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Saudi Journal of Kidney Diseases and Transplantation
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Year : 2020  |  Volume : 31  |  Issue : 2  |  Page : 388-394
Endoscopic findings in hemodialysis patients upon workup for kidney transplantation

1 Department of Internal Medicine; Shiraz Nephro-Urology Research Center, Shiraz University of Medical Sciences, Shiraz, Iran
2 Shiraz Nephro-Urology Research Center, Shiraz University of Medical Sciences, Shiraz, Iran
3 Department of Internal Medicine; Gastroenterohepatology Research Center, Shiraz University of Medical Sciences, Shiraz, Iran

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Date of Submission17-Oct-2018
Date of Decision01-Dec-2018
Date of Acceptance03-Dec-2018
Date of Web Publication09-May-2020


Upper gastrointestinal (GI) abnormality is believed to be higher in patients with end-stage renal disease (ESRD) which can make a big trouble for whom undergo kidney transplant. We conducted this study to assess upper GI findings of patients with ESRD. In the present retrospective study we recorded upper GI endoscopy results in hemodialysis patients who were candidate for renal transplantation during a 10-year period. We reviewed files of 1256 patients with a mean age of 37.6 ± 13.4 years. Half of patients (50.6%) had an abnormal endoscopy. Two most common abnormalities were mild gastritis (35.6%) and gastro-esophageal reflux disease (16.7%). GI ulcers were observed in 11% of patients. Duodenal ulcer was the most common ulcer which was seen in 6.8% of patients. Helicobacter pylori was positive in 32.9% of patients and correlated with GI lesions (P = 0.000, r = 0.371). Longer dialysis duration and older patients revealed more upper GI abnormality (P = 0 .032, <0.001). As long as more than half of our patients have at least one upper GI involvement, we recommended that endoscopy must be done as a pretransplantation evaluation for patients without symptoms who have risk factors for ulcers.

How to cite this article:
Pakfetrat M, Malekmakan L, Roozbeh J, Tadayon T, Moini M, Goodarzian M. Endoscopic findings in hemodialysis patients upon workup for kidney transplantation. Saudi J Kidney Dis Transpl 2020;31:388-94

How to cite this URL:
Pakfetrat M, Malekmakan L, Roozbeh J, Tadayon T, Moini M, Goodarzian M. Endoscopic findings in hemodialysis patients upon workup for kidney transplantation. Saudi J Kidney Dis Transpl [serial online] 2020 [cited 2022 Nov 26];31:388-94. Available from: https://www.sjkdt.org/text.asp?2020/31/2/388/284013

   Introduction Top

Renal transplant is the best treatment for patients with end-stage renal disease (ESRD).[12] The annual incidence of renal transplantation in 2005 was reported 66,000.[3] The average cost spends in the 1st year after transplantation is $87,400/ Annually, 4.4% of kidney transplants end up with failure.[1] Graft loss imposes a great economical and psychological burden to patients, their family and community.[1] Gastrointestinal (GI) diseases such as peptic ulcer perforation and hemorrhage are one of the situations that lead to transplant failure.[45]

The prevalence of upper GI disease in chronic renal failure (CRF) patients is controversial. Some studies reported that all CRF patients suffered from upper GI disease while some studies mentioned no difference between these patients and normal population.[6] Previous reports also mentioned that the prevalence of upper GI complications especially ulcers is increasing among patients with renal transplantation mainly due to stressful condition and immunosuppressant drugs consumption.[4],[5] GI complications may result in graft loss and even death.[4],[7],[8] As long as abnormal endoscopy findings do not correlate with upper GI complaints, many centers consider endoscopy for all patients who want to go under transplant. In addition, there some literature recommended that upper digestive endoscopies might be beneficial to kidney transplant candidates, regardless of symptomatology presented.[9]

We conducted this study to assess the endoscopies results for ESRD patients who were on hemodialysis (HD) and to find out the most common disease that involves upper GI tract of them. Furthermore, we aimed to find out the relation between baseline characteristics and Helicobater pylori (H. pylori) infection with developing upper GI disease specifically ulcers.

   Material and Methods Top


In the present retrospective cross-sectional study, we evaluated the endoscopic findings of ESRD patients who were on HD and candidate for renal transplant in hospitals affiliated to Shiraz University of Medical Sciences during a 10-year period. We included all patients of either gender with the age range from 18 to 70 years who were on HD for ≥3 months with a frequency of two times or more in a week.

Data collection

We prepared a data gathering sheet containing sex, CRF causes and duration, dialysis duration, hepatitis B surface (HBS) antigen (Ag), hepatitis C virus (HCV) antibody (Ab), and polymerase chain reaction, upper GI endoscopy findings and the presence of H. pylori. All data had been documented in each patient’s folder in hospital. We referred to archives of hospital and extracted data from patients’ folders and recorded them in our preformed gathering sheet. We called each patient and after informing them completely, we obtained the verbal consent. We asked them to come over to answer the missing data and also to fulfill the informed consent.

Ethical consideration

The present study was approved by Ethics Committee of Shiraz University of Medical Sciences. Verbal and written informed consent was obtained from patients.

   Statistical Analysis Top

Data were analyzed using the Statistical Package for the Social Sciences (SPSS) for Windows version 18.0 (SPSS Inc., Chicago, Ill, USA). Quantitative data represented by mean and standard deviation. Chi-square was used to assess the relation of two qualitative data and Independent t-test was used to evaluate the correlation of a quantitative data with qualitative data. P <0.05 was considered statistically significant.

   Results Top

Totally, we gathered 1303 patients that after omission based on exclusion criteria and missing data 1256 patients remained. Men were dominant gender in our study. They were 804 (64.1%) of our patients. The mean age of our patients was 37.6 ± 13.4 years. On average, our patients had developed CRF 38.0 ± 38.9 months before our study and they were on dialysis 17.9 ± 20.8 months before the study. The most common underlying disease that leading to CRF was hypertension that was seen in 393 (31.3%) patients, followed by glomerulonephritis seen in 244 (19.4%) patients and diabetes mellitus (DM) seen in 156 (12.4%).cases of patients Totally, 1% of our studied patients (12 cases) was HCV Ab positive and 17 cases (1.4%) was HBS Ag positive. [Table 1] shows the baseline characteristics and their correlation with abnormal endoscopy findings and also upper GI ulcers which revealed there were no relation between gender, CRF duration, HCV and HBS positivity, and abnormal endoscopy. We found that patients with older age and longer dialysis duration, showed more abnormal endoscopy (P <0.001, 0.032). The only underlying disease that correlated with abnormal endoscopy was DM (P = 0.001). Totally, 66 (10.4%) of patients with abnormal endoscopy had DM.
Table 1: Baseline characteristics and their correlation with abnormal endoscopy.

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Endoscopy was abnormal in 636 (50.6%) of our patients. The most common abnormality in our patients’ endoscopy was mild gastritis which was seen in 445 cases (35.6%) of our patients following by gastro esophageal reflux disease (GERD) and stomach erosion found in 211 cases (16.7%) and 193 cases (15.5%) of patients. Duodenal ulcer was the most common ulcer which seen in 85 cases (6.8%), while gastric ulcer and esophageal ulcer was seen in 28 cases (2.2%) and 25 cases (2.0%). Endoscopy findings were shown in detail in [Table 2].
Table 2: Gastrointestinal endoscopy findings among our studied population.

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In general, H. pylori was positive in 384 (32.9%) of our patients, while it was positive in more than half of patients with ulcer [Table 3]. It was positive in 30 (52%) of patients with esophageal ulcer, 18 (64.3%) of patients with gastric and 56 (65.9%) of duodenal ulcer. There was a significant correlation between positive H. pylori and esophageal, gastric, and duodenal ulcer (P = 0.023, P <0.001, P <0.001, respectively). We found no relation between dialysis duration and positive H. pylori (P =0.418).
Table 3: H. pylori presence and correlation with gastrointestinal ulcers in our studied group.

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   Discussion Top

Nowadays, chronic diseases such as CRF become a global problem.[10] Annually, $32.9 billion spent on ESRD.[11] Transplantation is the final treatment for ESRD patients. Transplant failure has disastrous psychological and economic consequences on patients, their family and also public health. Upper GI disorder could be one of the causes of this failure.

Previous studies mentioned that patients with abnormal renal function were at a higher risk of upper GI mucosal damage.[12],[13] The patho- physiology is multifaceted including use high- dose corticosteroid and immunosuppressant therapy and metabolic alterations arising from CKD (increased gastrin and ammonia serum levels, gastroesophageal reflux disease, and infection by H. pylori).[14] Some theories were suggested to explain the higher prevalence of upper GI disease in CRF patients. One theory mentioned the role of kidney in gastrin break down while in CRF gastrin increases due to kidney malfunction and results in hyper acid secretion. Although there is some controversy on gastric acid secretion in patients with azotemia while some studies reported normal or decreased gastric acid in CRF patients. Watanabe et al related these controversies to H. pylori bacteria. They reported that in normal population H. pylori do not change the gastric acid level, but in patients with CRF, it may decrease the gastric acid due to higher ammonia production and also gastric atrophy.[15] Due to abnormal endoscopy results do not associate with upper GI complaints, many centers such as our center consider endoscopy for all patients who candidate to renal transplant. Similarly, there are some recommendation for upper GI endoscopies in HD patients who were transplant candidates, regardless of symptomatology presented.[9] In this regard, we conducted the present study to evaluate the upper GI tract in patients who were waiting for transplantation.

Approximately half of our patients revealed abnormality in their endoscopy. Different studies reported a variety of prevalence for abnormal endoscopy findings in ESRD patients. These differences might be due to differences in diagnostic tools, diets, most common underlying diseases, etc. Al-Mueilo reported that 90.7% of patients had abnormal mucosa, while Kang et al found macroscopic abnormal mucosa in 57% of their patients.[1617] Emir et al who conducted a study on 37 children with ESRD revealed that 46% of them had abnormal endoscopic findings.[18] Same as our result, previous studies revealed that non ulcer mucosal lesions occurred more than ulcer diseases in ESRD patients.[16171920] The most common abnormal finding among our patients was mild gastritis and GERD which were seen in 35.6% and 16.4% of our patients. Al-Mueilo found GERD in only 3.7% of patients while Kawaguchi et al who evaluated GERD in CRF patients mentioned a higher prevalence of GERD especially in HD patients (34% in CRF and 44% in HD).[21] Another study from the south of Iran that conducted on normal population revealed GERD in 58.5% of patients, although they did not perform endoscopy and their diagnosis was only based on clinical symptoms.[22] The previous study mentioned high blood urea as a risk factor for H. pylori infection and upper GI lesion.[12] On the other hand, Jaspersen et al who assessed the prevalence of H. pylori in different stages of renal failure reported lower prevalence of H. pylori in renal dysfunction and they concluded that uremia can protected patients against H. pylori.[23] Another study conducted by Cekin also supported this conclusion.[24]

H. pylorus was positive in one-third of our patients. We found no relation between dialysis duration and the presence of H. pylori; though shorter dialysis duration was correlated with abnormal endoscopy. In spite of our result, previous studies mentioned that longer dialysis duration leads to decrease in H. pylori infection.[1325] Sugimoto et al reported that although the prevalence of H. pylori infection decreased with longer dialysis, still patients represented a specific gastro duodenal abnor- mality.[13] Same as our results, previous studies revealed relation between H. pylori presence and development of upper GI abnormality.[4],[5]

Candida albicans is a flora of the GI tract, but it is also a potential pathogen and cause of systemic infection in some patients such as HD patients.[26] We found 0.3% Candida in upper GI endoscopy among our studied population.

Spinelli et al, also reported less common upper GI tract cancer in their CRF patients. It seems that the most common neoplasms among CRF are mesenchymal ones, while after transplant epithelial and lymphoproliferative ones. It is still discussed the role of CRF in the onset of tumors.[27] Esophageal tumors was found in 0.2% of our patients. Dhar et al reported that 1.5% of their endoscopic findings in their renal patients was upper GI malignancy.[28]

Among underlying diseases only, we found correlation between abnormal findings of endoscopy and DM. This is probably due to the effect of DM on GI motility.[29] Furthermore, same as previous studies, we found that older patients developed upper GI abnormality more.[22] The correlation of gender and upper GI abnormality is controversial in literature. Khodamoradi et al reported female gender as a risk factor of GERD, while three and his colleagues who assessed 206 ESRD patients mentioned male gender as a risk factor for upper GI lesion.[4],[22] We found no correlation between sex and GI abnormality.

   Conclusion Top

Based on this study, more than half of ESRD patients have at least one upper GI involvement. Although the prevalence of ulcer diseases is less than nonulcer diseases and the most inconvenient involvement after trans-plantation is ulcers, there is no relation between upper GI complaints and endoscopic findings. As a result, endoscopy must be considered also for patients without symptoms at least for patients who have risk factors for ulcers. There should be more studies to determine the prevalence and incidence of upper GI complications before and after transplantation and risk factors that can increase upper GI involvements, especially ulcers in patients with ESRD, and hence, centers able to consider endoscopy for the right patient.

   Acknowledgment Top

The Vice-Chancellery of Research and Technology of Shiraz University of Medical Sciences financially supported this study. This article is based on a thesis written by Maryam Goodarzian and supported financially by Shiraz University of Medical Sciences with Grant No 6889. The authors declare that they have no conflict of interest

Conflict of interest: None declared.

   References Top

Yen EF, Hardinger K, Brennan DC, Woodward RS, Desai NM, Crippin JS, et al. Cost-effectiveness of extending Medicare coverage of immunosuppressive medications to the life of a kidney transplant. Am J Transplant 2004;4:1703-8  Back to cited text no. 1
Vanholder R, Lameire N, Annemans L, van Biesen W. Cost of renal replacement: How to help as many as possible while keeping expenses reasonable? Nephrol Dial Transplant 2016;31:1251-61  Back to cited text no. 2
Shimazono Y. The state of the international organ trade: A provisional picture based on integration of available information. Bull World Health Organ 2007;85:955-62  Back to cited text no. 3
Sotoudehmanesh R, Ali Asgari A, Ansari R, Nouraie M. Endoscopic findings in end-stage renal disease. Endoscopy 2003;35:502-5  Back to cited text no. 4
Wee A, Kang JY, Ho MS, Choong HL, Wu AY, Sutherland IH. Gastroduodenal mucosa in uraemia: Endoscopic and histological correlation and prevalence of helicobacter-like organisms. Gut 1990;31:1093-6  Back to cited text no. 5
Nardone G, Rocco A, Fiorillo M, et al. Gastro- duodenal lesions and Helicobacter pylori infection in dyspeptic patients with and without chronic renal failure. Helicobacter 2005;10:53- 8  Back to cited text no. 6
Ponticelli C, Passerini P. Gastrointestinal complications in renal transplant recipients. Transpl Int 2005;18:643-50  Back to cited text no. 7
Helderman JH, Goral S. Gastrointestinal complications of transplant immunosuppression. J Am Soc Nephrol 2002;13:277-87  Back to cited text no. 8
Homse Netto JP, Pinheiro JP, Ferrari ML, et al. Upper gastrointestinal alterations in kidney transplant candidates. J Bras Nefrol 2018;40: 266-72  Back to cited text no. 9
Perico N, Remuzzi G. Chronic kidney disease: A research and public health priority. Nephrol Dial Transplant 2012;27 Suppl 3:iii19-26  Back to cited text no. 10
Hoerger TJ, Simpson SA, Yarnoff BO, et al. The future burden of CKD in the United States: A simulation model for the CDC CKD Initiative. Am J Kidney Dis 2015;65:403-11  Back to cited text no. 11
Khedmat H, Ahmadzad-Asl M, Amini M, et al. Gastro-duodenal lesions and Helicobacter pylori infection in uremic patients and renal transplant recipients. Transplant Proc 2007;39: 1003-7  Back to cited text no. 12
Sugimoto M, Sakai K, Kita M, Imanishi J, Yamaoka Y. Prevalence of Helicobacter pylori infection in long-term hemodialysis patients. Kidney Int 2009;75:96-103  Back to cited text no. 13
Homse Netto JP, Pinheiro JPS, Ferrari ML, et al. Upper gastrointestinal alterations in kidney transplant candidates. J Bras Nefrol 2018;40: 266-72  Back to cited text no. 14
Watanabe H, Hiraishi H, Ishida M, Kazama JJ, Terano A. Pathophysiology of gastric acid secretion in patients with chronic renal failure: Influence of Helicobacter pylori infection. J Intern Med 2003;254:439-46  Back to cited text no. 15
Kang JY, Wu AY, Sutherland IH, Vathsala A. Prevalence of peptic ulcer in patients undergoing maintenance hemodialysis. Dig Dis Sci 1988;33:774-8  Back to cited text no. 16
Al-Mueilo SH. Gastroduodenal lesions and Helicobacter pylori infection in hemodialysis patients. Saudi Med J 2004;25:1010-4  Back to cited text no. 17
Emir S, Bereket G, Boyacioglu S, Varan B, Tunali H, Haberal M. Gastroduodenal lesions and Helicobacter pylori in children with end- stage renal disease. Pediatr Nephrol 2000;14: 837-40  Back to cited text no. 18
Hwang JS, Kang YW, Park SB, Her JW, Ahn SH, Park SK. Upper gastrointestinal endos- copic findings in chronic renal failure patients. Korean J Gastrointest Endosc 1992;12:215-20  Back to cited text no. 19
Margolis DM, Saylor JL, Geisse G, DeSchryver- Kecskemeti K, Harter HR, Zuckerman GR. Upper gastrointestinal disease in chronic renal failure. A prospective evaluation. Arch Intern Med 1978;138:1214-7  Back to cited text no. 20
Kawaguchi Y, Mine T, Kawana I, et al. Gastroesophageal reflux disease in chronic renal failure patients: Evaluation by endos- copic examination. Tokai J Exp Clin Med 2009;34:80-3  Back to cited text no. 21
Khodamoradi Z, Gandomkar A, Poustchi H, et al. Prevalence and correlates of gastro- esophageal reflux disease in Southern Iran: Pars cohort study. Middle East J Dig Dis 2017;9:129-38  Back to cited text no. 22
Jaspersen D, Fassbinder W, Heinkele P, Kronsbein H, Schorr W, Raschka C, et al. Significantly lower prevalence of Helicobacter pylori in uremic patients than in patients with normal renal function. J Gastroenterol 1995; 30:585-8  Back to cited text no. 23
Cekin AH, Boyacioglu S, Gursoy M, et al. Gastroesophageal reflux disease in chronic renal failure patients with upper GI symptoms: Multivariate analysis of pathogenetic factors. Am J Gastroenterol 2002;97:1352-6  Back to cited text no. 24
Nakajima F, Sakaguchi M, Amemoto K, et al. Helicobacter pylori in patients receiving long- term dialysis. Am J Nephrol 2002;22:468-72  Back to cited text no. 25
Wiesner SM, Jechorek RP, Garni RM, Bendel CM, Wells CL. Gastrointestinal colonization by Candida albicans mutant strains in antibiotic-treated mice. Clin Diagn Lab Immunol 2001;8:192-5  Back to cited text no. 26
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Dhar A, Pattni S, Westaby D, Vlavianos P. Endoscopic findings in renal patients: Diagnostic yield by indication for gastroscopy and colonoscopy. Gastrointestinal Endoscopy 2009;69:AB318  Back to cited text no. 28
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Correspondence Address:
Leila Malekmakan
Shiraz Nephro-Urology Research Center, Shiraz University of Medical Sciences, Shiraz
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/1319-2442.284013

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