Literature DB >> 30547769

Prevalence and risk factors of gestational diabetes mellitus in Asia: a systematic review and meta-analysis.

Kai Wei Lee1, Siew Mooi Ching2,3, Vasudevan Ramachandran4, Anne Yee5, Fan Kee Hoo6, Yook Chin Chia7, Wan Aliaa Wan Sulaiman6, Subapriya Suppiah8, Mohd Hazmi Mohamed9, Sajesh K Veettil10.   

Abstract

BACKGROUND: Gestational diabetes mellitus (GDM) is a of the major public health issues in Asia. The present study aimed to determine the prevalence of, and risk factors for GDM in Asia via a systematic review and meta-analysis.
METHODS: We systematically searched PubMed, Ovid, Scopus and ScienceDirect for observational studies in Asia from inception to August 2017. We selected cross sectional studies reporting the prevalence and risk factors for GDM. A random effects model was used to estimate the pooled prevalence of GDM and odds ratio (OR) with 95% confidence interval (CI).
RESULTS: Eighty-four studies with STROBE score ≥ 14 were included in our analysis. The pooled prevalence of GDM in Asia was 11.5% (95% CI 10.9-12.1). There was considerable heterogeneity (I2 > 95%) in the prevalence of GDM in Asia, which is likely due to differences in diagnostic criteria, screening methods and study setting. Meta-analysis demonstrated that the risk factors of GDM include history of previous GDM (OR 8.42, 95% CI 5.35-13.23); macrosomia (OR 4.41, 95% CI 3.09-6.31); and congenital anomalies (OR 4.25, 95% CI 1.52-11.88). Other risk factors include a BMI ≥25 kg/m2 (OR 3.27, 95% CI 2.81-3.80); pregnancy-induced hypertension (OR 3.20, 95% CI 2.19-4.68); family history of diabetes (OR 2.77, 2.22-3.47); history of stillbirth (OR 2.39, 95% CI 1.68-3.40); polycystic ovary syndrome (OR 2.33, 95% CI1.72-3.17); history of abortion (OR 2.25, 95% CI 1.54-3.29); age ≥ 25 (OR 2.17, 95% CI 1.96-2.41); multiparity ≥2 (OR 1.37, 95% CI 1.24-1.52); and history of preterm delivery (OR 1.93, 95% CI 1.21-3.07).
CONCLUSION: We found a high prevalence of GDM among the Asian population. Asian women with common risk factors especially among those with history of previous GDM, congenital anomalies or macrosomia should receive additional attention from physician as high-risk cases for GDM in pregnancy. TRIAL REGISTRATION: PROSPERO (2017: CRD42017070104 ).

Entities:  

Keywords:  Asia; meta-analysis; Gestational diabetes mellitus; Prevalence; Risk factors

Mesh:

Year:  2018        PMID: 30547769      PMCID: PMC6295048          DOI: 10.1186/s12884-018-2131-4

Source DB:  PubMed          Journal:  BMC Pregnancy Childbirth        ISSN: 1471-2393            Impact factor:   3.007


Background

Gestational diabetes mellitus (GDM) is defined as any degree of dysglycaemia that occurs for the first time or is first detected during pregnancy [1, 2]. It has become a global public health burden [3]. GDM is one of the leading causes of mortality and morbidity for both the mother and the infant worldwide [4-13]. Mothers with GDM are at risk of developing gestational hypertension, preeclampsia and caesarean section [7, 14–16]. Apart from this, women with a history of GDM are also at significantly higher risk of developing subsequent type 2 diabetes mellitus (T2DM) and cardiovascular diseases [17, 18]. Babies born from GDM women are at risk of being macrosomic, may suffer from more congenital abnormalities and have a greater propensity of developing neonatal hypoglycaemia, and T2DM later in life [7, 19–24]. As such, it is important for healthcare policy makers to understand the burden of GDM for early detection and further intervention. Up to now, there has been no gold standard criterion for the diagnosis. Different countries use different diagnostic criteria in determining its prevalence (Appendix 1). Based on these criteria, the estimated prevalence of GDM worldwide is 7.0% [25]. Prevalence varies from 5.4% in Europe [26] to 14.0% Africa [27]. In Asia, the prevalence of GDM ranges from 0.7 to 51.0% [28-30]. This vast disparity in prevalence rates may be due to differences in ethnicity [28, 30], diagnostic criteria [31-33], screening strategies [29, 34], and population characteristics [35, 36]. Diagnostic criteria have been developed by numerous associations such as: O′ Sullivan; American Diabetes Association (ADA); Australian Diabetes in Pregnancy Society (ADIPS); Carpenter-Coustan (CC); International Association of the Diabetes and Pregnancy Study Groups (IADPSG); International Classification of Diseases (ICD); European Association for the Study of Diabetes (EASD); The American College of Obstetricians and Gynecologists (ACOG); Diabetes in Pregnancy Study group of India (DIPSI); Japan Diabetes Society (JDS); National Diabetes Data Group (NDDG); and World Health Organization (WHO); Canadian Diabetes Association (CDA); and so on. These diagnostic criteria vary in terms of screening methods and screening threshold. Diagnosis of GDM primarily depends on the results of an oral glucose tolerance test (OGTT). The OGTT can be carried out via a 75-g two-hour test or a 100-g three-hour OGTT. The 75-g two-hour OGTT is a one-step approach, while the 100-g three-hour OGTT is usually implemented as the second step of a two-step approach. A diagnosis of GDM is made when one glucose value is elevated for the 75-g two-hour OGTT. Despite the presence of multiple diagnostic criteria to diagnose GDM, to date, there has been a degree of uncertainty around the optimum thresholds for a positive test [25, 37–59]. The thresholds for an elevated fasting glucose range from 92 mg/dl (5.1 mmol/L) to 140 mg/dl (7.8 mmol/L) [41, 44] while values for the two hours after OGTT range from 7.8 to 11.1 mmol/L [44, 46]. The IADPSG criteria is the most commonly used threshold for defining elevated values recently following the Hyperglycemia and Adverse Pregnancy Outcome (HAPO) study [60]. Overall, the 75-g two-hour test is more practical and convenient compared with the 100-g three-hour test. Furthermore, it appears to be more sensitive in predicting the pregnancy’s complication like gestational hypertension, preeclampsia and macrosomia than the 100-g three-hour test [61]. The reason for increased sensitivity is mainly that only one elevated glucose value is needed to diagnose GDM in 75-g two-hour test compared to 100-g three-hour test which requires two abnormal glucose values [60]. The thresholds used to define the abnormal values in the 100-g three-hour test have been based on the Carpenter and Coustan, NDDG and O’Sullivan criteria [49-51]. Moreover, the prevalence of GDM is expected to increase over years [62-64], especially in Asia. This is possibly due to increase in maternal age and obesity in Asia [65, 66]. A recent review reported the prevalence of GDM in Eastern and Southeast Asia is 10.1% (95% CI: 6.5–15.7%) [29]. There has been no review on the overall prevalence of GDM in Asia. Therefore, the aim of this meta-analysis is to estimate the prevalence of GDM in a broader scope including the countries across Asia. In addition, we also examine the odds ratio of risk factors for GDM among the Asian populations. The recognition of risk factors of GDM for the Asian population is therefore important to identify women at risk, making an early diagnosis and instituting intensive lifestyle modification and metformin treatment to control blood glucose to reduce the likelihood of problems of GDM, before they become more severe. This may help prevent or ameliorate adverse complications. We therefore conducted a systematic review and meta-analysis to determine the prevalence and factors associated with GDM in Asia.

Methods

The present review was registered with PROSPERO (2017: CRD42017070104) and conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) [67].

Search strategy

Four databases were searched (PubMed, Ovid, Scopus and ScienceDirect) to do the literature search with the following search terms: (prevalence or incidence and/or risk factor) and (gestational diabetes or diabetes in pregnancy or gestational diabetes mellitus) and (Asia). A combination of expanded MeSH term and free-text searches were used as shown in Appendix 2. Then the reference lists of relevant articles were screened for its suitability to be recruited into this review.

Inclusion criteria

Any studies in Asia that reported prevalence and risk factors for GDM and fulfilled the following criteria were entered into the analysis, including the following factors: (1) conducted in Asian countries classified by the United Nations Statistics Division [68]; (2) reported prevalence and risk factors as primary results; (3) English peer review articles published in journals from inception to August 22, 2017; and (4) a sample size no less than 100 subjects. When several publications were actually derived from the same dataset or cohorts, we chose the data from the latest publication or largest cohort only. Similarly, when different screening criteria was used to diagnose GDM, we used the criteria with the highest prevalence for the risk factor calculation. We identified other pertinent studies through reverse-forward citation tracking and reference lists of related review articles.

Study selection

We imported those relevant articles identified through the databases into EndNote programme X5 version and we removed duplicate publications. Two reviewers independently performed the screening using the titles and abstracts to search for potentially eligible articles based on the inclusion and exclusion criteria mentioned above. If there was a lack of information on the prevalence of GDM in the title and/or abstract, the full text was retrieved for further assessment. Discussions were held to resolve any disagreement for a final consensus before reviewing the full text each relevant article.

Quality assessment and data extraction

The checklist Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) was used to assess the quality of searched articles by two independent investigators [69]. The tool consists of 22 items that assess components in observation studies and whenever the information provided was not enough to assist in making judgement for a certain item, we agreed to grade that item with a ‘0’ meaning high risk of bias. Each article’s quality was graded as ‘good’ if STROBE score ≥14/22; or graded as ‘poor’ if STROBE score < 14/22 [69]. In this review, studies with STROBE score ≥ 14 were included in analysis. The scoring result was shown in Appendix 3. One of the reviewers recorded the data from the selected studies into the extraction form using Excel, while the second reviewer verified the accuracy and completeness of the extracted data. The characteristics of the selected studies were extracted as follows: first author, year of publication, year of survey, country, setting, gestational age, screening procedure (one and/or two steps), diagnostic criteria for GDM, sample size, GDM cases, prevalence of GDM, odds ratio, relative risk of certain risk factors. Since we only collected published studies, the outcome measures extracted were gestational diabetes incidence and risk factors in terms of differences of proportion/percent of gestational diabetes in the total subjects examined. No ethics approval was needed in this review as the work consisted of secondary data collection and analysis only.

Data analysis

A random-effects (DerSimonian and Laird method) meta-analysis was used to pool the prevalence and odds ratio (OR) estimated from individual studies and reported with 95% confidence interval (CI). Heterogeneity across studies was assessed using the I2 index (low is < 25%, moderate 25–50%, and high > 50%), indicating the percent of total discrepancy due to studies variation [70]. Subgroup analyses for prevalence were performed by country, diagnostics criteria, screening methods and study setting. For Statistical analysis, StatDirect Statistical Software version 2.7.9 was employed. The prevalence of GDM in Asia was analysed by subgrouping the country, and by the 10 different diagnostic criteria according to (1) IADPSG, (2) China Ministry of Health (China MOH), (3) ADA, (4) WHO, (5) DIPSI, (6) CC, (7) NDDG, (8) CC and WHO, (9) ICD 10th (ICD-10), (10) JDS. The data were also analysed by subgrouping the screening method and study setting. The risk factors for GDM were reported in odds ratio (OR) with 95% confidence interval (CI) by using a random effect.

Operational definitions

Oral glucose tolerance test (OGTT) is a diagnostic test for gestational diabetes mellitus based on the glucose concentration in venous plasma using an accurate and precise enzymatic method [71]. Congenital anomaly in infants was defined as malformations involving the cardiovascular, genitourinary, musculoskeletal, and central nervous systems [72].

Results

Description of included studies

We identified 2533 manuscripts in the initial search as shown in Fig. 1. After removal of duplicate records (n = 617), 1916 studies were retrieved for further assessment. After careful evaluation of the inclusion/exclusion criteria, 107 studies fulfilled our criteria. Among 107 studies, 84 studies (1988–2017) were of STROBE score of ≥14. These studies were and these studies were included in this systematic review and meta-analysis.
Fig. 1

PRISMA flow diagram of the literature screening process

PRISMA flow diagram of the literature screening process

Characteristics of included studies

The main characteristics of the included studies are shown in the Appendix 4. A total sample of 2, 314,763 pregnant women from 20 countries were included in the analysis. Twenty-four were in India [73-96], nine in Iran [97-105], 8 in China [106-113], 7 in Saudi Arabia [28, 114–119], four in Thailand [120-123], Sri Lanka [124-127] and Japan [128-131], three in South Korea [132-134], Bangladesh [135-137] and Israel [138-140]. Additionally, two were in Vietnam [141, 142], Malaysia [143, 144], Qatar [145, 146], Pakistan [147, 148] and Nepal [149, 150]. One each were from Yemen [151], Hong Kong [152], Singapore [153], Taiwan [154] and Turkmenistan [155]. In terms of diagnostic criteria, a total of 23 studies used the WHO criteria, 13 used IADPSG, 13 used ADA, 13 used CC, 12 used DIPSI, 4 used NDDG, 3 used JDS, 1 used ICD-10, 1 used China MOH criteria and 1 used the combination of the CC and WHO criteria (Table 1). Out of 84 studies, the most commonly used one-step screening procedure was applied in 53 studies (Table 1). A One step screening procedure is defined as the pregnant women undergoing a 75 g OGTT. Two-step screening procedure was used in 30 studies. Two-step screening procedure is defined as pregnant women firstly undergoing a 50 g one-hour Glucose Challenge Test (GCT). If the woman tested positive in the 50 g GCT, they were then required to undergo either a 75 g or 100 g OGTT.
Table 1

Pooled prevalence and 95% confidence interval of gestational diabetes by subgroup analysis

Variable N Total sample sizeTotal GDMPrevalence, %95% CIP-valueI2, %
Country
 Taiwan11325138.630.3–46.9NANA
 Hong Kong152016932.528.5–36.5NANA
 Saudi Arabia713,865319222.912.9–32.999.51< 0.0001
 Vietnam25474122422.318.4–26.291.94< 0.0001
 Malaysia2213635918.56.2–30.897.97< 0.0001
 Singapore190916017.615.1–20.1NANA
 Thailand424,168187217.16.3–27.899.11< 0.0001
 Iran99872114614.910.2–19.698.58< 0.0001
 Qatar2220532313.37.4–19.393.54< 0.0001
 China8156,94211,39412.68.6–16.799.78< 0.0001
 Sri lanka4357738011.45.1–17.897.93< 0.0001
 South Korea31,316,30798,84510.55.8–15.399.87< 0.0001
 India2417,04916798.86.7–10.996.57< 0.0001
 Bangladesh327852268.26 l.0–10.571.610.03
 Pakistan216421277.76.4–9.000.752
 Turkmenistan116201096.75.5–7.9NANA
 Israel3737,97836,8225.33.7–7.099.89< 0.0001
 Yemen1311165.12.7–6.6NANA
 Japan415,1093902.81.9–3.784.4< 0.0001
 Nepal22162261.50.2–3.284.130.012
 Subtotal842,314,763158,51011.510.9–12.199.57< 0.0001
Diagnostic criteria
 IADPSG1342,317514820.917.3–24.699.17< 0.0001
 CHINA MOH114,986298719.919.3–20.6NANA
 ADA13379,58315,50113.911.5–16.298.68< 0.0001
 WHO23134,1529750139.6–16.499.38< 0.0001
 DIPSI12987911148.35.7–10.994.76< 0.0001
 CC13384,14623,7147.66.6–8.799< 0.0001
 NDDG431,73415774.31.4–7.399.2< 0.0001
 CC&WHO12000753.72.9–4.6NANA
 ICD-1011,306,28198,4033.71.2–6.2NANA
 JDS396852413.61.2–6.088.33< 0.0001
 Subtotal842,314,763158,51011.510.9–12.199.59< 0.0001
Setting
 Hospital71423,87831,59812.111–13.199.34< 0.0001
 Community131,890,885126,91211.19.8–12.599.87< 0.0001
 Subgroup842,314,763158,51011.510.9–12.199.59< 0.0001
Screening Methods
 One-step53631,80838,51514.713.5–15.999.5< 0.0001
 Not stated11,306,28198,4037.57.5–7.6NANA
 Two-steps30376,67421,5927.26.4–8.098.82< 0.0001
 Subtotal842,314,763158,51011.510.9–12.199.57< 0.0001
Pooled prevalence and 95% confidence interval of gestational diabetes by subgroup analysis The setting of the study was examined in subgroup analysis; 71 studies were hospital-based and 13 studies were community based.

Prevalence of GDM

The overall mean prevalence of GDM was 11.5% (95% CI 10.9–12.1) (Fig. 2). Table 1 shows the prevalence of GDM across difference covariates such as by country, diagnostics criteria, screening step and study setting. The prevalence of GDM by country was highest in Taiwan (38.6%), followed by Hong Kong (32.5%) and Saudi Arabia (22.9%). The lowest prevalence of GDM was in Nepal (1.5%) followed by Japan (2.8%). The prevalence of GDM by diagnostic criteria was highest with IADPSG (20.9%) followed by China MOH (19.9%). The prevalence of GDM was much lower when the studies used the common and popular criteria of WHO 1980–2013 or ADA 2002–2014 (13.0 to 13.9%) versus the IADPSG and China MOH which gave a prevalence of 19.9 and 20.9%, respectively. The prevalence of GDM by screening methods was very different, where the one-step screening methods reported a prevalence of GDM of 14.7%, while the prevalence of GDM two-step screening method (7.2%) was half that of the one-step method. The prevalence of GDM was almost similar between hospital and community setting (12.1% versus 11.1%).
Fig. 2

The forest plot of the prevalence of gestational diabetes mellitus in Asia

The forest plot of the prevalence of gestational diabetes mellitus in Asia

Risk factors of GDM

The risk factors of GDM was analysed in this current review. The most important risk factors in GDM among Asian population were rated based on pooled analysis of the included studies (Table 2). This meta-analysis found that the odds of GDM was increased by history of previous GDM (OR 8.42, 95% CI: 5.35–13.23), congenital anomalies (OR 4.25, 95% CI 1.52–11.88), and macrosomia (OR 4.41, 95% CI 3.09–6.31). Other risk factor included BMI ≥25 (OR 3.27, 95% CI 2.81–3.80) and pregnancy-induced hypertension (PIH) (OR 3.20, 95% CI 2.19–4.68).
Table 2

Pooled prevalence and 95% confidence interval of gestational diabetes according to the risk factors

Variable N Exposure in GDMTotal GDMExposure in Non-GDMTotal Non-GDMOR95% CII2, %P-value
History of previous GDM24343324627220,6468.425.35–13.2380.92< 0.001
History of congenital anomalies6326555032624.251.52–11.8864.640.015
History of macrosomia293974275100129,5064.413.09–6.3181.14< 0.001
BMI ≥ 25 kg/m23313,30442,30680,126582,7073.272.81–3.8093.49< 0.001
PIH12163189161218,4683.22.19–4.6868.96< 0.001
Family History of Diabetes60317711,06812,33694,9622.772.22–3.4793.76< 0.001
History of stillbirth252612786115821,2572.391.68–3.4075.38< 0.001
PCOS72424113,82726,7771,566,0262.331.72–3.1794.07< 0.001
History of abortion198032658240416,8442.251.54–3.2991.37< 0.001
Age ≥ 2534226,788354,0802,637,5454,798,6782.171.96–2.4196.91< 0.001
Multiparity ≥23221,06931,901290,125434,1981.371.34–1.5286.55< 0.001
History of preterm delivery9230227483712,7481.931.21–3.0776.09< 0.001
History of neonatal death5265505815931.80.86–3.7943.290.133
Illiteracy7118291960410,3721.290.82–2.0465.630.008
Current smoking8125714,16218,924213,4951.040.98–1.1100.93
Current drinking530242291638,4330.790.54–1.1400.66
Primigravida187363875338,87147,2280.550.41–0.7385.99< 0.001
Pooled prevalence and 95% confidence interval of gestational diabetes according to the risk factors Risk factors such as family history of diabetes (OR 2.77, 2.22–3.47), history of stillbirth (OR 2.39, 95% CI 1.68–3.40), Polycystic ovary syndrome (PCOS) (OR 2.33, 95% CI1.72–3.17), history of abortion (OR 2.25, 95% CI 1.54–3.29), age ≥ 25 (OR 2.17, 95% CI 1.96–2.41), multiparity ≥2 (OR 1.37, 95% CI 1.24–1.52), and a history of preterm delivery (OR 1.93, 95% CI 1.21–3.07) in relation to GDM, ranging from 1.93–2.77 (p value < 0.05). On the other hand, for risk factors such as history of neonatal death, illiteracy and current smoking, the odds for GDM ranged from 1.04 to 1.80 (p value > 0.05). Primigravida status and current drinking was found to be protective factors for GDM with an OR of 0.55 and 0.79 (p value < 0.05), respectively.

Discussion

The present meta-analysis included 84 studies from 20 countries across Asia. We compiled the prevalence and risk factors data from a huge population size (n = 2,314,763). The pooled prevalence of GDM was 11.5% (95% CI 10.9–12.1). This figure is considered more representative of the burden of GDM across Asian populations. This prevalence of GDM in Asia is found to be higher than European countries (5.4%) but lower than in African countries (14.0%) [27, 51]. We have no clear reason for such a discrepancy, but we speculate that it may due to maternal age and BMI disparities, as well as ethnic background [156]. For example, South Asian have greater odds of developing GDM than White European and Black Africa at same age [157]. Similarly, South Asian women were older and more obese among GDM patients [157]. Therefore, advancing age, increasing BMI and racial group are associated to the high prevalence of GDM in Asia. It could also be due to a genetic predisposition of Asians to have a higher risk of insulin resistance compared to Caucasian [158]. The higher prevalence of GDM in Asia and Africa is higher than that of Europe. This is consistent with the higher prevalence of T2DM and GDM seen in Asia compared to Europe [62]. Prevalence of GDM including India and Middle Eastern countries makes a total of 20 countries. Our findings on prevalence of GDM are fairly similar to a recent study that reported the prevalence of GDM in 8 Eastern and Southeast Asian countries 10.1% (95% CI 6.5–15.7) [29]. The high heterogeneity in the overall prevalence seen in our study may be due to several reasons, such as different diagnostic criteria and screening methods used by different countries. For example, while several studies used the ADA criteria to screen for GDM, they also used different cut-off value of 92 mg/dl (5.1 mmol/l values as well) or 95 mg/dl (5.2 mmol/l) for the 75 g OGTT. Furthermore, even though within the same country, different diagnostic criteria were used to diagnose GDM. For example, seven diagnostic criteria were used in India and three in Vietnam, giving a broad range of prevalence of GDM ranging from 6.7–10.9 and 18.4.4–26.2, respectively. Hence it is not surprising that high heterogeneity of prevalence of GDM within a country is seen. Similarly, the sample size was important when determining prevalence of GDM, as the literature reports that there is a positive correlation between sample size and the prevalence [159]. In our meta-analysis, there were 5 studies [109, 133, 138–140] with a large sample size which gives larger weight to the prevalence of GDM. This may contributed to the heterogeneity in the results. The IADPSG and China MOH diagnostic criteria usually results in higher prevalence of GDM where the prevalence can be higher by 3.5 to 45.3% [160]. This is partly because a lower cut-off value for fasting glucose is used [161]. These two diagnostic criteria are less popular in the screening for GDM. China MOH was another diagnostic criterion with higher prevalence of GDM. This criterion acknowledged hyperglycaemia in pregnancy be tested at an early stage of pregnancy and later divided them into T2DM in pregnancy and GDM [156] . Hence, this significantly increased the detection and prevalence rate. The ADA and WHO criteria are the most popular diagnostic screening criteria used. The prevalence of GDM based on these criteria are lower than other criteria. There are also many different versions of these criteria over the years, with different cut-off glucose values to classify GDM. For instance, the WHO 2013 has a higher cut-off value for the 2-h plasma glucose compared to WHO 1999, and other diagnostic criteria. Different countries and studies used different diagnostic criteria and it has an impact on the prevalence of GDM. Using a lower threshold value in GDM screening would result in more cases compared to those using higher threshold values. This review demonstrated differences in prevalence of GDM by subgroup screening methods in terms of other than diagnostic criteria that need to be examined when trying to explain the inconsistency in the prevalence of GDM between studies. In the analysis, the prevalence of GDM using one-step screening was nearly double that using the two-steps screening (14.7 and 7.2%. respectively). This is an unexpected finding because a bigger dose of glucose of 75-g will be used in one-step screening method. In comparison with two step method, a 50-g oral glucose will be used in the first round so it will detect fewer GDM cases as only those who are positive on 50-g proceed to the next step using 75 or 100-g. Hence, the overall prevalence of GDM based on one-step screening method will be higher. This is consistent with the literature where the two-step screening method is less sensitive than the one-step screening method in diagnosing GDM, and the two-step screening method will miss approximately 25% of cases [162]. In view of one-step screening method is more practical, cost effective and more convenient [161, 163]. Hence, it is a more advantage to use one-step method instead of two-steps method in diagnosing GDM. Having say so till now there is no consensus for use of the one-step versus two-step screening method among national and international organizations. Recent Cochrane review in 2017 reported that there is insufficient evidence to suggest which strategy is best for diagnosing GDM [164]. The majority of the included studies in this review were conducted in hospitals (12.0%). 71 studies had conducted the screening for GDM during antenatal visits at the hospitals. Meanwhile, 13 studies were conducted in the community hospitals, which mostly involved the authorities in healthcare such as the MOH to perform wide coverage screening for GDM at national, state or regional level. Taiwan had the highest prevalence of GDM (38.6%). The study conducted in Taiwan had a small sample size (n = 132) and the pregnant women were older (mean age of 32) and the chosen study location was mainly inhabited by aboriginal tribes. On top of that the data were collected using 2 different diagnostic criteria. The 100 g three-hour OGTT test was used before 2012 and 75 g OGTT test with a better sensitivity was used since 2012. As we know the prevalence of GDM may be varied according to different diagnostic criteria used [165]. Hong Kong also had a high prevalence of GDM (32.5%) due to the screening was performed at referral hospital for GDM cases, and these GDM group are those in advance age as the mean age of the study population was 34 and higher parity. The prevalence of GDM in Taiwan and Hong Kong were derived from only one study each and hence the reported prevalence are not representable for the true burden of GDM in their countries. The risk factors of GDM was analysed in this current review. Those with multiparity ≥2, previous history of GDM, congenital anomalies, stillbirth, abortion, preterm delivery, macrosomia, having concurrent PIH, PCOS, age ≥ 25, BMI ≥25, and family history of diabetes are the significant risk factors predictive of GDM in current pregnancy (OR values ranged from 1.90 to 8.42). Most of the guidelines, including those of ADA in 2016, recommend universal screening for GDM in second trimester [166]. Other organizations, such as NICE in 2015, recommend screening for GDM using risk factors at the booking appointment. The risk factors considered by NICE in 2015 are BMI ≥ 30, a history of macrosomia of 4.5 kg or more, previous gestational diabetes, a family history of diabetes, or belonging to an ethnic minority with a high prevalence of gestational diabetes such as South Asian and Middle Eastern [167]. In Malaysia, pregnant women age ≥ 25 together with risk factors should be screened for GDM at booking. The risk factors for GDM are those with BMI ≥ 27, previous history of GDM, macrosomia (birth weight > 4 kg), bad obstetric history, glycosuria ≥2 + on two occasions, first degree relative with diabetes mellitus, concomitant obstetrics problems such as hypertension or pregnancy-induced hypertension, polyhydramnios and current use of corticosteroids [168]. While in France, the identified risk factors requiring the search for GDM are maternal age ≥ 35 years, BMI ≥ 25, history of diabetes in first-degree relatives, personal history of GDM or GDM [169]. Our study showed that those with history of previous GDM have 3.5 times odds more likely to develop GDM compare those without history of previous GDM. This finding is consistent with previous study [28, 114]. History of congenital anomalies have 4.3 times odds more likely to develop GDM compare those without history of congenital anomalies. This finding is consistent with previous study [28, 93]. Similarly, to those with history of macrosomia and PIH have 4 times and 3 times for odds to have higher insulin resistance. This is consistent with the previous finding [84, 91]. Polycystic ovarian syndrome (PCOS) is a common cause of insulin resistance [104, 151]. Women with PCOS have higher risk of developing GDM [104, 151] and this is consistent with our study (OR 2.33, 95% CI 1.72–3.17). BMI is commonly used in risk-based screening for GDM. Prevalence of GDM is also increased with increasing pre-pregnancy BMI [170]. For instance, prevalence of GDM was highest among Asian women with BMI ≥ 30 kg/m2 (13.78%), followed by BMI ≥ 25 kg/m2 (10.22%) and BMI ≥ 20 kg/m2 (6.09%). In this current review, we used a BMI cut-off of ≥25 kg/m2 and found the odds ratio for GDM is 3.39 (95% CI2.92–3.93). Our result is consistent with previous studies where the odds of BMI ≥25 kg/m2 for GDM ranged from 2.78 (95% CI: 2.60–2.96) to 3.56 (95% CI: 3.05–4.21) [65, 171]. A BMI ≥ 25 kg/m2 has a lower sensitivity (24.9%) but a good specificity (88.7%) in comparison to using a cut-off level of BMI ≥ 21 kg/m2 which has a higher sensitivity of 68.4% but a lower specificity of 53.6% [170]. Literature suggests a BMI ≥25 kg/m2 is more suitable to be used among African-American women as the sensitivity (46.2%) and specificity (81.5%) are higher. A BMI ≥21.0 kg/m2 would be recommended as cut off threshold to screen GDM with a better sensitivity however BMI I ≥ 25.0 kg/m2 was the most commonly used threshold among the included studies [170]. Obesity is one of the main factors in the development of diabetes and GDM [64, 172]. BMI is a commonly used method to measure the severity of obesity [173]. However, the cut-off point used to diagnose obesity is different between western and Asian countries [170]. For example, prevalence of GDM was highest among Asian women with BMI ≥ 30 kg/m2 (13.78%), followed by BMI ≥ 25 kg/m2 (10.22%) and BMI ≥ 20 kg/m2 (6.09%). In this current review, we have employed a BMI cut-off of ≥25 kg/m2 and found the odds ratio for GDM is 3.27 (95% CI2.81–3.80). Our results are consistent with previous studies in which the odds of BMI ≥25 kg/m2 for GDM ranged from 2.78 (95% CI: 2.60–2.96) to 3.56 (95% CI: 3.05–4.21) [65, 171]. Maternal age is an established risk factor for GDM, but there is no consensus on age’s relation to increased risk of GDM [174]. ADA recommended the lowest cutoff of ≥25 years to screen for GDM as early as possible [43]. This is supported by our results showing that the odds of GDM by age ≥ 25 is OR 2.17 (95% CI 1.96–2.41), and consistent with previous study findings showing that screening for GDM among patients aged 25 years and above with other risk factors indeed has a higher predictive value in identifying GDM [175]. According to previous studies, family history of diabetes (particularly in a first-degree relative) increases the risk for GDM [64, 66]. Onset of GDM has a familial tendency and this potentially suggests that there is a genetically predisposition to develop GDM [176-178]. In current review, family history of diabetes has OR 2.77(95% CI 2.22–3.47) of GDM. Our results are consistent with a previous study in which the odds of family history of diabetes for GDM among Iranian women was determined to be OR 3.46 (95%CI 2.8–4.27) [179]. The strength of this review paper is that it not only included more countries, including India and countries in Middle East which were both not included in previous reports. Furthermore, the articles with poor quality in STROBE were excluded to maintain the reliability of findings of current review. Our meta-analysis has the following limitations. Firstly, we are aware that the studies included in this meta-analysis are not a true reflection of the Asian population. Although there were 24 studies in the meta-analysis come from India, they only contributed 17,049 patients out of the general population of 1.3 billion in India. Similarly, the 8 Chinese studies only contributed 156,942 patients out of 1.4 billion in China. Based on the inclusion criteria, we have recruited the above 32 studies in this review. Thus, we must interpret the results of this meta-analysis cautiously within the context of their limitations. Secondly, there was a high heterogeneity in our result. This could be due to different diagnostic criteria and screening methods used by different countries. This high heterogeneity may also be due to the different population characteristics as 20 countries were included in this meta-analysis. Thirdly, this meta-analysis included manuscripts from the inception to 2018, covering a vast range of clinical and diagnostic criteria and practice changes. The threshold value of two-hour in one-step 75-g method and three-hour in 100-g two-steps methods are reduced over time, increasing the identification rates of GDM cases over time. Therefore, changes of threshold value to identify GDM could inevitably cause high heterogeneity to the results. Finally, studies with small sample size were also included in this meta-analysis. Hence the result of this meta-analysis may suffer from high variability. Therefore, some estimates of the meta-analysis could be influenced by heterogeneity between the studies.

Conclusions

Our current study provides an estimation of the prevalence and risk factors of GDM in Asia. Our study shows that the pooled estimation of prevalence was 11.5%. We have identified the following risk factors of developing GDM: multiparity≥2; previous history of GDM; congenital anomalies; stillbirth; abortion; preterm delivery; macrosomia; concurrent PIH; PCOS; age ≥ 25; BMI ≥25; and family history of diabetes. It is important that the risk factors for GDM are recognized in order the clinicians are able to identify those at risk of getting GDM for early diagnosis and further intervention. We recommend that clinicians screen for GDM as early as possible among those with risk factors using one-step screening method instead of two-step screening method. If the results are negative, the test should be repeated in between 24 and 28 weeks of gestation.
Table 3

Screening criteria for the diagnosis of Gestational Diabetes Mellitus

Diagnostics criteriaStepsOGTTNo. abnormalFasting mg/dl (mmol/l)1 H mg/dl (mmol/l)2 H mg/dl (mmol/l)3H mg/dl (mmol/l)
O′ Sullivan 1964 [49]2100 g≥ 290 (5)165 (9.2)145 (8.1)125 (6.9)
NDDG 1979 [50]2100 g≥ 2105 (5.8)190 (10.6)165 (9.2)145 (8.0)
CC 1982 [51]2100 g≥ 295 (5.3)180 (10)155 (8.6)140 (7.8)
EASD 2012 [52]175 g≥ 1108 (6)162 (9)
ACOG [53]2100 g≥ 295 (5.30180 (10)155 (8.6)140 (7.8)
ADIPS 1998 [54]175 g≥ 1100 (5.5)144 (8.0)
IADPSG 2010 [55]175 g≥ 292 (5.1)180 (10)153 (8.5)
DIPSI [25]175 g≥ 1140 (7.8)
JDS [56]175 g≥ 2126 (7)200 (11.1)
China MOH [57]175 g≥ 192 (5.1)180 (10)153 (8.5)
ICD-10 O24.4 (58)275 g≥ 192 (5.1)180 (10)153 (8.5)
ADA 1997 [59]175 g≥ 1126 (7)200 (11.1)
ADA 2002 [37]175 g≥ 1126 (7)200 (11.1)
ADA 2003 [38]2100 g≥ 295 (5.3)180 (10)155 (8.6)140 (7.8)
ADA 2004 [39]2100 g≥ 195 (5.3)180 (10)155 (8.6)140 (7.8)
ADA 2011 [40]175 g≥ 192 (5.1)
ADA 2012 [41]175 g≥ 192 (5.1)180 (10)153 (8.5)
ADA 2014 [42]175 g≥ 1180 (10)153 (8.5)
WHO 1980 [43]175 g≥ 1140 (7.8)200 (11.1)
WHO 1998 [44]175 g≥ 1126 (7)200 (10)
WHO 1985 [45]175 g≥ 1140 (7.8)
WHO 1999 [44]175 g≥ 1126 (7)140 (7.8)
WHO 2006 [46]175 g≥ 1126 (7)180 (10)200 (11.1)
WHO 2013 [47]175 g≥ 192 (5.1)180 (10)153 (8.5)
CDA 2008 [48]175 g≥ 295 (5.3)190 (10.6)160 (8.9)

ACOG The American College of Obstetricians and Gynecologists, ADA American Diabetes Association, ADIPS Australian Diabetes in Pregnancy Society, CC Carpenter-Coustan, CDA Canadian Diabetes Association, DIPSI Diabetes in Pregnancy Study group of India, EASD European Association for the Study of Diabetes, IADPSG International Association of the Diabetes and Pregnancy Study Groups, ICD International Classification of Diseases, JDS Japan Diabetes Society, NDDG National Diabetes Data Group, OGTT Oral Glucose tolerance Test, WHO World Health Organization, MOH Ministry of Health

Table 4

Search terms used for final search 22 August 2017

SearchesSearch termsPubmedOvidSciencedirectScopus
# 1Incidence2,424,449230,603194,4042,761,766
# 2Prevalence2,583,495253,174141,4052,490,683
# 3Risk factor1,264,673726,298209,9664,281,945
# 4Diabetes in pregnancy36,32610,3314542135,425
# 5Gestational diabetes mellitus18,3758665215646,028
# 6Asia755,31726,03752,8581,413,577
# 7#1 OR #22,812,427461,976322,2374,476,331
# 8#4 OR #536,32618,1215314145,571
#9#7 AND #8 AND #3 AND #6608630318838
Table 5

Assessment of risk of bias of included studies by STROBE Checklist

1a1b23456a6b789101112a12b12c12d12e13a13b13c14a14b14c1516a16b16c171819202122
Alfadhli et al., 20151111111111011110101111011110011110
Ali et al., 20161111111111001110101001111110011111
Al-Kuwari et al., 20111111111011001110101101011110010110
Al-Rowaily et al., 20100111011011011110101001001110011110
Al-Rubeaan e al., 20141111111111011100101111011110011111
Al-Shawaf et al., 19880111011111001100101001011010010110
Aziz et al., 20171111111111010000001001011010010110
Bener et al., 20111111111111011110101001011110010110
Bhatt et al., 20150111010111011100011001011110011111
Cheuk et al., 20161111111011001110101111011000011110
Chodick et al., 20101111111011001110101101111111011110
Dahiya et al., 20140111111111001100101001011110010110
Das et al., 20041101111111010000101101011000010110
De Seymour et al., 20161111111111011111001111111110011111
Deerochanawong et al., 19960111011111001100001001011111010110
Garshasbi et al., 20081111111111011110101111011110010110
Gracelyn and Saranya20161111111111101100101001011110010111
Haideagh et al., 20050111011011011000101101111010010110
Hariharan et al., 20171111111111010100101000011000011110
Herath et al., 20161111111111001100111001111010110110
Hirst et al., 20121111111111101111011111111110101111
Hossain et al., 20171111111011001110111001011110111110
Hossein-Nezhad et al.,20071111111111011110101001011110010110
Iqbal et al., 20071111111011001110101101111110011111
Jadhav and Wankhede 20170111011111100000001001011010010111
Jang et al., 19981111111111011110101101011110010111
Jesmin et al., 20141111110111101110000000100110011111
Kalra et al., 20130111011111011000011001011010010110
Kalyani et al., 20140111011111100000001001011010010111
Khwaja et al., 19890011011111011100001001111010010110
Koo et al., 20161111011010000110101001011110011111
Krishnaveni et al., 20070111011111011000101001011110010111
Leng et al., 20161111111111011110101001011110111111
Li et al., 20141111111111011110101001011110011111
Li et al., 20161111111011001110111001011110111110
Lin et al., 20151111011011000000101101011110011110
Maegawa et al., 20030111010111011110011001111010111110
Makwana et al., 20170111011011001000001001011010010111
Mizuno et al., 20161111011111011100101111011110011111
Mohammadzadeh et al., 20150111111111001110101101111110011111
Moradi et al., 20150111011111001100101001011010011110
Mustafa 20151111111111001000000001011010011110
Nayak et al., 20131111111111011100101001011000011111
Nielsen et al., 20161111111011011110011001011110111111
Parhofer et al., 20131111011011001100001111011000011111
Pirjani et al.,20161111111001001110100001011110111110
Raja et al., 20141111111011011100000001011000010110
Rajput et al., 20131111011011010100101001011110010110
Rajput et al., 20140111111111011100000001011110010110
Rao et al., 20150111011111001000001001010010010110
Saisho et al., 20130111111111011000000001011010011110
Sayeed et al., 20050111111111011101101111111110011111
Sella et al., 20131111111011011110001101011110010110
Sella et al., 20111111111011000111101001011110011110
Shahbazian et al.,20161111111111000110101001011110011111
Shaman et al., 20151111111111011100101001011000010111
Shamsuddin et al., 20011101111011000100111101011000110110
Shang et al., 20140111011011001110101111001110010111
Sharma et al., 20161111111011001100111001011010111111
Shimodaira et al., 20161111111111111111001101011110011110
Shrestha and Chawla 20111111110111011100001001011010010110
Shridevi et al., 20150111011111011100101001011010010111
Singh and Uma 20131111111011001110101001011000010110
Siribaddana et al., 19981111111111001000101001011010010110
Soheilykhak et al., 20101111111011101100101101011111010111
Song et al., 20171111111111011111001001111110011111
Srichumchit et al., 20151101111111000100101111011110011111
Sudasinghe et al., 20161111111101010100101101011000011111
Suntorn and Panichkul 20151111111011001110101101011010011110
Swaroop et al., 20151111111011000100001001011000010111
Tan et al., 20091111111111011110101111011110011110
Thapa et al., 20150111111111011100001001011010011111
Thathagari et al., 20161111111111011110101001011110010111
Tran et al., 20131111111111011110111101101000111111
Tripathi et al., 20111111111111011000101011011110010110
Vakili et al., 20161111111111011100101001011100011110
Wagaarachchi et al., 20011111011110010100101101011000010111
Wahabi et al., 20170111111111001100101101011110011111
Warunpitikul and Aswakul 20141111111111001100101001011110010111
Yang et al., 20131101011111011110101001011000011111
Zargar et al., 20041111111011001100101001011110010110
Zhang et al., 20111111111101011100101001011110011111
Zhang et al., 20151111111111011110111001011110111111
Zhu et al., 20170111011111011100101001011110011111

1(Presence of item)

0(Absence of item)

†Quality is defined by a STROBE score ≥ 14/22 (good) and < 14/22 (poor)

Table 6

Characteristics of Included studies

Author, yearCountryAssociationDiagnostic criteriaStudy SettingScreening MethodsScreening dosageGDM +Sample sizePrevalence
Alfadhli et al., 2015Saudi ArabiaIADPSGIADPSGHospital175 g29257351.0
Ali et al., 2016YemenADAADA 2002Hospital175 g163115.1
Al-Kuwari et al., 2011QatarADAADA 2004Hospital250 g, 75 g6159710.2
Al-Rowaily et al., 2010Saudi ArabiaWHOWHO 1999Hospital175 g7963312.5
Al-Rubeaan e al., 2014Saudi ArabiaADAADA 2011Community175 g20152938.0
Al-Shawaf et al., 1988Saudi ArabiaWHOWHO 1985Hospital275 g4111023.7
Aziz et al., 2017IndiaCCCCHospital1100 g567008.0
Bener et al., 2011QatarWHOWHO 2006Hospital175 g262160816.3
Bhatt et al., 2015IndiaDIPSIDIPSICommunity175 g949899.5
Cheuk et al., 2016Hong KongWHOWHO 1999Hospital175 g16952032.5
Chodick et al., 2010IsraelCCCCCommunity1100 g11,270185,4166.1
Dahiya et al., 2014IndiaDIPSIDIPSIHospital175 g355007.0
Das et al., 2004IndiaNDDGNDDGHospital250 g, 100 g123004.0
De Seymour et al., 2016SingaporeWHOWHO 1999Hospital116090917.6
Deerochanawong et al., 1996ThailandWHOWHO 1985Hospital250 g, 75 g11170915.7
Garshasbi et al., 2008IranCCCCHospital250 g, 100 g12418046.9
Gracelyn and Saranya2016IndiaADAADA 2014Hospital175 g5950011.8
Haideagh et al., 2005IranCCCCCommunity250 g, 100 g628007.8
Hariharan et al., 2017IndiaWHOWHO 2013Hospital175 g1613511.9
Herath et al., 2016Sri lankaIADPSGIADPSGHospital175 g10545223.2
Hirst et al., 2012VietnamIADPSGIADPSGHospital175 g550270220.4
Hossain et al., 2017PakistanDIPSIDIPSIHospital175 g7810307.6
Hossein-Nezhad et al.,2007IranCCCCHospital250 g, 100 g11424164.7
Iqbal et al., 2007PakistanADAADA 2004Hospital275 g, 100 g496128.0
Jadhav and Wankhede 2017IndiaDIPSIDIPSIHospital175 g8010008.0
Jang et al., 1998South KoreaNDDGNDDGHospital250 g, 100 g17388632.0
Jesmin et al., 2014BangladeshWHOWHO 1999Hospital250 g, 75 g11211499.7
Kalra et al., 2013IndiaDIPSIDIPSIHospital175 g335006.6
Kalyani et al., 2014IndiaWHOWHO 1999Hospital175 g253008.3
Khwaja et al., 1989Saudi ArabiaWHOWHO 1985Hospital150 g5045511.0
Koo et al., 2016South KoreaICD-10ICD-10Community98,4031,306,2817.5
Krishnaveni et al., 2007IndiaCCCCHospital1100 g215244.0
Leng et al., 2016ChinaIADPSGIADPSGCommunity250 g, 75 g84011,4507.3
Li et al., 2014ChinaADAADA 2012Hospital175 g6953912.8
Li et al., 2016ChinaIADPSGIADPSGHospital175 g4832714.7
Lin et al., 2015TaiwanADAADA undefinedHospital175 g or 100 g5113238.6
Maegawa et al., 2003JapanJDSJDSHospital250 g or 75 g227492.9
Makwana et al., 2017IndiaDIPSIDIPSIHospital175 g384768.0
Mizuno et al., 2016JapanJDSJDSHospital175 g20488742.3
Mohammadzadeh et al., 2015IranCCCCHospital250 g, 100 g6212764.9
Moradi et al., 2015IranWHOWHO 2006Hospital175 g4429015.2
Mustafa 2015BangladeshWHOWHO 1999Hospital175 g10214896.9
Nayak et al., 2013IndiaIADPSGIADPSGHospital175 g8330427.3
Nielsen et al., 2016IndiaDIPSIDIPSIHospital175 g659405316.3
Parhofer et al., 2013TurkmenistanADAADA undefinedHospital250 g, 75 g10916206.7
Pirjani et al.,2016IranADAADA 2012Hospital175 g7825630.5
Raja et al., 2014IndiaDIPSIDIPSICommunity175 g243067.8
Rajput et al., 2013IndiaADAADA 2004Hospital175 g436077.1
Rajput et al., 2014IndiaWHOWHO 1999Community175 g12791313.9
Rao et al., 2015IndiaDIPSIDIPSIHospital175 g52002.5
Saisho et al., 2013JapanJDSJDSHospital250 g, 75 g156224.2
Sayeed et al., 2005BangladeshWHOWHO 1999Community175 g121478.2
Sella et al., 2011IsraelCCCCHospital250 g, 100 g11,264185,3156.1
Sella et al., 2013IsraelADAADA 2003Community1100 g14,288367,2473.9
Shahbazian et al.,2016IranIADPSGIADPSGHospital175 g22475029.9
Shaman et al., 2015Saudi ArabiaIADPSGIADPSGHospital175 g17585020.6
Shamsuddin et al., 2001MalaysiaWHOWHO 1985Hospital175 g19176824.9
Shang et al., 2014ChinaIADPSGIADPSGHospital175 g612308319.9
Sharma et al., 2016IndiaIADPSGIADPSGHospital175 g7441717.7
Shimodaira et al., 2016JapanADAADA 2004Hospital250 g, 75 g14954242.7
Shrestha and Chawla 2011NepalCCCCHospital250 g, 100 g1215980.8
Shridevi et al., 2015IndiaDIPSIDIPSIHospital250 g, 75 g2320011.5
Singh and Uma 2013IndiaDIPSIDIPSIHospital175 g234005.8
Siribaddana et al., 1998Sri lankaWHOWHO 1985Hospital250 g, 75 g407215.5
Soheilykhak et al., 2010IranCCCCHospital250 g, 100 g110107110.3
Song et al., 2017ChinaIADPSGIADPSGHospital175 g1005688614.6
Srichumchit et al., 2015ThailandNDDGNDDGHospital250 g, 100 g135021,7716.2
Sudasinghe et al., 2016Sri lankaWHOWHO 1999Community175 g194140013.9
Suntorn and Panichkul 2015ThailandIADPSGIADPSGHospital175 g7132521.8
Swaroop et al., 2015IndiaDIPSIDIPSIHospital175 g222259.8
Tan et al., 2009MalaysiaWHOWHO 1999Hospital250 g, 75 g168136812.3
Thapa et al., 2015NepalWHOWHO 1999Hospital175 g145642.5
Thathagari et al., 2016IndiaNDDGNDDGHospital250 g, 100 g428005.3
Tran et al., 2013VietnamWHOWHO 1999Hospital175 g674277224.3
Tripathi et al., 2011IndiaCCCCHospital250 g, 100 g107001.4
Vakili et al., 2016IranADAADA 2004Community175 g328120927.1
Wagaarachchi et al., 2001Sri lankaWHOWHO 1980Hospital175 g4110044.1
Wahabi et al., 2017Saudi ArabiaWHOWHO 2013Hospital175 g2354972324.2
Warunpitikul and Aswakul 2014ThailandCCCCHospital250 g, 100 g340136324.9
Yang et al., 2013South KoreaCCCCHospital250 g, 100 g269116323.1
Zargar et al., 2004IndiaCC and WHOCC and WHO 1999Hospital250 g, 75 g/100 g7520003.8
Zhang et al., 2011ChinaWHOWHO 1999Hospital250 g, 75 g4764105,4734.5
Zhang et al., 2015ChinaIADPSGIADPSGCommunity250 g, 75 g106914,1987.5
Zhu et al., 2017ChinaCHINA MOHCHINA MOHHospital175 g298714,98619.9
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