- Research note
- Open Access
Helicobacter pylori infection, gestational diabetes mellitus and insulin resistance among pregnant Sudanese women
BMC Research Notes volume 11, Article number: 517 (2018)
To assess the association between Helicobacter pylori (H. pylori) infection and insulin resistance among pregnant Sudanese women attending Saad Abuelela hospital (Khartoum). A cross-sectional study was conducted from 1st July 2017 to 31st January 2018. One hundred and sixty-six women were enrolled and underwent testing for H. pylori IgG antibodies using specific ELISA kits. The Quantitative insulin sensitivity check index (QUICKI) was computed from the fasting insulin and glucose levels.
Median age, gravidity and gestational age were 27 years, 2 and 26 weeks, respectively. Twenty (12%) women were found to have gestational diabetes mellitus (GDM). H. pylori IgG seroprevalence was 66.0% among the study population. Univariate analysis showed that H. pylori-seropositivity was significantly higher among women who have GDM while Log (Homeostatic Model Assessment-β) HOMA-B% was lower (P value = 0.038, and 0.028) respectively. There was no difference between the GDM group and the other group in terms of demographics, body mass index, haemoglobin and QUICKI index results. In multivariate analysis, a higher prevalence of H. pylori was associated with GDM (OR = 2.8, 95% CI 1.1–7.5, P = 0.036). The current study concludes that an increased prevalence of H. pylori is a risk factor for the development of GDM.
The gram-negative bacillus Helicobacter pylori (H. pylori) is the main cause of chronic gastric infection . It is estimated that fifty percent of the world population is infected with H. pylori, with a higher prevalence in the developing countries [2, 3]. It is not only regarded as pathogenic but also a high class carcinogen . While the majority of patients infected with H. pylori tend to develop chronic gastritis, some of them progress to gastric and duodenal ulcers, atrophic gastritis, mucosa-associated lymphoid tissue lymphoma, intestinal metaplasia and gastric cancer [5,6,7].
A number of reports have observed the association between H. pylori and cardiovascular disease and the metabolic syndrome [8, 9]. Furthermore, H. pylori infection has also been indirectly linked to toll-like receptors activation via lipopolysaccharides, leading to metabolic changes culminating in insulin resistance . The association between H. pylori infection and insulin resistance remains controversial. While some studies reported the association between H. pylori infection and insulin resistance [11,12,13,14,15,16], others refuted such a relationship [17,18,19]. Cardaropoli et al. described a strong link between gestational diabetes and H. pylori . Furthermore, few of these studies investigated the association between H. pylori and insulin resistance among pregnant women. Therefore, further research addressing the interplay between H. pylori and insulin resistance is needed.
In Sudan, there is high prevalence of H. pylori among pregnant women regardless of their age and parity [21, 22]. The current study aimed to investigate the association between H. pylori infection and insulin resistance among pregnant Sudanese women.
A cross-sectional study was conducted at Saad Abuelela hospital, Khartoum, Sudan from the 1st of July 2017 to 31st of January 2018. After signing an informed consent, women with single viable pregnancies were included in the study. Women with twins, diabetes, hypertension, lipid disorders, kidney disease and hemolytic anemia/thalassemia/haemoglobin variants were excluded. Data was collected using a questionnaire that included demographic, obstetrics and clinical data (age, residence, education, occupation, gravidity, parity). The women’s weight and height were measured using standard methods and then their body mass indices were computed.
The glucose tolerance test was performed at 24–28 weeks of gestation. The diagnosis of gestational diabetes mellitus was based on the recommendations of International Association of Diabetes and Pregnancy Study Groups (IADPSG), “fasting blood glucose (FBG) ≥ 92 mg/dl or 1-h blood glucose was ≥ 180 mg/dl and/or 2-h blood glucose ≥ 153 mg/dl, after a 75-g oral glucose load .
The glucose level was measured by the glucose oxidase method (Shino-Test Corp. Tokyo, Japan).
The fasting insulin was measured using immunoassay analyzer (AIA 360, Tosoh, Tokyo, Japan. Insulin resistance was calculated using the quantitative insulin sensitivity check index (QUICKI) = 1/[log fasting insulin level (µU/ml) + log fasting glucose level (mg/dl)] . Insulin secretion was indicated by the HOMA of β-cell function (HOMA-β) (%) = 360 × fasting insulin level (µU/ml)/[fasting glucose level (mg/dl) − 63] .
Helicobacter pylori IgG antibodies were tested using commercial H. pylori-specific ELISA (Euroimmun, Lu¨beck, Germany). The tests were performed as per the manufacturer’s instructions. Five millilitres of blood were withdrawn in a plain tube, allowed to clot, centrifuged and stored at − 20 °C. Test values of ≥ 1.1 units were regarded as positive. Those ranging between 0.9 and 1.1 units were regarded as weakly positive and those ≤ 0.9 units were considered as negative for H. pylori.
SPSS for Windows (version 20.0) was used for data analyses. After checking for normality of distribution of data, the studied variables were described as means, medians and percentages. The difference of medians and proportions were compared between the H. pylori IgG seropositive and IgG seronegative using Mann–Whitney U test and χ2, respectively. All variables were entered into a logistic regression model where the dependent variable was gestational diabetes presence or absence. A P value less than 0.05 was considered statistically significant.
A total number of 166 women were recruited to the study. Respectively, the median age, gravidity and gestational age were 27 years, 2, and 26 weeks. Twenty (12%) of these women had gestational diabetes mellitus, 109 (65.7%) women were H. pylori IgG seropositive. Univariate analysis showed that the mean fasting blood sugar (FBS), the median of first hour post prandial blood sugar (1hpp), the median of the 2 h post prandial blood sugar (2hpp) and the proportion of the H. pylori-positive patients were significantly higher among those who have gestational diabetes mellitus (P value = 0.010, < 0.001, < 0.001, 0.038). The Log HOMA-B% was lower (0.028) respectively. There was no difference between the gestational diabetes mellitus group and the other group in terms of age, education, employment, gravidity, parity, gestational age, BMI, haemoglobin and QUICKI index results. See Table 1.
In multivariate analysis, a higher seropositivity of H. pylori was found to be a risk factor for the development of gestational diabetes mellitus (OR = 2.8, 95% CI 1.1 − 7.5, P = 0.036). See Table 2.
The main finding in the current study was the association between gestational diabetes mellitus and H. pylori IgG seropositivity, where the gestational diabetes group was more likely to be H. pylori IgG seropositive. Wang et al. concluded in their meta-analysis that included 39 studies involving 20,000 subjects that there is an association between H. pylori infection and diabetes mellitus . Cardaropoli et al. found a strong association between GDM and H. pylori among 2820 pregnant women . A large Chinese cohort of more than 30,000 showed an increased association between H. pylori infection and type 2 diabetes mellitus among middle-aged people . In their recent publication of 2016, Bonfigli et al. demonstrated that the elimination of H. pylori infection improved glucose metabolism in patients with type 2 diabetes . On the other hand, a study from Nigeria concluded that type 2 diabetes was not statistically different between H. pylori-infected subjects and controls. However, this study was not powered enough to come out with solid conclusions .
In our current study, we found no significant association between the QUICKI index and H. pylori IgG seropositivity among the pregnant Sudanese women. Gerig et al. reported a similar finding among 370 severely obese European subjects from both genders . In the same line, a Lebanese study described no association between H. pylori and insulin resistance among Lebanese adults. In this study, they used stored blood samples of subjects participating in a national non-communicable disease survey . Likewise, no association between H. pylori infection and insulin resistance was documented in a systematic review that included 9 studies with a total number of 2120 subjects . On the other hand, a number of researchers reported the association between H. pylori infection and insulin resistance [11, 12, 18, 31].
The association between H. pylori infection and insulin resistance can be explained by some biological mechanisms. First, changes in glucose metabolism might lead to chemical alterations in the gastric mucosa that facilitates the detection of H. pylori infection . A second explanation is an increase in the proinflammatory cytokines levels in response to H. pylori gastric infection that results in structural alterations to the insulin receptors inhibiting their interaction with insulin . He et al. in their study among mice suggested an interaction between H. pylori and gut microbiota resulting in an increased insulin resistance .
The current study concludes that an increased seroprevalence of H. pylori is a risk factor for the development of gestational diabetes mellitus.
We acknowledge the need for a larger sample size study.
quantitative insulin sensitivity check index
- HOMA-B :
homeostatic model assessment-beta
gestational diabetes mellitus
body mass index
Diabetes and Pregnancy Study Groups
fasting blood sugar
first hour post prandial blood sugar
two hours post prandial blood sugar
Sgouras DN, Trang TTH, Yamaoka Y. Pathogenesis of Helicobacter pylori infection. Helicobacter. 2015;20:8–16.
Everhart JE. Recent developments in the epidemiology of Helicobacter pylori. Gastroenterol Clin North Am. 2000;29:559–78.
Bruce MG, Maaroos HI. Epidemiology of Helicobacter pylori infection. Helicobacter. 2008;13(Suppl 1):1–6.
Sugano K, Tack J, Kuipers EJ, Graham DY, El-Omar EM, Miura S, et al. Kyoto global consensus report on Helicobacter pylori gastritis. Gut. 2015. https://0-doi-org.brum.beds.ac.uk/10.1136/gutjnl-2015-309252.
Mégraud F, Bessède E, Varon C. Helicobacter pylori infection and gastric carcinoma. Clin Microbiol Infect. 2015;21(11):984–90. https://0-doi-org.brum.beds.ac.uk/10.1016/j.cmi.2015.06.004.
Testerman TL, Morris J. Beyond the stomach: an updated view of Helicobacter pylori pathogenesis, diagnosis, and treatment. World J Gastroenterol. 2014;20(36):12781–808.
Bauer B, Meyer TF. The human gastric pathogen Helicobacter pylori and its association with gastric cancer and ulcer disease. Ulcers. 2011;2011:1–23.
Georges JL, Rupprecht HJ, Blankenberg S, Poirier O, Bickel C, Hafner G, et al. Impact of pathogen burden in patients with coronary artery disease in relation to systemic inflammation and variation in genes encoding cytokines. Am J Cardiol. 2003;92(5):515–21.
Nabipour I, Vahdat K, Jafari SM, Pazoki R, Sanjdideh Z. The association of metabolic syndrome and Chlamydia pneumoniae, Helicobacter pylori, Cytomegalovirus, and Herpes simplex virus type 1: The Persian Gulf healthy heart study. Cardiovasc Diabetol. 2006;5:25.
Manco M, Putignani L, Bottazzo GF. Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocr Rev. 2010;31:817–44.
Eshraghian A, Hashemi SA, Jahromi AH, Eshraghian H, Masoompour SM, Davarpanah MA, et al. Helicobacter pylori infection as a risk factor for insulin resistance. Dig Dis Sci. 2009;54(9):1966–70.
Vafaeimanesh J, Parham M, Seyyedmajidi M, Bagherzadeh M. Helicobacter pylori infection and insulin resistance in diabetic and nondiabetic population. Sci World J. 2014;2014:391250.
Chen L-W, Chien C-Y, Yang K-J, Kuo S-F, Chen C-H, Chien R-N. Helicobacter pylori infection increases insulin resistance and metabolic syndrome in residents younger than 50 years old: a community-based study. PLoS ONE. 2015;10(5):e0128671. https://0-doi-org.brum.beds.ac.uk/10.1371/journal.pone.0128671.
Li J-Z, Li J-Y, Wu T-F, Xu J-H, Huang C-Z, Cheng D, et al. Helicobacter pylori infection is associated with type 2 diabetes, not type 1 diabetes: an updated meta-analysis. Gastroenterol Res Pract. 2017;2017:5715403.
Haj S, Chodick G, Refaeli R, Goren S, Shalev V, Muhsen K. Associations of Helicobacter pylori infection and peptic disease with diabetic mellitus: results from a large population-based study. PLoS ONE. 2017;12:0183687.
Vafaeimanesh J, Bagherzadeh M, Mirzaei A, Parham M, Norouzinia M, Vafaee R. Effect of Helicobacter pylori on metabolic syndrome parameters in diabetic patients. Gastroenterol Hepatol Bed Bench. 2016;9:S36.
Gerig R, Ernst B, Wilms B, Thurnheer M, Schultes B. Gastric Helicobacter pylori infection is associated with adverse metabolic traits in severely obese subjects. Obesity. 2013;21(3):535–7.
Tamura T, Morita E, Kawai S, Sasakabe T, Sugimoto Y, Fukuda N, et al. No association between Helicobacter pylori infection and diabetes mellitus among a general Japanese population: a cross-sectional study. Springerplus. 2015;4(1):602.
Naja F, Nasreddine L, Hwalla N, Moghames P, Shoaib H, Fatfat M, et al. Association of H. pylori infection with insulin resistance and metabolic syndrome among lebanese adults. Helicobacter. 2012;17(6):444–51.
Cardaropoli S, Giuffrida D, Piazzese A, Todros T. Helicobacter pylori seropositivity and pregnancy-related diseases: a prospective cohort study. J Reprod Immunol. 2015;109:41–7.
Mubarak N, Gasim GI, Khalafalla KE, Ali NI, Adam I. Helicobacter pylori, anemia, iron deficiency and thrombocytopenia among pregnant women at Khartoum, Sudan. Trans R Soc Trop Med Hyg. 2014;108(6):380–4.
Gasim GI, Elmugabil A, Hamdan HZ, Rayis DA, Adam I. O blood group as a risk factor for Helicobacter pylori IgG seropositivity among pregnant Sudanese women. Clin Pract. 2017;7:958–81.
International Association of Diabetes and Pregnancy Study Groups Consensus Panel, Metzger BE, Gabbe SG, Persson B, Buchanan TA, Catalano PA, et al. International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care. 2010;33(3):676–82.
Katz A, Nambi SS, Mather K, Baron AD, Follmann DA, Sullivan G, et al. Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab. 2000;85(7):2402–10.
Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9.
Wang F, Liu J, Lv Z. Association of Helicobacter pylori infection with diabetes mellitus and diabetic nephropathy: a meta-analysis of 39 studies involving more than 20,000 participants. Scand J Infect Dis. 2013;45(12):930–8.
Han X, Li Y, Wang J, Liu B, Hu H, Li X, et al. Helicobacter pylori infection is associated with type 2 diabetes among a middle- and old-age Chinese population. Diabetes Metab Res Rev. 2016;32(1):95–101.
Bonfigli AR, Boemi M, Festa R, Bonazzi P, Brandoni G, Spazzafumo L, et al. Randomized, double-blind, placebo-controlled trial to evaluate the effect of Helicobacter pylori eradication on glucose homeostasis in type 2 diabetic patients. Nutr Metab Cardiovasc Dis. 2016;26:893.
Oluyemi A, Anomneze E, Smith S, Fasanmade O. Prevalence of a marker of active Helicobacter pylori infection among patients with type 2 diabetes mellitus in Lagos, Nigeria. BMC Res Notes. 2012;5:284.
Polyzos SA, Kountouras J, Zavos C, Deretzi G. The association between Helicobacter pylori infection and insulin resistance: a systematic review. Helicobacter. 2011;16:79–88.
Isiktas Sayilar E, Celik B, Dumlu S. Relationship between Helicobacter pylori infection and metabolic syndrome. Turk J Gastroenterol. 2015;26(6):468–73.
de Luis DA, de la Calle H, Roy G, de Argila CM, Valdezate S, Canton R, et al. Helicobacter pylori infection and insulin-dependent diabetes mellitus. Diabetes Res Clin Pract. 1998;39(2):143–6. http://0-ovidsp.ovid.com.brum.beds.ac.uk/ovidweb.cgi?T=JS&PAGE=reference&D=emed4&NEWS=N&AN=1998167333.
Bener A, Micallef R, Afifi M, Derbala M, Al-Mulla HM, Usmani MA. Association between type 2 diabetes mellitus and Helicobacter pylori infection. Turk J Gastroenterol. 2007;18(4):225–9.
He C, Yang Z, Cheng D, Xie C, Zhu Y, Ge Z, et al. Helicobacter pylori infection aggravates diet-induced insulin resistance in association with gut microbiota of mice. EBioMedicine. 2016;12:247–54.
SA, IA, DR designed the study. SA and AR gathered and entered the data. GI, IA conducted the statistical analysis. GI and IA drafted the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Availability of data and materials
The datasets used and/or analysed in the current study are available from the corresponding author on reasonable request.
Consent for publication
Ethics approval and consent to participate
Ethical approval for the current study was obtained from the Research Board at the Department of Obstetrics and Gynaecology, Faculty of Medicine, University of Khartoum, Sudan (Ethical Approval No. #2017,23) for the year 2017. After signing an informed consent, women with single viable pregnancies were included in the study.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Alshareef, S.A., Rayis, D.A., Adam, I. et al. Helicobacter pylori infection, gestational diabetes mellitus and insulin resistance among pregnant Sudanese women. BMC Res Notes 11, 517 (2018). https://0-doi-org.brum.beds.ac.uk/10.1186/s13104-018-3642-9
- Insulin resistance
- H. pylori