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Table of Contents
ORIGINAL ARTICLE
Year : 2019  |  Volume : 39  |  Issue : 2  |  Page : 325-335

Helicobacter pylori-related gastric corpus pathological changes in obese patients referred for laparoscopic sleeve gastrectomy


Department of Pathology, Faculty of Medicine, Minia University, Minya, Egypt

Date of Submission17-Jul-2019
Date of Acceptance01-Aug-2019
Date of Web Publication30-Sep-2020

Correspondence Address:
Rabab A Moussa
Department of Pathology, Faculty of Medicine, Minia University, 61111
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/EGJP.EGJP_40_19

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  Abstract 


Background Obesity is a serious health problem worldwide and laparoscopic sleeve gastrectomy (LSG) is a therapeutic option in obese patients. Helicobacter pylori infection increases the risk for gastric pathology and plays a role in limiting access to bariatric surgery. This study aimed to evaluate prevalence of different histopathologic changes in LSG, including H. pylori and non-H. pylori gastritis in the gastrectomy specimens and risk factors associated.
Materials and methods Sleeve gastrectomy specimens (542 patients) were examined histopathologically for detection of different histopathologic changes and presence of H. pylori, which was confirmed with Giemsa stain. Assessment of association of different risk factors with frequent histopathologic changes was done. Lastly, we examined the agreement of histopathology and serology methods for H. pylori diagnosis.
Results The results demonstrated a relatively high H. pylori infection (38.7%), and it was significantly associated with chronic active gastritis, chronic superficial gastritis, and follicular gastritis (P<0.001). The serological diagnosis has sensitivity of 64.4% and specificity of 79.6%.
Conclusion Routine histopathological biopsies with LSG are useful in detection of different histopathological changes, including H. pylori infection, which may affect the prognosis of the surgery. Biopsy is still to be preferred to serology as a detection method for H. pylori infection.

Keywords: gastritis, Helicobacter pylori, laparoscopic sleeve gastrectomy, obesity


How to cite this article:
Moussa RA, Omar AM. Helicobacter pylori-related gastric corpus pathological changes in obese patients referred for laparoscopic sleeve gastrectomy. Egypt J Pathol 2019;39:325-35

How to cite this URL:
Moussa RA, Omar AM. Helicobacter pylori-related gastric corpus pathological changes in obese patients referred for laparoscopic sleeve gastrectomy. Egypt J Pathol [serial online] 2019 [cited 2021 Mar 2];39:325-35. Available from: http://www.xep.eg.net/text.asp?2019/39/2/325/296062




  Introduction Top


Obesity is one of the critical public health problems all over the world. Approximately 33% of the US population have obesity (BMI is ≥30 kg/m2). In the Middle East, obesity is found among 74–86% of women and 69–77% of men (WHO, 2011), with increased risk of type 2 diabetes, hypertension, hyperlipidemia, coronary artery disease, and shorter life span (Kitahara et al., 2014). Furthermore, the Gulf countries (Kuwait, Bahrain, Saudi Arabia, and the United Arab Emirates, etc.) are the top ten countries worldwide in term of obesity (Ono et al., 2005). Dietary management and exercise can induce a weight loss of 5–10% in patients with severe obesity. Achieving this level of weight loss has positive effects on the diseases associated with metabolism and the heart (Ryan et al., 2010), but the benefits are not permanent. Thus, bariatric surgery (BS) is the best choice for this group of patients as it has greater efficiency and more durable benefits (Sjostrom et al., 2004). For patients having severe obesity, where either lifestyle or medication has not been effective, BS is a treatment option. Laparoscopic sleeve gastrectomy (LSG) has become one of the successful BS for obesity (DeMaria, 2007).

Histopathologic examination of sleeve resections demonstrated a wide range of pathological changes seen in these cases. However, there are some reports of the high incidence of gastritis in obese patients (Almazeedi et al., 2013; Clapp, 2015). Moreover, a preoperative prevalence of Helicobacter pylori was noticed, ranging from 8.7% in a German cohort (Kuper et al., 2010) to 85.5% in a Saudi cohort (Al-Akwaa, 2010), with other reports showing intermediate values (Carabotti et al., 2014). H. pylori infection plays a special role in patients with obesity. It can aggravate the complications and diseases associated with obesity, through the complementary effect on weight status, and it can be a negative factor in limiting access to BS (Carabotti et al., 2014). To avoid such potential consequences, routinely checking for bacteria and eradicating the infection before performing BS are recommended by experts (Papasavas et al., 2008).

The rationale of this study was to find out different types of abnormal histopathologic changes and their prevalence, in terms of associated risk factors. Age, BMI, sex, and H. pylori infection were assessed as risk factors for abnormal histopathologies. Additionally, we assessed risk factors associated with potentially premalignant abnormal histopathologic change (e.g. follicular gastritis), risk factors associated with a particularly frequent abnormal histopathologic change, and the prevalence of H. pyloriH. pylori and non-H. pylori gastritis and its correlation with other risk factors.


  Materials and methods Top


Procedures and data collection

This is a cross-sectional study, involving obese patients who had been scheduled for LSG, Doha Center for Obesity Surgery, Doha, Qatar. This study was approved from the Research Ethics Committee of Doha Center for Obesity Surgery, Qatar. All demographic, clinical, and histopathologic data were extracted from the medical records of 542 patients who underwent LSG from February 2013 to December 2014 and were retrospectively retrieved and systematically reviewed.

Pathology examination

The sleeve gastrectomy specimens were sent routinely for pathological examination. Three samples were taken from each specimen, one from each surgical margin and one random sample. When macroscopic alterations were noticed, an extra sample was taken from these areas. The specimens were fixed in 4% formaldehyde and embedded in paraffin, sectioned at 3 µm, which were subsequently stained with hematoxylin and eosin. Giemsa special stain for spirochetes was performed on at least one randomly selected section from each case. Accordingly, the following histopathologic variables were examined on each case: H. pylori presence and density, degree of chronic inflammation, presence of lymphoid follicles, presence and density of plasma cells, polymorphonuclear neutrophil activity, and presence and density of eosinophils. Each variable was graded as mild, moderate, or severe using a visual analog scale (Dixon et al., 1996). H. pylori density was graded as none, mild (when few microorganisms were present), moderate (when bacteria were present in separate foci), and severe (when near complete or complete surface layering with H. pylori was observed).

Statistical analysis

Data were analyzed using the SPSS statistical package version 20 (IBM SPSS, version 20, Armonk, NY: IBM Corp.). Numerical data were expressed as means and SD, and significant differences between numerical data were assessed using Student t-test. For the description of categorical variables, we used frequencies and percentages, and the significant differences were assessed with the χ2-test (or Fisher’s test for small samples). Analysis of variance and post-hoc tests were used to compare the three groups.

Sensitivity and specificity were calculated as follows:



The measure of agreement (K value) was analyzed using Cronbach’s α test (Altman, 1990).

For all tests, probability (P) was considered as follows:

Nonsignificant if greater than or equal to 0.05, significant if less than 0.05, and highly significant if less than 0.01


  Results Top


Characteristics of the sample

The study cohort included 542 patients, among which 174 (32.1%) were men. The average age was 30.51±9.90 years, with an age range from 12 to 62 years. More than 90% of patients included in this study are Arab patients compared with only 2.2% being foreign patients. Patients in this study group had a high BMI, with an overall mean BMI of 39.95±5.9. One hundred and twenty-two patients in the study population had different comorbidities; the most common associated diseases were diabetes mellitus 32/542 (5.9%), systemic hypertension, 18/542 (3.5%), hypothyroidism 26/542 (4.8%), and hyperlipidemia 19/542 (3.5%). All descriptive data for the study group are included in [Table 1].
Table 1 Characteristics of patients and findings

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Types and prevalence of laparoscopic sleeve gastrectomy histopathologic changes

[Table 1] shows the diversity of diagnoses of the LSG histopathologic specimens. Nearly one-third of the specimens (31.7%) were normal ([Figure 1]). The first most common histopathologic change (52.5%) was chronic superficial gastritis (categorized into mild/moderate/severe according to the amount/density of chronic inflammatory cells in the lamina propria) ([Figure 2]). The second most common histopathologic change (12.5%) was active chronic gastritis ([Figure 3]). To a lesser extent, follicular gastritis ([Figure 4]) comprised 2.3% of the cases, and other rare diagnoses including gastrointestinal stromal tumor (GIST), lipoma, and leiomyoma formed 1% of the studied specimens ([Figure 5]a–c).
Figure 1 Normal gastric mucosa. Hematoxylin and eosin staining, ×100.

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Figure 2 Chronic superficial gastritis: inflammatory cell infiltrates with lymphocytes and plasma cells in the upper third of the lamina propria. Hematoxylin and eosin staining, ×200.

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Figure 3 Chronic active gastritis: chronic inflammatory infiltrate with lymphocytes and plasma cells in the lamina propria associated with neutrophilic infiltrate of crypts. Hematoxylin and eosin staining, ×200.

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Figure 4 Follicular gastritis: abundant mononuclear inflammatory infiltrates with lymphoid follicles. Hematoxylin and eosin staining ×200.

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Figure 5 Other pathological lesions, including (a) gastrointestinal stromal tumor, (b) lipoma, and (c) leiomyoma. Hematoxylin and eosin staining, ×100.

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Detailed microscopic examination revealed that 172 cases presented normal morphology, as no neutrophils were observed. Minimal edema and congestion were considered to be normal, and on Giemsa staining, the presence of H. pylori was not observed in most cases 170/172 (98.8%). In 285 cases, chronic superficial gastritis was diagnosed based on the presence of inflammatory cell infiltrate with lymphocytes and plasma cells in the upper third of the lamina propria, edema, and/or congestion. Overall, 128/285 (44.9%) of these cases were associated with H. pylori infection.

Sixty-seven (12.4%) patients were diagnosed with chronic gastritis in the active phase characterized with chronic inflammatory infiltrate with lymphocytes and plasma cells in the lamina propria associated with neutrophilic infiltrate of lamina propria, pit, or surface epithelium. Most of these cases, that is, 63 (94%), were H. pylori positive on Giemsa staining. A smaller number of patients 13/67 (2.3%) were diagnosed with follicular gastritis, when the inflammatory infiltrate was present diffusely in the whole thickness of lamina propria with lymphoid aggregates with germinal center (follicles). All of these cases [13/13 (100%)] were H. pylori positive on Giemsa staining. No atrophy, intestinal metaplasia, or dysplasia was seen in our cases.

According to the histological results, the cases were subdivided into three groups: H. pylori gastritis (198 patients) when H. pylori was found in the histological sections ([Figure 6]a–c), non-H. pylori gastritis (168 patients) when inflammatory infiltrate was present without H. pylori, and normal mucosa (172 patients), with no H. pylori and no inflammatory infiltrate in the gastric mucosa. Their clinical data are summarized in [Table 2]. Regarding age, it was noticed that patients with H. pylori gastritis have older age compared with patients with normal gastric mucosa specimen and patients with non-H. pylori gastritis (P=0.021 and 0.017, respectively). A statistically significant difference was observed according to BMI; patients with H. pylori gastritis specimen had a lower BMI compared with patients with non-H. pylori gastritis (39.0±5.7 vs 40.6±6.0) (P=0.044). Regarding sex, it was noticed that more than two-thirds of the patients with H. pylori gastritis were females, whereas females were ∼60% of both patients with normal gastric mucosa specimen and non-H. pylori gastritis (P=0.005 and 0.006, respectively). Regarding marital status, more than half of the cases with H. pylori gastritis are married compared with only 39.9% in the non-H. pylori gastritis group (P=0.001). Meanwhile, no statistical difference was noticed regarding other variables, including ethnicity, smoking, and associated chronic diseases.
Figure 6 Chronic gastritis associated with variable H. pylori infection density: (a) mild infection, (b) moderate infection, and (c) severe infection. Giemsa staining, ×400.

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Table 2 Comparison between patients with normal gastric mucosa, H. pylori, and non H. pylori gastritis

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Risk factors associated with the most frequent abnormal histopathologic change.

[Table 3] shows the comparisons between patients with chronic superficial gastritis, which is the first most common histopathologic change among the studied groups and normal specimens. Although no statistical difference was observed between the two groups according to different variables including age, BMI, sex, ethnicity, marital status, smoking, or associated chronic diseases, a highly significant difference was noticed regarding the presence of H. pylori infection: ∼44% of patients with chronic superficial gastritis had H. pylori infection compared with only 1.2% in patients with normal gastric mucosa specimen (P<0.001). A particularly frequent abnormal histopathologic change is chronic active gastritis. It is a frequent precursor of peptic ulcer. [Table 4] emphasizes the comparison of patients with chronic active gastritis (n=67) versus normal specimens (n=172). It is clearly noticed, that 94% of patients with chronic active gastritis has H. pylori infection compared with only 1.2% of patients with normal gastric mucosa specimen (P<0.001). Moreover, a statistically significant difference was noticed regarding age among the two studied groups; older age (32.8±10 years) was noticed in the cases with chronic active gastritis specimen compared with the normal cases (29.5±10.0 years) (P=0.02). Regarding sex, it was noticed that more than two-thirds of patients with chronic active gastritis are female compared with 60% in patients with normal gastric mucosa (P=0.023). For marital status, more than 60% of patients with chronic active gastritis specimen are married compared with 48.3% of cases with normal gastric mucosa specimen (P=0.07); however, it did not reach a level of significance. Meanwhile, no significant difference was recorded with other variables including BMI, ethnicity, smoking, and associated chronic diseases.
Table 3 Comparisons between patients with chronic superficial gastritis and patients with normal specimens among studied group

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Table 4 Comparison of patients with chronic active gastritis versus patients with normal specimens

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A more detailed comparative subanalysis between the individual cases of follicular gastritis and infiltrates specimens was undertaken ([Table 5]). This revealed no differences between the two groups in terms of age, BMI, ethnicity, marital status, smoking, or sex. Regarding age, it was noticed that patients with follicular gastritis have younger ager than patients with normal gastric mucosa (35.7±4.7 vs 40.1±6.0 years); however, this difference did not reach a level of significance (P=0.052). Regarding associated chronic diseases, it was noticed that diabetes mellitus is more associated with patients with follicular gastritis compared with patients with normal gastric mucosa specimen (P=0.02). In addition, it was noted that H. pylori infection was significantly more associated with follicular gastritis (13/13) compared with normal specimens (2/172) (P<0.001).
Table 5 Comparison between patients with follicular gastritis versus patients with normal specimens

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On comparing different methods of diagnosis of H. pylori infection, analyzing the serological titers of anti-H. pylori antibodies, and the histological examination of the gastric biopsy (Giemsa staining), only 94 patients were applicable to have results of both methods of diagnosis. Patients were divided into two categories: H. pylori positive and H. pylori negative, as 41.5% of the patients were H. pylori positive by serology, whereas in the histological examination of the biopsy, 47.9% of patients were found to be H. pylori positive. Among those patients who were H. pylori positive in serology, 64.4% were also positive in the histological examination. Among those who were H. pylori negative in serology, 29.1% were H. pylori positive in the histological examination. Cohen’s κ agreement factor between the serological and histological diagnosis was moderate (κ=0.443). Binary logistic regression revealed that positive serology is 7.069 times more associated with positive histopathology than negative ones (P<0.001, confidence interval: 2.804–17.822) and that serology can predict only 18.7% of histopathology results (R2=0.187). Considering the histological diagnosis as a gold standard, it has been found that the serological diagnosis of H. pylori had a sensitivity of 64.4% and a specificity of 79.6% ([Table 6]).
Table 6 Sensitivity and specificity of serology method for detection of H. pylori

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  Discussion Top


This study comprised gastric specimens following LSG from 542 patients with a mean age of 30.51±9.90 years (males 32.1% and females 67.9%). In this study, the mean age and sex compositions were similar to those reported by Almazeedi et al. (2013), AbdullGaffar et al. (2016), and Safaan et al. (2017). More than 90% of patients included in this study are Arab patients compared with only 2.2% of foreign patients. Regarding obesity and BMI, this study reported a BMI of 39.95±5.9; however, different values were reported by other studies among different populations ranging from 44.3±6.8, 46.8±8.4, to 49 (Albawardi et al., 2013; Danciu et al., 2016; Safaan et al., 2017). In this study’s groups, it was found that the most common comorbidities were diabetes mellitus (5.9%), systemic hypertension (3.5%), hypothyroidism (4.8%), and hyperlipidemia (3.5%). Similar results (a range of 8.4–14.4% of the study population have diabetes) were reported by Rath-Wolfson et al. (2017) and Otero et al. (2015). However, Otero et al. (2015) demonstrated a higher prevalence of patients having arterial hypertension (72.28%) and high aminotransferase levels (75.9%); furthermore, all patients were diagnosed with fatty liver disease by ultrasound. These differences probably reflect the difference in the lifestyle among study groups.

Regarding normal histopathology among the LSG patients and their prevalence, it was observed that 32.7% of the LSG specimens were normal, which is almost the same result of Raess et al. (2015), who reported that no specific finding was noticed in 35.2% of the post-LSG patients. However, other reports recorded a higher normal histopathology rate: 50.3, 52, and up to 69% (Clapp, 2015; Ohanessian et al., 2016; Safaan et al., 2017). In contrast, Almazeedi et al. (2013) mentioned that no normal specimens were found among the post-LSG patients. This diversity might relate to the epidemiology of disease among different countries.

It was clearly noticed that the most common abnormal pathological finding among the groups in this study was chronic superficial gastritis (52.6%), followed by chronic active gastritis (12.6%) and nodular gastritis (2.4%). This was in accordance with AbdullGaffar et al. (2016) and Safaan et al. (2017) who reported a similar common histopathological findings incidence rate based on a similar classification of abnormal histopathological changes; however, this was partially in agreement with Almazeedi et al. (2013) who reported that the first pathological abnormality in his study groups is chronic gastritis with an incidence rate of 74.4%, followed by chronic active gastritis form with a rate of 6.8%. However, Almazeedi et al. (2013) described two subtypes: follicular and active follicular gastritis (9.6 and 4.9%, respectively), which is in contrast to this study, we recorded follicular gastritis in 2.4% of these specimens with no distinction between follicular and active follicular gastritis. Notably, these different classifications of abnormal histopathological changes among different countries may explain that difference in the percentage among different countries.

In this study, no malignancies among these abnormal histopathologic specimens were noticed. This was in agreement with many reports which confirmed that no malignancies were detected in the post-LSG specimens (Almazeedi et al., 2013; Raess et al., 2015; AbdullGaffar et al., 2016; Lauti et al., 2016; Ohanessian et al., 2016; Safaan et al., 2017).

Regarding the prevalence of H. pylori infection among these study groups, it was found that 36.5% were H. pylori positive. Safaan et al. (2017) reported a similar rate of 40.9% of the LSG specimens that were positive for HP. Similarly, other studies confirmed a high prevalence of H. pylori (between 20 and 97%) in Middle Eastern populations (Khedmat et al., 2013). Furthermore, a Saudi Arabian study recorded a higher prevalence of 85.5% (Al-Akwaa, 2010). Such a high prevalence of this bacterium in this study might be attributed to socioeconomic and sanitary factors. Meanwhile, other studies reported less much prevalence of H. pylori infection at 5.2, 7.3, and 8.6% (Almazeedi et al., 2013; Raess et al., 2015; Lauti et al., 2016). In addition, a German study found a less prevalence rate of 8.7% (Kuper et al., 2010). These differences probably reflect the local epidemiology of the infection.

Regarding the risk factors associated with H. pylori gastritis, a significant relationship with lower BMI was found: patients with H. pylori gastritis specimen have lower BMI compared with patients with non-H. pylori gastritis. This was supported by the hypothesis based on that H. pylori has important effects on gastric endocrine, including decreased production of ghrelin, which causes loss of appetite, and it had been thought that this organism may protect against obesity (Nweneka and Prentice, 2011). This also comes in agreement with decreasing rates of H. pylori infection and a parallel increase in obesity, which has been found in developed countries in recent decades, suggesting a causal association (Lender et al., 2014). To the best of our knowledge, the current study could be the first to report such an association between H. pylori infection and both the female sex and marital status, whereas no statistical difference in other risk factors including chronic disease was seen. A previous study done by Yamamoto et al. (2012) has suggested that obesity may be a risk factor for gastritis and gastritis could be H. pylori induced; in addition, obesity is more prevalent in females. Such considerations might contribute to explain these findings of the significant association between H. pylori infection and the female sex, with most being married.

Furthermore, this study revealed that H. pylori infection was significantly associated with chronic active gastritis, chronic superficial gastritis, and follicular gastritis (P<0.001). Previous reports have similarly shown associations of H. pylori with such conditions (Kara et al., 2014; Safaan et al., 2017). In addition, it is noticed that there is a significant association between chronic active gastritis and many risk factors, including older age, female sex, marital status, and H. pylori infection. Meanwhile, follicular gastritis revealed significant association only with H. pylori infection and diabetes milletus. This denotes that chronic active gastritis has many risk factors that may interact with each other. On the contrary, follicular gastritis is particularly associated with H. pylori infection, which could be a risk factor associated with potentially premalignant abnormal histopathologic change, for example, follicular gastritis, in addition to the coexistence of diabetic state, which may reduce immunity favoring more H. pylori infection. Moreover, these findings did not reveal any significant association between chronic superficial gastritis and any of other risk factors except for H. pylori infection. Compared with these findings, a study done by Safaan et al. (2017) observed that BMI and sex were not associated with any of these abnormal histopathologies, including chronic active gastritis, lymphoid aggregates, follicular gastritis, GIST, and intestinal metaplasia, except for chronic active gastritis, which was significantly associated with females.

Different methods of diagnosis of H. pylori infection exist in many previous reports. The serological assessment of the level of anti-H. pylori IgG antibodies is considered one of the commonly used techniques to detect H. pylori infection although there is a wide range of commercially cheap and easy-to-use available kits. However, this method cannot differentiate between active infection and asymptomatic colonization, or between current or previous infection, as the level of antibodies could remain high even a few months after the eradication of infection, which makes this test unsuitable for assessing the efficiency of treatment (Koletzko, 2005). Definitive evidence of H. pylori infection is a bacterial culture from the gastric biopsy. However, the sensitivity and specificity of the test, owing to technical difficulties, may vary greatly, up to 42% (Onders, 1997). Consequently, it cannot be considered the gold standard. Urea breath test has a higher sensibility and specificity compared with other invasive tests, but its specificity declines when other urease-producing bacteria are found in the intestine (Ferwana et al., 2015). In this study, on comparing the serological assessment of anti- H. pylori IgG antibodies and the histological examination of the gastric biopsy (Giemsa staining), we demonstrated that the prevalence of H. pylori infection was 47.9% in the histological examination, and the serological method showed the poorest specificity and accuracy compared with other tests (a sensitivity of 64.4% and a specificity of 79.6%). This was in agreement with a study done by Khalifehgholi et al. (2013) who demonstrated a lower H. pylori infection prevalence in the histological examination as compared with the serological test associated with the poorest specificity and accuracy compared with other tests. Therefore, it could be suggested that biopsy is to be preferred to serology; however; the two methods combined in confirming the diagnosis of H. pylori infection may be used in some circumstances.


  Conclusion Top


The most common abnormal histopathological change among the LGS was chronic superficial gastritis (52.6%). Some rare benign lesions (1%) were found such as GIST, lipoma, and leiomyoma; however, no malignancies were among abnormal histological specimen. A relative high H. pylori infection (38.7%) among this study groups was observed. The results demonstrated an association between H. pylori infection and lower BMI, female sex, and marital status. In addition, it has observed a significant association between H. pylori infection and chronic active gastritis, chronic superficial gastritis, and follicular gastritis. Many risk factors such as older age, female sex, marital status, and H. pylori infection are associated with chronic active gastritis, whereas H. pylori infection is strongly associated with follicular gastritis, which is a premalignant lesion for gastritis lymphoma. In this study, a lower H. pylori infection prevalence in the histological examination was detected as compared with the serological test associated with the poorest specificity and accuracy compared with other tests, so it could be suggested that biopsy is to be preferred to serology as a detection method for H. pylori infection. Finally, it is recommend that routine histopathological biopsies with LSG is useful in the detection of different histopathological changes, including H. pylori infection, which may affect the prognosis and outcome of the surgery.[32]

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

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