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Table 1 Characteristics of studies that evaluated the modification effects of TCF7L2 on the lifestyle factors and glycemic parameters

From: Effect of TCF7L2 on the relationship between lifestyle factors and glycemic parameters: a systematic review

Reference

Study type

Country (study name)

study population

Intervention in trial or lifestyle variables in observational studies

Measurement

Glycemic parameters

Mean of BMI at baseline

Mean of age at baseline

Genotype

Dietary variables

  Pilgaard et al., 2009 [41]

Meal test trial

Denmark

47 young healthy men with glucose-tolerant

Standardized meals that served at 15 min (breakfast), 3 h and 15 min (lunch), 9 h (dinner), and 12 h and 30 min (sandwich), and a standardized light exercise on a bicycle was performed at 2 and 5 h

24 h profiles

glucose, insulin

23.8 in CC and 22.7 in CT/TT

18 to 23 years

rs7903146

  Gjesing et al., 2011 [38]

Meal test trial

Denmark (Inter99 population-based study)

Thirty-one glucose tolerant individuals with TT genotype and 31 age- and BMI matched individual with CC genotype

A test meal consisting of 50 g white bread, 50 g black bread, 10 g butter, 40 g cheese, 20 g sugar-free jam and 200 ml milk (34% fat, 47% carbohydrate, 19% protein)

20, 10 and 0 min before and 15, 30, 45, 60, 75, 90, 105, 120, 135, 150, 180, 210 and 240 min after ingestion of the meal

Plasma glucose, serum Insulin

26.3 in CC and 25.7 in TT

53.6 in CC and 53.3 in TT

rs7903146

  Perez-Martinez et al., 2012 [29]

Meal test trial

Spain

Eighty-eight healthy male with BMI < 30 kg/m2

Fatty meal (contained 65% of energy as fat, 10% of energy as protein, and 25% of energy as carbohydrates)

Before the meal and every hour until hour 6, and every 2.5 h until hour 11

HOMA-B

24.8 to 25.9 in CC, TT, CT

21.6 to 22.7 in CC, TT, CT

rs7903146

  Daniele et al., 2015 [39]

Meal test trial

Italy (Genetic, physiopathology and evaluation of type 2 diabetes study)

Twenty three individuals with IFG and/or IGT and CT/TT genotype and 13 age-, gender-, and weight-matched individuals with CC genotype

A mixed meal consisting of 75 g of glucose dissolved in water spiked with 1.5 g U-13C6-glucose (CIL), 60 g of cheese, and one boiled egg

5, 15, 30, 60, 90, 120, 150, 180, and 240 min after ingestion of the meal

Glucose peak level, insulin concentration,

peak insulin secretion rate, glucose sensitivity, plasma glucose levels

27.5 in CT/TT and 28.9 in CC

56.4 in CT/TT and 52.6 in CC

rs7901346

  Ferreira et al., 2018 [40]

Meal test trial

Brazil

Thirty subjects with type 2 diabetes and CT/TT genotype and 26 age-, BMI, and diabetes duration matched individuals with CC genotype

500-kcal breakfast comprising 50% carbohydrates, 30% proteins, and 20% fat

at 0, 15, 30, 45, 60, 90, 120, 180, and

240 min after ingestion of meal

Plasma glucose

Serum insulin and levels, HbA1c

29.8 in CT/TT

30.2 in CC

59.6 in CC

57.8 in CT/TT

rs7903146

  Adamska et al., 2018 [42]

Meal test trial

polish (1000PLUS cohort)

59 men who were free from T2DM

A standardized high carbohydrate

meal (450 kcal: 89% from carbohydrate, 11% from protein, 0% from fat)

30, 60, 120, 180 and

240 min after ingestion of meal

Glucose, insulin, HOMA-IR

28.3 in TT, 30.0 in CT and 28.6 in CC

39.2 in TT, 38.6 in CT and 32.0 in CC

Rs7901695, rs7903146, rs4506565

  Justesen et al., 2019 [10]

Meal test trial

Denmark

40 healthy men with low birth weight and

age-matched controls

with normal birth weight

subjects

5-day high fat overfeeding diet (50% excess energy, 60% of energy from fat)

and weight maintaining 3-day control diet (35%of energy from fat)

5-day after intervention and 3-day after control diet

hepatic glucose production, peripheral insulin sensitivity, insulin stimulated glucose disposal rate, hepatic insulin resistance index, first phase insulin response

23.4 in normal birth weight and 24.8 in low birth weight

(Not reported by genotype)

24 y

(Not report by genotype)

rs7903146

  Cauchi et al., 2008 [32]

RCT

Seven European countries: United Kingdom (England), The Netherlands, France (two centers), Spain, Czech Republic, Sweden and Denmark

Six hundred and sixty-two individuals with normal glucose tolerance and obesity

Two low calorie diets:

Low-fat diet (20–25% of total energy from fat, 15% from protein and 60–65% from carbohydrate)

High-fat diet (40–45% of total energy from fat, 15% from protein and 40–45% from carbohydrate)

10-week

glucose, Insulin, HOMA-IR, HOMA-β

35.7 in CC, 35.2 in CT, 35.2 in TT

20–50 year

(did not report based on genotype)

rs7903146

  Grau et al., 2010 [28]

RCT

Seven European countries: United Kingdom (England), The Netherlands, France (two centers), Spain, Czech Republic, Sweden and Denmark (NUGENOB study)

Six hundred and sixty-two individuals with obesity

Two low calorie diets:

Low fat diet (20–25% of total energy from fat, 15% from protein, and 60–65% from carbohydrate)

High fat diet (40–45% of total energy from fat, 15% from protein, and 40–45% from carbohydrate)

10 week

Fasting plasma glucose, fasting serum insulin, HOMA-IR, HOMA-B

34.4 to 36.7 in CC, CT and TT genotype in High fat and Low fat interventions groups

Not report

rs7903146

  Perez-Martinez et al., 2012 [29]

RCT

Spain & Poland (LIPGENE study)

Study 1) One hundred and seventeen individuals with metabolic syndrome

Study 2) Twenty elderly with non-diabetes

Study 1) Four isoenergetic diets which differed in fat quantity and quality

A high-fat,saturated fatty acids-rich diet

A high-fat, monounsaturated fatty acids-rich diet

The other 2 diets were low fat, high carbohydrate diets

Study 2) Three dietary intervention

A Mediterranean diet supplemented with coenzyme Q

Mediterranean diet not supplemented with coenzyme Q

A Western diet rich in SFA

Study 1) 12 weeks

Study 2) 4-week

HOMA-B

study 1) 34.7 in CT/TT and 34.5 in CC

study 2) 30.1 in CT/TT and 33.1 CC

1) 55.6 in CT/TT and 54.2 in CC

2) 68.4 in CT/TT and 67.5 CC

rs7903146

  Guevara-Cruz et al., 2012 [44]

RCT

Mexico

Thirty-two

individuals with metabolic syndrome

Two low calorie diet:

Mixture of dehydrated nopal (7 g) equivalent to 100 g of nopal, 4 g of chia seeds, 22 g of oats, 32 g of soybean protein, 0.02 g of sweetener (Splenda), and 1 g flavoring;

30 g of calcium caseinate, 30 g of maltodextrin, 0.02 g sweetener, and 1 g flavoring

2 month

Glucose and insulin

31.4 in intervention group and 32.6 in control group

Not reported

TCF7L2 C/T

  López-Ortiz et al., 2016 [43]

RCT

Mexico

Seventy-four subjects with type 2 diabetes

Two high fiber diets:

Nopal tortillas (equivalent to 6·2 g of fiber)

Diet including three slices of wheat bread (equivalent to 5.5 g of fiber)

8 week

Glucose, HBA1c, insulin, HOMA-IR and HOMA-B

31 to 31.3 in both rs7903146 and rs12255372 genotype variants

51 y

rs7903146 rs12255372

  Rezazadeh et al., 2018 [45]

RCT

Iran

Fifty six women with metabolic syndrome

Four tablets of artichoke leaf extract (ALE) supplementation

Four placebo per day

12 weeks

FBS, Insulin, HOMA_IR, Quantitative sensitivity check index (QUICKI)

among TT allele 34.7 in ALE group and 32.4 in placebo group; among C allele 36.6 in ALE group and 33.0 in placebo group

37.8 in ALE group and 39.0 in placebo group

rs7903146

  Ebrahimi-Mameghani et al., 2018 [49]

RCT

Iran

Eighty women with metabolic syndrome

1800 mg/d of artichoke leaf extract (ALE) as four tablets

1800 mg/d of placebo as four tablets

12 weeks

FBS, insulin, HOMA-IR

35.3 in ALE and 33.3 in placebo groups

38.7 in ALE and 39.1 in placebo

rs7903146

  Florez et al., 2006 [33]

RCT

USA (Diabetes Prevention Program)

3548 individuals with IGT and BMI ≥ 24 kg/m2

Intensive lifestyle modification

Standard care plus metformin,

Standard care plus placebo

1 year

insulin secretion, insulin sensitivity

33.6 to 34.2 in GG, GT and TT in rs1225372

33.1 to 34.4 in CC, CT, and TT in rs7903146

50.5 to 51.3 in GG, GT and TT in rs1225372

50.6 to 51.7 in CC, CT, and TT in rs7903146

rs7903146

rs12255372

  Reinehr et al., 2008 [26]

RCT

Germany (Obeldicks intervention program)

236 children with overweight

Intervention: physical exercise, nutrition education and behavior therapy

Controls: without any intervention

1 year

Glucose, insulin, HOMA-IR, HOMA-β, QUICKI

BMI-SDS: 2.42 in CC, 2.52 in CT, 2.55 in TT

10.8 in CC, 10.6 in CT, 10.9 in TT

rs7903146

  Bo et al., 2009 [46]

RCT

Italy (Asti)

335 individuals with metabolic syndrome (139 were carrier of the CC variant and 196 were varies of the CT/TT variants)

Intervention: A lifestyle intervention program with general recommendations carried out by trained professionals

Control: Standard, unstructured information given by the family physician

1-y and 4-y

Glucose, Insulin, HOMA-IR and HOMA-B, IFG

Intervention group:

30.1 in CC variant and 28.8 in CT variant and 31.0 in TT variants

Control group: 29.8 in CC variant, 30.1 in CT variant and 29.2 in TT variant

Intervention group:

55.5 in CC variant, 55.5 in CT variant and 56.8 in TT variants

Control group: 56.3 in CC variant, 55.2 in CT variant and 55.8 in TT variant

Rs7903146

  Haupt et al., 2010 [47]

RCT

Germany (Tuebingen Lifestyle Intervention Program)

309 individuals who were at risk of type 2 diabetes

Exercise and dietary intervention

The participants aimed at a weight loss of at least 5%, a reduction of caloric intake from fat of < 30% and an increase of fiber intake to at least 15 g/1000 kcal, and reduction of DFA < 10%. Individual were asked to perform at least 3 h of moderate exercise per week

9 month

Fasting glucose, glucose 120 min, insulin sensitivity,

30.3 in CC and 30.0 in CT/TT

46 in CC and 47 in Ct/TT

Rs7903146, rs12255372

  McCaffery et al., 2011 [34]

RCT

USA (Diabetes prevention program)

2994 individuals that were at risk of progression to type 2 diabetes

lifestyle intervention aiming at ≥ 7% weight loss and ≥ 150 min of physical activity per week

Metformin 850 mg twice daily

Placebo group

Median 2.5 year of follow-up

Insulin

34.3 in placebo, 34.0 in metformin, 34.0 in lifestyle group

50.5 y in placebo, 51.0 y in metformin, 50.7 in lifestyle group

rs7903146

  Mattei et al., 2012 [27]

RCT

USA (The Preventing overweight using novel dietary strategies)

591 individuals with overweight and obese

Two low calorie diet

Low fat (2 diets with an aim of 20% from total energy)

High fat (2 diets with an aim of 40% from total energy)

6 month and 2 year

Glucose, insulin,

32.5 to 32.7 in rs7903146 variant and 32.1 to 32.8 in rs12255372 variant

51.6 to 52.5 in rs7903146 variant and 51.4 to 52.6 in rs12255372 variant

rs12255372

rs7903146

  Walker et al., 2012 [48]

RCT

UK (RISCK study)

354 individuals who were at risk of

cardiometabolic risk factors

Four isoenergetic diets:

High monounsaturated fatty acids (MUFA)/high glycemic index (GI)

High MUFA/low GI

Low fat /high GI

LF/low GI

24 weeks

AIRg (actue insulin secretion), deposition index, insulin sensitivity

28.7 for total population

53.5 for total population

rs7901695

  Ruchat et al., 2009 [51]

Cross-sectional

Canada (Quebec Family Study)

669 adults with non-diabetes

Dietary fatty acid

(3-day (2 week days, 1

weekend day))

––-

Fasting glucose, HOMA-IR, HOMA-B, insulin secretion, Two hour glucose,

The Cederholm index (adjusted for age and sex)

27.7 in total population

40.5 in total population

rs12573128

rs10128255

rs7903146

rs17685538

rs11196205

rs11196203

rs4918789

rs3750804

rs3750805

rs176632

rs11594610

rs1885510

rs7901695

  Nettleton et al., 2010 [52]

cross-sectional

Europe (14 cohort study)

48,000 participants with non-diabetes

Whole grain (FFQ (11 cohorts)

a lifestyle questionnaire

(1 cohort)

multiple

24-h recalls (1 cohort)

7-day dietary diaries (1 cohort))

–-

Fasting glucose and fasting insulin (adjusted for Age, gender, energy intake and center)

From 20.0 to 29.7 in different cohort studies

From 11.2 to 76.4 in different cohort studies

Rs4506565

  Delgado-Lista et al., 2011 [53]

cross-sectional

Ireland, UK, Norway, France, The Netherlands, Spain,

Poland and Sweden (LIPGENE dietary intervention study)

450 participants with non-diabetes

Plasma saturated fatty acids concentration

–-

insulin, glucose, HOMA-IR, HOMA-β, acute insulin response to glucose (AIRg)

32.6 in CC, 32.3 in CT, 32.5 in TT

53.7 in CC, 54.9 in CT, 55.3 in TT

rs12255372

rs4506565

rs7901695

rs7903146

rs17685538

rs290481

rs11196224

rs3814573

rs6585196

rs1885510

  Phillips et al., 2012 [61]

Prospective case control study

with 7.5 year follow-up

France (LIPGENE)

964 participants (participants with Metabolic syndrome who were matched participants with non-metabolic syndrome)

Dietary fatty acid (food frequency questionnaire)

–-

Fasting glucose, insulin, HOMA-IR, QUICKI (adjusted for Age, gender, BMI, smoking status, energy intake, physical activity and medication use)

25.0 to 26.2 in CC, CT and TT

57.9 to 58.3 in CC, CT and TT

rs7903146

  Hindy et al., 2012 [54]

Cross sectional

Sweden (The Malmö Diet and Cancer Study (

MDCS))

5216 participants with non-diabetes

Dietary fiber (a 7-day menu book where lunch, dinner

meals and cold beverages, including alcohol, were recorded;

and a dietary 168-item questionnaire)

–-

HBA1c, fasting glucose

25.5 to 25.7 in CC, CT and TT (Age, gender, BMI, total energy intake, season and method)

58.0 to 58.1 in CC, CT and TT

Rs7903146

  Corella et al., 2013 [55]

cross-sectional

Spain (the PREvención con DIetaMEDiterr_anea

(PREDIMED))

7018 patients with type 2 diabetes or participants at high risk of cardiovascular risk factors

Mediterranean dietary pattern

(food frequency questionnaire)

–-

Fasting glucose concentrations (adjusted for age, sex, BMI, type 2 diabetes, total energy intake, alcohol consumption, smoking, physical activity, medication)

30.0 in total population

67.0 in total population

rs7903146

  Ouhaibi-Djellouli et al., 2014 [56]

Cross sectional

Algeria (Insulino-résistance à Oran (ISOR))

720 participants (both diabetic and non-diabetes participants)

Milk and dessert (food frequency questionnaire)

–-

Glucose, insulin, HOMA-IR, HOMA-B (adjusted for age, gender, smoking status, physical activity, BMI)

26.4 in CC, 25.7 in CT, 24.9 in TT

42.8 in non-T2D and 52.0 in T2D subjects

rs7903146

  Lu et al., 2017 [57]

cross sectional

USA

120 patients with non-diabetes

Free fatty acid concentration

––

HOMA-IR (adjusted for Age, gender, BMI)

27.4 in CC and 27.3 in TT

41 in CC and 42 in TT

rs7903146

  Bodhini et al., 2017 [58]

Cross sectional

India (Chennai Urban Rural

Epidemiology Study (CURES))

1681 participants (821 normal glucose tolerance and 861 participants with diabetes)

Macronutrient and dietary fiber (food frequency questionnaire)

–-

Fasting plasma glucose (adjusted for age, gender, BMI, energy intake)

23.6 in normal glucose tolerant and 25.3 in type 2 diabetes participants

41.3 in normal glucose tolerant and 50.5 in type 2 diabetes participants

rs12255372

rs7903146

  Barabash et al., 2020 [59]

Cross sectional

Spain (St Carlos GDM prevention study)

874 pregnant women

Mediterranean dietary pattern (food frequency questionnaire)

––

Fasting blood glucose (Ethnicity, age, parity, family history of diabetes and BMI)

23.3 to 24.3 based on adherence to Mediterranean diet

31.2 to 33.9 based on adherence to Mediterranean diet

rs7903146

  Bauer et al., 2021 [60]

Cross sectional

Poland

810 subjects with non-diabetes

Macronutrient intake (3-day food diaries)

––-

Fasting plasma glucose, Insulin concentrations, HbA1c, HOMA-IR, HOMA-β (adjusted for Age, gender, BMI, energy intake, physical activity levels)

28.7 in TT, 28.2 in CT and 28.3 in CC

40.9 in TT, 40.9 in CT, and 40.8 in CC

rs7901695

Physical activity

  Ruchat et al., 2010 [50]

Trial

United States and Canada ( HEealth, Risk factors, exercise Training, AND Genetics (HERITAGE))

481 participants without of chronic diseases

Exercise

Program (three times per week)

20-week

Fasting glucose,

Fasting insulin

insulin sensitivity index, acute insulin response to glucose,

disposition index, glucose effectiveness

25.8 kg/m2

35.9 y

rs4903146

  Alibegovic et al., 2010 [11]

Trial

Denmark

38 healthy young Caucasian men

Bed rest

9 days

Insulin, glucose, Intravenous glucose tolerance test (β-cell test)

first-phase insulin response,, second-phase

insulin secretion

23.0 in TT/CT and 24.4 in CC

25.6 in TT/CT and 25.2 in CC

rs7903146

  Brito et al., 2009 [62]

Cohort

Sweden (Malmo¨ Preventive Project)

16,003 individuals at high risk of developing chronic disease

Physical activity that assessed using computer-based questionnaire

16 years’ mean follow-up time

Impaired glucose regulation, 2-h plasma glucose

24.6 in physical inactive and 24.2 in physical active participants

44.7 in physical inactive and 45.7 in physical active participants

rs7903146

  Scott et al., 2012 [30]

All data were cross-sectional except for atherosclerosis Risk in Communities Study

(ARIC) where PA data were available at the visit 3 years before 2-h glucose measurement

USA, Finland, Switzerland, UK, Sweden, Denmark, Europe, German, British (Meta-analyses of glucose and insulin related traits consortium (MAGIC))

48,362 individuals with Non-diabetes and BMI ≥ 18.5 kg/m2

Physical activity that assessed using Different questionnaire

––-

2-h glucose

Not reported

Not reported

Rs12243326

  Jung et al., 2016 [64]

Cross sectional

Korean (Genomics and Randomized Trials Network (GARNET))

1027 postmenopausal women

Physical activity that assessed using questionnaire, dietary intake by FFQ

–-

Insulin, fasting glucose, HOMA-IR

Not reported

63 to 65 in obese and non-obese women, respectively

Rs4506565

Smoking status

  Wu et al., 2020 [31]

Cohort

Europe and Africa (The Atherosclerosis Risk in Communities Study (ARIC), the Coronary Artery Risk Development

in Young Adults Study (CARDIA), the Cardiovascular Health Study (CHS), the Framingham

Heart Study (FHS), and the Multi-Ethnic Study of Atherosclerosis (MESA))

97,773 participants with non-diabetes

Smoking status:

Current or former smokers at baseline (ever smokers)

No current or past smoking history (never smokers)

Not reported

Fasting glucose

23.9 to 40.8 in different cohorts

25.6 to 76.9 in different cohorts

rs4132670

rs12243326

  Lin, 2020 [63]

Cross sectional

Taiwan

25,460 participants aged 30–70 year

Smoking status:

Smokers

Nonsmokers

––

Fasting glucose

HbA1c

25.4 in smokers and 24.2 in nonsmokers

46.4 in smokers and 49.2 in nonsmokers

rs4132670

rs12243326