The Prevalence of Helicobacter pylori Infection in Patients with Chronic Kidney Disease Undergoing Hemodialysis
Categoría del artículo: Original Scientific Article
Publicado en línea: 22 mar 2022
Páginas: 225 - 232
Recibido: 02 ago 2021
Aceptado: 28 sept 2021
DOI: https://doi.org/10.2478/sjecr-2021-0044
Palabras clave
© 2024 Batric Babovic et al., published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Chronic kidney disease (CKD) is a progressive loss of kidney function that is presented by glomerular filtration rate below 60 ml/min/1.73m2 for a period longer than 3 months (1). Because of growing prevalence, it has been recognised as one of the main death causes among the chronic non-communicable diseases (2). Data from 2017 testify the age-standardised morbidity rate for Montenegrin population was 13.1% (3).
Progressive CKD has been associated with a number of serious complications including gastrointestinal disturbances (4, 5). Most often it is about dyspeptic symptoms like occasional or constant epigastric pain, early satiety, bloating, nausea, excessive belching and postprandial fullness (6, 7). The pathogenetic aspects of dyspepsia have been sufficiently unexplored. Many factors are thought to be involved in pathogenesis of this condition like uremic toxins (8), digestive hypomotility (9), amyloid protein deposition (10), sensory disturbances (11), and
The prevalence of HP infection and its relationship to gastroduodenal lesions in hemodialysis patients have been extensively studied (13). Nevertheless, the available literature data on the HP presence in hemodialysis patients are quite unequal with a wide range of variation (20–80%) (14, 15). There are also different opinions on the frequency of gastroduodenal lesions in hemodialysis CKD patients compared to non-CKD subjects (16). Some authors reported that hemodialysis patients suffered more often from gastroduodenal disorders while the others not found the differences between hemodialysis and the general population (13, 17, 18).
Thus, the aim of our study was to determine the prevalence of HP infection and gastroduodenal lesions as well as their connections with certain biochemical findings and hemodialysis quality in Montenegrin CKD patients with dyspeptic symptoms.
The investigation has been conducted as a single center, cross-sectional study with one-time point evaluation during 2019 and early 2020s in Clinical Center of Montenegro, Podgorica. The study initially enrolled 70 patients with diagnosis of CKD undergoing hemodialysis, but further research was continued with 55 patients in whom dyspeptic symptoms have been identified for at least 3 months. The control group consisted of 50 consecutive, age and gender matched, subjects with preserved kidney function referred for endoscopic examination due to dyspepsia. The exclusion criteria for participation in the study were: (1) recent active infections, (2) chronic inflammatory or autoimmune diseases; (3) previously diagnosed gastroduodenal structural changes like inflammation or ulcer; (4) contraindications for performing upper gastrointestinal endoscopy, (5) therapy with H2 inhibitors, proton pump antagonists and/or nonsteroidal anti-inflammatory drugs; (6)
The study was planned according to the Declaration of Helsinki. All patients and control subjects gave informed consent for the participation. The investigation has been approved by the institutional Ethical Committee according to local research regulations.
We performed an interview about dyspeptic symptoms in all study subjects as well as physical and biochemical examination. Gastroduodenoscopy with pathohistological analysis of biopsy specimens was applied only in the cases of confirmed dyspepsia. The study also concerned to dialysis parameters such as the duration of hemodialysis (in months) and its efficiency.
Dyspepsia was defined based on Roma III criteria (19): the presence of certain symptoms, which exist for the last 3 months onset and continue at least 6 months prior to diagnosis (excluding structural gastroduodenal disease). A questionnaire included the following dyspeptic symptoms: constant and occasional epigastric pain, bloating, early satiety, nausea, vomiting and heartburn.
Biochemical parameters (hemoglobin, urea, creatinine) were investigated by standard laboratory methods, while the acid-base balance was assessed by pH and bicarbonate (HCO3−) concentration.
Chemiluminescent immunoassay and
The efficiency of hemodialysis was assessed by calculation of Kt/V with dialysis machine software. Kt/V presents dialyzer clearance of urea (expressed in ml/min) multiplied by the dialysis time (expressed in minutes) and divided by volume of distribution of urea.
Gastroduodenoscopy with Olympus XQ 40 endoscope was performed in all study participants in whom the presence of dyspeptic symptoms was previously determined by the questionnaire. During the procedure, the biopsy specimens were taken from the corpus and antrum of the stomach, and stored in 4% formalin to further processing. The final diagnosis was made by endoscopic and histopathological findings of mucosal lesions regarding the degree of inflammation and its activity, the degree of atrophy, intestinal metaplasia and
The commercial software SPSS version 22.0 for Windows was used for the statistical analysis. Data are presented as mean ± standard deviation (SD). Differences in the parameters between the groups of patients were estimated by the Independent samples T-test or Mann-Whitney U-test (depending on the distribution). Chi-square (χ2) test served to compare the frequency of categorical variables. For all tests described above,
The results of our study are presented in Tables 1–3 and Figures 1–3.
Frequency of pathohistological categories of corpus mucosa in two study groups
| Category | Hemodialysis patients n = 55 | Control patients n = 50 | χ2 | significance | |
|---|---|---|---|---|---|
| Inflammation activity | Yes | 28 (50.9%) | 31 (62.5%) | 1.084 | p = 0.298 |
| No | 27 (49.1%) | 19 (37.5%) | |||
| Atrophy | Yes | 23 (41.9%) | 8 (15%) | 7.274 | |
| No | 32 (58.1%) | 42 (85%) | |||
| Intestinal metaplasia | Yes | 0 | 0 | – | – |
| No | 55 (100%) | 50 (100%) | |||
| Helicobacter pylori | Yes | 28 (50.9%) | 22 (44%) | 0.315 | p = 0.574 |
| No | 27 (49.1%) | 28 (56%) | |||
Frequency of pathohistological categories of antrum mucosa in two study groups
| Category | Hemodialysis patients n = 55 | Control patients n = 50 | χ2 | significance | |
|---|---|---|---|---|---|
| Inflammation activity | Yes | 39 (72.1%) | 21 (42.5%) | 0.485 | p = 0.486 |
| No | 16 (27.9%) | 29 (57.5%) | |||
| Atrophy | Yes | 24 (44.2%) | 21 (42.5%) | 0.024 | p = 0.877 |
| No | 31 (55.8%) | 29 (57.5%) | |||
| Intestinal metaplasia | Yes | 2 (4.7%) | 0 | 1.906 | p = 0.167 |
| No | 53 (95.3%) | 50 (100%) | |||
| Helicobacter pylori | Yes | 33 (60.6%) | 26 (52.5%) | 0.890 | p = 0.355 |
| No | 22 (39.4%) | 24 (47.5%) | |||
The relationships of HP presence and laboratory parameters
| Parameter | Corpus mucosa | Antrum mucosa | |||
|---|---|---|---|---|---|
| Mean value | p | Mean value | p | ||
| Hemoglobin (g/dl) | HP− | 10.47 | p = 0.269 | 10.52 | p = 0.508 |
| HP+ | 10.89 | 10.78 | |||
| Creatinine (μmol/l) | HP− | 1017.0 | p = 0.394 | 1024.3 | p = 0.394 |
| HP+ | 963.64 | 969.18 | |||
| PTH (pg/ml) | HP− | 473.73 | p = 0.537 | 480.59 | p = 0.568 |
| HP+ | 396.87 | 407.01 | |||
| pH | HP− | 7.310 | p = 0.133 | 7.309 | p = 0.169 |
| HP+ | 7.323 | 7.322 | |||
| HCO3− (mmol/l) | HP− | 13.70 | 13.78 | p = 0.156 | |
| HP+ | 14.70 | 14.47 | |||
| Dialysis duration (months) | HP− | 91.10 | 106.38 | ||
| HP+ | 31.68 | 33.63 | |||
| Kt/V | HP− | 1.226 | p = 0.447 | 1.199 | p = 0.765 |
| HP+ | 1.190 | 1.213 | |||
The prevalence of dyspeptic symptoms in hemodialysis patients and control subjects
Endoscopic findings of the stomach in hemodialysis patients and control subjects
Endoscopic findings of the duodenum in hemodialysis patients and control subjects
The study included 55 maintenance hemodialysis patients with dyspepsia and 50 control subjects, who underwent endoscopic examination because of dyspeptic symptoms. There were 29 (52.8%) males and 26 (47.2%) females in the group of hemodialysis patients, respectively 27 males (54%) and 23 females (46%) in the control group. The average age of hemodialysis patients was 56.48 ± 13.66ys, while in the control group it was 54.45 ± 11.38ys (Independent samples T test, p = 0.311).
Analysis of dyspeptic symptoms showed that occasional epigastric pain, bloating and nausea were the dominant symptoms in the group of hemodialysis patients, while the control group mostly showed early satiety, bloating and nausea (Figure 1). It estimated the significant difference in the frequency of constant epigastric pain (χ2 = 4.335, p=0.037) and vomiting (χ2 = 10.772, p=0.005) between the groups.
Data obtained by gastroduodenal examination did not confirm a statistically significant difference in endoscopic findings of the stomach between hemodialysis patients and control subjects (χ2 = 5.758, p=0.451).
The most common finding in both study groups was gastritis, confirmed in 27 (49.1%) hemodialysis patients and 28 (56%) control subjects. When it comes to duodenal lesions, majority of hemodialysis patients had a normal endoscopic finding (67.9%), while in control participants duodenitis was the most frequent (42%) (p < 0.001) (Figures 2–3).
The results of pathohistological examination of biopsy samples taken from the corpus and antrum of the stomach are shown in Tables 1–2.
We found that atrophy of corpus mucosa was significantly more prevalent in hemodialysis patients (p = 0.007) compared to control subjects, who mainly showed the signs of inflammatory activity in the corpus. There was no statistically significant difference in the presence of HP infection neither in the samples of a corpus or an antrum between two study groups. HP was confirmed in 50.9% of corpus mucosa i.e. 60.6% of antrum mucosa of hemodialysis maintain patients.
In further research, we analyzed the influence of certain biochemical parameters and dialysis treatment on the occurrence of gastric atrophy and HP positivity. It has been estimated that gastric atrophy was more common to CKD patients that underwent hemodialysis for a longer time (p < 0.001). No influence of Kt/V (p = 0.385), concentration of hemoglobin (p = 0.338), creatinine (p = 0.100) and PTH (p = 0.201) on atrophic changes was observed. The disturbance of acid-base balance (lower pH) had a positive effect on the occurrence of gastric atrophy (p = 0.011).
When it comes to relationships of HP presence and the above-mentioned parameters, the data are shown in Table 3.
HP presence was higher in both corpus and antrum samples of CKD patients that underwent hemodialysis for a shorter period. Also, a positive relationship between bicarbonate concentration and HP infection was demonstrated (p = 0.031).
The current study analyzed the presence of gastroduodenal lesions and Helicobacter pylori infection in Montenegrin hemodialysis patients with dyspeptic symptoms.
We estimated that CKD patients undergoing hemodialysis commonly presented as dyspepsia as occasional epigastric pain, bloating and nausea. However, dyspeptic symptoms were more pronounced in control subjects. There were no significantly differences in endoscopic findings between the two study groups of participants, although control subjects had more often the lesions of the duodenum. Pathohistological analysis demonstrated that atrophy of corpus mucosa was more prevalent in hemodialysis patients and it positively correlated with dialysis duration. Lower pH also stimulated atrophic changes. The prevalence of HP was over 50 percent so that its presence was higher in the patients that underwent hemodialysis for a shorter time.
HP is a gram-negative bacillus that inhabits the gastric mucosa and it seems to have an important role in the pathogenesis of gastroduodenal disorders in hemodialysis patients (20, 21). Namely, HP modulates gastric secretion by increasing serum gastrin concentration and decreasing the level of somatostatin in the gastric mucosa (22). On the other hand, the inflammatory response to HP can induce the dysfunction of gastric smooth muscles and lower sensation for gastric distension (5, 23).
The results of previous studies on gastroduodenal lesions and HP infection in hemodialysis patients are quite inconsistent (13, 17). There is no single view on the frequency of endoscopic findings in CKD patients that underwent hemodialysis (existence of an equal or higher rate of lesions compared to the general population). Our investigation showed that duodenal lesions were more common in control subjects, who mainly had a histopathological finding of inflammation and a pronounced clinical presentation of dyspepsia. Contrary, atrophic mucosal changes and HP presence was higher in hemodialysis patients. These results indicate the potential effect of HP on the occurrence of mucosal atrophy. Namely, ammonia, a product of urea
Our results are in agreement with the findings of Khedmat and coworkers (13), who also reported higher prevalence of HP infection in CKD patients. Here, we must emphasize that, although higher in hemodialysis patients, the prevalence of HP did not differ significantly between two groups enrolled in the study. A meta-analysis conducted by Wijarnpreecha (26) estimated HP infection prevalence of 44% in end-stage CKB patients, which is similar to our findings in the stomach (HP confirmed in just over 50% of cases). However, current literature data indicates a wide range of variation in HP positivity in hemodialysis patients (14, 27, 28), which could be a consequence of the different design and methodology of the conducted studies.
Interestingly, we have shown the reduction of HP positivity in the patients that underwent hemodialysis for a longer time. In other words, the duration of dialysis was significantly longer in HP negative patients and
However, further investigations are needed to determine the association between the duration of dialysis and HP prevalence by continuous monitoring of CKD patients at multiple time points. Previous research, including ours, have focused on HP infection in dialysis patients by single sampling and measurement of appropriate variables.
The estimated prevalence of Helicobacter pylori in Montenegrin hemodialysis patients was over 50%, with a somewhat greater presence in the antral mucosa. There were no significant differences in endoscopic findings between CKD patients undergoing hemodialysis and non-CKD patients with dyspepsia. Atrophic mucosal changes were more common in hemodialysis patients and they positively correlated with dialysis duration. Helicobacter pylori presence was reduced in the patients that underwent hemodialysis for a longer time.