Significance of serum pepsinogens and their relationship to Helicobacter pylori infection and histological gastritis in dialysis patients

Hideo Araki1,2, Ryoichi Miyazaki2, Tetsuhisa Matsuda2, Fumitake Gejyo3 and Ichiro Koni1

1 Second Department of Internal Medicine, School of Medicine, Kanazawa University, Kanazawa, 2 Department of Internal Medicine, Fujita Memorial Hospital, Fukui and 3 Department of Clinical and Laboratory Medicine, Fukui Medical University, Fukui, Japan

Correspondence and offprint requests to: Hideo Araki, MD, Second Department of Internal Medicine, School of Medicine, Kanazawa University, Takara-machi 13–1, Kanazawa, 920–8640, Japan.



   Abstract
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Background. Previous investigations reported that patients undergoing dialysis therapy had significantly higher serum pepsinogen (PG) levels than patients with normal renal function. However, in dialysis patients, the relationship between serum PG levels and Helicobacter pylori infection remains unknown.

Methods. Sixty three maintenance dialysis patients (54 haemodialysis and nine continuous ambulatory peritoneal dialysis) who required endoscopic examination were enrolled in the study. Sixty four age- and sex-matched patients with normal renal function served as controls. We performed endoscopic examination and obtained both the gastric antral and corpus mucosa for histopathological evaluation and H. pylori identification. Twenty three patients on dialysis underwent H. pylori eradication therapy.

Results. In dialysis patients, H. pylori-positives had significantly higher serum PG II levels than H. pylori-negatives (26.6±21.5 vs 14.1±7.1 ng/ml, P<0.05), but no significant difference was found in serum PG I between H. pylori-positives and H. pylori-negatives (228.8±158.5 vs 179.4±113.5 ng/ml). There was no significant difference in serum PG II between dialysis patients and controls (19.9±16.5 vs 18.6±14.9 ng/ml), while serum PG I levels were significantly higher in dialysis patients than in controls (201.7±136.8 vs 77.6±85.8 ng/ml, P<0.05). Serum PG II levels, but not those of PG I, significantly correlated with the inflammation and activity scores of antrum in dialysis patients, and these scores were highly influenced by H. pylori infection. Dialysis patients in whom H. pylori was eradicated successfully showed siginificant reductions of serum PG II levels but not of PG I.

Conclusions. In dialysis patients, high serum levels of PG II, but not PG I, are significantly related to H. pylori infection and mucosal inflammation. A significant decrease in serum PG II levels could be used as a predictor of the eradication of H. pylori infection in dialysis patients.

Keywords: dialysis patients; gastritis; Helicobacter pylori; pepsinogen; Helicobacter pylori eradication



   Introduction
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Gastric symptoms are common in uraemic patients, and gastroduodenal diseases are an important complication in long-term dialysis patients [1]. However, the precise nature of the gastroduodenal involvement in these patients remains unclear. Recently, the link between Helicobacter pylori, chronic gastritis and peptic ulcer disease has grown stronger [2,3]. In general, patients who are positive for H. pylori have significantly higher serum pepsinogen (PG) I and PG II levels and a significantly lower PG I:PG II ratio than patients negative for this organism, with this possibly related to gastric mucosal change [4,5]. On the other hand, previous investigations reported that patients undergoing dialysis therapy had significantly higher serum PG levels than patients with normal renal function [6,7]. However, in dialysis patients, the relationship between serum PG levels and H. pylori infection remains unknown.

Several studies have demonstrated that H. pylori eradication therapy causes a significant reduction in serum PG I and PG II levels in patients with normal renal function [5,8,9]. However, little is known about the changes in serum PG levels when dialysis patients undergo H. pylori eradication therapy.

In the present study, we measured the serum pepsinogen levels in dialysis patients and investigated the effect of H. pylori infection on such serological parameters and histopathological alterations. Furthermore, we studied the effect of H. pylori eradication therapy on serum PG levels in dialysis patients.



   Subjects and methods
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 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Subjects
Sixty three maintenance dialysis patients (40 males and 23 females, age range 33–87 years, mean age 57.4±12.8 (SD) years) who required endoscopic examination for routinely accepted clinical indications from October 1995 to October 1997 were enrolled in this study. Fifty four were haemodialysis (HD) patients and nine were continuous ambulatory peritoneal dialysis (CAPD) patients. The disease underlying end-stage renal failure was chronic glomerulonephritis in 34 cases, diabetes mellitus in 11, benign nephrosclerosis in five, polycystic kidney in four, and others in nine. The mean duration of dialysis therapy was 7.6±5.2 years. Sixty four age- and sex-matched patients (36 males and 28 females, age range 20–88 years, mean age 57.8±17.3 years) with normal renal function referred for endoscopy during the same period served as controls. Consent was obtained from all patients before the procedure. None of the patients examined had ever undergone gastric surgery and none had received antibiotics during the 2 month period preceding the study. Gastric complaints (epigastric pain, nausea, vomiting, etc) were recorded in 41 of the 63 dialysis patients (65.1%) and in 39 of the 64 controls (60.9%).

Pepsinogen I, pepsinogen II and gastrin
Fasting serum PG I and PG II levels were determined by competitive binding double-antibody radioimmunoassay, as described by Ichinose et al. [10]. Serum gastrin levels were determined by radioimmunoassay using a commercial kit (Dinabott Company, Tokyo, Japan).

Helicobacter pylori specific IgG antibodies
We measured H. pylori-specific IgG antibody titres by enzyme-linked immunosorbent assay (ELISA), using a Helico-G kit (Porton Cambridge, Maidenhead, UK), based on the method of Newell et al. [11]. A titre >10 U/ml was interpreted as positive according to the manufacturer's instructions.

Endoscopy
Gastroduodenal endoscopical examinations were performed using a Fujinon EG-300FP endoscope (Fuji Photo Optical Company, Omiya, Japan), and the presence of lesions in the gastroduodenal mucosa was noted. Criteria for ulcer disease included healing ulcers and ulcer scarring. For histological examination, cultivation and for the rapid urease test, specimens from both the antrum and the corpus were collected.

Histological studies
Biopsy specimens for histological examination were fixed in 10% buffered formalin and processed routinely. Paraffin sections were cut and stained with haematoxylin and eosin. Sections were graded for inflammation (chronicity) and polymorphonuclear leukocytes (activity), in accordance with the recommendations of the working party that developed the Sydney system for the histological grading of gastritis [12,13]. Each parameter in the Sydney system was scored from 0 to 3 (0=none, 1=mild, 2=moderate, 3=marked), which is well illustrated in the full description of the classification.

Helicobacter pylori screening
Immediately after endoscopy, the biopsy specimens were transferred to the transport medium, plated onto Modified-belo-horizonte medium pylori agar medium (Nikken Biomedical Laboratories, Kyoto, Japan) and cultured at 35°C under microaerobic conditions. Five or 7 days later, the plates were checked and identification of H. pylori was made on the basis of the morphological features of the colony, Gram's stain and positive reactions to oxidase and urease.

Patients were judged to be infected with H. pylori if the organism was demonstrated in the biopsy by either histology or culture.

Helicobacter pylori eradication therapy
Nineteen patients were treated with a combination of amoxicillin (AMPC), clarithromycin (CAM), omeprazole and polaprezinc, and four subjects received a combination of AMPC, omeprazole and polaprezinc. The details of the former protocol are as follows: 250 mg of AMPC twice a day for 3 weeks, 200 mg of CAM twice a day for 3 weeks, 20 mg of omeprazole once a day for 8 weeks, 0.5 g of polaprezinc twice a day for 24 weeks. The latter protocol was 250 mg of AMPC twice a day for 3 weeks, 20 mg of omeprazole once a day for 8 weeks, 0.5 g of polaprezinc twice a day for 24 weeks. Two months after the beginning of the medical treatment, the patients underwent a second upper gastrointestinal endoscopy with at least three antral and three corpus gastric biopsies, plus repeat testing for fasting serum PG I, PG II, gastrin and H. pylori IgG antibodies. Eradication of H. pylori was defined by negative results on all the tests described above. The eradication was considered a failure if any of the three methods showed positive results for H. pylori.

Statistical methods
Categorical data were assessed by the X2 test. The Mann–Whitney U test was used for non-parametric data analysis as required. The relationship between serum parameters and degree of gastritis was investigated by linear regression analysis using the Spearman's rank correlation test. Wilcoxon's test was used for the paired data. Probability values P<0.05 were considered statistically significant. All data are expressed as mean values±SD.



   Results
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 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
The endoscopic appearance of the gastroduodenal mucosa in dialysis patients was similar to that of controls, as was the incidence of peptic ulcers. Dialysis patients had a significantly lower prevalence of H. pylori infection than control subjects (Table 1Go).


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Table 1. Endoscopic appearance of gastroduodenal mucosa and prevalence of H. pylori in dialysis patients and controls
 
There was no significant difference in serum levels of PG II between dialysis patients and controls, while the former had significantly higher serum levels of PG I and gastrin and a significantly higher PG I:PG II ratio than the latter (Table 2Go). A lower incidence of seropositivity of H. pylori IgG antibodies in dialysis patients was found, the titres of which were significantly lower in dialysis patients than in controls (Table 2Go).


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Table 2. Comparison of clinicopathological parameters between dialysis patients and controls (mean±SD)
 
Both in dialysis patients and in controls, the H. pylori-positive patients had significantly higher serum PG II levels and a significantly lower PG I:PG II ratio than H. pylori-negative patients, while no significant differences were found in serum PG I levels and gastrin between H. pylori-positive and H. pylori-negative patients (Table 3Go). H. pylori-negative patients on dialysis had significantly higher serum PG I and gastrin levels than H. pylori-negative controls. In contrast, the difference in PG II between H. pylori-negative dialysis patients and H. pylori-negative controls, which was statistically significant, was markedly smaller than for PG I and gastrin. The same tendency of these serum parameters could be seen in H. pylori-positive subjects.


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Table 3. Comparison of clinicopathological parameters between H. pylori-positive and negative subjects in both dialysis patients and controls (mean±SD)
 
In the histological study, H. pylori-positive patients had significantly higher inflammation and activity scores than H. pylori-negative patients for both dialysis patients and controls. When all patients were divided into H. pylori-positives and negatives, no significant differences were found between dialysis patients and controls in any Sydney scores (Table 3Go).

We investigated the relationship between serological parameters and histological findings. In control patients, serum PG I and PG II levels showed a significant correlation with antral inflammation and activity scores (Table 4aGo, Fig. 1Go). When patients were divided into H. pylori-positives and negatives, these significant correlations were found only in the former (Table 4aGo).


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Table 4. Correlation between serum PG I and PG II with gastritis of antrum and corpus mucosa
 


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Fig. 1. Relationship between serum PG II levels and inflammation and activity scores in dialysis patients and controls. ({circ}, H. pylori-positive; {blacktriangleup}, H. pylori-negative. The mean values of the PG II levels for each inflammation and activity score are shown as bars.).

 
Although in dialysis patients serum PG II levels showed significant correlations with antral inflammation and activity scores, there was no significant relationship between serum PG I and Sydney scores (Table 4bGo, Fig. 1Go). When dialysis patients were divided into H. pylori-positives and negatives in antral inflammation score, a significant correlation was found only in the former (Table 4bGo).

For serum gastrin levels, significantly higher serum levels were found in dialysis patients than in controls (Table 2Go). There were no significant correlations between serum gastrin and PG levels in either the dialysis patients or controls.

In eradication therapy, 21 dialysis patients completed the treatment protocol; one dropped out 4 days after the initiation of AMPC, CAM, omeprazole and polaprezinc due to diarrhoea, and another patient dropped out from the same protocol due to oral candidiasis 7 days after the beginning of the therapy. The rest of the patients showed no side effects as judged by symptoms and laboratory findings. Helicobacter pylori was eradicated in 15 of 17 patients who were treated with AMPC, CAM, omeprazole and polaprezinc, and in three of four treated with AMPC, omeprazole and polaprezinc.

Dialysis patients in whom H. pylori was successfully eradicated showed significant reductions of serum PG II levels and H. pylori IgG antibodies and significant elevations of their PG I:PG II ratio (Table 5Go). Serum PG I levels and gastrin did not show significant changes after successful H. pylori eradication therapy. In dialysis patients who were still infected with H. pylori after eradication therapy, serum PG II levels increased and H. pylori IgG antibodies did not change (Table 5Go). Elevation of the serum PG I:PG II ratio was also shown in those dialysis patients in whom H. pylori was not eradicated.


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Table 5. Changes in serum PG I, PG II, PG I : PG II ratio and H. pylori IgG antibodies after eradication treatment in dialysis patients
 


   Discussion
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
In this study, we found that high serum levels of PG II are significantly related to H. pylori infection in dialysis patients as well as in controls, while serum levels of PG I are not useful as a diagnostic tool for H. pylori infection in dialysis patients. We also showed that serum PG II levels, but not those of PG I, were useful markers of the histological features of gastritis in dialysis patients. In addition, we showed that eradication of H. pylori resulted in a significant decrease of serum PG II levels, but not of PG I, in patients on dialysis.

Several factors may be involved in the difference between PG I and PG II. One is the different distribution in the stomach of PG I and PG II. PG I is restricted to the corpus mucosa, whereas PG II is present in both the corpus and antral mucosa [14,15]. It has been suggested that H. pylori-associated gastritis is more severe in the antrum than in the corpus mucosa [2,16], possibly accounting for the greater correlation between PG II levels and H. pylori-associated gastritis as compared with PG I which is present to a lesser extent in the antrum. However, our findings as well as those of another investigation that showed similar degrees of inflammation in the antrum and corpus do not support this hypothesis [17]; this matter is still controversial.

A second factor may be the different degrees of susceptibility to H. pylori infection of PG I and PG II. It has been suggested that PG II is a more sensitive indicator of H. pylori load than PG I [17]. Furthermore, previous studies showed that PG II was a more sensitive marker of H. pylori eradication therapy than PG I in patients with normal renal function [8,18].

A third factor is the difference in the metabolic pathways of PG I and PG II, namely the relatively high renal excretion rate of PG I. Unfortunately, this is not yet fully understood, and very few reports have focused on this matter. In healthy subjects, the mean fractional excretion in the urine of PG I was 27.6%, while in contrast, that of PG II was only 1.0%, and the difference between PG I and PG II in healthy subjects was considered to be due to different renal tubular reabsorption rates [19]. Metabolic pathways of PG II other than renal might be important, and further studies are necessary to elucidate these points.

Our data showed that dialysis patients had serum levels of PG II similar to those of control patients. However, elevated serum levels of PG II as well as PG I in dialysis patients were reported previously by Nakahama et al. [7], who studied 51 normal volunteers, 40 HD patients and 21 CAPD patients. They showed that serum PG II levels were 14.45±8.55 ng/ml in normal volunteers and 29.0±16.6 ng/ml in HD patients, being significantly higher in the latter (P <0.05) [7]. Because our findings do not support that study, we are interested in the causes of this discrepancy. All the subjects studied by Nakahama et al. were free from gastroduodenal symptoms. In contrast, we included dyspeptic patients, and the proportion of dyspepsia in our dialysis patients was matched to that of controls. We speculate that our patients studied have more gastric symptomatic diversity and a higher rate of H. pylori-positivity than had the subjects studied by Nakahama et al., which could explain the discrepancy between our data and theirs. In our H. pylori-negative patients, dialysis patients had significantly higher serum PG II levels than controls, suggesting that the former have significantly higher serum PG II levels than the latter when patients are not infected with H. pylori.

In patients with normal renal function, previous studies showed that the best diagnostic accuracy in H. pylori eradication therapy between the different biochemical parameters was obtained by the changes in the serum PG I:PG II ratio [20,21] and the serum PG II levels [9,22]. Our data also showed that dialysis patients in whom H. pylori was eradicated showed a significant reduction of serum PG II levels and a significant elevation of the serum PG I:PG II ratio. However, in our dialysis patients, an increased PG I:PG II ratio after eradication therapy was found not only in 18 patients in whom H. pylori had been eradicated successfully but also in three patients in whom it had not been eradicated. Though our eradication study was preliminary, these findings suggest that in dialysis patients the changes in serum PG II levels may be the most useful index to distinguish success from failure in eradication therapy for H. pylori.

Serum gastrin levels were higher in dialysis patients than in controls, as expected. That was accounted for by impaired renal clearance and hyperproduction due to lack of a negative acid feedback mechanism [23,24]. In asymptomatic healthy subjects and patients with duodenal ulcers, H. pylori infection contributes to the elevation of serum gastrin concentration [25,26]. With regard to HD patients, one study showed that H. pylori-positives had significantly higher serum gastrin concentrations than H. pylori-negatives [27], while other studies and our study have not found such a difference [28,29]. The mechanism of increased gastrin concentration in H. pylori infection is still unclear, but one hypothesis is that H. pylori produces a specific biochemical substance that stimulates G-cell function (e.g. by cytokines) or that inflammation self-stimulates gastrin hypersecretion [30]. We speculate that in subjects with normal renal function, a link between H. pylori infection and hypergastrinaemia may exist, but in dialysis patients this may be obscured by elevated serum gastrin concentrations. We did not find any significant relationship between serum gastrin and PG levels either in dialysis patients or controls with regard to H. pylori infection. Large-scale testing will be necessary to elucidate this point.

Our data suggest that dialysis patients have a lower degree of inflammation of gastritis in comparison with patients with normal renal function, which is consistent with the findings of a previous study [29]. These findings are explained by the fact that our dialysis patients had a significantly lower prevalence of H. pylori infection, and this organism is now recognized as the major cause of histological gastritis [2,31]. The lower prevalence of H. pylori infection in dialysis patients had been supported previously by other investigations [29,32,33], and may be explained by the use in these studies of a wide variety of medications, including antibiotics.

In summary, our data suggest that in dialysis patients, high serum levels of PG II, but not of PG I, are significantly related to H. pylori infection and mucosal inflammation. Dialysis patients have a lower degree of inflammation of gastritis compared with normal renal function subjects, probably attributable to a significantly lower prevalence of H. pylori infection in the former. A significant decrease in the serum PG II level could be used to predict the eradication of H. pylori infection in dialysis patients.



   Acknowledgments
 
We are indebted to Professor H. Mabuchi for his critical reading of this manuscript. We thank H. Sugimoto for his technical assistance and Drs H. Sudoh, M. Kawano and T. Konoshita for their helpful discussions.



   References
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 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 

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