Dynamics of the prevalence of Helicobacter pylori infection from 2015 to 2023

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

BACKGROUND: The global prevalence of Helicobacter pylori infection has decreased from 58.2% (1980–1990) to 43.1% (2011–2022). To develop clinical recommendations for prevention diseases associated with Helicobacter pylori, it is important to assess changes in Helicobacter pylori infection in the world and in the Russian Federation, in particular.

AIM: To assess the dynamics of Helicobacter pylori infection among patients in St. Petersburg, who undergone 13С-urease breath test in the period from 2015 to 2023.

MATERIALS AND METHODS: All the patients have been included in the descriptive study to conduct 13C-urease breath test. If the Delta Over Baseline was less than 2.5‰, the test was considered negative. The value of this indicator of more than 2.5‰ indicated infection with Helicobacter pylori. The database for subsequent statistical analysis included age, gender, the facts of prior eradicative therapy, test results, including degree of infection.

RESULTS: Helicobacter pylori was detected in 32.7% (16,642; 95% confidence interval 32.3–33.1%) of the patients. Of the 50,884 study participants, 83.6% (42,543; 95% confidence interval 83.3–83.9%) of the patients had not received eradication therapy in the past (primary “naive” patients), 16.4% (8341; 95% confidence interval 16.1–16.7%) had undergone eradication therapy in the past therapy (treated “recurrent” patients). The average infection rate among primary patients was 36.1% (15,358; 95% confidence interval 35.6–36.6%), among recurrent patients — 15.4% (1284; 95% confidence interval 14.6–16.2%). From 2015 to 2017, a decrease in Helicobacter pylori infection was detected in “naive” and “recurrent” patients in all the groups by 14.8 and 21.1%, respectively, and from 2020 to 2023 — by 3.6 and 6.2%, respectively. The majority of both primary and recurrent patients showed a very high (IV) degree of infection — 73.0 and 66.5%, respectively.

CONCLUSIONS: The study demonstrated significant reduction of Helicobacter pylori infection from 2015 to 2017 indicating that information from doctors about the importance of diagnosing and treating Helicobacter pylori infection is a priority task. The new coronavirus infection also had an impact on the incidence of the infection; however, it is still unclear what the negative consequences of the active use of antibacterial agents in patients with COVID-19 are, first of all, potential impact on Helicobacter pylori resistance to key antibacterial drugs.

Full Text

BACKGROUND

Helicobacter infection is the most prevalent chronic bacterial infection [1]. About 90% of gastric cancer cases are associated with Helicobacter pylori [2]. The guidelines on preventing, diagnosing, and treating gastric cancer indicate that eradicating H. pylori is a very effective approach to preventing gastric cancer [3].

The epidemiology of H. pylori infection has been determined through noninvasive diagnostic techniques, including identifying H. pylori antigens in fecal specimens and class G immunoglobulins to H. pylori antigens in the blood (serologic method), along with the 13C-urease breath test (13C-UBT). The 13C-UBT is recommended for the primary diagnosis and to monitor eradication efficiency because of its equivalent sensitivity and specificity compared with other invasive and noninvasive methods. The Delta over Baseline value, which measures the increase in 13C content in exhaled air after administering 13C-labeled urea, is positively correlated with Helicobacter urease activity and the number of microbes and reflects the degree of H. pylori contamination of the gastric mucosa [4].

In 2014, approximately 7 million 13C-UBTs were taken in the USA [5]. In contrast, the national 2014 publication reported a maximum of 15–20 thousand such tests per annum in the Russian Federation [6]. According to data from a laboratory that has provided the 13C-UBT service since May 2017 with extensive representation in our country, 42,843 individuals were examined using this method in 2019–2020. These findings suggest a favorable trend toward the use of a noninvasive reference diagnosis of H. pylori infection in Russia [7]. However, this quantity of tests is inadequate for prompt identification and treatment of H. pylori infection to prevent cancer. Russia should conduct at least 1–1.5 million 13C-UBTs annually. Notably, despite regulatory measures, the 13C-UBT is not covered by compulsory health insurance [8].

Assessing the changes in H. pylori infection worldwide and in the Russian Federation in particular is important to develop clinical recommendations to prevent H. pylori-related diseases. Half of the world’s population is thought to be infected with H. pylori; however, annually updated data indicate a decrease in the prevalence of this infection, suggesting the effectiveness of treatment and prevention strategies. The prevalence of H. pylori infection decreased globally from 58.2% during 1980–1990 to 43.1% during 2011–2022 [9].

Significant variations in the prevalence of infection are observed between different countries and within countries, as well as between different subgroups within populations in those countries (such as people of different ages, social statuses, or educational backgrounds). An examination of 410,879 patients from 73 countries across six continents revealed that Nigeria, Serbia, South Africa, Nicaragua, and Colombia have the highest incidence rates of H. pylori infection (89.7%, 88.3%, 86.8%, 83.3%, and 83.1%, respectively), while Yemen, Indonesia, Belgium, Ghana, and Sweden have the lowest (8.9%, 10.0%, 11.0%, 14.2%, and 15%, respectively) [10].

Children are a unique group regarding the diagnosis of Helicobacter infection. Unlike adults, children infected with H. pylori usually show no symptoms, particularly no abdominal symptoms [11]. The “test and treat” strategy, which is popular in some countries, is not recommended for the pediatric population [12]. Studying the prevalence of H. pylori infection in children is valuable for predicting future associated diseases. The prevalence of H. pylori infection varies by country and diagnostic test type. Countries with higher income levels have lower infection rates (21.7%) than low- and middle-income countries (43.2%). Serologic diagnostic methods produce lower infection rates (28.6%), whereas the 13C-UBT produces higher rates (35.9%) [13]. Most studies indicate a rate of asymptomatic H. pylori infection >30% in children, and the overall prevalence among children with digestive symptoms is 40% [14]. Developed countries, such as Japan, Germany, the Netherlands, and the USA, have relatively low reported serologic detection rates of H. pylori in children (7.7%, 11.8%, 9.8%, and 5.7%, respectively). High rates of infection among children have been recorded in Chile, Venezuela, Iran, and Nigeria, with percentages of 27.2%, 65.9%, 25.8%, and 40.4%, respectively [15].

The prevalence of H. pylori infection in Russia, as per the outcome of the 13C-UBT (n = 19,875) between 2017 and 2019, was 38.8%–42.5% [16]. The Southern and Northern Caucasus Federal Districts recorded the highest levels. H. pylori infection among patients aged 41–50 years [17]. Based on the findings from a 2016 study in St. Petersburg among patients with gastrointestinal symptoms (n = 4,181), H. pylori infection was prevalent in 50% of cases. In addition, 55% of patients revealed a substantial level of contamination [18].

Data on the effect of the COVID-19 pandemic on the prevalence of Helicobacter infection are limited, including in the Russian Federation.

A register was established at the North-Western State Medical University named after I.I. Mechnikov, St. Petersburg to evaluate the infection trends among patients referred for Helicobacter diagnosis. This registry, reflecting clinical indicators, encompasses data from 50,884 patients who underwent the 13C-UBT procedure between 2015 and 2023 at the time of data analysis for this study.

MATERIALS AND METHODS

The North-Western State Medical University named after I.I. Mechnikov conducted a descriptive study on the prevalence of Helicobacter infection from 2015 to 2023. This study is a continuation of the research conducted in 2015 [18].

All patients referred for UBT enriched with carbon-13 were included. The 13C-UBT procedure was performed according to a standardized technique using an IRIS infrared spectrometer (Kibion/Wanger, Erlangen, Germany). The principle and the examination procedure for the 13C-UBT have been explained previously [18]. The test was performed using the 4-point technique, which helped to lower the likelihood of false negatives.

The study excluded patients who were administered antimicrobials, bismuth preparations for 1 month, or antisecretory drugs for 2 weeks before testing. The test results were evaluated according to the manufacturer’s instructions. A negative test result (minimal enzymatic hydrolysis of urea) was recorded if the Delta over Baseline value was <2.5. An index value >2.5 indicated the presence of H. pylori infection. This citation verified our research, which compared the accuracy of the 13C-UBT with the H. pylori morphological method for diagnosis, confirming its sensitivity and specificity.

Age, gender, previous eradication treatment, and the test results, including the severity of infection were recorded in the database for subsequent statistical analysis.

The participants were classified into four age categories for the statistical analysis: children (2–17 years), young adults (18–44 years), middle-aged adults (45–59 years), and older adults (>60 years). In addition, cases of infection diagnosed in older individuals (>75 years old) and long-lived individuals (>90 years old) were assessed alongside the elderly population. A comparative analysis was conducted on the frequency of infection during 2015–2017, 2018–2020, and 2021–2023. The key point of division occurred in 2020, which marked the onset of the COVID-19 pandemic in the Russian Federation. The incorporation of azithromycin into the treatment protocols for patients with the new coronavirus infection, in addition to the excessive administration of amoxicillin, clarithromycin, and azithromycin, may have had a significant effect on the occurrence of H. pylori infection.

Data analysis was performed using Microsoft Excel 2016 (Microsoft Inc., Redmond, WA, USA), GraphPad Prism 10.1.0, (GraphPad Software Inc., La Jolla, CA, USA), and Statistica 10 (Statsoft Inc., Tulsa, OK, USA). The Kolmogorov–Smirnov test was used to assess the normality of the distribution with the Lilliefors correction for quantitative indicators. The median and interquartile range [Me (Q25%; Q75%)] was used to explain quantitative indices that were abnormally distributed. Differences were detected using Pearson’s χ2 test. Confidence intervals (CIs) were determined using Fisher’s angular transformation. A p-value < 0.05 was considered significant.

RESULTS

The study included 50,884 patients, and H. pylori was found in 32.7% [16,642; 95% CI 32.3%–33.1%].

Of the 50,884 participants in the study, 83.6% (42,543; 95% CI 83.3%–83.9%) were primary or “naïve” patients who had not undergone eradication therapy, whereas 16.4% (8,341; 95% CI 16.1%–16.7%) were recurrent patients who had received treatment. Primary patients had a younger mean age than the treated patients, with an age of 42.9 (95% CI 31.0–55.0) years compared with 45.8 (34.0–58.0) years (p < 0.05). No differences were observed in the gender composition between the primary and recurrent patients.

Group of patients who have not received eradication therapy in the past (primary patients)

The prevalence of H. pylori infection among primary care patients was 36.1% (15,358; 95% CI 35.6%–36.6%).

No significant differences were observed between the infected and noninfected primary patient groups of males or females. However, infected patients tended to have a higher median age of 44.5 years (33.0; 56.0) compared to 41.9 years (30.0; 55.0) for noninfected patients (p < 0.05). Details of the primary patients, including the distribution by time triad, are presented in Table 1.

 

Table 1. Characteristics of the primary patients included in the study

Таблица 1. Характеристики первичных пациентов, включенных в исследование

Indicator

Positive 13C-urease breath test result

Negative 13C-urease breath test results

Total

Statistical significance

Total number of patients, n (%)

15,358 (36.1)

27,185 (63.9)

42,543 (100)

–

Those examined in 2015–2017, n (%)

3,537 (41.4)

5,016 (58.6)

8,553 (20.1)

p < 0.0001

Those examined in 2018–2020, n (%)

6,431 (36.2)

11,354 (63.8)

17,785 (48.1)

Those examined in 2021–2023, n (%)

5,390 (33.3)

10,815 (66.7)

16,205 (52.8)

Women, n (%)

8,804 (57.3)

15,901 (58.5)

24,705 (58.1)

p < 0.05

Men, n (%)

6,554 (42.7)

11,284 (41.5)

17,838 (41.9)

Mean age, median and interquartile range, years

44.5 (33.0; 56.0)

41.9 (30.0; 55.0)

42.9 (31.0; 55.0)

p < 0.05

Age range, years

4–97

2–93

2–97

 

The majority of primary patients, 73.0% (11,215; 95% CI 72.3%–73.7%), had a very high (IV) grade of infection; a high (III) grade of infection was detected in 11.7% (1,802; 95% CI 11.2%–12.3%), moderate (II) in 10.5% (1,605; 95% CI 10.0%–10.9%), and mild (I) in 4.8% (736; 95% CI 4.5%–5.1%). Table 2 shows a higher number of patients with grade IV infection across all age groups (p < 0.0001). Notably, the H. pylori detection frequency was highest among patients aged 18–44 years, reaching 51.5% (7,918; 95% CI 50.8%–52.3%; p < 0.0001). A significantly higher prevalence of infection was observed among middle-aged patients (aged 45–59 years) than among children, young, or elderly patients. The rates of infection were 76.1% (95% CI 74.8–77.3%) in middle-aged patients vs. 55.0% (95% CI 48.8%–61.1%) in children, 71.7% (95% CI 70.7%–72.7%) in young adults, and 73.5% (95% CI 71.9%–75.2%) in the elderly (p < 0.0001). A higher infection rate was found more frequently in females than males, with 77.3% (6,808; 95% CI 76.4%–78.2%) vs. 67.2% (4,407; 95% CI 66.1%–68.4%) of cases (p < 0.0001).

 

Table 2. Characteristics of the primary patients who had taken the 13C-urease breath test (+) according to sex, age, and degree of infection

Таблица 2. Характеристики первичных пациентов с 13С-уреазным дыхательным тестом (+) в зависимости от пола, возраста, степени инфицированности

Indicator

Patients aged 2–17 years, n (%)

Patients aged 18–44 years, n (%)

Patients aged 45–59 years, n (%)

Patients over 60 years of age, n (%)

Total number of patients, n (%)

Statistical significance

Total

247 (1.6)

7,918 (51.6)

4,401 (28.6)

2,792 (18.2)

15,358 (100)

–

Women

134 (54.3)

4,076 (51.5)

2,675 (60.8)

1,919 (68.7)

8,804 (57.3)

p < 0.0001

Men

113 (45.7)

3,842 (48.5)

1,726 (39.2)

873 (31.3)

6,554 (42.7)

IG I (2.5–3.4)

32 (13.0)

357 (4.5)

183 (4.2)

164 (5.9)

736 (4.8)

p < 0.0001

IG II (3.5–6.4)

47 (19.0)

861 (10.9)

407 (9.2)

290 (10.4)

1,605 (10.5)

IG III (6.5–9.4)

32 (13.0)

1,023 (12.9)

463 (10.5)

284 (10.2)

1,802 (11.7)

IG IV (over 9.5)

136 (55.0)

5,677 (71.7)

3,348 (76.1)

2,054 (73.5)

11,215 (73.0)

Note. IG, infection grade (with reference values).

 

A significant decrease of 18.7% in H. pylori infection was observed among primary patients during the follow-up period, ranging from 51.4% (874; 95% CI 49.0%–53.8%) in 2015 to 32.7% (1,450; 95% CI 31.3%–34.1%) in 2023 (p < 0.0001). The lowest index value was recorded in 2022 at 32.2% (1,904; 95% CI 31.0%–33.4%) (Fig 1).

 

Fig. 1. Change in degree of Helicobacter pylori infection in the primary patients from 2015 to 2023

Рис. 1. Изменение показателя инфицированности Helicobacter pylori у первичных пациентов с 2015 по 2023 г.

 

The infection rate among primary patients decreased 41.4% (3,537; 95% CI 40.3%–42.4%) between 2015 and 2017, 36.2% (6,431; 95% CI 35.5%–36.9%) from 2018 to 2020, and 33.3% (5,390; 95% CI 32.5%–34.0%) between 2021 and 2023 (p < 0.0001). The prevailing age group among the primary patients with confirmed H. pylori infection was 18–44 years. However, prevalence increased significantly during 2021–2023, comprising 54.4% (2,931; 95% CI 53.0%–55.7%) (p < 0.0001) (Table 3). The analysis revealed a significant prevalence of very high (IV) grade of infection (p < 0.0001) during all follow-up periods (Fig. 2).

 

Table 3. Characteristics of the primary patients who received the 13C-urease breath test (+) according to the year of the test, sex, age, and degree of infection

Таблица 3. Характеристика первичных пациентов с 13С-уреазным дыхательным тестом (+) в зависимости от года выполнения теста, пола, возраста и степени инфицированности

Indicator

2015–2017

2018–2020

2021–2023

Total

Statistical significance

Total, n (%)

3,537 (23.1)

6,431 (41.8)

5,390 (35.1)

15,358 (100)

–

Women, n (%)

2,210 (62.5)

3,596 (55.9)

2,998 (55.6)

8,804 (57.3)

p < 0.0001

Men, n (%)

1,327 (37.5)

2,835 (44.1)

2,392 (44.4)

6,554 (42.7)

Mean age, median and interquartile range, years

44.72 (34; 56)

44.68 (33; 56)

44.09 (33; 55)

44.5 (33.0; 56.0)

–

2–17 years old, n (%)

57 (1.6)

121 (1.9)

69 (1.3)

247 (1.6)

p < 0.0001

18–44 years old, n (%)

1,729 (48.9)

3,258 (50.7)

2,931 (54.4)

7,918 (51.5)

45–59 years old, n (%)

1,147 (32.4)

1,864 (28.9)

1,390 (25.8)

4,401 (28.7)

Over 60 years old, n (%)

604 (17.1)

1,188 (18.5)

1,000 (18.5)

2,792 (18.2)

IG I (2.5–3.4), n (%)

116 (3.3)

304 (4.7)

316 (5.8)

736 (4.8)

p < 0.0001

IG II (3.5–6.4), n (%)

313 (8.9)

438 (6.8)

854 (15.9)

1,605 (10.5)

IG III (6.5–9.4), n (%)

334 (9.4)

542 (8.4)

926 (17.2)

1,802 (11.7)

IG IV (over 9.5), n (%)

2,774 (78.4)

5,147 (80.1)

3,294 (61.1)

11,215 (73.0)

Note. IG, infection grade (with reference values).

 

Fig. 2. Distribution of the primary patients according to time triads and degree of infection

Рис. 2. Распределение первичных пациентов по временным триадам и степени инфицированности

 

Group of patients with a history of eradication therapy (recurrent patients)

In patients with a previous history of eradication therapy, a positive 13C-UBT was detected in 15.4% (1,284; 95% CI 14.6%–16.2%). Therefore, eradication efficacy was 84.5%, which is not acceptable for therapy.

The median age was not significantly different between the infected and noninfected groups: 45.8 (35.0–57.0) and 45.8 (34.0–58.0) years respectively (p = 0.85). Furthermore, gender was not a distinguishing factor between the two groups.

Among the primary patients, most of the recurrent patients exhibited a very high (IV) infection grade of 66.5% (854; 95% CI 63.9%–69.0%), followed by a high (III) grade of infection in 10.3% (132; 95% CI 8.7%–12.1%), a moderate (II) grade in 13.9% (179; 95% CI 12.2%–15.9%), and a mild (I) grade in 9.3% (119; 95% CI 7.8%–11.0%). Table 4 shows that patients with grade IV infection were predominant in all age groups (p < 0.0001), despite undergoing antibiotic therapy. Additionally, patients between the ages of 18–44 years had the highest frequency of H. pylori infection at 47.7% (613; 95% CI 45.0%–50.5%) (p < 0.0001). The prevalence of high infection rates was greater in middle-aged patients (aged 45–59 years) than in pediatric, young, or elderly patients, with rates of 72.0% (290; 95% CI 67.4%–76.1%), 64.7% (11; 95% CI 41.3%–82.7%), 64.4% (395; 95% CI 60.6%–68.1%), and 62.9% (158; 95% CI 56.8%–68.7%), respectively (p < 0.05). Women with a significantly higher level of infection were more frequent than men, with prevalence rate of 71.3% (519; 95% CI 67.9%–74.5%) compared with 60.3% (335; 95% CI 56.1%–64.2%) in males (p < 0.0006).

 

Table 4. Characteristics of the recurrent patients who received the 13C-urease breath test (+) according to sex, age, and degree of infection

Таблица 4. Характеристика повторных пациентов с 13С-уреазным дыхательным тестом (+) в зависимости от пола, возраста и степени инфицированности

Indicator

Patients aged 2–17 years, n (%)

Patients aged 18–44 years, n (%)

Patients aged 45–59 years, n (%)

Patients aged over 60 years, n (%)

Total number of patients, n (%)

Statistical significance

Total

17 (1.3)

613 (47.7)

403 (31.4)

251 (19.6)

1284 (100)

 

Women

12 (70.6)

311 (50.7)

236 (58.6)

169 (67.3)

728 (56.7)

p < 0.0001

Men

5 (29.4)

302 (49.3)

167 (41.4)

82 (32.7)

556 (43.3)

IG I (2.5–3.4)

1 (5.9)

51 (8.3)

33 (8.2)

34 (13.5)

119 (9.3)

p = 0.0497

IG II (3.5–6.4)

2 (11.8)

96 (15.7)

43 (10.7)

38 (15.1)

179 (13.9)

IG III (6.5–9.4)

3 (17.6)

71 (11.6)

37 (9.2)

21 (8.4)

132 (10.3)

IG IV (over 9.5)

11 (64.7)

395 (64.4)

290 (72.0)

158 (62.9)

854 (66.5)

Note. IG, infection grade (with reference values).

 

Helicobacter infection was detected in 17.8% (410; 95% CI 16.3%–19.5%) of recurrent patients in 2015–2017, 16.0% (487; 95% CI 14.8%–17.4%) in 2018–2020, and 12.9% (387; 95% CI 11.7%–14.1%) in 2021–2023. The rate of H. pylori infection during the follow-up in recurrent patients decreased threefold from 2015 to 2023, dropping from 39.1% to 13.2% (p < 0.001). Table 5 presents the data on recurrent patients based on age, gender, grade of infection, and time of study. The change in the rate of H. pylori infection in recurrent patients from 2015 to 2023 is depicted in Fig. 3.

 

Table 5. Characteristics of the recurrent patients who received the 13C-urease breath test (+) according to year of test performance, sex, age, and degree of infection

Таблица 5. Характеристика повторных пациентов с 13С-уреазным дыхательным тестом (+) в зависимости от года выполнения теста, пола, возраста и степени инфицированности

Indicator

2015–2017

2018–2020

2021–2023

Total

Statistical significance

Total

410 (31.9)

487 (37.9)

387 (30.2)

1,284 (100)

 

Women, n (%)

244 (59.5)

278 (57.1)

206 (53.2)

728 (56.7)

p = 0.1971

Men, n (%)

166 (40.5)

209 (42.9)

181 (46.8)

556 (43.3)

2–17 years old, n (%)

3 (0.7)

10 (2.1)

4 (1.0)

17 (1.3)

p = 0.0721

18–44 years old, n (%)

188 (45.9)

241 (49.5)

184 (47.5)

613 (47.7)

45–59 years old, n (%)

146 (35.6)

148 (30.4)

109 (28.2)

403 (31.4)

Over 60 years old, n (%)

73 (17.8)

88 (18.1)

90 (23.3)

251 (19.5)

IG I (2.5–3.4), n (%))

40 (9.8)

35 (7.2)

44 (11.4)

119 (9.3)

p < 0.0001

IG II (3.5–6.4), n (%)

49 (12.0)

61 (12.5)

69 (17.8)

179 (13.9)

IG III (6.5–9.4), n (%)

35 (8.5)

34 (7.0)

63 (16.3)

132 (10.3)

IG IV (over 9.5), n (%)

286 (69.8)

357 (73.3)

211 (54.5)

854 (66.5)

Note. IG, infection grade (with reference values).

 

Fig. 3. Change in degree of Helicobacter pylori infection in the recurrent patients from 2015 to 2023

Рис. 3. Изменение показателя инфицированности Helicobacter pylori у повторных пациентов с 2015 по 2023 г.

 

Figure 4 illustrates the variation in the H. pylori infection rates among the primary and recurrent patients between 2015 and 2023. Notably, the infection rates for primary and recurrent patients decreased significantly by 14.8% and 21.1%, respectively from 2015 to 2017. The rates remained relatively stable from 2017 to 2020. However, there were additional decreases of 3.6% and 6.2% for the primary and recurrent patients, respectively from 2020 to 2023.

 

Fig. 4. Change in degree of Helicobacter pylori infection in the primary and recurrent patients from 2015 to 2023

Рис. 4. Изменение показателя инфицированности Helicobacter pylori у первичных и повторных пациентов с 2015 по 2023 г.

 

DISCUSSION

Helicobacter infection is the primary cause of chronic gastritis, precancerous changes in the mucosa (atrophy, metaplasia, and dysplasia), and gastric adenocarcinoma [2]. The infection rate of H. pylori among the population changes [9]. The decrease in infection in recent decades has been associated with the use of eradication therapy. Y. Zhou et al. reported that the rate of spontaneous eradication is 2.9% in children aged 7–12 years [19]. Spontaneous eradication can be induced by antibacterial drugs for indications unrelated to eradication [20].

Given the widespread use of antibacterial drugs against the backdrop of the COVID-19 pandemic in 2020–2021, current research on the dynamics of H. pylori infection among gastroenterology patients from 2015 to 2023 is significant.

Of the 50,884 patients who underwent the 13C-UBT between 2015 and 2023, 83.6% were primary (never having received eradication therapy) and 16.4% were recurrent (indicating at least one course of eradication therapy in the past). The mean incidence of infection among the primary patients was 36.1% (15,358; 95% CI 35.6%–36.6%), whereas the rate was 15.4% (1,284; 95% CI 14.6%–16.2%) among recurrent patients. The prevalence of H. pylori infection was 38.8% among 19,875 patients in a national study conducted between 2017 and 2019 [21]. According to the study design, the detection frequency of H. pylori in patients who had previously undergone eradication therapy may have been associated with eradication failure instead of reinfection.

Our study revealed that the primary and recurrent patients within the 18–44-year age group had the highest frequency of infection at 51.6% and 47.7%, respectively. However, the frequency was the lowest in children, with only 1.6% of primary patients and 1.3% of recurrent patients infected. This finding suggests that social contact after reaching 18 years of age may have contributed to the majority of infections in the study participants. The infection rates were significantly lower in the primary and recurrent patient groups (18.2% and 19.5%, respectively) aged >60 years. This decrease in infection frequency with age could be associated with spontaneous eradication due to the use of antibacterial drugs and/or the progression of atrophic mucosal changes in patients with chronic gastritis [22].

The 13C-UBT enabled the detection of Helicobacter infection and a determination of its severity based on the Delta over Baseline value. The data show that most of the primary and recurrent patients exhibited a very high (IV) grade of infection, with rates of 73.0% and 66.5%, respectively. Bacterial contamination of the gastric mucosa suggests a severe course of Helicobacter gastritis and an increased risk of complications [23].

The infection rate among primary patients decreased during the time triads, with decreases of 41.4% (2015–2017), 36.2% (2018–2020), and 33.3% (2021–2023). The analysis revealed an 18.7% decrease in the incidence of H. pylori infection among primary patients during the follow-up period, from 51.4% in 2015 to 32.7% in 2023 (p < 0.0001). The largest decreases occurred from 2015 to 2016 (7.8%) and from 2016 to 2017 (7%). The percentage of infected patients decreased by 3.6% between 2020 and 2023.

The infection rates in the recurrent patients decreased during the time triads, amounting to 17.8% for 2015–2017, 16.0% for 2018–2020, and 12.9% for 2021–2023. Notably, the indicator decreased nearly threefold from 39.1% to 13.2% during 2015–2023 (Fig. 4) when analyzing the infection rate in recurrent patients. The most significant decrease occurred from 2015 to 2016 (by 19.3%) and from 2020 to 2021 (by 5.1%). The proportion of infected patients decreased by 6.7% from 2020 to 2023.

The infection rates of all groups decreased between 2015 and 2023. The infection rates were 14.8% and 21.1% between 2015 and 2017, respectively, and 3.6% and 6.2% between 2020 and 2023, respectively.

The significant decrease in the incidence of infection in St. Petersburg from 2015 to 2017 was associated with the dissemination of the initial stage of the study findings in 2015 and the proactive execution of eradication work with general practitioners and gastroenterologists. The potential correlation between the repeated decrease in infection rates after 2020 and the spontaneous elimination of H. pylori, coupled with the extensive use of antibacterial agents during the new coronavirus pandemic, specifically amoxicillin, clarithromycin, azithromycin, and levofloxacin, warrants further investigation.

CONCLUSIONS

The findings demonstrated a significant decrease in H. pylori infection between 2015 and 2017, emphasizing the importance of physician education in diagnosing and treating this infection. The COVID-19 pandemic influenced the infection rate, but the adverse effects of antibacterial medications, particularly on H. pylori resistance to some key drug groups, remain uncertain.

ADDITIONAL INFORMATION

Funding. The study had no external funding.

Conflict of interest. The authors declare that there is no potential conflict of interest requiring disclosure in this article.

Author contributions. Thereby, all the authors confirm that their authorship complies with the international ICMJE criteria (all the authors have made a significant contribution to the development of the concept, research, and preparation of the article as well as read and approved the final version before its publication).

Personal contribution of the authors: N.V. Bakulina — experimental design, collecting and preparation of the samples, GC–MS, data analysis, writing the main part of the text, literature review, making final edits, funding acquisition; S.V. Tikhonov, A.V. Zharkov — gas chromatography – mass spectrometry, data analysis, writing the main part of the text; I.V. Savilova — data analysis, writing the main part of the text; V.A. Ponomarenko — collecting and preparation of the samples, writing the main part of the text, literature review.

Ethics approval. Non-interventional study.

ДОПОЛНИТЕЛЬНАЯ ИНФОРМАЦИЯ

Источник финансирования. Исследование проведено без финансового обеспечения и спонсорской поддержки.

Конфликт интересов. Авторы заявляют об отсутствии потенциального конфликта интересов, требующего раскрытия в данной статье.

Вклад авторов. Все авторы подтверждают соответствие своего авторства, согласно международным критериям ICMJE (все авторы внесли существенный вклад в разработку концепции, проведение исследования и подготовку статьи, прочли и одобрили финальную версию перед публикацией).

Наибольший вклад распределен следующим образом: Н.В. Бакулина — концепция и дизайн исследования, сбор и обработка материалов, хроматографическое исследование, анализ полученных данных, написание текста, обзор литературы, внесение окончательной правки; С.В. Тихонов, А.В. Жарков — хроматографическое исследование, анализ полученных данных, написание текста; И.В. Савилова — анализ полученных данных, написание текста; В.А. Пономаренко — сбор и обработка материалов, написание текста, обзор литературы.

Этическое утверждение. Неинтервенционное исследование.

×

About the authors

Natalia V. Bakulina

North-Western State Medical University named after I.I. Mechnikov

Email: nv_bakulina@mail.ru
ORCID iD: 0000-0003-4075-4096
SPIN-code: 9503-8950

MD, Dr. Sci. (Med.), Professor

Russian Federation, Saint Petersburg

Sergey V. Tikhonov

North-Western State Medical University named after I.I. Mechnikov

Email: sergeyvt2702@gmail.com
ORCID iD: 0000-0001-5720-3528
SPIN-code: 6921-5511

MD, Cand. Sci. (Med.)

Russian Federation, Saint Petersburg

Inna V. Savilova

North-Western State Medical University named after I.I. Mechnikov

Email: inna.savilova@gmail.com
ORCID iD: 0000-0001-6463-6663

MD, Cand. Sci. (Med.)

Russian Federation, Saint Petersburg

Alexander V. Zharkov

North-Western State Medical University named after I.I. Mechnikov; Healthcare Committee of the Leningrad Region

Email: al.zharkov@bk.ru
ORCID iD: 0000-0001-6649-0928

MD, Cand. Sci. (Med.)

Russian Federation, Saint Petersburg; Saint Petersburg

Viktoriia A. Ponomarenko

North-Western State Medical University named after I.I. Mechnikov

Author for correspondence.
Email: ponomarenkotori@mail.ru
ORCID iD: 0000-0002-0377-6635

MD, postgraduate student

Russian Federation, Saint Petersburg

References

  1. Hooi JKY, Lai WY, Ng WK et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology. 2017; 153: 420–9.
  2. Malfertheiner P, Megraud F, Rokkas T, Gisbert JP, Liou JM, Schulz C, Gasbarrini A, Hunt RH, Leja M, O'Morain C, Rugge M, Suerbaum S, Tilg H, Sugano K, El-Omar EM; European Helicobacter and Microbiota Study group. Management of Helicobacter pylori infection: the Maastricht VI/Florence consensus report. Gut. 2022 Aug 8:gutjnl-2022-327745. doi: 10.1136/gutjnl-2022-327745. Epub ahead of print. PMID: 35944925
  3. Хатьков И. Е., Абдулхаков С. Р., Алексеенко С. А., Амелина И. Д., Андреев Д. Н., Артамонова Е. В., Н.В. Бакулина и соавт. Российский консенсус по профилактике, диагностике и лечению рака желудка. Злокачественные опухоли 2023 : 13 (2) : 4.
  4. Eisdorfer I, Shalev V, Goren S, Chodick G, Muhsen K. Sex differences in urea breath test results for the diagnosis of Helicobacter pylori infection: a large cross-sectional study/ Biol Sex Differ. 2018; 9: 1. doi: 10.1186/s13293-017-0161-7.
  5. Эльман А.Р., Рапопорт С.И. Стабильно-изотопная диагностика в России: итоги и перспективы. 13С-препараты, приборы, методы. Клиническая медицина. 2014; 92(7): 5-11
  6. Рапопорт Семен Исаакович, Шубина Нина Алексеевна 13-летний период применения 13С-уреазного дыхательного теста для определения Helicobacter pylori в клинической практике в России // Клиническая медицина. 2014. №11.
  7. Абдулова М. С., Игонина Н. А., Торшина И. Г., Чащихина Е. В., Кондрашева Е. А., Гасилова Н. А., Липилина П. А., Насоненко И. В., Аксенова А. В., Долуденко И. И. Оценка ориентировочной популяционной распространенности инфекции Helicobacter pylori и частоты достижения эрадикации после лечения на основе результатов 13С-уреазного дыхательного теста у лиц, обратившихся в федеральную сеть лаборатории ИНВИТРО (2019–2020 гг., n=42 843). Экспериментальная и клиническая гастроэнтерология. 2021;186(2): 47–51. doi: 10.31146/1682-8658-ecg-186-2-47-51
  8. Ивашкин В.Т., Лапина Т.Л., Маев И.В., Драпкина О.М., Козлов Р.С., Шептулин А.А., Трухманов А.С., Абдулхаков С.Р., Алексеева О.П., Алексеенко С.А., Андреев Д.Н., Бордин Д.С., Дехнич Н.Н., Кляритская И.Л., Корочанская Н.В., Осипенко М.Ф., Полуэктова Е.А., Сарсенбаева А.С., Симаненков В.И., Ткачев А.В., Ульянин А.И., Хлынов И.Б., Цуканов В.В. Клинические рекомендации Российской гастроэнтерологической ассоциации, Научного сообщества по содействию клиническому изучению микробиома человека, Российского общества профилактики неинфекционных заболеваний, Межрегиональной ассоциации по клинической микробиологии и антимикробной химиотерапии по диагностике и лечению H. pylori у взрослых. Российский журнал гастроэнтерологии, гепатологии, колопроктологии. 2022;32(6):72–93. https://doi.org/10.22416/1382-4376- 2022-32-6-72-93
  9. Li Y, Choi H, Leung K, Jiang F, Graham DY, Leung WK. Global prevalence of Helicobacter pylori infection between 1980 and 2022: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol. 2023 Jun;8(6):553-564. doi: 10.1016/S2468-1253(23)00070-5. Epub 2023 Apr 20. PMID: 37086739.
  10. Zamani M, Ebrahimtabar F, Zamani V, et al.. Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther 2018;47:868–76. 10.1111/apt.14561
  11. Ravikumara M. Helicobacter Pylori in Children: Think before You Kill the Bug! Therap. Adv. Gastroenterol. 2023;16:17562848231177610. doi: 10.1177/17562848231177610.
  12. Nguyen J, Kotilea K, Bontems P, Miendje Deyi VY. Helicobacter pylori Infections in Children. Antibiotics (Basel). 2023 Sep 12;12(9):1440. doi: 10.3390/antibiotics12091440. PMID: 37760736; PMCID: PMC10525885.
  13. Yuan C, Adeloye D, Luk TT, et al. The global prevalence of and factors associated with Helicobacter pylori infection in children: a systematic review and meta-analysis. Lancet Child Adolesc Health. 2022;6(3):185-194. doi: 10.1016/S2352-4642(21)00400-4
  14. Zabala Torrres B, Lucero Y, Lagomarcino AJ, et al. Review: Prevalence and dynamics of Helicobacter pylori infection during childhood. Helicobacter. 2017;22(5):10.1111/hel.12399. doi: 10.1111/hel.12399
  15. Park JS, Jun JS, Seo JH, Youn HS, Rhee KH. Changing prevalence of Helicobacter pylori infection in children and adolescents. Clin Exp Pediatr. 2021 Jan;64(1):21-25. doi: 10.3345/cep.2019.01543. Epub 2020 Jul 15. PMID: 32668822; PMCID: PMC7806412.
  16. Plavnik R., Nevmerzhitskiy V., Embutniex Yu. et al. The prevalence of Helicobacter pylori in Russia // Helicobacter. 2018. Vol. 23. № S1. P. 24.
  17. Bordin D, Morozov S, Plavnik R, Bakulina N, Voynovan I, Skibo I, Isakov V, Bakulin I, Andreev D, Maev I. Helicobacter pylori infection prevalence in ambulatory settings in 2017-2019 in RUSSIA: The data of real-world national multicenter trial. Helicobacter. 2022 Oct;27(5):e12924. doi: 10.1111/hel.12924. Epub 2022 Aug 16. PMID: 35971900.
  18. Захарова Н.В., Симаненков В.И., Бакулин И.Г., Саблин О.А., Ильчишина Т.А., Захаров Д.В. Распространенность хеликобактерной инфекции у пациентов гастроэнтерологического профиля в Санкт-Петербурге. Фарматека. 2016;Гастроэнтерология/Гепатология:33–9.
  19. Zhou Y, Ye Z, Huang J, Huang Y, Yan W, Zhang Y. High prevalence and low spontaneous eradication rate of Helicobacter pylori infection among schoolchildren aged 7-12 years. Acta Paediatr. 2018 May 3. doi: 10.1111/apa.14387. PMID: 29723912.
  20. Broussard CS, Goodman KJ, Phillips CV, Smith MA, Fischbach LA, Day RS, Aragaki CC. Antibiotics taken for other illnesses and spontaneous clearance of Helicobacter pylori infection in children. Pharmacoepidemiol Drug Saf. 2009 Aug;18(8):722-9
  21. Бордин, Д., Морозов, С., Плавник, Р. и др. Распространенность инфекции Helicobacter pylori в амбулаторных условиях в 2017-2019 гг. в РОССИИ: данные реального национального многоцентрового исследования. Helicobacter. 2022; 00:e12924
  22. Xia HH, Talley NJ. Natural acquisition and spontaneous elimination of Helicobacter pylori infection: clinical implications. Am J Gastroenterol. 1997 Oct;92(10):1780-7. PMID: 9382036.
  23. Varbanova M, Malfertheiner P. Bacterial load and degree of gastric mucosal inflammation in Helicobacter pylori infection. Dig Dis. 2011;29(6):592-9.).

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. Change in degree of Helicobacter pylori infection in the primary patients from 2015 to 2023

Download (52KB)
Indexing metadata
3. Fig. 2. Distribution of the primary patients according to time triads and degree of infection

Download (38KB)
Indexing metadata
4. Fig. 3. Change in degree of Helicobacter pylori infection in the recurrent patients from 2015 to 2023

Download (48KB)
Indexing metadata
5. Fig. 4. Change in degree of Helicobacter pylori infection in the primary and recurrent patients from 2015 to 2023

Download (85KB)
Indexing metadata

Copyright (c) 2023 Eco-Vector

Creative Commons License
This work is licensed under a Creative Commons Attribution-NoDerivatives 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 71733 от 08.12.2017.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies