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. 2021 Dec 18;13:145. doi: 10.1186/s13098-021-00765-x

Table 1.

The characteristics of studies evaluating the effect of H. pylori infection on the risk of metabolic syndrome and insulin resistance in different populations

Authors (Years) (R) Country Type of Study
(Cohort or case control)
Study Population (Children, Adults, Women, or ……) Type of diabetes (IDDM, NIDDM, GDM) H. pylori detection methods Outcome (metabolic syndrome or insulin resistance) Age
(Mean)
BMI (Mean) Effect size (OR with a 95% CI) or (RR with a 95% CI)
Gunji et al. (2008) [54] Japan Case control 9582 Japanese (5488 men and 1906 women) IgG antibody without further laboratory assessment Metabolic syndrome (Japanese criteria) 47.3 22.9 1.39 (1.18–1.62)
So et al. (2009) [55] China Case control 288 men (107 Low adiponectin and 181 Normal adiponectin) IgG antibody concentrations were measured by a two-step immunometric assay (Immulite) Insulin resistance 40.7 25.3 1.30 (1.02, 1.65)
Jeon et al. (2012) [40] USA Cohort 63 Diabetes Type-specific IgG anti-body responses Insulin resistance 66.8 30.1 (HR) Sex and education adjusted (HR) Multivariate analysis
2.42 (0.99–5.92) 2.6 (1.10–6.60)
Naja et al. (2012) [56] Lebanon Case control 308 Lebanese adults (H. pylori (+) 160 And H. pylori (−)148) Immunoglobulin G antibody titers Metabolic syndrome (IDF) 40.97 27.3 Bivariate logistic regression: 0.71 (0.44–1.12)
Multivariate logistic regression: 0.54 (0.19–1.51)
Naja et al. (2012)[56] Lebanon Case control 308 Lebanese adults (H. pylori (+) 160 And H. pylori (−)148) Immunoglobulin G antibody titers Insulin resistance 40.97 27.03 Bivariate logistic regression: 0.70 (0.43–1.16)
Multivariate logistic regression: 0.74 (0.40–1.36)
Shin et al. (2012) [71] South Korea Cohort 5889 included subjects (3297 men and 2592 women) Anti-HP immunoglobulin G (IgG) antibody titers + detection of HP by histologic analysis Metabolic syndrome (NCEP) 48.0 23.8 serological status histologic status
IDF: 1.29 (1.10–1.50) 1.29 (1.11–1.50)
NCEP: 1.30 (1.13–1.50) 1.31 (1.15–1.50)
Hsieh et al. (2013) [72] Taiwan Cohort 2070 participants (H. pylori (+) 903 And H. pylori (−)1167) NIDDM RUT Insulin resistance 57.16 23.5 1.61
Bajaj et al. (2014) [57] India Case control 140 (aged ≥ 18 years) participants (80 type 2, 60 controls) NIDDM Rapid urease tests, histological examination of antral endoscopic biopsy specimens and serology Insulin resistance 55.6 2.4
Malamug et al. (2014)[58] USA Case control 4,136 aged 18 and over (NHW 1949, NHB 853, MA 1334) IgG anti- bodies to H. pylori in human serum Insulin resistance 50 29.40 Male Female
NHW 1.6 (1.2–2.2) 1.8 (1.31–2.54)
NHB:1.5 (1.03–2.37) 1.3 (0.92–1.98)
MA :1.4 (0.99–2.05) 1.8 (1.32–2.66)
Vafaeimanesh et al. (2014)[59] Iran Case control 429 (211 diabetic, 218 without diabetes) NIDDM Anti-HP IgG anti- body Insulin resistance 51 1.26
Chen et al. (2015) [60] Taiwan Case control 811 Residents Younger than 50 Years Old (H. pylori (+)509 And H. pylori (−)302) H. pylori-specific immunoglobulin G (IgG) antibody Metabolic syndrome (NCEP) 59.2 24.9 3.717(1.086–12.719)
Chen et al. (2015) [61] Taiwan Case control 3578 subjects ((H. pylori (+)724 And H. pylori (−)2854) UBT Metabolic syndrome (NCEP) 39.8 24.9 Male: 1.76 (1.26–2.47)
Female: 3.11 (1.73–5.62)
Sayilar et al. (2015) [73] Turkey Cohort 200 patients (H. pylori (+)99 And H. pylori (−)101) H. pylori was observed in the biopsy specimens by microscopic examination of the slides stained with hematoxylin and eosin Metabolic syndrome (NCEP) 48.1 30.1 3.61 (2.46–5.30)
Kayar et al. (2015) [42] Turkey Case control 133 dyspeptic patients (H. pylori (+)71 And H. pylori (−)62) H. pylori antigen stool test Insulin resistance 1.47
Chen et al. (2016) [62] Taiwan Case control 2113 MS + 557, MS− 1556) C-UBT Metabolic syndrome (NCEP) 59.9 27.3 1.50 (1.20–1.87)
Takeoka et al. (2016) [63] Japan Case control 1044 participants (H. pylori (+)247 And H. pylori (−)797) HP-specific IgG measured Metabolic syndrome (NCEP) 46.6 22.4 IgG concentration
Moderate: 3.47 (0.83–23.9) High: 3.70 (0.62–71.3)
Alzahrani et al. (2017) [64] USA Case control 842(421 adults with newly diagnosed diabetes and 421 matched controls) NIDDM H. pylori immunoglobulin G (IgG) antibody in serum Insulin resistance 49.6 35.6 1.03(0.74–1.42)
Allam et al. (2018) [65] Egypt Case control 80 patients (H. pylori (+)40 And H. pylori (−)40) microscopy of histological sections stained with Giemsa stain Insulin resistance 30.4 24 0.642 (0.525–0.767)
Alshareef et al. (2018) [66] Sudan Case control 166 women (20 GDM + , 146 GDM−) GDM Helicobacter pylori IgG antibodies Insulin resistance 26.5 26.2 2.8 (1.1–7.5)
Refaeli et al. (2018) [67] Case control 147,936 individuals 25–95 years UBT Metabolic syndrome (IDF) 42.8 1.15 (1.10–1.19)
Chen et al. (2019) [68] Taiwan Case control 6024 adults RUT Metabolic syndrome (THPA) 51.6 25.19 1.26 (1.00–1.57)
Chen et al. (2019) [68] Taiwan Case control 6024 adults DM RUT Insulin resistance 51.6 25.19 1.59 (1.17–2.17)
Lim et al. (2019) [69] South Korea Case control 15,195 subjects (H. pylori (+)6569 And H. pylori (−)8626) Serum HP immunoglobulin G antibody (anti-HP IgG) Metabolic syndrome (NCEP) 50.7 23.5 1.19 (1.09–1.31)
Yu et al. (2019) [70] China Case Control 5884 participants C-UBT for the detection of H. pylori Metabolic syndrome (IDF) 50.9 26.8 1.21 (1.02–1.36)

OR: odds ratio; RR: risk ratio; HP: Helicobacter pylori; NIDDM: Non-insulin-dependent diabetes mellitus; RUT: rapid urease test; UBT: urea breath test; GDM: gestational diabetes mellitus; NCEP: National Cholesterol Education Program; IDF: International Diabetes Federation; IDDM: Insulin-dependent diabetes mellitus; THPA: The Taiwan Health Promotion Administration of the Ministry of Health and Welfare; CI: confidence interval; BMI: body mass index