Abstract
Objectives: Helicobacter pylori (H. pylori) infection causes a variety of intragastric and extragastric diseases. Despite its decreasing global prevalence, it remains a major public health problem in many developing countries. This study aimed to understand the prevalence of H. pylori infection and its risk factors in five cities of the Ningxia Hui Autonomous Region, an area with high incidence of gastric cancer. Methods: Cross-sectional studies were conducted in Ningxia from 2017 and 2022, to detect the prevalence of H. pylori using the 14C urea breath test. All participants completed a questionnaire that included demographics, personal habits, household economic characteristics, and previous health status. Multiple logistic regression analyses were used to identify independent factors for H. pylori infection. Results: Our findings demonstrated that the prevalence of H. pylori infection in Ningxia decreased significantly from 60.3% in 2017 to 43.6% in 2022, with an increase in public awareness rate from 35.9% in 2017 to 68.5% in 2022. The lowest infection rate was found in Zhongwei and highest in Guyuan. The prevalence of H. pylori infection was higher among Hui ethnicity, farmers, individuals living in rural areas, individuals with lower income, low education, and those who consumed less fruit. Gallbladder, respiratory, cardiovascular and autoimmune diseases were not associated with H. pylori infection. Conclusions: The prevalence of H. pylori in Ningxia decreased in the past five years. Ethnicity, location, occupation, income, education, and consumption of fruits were independent risk factors for H. pylori infection in Ningxia. It was not associated with extra-gastric disease.
Keywords: Helicobacter pylori, prevalence, risk factors, Ningxia
Introduction
Helicobacter pylori (H. pylori) is a gram-negative microaerobic bacillus that is found primarily in the gastrointestinal tract. It is widely recognized as an important causative agent of various gastric diseases [1,2]. H. pylori has been estimated to coexist with humans since 100,000 years ago [3]. A recent meta-analysis showed an estimated overall global H. pylori infection rate of 44.3% and in developing countries, the rate is 50.8% [4]. The prevalence of H. pylori infection in the Chinese population is higher than the rest of the world, with an average of approximately 55-56% [5,6]. Many studies have shown that various factors [7-10], including geographical location, living environment, socioeconomic status, personal habits, and socio-demographic characteristics, may be responsible for the wide variation in H. pylori infection rates among regions. In addition, H. pylori infection is an infectious disease and humans are the main source of H. pylori transmission [11]. It is currently thought to be transmitted mainly through fecal-oral and oral-oral routes, but its exact transmission mechanism remains unclear.
Gastric cancer is the 5th leading cancer in incidence and the 4th in causes of death globally [12]. Chronic H. pylori infection is the most important risk factor for gastric cancer, and it is defined as a group I carcinogen [13]. China is a country with a large incidence of gastric cancer, and nearly half (43.9%) of new gastric cancer cases in the world occur in China [12]. The Ningxia region in northwest China ranks among the top three in the country for the incidence of gastric cancer. In 2017, a tumor survey in Ningxia showed that the incidence and mortality of gastric cancer were as high as 31.57/100,000 and 19.18/100,000, respectively [14], which were 2.8 and 2.5 times the global average, respectively [12]. H. pylori infection is a clear and treatable risk factor for the occurrence and development of gastric diseases including gastric cancer. Therefore, it is of great significance to clarify the current prevalence of H. pylori infection and risk factors in the Ningxia population.
Eradication of H. pylori is one of the most effective ways to prevent gastric cancer, and can significantly reduce the incidence and mortality, especially intestinal type gastric cancer or non-cardiac gastric adenocarcinoma [15,16]. H. pylori eradication also has the potential to block and reverse gastric mucosal intestinal metaplasia, atrophy, and other gastric precancerous lesions [17,18]. In 2017, the Ningxia government proposed the “Healthy Ningxia Action” and organized a region-wide standardized H. pylori eradication treatment program. We conducted a region-wide H. pylori epidemiological survey study twice, in January 2017 before the project started and in January 2022, 5 years after the project was carried out. We investigated the changes in H. Pylori infection rate and its influencing factors as a latest reference for appropriate prevention and treatment in Ningxia region.
H. pylori infection may also be associated with extra-gastric diseases including respiratory, cardiovascular, rheumatic immune, hepatobiliary and metabolic diseases [19]. Therefore, we added extra-gastric diseases to the questionnaire to understand the correlation between H. pylori infection and extra-gastric diseases.
Materials and methods
Study subjects
We conducted two cross-sectional studies in five cities in Ningxia (Yinchuan, Wuzhong, Guyuan, Zhongwei, and Shizuishan) incorporating 21 communities from January-May 2017 and from January-May 2022 (Figure 1). Specific institutions include the following: Yinchuan (Fengdeng Town Community Health Center, Xixia District Hospital 217, Yongning County Hospital, Bishui Blue Community Health Center, Sun Garden Community Health Center); Wuzhong (Wuzhong City People’s Hospital, Yuxi Community Health Center, Jinhuayuan Community Health Center, New Jaguar Community Health Center); Guyuan (Baiyang Town Health Center, Jinyuan County People’s Hospital, Perfume Town Health Center, Guyuan City People’s Hospital, Yuanzhou District People’s Hospital); Zhongwei (Yingshuiqiao Community Health Center, Rouyuan Community Health Center, Zhenluo Community Health Center, Xuanhe Town Community Health Center); and Shizuishan (Shizuishan Second People’s Hospital, Pingluo County Hospital, Huinong Hospital). A random sample of residents who came to the hospital for inspection was surveyed. Inclusion criteria included those who voluntarily underwent the 14C urea breath test (UBT) and awareness of the study. Exclusion criteria were as follows: (1) those who had taken proton pump inhibitors, gastric mucosal protective agents and antibiotics such as amoxicillin, clarithromycin, metronidazole, and sulfonamides within the last 1 month; (2) those who suffered from severe mental illnesses such as anxiety, depression, cognitive dysfunction and other diseases that might affect cooperation with the test; (3) pregnant, lactating and pregnant women; and (4) those aged < 18 years. All enrolled participants answered a structured questionnaire and underwent a 14C-UBT.
Figure 1.
Geographic location of Ningxia and 21 community health care centers that participated in this study (triangle symbols).
The study was approved by the Ethics Committee of People’s Hospital of Ningxia Hui Autonomous Region (approval number: 20170906, 2021-LL-017).
Questionnaire
All participants completed the H. pylori questionnaire (Table S1). It consisted of three main modules: (1) general personal information (sex, age, ethnicity, education, occupation, living area, permanent household size, etc.); (2) personal habits (smoking history, drinking history, usual living habits, dietary habits); and (3) personal health status (presence of digestive symptoms, chronic gastritis, peptic ulcer, cardiovascular disease, respiratory disease, autoimmune disease, etc.). Smoking was defined as smoking more than one cigarette per day, continuously or cumulatively for 6 months. Alcohol consumption was defined as drinking more than 25 g per day for men and 15 g for women in the past year. The frequency of consumption of fruits, vegetables, pickled foods, spicy and stimulating foods, and tea was defined and valued as follows: frequent consumption was defined as participants having eaten food more than three times in 1 week in the past 6 months. Other consumption was considered occasional. All questionnaires were filled in by specialized medical personnel to ensure their reliability, authenticity, and completeness.
Detection of H. pylori infection
H. pylori infection was detected by 14C-UBT, which was administered by trained investigators following the instructions. Briefly, participants took one capsule of urea 14C capsule (Shanghai Xinko Pharmaceutical Co., Ltd., State Drug Administration H20000228) with about 20 ml of drinking water on an empty stomach, sat for 15 min, and then blew into the breath card (Anhui Yanghe Medical Equipment Co., Ltd., Anhui Arm Note 20152400145) and stopped when the indicator in the indicator window of the breath card changed from blue to white. After this, the participant’s name, sex, and test time were filled on the breath card label, which was inserted into the sample inlet of the H. pylori detector (Anhui Yanghe Medical Equipment Co., Ltd., YH04E). This instrument automatically detected and recorded the results obtained about 4 min after the measurement was taken. The sample was considered positive when the value was greater than or equal to 100 DPM/mmol CO2.
Statistical analysis
Epidate (v3.1) was used to create a database from the participants’ date. Statistical analyses were performed using SPSS 25.0, with continuous variables expressed as means, and categorical variables expressed as % and compared using chi-square test. A logistic regression model was used to conduct a multi-factor analysis of the influencing factors. P < 0.05 was considered significant. The figures were presented using the software Origin®2019 (OriginLab Corp., USA, Washington).
Results
Baseline characteristics
In 2017, there were a total of 4780 participatants, including 2178 men (45.6%). The mean age was 50.8 ± 12.2 years, with the highest number aged 44-59 years (45.4%). Participants from the Hui ethnic group accounted for 27.9%. The proportions of urban and rural participants were comparable. Occupation as a farmer or worker accounted for 56.8%. The most common place of residence of participants was from Guyuan. In 2022, a total of 3734 participants participated in the study, including 1340 men (35.9%). The mean age was 55.2 ± 13.4 years. Participants from the Hui ethnic group accounted for 30.2%. Urban and rural participants were equally represented. Occupation as a farmer or worker accounted for 8.9%. Participants from Yinchuan made up the largest proportion. The distribution of sex, age, and place of residence was significantly different in 2022 compared to 2017 participants’ data (P < 0.001) (Table 1).
Table 1.
Baseline characteristics of the participants in 2017 and 2022
| Variable | N (%) [2017] | N (%) [2022] | P |
|---|---|---|---|
| Total | 4780 (100.0) | 3734 (100.0) | |
| Sex, male | 2178 (45.6) | 1340 (35.9) | < 0.001 |
| Age, mean ± SD | 50.8 ± 12.2 | 55.2 ± 13.4 | < 0.001 |
| < 44 | 2008 (42.0) | 1166 (31.3) | |
| 44~59 | 2169 (45.4) | 1577 (42.2) | |
| > 60 | 603 (12.6) | 991 (26.5) | |
| Ethnicity | |||
| Hui | 1334 (27.9) | 1127 (30.2) | |
| Han | 3321 (69.5) | 2510 (67.2) | |
| Others | 125 (2.6) | 97 (2.6) | |
| Living area | |||
| Rural | 2358 (49.3) | 1835 (49.1) | |
| Town | 2422 (50.7) | 1899 (50.9) | |
| Jobs | |||
| Farmer or worker | 2716 (56.8) | 2200 (58.9) | |
| Civil servant or Other | 2064 (43.2) | 1534 (41.1) | |
| Province | < 0.001 | ||
| Yinchuan | 800 (16.7) | 1150 (30.8) | |
| Wuzhong | 841 (17.6) | 426 (11.4) | |
| Shizuishan | 710 (14.9) | 590 (15.8) | |
| Zhongwei | 730 (15.3) | 826 (22.1) | |
| Guyuan | 1699 (35.5) | 742 (19.9) |
Prevalence and awareness of H. pylori infection
We added questions about H. pylori awareness to the questionnaire. The 2022 survey showed that 68.5% of participants were aware of H. pylori, which is significantly higher than that in 2017 (35.9%, P < 0.0001) (Figure 2A). The H. pylori infection rate in 2022 was 43.6% in Ningxia, significantly lower than that in 2017 (60.3%, P < 0.001) (Figure 2B). In addition, we compared the H. pylori infection rate for different age groups and regions. Overall trends for both 2017 and 2022 showed an increasing trend of H. pylori infection with increasing age. However, the results in 2017 showed the highest prevalence of infection at the age of 51-60 years, and in 2022 at age ≥ 71 years. For different age groups and regions, the prevalence of H. pylori infection in 2022 was significantly lower than that in 2017 (P < 0.001) (Figure 2C, 2D). Futhermore, we found that among the five cities in Ningxia, the infection rate in Guyuan was highest in both 2017 and 2022.
Figure 2.
Awareness of Helicobacter pylori (A), and prevalence of Helicobacter pylori stratified by sex, ethnicity (B), age (C), and geographic region (D) in 2017 and 2022. * represent P < 0.001. (A) Awareness rate of Helicobacter pylori in the participating population in 2017 and 2022 by questionnaire. The prevalence of Helicobacter pylori infection in the participating population was detected by 14C urea breath test in 2017 and 2022, respectively. (B) The prevalence of Helicobacter pylori and the comparison of prevalence by gender and ethnicity in 2017 and 2022. (C) Trends in prevalence of Helicobacter pylori by age in 2017 and 2022. (D) Prevalence of Helicobacter pylori in five regions of Ningxia in 2017 and 2022.
Factors associated with H. pylori infection in 2017 and 2022
The factors associated with the H. pylori infection are described in Table 2. The survey data in 2017 showed that the prevalence gradually increased with increasing age, and was significantly higher (P < 0.05) in men than in women, but this result was not reflected in the 2022 data. In addition, both the 2017 and 2022 data showed that the prevalence of H. pylori infection was associated with ethnicity, living area, education level, occupation, and household income (P < 0.05). Specifically, the prevalence of H. pylori infection was higher in Hui ethnicity than in Han ethnicity; higher in those living in rural areas than in urban areas; higher in those with occupations such as farmers or workers than in civil servants and other groups; higher in those with monthly household income < 3,000 CNY and between 3,000-5,000 CNY than in those with income > 5,000 CNY; and lower in those with college or a tertiary education level.
Table 2.
Correlation between the prevalence of Helicobacter pylori infection and demographic-economic, and lifestyle risk factors in 2017 and 2022
| Variable category | 2017 (n=4780) | 2022 (n=3734) | ||||
|---|---|---|---|---|---|---|
|
|
|
|||||
| No. | No. (%) positive | P | No. | No. (%) positive | P | |
| Gender | 0.003 | 0.918 | ||||
| Male | 2178 | 1363 (62.6%) | 1340 | 582 (43.4%) | ||
| Female | 2602 | 1517 (58.3%) | 2394 | 1045 (43.7%) | ||
| Ethnicity | < 0.001 | 0.001 | ||||
| Hui | 1334 | 931 (69.8%) | 1127 | 536 (47.8%) | ||
| Han | 3321 | 1878 (56.5%) | 2510 | 1050 (41.8%) | ||
| Age (years) | < 0.001 | 0.236 | ||||
| < 44 | 2008 | 1070 (53.3%) | 1166 | 491 (42.1%) | ||
| 44~59 | 2169 | 1315 (60.6%) | 1577 | 683 (43.3%) | ||
| > 59 | 603 | 495 (82.1%) | 991 | 453 (45.7%) | ||
| Geographical location | < 0.001 | 0.013 | ||||
| Rural | 2358 | 1587 (67.3%) | 1835 | 762 (41.5%) | ||
| Town | 2422 | 1420 (58.6%) | 1899 | 865 (45.6%) | ||
| Jobs | < 0.001 | 0.019 | ||||
| Farmer or worker | 2716 | 1743 (64.2%) | 2200 | 994 (45.2%) | ||
| Civil servant or other | 2064 | 1137 (55.1%) | 1534 | 633 (41.3%) | ||
| Education level | < 0.001 | < 0.001 | ||||
| Elementary | 2907 | 1978 (68.0%) | 1925 | 911 (47.3%) | ||
| Junior/High School | 992 | 567 (57.2%) | 691 | 276 (39.9%) | ||
| College and above | 881 | 335 (38.0%) | 1118 | 440 (39.4%) | ||
| Household members | 0.445 | 0.012 | ||||
| 1 | 376 | 226 (60.1%) | 125 | 50 (40.0%) | ||
| 2-4 | 3890 | 2331 (59.9%) | 3096 | 1323 (42.7%) | ||
| > 5 | 514 | 323 (62.8%) | 513 | 254 (49.5%) | ||
| Monthly household income | < 0.001 | 0.002 | ||||
| ≤ 3000 | 1124 | 817 (72.9%) | 1388 | 657 (47.3%) | ||
| 3000~5000 | 1942 | 1110 (57.2%) | 1723 | 717 (41.6%) | ||
| ≥ 5000 | 1714 | 935 (54.6%) | 623 | 253 (40.6%) | ||
| Smoking | < 0.001 | 0.958 | ||||
| Yes | 747 | 561 (75.1%) | 413 | 179 (43.3%) | ||
| No | 4033 | 2319 (57.5%) | 3321 | 1448 (43.6%) | ||
| Drinking | < 0.001 | 0.550 | ||||
| Yes | 574 | 406 (70.7%) | 192 | 88 (45.8%) | ||
| No | 4206 | 2474 (58.8%) | 3542 | 1539 (43.5%) | ||
| Eating raw vegetables | 0.090 | 0.460 | ||||
| Yes | 1452 | 849 (58.5%) | 1026 | 437 (42.6%) | ||
| No | 3328 | 2031 (61.0%) | 2708 | 1190 (43.9%) | ||
| Eating fruits | < 0.001 | 0.001 | ||||
| Occasionally | 1314 | 962 (73.2%) | 993 | 479 (48.25) | ||
| Frequently | 3466 | 1918 (55.3%) | 2741 | 1148 (41.9%) | ||
| Eating fried foods | < 0.001 | 0.814 | ||||
| Occasionally | 3471 | 2074 (59.8%) | 2881 | 1252 (43.5%) | ||
| Frequently | 1039 | 806 (77.6%) | 853 | 375 (44.0%) | ||
| Eating spicy foods | 0.180 | 0.647 | ||||
| Occasionally | 2826 | 1725 (61.0%) | 2516 | 1103 (43.8%) | ||
| Frequently | 1954 | 1155 (59.1%) | 1218 | 524 (43.0%) | ||
| Eating pickled foods | 0.029 | < 0.001 | ||||
| Occasionally | 3859 | 2296 (59.5%) | 3208 | 1322 (41.2%) | ||
| Frequently | 921 | 584 (63.4%) | 526 | 305 (58%) | ||
| Drinking tea | 0.021 | 0.146 | ||||
| Occasionally | 3136 | 1852 (59.1%) | 2647 | 1133 (42.8%) | ||
| Frequently | 1644 | 1028 (62.5%) | 1087 | 494 (45.4%) | ||
| Wash hands before eating and after using the toilet | < 0.001 | 0.607 | ||||
| Occasionally | 872 | 603 (69.2%) | 342 | 154 (45.0%) | ||
| Frequently | 3908 | 2277 (58.3%) | 3392 | 1473 (43.4%) | ||
| Families sharing tableware | < 0.001 | 0.974 | ||||
| Yes | 2928 | 2036 (69.5%) | 2043 | 891 (43.6%) | ||
| No | 1852 | 844 (45.6%) | 1691 | 736 (43.5%) | ||
| Indoor pets | < 0.001 | 0.170 | ||||
| Yes | 927 | 660 (71.2%) | 375 | 176 (46.9%) | ||
| No | 3853 | 2220 (57.6%) | 3359 | 1451 (43.2%) | ||
In terms of lifestyle, the survey data in 2017 showed that the prevalence of H. pylori infection was significantly associated with smoking, alcohol consumption, eating fried foods, drinking tea, washing hands before and after meals, sharing utensils at home, and keeping pets indoors (P < 0.05), which was not reflected in the 2022 survey results. However, the results of the 2022 survey showed that the prevalence gradually increased with an increase in household members (P < 0.05). Moreover, both the 2017 and 2022 data showed that the prevalence of H. pylori infection was significantly associated with the consumption of fruits and pickled foods (P < 0.05). Specifically, the prevalence of H. pylori infection was lower in participants who ate fruit regularly than in those who ate fruit occasionally. In addition, participants who ate pickled foods frequently had higher prevalence rates than those who ate these food occasionally.
Logistic regression model analysis
The odds ratio (OR) for the the indicators with significant differences (P < 0.05) after screening were included in the logistic regression model (Table 3). The results showed that independent risk factors affecting H. pylori infection were Hui ethnicity (OR=1.919, 95% CI: 1.253~2.954), living in a rural area (OR=1.557, 95% CI: 1.029~2.321), occupation as farmer or worker (OR=2.329, 95% CI: 1.144~4.742), lower education level (OR=1.920, 95% CI: 1.209~3.049), lower income (OR=1.617, 95% CI: 1.191~2.196), and infrequent fruit consumption (OR=1.474, 95% CI: 1.077~2.018).
Table 3.
Multifactorial logistic regression analysis for Helicobacter pylori infection
| Variable category | β | SE | Wald χ2 | P | OR | 95% CI |
|---|---|---|---|---|---|---|
| Ethnicity | 0.644 | 0.220 | 9.012 | 0.003 | 1.919 | 1.253~2.954 |
| Geographic Location | 0.429 | 0.211 | 4.429 | 0.038 | 1.557 | 1.029~2.321 |
| Job | 0.844 | 0.362 | 5.429 | 0.020 | 2.329 | 1.144~4.742 |
| Education Level | 0.652 | 0.236 | 7.630 | 0.006 | 1.920 | 1.209~3.049 |
| Income | 0.481 | 0.156 | 9.480 | 0.002 | 1.617 | 1.191~2.196 |
| Eating fruits | 0.388 | 0.160 | 5.867 | 0.015 | 1.474 | 1.077~2.018 |
Relationship between H. pylori infection and personal health status
The questionnaire for this study also included questions related to the personal health status of the participants, and its relationship with H. pylori infection (Table 4). The results of both 2017 and 2022 surveys showed a higher prevalence of H. pylori infection in participants with chronic gastritis and peptic ulcer (P < 0.05); whereas the presence of gallbladder, respiratory, cardiovascular, or autoimmune diseases did not correlat with the infection (P > 0.05).
Table 4.
Correlation between the prevalence of Helicobacter pylori infection and medical history in 2017 and 2022
| Variable category | 2017 (n=4780) | 2022 (n=3734) | ||||
|---|---|---|---|---|---|---|
|
|
|
|||||
| No. | No. (%) positive | P | No. | No. (%) positive | P | |
| Chronic gastritis | 0.006 | 0.001 | ||||
| Yes | 1465 | 922 (62.9%) | 1269 | 504 (39.7%) | ||
| No | 3315 | 1958 (59.1%) | 2465 | 1123 (45.6%) | ||
| Peptic ulcer | < 0.001 | 0.009 | ||||
| Yes | 1213 | 795 (65.5%) | 555 | 270 (48.6%) | ||
| No | 3567 | 2085 (58.5%) | 3179 | 1357 (42.7%) | ||
| Spouse’s gastric disease | 0.015 | 0.490 | ||||
| Yes | 1279 | 807 (63.1%) | 663 | 297 (44.8%) | ||
| No | 3501 | 2073 (59.2%) | 3071 | 1330 (43.3%) | ||
| Gallbladder disease | 0.751 | 0.382 | ||||
| Yes | 1058 | 633 (59.8%) | 567 | 257 (45.3%) | ||
| No | 3722 | 2247 (60.4%) | 3167 | 1370 (43.3%) | ||
| Respiratory disease | 0.559 | 0.770 | ||||
| Yes | 436 | 257 (58.9%) | 109 | 49 (45.0%) | ||
| No | 4344 | 2623 (60.4%) | 3625 | 1578 (43.5%) | ||
| Cardiovascular disease | 0.255 | 0.612 | ||||
| Yes | 484 | 280 (57.9%) | 271 | 114 (42.1%) | ||
| No | 4296 | 2600 (60.5%) | 3463 | 1513 (43.7%) | ||
| Autoimmune disease | 0.47 | 0.677 | ||||
| Yes | 543 | 335 (61.7%) | 224 | 101 (45.1%) | ||
| No | 4237 | 2545 (60.1%) | 3510 | 1526 (43.5%) | ||
Discussion
H. pylori infection is still an issue of public concern worldwide. The current infection status in Ningxia, a region with a high incidence of gastric cancer, remains unclear. Using 14C-UBT to determine H. pylori infection, we found that the prevalence in Ningxia was as high as 60.3% in 2017, but had decreased to 43.6% by 2022. The observed decline over time was consistent with a recent report on the decline in the seropositivity of H. pylori infection in Korea [20]. The prevalence of H. pylori infection has been reported to have been declining in highly industrialized countries in the western world, while in developing and newly industrialized countries, has remained high at the turn of the 21st century [5]. Furthermore, this decline may be associated with higher socioeconomic status, better sanitation, and greater changes in nuclear family distribution [21,22]. However, in the current study, the decline in H. pylori infection may be associated with the implementation of a region-wide standardized H. pylori diagnosis and treatment initiative, i.e., spontaneous H. pylori eradication, during this period. Moreover, the survey results showed a significant increase in the participants’ knowledge of H. pylori, which, in addition to the increasing standard of living and greater concern for their health, could not be separated from the efforts made by the government during these 5 years.
Consistent with previous studies, both findings in the present study showed a gradual increase in H. pylori infection with age [20,23,24]. However, the decrease in infection rate observed in participants over 70 years of age may be due to the lower H. pylori load after the development of atrophic gastritis, which limits UBT detection; and secondly to the somewhat higher odds of oral antibiotics in the elderly, which suppresses H. pylori after coincidental treatment with antibiotics [25,26]. In terms of the geographical area, an overall declining trend in infection rate was observed in all areas. However, we found that H. pylori infection rates were consistently lowest in Zhongwei and highest in Guyuan. This is closely related to the fact that Ningxia is an ethnic minority (Hui) concentrated area. Coincidentally, multivariate analysis found that Hui ethnicity was an independent risk factor for H. pylori infection. The proportion of individuals of Hui ethnicity in Zhongwei (35.31%) was significantly lower than that in Guyuan (47.5%). Guyuan has the highest proportion of Hui ethnicity in Ningxia, so its highest infection rate may be related to ethnicity. The difference in H. pylori infection rate between Hui ethnicity and Han ethnicity may be due to their different dietary structure; while the Hui population prefers beef and mutton. Some literature reported that H. pylori was detected in both beef and mutton by bacterial culture and PCR analysis [27-29].
In addition, we analyzed the participants’ general personal information and lifestyle habits, and found both different and consistent factors. Data from 2017 alone using univariate analysis showed a higher prevalence of H. pylori infection in men, but after adjusting for OR, multifactorial results showed no correlation between sex and infection, which was consistent with the findings of Wang et al. [30] and Van et al. [31]. However, a meta-analysis pooling 244 studies showed that H. pylori infection was predominant in men [32]. Multifactorial logistic analysis showed that residence area, occupation, educational level, and monthly income were correlated with H. pylori infection, which was consistent with the findings of other studies [26,33]. The risk of H. pylori infection was higher in participants living in rural areas, working in agriculture, with less education, and lower household income than in those living in towns, working in non-agricultural occupations, with higher education, and higher household income. This may be attributed to poor health habits, lifestyles, relative lack of medical facilities, family size clustering among farmers, less education in people, and low-income families [34].
H. pylori is usually transmitted by both direct and indirect means. Direct transmission usually refers to intimate interactions between people, while indirect transmission requires a medium such as water, food or other animals [35,36]. The present study showed a higher prevalence of infection in participants with a larger household size and shared utensils, which is also consistent with the oral-oral transmission route of H. pylori. In addition, the prevalence was higher in households with pets than in households without pets. Many studies have found a high prevalence of H. pylori infection in butchers and meat processors, and H. pylori has been isolated from animals such as cattle, sheep, camels, and dogs [28,29]. These animals may be reservoirs of H. pylori, but whether H. pylori infection is zoonotic has not yet been confirmed, and it has only been speculated that H. pylori may be transmitted from animals to humans. Hence, more studies are required to determine whether pet ownership leads to increased H. pylori infection in humans.
The relationship between smoking, drinking, and H. pylori infection is highly controversial. A study from asymptomatic individuals showed that smoking and drinking were risk factors for males but protective factors for women after adjusting for age [37]. However, there are also studies showing that smoking was inversely associated with H. pylori infection [38]. Our fingdings showed no significant correlation between smoking and H. pylori infection, which is consistent with the results of two studies from China [30,39]. This result may be related to detailed data on the frequency and amount of drinking and smoking. Adjusting for relevant factors together may lead to consistent conclusions.
H. pylori infection was also associated with eating habits. Through analyzing dietary habits, we found that eating fruits may be a protective factor, and that regular consumption of fruits is associated with a lower risk of H. pylori infection, as supported by other studies [26,30]. It has been reported that H. pylori infection is related to lipid metabolism [40,41], and that good dietary habits can help prevent H. pylori infection. Individuals who consume fruits and vegetables regularly are better able to eliminate excess accumulated cholesterol in their bodies, which has the effect of lowering blood pressure and blood lipids. In addition, the high content of vitamin C in fresh vegetables and fruits can protect the gastric mucosa from H. pylori infection [42], but the specific mechanism at work needs further investigation. Some studies have shown a positive association between the consumption of pickled and fried foods and H. pylori infection [39]. However, the results of this study do not support this conclusion. Moreover, previous studies have reported that drinking tea is a protective factor against H. pylori infection, and it is believed that tea polyphenols have bactericidal effects reducing infection rate, but this study does not support these results [43]. The differences in these findings may be related to varying data such as the type and amount of tea consumed. Therefore, the correlation between tea drinking and H. pylori infection still needs to be confirmed by further studies.
Participants with a history of peptic ulcer and chronic gastritis had a higher rate of H. pylori infection (P < 0.05). This is consistent with the fact that H. pylori is the causative agent of various chronic gastric diseases; hence it is important to actively eradicate H. pylori to prevent peptic ulcer and gastric cancer. In addition, it has been reported that H. pylori is also the cause of some extra-gastric diseases including blood, cardiovascular, metabolic, immune and other diseases [19]. However, by analyzing the contents of the questionnaire, this study did not find H. pylori to be associated with extragastric disease.
Our research has the following advantages. First of all, we explored various regions of Ningxia and completed a population-based sampling design covering all areas of the population. Almost all participants provided complete data based on the questionnaires. Secondly, the centralized 14C-UBT and strict exclusion criteria ensured the reliability of the test results. Third, Ningxia is an area inhabited by ethnic minorities, and there were few studies on H. pylori infection based on Hui and Han populations. This study makes a significant contribution to the literature as the findings provide new insights into the relationship between H. pylori infection and high prevalence of gastric cancer in thses populations. In terms of limitations, this study did not involve all age groups, that is, people under the age of 18 years were not included in the study, which may lead to an overestimation of the infection rate in this region. Second, although we informed all participants of their H. pylori infection status, there was no follow-up or treatment, and future studies may require us to assist them for monitoring throughout their treatment.
In summary, this is the first study to investigate the prevalence of H. pylori infection and its associated risk factors on a large scale in the general population of Ningxia Hui Autonomous Region, a region with a high prevalence of gastric cancer. In 2017, the infection rate of H. pylori in Ningxia was 60.3%, which exceeded the national average. After 5 years of standardized diagnosis, treatment, and education, the prevalence of H. pylori infection decreased to 43.6% in 2022, and the public had a broader awareness of H. pylori. This showed that the “Healthy Ningxia Action” advocated by the Ningxia Hui Autonomous Region government had played a criticalrole. Moreover, binary multifactorial logistic regression analysis found that ethnicity, living area, occupation, income, level of education, and consumption of fruits were independent risk factors for H. pylori infection. The results of this study provide a new perspective on the reasons for the high incidence of gastric cancer in Ningxia, and could help reduce and control the incidence of gastric cancer in this region. In the future, we should follow up with established cohorts to study the changes in H. pylori infection and disease spectrum in the local population.
Acknowledgements
We thank the government departments county hospitals and community health centers of Ningxia Hui Autonomous Region for facilitating the study for the people of Ningxia region. This study is supported by the Central Guide Local Science and Technology Development Special Project fund (No. YDZX20176400004650), Ningxia Hui Autonomous Region Key Research and Development Program (No. 2019BFG02003), Ningxia Hui Autonomous Region Key Research and Development Program (No. 2021BEG02025), Ningxia Hui Autonomous Region Science and Technology Special Project to Benefit the People (No. 2022CMG03039), and Hainan Province Clinical Medical Center (No. 2021818).
Disclosure of conflict of interest
None.
Supporting Information
References
- 1.Tshibangu-Kabamba E, Yamaoka Y. Helicobacter pylori infection and antibiotic resistance - from biology to clinical implications. Nat Rev Gastroenterol Hepatol. 2021;18:613–629. doi: 10.1038/s41575-021-00449-x. [DOI] [PubMed] [Google Scholar]
- 2.Yamaoka Y. How to eliminate gastric cancer-related death worldwide? Nat Rev Clin Oncol. 2018;15:407–408. doi: 10.1038/s41571-018-0029-8. [DOI] [PubMed] [Google Scholar]
- 3.Maixner F, Krause-Kyora B, Turaev D, Herbig A, Hoopmann MR, Hallows JL, Kusebauch U, Vigl EE, Malfertheiner P, Megraud F, O’Sullivan N, Cipollini G, Coia V, Samadelli M, Engstrand L, Linz B, Moritz RL, Grimm R, Krause J, Nebel A, Moodley Y, Rattei T, Zink A. The 5300-year-old Helicobacter pylori genome of the Iceman. Science. 2016;351:162–165. doi: 10.1126/science.aad2545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Zamani M, Ebrahimtabar F, Zamani V, Miller WH, Alizadeh-Navaei R, Shokri-Shirvani J, Derakhshan MH. Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther. 2018;47:868–876. doi: 10.1111/apt.14561. [DOI] [PubMed] [Google Scholar]
- 5.Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, Malfertheiner P, Graham DY, Wong VWS, Wu JCY, Chan FKL, Sung JJY, Kaplan GG, Ng SC. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology. 2017;153:420–429. doi: 10.1053/j.gastro.2017.04.022. [DOI] [PubMed] [Google Scholar]
- 6.Wandai Z, Fulian H, Shudong X, Zhimin X. Epidemiological survey of Helicobacter pylori infection in anatural population in China. Modern Gastroenterol Intervent Med. 2010;15:265–270. [Google Scholar]
- 7.Olokoba AB, Gashau W, Bwala S, Adamu A, Salawu FK. Helicobacter pylori infection in Nigerians with dyspepsia. Ghana Med J. 2013;47:79–81. [PMC free article] [PubMed] [Google Scholar]
- 8.Amaral O, Fernandes I, Veiga N, Pereira C, Chaves C, Nelas P, Silva D. Living conditions and Helicobacter pylori in adults. Biomed Res Int. 2017;2017:9082716. doi: 10.1155/2017/9082716. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Mapel D, Roberts M, Overhiser A, Mason A. The epidemiology, diagnosis, and cost of dyspepsia and Helicobacter pylori gastritis: a case-control analysis in the Southwestern United States. Helicobacter. 2013;18:54–65. doi: 10.1111/j.1523-5378.2012.00988.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, Forman D, Plummer M. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol. 2012;13:607–615. doi: 10.1016/S1470-2045(12)70137-7. [DOI] [PubMed] [Google Scholar]
- 11.Sugano K, Tack J, Kuipers EJ, Graham DY, El-Omar EM, Miura S, Haruma K, Asaka M, Uemura N, Malfertheiner P. Kyoto global consensus report on Helicobacter pylori gastritis. Gut. 2015;64:1353–1367. doi: 10.1136/gutjnl-2015-309252. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209–249. doi: 10.3322/caac.21660. [DOI] [PubMed] [Google Scholar]
- 13.Mégraud F, Bessède E, Varon C. Helicobacter pylori infection and gastric carcinoma. Clin Microbiol Infect. 2015;21:984–990. doi: 10.1016/j.cmi.2015.06.004. [DOI] [PubMed] [Google Scholar]
- 14.Fang M, Chenzhe D, Rong W, Yine Z, Jianhua Z, Jinxing C. Analysis of malignant tumor incidence and death in Ningxia tumor registration area in 2016. J Pract Oncol. 2020;34:298–303. [Google Scholar]
- 15.Ma JL, Zhang L, Brown LM, Li JY, Shen L, Pan KF, Liu WD, Hu Y, Han ZX, Crystal-Mansour S, Pee D, Blot WJ, Fraumeni JF, You WC, Gail MH. Fifteen-year effects of Helicobacter pylori, garlic, and vitamin treatments on gastric cancer incidence and mortality. J Natl Cancer Inst. 2012;104:488–492. doi: 10.1093/jnci/djs003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Doorakkers E, Lagergren J, Engstrand L, Brusselaers N. Helicobacter pylori eradication treatment and the risk of gastric adenocarcinoma in a Western population. Gut. 2018;67:2092–2096. doi: 10.1136/gutjnl-2017-315363. [DOI] [PubMed] [Google Scholar]
- 17.Kodama M, Murakami K, Okimoto T, Sato R, Uchida M, Abe T, Shiota S, Nakagawa Y, Mizukami K, Fujioka T. Ten-year prospective follow-up of histological changes at five points on the gastric mucosa as recommended by the updated Sydney system after Helicobacter pylori eradication. J Gastroenterol. 2012;47:394–403. doi: 10.1007/s00535-011-0504-9. [DOI] [PubMed] [Google Scholar]
- 18.Hwang YJ, Kim N, Lee HS, Lee JB, Choi YJ, Yoon H, Shin CM, Park YS, Lee DH. Reversibility of atrophic gastritis and intestinal metaplasia after Helicobacter pylori eradication - a prospective study for up to 10 years. Aliment Pharmacol Ther. 2018;47:380–390. doi: 10.1111/apt.14424. [DOI] [PubMed] [Google Scholar]
- 19.Pellicano R, Ianiro G, Fagoonee S, Settanni CR, Gasbarrini A. Review: extragastric diseases and Helicobacter pylori . Helicobacter. 2020;25(Suppl 1):e12741. doi: 10.1111/hel.12741. [DOI] [PubMed] [Google Scholar]
- 20.Lim SH, Kim N, Kwon JW, Kim SE, Baik GH, Lee JY, Park KS, Shin JE, Song HJ, Myung DS, Choi SC, Kim HJ, Yim JY, Kim JS. Trends in the seroprevalence of Helicobacter pylori infection and its putative eradication rate over 18 years in Korea: a cross-sectional nationwide multicenter study. PLoS One. 2018;13:e0204762. doi: 10.1371/journal.pone.0204762. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Peleteiro B, Bastos A, Ferro A, Lunet N. Prevalence of Helicobacter pylori infection worldwide: a systematic review of studies with national coverage. Dig Dis Sci. 2014;59:1698–1709. doi: 10.1007/s10620-014-3063-0. [DOI] [PubMed] [Google Scholar]
- 22.Hoed CM, Vila AJ, Holster IL, Perez-Perez GI, Blaser MJ, Jongste JC, Kuipers EJ. Helicobacter pylori and the birth cohort effect: evidence for stabilized colonization rates in childhood. Helicobacter. 2011;16:405–409. doi: 10.1111/j.1523-5378.2011.00854.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Tarkhashvili N, Chakvetadze N, Mebonia N, Chubinidze M, Bakanidze L, Shengelidze V, Mirtskhulava M, Chachava T, Katsitadze G, Gabunia U, Kordzaia D, Imnadze P, Guarner J, Sobel J. Traditional risk factors for Helicobacter pylori infection not found among patients undergoing diagnostic upper endoscopy-Republic of Georgia, 2007-2008. Int J Infect Dis. 2012;16:e697–702. doi: 10.1016/j.ijid.2012.05.1031. [DOI] [PubMed] [Google Scholar]
- 24.Yim JY, Kim N, Choi SH, Kim YS, Cho KR, Kim SS, Seo GS, Kim HU, Baik GH, Sin CS, Cho SH, Oh BH. Seroprevalence of Helicobacter pylori in South Korea. Helicobacter. 2007;12:333–340. doi: 10.1111/j.1523-5378.2007.00504.x. [DOI] [PubMed] [Google Scholar]
- 25.Pounder RE, Ng D. The prevalence of Helicobacter pylori infection in different countries. Aliment Pharmacol Ther. 1995;9(Suppl 2):33–39. [PubMed] [Google Scholar]
- 26.Zhang F, Pu K, Wu Z, Zhang Z, Liu X, Chen Z, Ye Y, Wang Y, Zheng Y, Zhang J, An F, Zhao S, Hu X, Li Y, Li Q, Liu M, Lu H, Zhang H, Zhao Y, Yuan H, Ding X, Shu X, Ren Q, Gou X, Hu Z, Wang J, Wang Y, Guan Q, Guo Q, Ji R, Zhou Y. Prevalence and associated risk factors of Helicobacter pylori infection in the Wuwei cohort of north-western China. Trop Med Int Health. 2021;26:290–300. doi: 10.1111/tmi.13517. [DOI] [PubMed] [Google Scholar]
- 27.Stevenson TH, Bauer N, Lucia LM, Acuff GR. Attempts to isolate Helicobacter from cattle and survival of Helicobacter pylori in beef products. J Food Prot. 2000;63:174–178. doi: 10.4315/0362-028x-63.2.174. [DOI] [PubMed] [Google Scholar]
- 28.Saeidi E, Sheikhshahrokh A. vacA genotype status of Helicobacter pylori isolated from foods with animal origin. Biomed Res Int. 2016;2016:8701067. doi: 10.1155/2016/8701067. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Gilani A, Razavilar V, Rokni N, Rahimi E. VacA and cagA genotypes status and antimicrobial resistance properties of Helicobacter pylori strains isolated from meat products in Isfahan province, Iran. Iran J Vet Res. 2017;18:97–102. [PMC free article] [PubMed] [Google Scholar]
- 30.Wang W, Jiang W, Zhu S, Sun X, Li P, Liu K, Liu H, Gu J, Zhang S. Assessment of prevalence and risk factors of Helicobacter pylori infection in an oilfield Community in Hebei, China. BMC Gastroenterol. 2019;19:186. doi: 10.1186/s12876-019-1108-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.van Blankenstein M, van Vuuren AJ, Looman CW, Ouwendijk M, Kuipers EJ. The prevalence of Helicobacter pylori infection in the Netherlands. Scand J Gastroenterol. 2013;48:794–800. doi: 10.3109/00365521.2013.799221. [DOI] [PubMed] [Google Scholar]
- 32.Ibrahim A, Morais S, Ferro A, Lunet N, Peleteiro B. Sex-differences in the prevalence of Helicobacter pylori infection in pediatric and adult populations: systematic review and meta-analysis of 244 studies. Dig Liver Dis. 2017;49:742–749. doi: 10.1016/j.dld.2017.03.019. [DOI] [PubMed] [Google Scholar]
- 33.Hollander WJ, Holster IL, Hoed CM, Deurzen F, Vuuren AJ, Jaddoe VW, Hofman A, Perez Perez GI, Blaser MJ, Moll HA, Kuipers EJ. Ethnicity is a strong predictor for Helicobacter pylori infection in young women in a multi-ethnic European city. J Gastroenterol Hepatol. 2013;28:1705–1711. doi: 10.1111/jgh.12315. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Wang B, Lv ZF, Wang YH, Wang H, Liu XQ, Xie Y, Zhou XJ. Standard triple therapy for Helicobacter pylori infection in China: a meta-analysis. World J Gastroenterol. 2014;20:14973–14985. doi: 10.3748/wjg.v20.i40.14973. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Burucoa C, Axon A. Epidemiology of Helicobacter pylori infection. Helicobacter. 2017;22(Suppl 1) doi: 10.1111/hel.12403. [DOI] [PubMed] [Google Scholar]
- 36.Allaker RP, Young KA, Hardie JM, Domizio P, Meadows NJ. Prevalence of Helicobacter pylori at oral and gastrointestinal sites in children: evidence for possible oral-to-oral transmission. J Med Microbiol. 2002;51:312–317. doi: 10.1099/0022-1317-51-4-312. [DOI] [PubMed] [Google Scholar]
- 37.Wu W, Leja M, Tsukanov V, Basharat Z, Hua D, Hong W. Sex differences in the relationship among alcohol, smoking, and Helicobacter pylori infection in asymptomatic individuals. J Int Med Res. 2020;48:300060520926036. doi: 10.1177/0300060520926036. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Ogihara A, Kikuchi S, Hasegawa A, Kurosawa M, Miki K, Kaneko E, Mizukoshi H. Relationship between Helicobacter pylori infection and smoking and drinking habits. J Gastroenterol Hepatol. 2000;15:271–276. doi: 10.1046/j.1440-1746.2000.02077.x. [DOI] [PubMed] [Google Scholar]
- 39.Zhu Y, Zhou X, Wu J, Su J, Zhang G. Risk factors and prevalence of Helicobacter pylori infection in persistent high incidence area of gastric carcinoma in Yangzhong city. Gastroenterol Res Pract. 2014;2014:481365. doi: 10.1155/2014/481365. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Elizalde JI, Piqué JM, Moreno V, Morillas JD, Elizalde I, Bujanda L, De Argila CM, Cosme A, Castiella A, Ros E. Influence of Helicobacter pylori infection and eradication on blood lipids and fibrinogen. Aliment Pharmacol Ther. 2002;16:577–586. doi: 10.1046/j.1365-2036.2002.01202.x. [DOI] [PubMed] [Google Scholar]
- 41.Abdel-Razik A, Mousa N, Shabana W, Refaey M, Elhelaly R, Elzehery R, Abdelsalam M, Elgamal A, Nassar MR, Abu El-Soud A, Seif AS, Tawfik AM, El-Wakeel N, Eldars W. Helicobacter pylori and non-alcoholic fatty liver disease: a new enigma? Helicobacter. 2018;23:e12537. doi: 10.1111/hel.12537. [DOI] [PubMed] [Google Scholar]
- 42.Shi LQ, Zheng RL. DNA damage and oxidative stress induced by Helicobacter pylori in gastric epithelial cells: protection by vitamin C and sodium selenite. Pharmazie. 2006;61:631–637. [PubMed] [Google Scholar]
- 43.Akai Y, Nakajima N, Ito Y, Matsui T, Iwasaki A, Arakawa Y. Green tea polyphenols reduce gastric epithelial cell proliferation and apoptosis stimulated by Helicobacter pylori infection. J Clin Biochem Nutr. 2007;40:108–115. doi: 10.3164/jcbn.40.108. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.