RESEARCH ARTICLE
A modified Mediterranean diet against gestational diabetes mellitus
Sha Xiao, Qianqian Zhang, Ming Zhang, Rong Hu and Rong Liu*
Department of Obstetrics and Gynecology, Tianjin First Center Hospital, Tianjin, China
Abstract
Healthy lifestyle is reported to reduce the prevalence of gestational diabetes mellitus (GDM). The association between Mediterranean diet (MD) and GDM incidence remains unclear in China. Therefore, we aim to establish a Chinese-habit-based MD recipe and explore its effects on GDM. This study recruited gestational age women who were planning a pregnancy in the near future with at least one risk factor for GDM. The participants were randomly allocated into the control and MD groups. They were required to follow diet interventions at least 6 months prior to pregnancy until delivery. Average dietary intake, glucose and insulin metabolism in 26–28-week of gestation, and maternal and neonatal outcomes were analyzed to assess the effects of MD. The clinical outcomes of 580 participants, with 294 in the MD group and 286 in the control group, were analyzed. It was revealed that the MD group had a high intake of protein, vitamins, and dietary fibers, whereas low intake of fat, resulting in improved insulin and glucose metabolism. Meanwhile, women and their newborns in the MD group showed a reduced proportion of complications. The modified MD intervention started before pregnancy shows a preventive effect against GDM and also benefits the mother and their newborns in other outcomes.
Keywords: Gestational diabetes mellitus (GDM); Mediterranean-like diet; diet intervention; improved outcomes
Citation: STEMedicine 2022, 3(3): e129 - http://dx.doi.org/10.37175/stemedicine.v3i3.129
Copyright: © 2022 Sha Xiao et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), allowing third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material for any purpose, even commercially, provided the original work is properly cited and states its license.
Received: 7 May 2022; Revised: 13 May 2022; Accepted: 18 May 2022; Published: 2 July 2022
Competing interests and funding: The authors declare that they have no conflict of interest. The authors have not received any funding or benefits from industry or elsewhere to conduct this study.
*Rong Liu, Department of Obstetrics and Gynecology, Tianjin First Center Hospital, Tianjin 300192, China. Email: liuronghch1999@sina.com
Gestational diabetes mellitus (GDM) represents ‘glucose intolerance that begins or is first diagnosed during pregnancy’ (1). GDM is manifested in not only glucose intolerance but also insulin resistance. In recent years, GDM has become one of the most serious risks for pregnant women, and the prevalence of GDM is increasing all over the world. It was reported that GDM is associated with various obstetric complications, including hydramnios and preterm delivery (2), and several adverse outcomes in newborns, such as congenital malformation and neonatal respiratory distress syndrome (3). In addition, women with a history of GDM are at an increased risk of type 2 diabetes mellitus (T2DM) in later life, and they are also exposed to a high risk of GDM relapse when they become pregnant again (4, 5). However, with the thorough liberalization of two-child policy in China, more Chinese women tend to have a second child, including those who had GDM before. To help women release the burden of GDM during their pregnancy, it is important to establish a new lifestyle, especially a healthy diet recipe in accordance with traditional Chinese eating habits.
Nowadays, a Mediterranean-style diet is regarded as a healthy eating habit, which is wildly adopted in Greece, Spain, France, and other southern European countries along the Mediterranean coast. A Mediterranean diet (MD) refers to high intake of vegetables, fruits, fish, nuts, and olive oil, while low intake of red meat and sugary drinks (6). Mounting evidence has demonstrated that keeping a MD effectively reduces the risk of various chronic diseases, such as cancer, cardiovascular disease, and obesity (7–9). Nevertheless, in China with a high incidence rate of GDM at 21.9%, few studies were conducted on the effectiveness of the MD on GDM before and during pregnancy.
In this study, we aimed to access whether the MD has a control effect on GDM among women aged between 18 and 50 years old with at least one risk factor for GDM who were planning a pregnancy in the near future.
Materials and methods
Study design
This is a retrospective study. The current randomized clinical trial adopted the per-protocol analysis and was conducted to lessen the potential confounding effects (10). Women were recruited through advertising, telephone inquiring, and health care consulting. The eligible participants with matched physical condition were assigned to two test groups. This study was approved by Tianjin First Center Hospital.
Inclusion criteria
Women were eligible to enter the clinical trial if they met the following three conditions: at high risk for GDM; planning for pregnancy in the near future; of the childbearing age between 18 and 50 years old. If the participants had at least one of the following risk factors: body mass index (BMI) exceeds 25 kg/m2; a history of GDM; any signs of obesity in their family; diagnosis of polycystic ovary syndrome (PCOS) before pregnancy, they were regarded as high-risk cohorts. All participants were required to provide a written informed consent before they were randomly assigned into either the intervention group or the control group. To ensure objectivity, a randomized assignment was performed by an experienced clinical staff utilizing computer-generated random numbers, and researchers were blind to the allocation results until they finished the final analyses.
The intervention started immediately when the participants were assigned into the test groups. To accurately analyze the effects of improved MD on GDM, a longer time was needed in this clinical trial since the diet intervention was a long process. To meet this purpose, we believed that the participants should receive at least 6 months of intervention before their pregnancy (11). Therefore, women who become pregnant within 6 months were excluded. Furthermore, women who had any of the following items were excluded at the beginning of the trial: under the age of 18; unmarried; smoking; alcohol drinking; being pregnant at the time of enrollment; suffering from other types of diseases, such as urolithiasis, kidney disease, thyroid diseases, or gastrointestinal diseases; HIV, Hep-B, or Hep-C positive patients; diagnosed with diabetes before randomization assignment. In addition, women who had taken illegal drugs or other insulin interfering drugs within 6 months before pregnancy (12) and those who did not agree to sign the informed consent for certain reasons were also excluded.
Intervention
The intervention was based on a MD and continued from randomized assignment to delivery. All the participants were requested to take a comprehensive physical examination before the randomized assignment, in order to ensure the balance and accuracy of the assignment. From the beginning of the intervention, recruited women were required to take a physical examination every 4 weeks at the same medical center. Once participants became pregnant, they were asked to follow physical examinations at least 1) once in the first 3 months, 2) once every month in the middle 3 months, 3) once every 2 weeks during 28–36 gestation weeks, and 4) once every week after 36 weeks, until they completed a safe delivery.
The traditional MD prefers to cook with extra virgin olive oil and recommends to keep low intake of red meat and processed meat (13), which is difficult for Chinese women to follow completely during the intervention. To solve this problem, we established a nutrition support team, containing five nutritionists and three obstetricians, to propose an improved Mediterranean-like diet, which is better adapted for Chinese women. The nutrition support team delivered the intervention over a personalized one-to-one session at the beginning of the intervention. Since olive oil was not widely accepted in China, participants were allowed to use the ordinary rapeseed oil as a substitute for olive oil, but with an allocated amount of no more than 0.3 L per week. In addition, given the fact that Chinese women show a higher potential for mild anemia and hypotension (14), a moderate consumption of red meat per day was recommended. Moreover, alcohol drinking was inappropriate for women during pre-pregnancy or pregnancy. Taken together, we formulated an adapted intervention plan based on the MD, including: replacing olive oil with rapeseed oil, soybean oil, or peanut oil, and the daily intake was controlled at lower than 30 g; keeping a daily consumption of red meat at 50–70 g; and alcohol drinking was prohibited. The improved MD recipe was more suitable for Chinese women and improved the compliance of this trial.
For their thorough understanding of the MD, participants were requested to join in a training class after being assigned to test groups. The training class lasted 40–60 min, and all participants were provided with MD guidance when they finished the training. The diet intervention officially started from this face-to-face consulting. In the middle of the intervention, we followed-up with the women every few days through phone calls or Wechat messages to reinforce the dietary goals. Furthermore, our nutritionists provided the latest information about the MD and recipe guidance during the trial. When the participants had any questions or suggestions about the intervention plan, they could communicate with their nutritionists or doctors through phone calls or Wechat at any time.
Participants in the control group received routine nutrition guidance and health care, but no dietary requirements. All participants were requested not to adjust their daily physical activity, and an exercise time no less than 30 min per day was recommended for both the intervention group and the control group.
Dietary assessment
We referred to the methodology of calculating MD scores to assess dietary conditions of the participants (15). Briefly, daily servings of vegetables, fruits, legumes, cereals, fish, dairy products, and meat were recorded and scored. All participants recorded their daily food and physical activities using a phone app named Nutritional Calculator. Then, the individual’s daily intake was calculated and averaged using the Nutritionist IV software (16). The participants’ MD adherence was evaluated once a month. According to the evaluation reports, we adjusted the diet recipe of each individual to ensure all the participants followed an accurate intervention.
Data collection
All the basic information of the recruited women was collected though a computerized questionnaire before they joined the clinical trial. To safeguard participant privacy, the information was only accessible to the professional administrators who performed data analysis. The information involved in the questionnaire was listed as follows:
- Sociodemographic data: age, marital status, number of children, and level of education.
- Physical condition: body weight, BMI, blood glucose, blood pressure, etc.
- Medical history of diseases: macrosomia in previous pregnancies, PCOS, earlier gestational glucose intolerance/GDM, family history of diabetes, mild anemia, hypotension, etc.
- Food consumption and dietary intake information: dietary preferences and appetite.
Outcome
In this study, the primary outcomes were the occurrence of women with GDM in 26–28 gestation weeks, the newborns’ birth weight, and neonatal Apgar score. GDM was diagnosed based on the oral glucose tolerance test (OGTT) in 26–28 gestation weeks (11). Once the OGTT of participants varied abnormally, appropriate intervention and treatment would be guided by healthcare specialists. The quantitative insulin check index (QUICKI), homeostasis model of assessment of insulin resistance (HOMA-IR), and homeostasis model of assessment of beta cell function (HOMA-b) were detected to assess insulin resistance (17). As for the neonatal outcome, the birthweight of newborns was recorded. The newborn whose birthweight exceeds 4,000 g was defined as macrosomia, while those less than 2,500 g were defined as underweight (18).
Secondary outcome was weight gain during pregnancy, which was calculated on the last measured weight before parturition and the weight measured at the beginning of the gestation. According to the guidelines of Institute of Medicine, excessive weight gain is defined as follows: > 18 kg for underweight; > 16 kg for normal weight; > 11.5 kg for overweight; and > 9 kg for obese. The definition was based on the initial BMI of participants. Moreover, preterm delivery, natural childbirth or cesarean delivery, preeclampsia after 20 weeks of gestation, and blood pressure were also considered as secondary outcomes.
Sample size
Initially, we used a randomized clinical trial calculation formula to design the sample size, in which the risk å = 0.05, risk ß = 0.2, and a rate of 20% for follow-up lose. According to a previous study (11), the incidence of GDM was 40% under usual prenatal care, whereas the intervention was supposed to reduce the proportion. The statistical power of the study was 0.8. On the basis of the assumption, a total of 749 eligible women were recruited in the clinical trial. Except for 169 dropouts in allocation and follow-up process, data from 580 participants were analyzed, with 294 in the MD group and 286 in the control group.
Statistical analysis
The data were analyzed according to the purpose of the intervention trial. The statistical analysis in the current study was performed utilizing SPSS, version 18 (SPSS Inc., Chicago, IL, USA). Data were expressed as mean (standard deviation [SD]) unless otherwise stated. Continuous and nominal data were analyzed by Student t-test and χ2-test, respectively. P < 0.05 was considered as statistically significant.
Results
The flow chat illustrating the study design is shown in Fig. 1. A total of 749 women were enrolled into our trial at the beginning. After assessing their baseline information for eligibility, 70 women were excluded, and the remaining 679 women were randomly assigned into the intervention (MD group, n = 339) or the control groups (n = 340). During the course of the study, ~15% of the participants were withdrawn from each group. The interference factors included: the participants did not conceive during the study; the participants became pregnant within 6 months; the participants felt sickness in stomach because of the diet intervention, etc. (Fig. 1). In the end, 294 participants in the MD group and 286 in the control group were followed up and included in the analysis.
Fig. 1. Flow diagram of the study design: participant selection, allocation, and follow-up. MD group, Mediterranean Diet group.
The baseline characteristics of the participants are summarized in Table 1. No significant differences were observed between the two groups in baseline characteristics, in terms of age [29.5(4.6) years in the MD group and 30.3(4.5) years in the control group] and BMI before pregnancy [27.4(4.4) kg/m2 in the MD group and 27.5(3.7) kg/m2 in the control group], or BMI after randomization [overweight 135(45.9%) and obese 12(4.1%) in the MD group, and overweight 137(47.9%) and obese 10(3.5%) in the control group]. In addition, the percentage of primiparous [43.2% in the MD group and 39.5% in the control group], proportion of macrosomia in previous pregnancies [4.1% in the MD group and 3.8% in the control group], earlier GDM [36 in the MD group and 34 in the control group], family history of diabetes [111 in the MD group and 107 in the control group], and PCOS [nine in the MD group and eight in the control group] as well as other sociodemographic data were also statistically same between all participants in the two groups. The time to pregnancy was 8.9(2.8) and 8.7(3.2) weeks for the MD group and the control group, respectively. No significant difference was observed.
Nutritional differences in daily intakes between MD and routine diet
Average dietary intakes of participants in the MD group and the control group are shown in Table 2. During the intervention, participants in the MD group were required to consume high intakes of vegetables, fruits, legumes, cereals, and fish, and low intake of processed meat and food rich in animal fat. Meanwhile, participants in the control group kept their normal eating habits that are common for Chinese: they took more red meat and refined grain in daily life. Table 2 shows that in comparison with the control group, participants in the MD group consumed more vegetables [558.25(147.69) g/day vs. 449.43(132.63) g/day, P = 0.008], legumes [443.61(257.44) g/day vs. 435.47(249.81) g/day, P = 0.032], fish [60.74(23.59) g/day vs. 41.75(26.28) g/day, P < 0.001], and dairy products [468.43(176.72) g/day vs. 316.25(189.69) g/day, P < 0.001]. On the contrary, the participants’ average consumption of meat and derivatives in the control group was significantly higher than that in the MD group [65.35(27.42) g/day vs. 57.92(24.66) g/day, P < 0.001]. In terms of nutritional components, a MD is rich in dietary fibers and protein, but low in fat and energy. Therefore, participants in the MD group had significantly higher protein [15.32(3.19) vs. 12.71(3.27) (% of total energy), P < 0.001], dietary fibers [29.73(8.93) (g/d) vs. 24.61(8.62) (g/d), P = 0.016], and B12 [29.73(8.93) (g/d) vs. 24.61(8.62) (μg/d), P = 0.016)], whereas lower level of energy [1961.84(124.93) (kcal/d) vs. 2042.63(116.67) (kcal/d), P = 0.018] and fat [20.45(7.44) vs. 23.62(6.53) (% of total energy), P = 0.006].
Glucose and insulin metabolism of the participants
Glucose and insulin metabolism of the participants were assessed by fasting blood glucose (FBG), HOMA-IR, HOMA-β, and QUIKI (Table 3). All the evaluated indicators were detected at both baseline and 26–28 weeks of gestation, in order to demonstrate the variation of glucose intolerance and insulin resistance as well as to diagnose GDM. From baseline to 26–28 gestational weeks, the FBG level of participants in the MD group remained unchanged [97.25(9.97) (mg/dL) vs. 95.46(9.12) (mg/dL), P = 0.153], whereas it significantly increased in the control group [94.09(7.23) (mg/dL) vs. 106.37(8.29) (mg/dL), P = 0.022]. Thus, a big difference in the FBG level was observed between the MD group and the control group [95.46(9.12) (mg/dL) vs. 106.37(8.29) (mg/dL), P = 0.032] after intervention. In addition, HOMA-IR [2.7(1.7) vs. 2.5(1.3), P = 0.232] and HOMA-β [46.7(17.4) vs. 47.4(15.3), P = 0.114] remain at the same level in the MD group, while slight increased levels were observed in the control group {HOMA-IR [12.9(6.2) vs. 15.9(6.9), P = 0.012], HOMA-β [46.3(18.2) vs. 55.1(19.7), P = 0.017]}. The insulin [12.6(4.3) (μIU/mL) vs. 15.9(6.9), P = 0.011], HOMA-IR [2.5(1.3) vs. 3.3(2.1), P = 0.012], and HOMA-β [47.4(15.3) vs. 55.1(19.7), P = 0.021] were also significantly different between the MD group and the control group during gestational 26–28 weeks. Moreover, the QUICKI score was improved in the MD group [0.47(0.16) vs. 0.49(0.15), P = 0.042], whereas it was decreased in the control group [0.48(0.17) vs. 0.36(0.18), P = 0.021]. The QUICKI score was greatly increased in the intervention group compared with the control group [0.49(0.15) vs. 0.36(0.18), P = 0.014]. These data indicated that the diet intervention had a positive effect on glucose and insulin metabolism for pregnant women.
Other maternal and neonatal outcomes
Besides glucose and insulin metabolism, we also analyzed other maternal physical symptoms and neonatal outcomes. The final results are summarized in Table 4. Both the proportions of women with GDM [24.8% vs. 33.9%, P = 0.013] and the proportion of participants with excessive gestational weight gain [26.9% vs. 37.1%, P = 0.044] were markedly decreased in the MD group. Nevertheless, the type of delivery, the percentage of preeclampsia [3.7% vs. 31%, P = 0.297], and the preterm delivery proportion [6.1% vs. 7%, P = 0.179] showed no differences between the two groups.
Among the newborns, the average birthweight in the two groups stayed in a comparable level, whereas the proportion of macrosomia was lower in the MD group than in the control group [3.4% vs. 4.2%, P = 0.038]. Meanwhile, the 5-min Apgar score was significantly higher in the MD group [9.6(0.7) vs. 9.2(0.6), P = 0.021]. In addition, the 1-min Apgar score [9.5(0.6) vs. 9.4(0.5), P = 0.238] and the percentage of underweight newborn [6.1% vs. 8.0%, 0.147] did not differ in the two groups.
The change of living habits is a long process. So, the effect of intervention duration on maternal and neonatal outcomes was also assessed. The mean duration of intervention is 13.5 ± 8.9 months before pregnancy for participants in the intervention group. They were further divided into two subgroups by the duration of intervention: ≤1 years and > 1 years. The difference in occurrence of GDM and pregnancy outcomes between these two subgroups were analyzed (Table 5). Gestational weight gain [35.3% vs. 14.9%, P = 0.014] and the proportion of macrosomia [4.0% vs. 2.5%, P = 0.045] seemed to be most tightly associated with the duration of intervention.
Discussion
In recent years, the incidence of GDM is rising steadily. GDM was reported to be a risk factor for T2DM and is also associated with various adverse outcomes, causing long-term sufferings for both the mothers and their newborns. However, there has been increasing evidence that suggests that healthy lifestyle intervention has the potential to benefit the women with GDM and/or T2DM. For instance, the American National Institutes of Health proposed the Diabetes Prevention Program (19), which means an individualized intervention of eating and physical activity, leading to a 50% decrease in diabetes incidence in the prediabetes cohorts. Similarly, GDM women followed 1 month of DASH (Dietary Approaches to Stop Hypertension) diet, which showed improved pregnancy outcomes (20). Besides, women in western countries who complied with a healthy diet before pregnancy, such as MD, exhibited an ameliorative glucose tolerance and lower incidence of GDM during their pregnancy. In order to demonstrate the effect of a healthy diet on GDM among Chinese women, in this study, we provided an improved MD in accordance with traditional Chinese eating habits and conducted an intervention trial before and during women’s pregnancy.
The typical MD emphasizes on high intakes of fruits, vegetables, whole grains, legumes, nuts, and olive oil; moderate intake of fish and dairy products; low consumption of healthy fats, such as poultry; and limited intake of red meat. Also, there are other important components in traditional MD, including a glass of red wine and keeping proper physical activity. From the perspective of nutrition, the MD is rich in mono- and poly-unsaturated fatty acids, protein, vitamins, and dietary fibers (21), which are beneficial for preventing many metabolic and chronic diseases. For example, Thaminda et al. (22) and Asemi (23) found that the MD protected against vascular and coronary heart diseases. Moreover, Letenneur et al. (24) found that MD had a potential to decrease the risk of Alzheimer’s disease and cognitive decline. Artal et al. (25) confirmed that the low-energy and low-fat diet resulted in a dramatic reduction in the risk of T2DM and obesity.
Nevertheless, it is difficult for Chinese people, especially pregnant and pre-pregnant women, to entirely follow the typical MD. Because the traditional Chinese diet is composed in a large proportion of refined grains and red meat, which is quite different from the MD. And women who become pregnant or prepare to be pregnant should not drink alcohol. According to this situation, to better investigate whether MD intervention benefits GDM outcomes among Chinese women, we proposed a Chinese-habit-based Mediterranean-like diet in our current clinical study. We replaced olive oil with rapeseed oil and added an appropriate consumption of red meat in the daily intake, due to Chinese women’s high incidence of mild anemia and hypotension during their gestation. In addition, all the participants were recommended to take proper physical exercise every day. Meanwhile, other elements of MD remained unchanged except for alcohol consumption.
In the present trial, we analyzed clinical outcomes of 580 participants: 294 in the MD group and 286 in the control group. At the beginning of the diet intervention, no significant differences in baseline characteristics were observed between the two groups, including the levels of glucose intolerance and insulin resistance (Tables 1, 3). During the intervention, the MD group consumed more vegetable, legumes, fish, and dairy products, whereas less meat and derivatives. That helped participants obtain better protein, vitamins, and dietary fibers but less fat (Table 2). As a result, when the participants entered their 26–28 weeks of gestation, the MD group showed improved insulin and glucose metabolism. But participants in the control group exhibited a worse glucose intolerance and insulin resistance, which associated with an increased incidence of GDM (Tables 3, 4). These data indicated that our Mediterranean-like diet intervention started before pregnancy, which exhibited a preventive effect against GDM. Our results were consistent with an earlier study, which suggested that high adherence to the MD was related to declined GDM incidence in a dose- and time-dependent manner (26).
Besides diabetic symptoms, we also evaluated other maternal outcomes and neonatal complications. As expected, women in the MD group had fewer cases of excessive gestational weight gain, and their newborns showed reduced proportion of macrosomia as well as higher 5-min Apgar score (Table 4). These data implied that the MD intervention improved not only the physical condition of gravidae but also that of their newborns. Consistently, Rogozińska et al. observed that MD intervention and physical activity lessened the caesarean section rates (27). The study of He and coworkers suggested that women who followed MD presented better postpartum recovery and declined incidence of neonatal complications (28). Therefore, we conclude that our MD intervention strongly ameliorates GDM among Chinese women, which also benefits both the mothers and their newborns in other pregnancy outcomes.
We used average daily nutritional intake to estimate adherence to the MD, while other studies used different methods, such as Trichopoulou index and 24 h diet score (29). Several studies demonstrated the effect of MD in women without GDM in their previous pregnancies (30, 31). Whereas in our study, we recruited women with a history of GDM into both the intervention and control group and then analyzed the GDM-preventing potential of MD. As for evaluating the diet quality, some study tended to separate the effects of each nutrient (32). However, when assessing the results of a diet intervention, we should give priority to the synergistic effects of all the components. We, therefore, conclude that our MD intervention has a positive effect on GDM improvement, although a few dietary components differed between the two groups. In the future study, it is worth studying whether the Chinese-habit-based MD also has beneficial effects on T2DM, which may provide a new reference for clinical treatment of T2DM.
A common limitation of long-term clinical trials is participant-loss during the follow-up. To solve this problem, participants were encouraged to record their daily intake and physical activity using a phone app named Nutritional Calculator, and professional administrators collected the participants’ information every day from the cloud data. Furthermore, we used Wechat to keep constant contact with the participants and reminded them to keep recording, which facilitated the interaction between researchers and the participants. Since we expected an attrition rate of 20%, it was rational that our overall follow-up rate was 85%. However, another possible limitation is the deviation from MD. Although we adjusted the participants’ MD recipe every month according to their records, women still tend to have their own preference for what they should consume. This was the major cause for inaccurate intervention, leading to biased dietary intake. Moreover, although we found a significant decline in some maternal outcomes, the type of delivery, the rates of preterm delivery, and preeclampsia were not influenced by MD intervention. Finally, a further modification should be done in traditional MD diet before the intervention can be utilized to other diseases.
Conclusion
In conclusion, a Mediterranean-like diet before and during pregnancy had a preventive effect on the GDM development, also improved several maternal and neonatal outcomes. For controlling the development of GDM, adherence to a Mediterranean-like diet prior to pregnancy should be promoted among all Chinese women.
Acknowledgments
None.
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