DOI: 10.1111/hel.12514 REVIEW ARTICLE Epidemiology of Helicobacter pylori infection Olga Sjomina1,2 | Jelizaveta Pavlova1 | Yaron Niv3 | Marcis Leja1,2,4 1 Institute of Clinical and Preventive Medicine, Faculty of Medicine, University of Latvia, Riga, Latvia 2 Riga East University Hospital, Riga, Latvia 3 Department of Gastroenterology, Rabin Medical Center, Tel Aviv University, Tel Aviv, Israel 4 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 Digestive Diseases Centre GASTRO, Riga, Latvia East, the prevalence has remained relatively stable. A number of systematic reviews Correspondence Marcis Leja, Institute of Clinical and Preventive Medicine, 2 Hipokrata iela, LV1038 Riga, Latvia. Email: [email protected] prevalence rates of the infection in Oceania (24.4%), the highest in Africa (79.1%), and and meta-­analyses have been published during the past year indicating the lowest 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 1 | G LO BA L PR E VA LE N C E O F H ELI CO BAC TER PY LO R I I N FEC TI O N 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 Two independent systematic reviews and meta-­ analyses on et al3 who claimed that older data on the prevalence of H. pylori can- Helicobacter pylori global prevalence in the general population were not be used to describe the current situation, in particular, for Japan. published recently.1,2 The meta-­ analysis by Hooi et al1 included A lower prevalence was suggested by the second meta-­analysis2 studies published between 1970 and 2016; 183 papers from 62 reporting an overall global H. pylori prevalence of 44.3%, ranging countries were in the final analysis (11 from Africa, 75 from Asia, 66 from 50.8% in developing countries to 34.7% in developed coun- from Europe, 13 from Latin America and Caribbean, 13 from North tries; the prevalence of H. pylori was similar between males (46.3%) America, and 5 from Oceania) with a total population of 531 880 in- and females (42.7%). Inclusion of publications from different time dividuals. The meta-­analysis by Zamani et al2 included studies from periods should not be the cause of differences in the suggested a more recent time period (from 2000 to 2017); 183 studies from 73 prevalence since the publication by Hooi et al1 considered the time-­ countries in six continents included 410 879 participants. trends. Use of serology may result in an over-­estimation of the cur- In the study by Hooi et al,1 the highest prevalence of H. pylori was rent prevalence; however, this was the predominant test employed found in Africa (79.1%), Latin America and the Caribbean (63.4%), in both analyses. Although the distribution patterns are globally and Asia (54.7%), and the lowest prevalence in Northern America similar, substantial differences in the prevalences in several areas of (37.1%) and Oceania (24.4%). The authors suggested that approxi- the world were reported in the two studies (eg, in Russia, Portugal, mately 4.4 billion individuals were infected globally in 2015 which the Baltic States, Brazil). A possible explanation is the proportion of would account for 60.3% of the global population. At the turn of the studies on children and adults included in the analysis, eg, in Russia, Helicobacter. 2018;23(Suppl. 1):e12514. https://doi.org/10.1111/hel.12514 wileyonlinelibrary.com/journal/hel © 2018 John Wiley & Sons Ltd | 1 of 6 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 Cancer (the ENIGMA study). A report from Afghanistan indicated a 75.7% H. pylori positivity in a dyspeptic patient population.15 Venneman et al5 published another systematic review by addressing H. pylori prevalence in European countries. A total of 52 studies from 19 countries published until October 2015 were included. The lowest H. pylori prevalence was reported in Northern 1.3 | Africa 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 addressed gender differences in the prevalence of H. pylori infection 74.8%; but vacAs1/cagA+ was found in 72.6% of the H. pylori positive 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 Africa, Central Asia and Siberia. The key results of selected individual studies and reviews are briefly summarized below. Finally, an extensive review of H. pylori epidemiology, haplotypes, 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%. 1.1 | Europe Studies from several countries identified the correlation between 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 among the H. pylori-­positives)10 and in 35.8% of dyspeptic patients in Poland, marking a substantial decrease from ~75% 10 years 11 beforehand. 1.4 | Asia A meta-­analysis involving 170 752 Japanese inhabitants showed that 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) 1.2 | Near and Middle East reported a prevalence of 34.4%, 21 whereas a multicentre, nationwide 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. Myanmar (91.8% and 90.7%, respectively), when compared to Nepal and Bangladesh. 24 3 of 6 1.7 | Australia and Oceania Other studies addressed the prevalence of H. pylori genotypes Newly arrived refugees in Australia were found to have a nearly 1.5 in Nepal, 25 Thailand, 26 India, 27 and Vietnam. 28 In Thailand, the East times higher prevalence of H. pylori than the Australian population.36 Asian type cagA was the predominant genotype among strains from However, in absolute figures, the prevalence of the infection (21.5%) Hmong, Thai-­Chinese and Thai (96.0%, 85.7% and 62.7%, respec- is generally lower than in most of the previously reported studies on tively), whilst the Karen had mostly Western-­t ype cagA (73.3%). In migrating populations in other parts of the world.37 Vietnam, the cagA positivity was 99.4%, and of those, 57.1% were of East Asian type. 28 1.5 | North America A cross-­s ectional study, based on the Cernter Health Facts database in the United States and aiming at addressing racial/ethnic 2 | FAC TO R S A S S O C I ATE D W ITH H ELI CO BAC TER PY LO R I I N FEC TI O N 2.1 | Demographic and socioeconomic factors differences in gastrointestinal symptoms and diseases associated Demographic and socioeconomic factors were assessed in a study with H. pylori infection, was performed by Huerta-­Franco et al. 29 by Genta et al38 on 487 587 U.S. residents who underwent upper The analysis concerned the time period from 2000 to 2015, in- endoscopy with biopsy. Increasing levels of income and college edu- cluding 11 130 663 patients, among whom 152 086 were positive cation were associated with decreasing prevalence of H. pylori gas- for H. pylori. The highest prevalence of the infection was found tritis, as well as intestinal metaplasia and gastric atrophy. in Hispanic and Native American/Alaskan populations. Blacks Wen et al39 addressed the rural-­urban disparity by comparing and Asian Pacific/Islanders presented the highest relative risk of the populations in the urban city of Shijiazhuang and rural Shexian dyspepsia, peptic ulcer and atrophic gastritis associated with the County. Substantially higher rates of GC, as well as H. pylori prev- bacteria. Among Korean Americans, the H. pylori prevalence was alence (75% vs 50%), were found in the rural area. The two popu- found to be 25.3%. 30 lations (urban vs rural) were characterized by a difference in gross Another H. pylori prevalence study was reported from Alaska.31 domestic product (GDP) per capita (US$2700 vs US$6965) and ur- Altogether 710 participants from six communities and one urban city banization rate (48% vs 100%). Increasing urbanization in the rural to represent four geographical regions in Alaska were recruited from area was associated with a lower prevalence of H. pylori infection 1996 to 1997. The prevalence of the infection was 68%-­69% (de- and a decrease in GC. pending on the test used). The factors associated with H. pylori positivity were: Alaska Native racial status, age ≥20 years, rural region of residence, living in a crowded home, and drinking water that was not piped or delivered.31 2.2 | Diet and lifestyle An observational cross-­sectional study on 166 adults in Portugal5 A couple of studies addressed H. pylori epidemiology in Hispanic found a higher prevalence of H. pylori in adults with a lower con- populations. In Texas, an overall 20% seropositivity in men was sumption of vegetables and fruit and higher consumption of fried reported based on biorepository samples collected to study pros- food; in addition, lower frequency of handwashing before going to tate cancer. Hispanic origin participants had a significantly higher the bathroom and well water consumption was also found to be risk prevalence.32 factors, whereas no association was demonstrated with tobacco, al- In the Guerrero State of Mexico (southwestern part of the coun- cohol, coffee or other dietary factors.40 try), the prevalence of H. pylori among the endoscopy referrals was The relationship of H. pylori seroprevalence and CagA seropreva- 30.5%.33 A total of 80% of the strains were vacA s1m1, and the cagA lence to a number of dietary factors was addressed in a study of 294 and babA2 genes were detected in 74% and 32% of the strains, re- adult asymptomatic blood donors in Bulgaria.41 Frequent (>5 days spectively. The most frequent genotypes were vacA s1m1/cagA(+)/ per week) honey consumption was associated with both reduced babA2(−) and vacA s1m1/cagA(+)/babA2(+), with a prevalence of H. pylori seroprevalence (OR, 0.68; 95% CI, 0.473-­0.967) and re- 40% (20/50) and 28% (14/50), respectively. duced CagA IgG seroprevalence (OR, 0.65; 95% CI, 0.486-­0 859). Frequent (>5 days per week) yoghurt consumption was also asso- 1.6 | Central and South America A biorepository-­based cross-­sectional population study (528 samples) from Puerto Rico reported a 33% prevalence of H. pylori in this ciated with lower CagA positivity (OR, 0.56; 95% CI, 0.341-­0.921). 2.3 | Reservoirs and transmission population34; interestingly, the infection was less common among A study from Peru42 added to the previously available evidence that never-­ married subjects. Another cross-­ sectional study in Bolivia H. pylori DNA can be identified in drinking water samples; 20.3% of (263 asymptomatic volunteers) found 59% of subjects infected by drinking water samples were found to be contaminated in the Lince H. pylori.35 district of Lima. Links were found between lower temperatures and 4 of 6 | SJOMINA et al. 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 suggested by Junqueira et al 43 of 0.2% in the Netherlands.46,47 Reinfection and recrudescence were 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. 3 | H ELI CO BAC TER PY LO R I ACQU I S ITI O N A birth cohort of 105 newborns was prospectively studied in Bangladesh 45 from birth up to 24 months of age; 92.8% of the AC K N OW L E D G E M E N T S The work of the team in Latvia was supported in part by a grant from 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 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 D I S C LO S U R E S O F I N T E R E S T S The authors have declared no disclosures of interests related to this work. 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 | R ECU R R E N C E O F H ELI CO BAC TER PY LO R I 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 posteradication 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%. 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