Abstract
Background
Different gastrointestinal complications can occur due to moderate and severe kidney function loss in chronic kidney disease (CKD). This study examined the endoscopic and pathological findings in CKD patients with renal failure who were not receiving dialysis treatment and renal transplantation.
Material/Methods
A total of 60 pre-dialysis CKD patients who underwent upper-gastrointestinal endoscopy due to dyspeptic concerns were included. Endoscopic and pathological findings were compared with those of 68 non-uremic patients with similar concerns. Dyspeptic symptoms included upper-abdominal discomfort, nausea, vomiting, anorexia, indigestion, and regurgitation. Serum creatinine levels ≥1.5 mg/dL and eGFR stages 3a-4 (KDIGO guidelines) were used to define CKD.
Results
This study found no significant difference in gastroesophageal reflux frequency between the groups. However, antral gastritis, erythematous gastritis, active chronic gastritis, and non-ulcerative lesions were significantly more frequent in CKD patients (P<0.001). Conversely, erosive pangastritis was more prevalent in the non-CKD group. Helicobacter pylori (HP) frequency was significantly lower in CKD patients (23.5%) compared to the non-CKD group (59.1%, P<0.001). Intestinal metaplasia, atrophy, and metaplastic gastritis rates were similar in both groups. Multivariate analysis identified gastritis and serum calcium as independent factors affecting HP positivity.
Conclusions
In CKD patients, uremic toxins, impaired circulation, and hypergastrinemia likely contribute to mucosal damage and increased the risk of gastrointestinal complications. Early detection and management of these lesions in pre-dialysis CKD patients are crucial, especially for kidney transplant candidates. Endoscopic evaluation and appropriate treatment can help reduce potential complications associated with immunosuppressive therapy and can improve patient outcomes.
Keywords: Dialysis; Endoscopes, Gastrointestinal; Kidney Failure, Chronic; Gastritis; Helicobacter pylori; Dyspepsia; Pathology, Clinical
Introduction
Complications can occur due to decreased kidney function in patients with chronic kidney disease (CKD) [1]. Gastrointestinal problems are one of them. In patients with CKD, hypergastrinemia due to uremic toxins is associated with decreased gastrointestinal motility, hypo- and hypersecretion of stomach acid, polypharmacy, and the risk of gastrointestinal disturbances due to Helicobacter pylori (HP) infection [2,3]. Psychological problems are also an additional risk factor. Therefore, in patients with CKD, dyspeptic symptoms characterized by upper-abdominal discomfort, nausea, vomiting, abdominal pain, anorexia, indigestion, and regurgitation may occur, and the risk of malignancy increases [1,2]. HP can cause serious diseases such as peptic ulcer, gastritis, stomach cancer and lymphoma [2,4]. While it occurs in 15–74.4% of the non-CKD population, this rate is 20–64% in patients with CKD [4]. Patients with CKD who are not end-stage are potential candidates for dialysis and kidney transplantation. After these patients reach the end-stage, their gastrointestinal problems increase due to the effects of uremia and immunosuppressive drugs. Therefore, before moving on to this stage, especially for those who are symptomatic, endoscopic evaluation and treatment may be necessary.
In this study, we assessed endoscopic and pathological findings in patients with severe CKD who underwent upper-gastrointestinal system endoscopy due to dyspepsia.
Material and Methods
The study was a single-center cross-sectional study and data were collected from patients who underwent consecutive endoscopy between 2022 and 2023. Endoscopic and pathological findings of patients with and without chronic kidney disease who applied to the gastroenterology clinic due to similar dyspeptic concerns were compared. Patients who underwent endoscopy for upper-gastrointestinal symptoms were considered to have chronic kidney disease (CKD) if their serum creatinine level was ≥1.5 mg/dL and their estimated glomerular filtration rate (eGFR), as defined by the Kidney Disease: Improving Global Outcomes (KDIGO) guidelines, corresponded to stage 3a (45–60 mL/min/1.73 m2), stage 3b (30–44 mL/min/1.73 m2), or stage 4 (15–29 mL/min/1.73 m2) for at least 6 months.
Patients over 18 years of age, confirmed to have chronic kidney disease, and who underwent endoscopy due to their symptoms were included in the study. We excluded patients with acute renal failure, severe chronic disease, long-term use of antacid drugs (proton pump inhibitors and H2 receptor antagonists), taking anticoagulant drugs for more than 3 months, or receiving immunosuppressive drug use from the study. The control group was defined as having similar age, sex, and dyspepsia, without chronic kidney disease and with normal eGFR. The CKD group included 60 CKD patients (32 men, 28 women) who were not receiving dialysis treatment. Their median age was 59.5 (min: 25, max: 89) years. The control group (non-CKD group) consisted of 34 males and 34 females with normal kidney function and no kidney disease history. Their median age was 53.8 (min: 25, max: 85) years. The study was conducted according to Good Clinical Practice guidelines, and permission was obtained from the local institutional ethics committee to use patient data for publication (Approval Date: 03/04/2024; Reference number/Protocol Number: 2024-5/16). Laboratory data, clinical features, esophagogastroduodenoscopy findings, and biopsy (histological evaluation and identification of HP staining) results were obtained from the medical records retrospectively.
Statistical Analysis
We used the Shapiro-Wilk test to assess the normal distribution of continuous variables. We present descriptive statistics for group comparisons, including mean±standard deviation or median (minimum: maximum) values. We made comparisons of numerical variables in both groups using the Mann-Whitney U test and the independent paired-sample t test. We used a χ2 test (or Fisher’s exact test if any expected cell count was <5) and present descriptive statistics as numbers and percentages to analyze categorical data. Binary logistic regression analysis was performed to determine independent risk factors affecting the presence of endoscopic gastritis and duodenitis, pathological chronic gastritis, and HP. The backward elimination method was used in multivariate logistic regression analysis to find the best final model. Data were analyzed using SPSS Software (IBM Corp. Released 2015. IBM SPSS Statistics for Windows, Version 23.0. Armonk, NY: IBM Corp). A P value of <0.05 was considered statistically significant.
Results
A total of 128 patients were included in the study. The mean age in the CKD group was similar to that the non-CKD group (median age was 59) [59.5±11.5 (25–79) vs. 53.6±13.2 (29–86) years] (P>0.05). Sex and primary disease distributions were similar in the 2 groups. When comorbid diseases were evaluated, diabetes mellitus (38.6% vs 23.7%) and hypertension (65.3% vs 34.2%) were significantly higher in the CKD group compared to the non-CKD group (P<0.001). Laboratory values of both groups were given in Table 1. Serum urea, creatinine, potassium, phosphorus, CRP, and ferritin values were significantly higher in the CKD group, whereas eGFR, calcium, total protein, total and HDL cholesterol, erythrocyte, hemoglobin, and hematocrit values were significantly higher in the non-CKD group.
Table 1.
Comparison of laboratory parameters of both groups.
| Variables | Total (n: 128) | Non-CKD group (n: 68) | CKD group (n: 60) | P value |
|---|---|---|---|---|
| Glucose (mg/dL) | 102 | 96 | 115 | 0.170* |
| Urea (mg/dL) | 54.5 | 27 | 80 | <0.001* |
| Creatinine (mg/dL) (n: 110) | 1.4 | 0.7 | 2.4 | <0.001* |
| eGFR ml/dk/1.73 m2 (n: 110) | 44.6 | 98 | 28 | <0.001* |
| Uric acid (mg/dL) | 5.8 | 5.2 | 6.2 | 0.069* |
| Sodium (mmol/L) | 139.1 | 139.8 | 138.7 | 0.124# |
| Potassium (mmol/L) | 4.5 | 4.3 | 4.6 | 0.007# |
| Calcium (mg/dL) | 8.9 | 9.5 | 8.9 | <0.001# |
| Phosphorus (mg/dL) | 4.1 | 3.3 | 4.2 | 0.029* |
| Total protein (g/dL) | 62.9 | 71.4 | 59.8 | <0.001* |
| Total Cholesterol (mg/dL) | 174 | 207 | 145 | 0.005# |
| HDL (mg/dL) (n: 31) | 48 | 56 | 38 | <0.001* |
| Triglyceride (mg/dL) | 135 | 108 | 164 | 0.444* |
| LDL (mg/dL) | 113 | 117 | 105 | 0.270* |
| AST (IU/L) | 16.5 | 17 | 16 | 0.981# |
| ALT (IU/L) | 15 | 18.5 | 12 | 0.012* |
| CRP (mg/L) | 3.4 | 0.6 | 12 | <0.001* |
| Iron (μg/dl) | 63.2 | 67.9 | 59.2 | 0.519# |
| TIBC (μg/dl) | 253 | 266 | 243 | 0.421# |
| Ferritin (μg/L) | 77 | 40.5 | 215 | <0.001* |
| Erythrocytes (106 μL) | 4.2 | 4.7 | 3.5 | <0.001* |
| Hemoglobin (g/dL) | 11.8 | 13.3 | 10.1 | <0.001* |
| Hematocrit (%) | 36.1 | 40.2 | 30.5 | <0.001* |
| RDW (fL) | 14.6 | 13.6 | 15.9 | <0.001* |
| Platelet (103 μ/L) | 234 | 249.5 | 195.5 | <0.001* |
| MPV (fL) | 10 | 9.8 | 10.6 | 0.003* |
Data are expressed as median values. eGFR – estimated glomerular filtration rate; HDL – high-density lipoprotein; LDL – low-density lipoprotein; AST – aspartate aminotransferase; ALT – alanine aminotransferase; CRP – C-reactive protein; TIBC – total iron binding capacity; RDW – red cell distribution; MPV – mean platelet volume.
Mann-Whitney U test,
independent paired-sample t test.
Endoscopic findings are given in Table 2. The 2 groups had similar rates of non-ulcerous and ulcerous lesions, such as gastroesophageal reflux, antral erosive gastritis, duodenitis and fundus polyp. The CKD group had significantly higher rates of antral gastritis, erythematous gastritis, erosive pangastritis, active chronic gastritis, and esophageal varicose veins, whereas the non-CKD group had significantly higher rates of esophagitis LA and bulbitis (Figure 1). Pyloric diverticulum was not detected in either group.
Table 2.
Comparison of endoscopic findings of both groups.
| Variables n (%) | Total (n: 128) | Non-CKD group (n: 68) | CKD group (n: 60) | P value |
|---|---|---|---|---|
| Gastroesophageal reflux | 13 (10.2%) | 4 (6%) | 9 (15%) | 0.094* |
| Non-ulcerous lesion | ||||
| Esophagitis LA | 44 (34.6%) | 36 (53.7%) | 8 (13.3%) | <0.001* |
| Antral gastritis | 59 (46.5%) | 25 (37.3%) | 34 (56.7%) | 0.029* |
| Antral erosive gastritis | 14 (10.9%) | 19 (14.7%) | 4 (6.7%) | 0.146* |
| Erythematous gastritis | 4 (3.1%) | 0 | 4 (6.7%) | 0.046# |
| Duodenitis | 5 (3.9%) | 4 (5.9%) | 1 (1.7%) | 0.370# |
| Bulbitis | 20 (15.6%) | 16 (23.5%) | 4 (6.7%) | 0.009* |
| Erosive pangastritis | 8 (6.3%) | 0 | 8 (13.3%) | 0.002# |
| Fundus polyp | 5 (3.9%) | 3 (4.4%) | 2 (3.3%) | >0.99# |
| Active chronic gastritis | 16 (12.5%) | 1 (1.5%) | 15 (25%) | <0.001* |
| Esophageal varices | 4 (3.1%) | 0 | 4 (6.7%) | 0.046# |
| Ulcerous lesion | ||||
| Antral ulcer | 10 (7.8%) | 7 (10.3%) | 3 (5%) | 0.334# |
| Duodenal aphthous ulcer | 1 (0.8%) | 0 | 1 (1.7%) | 0.469# |
| Pyloric diverticulum | 0 | 0 | 0 | – |
Data are expressed as n%.
Chi-square test;
Fisher’s exact chi-square test.
Figure 1.
Esophagitis, chronic gastritis, and H. pylori rates determined according to the stages of chronic kidney disease.
Histopathological findings obtained from biopsy samples are shown in Table 3 and Figures 2–4. The groups had similar rates of intestinal metaplasia and oedema-congestion, atrophic metaplastic gastritis, fundic and hyperplastic polyps, and chronic gastritis. The incidence of inflammation in the CKD group was significantly higher than in the non-CKD group (48.3% vs 20.6%, P=0.008). The incidence of HP in the CKD group was significantly lower than in the non-CKD group (23.5% vs 59.1%, P<0.001). Dysplasia was not detected in either group.
Table 3.
Comparison of pathological findings in groups.
| Variables n (%) | Total (n: 128) | Non-CKD group (n: 68) | CKD group (n: 60) | P value |
|---|---|---|---|---|
| İntestinal metaplasia | 10 (10.6%) | 5 (14.7%) | 5 (8.3%) | 0.488* |
| Edema-congestion | 7 (7.4%) | 1 (2.9%) | 6 (10%) | 0.416* |
| Inflammation | 36 (38.3%) | 7 (20.6%) | 29 (48.3%) | 0.008# |
| Helicobacter pylori | 51 (43.6%) | 39 (59.1%) | 12 (23.5%) | <0.001# |
| Atrophy metaplastic gastritis | 2 (2.1%) | 0 | 2 (3.3%) | 0.533* |
| Fundic polyp | 3 (3.2%) | 1 (2.9%) | 2 (3.3%) | >0.99* |
| Hyperplastic polyp | 5 (5.3%) | 1 (2.9%) | 4 (6.7%) | 0.650* |
| Chronic gastritis | 54 (42.2%) | 28 (41.2%) | 26 (43.3%) | 0.805# |
| Dysplasia | 0 | 0 | 0 | – |
Data are expressed as n%.
Fisher’s exact chi-square test;
chi-square test.
Figure 2.
Stomach pathology stained with hematoxylin-eosin (H&E), Chronic gastritis; Marked inflammatory cell infiltration in the lamina propria. Possible glandular changes and lymphoid cell clusters.
Figure 3.
Stomach pathology stained with hematoxylin-eosin (H&E). Chronic active gastritis is usually seen in patients with Helicobacter pylori infection. Lymphocytic inflammation and neutrophilic epithelium infiltration.
Figure 4.
Stomach pathology stained with hematoxylin-eosin (H&E). Erythematous gastritis, mucosal structure, glandular structures on the upper left. In the lamina propria, clusters of red erythrocytes are evident on the left side.
Multivariate logistic regression analysis determined independent risk factors affecting the development of endoscopic gastritis, duodenitis, pathological chronic gastritis, and HP. The logistic regression models obtained in the last stage of the analysis were found to be significant, and the data set was found to be compatible with the models. The variables included in the regression analysis models were determined for each dependent variable. For the presence of endoscopic gastritis: pathological chronic gastritis, HP positivity, hypertension, triglyceride, LDL and HDL cholesterol (Model χ2=11.5, P=0.009; Hosmer-Lemeshow test P=0.903). For the presence of endoscopic duodenitis: age, sodium, hemoglobin, calcium and lipase (Model χ2=5.31, P=0.049; Hosmer-Lemeshow test P=0.724). For the presence of pathological chronic gastritis: sex, antral ulcer, bulbar ulcer, duodenal aphthous ulcer, endoscopic gastritis, urea, sodium, total protein, albumin, LDL cholesterol, ferritin, and phosphorus (Model χ2=12.22, P=0.007; Hosmer-Lemeshow test P>0.99). For HP positivity: endoscopic gastritis, erosive gastritis, urea, total and LDL cholesterol, ferritin, calcium, and gamma-glutamyl transferase (GGT) (Model χ2=12.51, P=0.002; Hosmer-Lemeshow test P=0.632). In multivariate analysis, only gastritis (P=0.028) and calcium (P=0.008) were associated with HP positivity. The variables included in the models created in the last step of the multivariate logistic regression analysis are shown in Table 4.
Table 4.
Multivariable logistic regression analysis of independent risk factors affecting the development of endoscopic gastritis and duodenitis and pathological chronic gastritis and HP positivity.
| Wald | P value | Odds ratio | 95% CI lower-upper | |
|---|---|---|---|---|
| Gastritis | ||||
| Triglyceride | 2.54 | 0.111 | 1.03 | 0.99–1.07 |
| Duodenitis | ||||
| Calcium | 3.47 | 0.063 | 0.58 | 0.33–1.03 |
| Chronic gastritis | ||||
| Gastritis (presence) | 2.16 | 0.998 | 0.85 | 0.71–0.96 |
| HP positivity | ||||
| Gastritis (presence) | 4.83 | 0.028 | 4.19 | 1.17–15.05 |
| Calcium | 7.08 | 0.008 | 3.54 | 1.39–8.98 |
HP – Helicobacter pylori; CI – confidence interval.
Discussion
Upper-gastrointestinal system disorders are common in CKD patients due to high ammonium levels, systemic and local circulatory disorders, frequent drug use, and hypergastrinemia [5]. However, in most patients, symptom severity does not correlate with severity of gastroduodenal lesions as assessed by endoscopy, and most patients have mild symptoms [6]. In our previous study of patients receiving hemodialysis (HD) or peritoneal dialysis (PD) maintenance therapy for end-stage renal disease, most did not have any significant upper-gastrointestinal symptoms despite the high rate of gastritis in HD (63.6%) and PD (61.3%) patients [7]. In the current study, antral gastritis, erythematous gastritis, erosive pangastritis, and active chronic gastritis were found to be significantly higher in our non-dialysis uremic patients with Stage 3b and Stage 4 CKD, while the rates of esophageal varicose veins, esophagitis, and bulbitis were higher in the non-uremic control group. Lower albumin, total cholesterol, and LDL and HDL levels are seen in addition to anemia in many patients, often due to infection, inflammation, nutritional deficiency, or erythropoietin deficiency.
In different studies conducted in chronic HD patients, erosive esophagitis 30.2%, gastroesophageal reflux 10%, esophagitis 5.8%, exanthematous pangastritis 57.3%, diffuse antral erythema 27.8%, gastric erosion 5.8%, gastric antral erosion 22.8%, gastric intestinal metaplasia 8.3%, gastritis and duodenitis 42%, duodenal erosion 18–32%, peptic ulcer 7.3%, gastric ulcer 7–14%, duodenal ulcer 7.3–18%, angiodysplasia 4.4%, and gastric polyp were observed at rates of 1.5% [5,8–11]. In our previous study of dialysis patients, we found gastroesophageal reflux in 41.5%, chronic gastritis in 75.5%, non-specific gastritis in 24.5%, intestinal metaplasia in 17%, atrophy in 15.1%, HP in 28.3%, and hyperplastic polyp in 3.8% [7]. Gastric dysplasia was not detected in either of our studies. While rates of antral gastritis, erythematous gastritis, erosive pangastritis, active chronic gastritis, and esophageal varicose veins were detected at lower rates in the CKD group, esophagitis and bulbitis rates were significantly higher in the non-CKD-group.
The frequency of ulcerous lesions was similar in both groups. The frequency of ulcerative lesions in the general population is 10–20% [12]. A retrospective study of dialysis patients found 31.8% had peptic ulcers, and age, low albumin, high GGT, peritoneal dialysis, and diabetes were reported as risk factors [13]. In the present study, intestinal metaplasia was detected in 8.3%, edema-congestion in 10%, inflammation in 48.3%, HP in 23.5%, atrophy metaplastic gastritis in 3.3%, fundus polyp in 3.3%, hyperplastic polyp in 6.7%, and chronic gastritis in 43.3%. The rates in the control group were 14.7% for intestinal metaplasia, 2.9% for edema-congestion, 20.6% for inflammation, 59.1% for HP, 2.9% for fundus polyp, 2.9% for hyperplastic polyp, and 41.2% for chronic gastritis. Inflammation was significantly higher in the CKD group than in the control group. However, although this rate in dialysis patients is reported to be as high as 75.5% in the literature, the frequency of chronic gastritis that we found to be higher in the CKD group in our study did not reach statistical significance [7].
HP was more common in the control group than in the CKD group (59.1% vs 23.5%). While the prevalence of HP is 24–32% in the general population, it was found to be 28.3% in dialysis patients [7,12]. In the present study, the rate of chronic gastritis was 41.2% in the non-uremic patient group with high HP and 43.3% in the CKD group. In a previous study of hemodialysis patients, the prevalence of H. pylori infection decreased as dialysis periods progressed within the first 4-year follow-up after the start of HD [14]. Possible protective mechanisms include antibiotic use or antiacid drugs causing hypochlorhydria, which could contribute to the decreased frequency of HP. Our study’s HP prevalence was 23.5%, less than in the non-CKD population. Also, uremia has a deteriorating effect on glycolipids and external membrane proteins resistant to the external environment, including the lipopolysaccharide cell wall structure of HP colonizing in the gastric mucosa. Our patients with CKD had a higher rate of chronic gastritis despite a lower HP rate, but we did not detect a relationship between HP and chronic gastritis. In multivariate regression analysis, only the presence of gastritis and serum calcium level were associated with HP positivity.
The rates of esophagitis (13.2%) and duodenitis (18.9%) in chronic dialysis patients in our previous study were close to the rates in the current study (13.3%) [7]. In the non-uremic patient group, the rate of esophagitis was higher (53.7%). In studies conducted in HD patients, gastroesophageal reflux was found in 10%, 15% in our patients, and 6% in the control group [5,9,10], while pangastritis was high in HD patients (57.3%), and this rate was lower in our patients (13.3%). Pangastritis is very common in HD patients. While antral erosive gastritis was found in 27.8% of HD patients, this rate was lower (6.7%) in our non-dialysis CKD patients. Antral gastritis, erythematous gastritis, erosive pangastritis, active chronic gastritis, and inflammation were significantly higher in our non-dialysis CKD patients than in the control group. Many drugs used for complications such as high serum urea level, inflammation, stress, mineral bone disorder, anemia, and hypertension in patients with CKD may be effective in this condition, together with uremic toxins [13,15].
A recent study found that gastrointestinal symptoms and signs were common in patients with CKD. Some symptoms and diseases also varied according to whether the renal replacement was peritoneal or hemodialysis type. The prevalence of esophagitis and gastritis diagnosed by symptomatic evaluation varied depending on the type of dialysis and whether it occurred in the pre-dialysis period. Although our study differed from this one in that it included endoscopic diagnostic classification of symptomatic pre-dialysis patients compared to non-uremic patients, the significant difference in the frequency of esophagitis and gastritis histologic subtypes between the groups is compatible with the above study [16].
In our study, no statistically significant independent relationships were detected between hemoglobin, urea, and total cholesterol and the presence of duodenitis, chronic gastritis, and HP in multivariate logistic regression analysis. Our previous study of dialysis patients showed the independent effect of HP and total cholesterol [7].
Conclusions
In uremic patients, risk factors like urea-related toxins, impairment of local and systemic circulations, and hypergastrinemia cause damage to the gastric mucosa. In addition, in chronic uremic patients with cardiovascular damage, anemia and mineral bone disease are frequently seen. These complications and the medications administered to treat them can adversely affect the upper-gastrointestinal system. In the general population, chronic gastritis, inflammation, and gastric and duodenal ulcers are seen frequently. These diseases generally cause symptoms such as vomiting, anorexia, abdominal pain, heartburn, and bleeding. Although most chronic uremic patients have these lesions, they remain asymptomatic.
Even though most chronic uremic patients have these lesions since they remain asymptomatic so, their diagnosis and treatment are often delayed; therefore, the lesions that arise in the gastrointestinal system among pre-dialysis uremic patients should be treated early, bearing in mind that they are potential candidates for kidney transplantation. Adverse effects on the gastrointestinal system of the drugs used, especially in uremic patients, should be minimized.
Footnotes
Conflict of interest: None declared
Publisher’s note: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher
Declaration of Figures’ Authenticity: All figures submitted have been created by the authors, who confirm that the images are original with no duplication and have not been previously published in whole or in part.
Financial support: None declared
References
- 1.KDIGO 2012 Clinic practice guideline for the evaluation and management of chronic kidney disease. Kidney Int Suppl. 2013;3:136. doi: 10.1038/ki.2013.243. [DOI] [PubMed] [Google Scholar]
- 2.Strid H, Simrén M, Johansson AC, et al. The prevalence of gastrointestinal symptoms in patients with chronic renal failure is increased and associated with impaired psychological general well-being. Nephrol Dial Transplant. 2002;17(8):1434–39. doi: 10.1093/ndt/17.8.1434. [DOI] [PubMed] [Google Scholar]
- 3.Leja M, Grinberga-Derica I, Bilgilier C, Steininger C. Review: Epidemiology of Helicobacter pylori infection. Helicobacter. 2019;24(Suppl 1):e12635. doi: 10.1111/hel.12635. [DOI] [PubMed] [Google Scholar]
- 4.Zhou F, Zhong X, Chen J, et al. Helicobacter pylori infection associated with type 2 diabetic nephropathy in patients with dyspeptic symptoms. Diabetes Res Clin Pract. 2015;110(3):328–34. doi: 10.1016/j.diabres.2015.09.008. [DOI] [PubMed] [Google Scholar]
- 5.Wijarnpreecha K, Thongprayoon C, Nissaisorakarn P, et al. Association between Helicobacter pylori and end-stage renal disease: A meta-analysis. World J Gastroenterol. 2017;23(8):1497–506. doi: 10.3748/wjg.v23.i8.1497. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Sotoudehmanesh R, Ali Asgari A, Ansari R, Nouraie M. Endoscopic findings in end-stage renal disease. Endoscopy. 2003;35(6):502–5. doi: 10.1055/s-2003-39672. [DOI] [PubMed] [Google Scholar]
- 7.Usta M, Ersoy A, Ayar Y, et al. Comparison of endoscopic and pathological findings of the upper gastrointestinal tract in transplant candidate patients undergoing hemodialysis or peritoneal dialysis treatment: A review of literature. BMC Nephrol. 2020;21(1):444. doi: 10.1186/s12882-020-02108-w. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Bunchorntavakul C, Atsawarungruangkit A. Prevalence of asymptomatic gastroduodenal lesions and Helicobacter pylori infection in kidney transplant candidates. J Med Assoc Thai. 2014;97(Suppl 11):S62–68. [PubMed] [Google Scholar]
- 10.Homse Netto JP, Pinheiro JPS, Ferrari ML, et al. Upper gastrointestinal alterations in kidney transplant candidates. J Bras Nefrol. 2018;40(3):266–72. doi: 10.1590/2175-8239-JBN-3829. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Karari EM, Lule GN, McLigeyo SO, Amayo EO. Endoscopic findings and the prevalence of Helicobacter pylori in chronic renal failure patients with dyspepsia. East Afr Med J. 2000;77(8):406–9. [PubMed] [Google Scholar]
- 12.Moriyama T, Matsumoto T, Hirakawa K, 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. doi: 10.1007/s00535-009-0196-6. [DOI] [PubMed] [Google Scholar]
- 13.Kim M, Kim CS, Bae EH, et al. Risk factors for peptic ulcer disease in patients with end-stage renal disease receiving dialysis. Kidney Res Clin Pract. 2019;38(1):81–89. doi: 10.23876/j.krcp.18.0060. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Huang C, Chen Q, Jiang J, et al. Gastric metaplasia and Helicobacter pylori infection in hemodialysis patients. Ren Fail. 2012;34(4):420–24. doi: 10.3109/0886022X.2011.649659. [DOI] [PubMed] [Google Scholar]
- 15.Zhang X, Bansal N, Go AS, Hsu CY. Gastrointestinal symptoms, inflammation and hypoalbuminemia in chronic kidney disease patients: A cross-sectional study. BMC Nephrol. 2015;16:211. doi: 10.1186/s12882-015-0209-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Karahan D, Şahin İ. Comparison of gastrointestinal symptoms and findings in renal replacement therapy modalities. BMC Nephrol. 2022;23(1):261. doi: 10.1186/s12882-022-02893-6. [DOI] [PMC free article] [PubMed] [Google Scholar]