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) | Â | 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) | Â | 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) | |