Prevalence of Helicobacter pylori infection in Chinese military personnel: A cross-sectional, multicenter-based study

Abstract

BACKGROUND

Helicobacter pylori (H. pylori) infection is a prevalent disease encountered in military internal medicine and recognized as the main cause of dyspepsia, gastritis, and peptic ulcer, which are common diseases in military personnel. Current guidelines in China state all patients with evidence of active infection with H. pylori are offered treatment. However, the prevalence of H. pylori infection and its regional distribution in the military population remain unclear, which hinders effective prevention and treatment strategies. Understanding the prevalence of H. pylori infection in the military population will aid in the development of customized strategies to better manage this infectious disease.

AIM

To investigate the prevalence of H. pylori infection in the Chinese military population in different geographic areas.

METHODS

This multicenter, retrospective study included 22421 individuals from five tertiary hospitals located in north, east, southwest, and northwest cities of China. H. pylori infection was identified using the urea breath test, which had been performed between January 2020 and December 2021.

RESULTS

Of the 22421 military service members, 7416 (33.1%) were urea breath test-positive. The highest prevalence of H. pylori was in the 30-39 years age group for military personnel, with an infection rate of 34.9%. The majority of infected subjects were younger than 40-years-old, accounting for 70.4% of the infected population. The individuals serviced in Lanzhou and Chengdu showed a higher infection prevalence than those in Beijing, Nanjing, and Guangzhou, with prevalence rates of 44.3%, 37.9%, 29.0%, 31.1%, and 32.3%, respectively.

CONCLUSION

H. pylori infection remains a common infectious disease among military personnel in China and has a relatively high prevalence rate in northwest China.

Key Words: Helicobacter pylori; Prevalence; Military personnel; Urea breath test; Multicenter study

Core Tip: This multicenter, retrospective study included 22421 participants from five tertiary hospitals located in north, east, southwest, and northwest China and investigated the current prevalence of Helicobacter pylori (H. pylori) infection in Chinese military personnel. The H. pylori infection rate was 33.1%, and the highest prevalence of H. pylori was in the 30-39 years age group. Among military service members, 70.4% of the infected personnel were aged < 40 years. The individuals stationed in Lanzhou and Chengdu showed a higher infection prevalence than those stationed in Beijing, Nanjing, and Guangzhou, with prevalence rates of 44.3%, 37.9%, 29.0%, 31.1%, and 32.3%, respectively.

INTRODUCTION

Helicobacter pylori (H. pylori) infection is estimated to affect approximately 50% of the world’s population, with approximately 4.4 billion individuals infected with H. pylori worldwide[1]. Its prevalence varies considerably with respect to geographical location, economic development, age, ethnicity, health habits, and population lifestyles. The prevalence tends to be low in developed countries (30.2%-39.3%) and high in developing countries (46.8%-54.7%)[2-4]. A continuous decrease in H. pylori prevalence has been reported in many countries, including Korea[5], Iran[6], Austria[7], and China[2,8]. A systematic review showed that the overall prevalence of H. pylori infection in mainland China has been decreasing over the past few decades. Specifically, the infection rate decreased from 58.3% in 1983-1994 to 40.0% in 2015-2019[2]. However, H. pylori infection remains a high-risk factor and a heavy burden in China, and there have been extensive variations in the prevalence of H. pylori infection across different regions. The prevalence was relatively high in the southwest (51.8%) and northwest (46.6%) regions, which could be related to lower economic living standards, unhealthy living habits, and poor environmental factors[2].

Risk factors for H. pylori infection include smoking, occupational risk factors, water supply, food, age, drinking, socioeconomic status, and living environment[3,9]. Since different occupations may represent distinct pathways for acquiring the infection, it is reasonable to assume that it could be much more contagious in closed communities, i.e., among military service members than in the civilian population. H. pylori infection is a common and significant problem in military internal medicine and is recognized as the main cause of dyspepsia, gastritis, and peptic ulcer disease, which are very common in the military population.

Current guidelines, including the recently published “Maastricht VI/Florence consensus report”[10], “Kyoto global consensus report on Helicobacter pylori gastritis”[11], and “Sixth Chinese national consensus report on the management of Helicobacter pylori infection” recommend eradicating H. pylori infection unless there are competing considerations[12]. However, evidence on the prevalence of H. pylori infection and its regional variation, particularly from large-scale and multiregional investigations in the military population, is scarce, hindering the establishment of effective prevention and treatment strategies for military personnel.

Moreover, most studies were conducted in the 1990s. Studies from other countries have reported a lower prevalence of infection in military population than in the general population[9]. A recent single hospital-based study in Shenyang, northeast China, showed that the prevalence of H. pylori infection in military service members was 33.9%, which was similar to that in the civilian population[13]. Furthermore, among the population aged 17-25 years, the infection rate was much higher in the military group than in the civilian group (35.6% vs 25.9%)[13]. Understanding the prevalence of H. pylori infection and its regional variation in the military population will aid in the development of customized strategies to better manage this infectious disease, with the premise of up-to-date information. The study presented herein aimed to determine the prevalence of H. pylori infection in military servicemen with a large sample from five tertiary hospitals located in the northwest, southeast, north, south, and southwest cities of China to help establish strategies for the prevention and eradication of H. pylori infection and related diseases in military servicemen.

MATERIALS AND METHODS

Participants and study design

This multicenter, retrospective study was performed in five tertiary hospitals in China, including Chinese People’s Liberation Army General Hospital in Beijing, General Hospital of Eastern Theater Command in Nanjing, General Hospital of Western Theater Command in Chengdu, General Hospital of Southern Theater Command in Guangzhou, and the 940^th Hospital of Joint Logistic Support Force of Chinese People’s Liberation Army in Lanzhou. H. pylori infection was identified by the urea breath test (UBT), which was performed between January 2020 and December 2021. The identity of eligible participants was recognized as military personnel based on their unique identity document numbers obtained from the electronic medical record system.

The exclusion criteria were as follows: (1) Lack of the disintegrations per minute (DPM) values for ¹⁴C-UBT or the delta-over-baseline (DOB) values for ¹³C-UBT; (2) Individuals aged > 79 years; (3) Missing information on demographics and/or individuals’ identity records; and (4) Repeated UBTs performed in the same individual. We primarily collected information regarding demographics (i.e., age and sex) and H. pylori infection status. This study was a retrospective study and did not obtain consent from all the patients. We had applied for a waiver of the informed consent form, and it was approved by the Medical Ethical Committee of the Chinese People’s Liberation Army General Hospital (Approval No. S2022-358-01).

Diagnosis of H. pylori infection

The UBT, including ¹³C and ¹⁴C, was used to identify H. pylori infection status. ¹³C-UBT was performed after an overnight fast. The baseline exhaled breath samples were collected by blowing through a disposable plastic straw into a CO₂ storage container. Then, patients were instructed to ingest the test meal with 75 mg of ¹³C-urea dissolved in 100 mL of water. Further, breath samples were collected 30 minutes after ingestion of the tracer. Breath samples were subjected to infrared spectroscopy for H. pylori detection. The results were presented as DOB values. According to the manufacturer, a DOB ≥ 4% indicates a diagnosis of H. pylori infection.

¹⁴C-UBT was performed after an overnight fast. Patients were instructed to take a ¹⁴C-urea (27.8 kBq) capsule with warm water. Breath samples were collected in a special bottle containing CO₂ gas collector 15 minutes after ingestion. Each breath sample was trapped in a 4.5 mL diluted scintillation solution. ¹⁴C content was measured in DPM mode using a liquid beta-scintillation counter. A cutoff value of 100 was set for the positive test result.

Statistical analyses

All statistical analyses were performed using SPSS statistical software version 26.0 (IBM Corp., Armonk, NY, United States). Categorical variables were expressed as frequency (percentage). Subgroup analyses were performed based on age, sex, and region. A two-sided P < 0.05 was considered statistically significant.

RESULTS

Participant characteristics

A total of 22421 individuals were included after excluding 227 cases lacking DOB values for ¹³C-UBT or DPM values for ¹⁴C-UBT, 2211 cases lacking medical records, 751 individuals older than 79 years, and 1819 cases with repeated tests (Figure 1). The ratio of males to females in the military group was 4.3:1. The majority of individuals were younger than 40-years-old, with 28.1% in the 18-29 years age group and 39.3% in the 30-39 years age group. The number of subjects collected from Beijing, Chengdu, Guangzhou, Lanzhou, and Nanjing were 6659, 1048, 1348, 3771, and 9595, respectively (Table 1).

Figure 1 Study flowchart for participant inclusion. DOB: Delta-over-baseline; DPM: Disintegration per minute; ¹³C-UBT: Carbon-13 urea breath test; ¹⁴C-UBT: Carbon-14 urea breath test.

Table 1 Characteristics of the eligible participants.

Characteristic	n	%
Total	22421	100
Sex
Female	4263	19.0
Male	18158	81.0
Age group in year
18-29	6301	28.1
30-39	8818	39.3
40-49	3487	15.6
50-59	2244	10.0
60-69	1138	5.1
70-79	433	1.9
Hospital location
Beijing	6659	29.7
Chengdu	1048	4.7
Guangzhou	1348	6.0
Lanzhou	3771	16.8
Nanjing	9595	42.8

H. pylori infection prevalence

Overall prevalence in the military personnel: Among the 22421 military cases, 7416 cases were UBT-positive, with an infection rate of 33.1%. No significant differences were observed between males and females (Table 2).

Table 2 Overall prevalence of Helicobacter pylori infection.

Parameter	Prevalence, % (n/total)	P value
Total	33.1 (7416/22421)
Sex		0.771
Male	33.1 (6014/18158)
Female	32.9 (1402/4263)
Age group in year		< 0.001
18-29	33.9 (2137/6301)
30-39	34.9 (3080/8818)
40-49	31.8 (1108/3487)
50-59	29.6 (664/2244)
60-69	26.2 (298/1138)
70-79	29.8 (129/433)
Hospital location		< 0.001
Beijing	29.0 (1929/6659)
Chengdu	37.9 (397/1048)
Guangzhou	32.3 (435/1348)
Lanzhou	44.3 (1671/3771)
Nanjing	31.1 (2984/9595)

Age demographics and H. pylori infection: The highest prevalence of H. pylori was in the age group of 30-39 years for military personnel, with infection rates of 34.9%, followed by the age groups of 18-29 years (33.9%), 40-49 years (31.8%), 50-59 years (29.6%), and 60-69 years (26.2%) (Figure 2A).

Figure 2 Prevalence of Helicobacter pylori infection in different groups. A: Age; B: Location.

H. pylori prevalence in different regions: Among military personnel, Lanzhou had the highest prevalence, followed by Chengdu (44.3% and 37.9%, respectively). On the contrary, Beijing, Nanjing, and Guangzhou were among the areas with lower prevalence (29.0%, 31.1%, and 32.3%, respectively) (Figure 2B).

DISCUSSION

A cross-sectional, multicenter-based study was conducted to investigate the prevalence of H. pylori infection among military service members in China. Patients from five participating hospitals located in north, east, south, southwest, and northwest China and the military members of active-duty service in combat and non-combat army were included. The H. pylori infection rate in the military group was 33.1% in our study.

There remains a high H. pylori infection rate in the Chinese army, especially when approximately 70% of the infected individuals are under the age of 40, which is an important part of the insurance of their health and effectiveness. Based on the data of this study, we infer that the actual prevalence of H. pylori infection in the Chinese military population should be lower than that found in this study because this was a hospital-based study, and most individuals were patients with gastrointestinal complaints. In line with most other studies, we showed that individuals from the armed forces had a lower prevalence of infection than the general population of the same country[9,14]. This result may be explained by the fact that most individuals in the military group were in the younger age group.

The prevalence of H. pylori infection in military populations varies among countries. The prevalence obtained in our study was higher than that reported in other countries; H. pylori seropositivity rate was 26.3% in army recruits in the United States[15], 33% in male recruits in Hungary[16], and 19.01% in navy recruits in Greece[17]. A recent systematic review and meta-analysis revealed that the overall prevalence of H. pylori infection was 32% in military personnel, with a lower rate of 19.9% in North America and 21.1% in Europe and a higher rate of 50.2% in Asia[18]. This rate may be related to the overall prevalence in the civilian population, national socioeconomic conditions, and military environment.

Although we could not obtain the exact risk factors for infection in the military population from the five hospitals by the retrospective data analysis, geographical location was found to be the important factor related with the infection rate. The data from the 940^th Hospital in Lanzhou showed that the prevalence was 44.3%, followed by 37.9% prevalence from the General Hospital of Western Theater Command in Chengdu. These two hospitals are located in the northwest and southwest regions of China, which have a low socioeconomic status. In contrast, in economically developed areas, such as Beijing (29.0%), Nanjing (31.1%), and Guangzhou (32.3%), the infection rate was relatively low. Similarly, a recent meta-analysis showed that the infection rate of H. pylori among the civilian population in China was relatively high in the northwest and southwest regions, which could be related to the lower economic living standards and poor environmental factors[19].

Among military service members with no significant difference in economic income in different regions, it is reasonable to speculate that the infection could be much more contagious if they had been exposed to harsher living environments attributed to performing tasks in fields or other special environments. Indeed, one of the most common risk factors for infection is the living environment of military personnel[18]. Military personnel in the United States were reported to be at an increased risk of H. pylori infection, with a rate of 1.9% per person-year when they were exposed in developing countries[20]. Similarly, the annual seroconversion rate was 7.3% in a group of army personnel from the United States after they served in the Persian Gulf[21]. Military personnel often work in close quarters, which increases the risk of H. pylori transmission. In challenging conditions, proper disinfection of tableware is often insufficient. Serving individual portions can be difficult, and sharing food using the same utensils or dishes is considered a significant risk factor for H. pylori infection[22].

In our study, infection rates in military personnel were not different between sexes, which may be attributed to the relatively small sample size of females. Considering age stratification, up to 70% of the patients who were H. pylori-positive were younger than 40 years. The proportion of soldiers or combat personnel is high among young recruits, and most lived in remote areas with poor sanitary environments and shared the same dormitory in barracks, which may have increased H. pylori infection and transmission. Young military personnel have more frequent high-intensity military activities, which may increase the risk of H. pylori infections[23]. In this study, a lower infection rate was found in the elder group, which may be related due to this group serving as non-combat personnel with better sanitary conditions or some individuals having received H. pylori eradication in time during their routine health check.

Considering age-stratified prevalence, our study found that people aged 30-39 years had the highest infection rate, consistent with a study assessing prevalence in a region with high-risk for gastric cancer[24,25]. However, it was inconsistent with other studies suggesting that infection rate gradually increases with age[2]. This may be attributed to different populations of subjects. This study was performed among military personnel, and they are mainly young and middle-aged, having a different age structure than the general population. This may also be attributed to different methods for evaluating prevalence, as UBT was used in our study and seroprevalence or stool antigen was used in other studies. Our study used ¹³C-UBT and ¹⁴C-UBT to investigate the prevalence of H. pylori. These two methods do not differ in sensitivity and specificity and have good performance for diagnosis and reflecting the current infection of H. pylori[26]. However, serum H. pylori antibodies may exist for a long period even after eradication therapy. Many older adults may show a negative status on UBT for reduced gastric acid secretion, and others may experience an unintentional eradication from using antibiotics.

This study had some limitations. First, in contrast to the epidemiological sampling survey, this study was based on a data set from hospitals, and individuals included were patients with gastrointestinal complaints. Therefore, the infection rate obtained in this study may have been higher than that obtained in an epidemiological survey. Second, the UBT used in this study may have led to false-negative results in patients with a history of use of antibiotics, proton-pump inhibitors, or bismuth[27]. However, this proportion is extremely low because these hospitals are large tertiary hospitals, and detection was carried out according to standard procedures, including the question of medication history before the test. Third, due to the retrospective design of the study, some information, such as H. pylori infection eradication history and detailed personal information, could not be accurately tracked through electronic medical records, and the risk factors for infection were not considered. Lastly, we could not distinguish between soldiers, officers, and combat and non-combat personnel. Thus, comparison data among rank groups could not be obtained. In the future, we plan to conduct prospective epidemiological surveys among general military personnel to gather more comprehensive data, reduce the bias of hospital-based sampling, and improve analysis of H. pylori infection risk factors. Additionally, the “test-and-treatment” strategy will be applied in military units to assess the health outcomes of infected personnel and evaluate the effectiveness of H. pylori eradication programs within military populations.

CONCLUSION

H. pylori infection has a high prevalence among Chinese military service members, affecting more than one-third of the military personnel. More than 70% of the infected personnel were aged < 40 years. There was a relatively high prevalence rate in northwest and southwest China. Ongoing efforts to control H. pylori infection are crucial in military internal medicine to reduce the incidence of digestive ulcers, dyspepsia, gastric precancerous lesions, and cancer. This study’s findings offer a significant foundation for allocating healthcare resources and developing H. pylori eradication strategies appropriate for military personnel.