Skip to main content

Association between renal function and co-infection with Clonorchis sinensis and Helicobacter pylori: a cross-sectional study

Abstract

Background

Studies have shown that liver fluke infections may be associated with kidney injury and that Helicobacter pylori (Hp) may be involved in the pathogenesis of kidney diseases. However, no studies have reported the relationship between co-infection with Clonorchis sinensis (Cs) and Hp and renal function. The aim of this study was to examine the relationship between co-infection with Cs and Hp and estimated glomerular filtration rate (eGFR) in a general population, and gender-related differences were also investigated.

Methods

In the cross-sectional study, 4122 subjects from the Health Examination Center of Guangdong Provincial Hospital of Integrated Traditional Chinese and Western Medicine from January 2017 to December 2018 were enrolled. All participants underwent stool examination for the diagnosis of Cs infection and 13C-urea breath test (UBT) for the diagnosis of Hp infection. Participants were categorized into four groups: (1) co-infection with Cs and Hp group comprising 207 cases (Hp(+) + Cs(+) group), (2) Cs infection group comprising 1392 cases (Hp(−) + Cs(+)group), (3) Hp infection group comprising 275 cases (Hp(+) + Cs(−) group), and (4) non-infection group comprising 2248 cases (Hp(−) + Cs(−) group). Multiple linear regression analysis was performed to evaluate the relationship between co-infection with Cs and Hp and eGFR.

Results

Hp infection without Cs infection was present in 6.67% (275/4122) of subjects, while Cs infection without Hp infection was present in 33.77% (1392/4122) of subjects. Co-infection with Hp and Cs were present in 5.02% (207/4122) of subjects. Median age of the participants was 43 years (IQR 35–51). Most of the participants were male (2955/4122, 71.69%). Median eGFR was 96.61 ml/min/1.73 m2 (IQR 85.05–106.24). Co-infection with Cs and Hp was negatively associated with eGFR after full adjusting (β = − 1.89, 95% CI: − 3.33 to − 0.45, p = 0.01). The relationship remained significant in females (β = − 9.37, 95% CI: − 11.60 to − 7.1, p < 0.001), but not in males.

Conclusion

Our findings suggest that co-infection with Cs and Hp may be associated with reduced renal function in females, but not in males.

Peer Review reports

Background

Infection of Clonorchis sinensis (Cs) is mainly prevalent in Asian countries and regions, including South Korea, China, Northern Vietnam, and Russian Far East [1,2,3]. China has the largest population with Cs infection, which is estimated at 13 million [3,4,5]. Helicobacter pylori (Hp) is the most common chronic bacterial infection in humans and is related to various gastrointestinal diseases, such as gastritis, peptic ulcer, gastric cancer, and extranodal marginal zone lymphoma of mucosa-associated lymphoid tissue [6, 7]. The prevalence of Hp infection is approximately 30% in developed countries and up to 80% in developing countries [8, 9].

It has been found that the prevalence of Hp infection was relatively high in Cs endemic areas [10]. In vivo experiment domonstrated that the liver fluke infected hamsters had significantly higher Hp infection rate than non-liver fluke infected hamsters, and co-infection with Cs and Hp can aggravate hepatobiliary abnormality and accelerate the fibrogenesis [11]. There is evidence that Hp can be detected in the gut epithelium of O viverrini (a species of the liver flukes), indicating that the liver fluke represents a reservoir of Hp in the biliary system [12]. In addition, it has been reported that liver fluke infections can lead to glomerulopathy in laboratory animal models [13, 14].

Studies on Hp infection and kidney injury revealed that long-term Hp infection increased the antibodies against Hp, promoted the production of IgA1 and its underglycosylation, aggravated renal function and caused more severe antigen deposition in IgA [15, 16]. These findings suggest that Hp might be involved in the pathogenesis of IgA nephropathy through inducing strong mucosal immune response. However, to our knowledge, there is no literature on the association between co-infection with Cs and Hp and renal function. Therefore, we conducted a cross-sectional study to examine the association between co-infection with Cs and Hp infection and estimated glomerular filtration rate (eGFR), and gender-related differences were also investigated.

Methods

Study area

The study was conducted at the city of Foshan, which is one of the largest cities in Guangdong Province, China, with a population of nearly 8 million. Clonorchiasis is mainly prevalent in China, and the infection rate in Guangdong province is the highest area of China [5, 17]. However, although the people in Foshan city have a traditional habit of eating raw or undercooked freshwater fish, the detection rate of Cs in this area is relatively low. Guangdong Provincial Hospital of Integrated Traditional Chinese and Western Medicine is the major public hospital responsible for the epidemiological investigation, diagnosis and treatment of infectious diseases in this area. In order to improve the detection rate of Cs, since 2018, the Kato-Katz (KK) method has been widely adopted in general health examinations to provide Clonorchiasis surveillance in this area.

Study population

We screened the subjects aged 18–65 years who were receiving annual health examinations including Kato-Katz (KK) method for Cs infection and 13C-urea breath test (UBT) for Hp infection from the Health Examination Center of Guangdong Integrated Hospital of Traditional Chinese and Western Medicine from January 2017 to December 2018. All subjects were categorized into four groups: (1) co-infection with Cs and Hp group (Hp(+) + Cs(+) group), (2) Cs infection group (Hp(−) + Cs(+)group), (3) Hp infection group (Hp(+) + Cs(−)group), (4) no-infection of Cs and Hp group (Hp(−) + Cs(−) group). All of the participants with Cs and (or) Hp infection were first diagnosed; No participants enrolled in the study received previous treatments for Hp and Cs infection. Participants with any of the following characteristics were excluded from the study: a) history of kidney disease (or GFR < 60 mL/min/1.73 m2); b) alcohol consumption of 2 or more drink units per week; c) history of cancer diseases; d) history of viral hepatitis; e) urinary tract infection; f) autoimmune diseases. This study conformed to the Declaration of Helsinki and was approved by the Ethical Committee of Guangdong Provincial Hospital of Integrated Traditional Chinese and Western Medicine. Written informed consent was acquired from all participants.

Data collection

Trained medical staff used a questionnaire to collect data on age, sex, alcohol intake and histories of hypertension, diabetes, kidney diseases, autoimmune diseases, cancer diseases and viral hepatitis (Additional file 1). The body mass index (BMI) was calculated as weight in kilograms divided by height in squared meters (kg/m2). Venous blood samples were collected after an overnight fast of 8–12 h. All blood samples were tested at the laboratory of Guangdong Provincial Hospital of Integrated Traditional Chinese and Western Medicine. Alanine aminotransferase (ALT), aspartate aminotransferase (AST), alkaline phosphatase (ALP), γ-glutamyltranspeptidase (γ-GT), triglyceride (TG), total cholesterol (TC), fasting plasma glucose (FPG), high-density lipoprotein (HDL), low-density lipoprotein (LDL), creatinine (CRE), blood urea nitrogen (BUN), β2-microglobulin (β2-MB) and uric acid (UA) levels were measured using an Olympus AU-640 autoanalyzer (Olympus, Japan), and routine blood test were measured using Sysmex 2100 whole blood cell analyzer (Sysmex, Japan).

Stool examination by the Kato-Katz (KK) method was used for the diagnosis of Cs infection, which was performed following the WHO protocol [18]. Briefly, the Kato-Katz thick smears were examined under a microscope by experienced technicians. The number of eggs was counted and recorded. The intensity of Cs infection was expressed by eggs per gram of feces (EPG) and classified into three categories according to WHO [19]: light (1–1999 EPG), moderate (2000–3999 EPG), and heavy (≥4000 EPG). 13C-urea breath test (13C-UBT) method can be diagnosed as Hp infection when δ13CO2 > 5‰ [20]. Estimated glomerular filtration rate (eGFR) was calculated using the Chronic Kidney Disease Epidemiology Collaboration (CKD-EPI) equation [21].

eGFR = 141 × min (SCr/κ, 1)α × max(SCr/κ, 1)-1.209 × 0.993Age × 1.018(if female), where SCr is serum creatinine (mg/dL), κ is 0.7 for females and 0.9 for males, α is − 0.329 for females and − 0.411 for males, age is in years, min indicates the minimum of SCr/κ or 1, and max is the maximum of SCr/κ or 1.

Statistical analysis

Normal distribution data were expressed as mean ± standard deviation, and ANOVA was used to compare the groups. Median (interquartile range) was used to describe the data with skewed distribution, and Kruskal-Wallis H test was used to compare the groups. Qualitative data are expressed in frequency (percentage) and compared with chi-square test. Ranked data of the groups were compared using Wilcoxon rank sum test or Kruskal-Wallis H test, as appropriate. In addition, multiple linear regression models were performed to estimate the associations between co-infection with Cs and Hp with eGFR (by the forced entry method). Multiple regression models were adjusted as follows: Model 1 was adjusted for age, gender, history of hypertension and history of diabetes; Model 2 was adjusted for Model 1 + BMI, SBP and DBP; Model 3 was adjusted for Model 2 + ALT, AST, ALP, γ-GT, TC, TG, HDL, LDL, BUN, β2-MB and UA. All data analyses were conducted using IBM SPSS (version 22.0). A two-tailed t test was employed, using a significant level of 0.05.

Results

Clinical and demographic characteristics

Overall, 4122 Chinese participants were enrolled in the study (Fig. 1). The baseline clinical characteristics of the participants were listed in Table 1. Hp infection without Cs infection was present in 6.67% (275/4122) of subjects, while Cs infection without Hp infection was present in 33.77% (1392/4122) of subjects. Co-infection with Hp and Cs were present in 5.02% (207/4122) of subjects. Median age of the participants was 43 years (IQR 35–51). Most of the participants were male (2955/4122, 71.69%). Median eGFR was 96.61 ml/min/1.73 m2 (IQR 85.05–106.24). Compared to individuals without Cs and Hp infection, those with co-infection with Cs and Hp were more likely to be older and have higher levels of BMI, γ-GT, TG, FPG, UA, β2-MB, CRE and lower levels of eGFR.

Fig. 1
figure1

Flow chart of participant selection

Table 1 Baseline clinical characteristics of participants according to the infection of Helicobacter pylori and Clonorchis sinensis

Association between gender and age-related differences of participants and different intensities of Clonorchis sinensis infection

In order to investigate the association between gender and age-related differences and different intensities of Cs infection, all participants were divided into male group and female group according to gender differences, and were divided into three age groups according to age differences (group A: ≤ 30 years; group B: 31–50 years; group C: ≥ 51 years). In addition, participants from gender and age-related groups were subdivided into four grades according to eggs per gram of feces (EPG), namely G1: non-infection, G2: light (1–1999 EPG), G3: moderate (2000–3999 EPG) and G4: heavy (≥ 4000 EPG). The percentages of each grade in the gender and age-related groups were shown in Fig. 2. For the gender-related groups, in the male group, the percentages of G1, G2, G3 and G4 were 60.41, 25.28, 12.49 and 1.83%, respectively; in the female group, the percentages of G1, G2, G3 and G4 were 62.81, 24.85, 10.71 and 1.63%, respectively. There was no significant difference between the gender-related groups with different intensities of Cs infection (Z = 1.64, p = 0.102). For the age-related groups, in group A (≤ 30 years), the percentages of G1, G2, G3 and G4 were 63.25, 22.49, 12.07 and 2.19%, respectively; in group B (31–50 years), the percentages of G1, G2, G3 and G4 were 61.55, 25.16, 11.47 and 1.81%, respectively; in group C (≥ 51 years), the percentages of G1, G2, G3 and G4 were 58.94, 26.49, 13.11 and 1.47%, respectively. No significant differences were found among the age-related groups with different intensities of Cs infection (H = 2.84, p = 0.242).

Fig. 2
figure2

Association between gender and age-related differences of participants and different intensities of Clonorchis sinensis infection. For the gender-related groups, in male group, the percentages of G1, G2, G3 and G4 were 60.41, 25.28, 12.49 and 1.83%, respectively; in female group, the percentages of G1, G2, G3 and G4 were 62.81, 24.85, 10.71 and 1.63%, respectively. For the age-related groups, in group A (≤ 30 years), the percentages of G1, G2, G3 and G4 were 63.25, 22.49, 12.07 and 2.19%, respectively; in group B (31–50 years), the percentages of G1, G2, G3 and G4 were 61.55, 25.16, 11.47 and 1.81%, respectively; in group C (≥ 51 years), the percentages of G1, G2, G3 and G4 were 58.94, 26.49, 13.11 and1.47%, respectively

Comparison of CRE, BUN, β2−MB and eGFR of participants with Clonorchis sinensis and helicobacter pylori infection

To further investigate the relationship between Cs and Hp infection and candidate renal function markers (CRE, BUN, β2-MB and eGFR). We respectively compared participants infected with Cs or (and) Hp with non-infected participants. As shown in Fig. 3a, for BUN, no differences were found between the infected group and non-infected group. In Fig. 3b, for CRE, there was statistical differences between Hp(+) + Cs(−) group and Hp(−) + Cs(−) group (p = 0.046), Hp(−) + Cs(+) group and Hp(−) + Cs(−) group(p = 0.043), and the Hp(+) + Cs(+) group and Hp(−) + Cs(−) group (p < 0.001). For β2-MB(Fig. 3c), significant differences were found between Hp(+) + Cs(+) group and Hp(−) + Cs(−) group (p < 0.001), but no differences were found between the Hp(−) + Cs(−) group and the Hp(+) + Cs(−) group (p = 0.340) or the Hp(−) + Cs(+) group (p = 0.442). For eGFR (Fig. 3d), significant differences were observed between Hp(+) + Cs(+) group and Hp(−) + Cs(−) group (p < 0.001). However, no differences were found between the Hp(−) + Cs(−) group and the Hp(+) + Cs(−) group or Hp(−) + Cs(+) group (p = 0.167, p = 0.144, respectively).

Fig. 3
figure3

Association between Clonorchis sinensis and Helicobacter pylori infection and candidate renal function markers (CRE, BUN, β2-MB and eGFR). The levels of CRE, β2-MB in co-infection with Clonorchis sinensis and Helicobacter pylori group were higher and the levels of eGFR was lower than those in non-infection group. In addition, the levels of CRE in infection group were higher than those in non-infection group. However, no differences were found between infection group and non-infection group for BUN

Comparison of CRE, BUN, β2−MB and eGFR of participants with different intensities of Clonorchis sinensis infection

We also analyzed the association between different intensities of Cs infection and renal function markers (CRE, BUN, β2-MB and eGFR). As shown in Fig. 4a, for BUN, there was no differences between infection group and non-infection group (p > 0.05). For CRE (Fig. 4b), significant differences were found between the non-infection group and the light, moderate and heavy infection groups (p < 0.001, p = 0.003, p = 0.04, respectively). For β2-MB (Fig. 4c), there were significant differences between non-infection group and the light or heavy infection group (p = 0.001, p = 0.007, respectively), but there were no differences between non-infection group and the moderate infection group (p = 0.154). For eGFR (Fig. 4d), significant differences were observed between non-infection group and the moderate infection group (p = 0.025). However, no differences were found between non-infection group and the light or heavy infection group (p = 0.092, p = 0.274, respectively).

Fig. 4
figure4

Association between different intensities of Clonorchis sinensis infection and renal function markers (CRE, BUN, β2-MB and eGFR). The intensity of Clonorchis sinensis infection was expressed by eggs per gram of feces (EPG) and classified into three categories: light (1–1999 EPG), moderate (2000–3999 EPG), and heavy (≥4000 EPG). As shown in Fig. 4, there was no differences between different intensities of infection and non-infection for BUN. The levels of CRE in different intensity infection group were higher and the levels of eGFR in moderate infection group was lower than those in non-infection group. The levels of β2-MB in the light and heavy infection groups were higher than those in non-infection group

Association between co-infection with Clonorchis sinensis and helicobacter pylori and eGFR

In Table 2, the associations among co-infection with Cs and Hp and eGFR were analyzed by multiple linear regression models. In model 1, Hp(+) + Cs(+) was significantly associated with reduced eGFR (β = − 3.08, 95% CI: − 4.63 to − 1.53, p < 0.001) after adjustment for age, gender, history of hypertension and history of diabetes. Model 2 (Model 1 + BMI, SBP and DBP) and Model 3 (Model2 + ALT, AST, ALP, γ-GT, TC, TG, HDL, LDL, BUN, β2-MB and UA) also showed significant β values. However, there was no association between HP(+) + Cs(−) or HP(−) + Cs(+) and eGFR in the three models. Interestingly, after categorizing subjects by gender differences (Table 3), the relationship remained significant in females but not in males in Model 1 (β = − 10.25, 95% CI: − 12.52 to − 7.98, p < 0.001), Model 2 (β = − 9.71, 95% CI: − 11.96 to − 7.47, p < 0.001) and Model 3 (β = − 9.37, 95% CI: − 11.60 to − 7.13, p < 0.001).

Table 2 Association between co-infection with Helicobacter pylori and Clonorchis sinensis and eGFR
Table 3 Association between co-infection with Clonorchis sinensis and Helicobacter pylori and eGFR in gender difference

Discussion

To our knowledge, this is the first study to examine the association between Cs and Hp infection with eGFR in the general adult population. The important role of co-infection with CS and Hp in the renal function was highlighted in our study. We found that subjects with CS and Hp co-infection showed relatively reduced eGFR. The association was more significant in females, but not in males.

Most studies on the effects of Cs infection on human were focused on liver and gallbladder diseases [22,23,24]. Several studies have found that chronic infection with O.·viverrini (OV, a species of the liver flukes) may cause hepatobiliary diseases including cholangitis, periductal fibrosis, cholecystitis, obstructive jaundice and cholangiocarcinoma (CCA) [22, 23]. In addition, it has been reported that approximately 10% of clonorchiasis patients are susceptible to CCA [24]. Although renal function is not usually considered in chronic clonorchiasis like many other parasitic infections (e.g. Plasmodium spp, Schistosoma spp, Filarioidea) [25], glomerular lesions have been reported in laboratory animal models of OV infection [26, 27]. There is evidence that chronic OV infection may result in significant burden of kidney disease in the form of immune complex-mediated glomerulopathy [28]. Our results showed that there were no significant changes in creatinine and urea nitrogen in Cs-infected patients without Hp infection compared with non-infected patients, and there was no correlation with eGFR, which is inconsistent with the above studies [25,26,27]. We also identified the association between different intensities of CS infection and renal function markers (CRE, BUN, β2-MB and eGFR). Our results indicated that there are significant differences between different intensity infection and non-infection participants for CRE (p < 0.05) and differences between moderate infection group and non-infection group for eGFR (p = 0.025). In addition, significant differences were observed between non-infection group and the light or heavy intensity infection group for β2-MB (p < 0.01). These findings suggest that patients with different intensities of Cs infection are likely to be associated with impairment of renal function, but its mechanism is not yet clear.

Hp is a spiral-shaped gram-negative bacterium that has been found to naturally colonize the human gastric epithelium. Numerous reports have demonstrated a causal relationship between this infection and chronic gastritis, peptic ulceration, and gastric carcinoma [29, 30]. However, the relationship between Hp infection and kidney injury remains controversial. Recently, a meta-analysis showed that Hp infection might affect the prognosis of kidney diseases, and Hp was the main cause of secondary gastrointestinal diseases for patients with impaired renal function [31]. Several studies suggest that the prevalence of Hp might be lower in long-term dialysis patients than in short-term dialysis patients [32,33,34]. However, other studies showed that no significant association was found between Hp infection and duration of dialysis [35, 36]. Rasmi et al. [37] found that Hp infection rate was higher in long-term dialysis patients than in short-term dialysis patients. In addition, several studies reported that chronic Hp infection might be a major cause of gastroduodenal and gastrointestinal bleeding in dialysis patients with renal failure [38,39,40]. Therefore, it can be inferred that Hp infection may directly affect the survival rate of dialysis patients. In addition, there is evidence that long-term infection of Hp infection could increase the antibodies against Hp and aggravate renal function, resulting in more severe antigen deposition in IgA [15]. These findings suggest that Hp might be involved in the pathogenesis of IgA nephropathy through inducing strong mucosal immune response. Similarly, in vitro experiments showed that CagA, a key virulence factor of Hp, may participate in the pathogenesis of IgA nephropathy by influencing the production and glycosylation of IgA1 in B cells [16].

Another meta-analysis [41] showed that Type 2 diabetes (T2DM) patients with Hp infection had a 2 times higher risk of the occurrence of proteinuria than patients without Hp infection, indicating that Hp infection was associated with the occurrence of proteinuria in T2DM patients. Hp radical surgery might be a therapeutic option for protecting renal function in patients with T2DM [42]. However, a cross-sectional study [43] investigating the association between Hp infection and chronic kidney disease (CKD) did not find any significant difference in the prevalence of proteinuria and the overall CKD between the Hp infection group and non-infection group. In addition, multiple linear regression analysis showed that the odds of decreased eGFR and proteinuria were still not significantly different between the Hp positive and negative subjects. In the present study, our results showed that whether Hp infection alone, or co-infection with Cs, there was a negative correlation with CRE and eGFR. However, when adjusting for the confounding factors, only co-infection with Cs and Hp had a negative correlation with eGFR. Further subgroup analysis showed that co-infection with Cs and Hp may be associated with reduced renal function in females, but not in males.

Up to now, there was no report about the relationship between co-infection with Cs and Hp and renal function, However, it has been reported that chronic OV infection may result in immune complex-mediated glomerulopathy [28] and Hp might be involved in the pathogenesis of IgA nephropathy through inducing strong mucosal immune response [15, 16]. Therefore, we speculate that co-infection with Cs and Hp is more closely related to renal function impairment. In addition, sex has been viewed as an important factor influencing both renal function and the progression of kidney disease [44]. We thus further hypothesized that there might be sex difference between co-infection with Cs and Hp and renal function impairment. Our results showed that the impairment of renal function was more significant in females, but not in males. It has been proposed that women have more intense immune reactions than men, so they may suffer more immune diseases [45]. In addition, there is evidence that women are more susceptible to immune-induced kidney injury, such as lupus nephritis [46]. However, the specific mechanism still needs further investigations.

We have to note that there are some potential limitations in our research. First, subjects were recruited from the Health Examination Center of our hospital. Most of the participants work in enterprises or institutions with relatively higher education level and economic income, which may not represent the general population. Second, it is a cross-sectional design which makes it difficult to confirm the causality of risk factors. We can only examine the relationship between co-infection with Cs and Hp and eGFR. Third, calculated GFR, but not measured GFR, was used in the study and this indicator was not the gold standard to estimate renal function. Fourth, information regarding medication was not available. Relevant renoprotective medications that block the reninangiotensin-aldosterone system, and potential harmful medications such as nonsteroidal anti-inflammatory drugs, would exert effect on renal function. Fifth, eGFR is a complicated indicator involved in many factors. In addition to hypertension, diabetes and other excluded diseases considered in our study, there are still many factors that may affect renal function. Therefore, our research conclusion is merely a preliminary assessment, and its clinical significance should be analyzed in combination with other indicators in clinical practice. Finally, participants with eGFR> 60 were included in our study, although these differences were statistically significant, the differences in eGFR between the groups were small and may not suggest a clinical difference.

Conclusion

In this study, our findings suggest that co-infection with Cs and Hp may be associated with reduced renal function in females, but not in males. Nevertheless, the association between co-infection with Cs and Hp and renal function deserves further investigations for the potential pathophysiological mechanisms.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

eGFR:

Estimated glomerular filtration rate

Cs:

Clonorchis sinensis

Hp:

Helicobacter pylori

CKD:

Chronic kidney disease

EPG:

Eggs per gram of feces

References

  1. 1.

    Lun ZR, Gasser RB, Lai DH, Li AX, Zhu XQ, Yu XB, et al. Clonorchiasis: a key foodborne zoonosis in China. Lancet Infect Dis. 2005;5(1):31–41.

    PubMed  Article  PubMed Central  Google Scholar 

  2. 2.

    Chung PR, Soh CT. Snail-borne parasitic zoonoses in Korea. Southeast Asian J Trop Med Public Health. 1991;22(Supp l):391–517.

    PubMed  PubMed Central  Google Scholar 

  3. 3.

    Qian MB, Utzinger J, Keiser J, Zhou XN. Clonorchiasis. Lancet. 2016;387(10020):800–10.

    PubMed  Article  PubMed Central  Google Scholar 

  4. 4.

    Ma YX, Wang H. Epidemiological evolvement of Clonorchiasis sinensis in China for the past 60 years. Int J Med Parasit Dis. 2009;36(5):362–7 (in Chinese).

    Google Scholar 

  5. 5.

    LQ X, Sun FH, Coordinating Office of the National Survey on the Important Human Parasitic Diseases. A national survey on current status of the important parasitic diseases in human population. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi. 2005;23:332–40 in Chinese.

    Google Scholar 

  6. 6.

    Graham DY, Malaty HM, Evans DJ, Klein PD, Adam E. Epidemiology of H. pylori inan asymptomatic population in the United States: effect of age, race, and socioeconomic status. Gastroenterology. 1991;100(6):1495–14501.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  7. 7.

    Bang Cs KYS, Park SH, Kim JB, Baik GH, Suk KT, et al. Additive effect of pronase on the eradication rate of first-line therapy for Helicobacter pylori infection. Gut Liver. 2015;9(3):340–5.

    PubMed  PubMed Central  Google Scholar 

  8. 8.

    Lu LJ, Hao NB, Liu JJ, Li X, Wang RL. Correlation between Helicobacter pylori infection and metabolic abnormality in general population: a cross-sectional study. Gastroenterol Res Pract. 2018. https://doi.org/10.1155/2018/7410801.

  9. 9.

    Ozaydin N, Turkyilmaz SA, Cali S. Prevalence and risk factors of Helicobacter pylori in Turkey: a nationally-representative, crosssectional, screening with the 13C-urea breath test. BMC Public Health. 2013;13(1):1215.

    PubMed  PubMed Central  Article  Google Scholar 

  10. 10.

    Uchida T, Miftahussurur M, Pittayanon R, R-k V, Wisedopas N, Ratanachu-ek T, et al. Helicobacter pylori infection in Thailand: a Nationwide study of the CagA phenotype. PLoS One. 2015;10(9):e0136775.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  11. 11.

    Dangtakot R, Pinlaor S, Itthitaetrakool U, Chaidee A, Chomvarin C, Sangka A, et al. Co-infection with Helicobacter pylori and Opisthorchis viverrini enhances the severity of hepatobiliary abnormalities in hamsters. Infect Immun. 2017;85(4):e00009–17.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  12. 12.

    Deenonpoe R, Chomvarin C, Pairojkul C, Chamgramol Y, Loukas A, Brindley PJ, et al. The carcinogenic liver fluke Opisthorchis viverrini is a reservoir for species of Helicobacter. Asian Pac J Cancer Prev. 2015;16(5):1751–8.

    PubMed  PubMed Central  Article  Google Scholar 

  13. 13.

    Ozgur O, Boyacioglu S, Ozdogan M, Gur G, Telatar H, Haberal M. Helicobacter pylori infection in hemodialysis patients and renal transplant recipients. Nephrol Dial Transplant. 1997;12(2):289–91.

    CAS  PubMed  Article  Google Scholar 

  14. 14.

    Gür G, Boyacioglu S, Gül C, Turan M, Gürsoy M, Baysal C, et al. Impact of Helicobacter pylori infection on serum gastrin in hemodialysis patients. Nephrol Dial Transplant. 1999;14(11):2688–91.

    PubMed  Article  Google Scholar 

  15. 15.

    Zhu TT, Wang L, Wang HL, He Y, Ma X, Fan JM. Helicobacter pylori participates in the pathogenesis of IgA nephropathy. Ren Fail. 2016;38(9):1398–404.

    CAS  PubMed  Article  Google Scholar 

  16. 16.

    Yang M, Li FG, Xie XS, Wang SQ, Fan JM. CagA, a major virulence factor of Helicobacter pylori, promotes the production and underglycosylation of IgA1 in DAKIKI cells. Biochem Biophys Res Commun. 2014;444(2):276–81.

    CAS  PubMed  Article  Google Scholar 

  17. 17.

    Fang YY, Chen YD, Li XM, Wu J, Zhang QM, Ruan CW. Current prevalence of Clonorchis sinensis infection in endemic areas of China. Zhong guo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi. 2008;26(2):99–103 109. (in Chinese).

    Google Scholar 

  18. 18.

    WHO Expert Committee. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. World Health Organ Tech Rep Ser. 2002;912:i–vi 1–57.

    Google Scholar 

  19. 19.

    WHO. Soil-transmitted helminthiases: eliminating as public health problem soil-transmitted helminthiases in children: progress report 2001–2010 and strategic plan 2011–2020; 2012.

    Google Scholar 

  20. 20.

    Connor SJ, Seow F, Ngu MC, Katelaris PH. The effect of dosing with omeprazole on the accuracy of the 13C-urea breath test in Helicobacter pylori-infected subjects. Aliment Pharmacol Ther. 1999;13(10):1287–93.

    CAS  PubMed  Article  Google Scholar 

  21. 21.

    Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, et al. A new equation to estimate glomerular filtration rate. Ann Intern Med. 2009;150(9):604–12.

    PubMed  PubMed Central  Article  Google Scholar 

  22. 22.

    IARC. A review of human carcinogens: Opisthorchis viverrini and Clonorchis sinensis. IARC Monogr Eval Carcinog Risks Hum. 2012;100:341–70.

    Google Scholar 

  23. 23.

    Sithithaworn P, Andrews RH, Van De N, Wongsaroj T, Sinuon M, Odermatt P, et al. The current status of opisthorchiasis and clonorchiasis in the Mekong Basin. Parasitol Int. 2012;61(1):10–6.

    PubMed  Article  Google Scholar 

  24. 24.

    Mairiang E, Haswell-Elkins MR, Mairiang P, Sithithaworn P, Elkins DB. Reversal of biliary tract abnormalities associated with Opisthorchis viverrini infection following praziquantel treatment. Trans R Soc Trop Med Hyg. 1993;87(2):194–7.

    CAS  PubMed  Article  Google Scholar 

  25. 25.

    Van Velthuysen ML, Florquin S. Glomerulopathy associated with parasitic infections. Clin Microbiol Rev. 2000;13(1):55–66.

    PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Boonpucknavig S, Boonpucknavig V, Tanvanich S, Doungchawee G, Thamavit W. Development of immune-complex glomerulonephritis and amyloidosis in Syrian golden hamsters infected with Opisthorchis viverrini. J Med Assoc Thai. 1992;75(Suppl 1):7–19.

    PubMed  PubMed Central  Google Scholar 

  27. 27.

    Boonpucknavig V, Soontornniyomkij V. Pathology of renal diseases in the tropics. Semin Nephrol. 2003;23(1):88–106.

    PubMed  Article  PubMed Central  Google Scholar 

  28. 28.

    Saichua P, Sithithaworn P, Jariwala AR, Deimert DJ, Sithithaworn J, Sripa B, et al. Microproteinuria during Opisthorchis viverrini infection: a biomarker for advanced renal and Hepatobiliary pathologies from chronic Opisthorchiasis. PLoS Negl Trop Dis. 2013;7(5):e2228.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. 29.

    Gray BM, Fontaine CA, Poe SA, Eaton KA. Complex T cell interactions contribute to helicobacter pylori gastritis in mice. Infect Immun. 2013;81(3):740–52.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  30. 30.

    Zhang Y, Weck MN, Schöttker B, Rothenbacher D, Brenner H. Gastric parietal cell antibodies, Helicobacter Pylori infection, and chronic atrophic gastritis: evidence from a large population-based study in Germany. Cancer Epidemiol Biomarkers Prev. 2013;22(5):821–6.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  31. 31.

    Li KJ, Chen L. Association between duration of dialysis and Helicobacter pylori infection in dialysis patients: a meta analysis. Int Urol Nephrol. 2019;51(8):1361–70.

    PubMed  Article  Google Scholar 

  32. 32.

    Nakajima F, Sakaguchi M, Oka H, Kawase Y, Shibahara N, Inoue T, et al. Prevalence of Helicobacter pylori antibodies in long-term dialysis patients. Nephrology. 2004;9(2):73–6.

    PubMed  Article  Google Scholar 

  33. 33.

    Mortazavi F, Rafeey M. Endoscopic findings and Helicobacter pylori in children on long-term hemodialysis. Pak J Biol Sci. 2008;11(14):1840–3.

    PubMed  Article  Google Scholar 

  34. 34.

    Antoniou S, Dimitriadis A, Kliridou M, Pavlitou K, Batzili H, Malaka E. Prevalence of Helicobacter pylori antibodies in CAPD patients. Nephron. 1997;75(3):358–9.

    CAS  PubMed  Article  Google Scholar 

  35. 35.

    Ozgur O, Boyacioglu S, Ozdogan M, Gür TH, Haberal M. Helicobacter pylori infection in hemodialysis patients and renal transplant recipients. Nephrol Dial Transplant. 1997;12(2):289–91.

    CAS  PubMed  Article  Google Scholar 

  36. 36.

    Gür G, Boyacioglu S, Gül C, Turan M, Gürsoy M, Baysal C, et al. Impact of Helicobacter pylori infection on serum gastrin in hemodialysis patients. Nephrol Dial Transplant. 1999;14(11):2688–91.

    PubMed  Article  Google Scholar 

  37. 37.

    Rasmi Y, Farshid S, Makhdomi K. Effect of duration on hemodialysis on prevalence of Helicobacter pylori infection. Saudi J Kidney Dis Transpl. 2012;23(3):489–92.

    PubMed  Google Scholar 

  38. 38.

    Tamadon MR, Saberi M, Soleimani A, Ghorbani R, Semnani V, Malek F, et al. Evaluation of noninvasive tests for diagnosis of Helicobacter pylori infection in hemodialysis patients. J Nephropathol. 2013;2(4):249–53.

    PubMed  PubMed Central  Google Scholar 

  39. 39.

    Shirazian S, Radhakrishnan J. Gastrointestinal disorders and renal failure: exploring the connection. Nat Rev Nephrol. 2010;6(8):480–92.

    PubMed  Article  Google Scholar 

  40. 40.

    Moriyama T, Matsumoto T, Hirakawa K, Ikeda H, Tsuruya K, Hirakata H, et al. Helicobacter pylori status and esophagogastroduodenal mucosal lesions in patients with end-stage renal failure on maintenance hemodialysis. J Gastroenterol. 2010;45(5):515–22.

    PubMed  Article  Google Scholar 

  41. 41.

    Li KJ, Chen L. Association between duration of dialysis and Helicobacter pylori infection in dialysis patients: a meta analysis. Int Urol Nephrol. 2019;51(8):1361–70.

    PubMed  Article  Google Scholar 

  42. 42.

    Shi Y, Duan JY, Liu DW, Qiao YJ, Han QX, Pan SK, et al. Helicobacter pylori infection is associated with occurrence of proteinuria in type 2 diabetes patients: a systemic review and meta-analysis. Chin Med J (Engl). 2018;131(22):2734–40.

    Article  Google Scholar 

  43. 43.

    Kong X, Xu D, Li F, Ma X, Su H, Xu D. Association of H. pylori infection with chronic kidney disease among Chinese adults. Int Urol Nephrol. 2017;49(5):845–50.

    PubMed  Article  Google Scholar 

  44. 44.

    Silbiger S, Neugarten J. Gender and human chronic renal disease. Gend Med. 2008;5(Suppl A):S3–S10.

    PubMed  Article  Google Scholar 

  45. 45.

    Whitacre CC, Reingold SC, O'Looney PA. A gender gap in autoimmunity. Science. 1999;283:1277–8.

    CAS  PubMed  Article  Google Scholar 

  46. 46.

    Wang H, Xu J, Zhang X, Ren YL, Cheng M, Guo ZL, et al. Tubular basement membrane immune complex deposition is associated with activity and progression of lupus nephritis: a large multicenter Chinese study. Lupus. 2018;27:545–55.

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgements

We would like to thank the participants in this study for their cooperation. We also thank the academic and non-academic staff of Guangdong Provincial Hospital of Integrated Traditional Chinese and Western Medicine for their help.

Funding

This study received no specific grant from any funding agency, commercial or not-for-profit sectors.

Author information

Affiliations

Authors

Contributions

WNX and YJD performed the statistical analysis and drafted the manuscript, participated in the validation. WNX and QHY participated in the design of the study. SXC, YFW and YL contributed to the collection of clinical samples, related experiments, and case records. The authors read and approved the final manuscript.

Corresponding author

Correspondence to Qinhe Yang.

Ethics declarations

Ethics approval and consent to participate

This study was approved by the Ethics Committee of Guangdong Provincial Hospital of Integrated Traditional Chinese and Western Medicine. All participants were informed regarding voluntary participation and they were advised that they could withdraw from the study at any time. Written informed consent was acquired from all participants. All data were kept confidential.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Xie, W., Deng, Y., Chen, S. et al. Association between renal function and co-infection with Clonorchis sinensis and Helicobacter pylori: a cross-sectional study. BMC Infect Dis 20, 868 (2020). https://doi.org/10.1186/s12879-020-05616-0

Download citation

Keywords

  • Clonorchis sinensis
  • Helicobacter pylori
  • Renal function
  • eGFR