Helicobacter ISSN 1523-5378 doi: 10.1111/hel.12165

REVIEW ARTICLE

Epidemiology of Helicobacter pylori Infection Leonardo H. Eusebi, Rocco M. Zagari and Franco Bazzoli Department of Medical and Surgical Sciences, Gastroenterology and Endoscopy Unit, Policlinico Sant’Orsola-Malpighi, University of Bologna, Bologna, Italy

Keywords Prevalence, risk factors, transmission, Helicobacter pylori. Reprint requests to: Franco Bazzoli, Department of Medical and Surgical Sciences, Gastroenterology and Endoscopy Unit, Policlinico Sant’Orsola-Malpighi, Bologna, Italy. E-mail: [email protected]

Abstract Medline and PubMed databases were searched on epidemiology of Helicobacter pylori for the period of April 2013–March 2014. Several studies have shown that the prevalence of H. pylori is still high in most countries. In north European and North American populations, about one-third of adults are still infected, whereas in south and east Europe, South America, and Asia, the prevalence of H. pylori is often higher than 50%. H. pylori remains highly prevalent in immigrants coming from countries with high prevalence of H. pylori. However, the lower prevalence of infection in the younger generations suggests a further decline of H. pylori prevalence in the coming decades. Low socioeconomic conditions in childhood are confirmed to be the most important risk factors for H. pylori infection. Although the way the infection is transmitted is still unclear, interpersonal transmission appears to be the main route. Finally, H. pylori recurrence after successful eradication can still occur, but seems to be an infrequent event.

The epidemiology of Helicobacter pylori has been changing over the last decades, with a decline of the prevalence of the infection in most countries. The changing epidemiology of the bacterium has been associated with a parallel decline in peptic ulcer disease and gastric cancer [1] and may have an impact on the changing epidemiology of other diseases, such as gastroesophageal reflux disease, allergies, and asthma [2]. Over the last year, several studies reported data on the prevalence of H. pylori infection in both adults (Table 1) and children (Table 2) in Europe, Canada, Latin America, Asia, and Africa.

Prevalence of Helicobacter pylori Infection In Europe, the prevalence of H. pylori seems to be lower in Northern countries than in Southern and Eastern countries. In the Netherlands, a randomly selected sample of 1550 blood donors from four different regions was tested for the presence of antibodies against H. pylori and the CagA antigen [3]. In this study, only native Dutch subjects were evaluated excluding non-European immigrants. This study reported a 32% prevalence of H. pylori infection, with 28% of H. pyloripositive subjects carrying a CagA-positive strain. The

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seroprevalence of H. pylori declined from 48% in subjects born between 1935 and 1946 to 16% in those born between 1977 and 1987, as a likely consequence of a birth cohort effect. Also the proportion of CagApositive subjects decreased from 38% to 14% in the same age cohorts. These data would suggest that a further reduction of H. pylori prevalence in the Netherlands over the coming decades could be expected. Additionally, from the Netherlands, a populationbased prospective study of a cohort of more than 6500 pregnant women was published [4]. This study found that the prevalence of H. pylori in Dutch women was 24%. The most important finding was that the prevalence of H. pylori was much higher in non-Dutch women with 64% of them being H. pylori seropositive. Moreover, in the latter group, infected subjects born abroad (first-generation immigrants) had a higher risk of H. pylori infection than second-generation immigrants. Thus, ethnicity was a strong predictor for H. pylori in this study. In contrast with northern European countries, a higher prevalence of H. pylori was reported in Portugal, where the prevalence of infection was 84.2%, with 61.7% of strains also positive for CagA [5]. A second evaluation, based on a proportion of included subjects, defined an incidence rate of infection of 3.6/100

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Table 1 Prevalence of Helicobacter pylori infection in adults reported by studies published in 2013

Setting

Number

Diagnostic method

Prevalence of Helicobacter pylori (%)

Blood donors Pregnant women General population

1550 6837 2067

Serology Serology Serology

31.7 46 84.2

Patients with dyspepsia General population

103 4622

PCR UBT

39.8 82.5

Aboriginal population Pregnant women

203 343

Histology Serology

37.9 52.2

Healthy individuals Routine health check-up Patients with dyspepsia

456 10796 2000

28.3 54.4 58

India [13]

Patients with dyspepsia

530

China [11] Bhutan [15]

Healthy individuals Volunteers

5417 372

Patients with dyspepsia Asymptomatic and patients with dyspepsia

244 835

Serology Serology Histology RUT Histology Urease test UBT Histology RUT Culture Serology Serology Serology

Selected population Patients with dyspepsia

1388 429

Patients with dyspepsia

125

Country (Reference) Western Europe The Netherlands [3] The Netherlands [4] Portugal [5] Eastern Europe Cyprus [35] Turkey [6] America Canada [7] Mexico [8] Asia Saudi Arabia [17] Korea [10] India [12]

Bhutan [16] Kazakhstan [14] Africa Ethiopia [21] Morocco [20]

Nigeria [22]

Serology Histology RUT Culture Serology Histology

62 63.4 73.4

86 76.5 65.7 75.5

93.6 80

UBT, urea breath test; RUT, rapid urease test.

Table 2 Prevalence of Helicobacter pylori infection in children reported by studies published in 2013 Age of included subjects (Years)

Number

Diagnostic method

Prevalence of Helicobacter pylori (%)

12–25 13

516 1312

UBT Serology

11 66.2

2–19

129

Histology RUT Culture

41.1

Asia China [26]

1–18

1634

32.1

Iran [27]

1–15

194

Histology RUT Serology

Country (Reference) Western Europe Belgium [23] Portugal [24] America Brazil [25]

50.5

UBT, urea breath test; RUT, rapid urease test.

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person-years, confirming that Portuguese rates of H. pylori infection remain among the highest in Europe. Similar high values were reported in eastern Europe. In Turkey, in a population-based cross-sectional survey, more than 4600 subjects were tested across the country, resulting in a weighted overall prevalence of infection of 82.5% [6]. Interestingly, the prevalence was lowest among individuals living in the southern part of the country who usually have a citrus fruit rich diet, as this is the major citrus fruit-growing area. Indeed, vitamin C is effective in the prevention of most infections; thus, the authors suggested that it might also play a role in H. pylori infection. In North America, the prevalence of H. pylori seems to be similar to northern Europe. Further evidence was provided by a Canadian study where the presence of H. pylori infection was evaluated in 203 aboriginal patients with dyspepsia referred for gastroscopy. H. pylori infection was reported by histology in 37.9% of patients [7]. To the contrary, a study from Mexico [8] confirmed the previously reported [9] high prevalence of H. pylori infection in Latin America. A seroprevalence of 52.2% was reported among 343 pregnant women living in rural areas in Mexico. In Asia, the studies published over the last year showed high prevalence rates of H. pylori infection ranging from 54% to 76% [10–16]. Only one study carried out on healthy individuals in Saudi Arabia showed a low prevalence of infection of about 28% [17]. In Korea, in a large cross-sectional nationwide multicenter study, more than 10,000 asymptomatic subjects without a history of H. pylori eradication were enrolled [10]. The seroprevalence of infection was 54.4%. However, this estimate was lower than that reported in the same country by two similar surveys performed in 1998 [18] and 2005 [19], where the prevalence of H. pylori was 66.9% and 59.6%, respectively. This decrease was significant across all age groups and in most areas of the country. In China, a survey of H. pylori infection was carried out on a sample of the general population from areas with high incidence of gastric cancer [11]. A total of 5417 healthy individuals aged between 30 and 69 years were tested with the 13C-urea breath test. The prevalence of H. pylori infection was 63.4%. Similar high values were reported in India, Kazakhstan, and Bhutan. In India, the prevalence of infection ranged from 58% to 62% in subjects with dyspeptic symptoms [12,13]. In Kazakhstan, among symptomatic and asymptomatic cases, the prevalence of H. pylori infection was 76.5% [14]. Similarly, in Bhutan, the infection was present in 73.4% of cases, although it was lower in the capital city, Thimphu, than in the rural areas, mainly

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related to sanitary conditions [15]. An even higher prevalence rate of 86% was reported from another study in the same country [16]. New data have also been published from African countries. Studies from Morocco and Ethiopia reported a prevalence of H. pylori infection of 75.5% and 65.7%, respectively. Both studies also found a significant increase with age [20,21]. A survey from Nigeria reported higher values: the prevalence was 80% when tested with histology and was even higher, reaching 93.6%, when serology was applied [22]. Finally, several studies investigated the prevalence of H. pylori infection in children, as reported in Table 2. In Belgium, a study carried out on children and young adults reported a prevalence of infection of 11%, ranging from 3.2% in Belgian-born children to 60% in children born of foreign parents coming from countries with a high prevalence of H. pylori infection [23]. Bastos et al. reported a very high prevalence of infection in Portuguese children [24]. Among 13-year-old students from Porto, the prevalence was 66.2%. More than half of the negative subjects were again tested after a median follow-up of 37 months, revealing an incidence rate of 4.1/100 person-years. In Brazil, Pacheco et al. compared several diagnostic tests and reported a high prevalence of 41.1% in subjects aged 2–19 years old [25]. In China, a total of 1634 children and adolescents with upper gastrointestinal symptoms, who underwent gastroscopy with gastric biopsies, were evaluated for the presence of H. pylori infection [26]. The histologic examination of gastric biopsies showed a 32.1% prevalence of H. pylori infection. A higher rate of infection in children was reported in Iran, where Ghasemi-Kebria et al. found a seroprevalence of 50.5%, with 61.7% of children also positive for CagA [27].

Risk Factors for Helicobacter pylori Infection Several studies investigated putative risk factors for H. pylori infection. Gender and age do not seem to be associated with an increased risk of infection. Indeed, most studies reported no significant difference of H. pylori infection between men and women, both in adults [3,13,15–17,20,21] and in children [23,24,27]. No significant association was found between infection and age in the adult population [4,8,13,14,16,17,23]. The age-specific gradient in H. pylori prevalence reported by some studies seems to be related to a birth cohort effect [3,10,20,21,26]. Several socioeconomic factors have been associated with H. pylori infection. In particular, subjects with a low

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socioeconomic status [4,17], measured also as a low family income [10,11], had a higher likelihood of carrying H. pylori infection. Furthermore, an inverse association between educational level and H. pylori infection was found in the majority of the studies [4–6,20]; indeed, except for two cases [8,11], individuals with lower educational levels had a higher risk than those with a higher education. The same association concerning the parents’ education was also found in studies on children [23,24]. Moreover, several factors related to residence have been found to be associated with the infection. Indeed, living in a rural area [10,15,17], in crowded homes [16,17,24], and having contaminated sources of drinking water [6] were risk factors for H. pylori infection. Among the main lifestyle habits, smoking and alcohol consumption showed discordant results: Although in most studies, there was no significant association with H. pylori infection [4,11,20], some authors reported that regular smokers [6,17] and drinkers [17] were at higher risk. In contrast, in one study, regular alcohol drinking was a protective factor for H. pylori infection [6].

Transmission The way H. pylori infection is transmitted is still unclear. Interpersonal transmission appears to be the main route, although environmental transmission, such as drinking contaminated water, remains possible. Parental transmission has been frequently reported. Didelot et al. sequenced the genomes of 97 H. pylori isolates from 52 members of two families living in rural conditions in South Africa [28]. Transmission events were more frequent between close relatives and between individuals living in the same house. Osaki et al. performed a multilocus sequence typing DNA analysis using the stools of parents belonging to three families with a child positive for H. pylori infection [29]. The study showed an intrafamilial transmission in all selected families, with a mother-to-child transmission in at least two families. Urita et al. investigated the intrafamilial transmission of H. pylori infection by testing 838 children and their family members from a small town in Japan [30]. The authors confirmed the mother-to-child transmission and also reported a grandmother-to-child transmission as important mechanism for the spread of H. pylori infection. Indeed, it seems that mothers could transmit the infection through mouth secretions, using common spoons or tasting the child’s food. Grandmothers, on the other hand, take care of their grandchildren when mothers are at work increasing the risk of transmission.

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Helicobacter pylori Recurrence After Eradication Treatment H. pylori recurrence after successful eradication is an infrequent event, usually a combination of both recrudescence of the infection and reinfection. Yan et al. performed a systematic review including previous studies reporting recurrence rates of infection [31]. Only studies performed on adults, with an adequate sample size and a follow-up of at least 6 months, were included. A total of 77 studies with 16,827 patients were included in the analysis, revealing a recurrence rate of 2.8% per patient-year and confirming that areas of low socioeconomic development are more likely to have a higher H. pylori recurrence rate. In Korea, the study by Kim et al. evaluated the reinfection rate during a much longer follow-up period. The mean follow-up was 37 months, and H. pylori reappeared in 3.5% of subjects per year [32]. Carraher et al. estimated the H. pylori reinfection in an Aboriginal community in the Northwest Territories of Canada. The estimated reinfection was 4.7% during the follow-up [33]. A study from Morocco, however, showed much lower rates of reinfection. The recurrence was only 0.42% in the first 6 months and 0.45% after one year [20]. On the other hand, in Latin America, a higher recurrence of H. pylori infection has been observed. A large trial involving 7 countries in which more than 1000 subjects were followed up for 1 year after a successful eradication therapy, confirmed by a negative UBT result, reported an H. pylori recurrence in 11.5% of cases [34].

Conclusions Data from recent studies show that the prevalence of H. pylori infection is still high in most countries worldwide. H. pylori seems to be less frequent in northern European and North American populations; however, about one-third of the adults seem to still be infected. In these countries, H. pylori remains highly prevalent in immigrants coming from countries with a high prevalence of H. pylori. Moreover, the lower prevalence of infection in the younger generations would suggest a further decline in H. pylori prevalence in the community over the coming decades.

Acknowledgements and Disclosures Competing interests: The authors have no competing interests.

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Epidemiology of Helicobacter pylori infection.

Medline and PubMed databases were searched on epidemiology of Helicobacter pylori for the period of April 2013-March 2014. Several studies have shown ...
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