PY LO R I 3. Sugano K, Hiroi S, Yamaoka Y. Prevalence of Helicobacter pylori
infection in Asia: remembrance of things past? Gastroenterology.
Recurrence (either by recrudescence or reinfection) is defined as 2018;154(1):257‐258.
4. Leja M, Cine E, Rudzite D, et al. Prevalence of Helicobacter pylori
evidence of an active H. pylori infection in a patient with previously
infection and atrophic gastritis in Latvia. Eur J Gastroenterol Hepatol.
confirmed H. pylori eradication: recrudescence is the reappearance 2012;24:1410‐1417.
of the original infection following an initially false-negative poster- 5. Venneman K, Huybrechts I, Gunter MJ, Vandendaele L, Herrero
adication test result, and reinfection can be an infection with a new R, Van HK. The epidemiology of Helicobacter pylori infection in
strain.46 Europe and the impact of lifestyle on its natural evolution toward
stomach cancer after infection: a systematic review. Helicobacter.
Hu et al46 performed a systematic review with meta-analysis of
2018;23:e12483.
H. pylori recurrence rates worldwide. A total of 132 studies (53 934 6. Ibrahim A, Morais S, Ferro A, Lunet N, Peleteiro B. Sex-differences
patient-years) were analyzed. The global annual recurrence rate of in the prevalence of Helicobacter pylori infection in pediatric and
H. pylori was 4.3%. It was inversely related to the human develop- adult populations: systematic review and meta- analysis of 244
studies. Dig Liver Disease. 2017;49(7):742‐749.
ment index (HDI) (3.1%, 6.2% and 10.9% in countries with a very
7. Kabamba ET, Tuan VP, Yamaoka Y. Genetic populations and vir-
high, high and medium or low HDI, respectively) and was directly re- ulence factors of Helicobacter pylori. Infect Genet Evol. 2018;60:
lated to H. pylori prevalence (10.9% 3.7%, 3.4% and 1.6% in countries 109‐116.
SJOMINA et al. |
5 of 6
8. Rejchrt S, Koupil I, Kopacova M, et al. The prevalence and socio- 27. Jeyamani L, Jayarajan J, Leelakrishnan V, Swaminathan M. cagA and
demographic determinants of uninvestigated dyspepsia in the vacA genes of Helicobacter pylori and their clinical relevance. Indian
Czech Republic: a multicentre prospective study accomplished J Pathol Microbiol. 2018;61:66‐69.
10 years after the first study from the same geographical areas. Eur 28. Binh TT, Tuan VP, Dung HDQ, et al. Molecular epidemiology of
J Gastroenterol Hepatol. 2018;30:76‐82. Helicobacter pylori infection in a minor ethnic group of Vietnam: a
9. Varela I, Tarpey P, Raine K, et al. Exome sequencing identifies fre- multiethnic, population-based study. Int J Mol Sci. 2018;19(3):pii:
quent mutation of the SWI/SNF complex gene PBRM1 in renal car- E708.
cinoma. Nature. 2011;469:539‐542. 29. Huerta-Franco MR, Banderas JW, Allsworth JE. Ethnic/racial dif-
10. Franck C, Hoffmann A, Link A, et al. Prevalence of Helicobacter ferences in gastrointestinal symptoms and diagnosis associated
pylori infection among blood donors in Saxony-Anhalt, Germany with the risk of Helicobacter pylori infection in the US. Clin Exp
-a region at intermediate risk for gastric cancer. Z Gastroenterol. Gastroenterol. 2018;11:39‐49.
2017;55:653‐656. 3 0. Stratton MS, Searcy BT, Tobet SA. GABA regulates corticotropin
11. Tacikowski T, Bawa S, Gajewska D, Myszkowska-Ryciak J, Bujko releasing hormone levels in the paraventricular nucleus of the hy-
J, Rydzewska G. Current prevalence of Helicobacter pylori infec- pothalamus in newborn mice. Physiol Behav. 2011;104:327‐333.
tion in patients with dyspepsia treated in Warsaw, Poland. Prz 31. Miernyk KM, Bulkow LR, Gold BD, et al. Prevalence of Helicobacter
Gastroenterol. 2017;12:135‐139. pylori among Alaskans: factors associated with infection and com-
12. Levenstein S, Jacobsen RK, Rosenstock S, Jorgensen T. Mental parison of urea breath test and anti-Helicobacter pylori IgG antibod-
vulnerability, Helicobacter pylori, and incidence of hospital-di- ies. Helicobacter. 2018;23:e12482.
agnosed peptic ulcer over 28 years in a population-based cohort. 32. Long Parma D, Munoz E, Ogden SM, et al. Helicobacter pylori infec-
Scandinavian journal of gastroenterology. 2017;52(9):954‐961. tion in Texas Hispanic and non-Hispanic white men: implications for
13. Salehi M, Ghasemian A, Shokouhi Mostafavi SK, Najafi S, Rajabi VH. gastric cancer risk disparities. Am J Mens Health. 2017;11:1039‐1045.
Sero-prevalence of Helicobacter pylori infection in Neyshabur, Iran, 33. Atrisco-Morales J, Martinez-Santos VI, Roman-Roman A, et al.
during 2010-2015. Iran J Pathol. 2017;12:183‐188. vacA s1m1 genotype and cagA EPIYA-ABC pattern are predominant
14. Dabiri H, Jafari F, Baghaei K, et al. Prevalence of Helicobacter pylori among Helicobacter pylori strains isolated from Mexican patients
vacA, cagA, cagE, oipA, iceA, babA2 and babB genotypes in Iranian with chronic gastritis. J Med Microbiol. 2018;67:314‐324.
dyspeptic patients. Microb Pathog. 2017;105:226‐230. 3 4. Gonzalez-Pons M, Soto-Salgado M, Sevilla J, et al. Seroprevalence
15. Hamrah MH, Hamrah MS, Hassan Hamrah M, et al. Prevalence of Helicobacter pylori in Hispanics living in Puerto Rico: a population-
of Helicobacter pylori infection in dyspeptic patients in Andkhoy based study. Helicobacter. 2018;23(1):e12453.
Afghanistan. Asian Pac J Cancer Prev. 2017;18:3123‐3127. 35. Campolmi I, Spinicci M, Mayaregua DR, et al. Seroprevalence of
16. Kasew D, Abebe A, Munea U, et al. Magnitude of Helicobacter pylori hepatitis A virus, hepatitis E virus, and Helicobacter pylori in rural
among dyspeptic patients attending at University of Gondar Hospital, communities of the Bolivian Chaco, 2013. Am J Trop Med Hyg.
Gondar, Northwest Ethiopia. Ethiop J Health Sci. 2017;27:571‐580. 2018;98:1275‐1280.
17. Archampong TN, Asmah RH, Aidoo EK, et al. Helicobacter pylori 36. Stratton SL, Horvath TD, Bogusiewicz A, et al. Urinary excretion of
cagA and vacA genes in dyspeptic Ghanaian patients. BMC Res 3-hydroxyisovaleryl carnitine is an early and sensitive indicator of
Notes. 2017;10:231. marginal biotin deficiency in humans. J Nutr. 2011;141:353‐358.
18. Raaf N, Amhis W, Saoula H, et al. Prevalence, antibiotic resis- 37. Morais S, Costa AR, Ferro A, Lunet N, Peleteiro B. Contemporary
tance, and MLST typing of Helicobacter pylori in Algiers, Algeria. migration patterns in the prevalence of Helicobacter pylori infection:
Helicobacter. 2017;22(6):e12446. a systematic review. Helicobacter. 2017;22(3):e12372.
19. Smith SI, Seriki A, Ndip R, Pellicano R. Helicobacter pylori infec- 38. Genta RM, Turner KO, Sonnenberg A. Demographic and socio-
tion in Africa: 2018 literature update. Minerva Gastroenterol Dietol. economic influences on Helicobacter pylori gastritis and its pre-
2018; doi: 10.23736/S1121-421X.18.02464-9 . In Press.. neoplastic lesions amongst US residents. Aliment Pharmacol Ther.
20. Wang C, Nishiyama T, Kikuchi S, et al. Changing trends in the prevalence 2017;46:322‐330.
of H. pylori infection in Japan (1908-2003): a systematic review and 39. Wen X, Wen D, Yang Y, Chen Y, Wang G, Shan B. Urban-rural dis-
meta-regression analysis of 170,752 individuals. Sci Rep. 2017;7:15491. parity in Helicobacter pylori infection-related upper gastrointestinal
21. Liu J, Wang Y, Zhao Q, et al. Prevalence and risk factors for cancer in China and the decreasing trend in parallel with socioeco-
Helicobacter pylori infection in southwest China: a study of health nomic development and urbanization in an endemic area. Ann Glob
examination participants based on 13C-urea breath test. Turk J Med Health. 2017;83:444‐462.
Sci. 2017;47:1456‐1462. 4 0. Amaral O, Fernandes I, Veiga N, et al. Living conditions and
22. Lee JH, Choi KD, Jung HY, et al. Seroprevalence of Helicobacter py- Helicobacter pylori in adults. Biomed Res Int. 2017;2017:9082716.
lori in Korea: a multicenter, nationwide study conducted in 2015 41. Yordanov D, Boyanova L, Markovska R, et al. Influence of dietary
and 2016. Helicobacter. 2018;23:e12463. factors on Helicobacter pylori and CagA seroprevalence in Bulgaria.
23. Khasag O, Boldbaatar G, Tegshee T, et al. The prevalence of Gastroenterol Res Pract. 2017;2017:9212143.
Helicobacter pylori infection and other risk factors among Mongolian 42. Boehnke KF, Brewster RK, Sanchez BN, et al. An assessment of
dyspeptic patients who have a high incidence and mortality rate of drinking water contamination with Helicobacter pylori in Lima, Peru.
gastric cancer. Gut Pathog. 2018;10:14. Helicobacter. 2018;23:e12462.
24. Ansari S, Kabamba ET, Shrestha PK, et al. Helicobacter pylori bab 43. Junqueira ACM, Ratan A, Acerbi E, et al. The microbiomes of blow-
characterization in clinical isolates from Bhutan, Myanmar, Nepal flies and houseflies as bacterial transmission reservoirs. Sci Rep.
and Bangladesh. PloS One. 2017;12:e0187225. 2017;7:16324.
25. Sharma RP, Miftahussurur M, Shrestha PK, Subsomwong P, Uchida 4 4. Siavoshi F, Sahraee M, Ebrahimi H, Sarrafnejad A, Saniee P. Natural
T, Yamaoka Y. Nepalese Helicobacter pylori genotypes reflects a fruits, flowers, honey, and honeybees harbor Helicobacter pylori-
geographical diversity than a true virulence factor. Asian Pac J positive yeasts. Helicobacter. 2018;23:e12471.
Cancer Prev. 2017;18:2637‐2641. 45. Kienesberger S, Perez-Perez GI, Olivares AZ, et al. When is
26. Subsomwong P, Miftahussurur M, Vilaichone RK, et al. Helicobacter Helicobacter pylori acquired in populations in developing countries?
pylori virulence genes of minor ethnic groups in North Thailand. Gut A birth-cohort study in Bangladeshi children Gut Microbes. 2018;
Pathog. 2017;9:56. doi: 10.1080/19490976.2017.1421887. In Press.
|
6 of 6 SJOMINA et al.
46. Hu Y, Wan JH, Li XY, Zhu Y, Graham DY, Lu NH. Systematic review
with meta-analysis: the global recurrence rate of Helicobacter pylori. How to cite this article: Sjomina O, Pavlova J, Niv Y, Leja M.
Aliment Pharmacol Ther. 2017;46:773‐779. Epidemiology of Helicobacter pylori infection. Helicobacter.
47. Shah E, Chey WD. Editorial: recurrence of Helicobacter pylori
2018;23(Suppl. 1):e12514. https://doi.org/10.1111/hel.12514
infection-still the same after all these years. Aliment Pharmacol Ther.
2018;47:131‐132.
48. Driscoll LJ, Brown HE, Harris RB, Oren E. Population knowledge,
attitude, and practice regarding Helicobacter pylori transmission and
outcomes: a literature review. Front Public Health. 2017;5:144.