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Table 1 General Characteristics of included studies

From: Gut microbiota in patients with obesity and metabolic disorders — a systematic review

First author, year

Country

Ethnicity

Disease

Sample size (case)

Sample size (control)

Age (years)

Sample

Sequencing Method

Definition of obesity

Definition of metabolic diseases

Andoh, 2016 [18]

Japan

Asian

OB

10

10

31–58

Stool

16s rRNA (V3–V4)

BMI ≥ 35.7 kg/m2

NA

Bai, 2019 [19]

USA

Caucasian

OB

43

224

7–18

Stool

16s rRNA (V4)

BMI > 95th percentile

NA

Chen, 2020 [20]

China

Asian

OB

28

23

6–11

Stool

16s rRNA (V4)

Body mass index cut-offs for overweight and obesity in Chinese children and adolescents aged 2–18 years*

NA

Da Silva, 2020 [21]

Trinidad

Asian/Black

OB

21

30

6–14

Stool

16s rRNA (not specified)

> 97th percentile

NA

Gao, 2018 [22]

China

Asian

OB

167(OB: n = 145;OW: n = 22)

25

NW:25.4 ± 3.2; OW:30.1 ± 11.2; OB:29.2 ± 11.4

Stool

16s rRNA (V4)

NA

NA

Gao, 2018 [23]

China

Asian

OB

39

38

OB: 6.8 ± 1.6; NW: 6.0 ± 2.7

Stool

16S rRNA (V3–V4)

BMI ≥ 30 kg/m2

NA

Haro, 2016 [24]

Spain

Caucasian

OB

49

26

Men: 61.15 ± 1.27; Women: 60.31 ± 1.40

Stool

16s rRNA (V4)

BMI ≥ 30 kg/m2

NA

Houttu, 2018 [25]

Finland

Caucasian

OB

47

52

30 ± 5

Stool

16s rRNA (not specified)

BMI ≥ 30 kg/m2

NA

Hu, 2015 [26]

Korea

Asian

OB

67

67

13–16

Stool

16s rRNA (V1–V3)

BMI ≥30 kg/m2 or ≥ 99th BMI percentile

NA

Kaplan, 2019 [27]

USA

Caucasian

OB

294

293

18–74

Stool

16s rRNA (V4)

BMI ≥ 30 kg/m2

NA

Liu, 2017 [28]

China

Asian

OB

72

79

OB:23.6 ± 3.7; NW:23.2 ± 1.8

Stool

Metagenomics/16S rRNA (V3–V4)

BMI ≥ 30 kg/m2

NA

Lopez-Contreras, 2018 [29]

Mexico

Hispanic/Latino

OB

71

67

6–12

Stool

16s rRNA (V4)

BMI ≥ 95th percentile

NA

Lv, 2019 [30]

China

Asian

OB

9

19

18–27

Stool

16S rRNA (V3–V4)

OW, BMI ≥ 24 kg/m2 OB, BMI ≥ 28 kg/m2

NA

Mendez-Salazar, 2018 [31]

Mexico

Hispanic/Latino

OB

12

12

9–11

Stool

16s rRNA (V3–V4)

BMI z-score≥ +2 standard deviations

NA

Nardelli, 2020 [32]

Italy

Caucasian

OB

19

16

20–80

Duodenal biopsies

16s rRNA V4–V6

BMI ≥ 30 kg/m2

NA

Blasco, 2017 [33]

Spain

Caucasian

OB

14

13

30–65

Stool

Metagenomics

BMI ≥ 30 kg/m2

NA

Davis, 2017 [34]

UK

Caucasian

OB

54 (OB/OW:n = 27)

27

19–70

Stool

Metagenomics/16s rRNA (V4)

NA

NA

Dominianni, 2015 [35]

USA

Caucasian

OB

11

82

30–83

Stool

16S rRNA (V3–V4)

BMI ≥ 25 kg/m2

NA

Escobar, 2015 [36]

Colombia

Hispanic/Latino

OB

NA

30

21–60

Stool

16s rRNA (V1–V3)

BMI ≥ 30.0 kg/m2

NA

Kasai, 2015 [37]

Japan

Asian

OB

33

23

Non-obese:45.6 ± 9.6; Obese:54.4 ± 8.2

Stool

16s rRNA (V3–V4)

BMI ≥ 25kg/m2

NA

Nirmalkar, 2018 [38]

Mexico

Hispanic/Latino

OB

96

76

6–18

Stool

16s rRNA V3

BMI ≥ 95th percentile

NA

Ottosson, 2018 [39]

Sweden

Caucasian

OB

NA

NA

> 18

Stool

16s rRNA (V1–V3)

BMI > 30.0 kg/m2

NA

Peters, 2018 [40]

USA

Caucasian

OB

388

211

18–86

Stool

16s rRNA V4

BMI ≥ 30 kg/m2

NA

Ppatil, 2012 [41]

India

Asian

OB

5

5

21–62

Stool

16s rRNA (not specified)

BMI: 25–53 kg/m2

NA

Rahat-Rozenbloom,2014 [42]

Canada

Caucasian

OB

11

11

> 17

Stool

16s rRNA (V6)

BMI > 25 kg/m2

NA

Riva, 2017 [43]

Italy

Caucasian

OB

42

36

9–16

Stool

16s rRNA V3–V4

BMI z-score

NA

Vieira-Silva, 2020 [44]

Belgium

Caucasian

OB

474

414

18–76

Stool

Metagenomics

BMI ≥ 30 kg/m2

NA

Ville, 2020 [45]

USA

Hispanic/Latino

OB

6

39

0.5–1

Stool

16s rRNA V4

BMI ≥ 95th percentile

NA

Yasir, 2015 [46]

France/Saudi Arabia

Caucasian/Asian

OB

21

25

≥ 18

Stool

16s rRNA (V3–V4)

BMI ≥ 30.0 kg/m2

NA

Yun, 2017 [47]

Korea

Asian

OB

745 (OB:n = 419; OW: n = 326)

529

> 18

Stool

16s rRNA V3–V4

BMI ≥ 25 kg/m2

NA

Zacarias, 2018 [48]

Finland

Caucasian

OB

29 (OB: n = 11, OW: n = 18)

25

NW:29.6 ± 4.2; OW:30.4 ± 3.6; OB:29.6 ± 2.3

Stool

16s rRNA V3–V4

BMI≥30 kg/m2

NA

Allin, 2018 [49]

Denmark

Caucasian

T2DM

134

134

55–68

Stool

16s rRNA (V4)

NA

Fasting plasma glucose of 6.1–7.0 mmol/l or HbA1c of 42–48 mmol/mol [6.0–6.5%]

Barengolts, 2018 [50]

USA

Black

T2DM

73

20

35–70

Stool

16s rRNA (V3–V4)

NA

HbA1c of 6.5–7.4%

Leite, 2017 [51]

Brazil

Hispanic/Latino

T2DM

20

22

36–75

Stool

16s rRNA (V3–V4)

NA

Fasting blood glucose levels ≥ 126 mg/dL

Qin, 2012 [52]

China

Asian

T2DM

170

174

25–86

Stool

Metagenomics

NA

NA

Karlsson, 2013 [53]

Sweden

Caucasian

T2DM

102

43

70

Stool

Metagenomics

NA

Glucose metabolism impairment: fasting hyperglycaemia (fasting venous plasma glucose ≥ 6.1 and < 7.0 mmol/L) or IGT (fasting venous plasma glucose <7 mmol/L, ≥ 7.8 and < 11.1 mg/dL 2 h after OGTT) or new onset T2DM (fasting glucose ≥ 7 mmol/L or ≥ 11.1 mmol/L 2 h after OGTT); Arterial hypertension (AH) (systolic/diastolic blood pressure level of 140/90–159/99 mmHg).

Larsen, 2010 [54]

Denmark

Caucasian

T2DM

18

18

31–73

Stool

16s rRNA (V4–V6)

NA

The diabetic group had elevated concentration of plasma glucose as determined by OGTT. Non-diabetic group based on the measurements of baseline glucose and biochemical analysis of blood samples.

Ahmad, 2019 [55]

Pakistan

Asian

T2DM

40

20

25–55

Stool

16s rRNA (V3–V4)

NA

NA

Koo, 2019 [56]

China, Malaysia, and India

Asian

T2DM

22

13

22–70

Stool

16s rRNA (V3–V6)

waist circumference ≥ 90 cm in men and ≥ 80 cm in women

DM were excluded by the absence of impaired glucose tolerance on fasting blood glucose.

Sroka-oleksiak, 2020 [57]

Poland

Caucasian

T2DM

OB: n = 17;OB+T2DM: n = 22)

27

20–70

Duodenal biopsies

16s rRNA (V3–V4)

BMI >35 kg/m2

NA

Thingholm, 2019 [58]

Germany

Caucasian

T2DM

OB: n = 494;OB+T2DM: n = 153)

633

21–78

Stool

Metagenomics/16s rRNA (V1–V2)

BMI > 30.0 kg/m2

Fasting glucose level ≥ 125 mg/dl

Zhao, 2019 [59]

China

Asian

NAFLD

OB: n = 18;NAFLD: n = 25)

15

9–17

Stool

Metagenomics

BMI ≥ 95th percentile

NA

Jiang, 2015 [60]

China

Asian

NAFLD

35

30

22–72

Stool

16s rRNA (V3)

NA

Based on evidence of hepatic steatosis via either imaging or histology

Shen, 2017 [61]

Chinese

Asian

NAFLD

25

22

> 18

Stool

16s rRNA (V3–V5)

NA

NAFLD can be diagnosed by the presence of three findings: (i) the histological findings of liver biopsy are in accord with the pathological diagnostic criteria of fatty liver disease. (ii) there is no history of alcohol drinking habit or the ethanol intake per week was less than 140 g in men (70 g in women) in the past 12 months; (iii) specific diseases that could lead to steatosis, such as viral hepatitis, drug-induced liver disease, total parenteral nutrition, Wilson’s disease, and autoimmune liver disease, can be excluded.

Sobhonslidsuk, 2018 [62]

Thailand

Asian

NASH

16

8

NASH:59.8 ± 9.6; control:43.4 ± 6.8

Stool

16s rRNA (V3–V4)

NA

NAFLD activity score ≥ 5

Wang, 2016 [63]

China

Asian

NAFLD

43

83

33–61

Stool

16s rRNA (V3)

NA

Evidence of fatty liver upon ultrasonography

Li, 2018 [64]

China

Asian

NAFLD

30

37

18–70

Stool

16s rRNA (V4)

NA

The diagnosis of NAFLD was based on the following criteria: (i) abdominal ultrasonography indicated a fatty liver; (ii) the patient’s alcohol consumption was less than 20 g/day and 10 g/day for male for female.

Nistal, 2019 [65]

Spain

Caucasian

NAFLD

53

20

20–60

Stool

16S rRNA (V3–V4)

NA

An NAFLD diagnosis was established by clinical, analytical criteria (liver function test) and from ultrasonographic data when steatosis was detected.

Yun, 2019 [66]

Korea

Asian

NAFLD

76

192

43.6 ± 8.2

Stool

16s rRNA (V3–V4)

BMI ≥ 25 kg/m2

U/S findings suggestive of fatty liver disease

Michail, 2015 [67]

USA

Caucasian

NAFLD

24

26

13.2 ± 3.8

Stool

16s rRNA (not specified)

BMI ≥ 95th percentile

Ultrasound findings and elevated transaminases suggestive of NAFLD

Zhu, 2013 [68]

USA

Caucasian

NASH

47

16

< 18

Stool

16s rRNA (not specified)

BMI ≥ 95th percentile

NAFLD activity score≥ 5

Chavez-Carbaja, 2019 [69]

Mexico

Hispanic/Latino

MS

42

25

18–59

Stool

16s rRNA (V4)

 

At least three of the following issues: waist greater than 102 cm in males or 82 cm in females, triglycerides levels greater or equal to 150 mg/dl, HDL cholesterol levels less than 40 mg/dl in males or less than 50 mg/dl in females, blood pressure greater or equal to 130/85 mmHg and a fasting blood glucose level higher or equal to 100 mg/dl.

De La Cuesta-Zuluaga, 2018 [70]

Colombia

Hispanic/Latino

MS

291

151

18–62

Stool

16s rRNA (V4)

BMI ≥ 30.0 kg/m2

At least two of the following conditions: systolic/diastolic blood pressure 130/85 mm Hg or consumption of antihypertensive medication; fasting triglycerides 150 mg/dl; HDL ≤ 40 mg /dl (men), ≤ 50 mg/dl (women) or consumption of lipid-lowering medication; fasting glucose 100 mg/dl or consumption of antidiabetic medication; HOMA-IR 43, and hs-CRP 43 mg L−1.

Gallardo-Becerra, 2020 [71]

Mexico

Hispanic/Latino

MS

17

10

7–10

Stool

16s rRNA (V4)

BMI> 95th percentile

At least two of the following metabolic traits: (1) triglycerides > 1.1 mmol/L (100 mg/dL); (2) HDL cholesterol < 1.3 mmol/L (50 mg/dL); (3) glucose > 6.1 mmol/L (110 mg/dL); (4) systolic blood pressure > 90th percentile for gender, age, and height.

Gozd-Barszczewska, 2017 [72]

Poland

Caucasian

MS

15

5

45–65

Stool

16s rRNA (V3–V5)

BMI ≥ 30.0 kg/m2

Lipid profile was assessed based on ESC/EAS Guidelines

Kashtanova, 2018 [73]

Russia

Caucasian

MS

57

35

25–76

Stool

16s rRNA (V3–V4)

BMI ≥ 30 kg/m2 and/or waist circumference ≥ 94 cm for men and ≥ 80 cm for women

Glucose metabolism impairment: fasting hyperglycaemia (fasting venous plasma glucose ≥ 6.1 and < 7.0 mmol/L) or IGT (fasting venous plasma glucose < 7 mmol/L, ≥7.8 and < 11.1 mg/dL 2 h after OGTT) or new onset T2DM (fasting glucose ≥ 7 mmol/L or ≥11.1 mmol/L 2 h after OGTT); Arterial hypertension (AH) (systolic/diastolic blood pressure level of 140/90–159/99 mmHg).

Lippert, 2017 [74]

Austria

Caucasian

MS

12

8

58–71

Stool

16s rRNA (V1–V3)

NA

At least two of the following conditions: systolic/diastolic blood pressure 130/85 mm Hg or consumption of antihypertensive medication; fasting triglycerides 150 mg/dl; HDL ≤ 40 mg/dl (men),≤ 50 mg/dl (women), or consumption of lipid-lowering medication; fasting glucose 100 mg/dl or consumption of antidiabetic medication; HOMA-IR 43, and hs-CRP 43 mg L−1.

Feinn, 2020 [75]

Italy

Caucasian

NAFLD

44

29

NAFLD: 13.3 ± 3.2; OB without NAFLD: 12.9 ± 2.8

Stool

16s rRNA (V4)

BMI ≥ 95th percentile

Hepatic fat fraction ≥ 5.5%

Li, 2021 [76]

China

Asian

OB

3

3

OB:34.33 ± 0.47; NW:25.67 ± 1.25

Stool

16s rRNA (V3–V4)

BMI≥ 30.0 kg/m2

NA

Yuan, 2021 [77]

China

Asian

MS

65

21

5–15

Stool

16s rRNA (V3–V4)

NA

The presence of at least one of the following metabolic traits: (1) FPG ≥ 5.6 mmol/L; (2) systolic blood pressure ≥ 90th percentile for gender and age; (3) fasting HDL-C < 1.03 mmol/L; and (4) fasting TG ≥ 1.7 mmol/L.

  1. OW overweight, OB obesity, T2DM diabetes mellitus type 2, NAFLD non-alcoholic fatty liver disease, MS metabolic syndrome, NASH non-alcoholic steatohepatitis, NA not appliable, IGT impaired glucose tolerance
  2. *Refers to a standard developed by the Department of Growth and Development, Capital Institution of Pediatrics, China, to define children of obesity