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Saudi Journal of Kidney Diseases and Transplantation
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ORIGINAL ARTICLE Table of Contents   
Year : 2010  |  Volume : 21  |  Issue : 4  |  Page : 694-700
Impact of cytotoxin-associated gene A of Helicobacter pylori strains on microalbuminuria in type 2 diabetes


1 Department of Internal Medicine, Faculty of Medicine, Zagazig University, Zagazig, Egypt
2 Department of Tropical Medicine, Faculty of Medicine, Zagazig University, Zagazig, Egypt
3 Department of Microbiology and Immunology, Faculty of Medicine, Zagazig University, Zagazig, Egypt

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Date of Web Publication26-Jun-2010
 

   Abstract 

Cytotoxin-associated gene A (CagA) positive strains of H. pylori have a significant correlation with gastritis and peptic ulcer, and may induce persistent systemic inflammatory response, increase vascular damage, and compromise glycemic control in diabetic patients. To evaluate correlation between infection by cagA positive strains of H. pylori and occurrence of microalbuminuria and glycemic control in type 2 diabetic patients, we prospectively studied 98 dyspeptic type 2 diabetic patients as a study group and 102 dyspeptic non-diabetic subjects as a control group. Gastric biopsy specimens obtained with endoscopy were cultured to isolate H. pylori. All the isolated H. pylori strains from cultures were used for detection of cagA gene by polymerase chain reaction. There was no significant difference between study and control groups regarding infection with cagA positive strains of H. pylori ( P= 0.145). Furthermore, there was no significant differences between both groups concerning the incidence of microalbuminuria ( P= 0.145). On the other hand, there was an extremely statistically significant difference in the inci­dence of microalbuminuria and glycemic control in the diabetic patients between those infected with cagA positive strains of H. pylori and cag A negative starins (P= 0.000). We conclude that infection with cagA positive strains of H. pylori are strongly associated with the increased inci­dence of microalbuminuria and poor glycemic control in type 2 diabetic patients.

How to cite this article:
Ibrahim A, Zaher T, Ghonemy TA, El-Azim SA, El-Azim MA, Ramadan A. Impact of cytotoxin-associated gene A of Helicobacter pylori strains on microalbuminuria in type 2 diabetes. Saudi J Kidney Dis Transpl 2010;21:694-700

How to cite this URL:
Ibrahim A, Zaher T, Ghonemy TA, El-Azim SA, El-Azim MA, Ramadan A. Impact of cytotoxin-associated gene A of Helicobacter pylori strains on microalbuminuria in type 2 diabetes. Saudi J Kidney Dis Transpl [serial online] 2010 [cited 2020 Oct 25];21:694-700. Available from: https://www.sjkdt.org/text.asp?2010/21/4/694/64649

   Introduction Top


Helicobatcer pylori (H. pylori) is one of the most common chronic infections world wide. [1] Diabetic patients are more susceptible to a wide range of infections as a result of chronic elevation of blood glucose level and impair­ment of immune response. [2] This deficiency of immunity is responsible for more frequent and severe infections such as H. pylori, [3] a gram­negative microaerophilic spiral bacterium that infects the gastroduodenal mucosa. [4] It is con­sidered the causative agent of many gastro­intestinal and extradiagestive conditions by pro­ducing excessive amounts of pro-inflammatory factors and cross linking to host antigens. [5] There are two phenotypically distinct H. pylori groups: type 1 bacteria, which express the cy­totoxin associated gene A antigen (cagA) and vacuolating cytotoxin associated gene antigen (vacA), and type 2 bacteria where cagA is ab­sent and vacuolating cytotoxin activity is not manifested although vacA gene is present. The type 1 bacteria are more strongly pathogenic than type 2 and induce a more intense inflam­matory response. [6]

CagA (120-145 KDa protein) is a highly anti­genic protein that is associated with a promi­nent inflammatory response. [7] It has a pathoge­nic effect on gastric and duodenal mucosa lea­ding to development of peptic ulcers. This is due to increased production of cytokines such as tumor necrosis factor (TNF) and interleukin (IL)-1, -6, and -8. [8] In addition, it causes poor glycemic control in type 2 DM patients. [9]

There were studies that discussed the rela­tionship between infection with H. pylori and presence of multiple diabetic atherosclerosis complications in the form of cerebrovascular accident, cardiac and peripheral vascular di­seases, retinopathy, neuropathy, and nephropa­thy. [4] Furthermore, there are reports that sug­gest an increased risk of recurrent atheroscle­rotic events due to infection with cagA posi­tive strains of H. pylori [5]

The aim of this study is to evaluate the asso­ciation between infection by cagA positive strains of H. pylori and incidence of micro­albuminuria and reduced glycemic control in the type 2 diabetic patients.


   Subjects and Methods Top


Study design

This is a prospective case-control study con­ducted at the Zagazig University Hospital, Za­gazig, Egypt. We studied 98 dyspeptic type 2 diabetic patients (53 males, 45 females, and mean age of 45 ± 5.4 years) and compared them to 102 consecutive dyspeptic non diabetic sub­jects (58 males, 44 females, mean age 46 ± 6.2 years). All the participants consented for the study. Dyspeptic symptoms were regarded as present complaints of epigastric pain, bloating, nausea, vomiting and early satiety, gastro­intestinal bleeding, and weight loss. Full phy­sical examination was performed, and body mass index (BMI) was calculated as weight in kilograms (clothing was subtracted) divided by height in meters squared. The subjects were further stratified into those with normal weight (BMI < 25), over weight (BMI: 25-30) and obese (BMI > 30).

We excluded patients with ischemic chest pain, previous cerebrovascular accident, decompen­sated heart failure, evidence of connective ti­ssue disorders, neoplastic diseases, hematolo­gical diseases, renal impairment, history of gastric surgery, cholecystectomy, peptic ulcer, previous H. pylori eradication, and non-steroi­dal anti-inflammatory drugs and/or antibiotics, H2 blocker, and proton pump inhibitors during the past two months prior to the study.

The laboratory investigations included fasting blood glucose, and only patients with a fasting blood glucose above 126 mg/dL were consi­dered as diabetic; [10] HBA1c (glycosylated HB) levels were obtained after 12 hours of fasting (was done for diabetic group only). HBA1c le­vel of 4% - 6% was considered normal; [10] Lipid profile was performed to exclude dyslipide­mia; Microalbuminuria was detected in 24-hour urine specimens, which were examined for uri­nary albumin excretion rate (UAER) with the use of a solid-phase enzyme-linked immuno­sorbent assay (ELISA) (Micro Albumin Quan­titative test; DRG International, Inc., USA), according to the manufacturer's protocol. The lowest detection limit was 1 μg/mL. According to 24-hour UAER, the patients were classified into: Normo-albuminuric (NA) (UAER < 30 mg/24 h), microalbuminuric (MA) (UAER 30­299 mg/24 h) and macroalbuminuric (UAER > 300 mg/24 h). The patients with macroalbu­minuria were excluded. [11]

All subjects were underwent endoscopy after overnight fasting using fiber-optic endoscope (ZIF XQ230; Olympus, Center Valley, PA) for evaluation of dyspepsia and infection with H. pylori. Two biopsies were obtained; an antral biopsy about 2 cm of the pylorus and another from the corpus of the stomach for bacterial isolation. [12] For cultures to detect H. pylori, the specimens were transported to the laboratory in 0.2 mL of 20% glucose broth (BioMerieux) in sterile screw-capped tubes at 4°C within two hours. Before culture, the specimens were grounded and homogenized with a sterile mor­tar and pestle in 1 mL of saline. The biopsy homogenate was placed onto a Columbia blood agar plate with supplements (trimethoprim, van­comycin, and amphotericin B. The plates were incubated under microaerophilic conditions; 5% O2, 7.5% CO2, 7.5% H2, and 80% N2 using CampyPak microaerophilic system envelopes (Columbia Diagnostics, Springfield, VA) at 37°C for up to ten days. The plates were checked every other day for growth. On day 5, the plates without obvious growth were sub­cultured onto Columbia blood agar plates to promote growth of lightly growing colonies that may have been missed visually. All colo­nies that were small, circular, and smooth co­lonies suggestive of H. pylori were tested with Gram-stain, oxidase, catalase, and urease tests to confirm the identification. [13]

The H. pylori infection was considered posi­tive if the culture and/or histopathological exa­mination and rapid urease test were positive. [14] All the isolated H.pylori were suspended in 2 mL of tryptone soy broth medium containing 20% (vol/vol) glycerol and kept frozen at -70°C until DNA extraction was performed. [15]

For the DNA extraction, the cultures were removed from the frozen stock by placing the vials in an alcohol-dry ice bath. A small amount of each frozen culture was scraped into the tip of a Pasteur pipette, and inoculated onto Co­lumbia blood an agar plate. Then, 5 mL of Bru­cella broth was inoculated with the H. pylori isolates and put in CO2 incubator under micro­aerophilic condition for 2-3 days. Later, 1.5 mL of the culture was spun in a microcentrifuge for two minutes at 13.000 rpm to obtain a compact pellet. The supernatant was discarded. The DNA was extracted from the pellets by use of the QIAamp DNA kit (QIAGEN, Hilden, Germany) according to the manufacturer's recommendations and the DNA was stored at -20°C until analysis. DNA extraction negative controls were performed in parallel by inclu­ding sterile tubes without samples to check for contamination of the DNA extraction reagents.

Polymerase Chain Reaction (PCR) was per­formed for detection of the CagA gene by using a primer pair: (forward: 5΄ AAT ACA CCA ACG CCT CCA AG 3΄ and reverse: 5΄TTG TTG CCG CTT TTG CTC TC 3΄).

PCR was carried out in a 25 μL volume in thermal cycler (Perkin Elmer- Cetus, USA). For both amplification and cycling condition, the procedure included initial denaturation at 95°C for 5 minutes, followed by 34 cycles of dena­turation at 94°C for one minute, annealing at 53°C for one minute, and extension at 94°C for one minute. A final extension cycle was extended to 5 minutes at 72°C.

Of the amplified DNA products with the size of 294 bp represented the ureC gene and those with 400 bp represented cagA gene, and they were detected on 2% agarose gel. An amount of 8 μl of each PCR mixture was mixed with 2 μl of a gel loading buffer and subjected to gel electrophoresis (2% agarose). Finally, 2 μl of 100-bp DNA MW marker (ABgene House, Blenheim Road, Epsom, Surrey, KT 19 9AP, U.K.) plus 2.5 μl of gel loading buffer (6X) were loaded into another well [Figure 1].


   Statistical Analysis Top


Statistical analysis was performed using SPSS version 13. Proportions were compared using Chi square test while means were compared using student-t test. P value < 0.05 was con­sidered significant.


   Results Top


[Table 1] shows no significant difference of age and gender between diabetic patients and controls (P= 0.367, P= 0.692), respectively. However, there was an extremely significant difference between the two groups regarding BMI (P= 0.000). Our results showed non-sig­nificant difference in distribution of H. pylori infection between patients 53/98 (54.1%) and controls 58/102 (56.9%) (P= 0.321). On the other hand, the numbers of diabetic patients and controls with CagA positive strains were 40/98 (40.8%) and 37/102 (36.3%), respectively; the statistical difference between the two groups was non-significant. There was also non-signi­ficant difference in the incidence of microalbu­minuria between patients 30/98 (30.6%) and controls 22/102 (21.6%) ( P= 0.145).

[Table 2] shows an extremely statistically significant difference between diabetic patients with CagA- positive and CagA- negative strains of H. pylori regarding glycemic control (fasting blood glucose and HbA1c) (P= 0.000 and P= 0.000, respectively). In addition, there was 27/40 (67.5%) CagA-positive patients who re­vealed microalbuminuria in contrast to only 3/58 (5%) of the CagA-negative patients, ( P= 0.000).

[Table 3] shows that 15/37 (40.5%) cagA-posi­tive non-diabetics (controls) compared to 7/65 (10.7%) cagA-negative non-diabetics (controls) had microalbuminuria ( P= 0.000).


   Discussion Top


There are equivocal and little data about the relationship between H. pylori infection and diabetes mellitus. Our results showed that the prevalence of this infection was similar in dia­betics and non diabetic. This is in agreement with several previous studies. [14],[15],[16],[17],[18] The decreased chance of growth of H. pylori in diabetics may due to factors such as reduction of acid sec­retion, achlorohydria, presence or absence of microangiopathy of gastric mucosa. [19],[20] How­ ever, in contrast to our findings, other studies reported significantly higher prevalence of H. pylori infection in type 2 DM patients. [21] These studies explained their results by the impair­ment of cellular and humoral immunity in dia­betics, [22],[23] reduction of gastrointestinal motility and autonomic neuropathy with bacterial colo­nization and overgrowth, which are common in DM. [24] Moreover, a higher secretion of pro­inflammatory cytokines attributable to the H. pylori gastric infection. [25] This discrepancy bet­ween our results and previous studies may be attributable to methods used to detect infection, difference in selection of control groups and sample sizes.

In our study, there was no significant statis­tical difference regarding CagA and microalbu­minuria in diabetics and non diabetics group. Microalbuminuria may occur in diabetics as a microvascular complication of DM, but also microalbuminuria was present in non diabetics to the extent as diabetics, and this suggests a causative correlation between infection by H. pylori and appearance of microalbuminuria. Our results are comparable with those of Fran­ceschi et al [26] and Demir et al. [16] In accordance with our result, some researchers found that chronic H. pylori infection causes an increased production of cytokines such as vascular per­meability growth factor (VPGF), tumor necro­sis factor alpha (TNF alpha), and IL-1. These cytokines may alter the permeability of the glomerular basement membrane resulting in the urinary loss of albumin and immuno­globulins, and they are stimulated in the CagA­positive H.pylori infected patients and may induce an inflammatory process of glomerulo­ nephritis and proteinuria. [12],[26],[27],[28] Another expla­nation for endothelial damage is the decrease in the level of vitamin B 12 and folic acid in patients with chronic H. pylori, which causes atrophic gastritis and results in increased levels of homocysteine in blood and consequently increases vascular endothelial damage. [28]

Finally, since HbA1c is a good indicator of blood glucose concentrations over the pre­ceding 1-3 months, [29] we depended in our study on its levels and those of the fasting blood glucose [16] to determine the glycemic control between CagA-positive and CagA-negative diabetics, and our results showed a high cor­relation between the impaired control of these parameters and the positivity of the CagA. Gino et al [30] also found a poor glycemic control in type two DM patients who were infected by H. pylori. The significant decrease in the gly­cemic control in patients infected with the vi­rulent CagA-positive of H. pylori could be explained by its ability to increase insulin resistance, [31] and decrease serum concentration of somatostatin, [32] which has an inhibiting effect on insulin release. [33] Also, CagA-positive strains are associated with increased production of cytokines such as tumor necrosis factor (TNF alpha), interleukin (IL)-1, -6, and -8, [2] which may affect carbohydrate metabolism and sti­mulate the secretion of insulin counter-regu­latory hormones leading to hyperglycemia in diabetic patients. [34] In contrast, other studies did not find an association between infection by H. pylori and glycemic control, [16] and ex­plained their findings by the fact that gastritis increases glucose-and meal-stimulated insulin release by increasing gastrin secretion, [35] which inhibit glucose absorption in the small intes­tine, and amplifies glucose stimulated insulin release. [36]

In conclusion, our study found a significant correlation between the infection with CagA virulent strains of H. pylori and poor glycemic control and development of microalbuminuria in type 2 diabetic patients. Further study about the effect of therapy on such patients to re­verse such disturbances is warranted.

 
   References Top

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19.McGowann CC, Cover TL. Blaser MJ. Helico­bacter pylori and gastric acid: biologic and therapeutic implications. Gastroenterology 1996;110:926-38.  Back to cited text no. 19      
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29.Goldstein DE, Little RR, Lorenz RA, et al. Tests of glycemia in diabetes. Diabetes Care 2004;27:1761-73. Full text via cross ref/view record in scopus/cited by in scopus (87).  Back to cited text no. 29      
30.Gino G, Fernandini-P, Mezones-Holguin E, et al. In patients with type 2 diabetes mellitus, are glycosylated hemoglobin levels higher for those with helicobacter pylori infection than those without infection? Clin Infect Dis Chicago J 2008;47(1):144-6.  Back to cited text no. 30      
31.Aydemir S, Bayraktaroglu T, Sert M, et al. The effect of Helicobacter pylori on insulin resistance. Dig Dis Sci 2005;50:2090-3.  Back to cited text no. 31      
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33.Begue RE, Gomez R, Compton T, Vargas A.. Effect of helicobacter pylori eradication in the glycemia of children with type 1 diabetes. South Med J 2002;95(8):842-5.  Back to cited text no. 33      
34.Sushil K, Ashok K, Vinod DK. Direct detec­tion and analysis of vac A genotypes and Cag A gene of Helicobacter pylori from gastric biopsies by a novel multiplex polymerase chain reaction assay. Diagn Microbiol Infect Dis 2008;62:366-73.  Back to cited text no. 34      
35.Colturi TJ, Unger RH, Feldman M. Role of circulating somatostatin in regulation of gatric acid secretion, gastrin release, and islet cell function. Studies in healthy subjects and duo­denal cell patients. J Clin Invest 1984;74:417­-23.  Back to cited text no. 35      
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Correspondence Address:
Tarek A Ghonemy
Renal Unit, Zagazig University Hospital, Zagazig
Egypt
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