Gestational diabetes mellitus (GDM) is one of the most common complications during pregnancy. The definition of GDM is evolving. Until recently, the accepted definition was “any degree of glucose intolerance with onset or first recognition during pregnancy”.1 Because this definition includes women with pre-existing diabetes who were not identified prior to pregnancy and because this definition blurs the line between morbidities associated with diabetes in pregnancy and gestational diabetes, renewed efforts are being made to improve the definition and classification of hyperglycemia during pregnancy. These efforts are also spurred by the increasing prevalence of diabetes and GDM and of greater prevalence of maternal and fetal complications resulting from diabetes mellitus antedating pregnancy. The American Diabetes Association (ADA) (2019)2 defines GDM as “diabetes first diagnosed in the second or third trimester of pregnancy that is not clearly overt diabetes prior to gestation”. Nowadays there is also an increased incidence of hyperglycemia not amounting to overt diabetes noted during routine testing even in the first trimester. Therefore, hyperglycemia first detected at any time during pregnancy should be classified either as diabetes mellitus in pregnancy (DIP) if it meets the criteria of overt diabetes outside pregnancy or GDM.3 GDM is associated with an increased risk of adverse pregnancy outcomes for both mothers and their offspring not only in the short term but also in the long term.4,5 The prevalence of GDM in China increased significantly when the much stricter cut-off values for GDM diagnosis issued by the International Association of Diabetes and Pregnancy Study Groups (IADPSG) was applied in 2010.6 According to a study conducted in 15 hospitals in Beijing, the prevalence of GDM was 19.7%.7 Therefore, it is important to diagnose and manage GDM appropriately in our country to face the challenge. Despite extensive research in the past 50 years, a universal approach to diagnose GDM around the world is remains elusive and clinical practices vary from country to country and unit to unit even with the same country.8–10 Differences in screening strategy and diagnostic criteria make it difficult to compare GDM prevalence in various populations. In China, the diagnostic criteria of GDM have also changed continuously since 1990s. In this current review, we will discuss the development of GDM diagnosis in China, and compare it to that in western countries to figure out the proper recommendations on the diagnosis of GDM for Chinese women.
History of GDM diagnostic criteria
The concept of GDM diagnostic criteria was initiated as early as 1960s, when O'Sullivan and Mahan described the first criteria for diagnosis of GDM in 1964 and modified it in 1973.11,12 In their study, 752 pregnant women underwent measurements of venous whole blood glucose levels at fasting, 1-, 2-, and 3 hours after oral administration of 100 g glucose load. Diagnostic cut of values were determined to be 5.0, 9.2, 8.0, and 6.9 mmol/L at each time point, and presence of two or more abnormal readings were considered as GDM. Then in 1979, the National Diabetes Data Group (NDDG) designated GDM as an independent type of diabetes mellitus and adopted the GDM diagnostic criteria proposed by O'Sullivan, converted the whole blood glucose value to the equivalent value measured in plasma, and suggesting 5.8, 10.6, 9.2, and 8.1 mmol/L as the plasma glucose diagnostic thresholds for GDM.13 Three years later, in 1982, Carpenter and Coustan recommended to perform a 50 g, 1-hour non fasting glucose challenge test (GCT) first, followed by, if abnormal, a 100 g, 3-hour OGTT tests according to O'Sullivan's diagnostic criteria. In their study, they measured plasma glucose with glucose oxidase method instead of measuring whole blood glucose with Somogyi-Nelson method used by O'Sullivan. So the thresholds were converted to 5.3, 10.0, 8.6, and 7.8 mmol/L at each time point, and two or more abnormalities were diagnosed as GDM.14 In 1998, the ADA updated GDM diagnostic criteria and adopted the cutoff values of 100 g, 3-hour OGTT proposed by Carpenter and Coustan after an abnormal GCT. Due to the obvious gastrointestinal reaction to a 100 g glucose load in fasting pregnant women, the ADA suggested that the glucose load be changed to 75 g, and instead of four readings, the 3-hour measurement be dispensed with and the cut off values for the other three measurements remained unchanged. Figure 1 outlines a selection of diagnostic criteria for GDM.
However, GDM diagnostic criteria recommended by both NDDG and ADA were derived from the study of O'Sullivan, and updated only because of the changes of glucose test methods. In addition, the glucose levels at each time point of 75 g OGTT were significantly lower than that after a 100 g OGTT.15 It was therefore considered unreasonable, arbitrary and lacking evidence-based supports to continue using the same diagnostic criteria after decreasing the glucose load from 100 to 75 g and omitting the 3-hour glucose value directly.16 What's more, the diagnostic criteria recommended by NDDG and ADA were mainly based on predicting type 2 diabetes risks in mothers after pregnancy, rather than considering the effects of hyperglycemia on maternal and fetal pregnancy outcomes. Several studies have shown that blood glucose levels that affect pregnancy outcomes were well below the cutoff values used in previous criteria.17 Regarding the above questions, more studies are needed to investigate the feasible diagnosis criteria of GDM.
Milestone in the history of GDM diagnostic criteria
In July 2000, the National Institute of Health (NIH) initiated an international multicenter prospective study: the Hyperglycemia and Adverse Pregnancy Outcomes (HAPO) study.18 This study enrolled 25,505 nondiabetic pregnant women at 15 centers in nine countries across North America, Europe, the Middle East, Asia, and Australia to explore the effects of blood glucose levels on pregnancy outcomes. The study results published eight years later, demonstrated a continuous linear association between fasting, 1-hour, and 2-hour glucose levels of 75 g OGTT and risks of adverse pregnancy outcomes, even within ranges of plasma glucose previously considered normal for pregnancy. Although in the study, the risk of adverse pregnancy outcomes associated with hyperglycemia was continuous with no obvious inflection point, the results provided a scientific basis for the development of GDM diagnostic criteria. Subsequently, in 2010, predominantly based on the results of HAPO study, additional unpublished HAPO study findings, and results of other work, the IADPSG proposed new diagnostic criteria for GDM using a one-step approach with 75 g OGTT, and cut-off values based on a 1.75-fold increased risk of macrosomia in HAPO study cohort and the plasma glucose cut off values were identified as 5.1, 10.0, and 8.5 mmol/L at fasting, 1-hour, and 2-hour after 75 g OGTT as the diagnostic thresholds for GDM; with one or more of these values equaling or exceeding the above thresholds.19
The new GDM diagnostic criteria marked a major milestone in the history of GDM diagnostic criteria, and many international organizations, including ADA,20 World Health Organization (WHO),21,22 and the international Federation of Gynecology and Obstetrics,23 advocated the use of 75 g OGTT during 24–28 gestational weeks as the diagnostic test and the new cutoff values recommended by IADPSG as GDM diagnostic criteria. However, other organizations expressed concern about the increased incidence of GDM after the adoption of IADPSG “one-step” diagnostic criteria, the increased health and economic burden caused by the consequent increased workload and expenses this would entail. They also pointed to the lack of high-quality large-scale randomized controlled trial (RCT) to support that “one-step” method is better than the previous “two-step” diagnostic criteria.24 The American College of Obstetricians and Gynecologists continued to recommend the old diagnostic criteria,25 and argued that more studies are needed to evaluate the feasibility of the “one-step” GDM diagnostic criteria. In addition, the HAPO study lacked data from two most populous countries i.e., mainland China and India, and the cutoff points were derived mainly from white populations raising questions on the validity and applicability of the criteria to China and India.
Progress on Chinese GDM diagnostic criteria
China has carried out substantial research in this field since the 1980s. The first study was conducted by the Chinese Islet β Cell Function Research Collaboration Group to compare the glucose response curves of 100, 75, and 50 g OGTT. They found that the glucose response curves of 100 and 75 g OGTT were similar. But the 100 g glucose load, more frequently caused gastrointestinal reactions, like nausea and vomiting, often occurred. Therefore, it is recommended to use 75 g instead of 100 g load for OGTT.26 However, this study was conducted in nonpregnant populations and more studies among pregnant women were still needed. Efforts to evaluate the GDM diagnostic criteria in China started as early as in 1989, when Dong et al. carried out a study in Peking University First Hospital, which collected data of 514 pregnant women without prepregnancy diabetes and endocrine diseases. According to their study, they proposed to use 5.5, 10.2, 8.2, and 6.6 mmol/L as the cutoff values at fasting, 1-hour, 2-hour, and 3-hour after 75 g OGTT, and two or more abnormalities to be considered as diagnostic of GDM in China.27 Although this new criteria did not gain wide acceptance in China due to the limited sample size, Dong's study found that 75 g OGTT values seemed much lower than the 100 g OGTT values in pregnant women, and it was not appropriate to use the 100 g OGTT criteria directly when changed to 75 g glucose load. Since then, more studies have been established to investigate the feasible diagnostic criteria for GDM among Chinese women. Studies had shown that even one abnormal OGTT value also increases the risk of adverse pregnancy outcomes.28 This was contrary to the GDM diagnostic criteria recommended by NDDG and ADA at that time,13,14 which recommended two or more abnormalities as GDM, and did not take into account the outcomes in women with only one OGTT abnormality. In 1999, a study conducted in Peking University First Hospital investigated whether treatment of women who had only one OGTT abnormality was associated with adverse outcome of fetus and newborns.29 Their results showed that the prevalence of neonatal metabolic complications in the untreated group were significantly higher than those treated with insulin or dietary intervention. This indicated that not only GDM pregnant women, defined as having gestational impaired glucose tolerance (GIGT), might benefit from early intervention and treatment. Therefore, they recommended that pregnant women with GIGT should also be intervened or treated to reduce adverse outcomes. Then in 2004, Yang et al. conducted a study among 647 GDM patients and 233 GIGT patients to demonstrate whether the 3-hour glucose value in OGTT was needed in diagnosis of GDM. Their results pointed out that even with the omission of the 3-hour OGTT value, there was still a high sensitivity in diagnosing GDM and GIGT among Chinese women,30 which indicated that it is practicable to omit 3-hour in the 75 g OGTT recommended by ADA. Another research carried out by Gao et al. in a national survey of 4179 pregnant women also concluded that omission of the 3-hour glucose in OGTT might be reasonable due to its convenience, better compliance, and a very small number of missed diagnosis of cases, and that the pregnancy outcomes in these cases had no significant difference from those of normal pregnant women.31 The above Chinese studies provided more evidence to support the idea to use 2-hour OGTT instead of 3-hour OGTT and had been cited by the WHO diagnostic criteria.32
As is well known, there are differences in glucose metabolism among different ethnic groups, and studies have shown that OGTT values at each point among Chinese women were different from western populations. In March 2006, the Chinese Gestational Diabetes Mellitus Collaboration Group, including 25 hospitals in 18 cities nationwide, was established to carry out prospective population-based studies to identify the suitable GDM screening and diagnostic criteria for Chinese women. This was the largest study focused on GDM in China at that time. The results highlighted that compared with NDDG criteria, the prevalence of GDM and GIGT was significantly higher by using ADA diagnostic criteria.33 As most hospitals in China use 75 g OGTT rather than 100 g OGTT, it was recommended to diagnose GDM based on ADA diagnostic criteria, with two or more abnormalities in 75 g OGTT for Chinese women.34 In the meantime, the multicentered population-based survey was used to explore the suitable cutoff values of 50 g GCT for GDM screening in China, which concluded that a cutoff value of 7.8 mmol/L for GCT was appropriate for Chinese people.35
In 2011, after the announcement of the landmark IADPSG diagnostic criteria, a retrospective population-based study of 14,593 pregnant women was conducted by Wei and Yang to compare the suitability of the new IADPSG criteria of GDM in China. Their results showed that the incidence of perinatal complications would increase in pregnant women who met the IADPSG criteria without interventions, and indicated that the IADPSG diagnostic criteria were more reasonable for use in China.36 Three years later, another prospective study conducted by Wei and Yang among 25,674 pregnant women in Peking University First Hospital concluded that treatment or intervention of women with GDM identified by IADPSG criteria was associated with significantly lower risk of multiple adverse pregnancy outcomes. Their findings provided more support for applying the IADPSG criteria in China.37 Although the 2010 IADPSG criteria recommended that fasting plasma glucose (FPG) greater than 5.1 mmol/L in early pregnancy could be diagnosed as GDM, retrospective studies conducted in China demonstrated a physiological reduction in fasting plasma glucose in early pregnancy and highlighted that FPG ≥5.1 mmol/L in early pregnancy were poorly predictive of later GDM. In addition, there was no significant correlation between FPG in early pregnancy and adverse pregnancy outcomes.38–40 So it recommended not to use FPG ≥5.1 mmol/L in early pregnancy as the diagnostic criteria for GDM in China, and an OGTT should be performed at 24–28 weeks to confirm or rule out GDM. But as some of these women might be at risk of GDM as the pregnancy progresses, so nutrition and exercise advice should be provided also to this group of women. The results of this study had been considered and cited by the WHO (2013) recommendations. All these studies conducted among Chinese populations have provided additional evidence to inform health care policy and decision making and promote the development of guidelines in China.
Development of guidelines for diagnosis of GDM in China
Clinical practice guidelines are an extremely important tool for medical institutions and health care practitioners, as substantial variability in clinical practice among different hospitals and districts can be minimized by the use of uniform guideline. But to achieve this the guidelines must be pragmatic and based on local evidence, bearing in mind the local cultural and social, health system and infrastructure challenges. It has been 12 years since the first guideline for diagnosis of GDM was issued in China. In 2007, the Obstetrics and Gynecology Branch of Chinese Medical Association and the Perinatal Medicine Branch of Chinese Medical Association drafted the “Guideline for Clinical Diagnosis and Treatment of Gestational Diabetes Mellitus” based on NDDG and ADA criteria for clinician reference.41 The 2007 guideline recommended to routinely perform a 50 g GCT during 24–28 weeks of gestation for all nondiabetic pregnant women, whereas for those pregnant women with high-risk factors for GDM, a 50 g GCT is recommended to be performed at the first time of prenatal care. Classical risk factors for GDM include obesity, family history of diabetes, polycystic ovarian syndrome (PCOS), fasting glycosuria positive in early pregnancy, medical history of GDM, history of multiple spontaneous abortions without obvious cause, history of fetal malformation, or macrosomia etc. A 75 or 100 g 3-hour OGTT was recommended if the 1-hour glucose value of 50 g GCT is equal to or greater than 7.8 mmol/L. GDM could be diagnosed if one of the following criteria is meet: (1) Fasting blood glucose (FBG) ≥7.8 mmol/L two or more times during pregnancy; (2) two or more OGTT glucose values equal to or exceeding the cutoff values of NDDG or ADA criteria; (3) 1-hour glucose of 50 g GCT ≥11.1 mmol/L, and FBG ≥5.8 mmol/L.
Four years later, with the launch of IADPSG new diagnostic criteria, China also revised the GDM diagnostic criteria according to the condition of the country to be in line with international standards. The Medical Service Specialty Standard Committee of the Ministry of Health in China adopted the new diagnostic criteria of GDM based on IADPSG guideline19 and formulated the “Diagnostic Criteria for Gestational Diabetes Mellitus (WS 331-2011)” on July 1 2011, which came into effect on December 1, 2011.42 The guideline recommended performing a diagnostic 75 g OGTT during 24 and 28 weeks of gestation for all pregnant women not previously diagnosed with overt diabetes. This one-step approach can be applied to well-resourced medical institutions. On the other hand, a two-step approach (step 1: fasting plasma glucose test; step 2: 75 g OGTT) is recommended if it is difficult to implement a formal 75 g OGTT in low-resourced rural areas of China. This stepwise approach fully considered the characteristics of imbalanced economic conditions in different regions of China and would help avoid almost half of the number of 75 g OGTT needed in China.43
To further standardize the diagnosis and management of GDM in China, the Obstetrics and Gynecology Branch of Chinese Medical Association as well as the Perinatal Medicine Branch of Chinese Medical Association formally published the “Guideline for Diagnosis and Treatment of Gestational Diabetes Mellitus (2014)”44 after repeated amendments to the 2007 guideline (draft).41 This guideline referred to the IADPSG diagnostic criteria of GDM proposed in 2010,19 the medical standards issued in China in 2011,42 the “Diagnostic and Classification Criteria for Hyperglycemia during Pregnancy” issued by WHO in 2013,21 and guidelines published by other international institutes and countries, adding more high-quality evidence for the diagnosis and treatment of GDM. The new guideline is more informative and clinically operable. This guideline quickly gained acceptance among medical institutes and health care practitioners across China. The current diagnostic criteria of GDM in China can be summarized as follows: (1) Screen for pregestational diabetes mellitus at the first prenatal visit: if FPG ≥7.0 mmol/L, or the 2-hour plasma glucose of 75 g OGTT ≥11.1 mmol/L, or random plasma glucose ≥11.1 mmol/L accompanied by typical hyperglycemia symptoms, the pregnant women should be diagnosed as pregestational diabetes mellitus. Glycohemoglobin (HbA1c) ≥6.5% is not recommended to be used as the screening tool for diabetes in China. (2) A 2-hour 75 g OGTT should be performed during 24–28 weeks of gestation in all pregnant women without overt diabetes. The GDM could be diagnosed if any of the OGTT plasma glucose values meets or exceeds the following cutoff values: 5.1 mmol/L at fasting; 10 mmol/L at 1 hour; and 8.5 mmol/L at 2 hours. (3) Although a 75 g OGTT is required to detect all women with GDM, due to the complexities of Chinese vast geography and population, this procedure is not feasible in many low-resourced medical centers and clinics in China. In these circumstances, FPG done during 24–28 gestational weeks, is an acceptable alternative approach to 75 g OGTT, to make a diagnosis in low-resourced regions to reduce the number of pregnant women requiring a formal OGTT, as it is relatively easy to perform, inexpensive, reliable, and reproducible. If FPG ≥5.1 mmol/L, GDM can be diagnosed; if FPG <4.4 mmol/L, women are less likely to develop GDM; only for those pregnant women with FPG above 4.4 mmol/L and below 5.1 mmol/L, a 75 g OGTT is needed for the diagnosis of GDM. (4) FPG levels in early pregnancy are not recommended to be used to diagnose GDM. This approach has been endorsed by FIGO.21 If a plasma calibrated glucometer is used in the point of care testing, women can be tested for the fasting glucose level and if the value is between 4.5 and 5.0 mmols/L they can be immediately given the 75 g glucose load and tested again after 2 hrs. this will ensure high compliance, low cost and no delay in compleing the test. Undoubtedly, this guideline has promoted the standardization of GDM diagnosis in different regions and makes it possible for the comparison of GDM prevalence in different parts of China. Figure 2 outlines the evolution of diagnostic criteria and guidelines for GDM in China.
Although Chinese research on clinical standardized diagnosis and treatment of GDM started relatively late, in just 20 years, Chinese scholars have made remarkable progress in the field of GDM research, and their academic achievements have been recognized by international counterparts. In 2019, “Standards of Medical Care in Diabetes-2019”,45 the most influential diabetes guideline based on clinical evidence issued by ADA, has cited 27 articles published by Chinese scholars; among them, 8 are original studies from the Department of Obstetrics and Gynecology, Peking University First Hospital (2 articles); Department of Endocrinology, Peking University People's Hospital; Department of Endocrinology, China-Japan Friendship Hospital, and others.
As we all know, with the implementation of contemporary criteria of GDM, the prevalence of GDM has increased significantly. Lifestyle interventions, including medical nutrition therapy and physical exercise, are the fundamental and most effective strategies for GDM prevention and management. In China, a GDM One-Day Care Program was launched in May 2011 at Peking University First Hospital to teach GDM patients the basic knowledge of GDM, weight management, medical nutrition therapy, physical exercise advice, and blood glucose self-monitoring methods by professional physicians, nurses, as well as clinical nutritionists. This GDM One-Day Care Model has been implemented throughout the country as part of the World Diabetes Foundation projects and many hospitals have followed and implemented this model. A prospective randomized clinical trial conducted at Peking University First Hospital has shown that supervised exercise training intervention (stationary cycling) three times per week for at least 30 minutes per session initiated early in pregnancy, could lead to a 45.8% reduction of GDM risk in overweight and obese pregnant women. Furthermore, no evidence to show that this exercise intervention increases the risk of preterm birth or reduces the mean gestational age at birth.46,47 Therefore, GDM One-Day Care Program is a good model for group management of GDM and more efforts are needed to promote its use on a larger scale.
The new IADPSG diagnostic criteria proposed that one or more OGTT values at each time point equal to or exceeding the thresholds should be diagnosed as GDM. However, whether different numbers of abnormalities for OGTT values or different characteristics of OGTT have different impacts on pregnancy outcomes have not been fully understood. Investigators from Peking University First Hospital carried out a study among 4090 GDM patients and divided them into three groups according to the number of abnormal OGTT values. Their results showed that as the number of abnormal OGTT values increased, the incidence of adverse pregnancy outcomes increased significantly, suggesting that we should pay more attention to intensive treatment for women with severe GDM.48 Moreover, Feng's study demonstrated that pregnant women with GDM and abnormal fasting glucose had a higher risk of macrosomia, large for gestational age (LGA), and cesarean delivery compared with normal fasting glucose, whereas pregnant women with GDM and hyperglycemia at 2 hour of OGTT had a higher risk of preterm birth and small for gestational age (SGA) than those with normal glucose at 2 hour.49 The above studies remind us to consider individualizing GDM management and use a hierarchical approach to management based on OGTT characteristics and the number of OGTT abnormalities.
Previous studies have focused on the impacts of GDM on short-term pregnancy outcomes and risk of type 2 diabetes mellitus after pregnancy; however, despite the known impact, the influence of GDM on long-term glucose metabolism of mothers and children have not been adequately addressed. Almost all guidelines suggest that attention should be paid to the postpartum follow-up of GDM. In recent years, HAPO has established a follow-up study (HAPO FUS) to evaluate the influence of GDM on maternal and children long-term outcomes, which might become the next milestone worth looking forward to in the future. The results demonstrate that after a median of 11.4 years, follow up among women with GDM compared to those without, GDM was significantly associated with development of maternal disorder of glucose metabolism.50 What's more interesting is that, offspring exposed to untreated GDM in utero were insulin resistant with limited β-cell compensation compared with offspring of mothers without GDM, and GDM was significantly and independently associated with childhood impaired glucose tolerance.51 However, it is unclear whether these results could be extrapolated to Chinese populations and whether these results would affect the diagnostic criteria of GDM. With the potential transgenerational impact of in utero exposure to GDM, well-powered studies are needed to address the impact of prevention and treatment of GDM on subsequent long-term outcomes in China to provide more informed perspective on public health implications and health policy development.
At present, China has established a Federation of Gestational Diabetes Mellitus and several multicenter, large-sample, and high-quality studies are underway. We believe that through bringing the best scientists and physicians in China together and with the combined use of large data resources and new technologies, the work of the Federation could help not only offer a unique opportunity to promote the standardization of GDM diagnosis prevention and care in China, but also establish an academic research platform and database, laying a solid foundation for the development of multicenter prospective studies in the future to accumulate more high-quality evidence in the field of GDM research and provide better evidence for decision making in China.
Conflicts of Interest
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