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 Table of Contents  
ORIGINAL ARTICLE
Year : 2016  |  Volume : 44  |  Issue : 2  |  Page : 76-80

Helicobacter pylori infection: a risk factor for insulin resistance in nonobese nondiabetic individuals


1 Department of Internal Medicine, Faculty of Medicine, Tanta University, Tanta, Egypt
2 Department of Clinical Pathology, Faculty of Medicine, Tanta University, Tanta, Egypt

Date of Submission17-Apr-2016
Date of Acceptance04-May-2016
Date of Web Publication29-Aug-2016

Correspondence Address:
Noha E Esheba
Department of Internal Medicine, Faculty of Medicine, Tanta University, 69 Saied Street, Tanta
Egypt
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DOI: 10.4103/1110-1415.189344

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  Abstract 

Background Helicobacter pylori is a pathogenic bacterium that has been linked to many disorders such as cardiovascular diseases, diabetes mellitus, and dyslipidemia. However, whether it is associated with insulin resistance still needs to be evaluated. In this work we aimed to delineate the possible relation of H. pylori infection with insulin resistance in nonobese nondiabetic patients.
Patients and methods
The study was carried out on 80 individuals who were divided into two groups. Forty patients were diagnosed to have H. pylori and 40 healthy volunteers formed the control group. All were subjected to history taking, clinical examination, routine laboratory investigations, evaluation of H. pylori immunoglobulin G level, and assessment of fasting blood glucose and fasting insulin level to calculate homeostasis model assessment of insulin resistance.
Results
There was a significant increase in C-reactive protein in H. pylori-positive patients when compared with H. pylori-negative controls. Also a significant positive correlation was found between homeostasis model assessment of insulin resistance and each of fasting blood glucose, fasting insulin, and C-reactive protein in both groups.
Conclusion
H. pylori infection was strongly associated with insulin resistance in nonobese, nondiabetic patients.

Keywords: Helicobacter pylori, homeostasis model assessment of insulin resistance, insulin resistance


How to cite this article:
Esheba NE, Nagy HM. Helicobacter pylori infection: a risk factor for insulin resistance in nonobese nondiabetic individuals. Tanta Med J 2016;44:76-80

How to cite this URL:
Esheba NE, Nagy HM. Helicobacter pylori infection: a risk factor for insulin resistance in nonobese nondiabetic individuals. Tanta Med J [serial online] 2016 [cited 2019 Nov 17];44:76-80. Available from: http://www.tdj.eg.net/text.asp?2016/44/2/76/189344


  Introduction Top


In recent years, a significant association has been documented to exist between cardiovascular diseases, diabetes mellitus, dyslipidemia, and Helicobacter pylori infection [1].

H. pylori is a noninvasive, microaerophile, Gram-negative, spiral-shaped pathogenic bacterium. It has a specific affinity to colonize the gastric epithelium leading to chronic gastritis, peptic ulcer disease, and/or gastric malignancy [2].

Insulin resistance (IR) is defined as a pathologic condition in which normal insulin levels produce a subnormal response in the peripheral tissues [3],[4]. The prevalence of IR syndrome is rapidly increasing all over the world as a result of the ongoing obesity epidemic that notably increases with age [5]. Chronic inflammation and production of a large amount of proinflammatory and vasoactive substances such as cytokines (IL-8, IL-10, IL-12) and acute-phase proteins such as C-reactive protein (CRP) were found to be involved in the pathogenesis of IR [6].

As the studies estimating the association of H. pylori and IR in nondiabetic individuals are few, we conducted this study to try shedding some light on this point.


  Aim Top


The aim of this study was to delineate the possible relation of H. pylori infection with IR in nonobese nondiabetic patients.


  Patients and methods Top


The present study was carried out on 80 patients selected from the outpatient clinic of the Internal Medicine Department, Tanta University Hospital, over a period of 3 years from January 2013 until December 2015.

The participants of this study were classified into two groups:

  1. Group I (the study group): it included 40 patients diagnosed to have H. pylori infection.
  2. Group II (the control group): it included 40 healthy volunteers of matching age and sex who were H. pylori negative.


Inclusion and exclusion criteria

Patients older than 18 years with dyspeptic symptoms (e.g. epigastric pain, heart burn, eructation, nausea, and vomiting) who were positive for H. pylori infection (positive H. pylori immunoglobulin G by ELISA) and not having any of the exclusion criteria were included in group I.

Patients with chronic renal failure, liver cirrhosis, diabetes mellitus, BMI more than 30 kg/m2, systemic or local infection or inflammation, polycystic ovary disease, patients using anti-inflammatory drugs and/or aspirin, patients who had undergone prior H. pylori eradication therapy in the last 1 month, and smokers were excluded from the study. All participants provided written informed consent.


  Methods Top


All patients and controls were subjected to the following: full history taking, complete clinical examination, routine laboratory investigations including complete blood count, serum total cholesterol, high-density lipoprotein, low-density lipoprotein, and triglycerides, liver and kidney functions tests, CRP by latex agglutination, fasting blood glucose (FBG) (with Pars Azmoon commercial kit; Pars Azmoon, Tehran, Iran), and fasting insulin level (by immune-enzymometric assay; IEMA, Tosoh St AIA, USA) to calculate homeostasis model assessment of insulin resistance (HOMA-IR=fasting glycemia (mg/dl)×fasting insulinemia (IU/ml)/405), first described by Matthews et al. [7], and serological test for detection of H. pylori infection by ELISA technique (H. pylori IgG ELISA kit, Padtan Elm Co, Iran). BMI was calculated as body weight (kg)/height (m2).

Statistical analysis

Comparisons between the two groups were performed using a two-tailed unpaired Student’s t-test. Data were presented as mean±SD and range. Correlations were assessed using the Pearson correlation test. P values less than 0.05 were considered statistically significant. All analyses were performed using SPSS statistical software (V.16; SPSS Inc., Chicago, Illinois, USA).


  Results Top


While comparing the two groups, there was no significant difference in any of the following: sex, age, BMI, total cholesterol, high-density lipoprotein, low-density lipoprotein, and triglycerides. There was a significant increase in CRP in H. pylori-positive patients when compared with H. pylori-negative controls (P<0.0001) [Table 1].
Table 1 Demographic and laboratory data of the studied groups

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The clinical presentation of group I patients is listed in [Table 2].
Table 2 Clinical presentation of group I patients

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The levels of fasting insulin and HOMA-IR were significantly higher in group I in comparison with group II (P<0.0001 and 0.0001, respectively). As for FBG, it was higher in group I than in group II, but did not reach statistical significance [Table 3].
Table 3 Levels of fasting blood glucose, fasting insulin, and homeostasis model assessment of insulin resistance in the studied groups

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As for the correlation between HOMA-IR and other variables, a significant positive correlation was found between it and each of FBG, fasting insulin, and CRP in group I (P<0.001, 0.0001, and 0.0001, respectively). The same was found in group II (P<0.006, 0.0001, and 0.027, respectively). There was no significant correlation between HOMA-IR and age or BMI in either group [Table 4].
Table 4 Correlation between homeostasis model assessment of insulin resistance and other variables in the studied groups

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  Discussion Top


The suspicion that H. pylori may be involved in pathological lesions is based on the following: (i) local inflammation may cause systemic effects; (ii) H. pylori gastric infection is chronic and lasts for decades; and (iii) persistent infection induces chronic inflammatory and immune responses that can cause lesions in both local and remote sites from the primary infection site [8],[9].

IR with a consequent hyperinsulinemia has a central role in the pathogenesis of many diseases such as diabetes mellitus, atherosclerosis, hypertension, and dyslipidemia [10].

It was mentioned that healthy men with exposure to some pathogens such as herpes virus types I and II, which are characterized by persistent and chronic infection, may present with increased fat mass and IR. The more the exposure to the pathogens, the lower the insulin sensitivity and the higher the levels of inflammatory markers [11].

The aim of this work was to investigate whether there is association of H. pylori infection with IR in nonobese, nondiabetic patients. We selected nonobese, nondiabetic patients to eliminate the effect of obesity and diabetes on IR in H. pylori-positive patients, which was proven years ago by other studies.

In the present study, although the mean FBG level was slightly higher in the H. pylori-positive group, it was not statistically significant (P=0.464).

Our results were in agreement with those of Eshraghian et al. [12], who recorded that the mean FBG level was 77.17±8.4 mg/dl in the H. pylori-negative group and 78.44±10.7 mg/dl in the H. pylori-positive group, with no statistically significant difference between the two groups (P=0.6).

The results of Aydemir et al. [3] and Aslan et al. [13] were somewhat different from ours as they stated that FBG was slightly higher in the H. pylori-negative group compared with the positive group, but the difference was also not statistically significant (P>0.05).

In the present study the mean fasting insulin level was statistically higher in group I in comparison with group II (P=0.0001).

This correlates well with the results obtained by Eshraghian et al. [12], who reported that fasting serum insulin level was significantly higher in the H. pylori-positive group compared with the H. pylori-negative group (P<0.05).

As for HOMA-IR, there was a statistically significant increase in the H. pylori-positive group (P=0.0001), which supports our hypothesis of the effect H. pylori infection has on the development of IR.

That could be explained by chronic inflammation and alteration in counterregulatory hormones that are responsible for IR pathogenesis [14].

These results were in agreement with those of Assal et al. [15], who reported that mean HOMA-IR in H. pylori-positive cases was significantly higher when compared with that in H. pylori-negative cases (P<0.001). Gen et al. [16] documented similar results (P=0.05).

Our results were partially in accordance with those of Vafaeimanesh et al. [17], who reported that in 218 nondiabetic patients IR was higher in H. pylori-positive patients than in seronegative individuals but the difference did not reach statistical significance (P=0.704).

Also the mean CRP was significantly higher in group I in comparison with group II (P=0.0001), with a significant association with H. pylori infection.

These results were compatible with those of Ishida et al. [18] and Gen et al. [16], who reported that CRP levels were significantly higher in patients with H. pylori infection compared with those in patients without H. pylori infection (P<0.05).

In the present study there was a significant positive correlation between HOMA-IR and CRP in group I (P=0.0001).

These results were in agreement with those of Nakanishi et al. [19], who documented that the elevated CRP levels were associated with increased fasting insulin levels, FBG levels, and HOMA-IR (P<0.001).

This finding was in agreement with that of Gelaye et al. [20], who reported that elevated CRP was significantly associated with increased mean fasting insulin and mean HOMA-IR concentrations (P<0.001).

The results obtained by Dimic et al. [21] were partially in accordance with ours, as they considered a cutoff value of 2 for HOMA-IR and reported that patients in group A had HOMA-IR less than 2 and those in group B had HOMA-IR higher than 2. In group A CRP level was 1.76±0.72 mg/l. In group B CRP level was 3.84±1.45 mg/l. There was a statistically significantly higher value of CRP in group B compared with group A (P<0.001).

This finding may suggest that the associations of high CRP levels with fasting insulin, FBG, and HOMA-IR might be due to the occurrence of a state of chronic systemic subclinical inflammation [19].

The relationship between inflammation and IR in type 2 diabetes has already been shown [22]. A higher prevalence of H. pylori in diabetic patients has also been documented [23]. However, studies on nonobese nondiabetic patients are lacking, which is why the results of this work are important because the study group was selected from among nonobese patients with normal blood glucose concentrations.

In 2009, Gunji et al. [24] studied 1107 nondiabetic Japanese patients and found that among those with higher IR score (HOMA-IR≥2.5) the prevalence of H. pylori was higher (39.4 vs. 28.7%, P=0.027).

H. pylori causes systemic host inflammatory responses including cytokine production such as TNF-α, CRP, IL-1β, lipid peroxides, hyperhomocysteinemia, and intercellular and vascular cell adhesion molecules (ICAM-1 and VCAM-1, respectively) [23],[25].

Although there are several mechanisms proposed for the association between H. pylori and IR, there are not enough data to clarify the effects of H. pylori eradication on IR. Some studies showed the favorable effect of H. pylori eradication therapy on IR and metabolic syndrome components [16].

Dogan et al. [26] suggested eradication of H. pylori to prevent diabetes and associated diseases. Also, Rizk et al. [27] concluded in their study that H. pylori infection is associated with dyslipidemia, IR, and elevated HbA1c in obese individuals.


  Conclusion Top


From these results we can conclude that there is a strong association between H. pylori infection, IR, and CRP in nonobese, nondiabetic patients.

Recommendations

Further studies on a larger number of patients are needed as an understanding of the role of H. pylori in IR is important to control important diseases such as diabetes mellitus. Follow-up of HOMA-IR after eradication of H. pylori is required.

Acknowledgements

The authors thank all participants for their help during this study.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

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  [Table 1], [Table 2], [Table 3], [Table 4]



 

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