ORIGINAL ARTICLE
A Low Glycemic Index Staple Diet Reduces Postprandial Glucose Values in Asian Women With Gestational Diabetes Mellitus Zhi-Geng Hu, MD,* Rong-Shao Tan, MD, PhD,Þ Di Jin, MD, PhD,þ Wei Li, MS,* and Xiao-Yan Zhou, MS*
Background: A low glycemic index (GI) diet is beneficial for glucose control in patients with diabetes mellitus. This study aimed to investigate the influence of a low-GI diet on postprandial glucose levels in women with gestational diabetes mellitus (GDM). Methods: Pregnant women with GDM were randomized to receive a normal diabetic control diet or a low-GI staple diet for 5 days. A low-GI staple food was used to replace rice in lunch and dinner for the low-GI staple diet group, whereas the total energy and carbohydrate levels remained equal in both groups. Fasting and postprandial glucose levels were determined daily. Results: A total of 140 pregnant women with GDM were included in the study, including 66 in the low-GI staple diet group and 74 in the normal diabetic diet control group. No differences existed in baseline characteristics between the 2 groups (all P 9 0.05). After dietary intervention, glucose levels were significantly reduced in the low-GI staple diet group (all P G 0.01) and the control group (all P G 0.008). Postintervention glucose values after breakfast, lunch, and dinner were significantly reduced in the treatment group compared with those in the control group (all P G 0.05). The percentage changes from baseline of all glucose values were significantly greater in the treatment group than in the control group (all P G 0.05). Conclusions: A low-GI staple diet significantly reduces postprandial glucose levels in women with GDM. Key Words: glycemic index, gestational diabetes, postprandial glucose, staple food package (J Investig Med 2014;62: 975Y979)
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estational diabetes mellitus (GDM) refers to any degree of glucose intolerance at onset or at first recognition during pregnancy.1 In recent years, changes in lifestyle, unhealthy dietary behaviors, insufficient activity, and later childbearing have increased the incidence of GDM, with a reported incidence in China of 9.6%.2,3 Gestational diabetes mellitus is an important factor influencing the health of a pregnant women and her fetus, and studies have shown that the nutritional intake of pregnant women with GDM or type 2 diabetes mellitus is not
From the *Department of Clinical Nutrition, Zhu Jiang Hospital, Southern Medical University; †Department of Clinical Nutrition, Guangzhou Red Cross Hospital, Jinan University; and ‡Department of Clinical Nutrition, General Hospital of Guangzhou PLA, Guangzhou, China. Received January 17, 2014, and in revised form June 26, 2014. Accepted for publication July 27, 2014. Reprints: Zhi-Geng Hu, MD, Department of Clinical Nutrition, Zhu Jiang Hospital, Southern Medical University. No. 253,Gongye Rd, Guangzhou 510282, Guangdong Province, China. E-mail: [email protected]. The study was funded by the Science and Technology Project of Guangdong Province (no. 2009B030801205). Copyright * 2014 by The American Federation for Medical Research ISSN: 1081-5589 DOI: 10.1097/JIM.0000000000000108
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adequate and that women consume an undesirable ratio of macronutrients.4,5 Gestational diabetes mellitus is currently treated with blood glucose monitoring, dietary restrictions, and insulin when necessary. Previous studies have shown that dietary adjustments can safely and effectively treat GDM.2 Traditional dietary changes for treating GDM emphasize controlling the total energy intake (i.e., calories) and the ratio of the 3 major nutrients, protein, fats, and carbohydrates. In general, dietary control emphasizes the amount of carbohydrates consumed.2 However, this is may not be sufficient dietary control because the effects of different types of carbohydrates may influence insulin secretion and postprandial glucose levels.6Y8 Therefore, to be effective, a therapeutic diet for GDM must consider both the amount and types of carbohydrates. The glycemic index (GI) is a relative measure of the blood glucose response to a carbohydrate and is defined as the incremental area under the glucose response curve following the intake of 50 g of available carbohydrate from the test food as compared with the area generated from intake of an equal amount of available carbohydrate in the form of white bread or glucose.6,7 In general, foods with a lower GI produce a smaller glucose response than foods with a higher GI.6Y8 Studies have clearly shown that ingestion of foods with a high GI is associated with an increased risk of type 2 diabetes mellitus and coronary heart disease.9Y12 Although it remains unclear which diet is the most suitable and beneficial for women with GDM,13 studies have suggested that the use of a low-GI diet is beneficial for the control of glucose in patients with GDM.4,14Y18 Our prior study showed that the typical breakfast of Cantonese inhabitants of Guangdong consists of high-GI foods such as rice porridge, rice noodles, and steamed buns, which are all made with high-GI refined rice or wheat flour that may significantly increase postprandial glucose levels.19 Some people also consume these foods at lunch and dinner. However, the addition of coarse grains to their diet may reduce the GI.20 Our hypothesis was that replacing the rice-based staple diet typical of Asian populations, which is known to be of high GI,21 with a diet of low-GI staple foods may lower the postprandial glucose levels in women with GDM. The purpose of this study, therefore, was to investigate the effects of a low-GI staple diet on the postprandial glucose levels in patients with GDM. Realization of the beneficial effects of a low-GI staple diet on postprandial glucose levels may, in turn, improve blood glucose control and compliance of patients with GDM.
MATERIALS AND METHODS Patients Pregnant women at 23 to 35 weeks’ gestation with GDM were recruited from October 2011 to April 2013 from 3 hospitals in Guangzhou, China, and randomly assigned to a low-GI staple diet group and a control group. Gestational diabetes
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mellitus was defined as gestational diabetes mellitus with any degree of glucose intolerance at onset or at first recognition during pregnancy. Normal blood glucose values after a 75-g oral glucose tolerance test were defined as lower than 5.1, 10.0, and 8.5 mmol/L for fasting and 1 and 2 hours after the oral glucose load, respectively. Patients with any blood glucose abnormality were diagnosed with GDM as previously defined.1 Patients who required insulin or any glucose-lowering drug and those with preexisting diabetes mellitus were excluded from the study. This study was approved by the institutional review boards of the hospitals, and all patients provided written informed consent.
Diets All subjects were hospitalized 5 days for diet management. All meals, including prepackaged staple foods for both groups, were prepared by the Department of Dietetics of each hospital, and patients were not allowed to have any food other than that provided by the hospital. Diet management started on day 2 of hospitalization and finished on day 5. To help ensure compliance, all patients also received education regarding GDM, including the cause, the effects to the mother and fetus, the principles of diet management, and other treatments. The education was unified and provided by trained staff. Written educational materials were also given to the patients. In this study, low GI was defined as a GI of less than 55, medium as a GI of 55 to 75, and high GI as a GI of greater than 75. In the low-GI staple diet group, patients received low-GI staple foods and nutritional education. Patients in the control group received a routine staple food (white rice) diet to the same as a normal diabetic control diet for patients with GDM and nutritional education. The commercially prepared low-GI staple food packages were provided by the Guangzhou Zhonghui Boyuan Trade Development Co, Ltd, and other foods to complete the meals were commercially available. The low-GI staple food was used only to replace the general staple food (white rice) for the lunch and dinner meals. Except for foods in the staple diets given to each group, other foods were consistent between the 2 groups. All patients received the same breakfast, which was designed for patients with GDM.
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The low-GI staple food packages consisted of 5 commercial formulas that met the energy and carbohydrate composition determined by the research team, as previously described.6 One formula was used on each of the 5 days of hospitalization. The amount of food in each serving package was 82 g. Preparation of the food packages by the hospitals’ Department of Dietetics involved adding 80 mL of water into a container with 82 g of the foods, followed by heating for 30 minutes; this was considered the ‘‘staple diet.’’ The components and nutritional content of the diets are shown in Table 1. The food preparation was standardized to provide equal amounts of total energy and total carbohydrates for the control and low-GI staple diet group. In short, the amount of total carbohydrate in the control group was adjusted to fit the carbohydrate contents of the staple food packages used for the low-GI staple diet group. The composition of side dishes (including meat and cooking oil) were the same, but the amounts used were adjusted to account for the energy differences between the 2 groups to make the overall energy the same. The total energy provided to individual patients was adjusted under the guidance of dietitians, depending on the weight of the patient.
Blood Glucose Levels In all patients, capillary blood was collected, and fasting blood glucose (fasting plasma glucose or FPG) and postprandial blood glucose at 2 hours after each meal were measured as recommended in the most recent obstetrics and gynecology guidelines used by clinicians in China.22
Data Analysis Continuous data were presented as means and SDs, and categorical data were expressed as numbers and percentages. Differences between the treatment and control groups were detected using the independent t test for continuous data, and W2 test or Fisher exact test for categorical data, as appropriate. Differences between postintervention and baseline glucose levels were compared by paired t test. The percentage change from baseline was calculated as the difference between postintervention and preintervention (postintervention j baseline)
TABLE 1. Components and Nutritional Content of the Diets Nutritional Composition of Staple Foods Based on Equal Carbohydrates Diet
Weight, g
Staple Components
Energy,* kJ
Protein, g
Formula 1
82
1321
11.6
Control 1 Formula 2
66 82
960 1333
Control 2 Formula 3
69 82
Control 3 Formula 4
71
Control 4 Formula 5
67 82
Control 5
78
Rice from Northeast China (brown rice), peanut kernel (raw), peeled mung beans, green millet Steamed rice from Southern China Rice from Northeast China (brown rice), peanut kernel (raw), corn (grit), green millet Steamed rice from Southern China Rice from Northeast China (brown rice), peanut kernel (raw), buckwheat, green millet Steamed rice from Southern China Rice from Northeast China (brown rice), corn, buckwheat, green millet Steamed rice from Southern China Rice from Northeast China (brown rice), peeled mung beans, buckwheat, green millet Steamed rice from Southern China
Fat, g
Carbohydrates, g
8
51.4
4.9 9.3
0.5 8.6
51.4 53.5
1006 1296
5.1 9.0
0.6 7.0
53.7 55
1032 1166
5.2 6.5
0.7 1.2
55 52
975 1158
5 8.1
0.5 0.8
52.2 61.1
1140
5.8
0.6
61
*The amounts of side dishes were adjusted for equal energy and carbohydrates.
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Low GI Diet and Gestational DM in Asians
TABLE 2. Baseline Characteristics of the Control and Low-GI Staple Diet Groups Control (n = 74) 29.7 T 27.9 T 52.7 T 20.9 T
Age, y Gestational age, wk Weight before pregnancy, kg BMI before pregnancy. kg/m2 Parity 1 2 3 Family history of DM‡ No Yes
P
Low-GI Staple Diet (n = 66) 30.3 T 27.0 T 54.3 T 21.2 T
3.7 3.8 8.9 3.4
4.9 2.7 7.1 2.5
0.454* 0.102* 0.264* 0.532*
68 (91.9) 4 (5.4) 2 (2.7)
62 (93.9) 4 (6.1) 0 (0.0)
0.639†
59 (84.3) 11 (15.7)
53 (81.5) 12 (18.5)
0.671§
Data are presented as mean T SD or number (percentage). *Determined by independent t test. †Determined by Fisher exact test. ‡Family history of DM was unknown for 4 patients in the control group and 1 in the treatment group. §Determined by W2 test. BMI indicates body mass index; DM, diabetes mellitus.
relative to the baseline level. Statistical analyses were performed with SAS software version 9.2 (SAS Institute Inc, Cary, NC). A 2-tailed P G 0.05 was considered to indicate statistical significance.
RESULTS Patient Baseline Characteristics A total of 140 pregnant women with GDM were enrolled in this study, with 74 in the control group and 66 in the low-GI staple diet group. The baseline characteristics of the patients are shown in Table 2. All women were free from tobacco smoking and alcohol consumption and had singleton pregnancies. Most of patients were primiparous (control vs low-GI staple diet group: 91.9% vs 93.9%) and did not have a family history of diabetes mellitus (control vs low-GI staple group: 84.3% vs 81.5%). All baseline characteristics were similar between the 2 groups (all P 9 0.05, Table 2).
measurements between the 2 groups (all P 9 0.05). After dietary intervention, blood glucose values at all time points were reduced in both groups. Among subjects in the control group, significant decreases in glucose levels were noted after breakfast (P G 0.001), after lunch (P G 0.001), and after dinner (P = 0.008), whereas all blood glucose measurements were significantly reduced in treatment group (all P G0.01). A comparison of postintervention glucose values showed that glucose levels after breakfast, lunch, and dinner were significantly lower in the treatment group than in the control group (all P G 0.05). The percentage changes from baseline of fasting blood glucose and glucose level after breakfast, after lunch, and after dinner were j1.2%, j11.9%, j8.0%, and j7.3% in the control group and j3.7%, j18.7%, j20.3%, and j22.1% in the treatment group, respectively. The percentage changes from baseline were significantly greater in the treatment group than in the control group for all blood glucose measurement (all P G 0.05).
Blood Glucose Levels The comparisons of blood glucose levels between the treatment and control groups are shown in Table 3. No significant differences were found in all baseline blood glucose
DISCUSSION In this study, we replaced white rice, a high-GI staple food, with a low-GI staple food in the diet of women diagnosed with
TABLE 3. Comparison of Blood Glucose Levels Between the 2 Groups Control (n = 74) Baseline Blood glucose, mmol/L Fasting 4.99 After breakfast 7.86 After lunch 7.51 After dinner 7.69
T 0.56 T 1.17 T 1.02 T 1.08
Postintervention 4.90 T 6.84 T 6.86 T 7.14 T
0.46 0.84† 0.66† 2.05†
Low-GI Staple Diet (n = 66)
Percentage Change From Baseline,* % j1.2 T j11.9 T j8.0 T j7.3 T
6.8 11.1 7.9 17.7
Baseline 5.09 T 8.21 T 7.67 T 7.91 T
0.78 1.42 0.95 1.02
Postintervention 4.87 6.52 6.05 6.07
T 0.49† T 0.68†‡ T 0.85†‡ T 0.77†‡
Percentage Change from Baseline,* % j3.7 T 7.6‡ j18.7 T 14.0‡ j20.3 T 11.9‡ j22.1 T 13.4‡
Data are presented a mean T SD. *Calculated as [(postintervention j baseline) / baseline 100%]. †P G 0.05 compared with baseline, determined by paired t test ‡P G 0.05 compared with control group, determined by independent t test.
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GDM and found that the low-GI staple diet was associated with significantly reduced postprandial glucose levels as compared with the normal diet consisting of a white rice staple. To our knowledge, this is the first study of the effect of a low-GI staple diet conducted solely in an Asian population of women with GDM. In 1981, Jenkins et al.6 for the first time proposed the concept of GI as an effective physiological parameter for determining the effect of different foods on blood glucose levels. Low-GI foods are generally fresh and unprocessed, and examples include milk, whole grains, fresh fruits, legumes, and nuts.23 LowGI foods tend to produce lower postprandial glucose levels than foods with a high GI.6Y8 The European Diabetes Nutrition Research Group24 and World Health Organization25 recommend low-GI diets for patients with diabetes mellitus, and the American Diabetes Association recommends a low-GI diet rich in dietary fiber and important nutrients.26 In South China, the high-carbohydrate, high-GI staple diet rich in refined rice and its processed products20 does not support blood glucose control in patients with GDM. Contrary to the recommendations of leading diabetes organizations, the southern Chinese staple diet is low in fiber and essential nutrients. Our findings are consistent with those of prior studies in which the GI theory was used in the nutritional education and treatment of patients with type 2 diabetes mellitus and showed that a low-GI diet significantly reduced postprandial glucose levels.7,27Y29 Although fewer studies have examined the effects of low-GI foods on women with GDM, those conducted have shown promising results. Grant et al.16 randomized women with GDM or impaired glucose tolerance of pregnancy to a low-GI or control diet and found that the low-GI diet was associated with better postprandial glucose control. Moses et al.14 randomized 63 women with GDM to a low-GI diet or conventional high-fiber diet and found that the low-GI diet reduced the number of women requiring insulin for glucose control by 50%. A recent review of the literature by Louie et al.17 concluded that although current evidence is limited, studies support the advantages of and demonstrate no disadvantages of a low-GI diet for the treatment of women with GDM. Traditional nutritional therapy focuses on the amount of total energy consumed, the ratio of the 3 major nutrients, and the amount of carbohydrates rather than the type and preparation of carbohydrates. Measures in nutritional therapy may require individuals to deal with complex calculations, strict weighing, and separate meal preparation. However, the GI of foods can become intuitive with some education, allowing patients to select foods simply and conveniently. Besides the demonstrated advantages of low-GI diets for women with GDM,7,27Y29 the low-GI diet overcomes the inherent difficulties in the selection, matching, weighing, and cooking of foods that are recommended in traditional diabetic diets. The diet in South China is rich in rice, and the diet in the control group was comparable before and after intervention, but after standardization to provide equal amounts of total energy and total carbohydrates as in the low-GI staple diet of the treatment group, the 2 groups consumed similar diets and the same side dishes with the same amount of total carbohydrates and total energy, except for the low-GI staple food given to the low-GI staple diet group. The amount of carbohydrates in the control group was adjusted to fit the carbohydrate contents of the staple food packages used for the low-GI staple diet group. This suggests that the reduction in blood glucose seen in the control group may be attributed to the overall similarity of the 2 diets in dietary control of glucose metabolism as well as to nutritional education. Although we did not make any
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comparisons of the quantity of staple food consumed by either group prior to the study, it appears that both groups benefitted from the standardized diets. Blood glucose levels after breakfast were also reduced in both groups, but low-GI staple foods were not used in the breakfast meal. This suggests that the reduction in blood glucose after breakfast is related to the influence of low-GI staple foods consumed regularly in lunch and dinner each day. We also believe that the overall reductions in blood glucose levels are supported by education provided about GDM, which motivates participants to adhere to the diets as prescribed. There are limitations to this study that should be considered. The study population consisted only of Asians who consume rice as the primary staple, and thus the results may not be generalizable to other populations. On the other hand, the results clearly show the benefit of a low-GI staple diet in Asian women with GDM. In addition, although a benefit was seen in Asian women with GDM, determination of the benefit of a low-GI staple diet in a general Asian population will require further study.
CONCLUSIONS The results of this study showed that substitution of white rice, a high-GI food, with a low-GI staple food in the diet of women diagnosed with GDM resulted in significantly reduced postprandial glucose levels as compared with the normal white riceYbased staple diet. These results suggest that a low-GI staple diet is useful for glucose control in patients with GDM. REFERENCES 1. Metzger BE, Coustan DR, eds. Proceedings of the Fourth International Work-shopVconference on gestational diabetes mellitus. Diabetes Care. 1998;21(suppl 2):B1YB167; 1998. 2. Diabetes Society of Chinese Medical Association. China Medical Nutritional Therapy Guideline for Diabetes. Merck Serono Co. Ltd. China: Beijing, P.R. China, 2010. 3. Lin Y, Lin YP, Lin JX. Incidence of gestational diabetes mellitus and monitoring of blood glucose in patients of different age groups. Strait J Prev Med. 2012;12:93. 4. Scholl TO, Chen X, Khoo CS, et al. The dietary glycemic index during pregnancy: influence on infant birth weight, fetal growth, and biomarkers of carbohydrate metabolism. Am J Epidemiol. 2004;159:467Y474. 5. Lim SY, Yoo HJ, Kim AL, et al. Nutritional intake of pregnant women with gestational diabetes or type 2 diabetes mellitus. Clin Nutr Res. 2013;2:81Y90. 6. Jenkins DJ, Wolever TM, Taylor RH, et al. Glycemic index of foods: a physiological basis for carbohydrate exchange. Am J Clin Nutr. 1981;34:362Y366. 7. Jenkins DJ, Kendall CW, Augustin LS, et al. Glycemic index: overview of implications in health and disease. Am J Clin Nutr. 2002;76:266Y273. 8. Wolever TMS, Jenkins DJA. The use of the glycemic index in predicting blood glucose response to mixed meals. Am J Clin Nutr. 1986;43:167Y172. 9. Schwingshackl L, Hoffmann G. Long-term effects of low glycemic index/load vs. high glycemic index/load diets on parameters of obesity and obesity-associated risks: a systematic review and meta-analysis. Nutr Metab Cardiovasc Dis. 2013;23:699Y706. 10. Salmeron J, Manson JE, Stampfer MJ, et al. Dietary fiber, glycemic load, and risk of nonYinsulin-dependent diabetes mellitus in women. JAMA. 1997;277:472Y477. 11. Salmeron J, Ascherio A, Rimm EB, et al. Dietary fiber, glycemic load and risk of NIDDM in men. Diabetes Care. 1997;20:545Y550.
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Low GI Diet and Gestational DM in Asians
12. Liu S, Willett WC, Salmeron J, et al. A prospective study of dietary glycemic load, carbohydrate intake, and risk of coronary heart disease. Am J Clin Nutr. 2000;71:1455Y1461.
21. Ding EL, Malik VS. Convergence of obesity and high glycemic diet on compounding diabetes and cardiovascular risks in modernizing China: an emerging public health dilemma. Global Health. 2008;4:4.
13. Han S, Crowther CA, Middleton P, et al. Different types of dietary advice for women with gestational diabetes mellitus. Cochrane Database Syst Rev. 2013;(3):CD009275.
22. Xie X, Guo W, eds. Obstetrics and Gynecology. 8th ed. Beijing, China: Peoples Health Publishing House; 2013.
14. Moses RG, Barker M, Winter M, et al. Can a low-glycemic index diet reduce the need for insulin in gestational diabetes mellitus? A randomized trial. Diabetes Care. 2009;32:996Y1000. 15. Gunderson EP. Gestational diabetes and nutritional recommendations. Curr Diab Rep. 2004;4:377Y86. 16. Grant SM, Wolever TM, O’Connor DL, et al. Effect of a low glycaemic index diet on blood glucose in women with gestational hyperglycaemia. Diabetes Res Clin Pract. 2011;91:15Y22. 17. Louie JC, Brand-Miller JC, Moses RG. Carbohydrates, glycemic index, and pregnancy outcomes in gestational diabetes. Curr Diab Rep. 2013;13:6Y11. 18. Louie JC, Markovic TP, Perera N, et al. A randomized controlled trial investigating the effects of a low-glycemic index diet on pregnancy outcomes in gestational diabetes mellitus. Diabetes Care. 2011;34:2341Y2346. 19. Hu ZG, Li W, Feng CS. A correlation study between glycemic index and breakfast foods in Guangdong residents. J Trop Med. 2011;1:82Y84. 20. Hu ZG, Li W, Zhou XY, et al. The glycemic index of mixed staple food. Guangdong Med J. 2013;7:1032Y1035.
23. Foster-Powell K, Holt SH, Brand-Miller JC. International table of glycemic index and glycemic load values: 2002. Am J Clin Nutr. 2002;76:5Y56. 24. Diabetes and Nutrition Study Group (DNSG) of the European Association for the Study of Diabetes (EASD). Recommendations for the nutritional management of patients with diabetes mellitus. Diabetes Nutr Metab. 1995;8:186Y189. 25. Carbohydrates in human nutrition. Report of a Joint FAO/WHO Expert Consultation, Rome, April, 14Y18, 1997. FAO Food and Nutrition Paper 66. Rome, Italy: Food & Agriculture Organization of the United Nations (FAO), 1998. 26. American Diabetes Association. Nutrition Recommendations and Interventions for Diabetes: a position statement of the American Diabetes Association. Diabetes Care. 2007;30(suppl 1):S48YS65. 27. Sun JQ, Shen XH, Chen XF. Glycemic index of foods and prevention and treatment of diabetes mellitus. Parenter Enteral Nutr. 2005;12:311Y314. 28. Brand-Miller JC. Postprandial glycemia, glycemic index, and the prevention of type 2 diabetes. Am J Clin Nutr. 2004;80:243Y244. 29. Ge Q, Lin J, Zhang BF, et al. Observation of nutritional therapy using glycemic index and food exchange for type 2 diabetes mellitus. J Clin Exp Med. 2008;12:5Y6.
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A Low Glycemic Index Staple Diet Reduces Postprandial Glucose Values in Asian Women With Gestational Diabetes Mellitus Zhi-Geng Hu, MD,* Rong-Shao Tan, MD, PhD,Þ Di Jin, MD, PhD,þ Wei Li, MS,* and Xiao-Yan Zhou, MS*
Background: A low glycemic index (GI) diet is beneficial for glucose control in patients with diabetes mellitus. This study aimed to investigate the influence of a low-GI diet on postprandial glucose levels in women with gestational diabetes mellitus (GDM). Methods: Pregnant women with GDM were randomized to receive a normal diabetic control diet or a low-GI staple diet for 5 days. A low-GI staple food was used to replace rice in lunch and dinner for the low-GI staple diet group, whereas the total energy and carbohydrate levels remained equal in both groups. Fasting and postprandial glucose levels were determined daily. Results: A total of 140 pregnant women with GDM were included in the study, including 66 in the low-GI staple diet group and 74 in the normal diabetic diet control group. No differences existed in baseline characteristics between the 2 groups (all P 9 0.05). After dietary intervention, glucose levels were significantly reduced in the low-GI staple diet group (all P G 0.01) and the control group (all P G 0.008). Postintervention glucose values after breakfast, lunch, and dinner were significantly reduced in the treatment group compared with those in the control group (all P G 0.05). The percentage changes from baseline of all glucose values were significantly greater in the treatment group than in the control group (all P G 0.05). Conclusions: A low-GI staple diet significantly reduces postprandial glucose levels in women with GDM. Key Words: glycemic index, gestational diabetes, postprandial glucose, staple food package (J Investig Med 2014;62: 975Y979)
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estational diabetes mellitus (GDM) refers to any degree of glucose intolerance at onset or at first recognition during pregnancy.1 In recent years, changes in lifestyle, unhealthy dietary behaviors, insufficient activity, and later childbearing have increased the incidence of GDM, with a reported incidence in China of 9.6%.2,3 Gestational diabetes mellitus is an important factor influencing the health of a pregnant women and her fetus, and studies have shown that the nutritional intake of pregnant women with GDM or type 2 diabetes mellitus is not
From the *Department of Clinical Nutrition, Zhu Jiang Hospital, Southern Medical University; †Department of Clinical Nutrition, Guangzhou Red Cross Hospital, Jinan University; and ‡Department of Clinical Nutrition, General Hospital of Guangzhou PLA, Guangzhou, China. Received January 17, 2014, and in revised form June 26, 2014. Accepted for publication July 27, 2014. Reprints: Zhi-Geng Hu, MD, Department of Clinical Nutrition, Zhu Jiang Hospital, Southern Medical University. No. 253,Gongye Rd, Guangzhou 510282, Guangdong Province, China. E-mail: [email protected]. The study was funded by the Science and Technology Project of Guangdong Province (no. 2009B030801205). Copyright * 2014 by The American Federation for Medical Research ISSN: 1081-5589 DOI: 10.1097/JIM.0000000000000108
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adequate and that women consume an undesirable ratio of macronutrients.4,5 Gestational diabetes mellitus is currently treated with blood glucose monitoring, dietary restrictions, and insulin when necessary. Previous studies have shown that dietary adjustments can safely and effectively treat GDM.2 Traditional dietary changes for treating GDM emphasize controlling the total energy intake (i.e., calories) and the ratio of the 3 major nutrients, protein, fats, and carbohydrates. In general, dietary control emphasizes the amount of carbohydrates consumed.2 However, this is may not be sufficient dietary control because the effects of different types of carbohydrates may influence insulin secretion and postprandial glucose levels.6Y8 Therefore, to be effective, a therapeutic diet for GDM must consider both the amount and types of carbohydrates. The glycemic index (GI) is a relative measure of the blood glucose response to a carbohydrate and is defined as the incremental area under the glucose response curve following the intake of 50 g of available carbohydrate from the test food as compared with the area generated from intake of an equal amount of available carbohydrate in the form of white bread or glucose.6,7 In general, foods with a lower GI produce a smaller glucose response than foods with a higher GI.6Y8 Studies have clearly shown that ingestion of foods with a high GI is associated with an increased risk of type 2 diabetes mellitus and coronary heart disease.9Y12 Although it remains unclear which diet is the most suitable and beneficial for women with GDM,13 studies have suggested that the use of a low-GI diet is beneficial for the control of glucose in patients with GDM.4,14Y18 Our prior study showed that the typical breakfast of Cantonese inhabitants of Guangdong consists of high-GI foods such as rice porridge, rice noodles, and steamed buns, which are all made with high-GI refined rice or wheat flour that may significantly increase postprandial glucose levels.19 Some people also consume these foods at lunch and dinner. However, the addition of coarse grains to their diet may reduce the GI.20 Our hypothesis was that replacing the rice-based staple diet typical of Asian populations, which is known to be of high GI,21 with a diet of low-GI staple foods may lower the postprandial glucose levels in women with GDM. The purpose of this study, therefore, was to investigate the effects of a low-GI staple diet on the postprandial glucose levels in patients with GDM. Realization of the beneficial effects of a low-GI staple diet on postprandial glucose levels may, in turn, improve blood glucose control and compliance of patients with GDM.
MATERIALS AND METHODS Patients Pregnant women at 23 to 35 weeks’ gestation with GDM were recruited from October 2011 to April 2013 from 3 hospitals in Guangzhou, China, and randomly assigned to a low-GI staple diet group and a control group. Gestational diabetes
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mellitus was defined as gestational diabetes mellitus with any degree of glucose intolerance at onset or at first recognition during pregnancy. Normal blood glucose values after a 75-g oral glucose tolerance test were defined as lower than 5.1, 10.0, and 8.5 mmol/L for fasting and 1 and 2 hours after the oral glucose load, respectively. Patients with any blood glucose abnormality were diagnosed with GDM as previously defined.1 Patients who required insulin or any glucose-lowering drug and those with preexisting diabetes mellitus were excluded from the study. This study was approved by the institutional review boards of the hospitals, and all patients provided written informed consent.
Diets All subjects were hospitalized 5 days for diet management. All meals, including prepackaged staple foods for both groups, were prepared by the Department of Dietetics of each hospital, and patients were not allowed to have any food other than that provided by the hospital. Diet management started on day 2 of hospitalization and finished on day 5. To help ensure compliance, all patients also received education regarding GDM, including the cause, the effects to the mother and fetus, the principles of diet management, and other treatments. The education was unified and provided by trained staff. Written educational materials were also given to the patients. In this study, low GI was defined as a GI of less than 55, medium as a GI of 55 to 75, and high GI as a GI of greater than 75. In the low-GI staple diet group, patients received low-GI staple foods and nutritional education. Patients in the control group received a routine staple food (white rice) diet to the same as a normal diabetic control diet for patients with GDM and nutritional education. The commercially prepared low-GI staple food packages were provided by the Guangzhou Zhonghui Boyuan Trade Development Co, Ltd, and other foods to complete the meals were commercially available. The low-GI staple food was used only to replace the general staple food (white rice) for the lunch and dinner meals. Except for foods in the staple diets given to each group, other foods were consistent between the 2 groups. All patients received the same breakfast, which was designed for patients with GDM.
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The low-GI staple food packages consisted of 5 commercial formulas that met the energy and carbohydrate composition determined by the research team, as previously described.6 One formula was used on each of the 5 days of hospitalization. The amount of food in each serving package was 82 g. Preparation of the food packages by the hospitals’ Department of Dietetics involved adding 80 mL of water into a container with 82 g of the foods, followed by heating for 30 minutes; this was considered the ‘‘staple diet.’’ The components and nutritional content of the diets are shown in Table 1. The food preparation was standardized to provide equal amounts of total energy and total carbohydrates for the control and low-GI staple diet group. In short, the amount of total carbohydrate in the control group was adjusted to fit the carbohydrate contents of the staple food packages used for the low-GI staple diet group. The composition of side dishes (including meat and cooking oil) were the same, but the amounts used were adjusted to account for the energy differences between the 2 groups to make the overall energy the same. The total energy provided to individual patients was adjusted under the guidance of dietitians, depending on the weight of the patient.
Blood Glucose Levels In all patients, capillary blood was collected, and fasting blood glucose (fasting plasma glucose or FPG) and postprandial blood glucose at 2 hours after each meal were measured as recommended in the most recent obstetrics and gynecology guidelines used by clinicians in China.22
Data Analysis Continuous data were presented as means and SDs, and categorical data were expressed as numbers and percentages. Differences between the treatment and control groups were detected using the independent t test for continuous data, and W2 test or Fisher exact test for categorical data, as appropriate. Differences between postintervention and baseline glucose levels were compared by paired t test. The percentage change from baseline was calculated as the difference between postintervention and preintervention (postintervention j baseline)
TABLE 1. Components and Nutritional Content of the Diets Nutritional Composition of Staple Foods Based on Equal Carbohydrates Diet
Weight, g
Staple Components
Energy,* kJ
Protein, g
Formula 1
82
1321
11.6
Control 1 Formula 2
66 82
960 1333
Control 2 Formula 3
69 82
Control 3 Formula 4
71
Control 4 Formula 5
67 82
Control 5
78
Rice from Northeast China (brown rice), peanut kernel (raw), peeled mung beans, green millet Steamed rice from Southern China Rice from Northeast China (brown rice), peanut kernel (raw), corn (grit), green millet Steamed rice from Southern China Rice from Northeast China (brown rice), peanut kernel (raw), buckwheat, green millet Steamed rice from Southern China Rice from Northeast China (brown rice), corn, buckwheat, green millet Steamed rice from Southern China Rice from Northeast China (brown rice), peeled mung beans, buckwheat, green millet Steamed rice from Southern China
Fat, g
Carbohydrates, g
8
51.4
4.9 9.3
0.5 8.6
51.4 53.5
1006 1296
5.1 9.0
0.6 7.0
53.7 55
1032 1166
5.2 6.5
0.7 1.2
55 52
975 1158
5 8.1
0.5 0.8
52.2 61.1
1140
5.8
0.6
61
*The amounts of side dishes were adjusted for equal energy and carbohydrates.
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Journal of Investigative Medicine
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Low GI Diet and Gestational DM in Asians
TABLE 2. Baseline Characteristics of the Control and Low-GI Staple Diet Groups Control (n = 74) 29.7 T 27.9 T 52.7 T 20.9 T
Age, y Gestational age, wk Weight before pregnancy, kg BMI before pregnancy. kg/m2 Parity 1 2 3 Family history of DM‡ No Yes
P
Low-GI Staple Diet (n = 66) 30.3 T 27.0 T 54.3 T 21.2 T
3.7 3.8 8.9 3.4
4.9 2.7 7.1 2.5
0.454* 0.102* 0.264* 0.532*
68 (91.9) 4 (5.4) 2 (2.7)
62 (93.9) 4 (6.1) 0 (0.0)
0.639†
59 (84.3) 11 (15.7)
53 (81.5) 12 (18.5)
0.671§
Data are presented as mean T SD or number (percentage). *Determined by independent t test. †Determined by Fisher exact test. ‡Family history of DM was unknown for 4 patients in the control group and 1 in the treatment group. §Determined by W2 test. BMI indicates body mass index; DM, diabetes mellitus.
relative to the baseline level. Statistical analyses were performed with SAS software version 9.2 (SAS Institute Inc, Cary, NC). A 2-tailed P G 0.05 was considered to indicate statistical significance.
RESULTS Patient Baseline Characteristics A total of 140 pregnant women with GDM were enrolled in this study, with 74 in the control group and 66 in the low-GI staple diet group. The baseline characteristics of the patients are shown in Table 2. All women were free from tobacco smoking and alcohol consumption and had singleton pregnancies. Most of patients were primiparous (control vs low-GI staple diet group: 91.9% vs 93.9%) and did not have a family history of diabetes mellitus (control vs low-GI staple group: 84.3% vs 81.5%). All baseline characteristics were similar between the 2 groups (all P 9 0.05, Table 2).
measurements between the 2 groups (all P 9 0.05). After dietary intervention, blood glucose values at all time points were reduced in both groups. Among subjects in the control group, significant decreases in glucose levels were noted after breakfast (P G 0.001), after lunch (P G 0.001), and after dinner (P = 0.008), whereas all blood glucose measurements were significantly reduced in treatment group (all P G0.01). A comparison of postintervention glucose values showed that glucose levels after breakfast, lunch, and dinner were significantly lower in the treatment group than in the control group (all P G 0.05). The percentage changes from baseline of fasting blood glucose and glucose level after breakfast, after lunch, and after dinner were j1.2%, j11.9%, j8.0%, and j7.3% in the control group and j3.7%, j18.7%, j20.3%, and j22.1% in the treatment group, respectively. The percentage changes from baseline were significantly greater in the treatment group than in the control group for all blood glucose measurement (all P G 0.05).
Blood Glucose Levels The comparisons of blood glucose levels between the treatment and control groups are shown in Table 3. No significant differences were found in all baseline blood glucose
DISCUSSION In this study, we replaced white rice, a high-GI staple food, with a low-GI staple food in the diet of women diagnosed with
TABLE 3. Comparison of Blood Glucose Levels Between the 2 Groups Control (n = 74) Baseline Blood glucose, mmol/L Fasting 4.99 After breakfast 7.86 After lunch 7.51 After dinner 7.69
T 0.56 T 1.17 T 1.02 T 1.08
Postintervention 4.90 T 6.84 T 6.86 T 7.14 T
0.46 0.84† 0.66† 2.05†
Low-GI Staple Diet (n = 66)
Percentage Change From Baseline,* % j1.2 T j11.9 T j8.0 T j7.3 T
6.8 11.1 7.9 17.7
Baseline 5.09 T 8.21 T 7.67 T 7.91 T
0.78 1.42 0.95 1.02
Postintervention 4.87 6.52 6.05 6.07
T 0.49† T 0.68†‡ T 0.85†‡ T 0.77†‡
Percentage Change from Baseline,* % j3.7 T 7.6‡ j18.7 T 14.0‡ j20.3 T 11.9‡ j22.1 T 13.4‡
Data are presented a mean T SD. *Calculated as [(postintervention j baseline) / baseline 100%]. †P G 0.05 compared with baseline, determined by paired t test ‡P G 0.05 compared with control group, determined by independent t test.
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Journal of Investigative Medicine
GDM and found that the low-GI staple diet was associated with significantly reduced postprandial glucose levels as compared with the normal diet consisting of a white rice staple. To our knowledge, this is the first study of the effect of a low-GI staple diet conducted solely in an Asian population of women with GDM. In 1981, Jenkins et al.6 for the first time proposed the concept of GI as an effective physiological parameter for determining the effect of different foods on blood glucose levels. Low-GI foods are generally fresh and unprocessed, and examples include milk, whole grains, fresh fruits, legumes, and nuts.23 LowGI foods tend to produce lower postprandial glucose levels than foods with a high GI.6Y8 The European Diabetes Nutrition Research Group24 and World Health Organization25 recommend low-GI diets for patients with diabetes mellitus, and the American Diabetes Association recommends a low-GI diet rich in dietary fiber and important nutrients.26 In South China, the high-carbohydrate, high-GI staple diet rich in refined rice and its processed products20 does not support blood glucose control in patients with GDM. Contrary to the recommendations of leading diabetes organizations, the southern Chinese staple diet is low in fiber and essential nutrients. Our findings are consistent with those of prior studies in which the GI theory was used in the nutritional education and treatment of patients with type 2 diabetes mellitus and showed that a low-GI diet significantly reduced postprandial glucose levels.7,27Y29 Although fewer studies have examined the effects of low-GI foods on women with GDM, those conducted have shown promising results. Grant et al.16 randomized women with GDM or impaired glucose tolerance of pregnancy to a low-GI or control diet and found that the low-GI diet was associated with better postprandial glucose control. Moses et al.14 randomized 63 women with GDM to a low-GI diet or conventional high-fiber diet and found that the low-GI diet reduced the number of women requiring insulin for glucose control by 50%. A recent review of the literature by Louie et al.17 concluded that although current evidence is limited, studies support the advantages of and demonstrate no disadvantages of a low-GI diet for the treatment of women with GDM. Traditional nutritional therapy focuses on the amount of total energy consumed, the ratio of the 3 major nutrients, and the amount of carbohydrates rather than the type and preparation of carbohydrates. Measures in nutritional therapy may require individuals to deal with complex calculations, strict weighing, and separate meal preparation. However, the GI of foods can become intuitive with some education, allowing patients to select foods simply and conveniently. Besides the demonstrated advantages of low-GI diets for women with GDM,7,27Y29 the low-GI diet overcomes the inherent difficulties in the selection, matching, weighing, and cooking of foods that are recommended in traditional diabetic diets. The diet in South China is rich in rice, and the diet in the control group was comparable before and after intervention, but after standardization to provide equal amounts of total energy and total carbohydrates as in the low-GI staple diet of the treatment group, the 2 groups consumed similar diets and the same side dishes with the same amount of total carbohydrates and total energy, except for the low-GI staple food given to the low-GI staple diet group. The amount of carbohydrates in the control group was adjusted to fit the carbohydrate contents of the staple food packages used for the low-GI staple diet group. This suggests that the reduction in blood glucose seen in the control group may be attributed to the overall similarity of the 2 diets in dietary control of glucose metabolism as well as to nutritional education. Although we did not make any
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comparisons of the quantity of staple food consumed by either group prior to the study, it appears that both groups benefitted from the standardized diets. Blood glucose levels after breakfast were also reduced in both groups, but low-GI staple foods were not used in the breakfast meal. This suggests that the reduction in blood glucose after breakfast is related to the influence of low-GI staple foods consumed regularly in lunch and dinner each day. We also believe that the overall reductions in blood glucose levels are supported by education provided about GDM, which motivates participants to adhere to the diets as prescribed. There are limitations to this study that should be considered. The study population consisted only of Asians who consume rice as the primary staple, and thus the results may not be generalizable to other populations. On the other hand, the results clearly show the benefit of a low-GI staple diet in Asian women with GDM. In addition, although a benefit was seen in Asian women with GDM, determination of the benefit of a low-GI staple diet in a general Asian population will require further study.
CONCLUSIONS The results of this study showed that substitution of white rice, a high-GI food, with a low-GI staple food in the diet of women diagnosed with GDM resulted in significantly reduced postprandial glucose levels as compared with the normal white riceYbased staple diet. These results suggest that a low-GI staple diet is useful for glucose control in patients with GDM. REFERENCES 1. Metzger BE, Coustan DR, eds. Proceedings of the Fourth International Work-shopVconference on gestational diabetes mellitus. Diabetes Care. 1998;21(suppl 2):B1YB167; 1998. 2. Diabetes Society of Chinese Medical Association. China Medical Nutritional Therapy Guideline for Diabetes. Merck Serono Co. Ltd. China: Beijing, P.R. China, 2010. 3. Lin Y, Lin YP, Lin JX. Incidence of gestational diabetes mellitus and monitoring of blood glucose in patients of different age groups. Strait J Prev Med. 2012;12:93. 4. Scholl TO, Chen X, Khoo CS, et al. The dietary glycemic index during pregnancy: influence on infant birth weight, fetal growth, and biomarkers of carbohydrate metabolism. Am J Epidemiol. 2004;159:467Y474. 5. Lim SY, Yoo HJ, Kim AL, et al. Nutritional intake of pregnant women with gestational diabetes or type 2 diabetes mellitus. Clin Nutr Res. 2013;2:81Y90. 6. Jenkins DJ, Wolever TM, Taylor RH, et al. Glycemic index of foods: a physiological basis for carbohydrate exchange. Am J Clin Nutr. 1981;34:362Y366. 7. Jenkins DJ, Kendall CW, Augustin LS, et al. Glycemic index: overview of implications in health and disease. Am J Clin Nutr. 2002;76:266Y273. 8. Wolever TMS, Jenkins DJA. The use of the glycemic index in predicting blood glucose response to mixed meals. Am J Clin Nutr. 1986;43:167Y172. 9. Schwingshackl L, Hoffmann G. Long-term effects of low glycemic index/load vs. high glycemic index/load diets on parameters of obesity and obesity-associated risks: a systematic review and meta-analysis. Nutr Metab Cardiovasc Dis. 2013;23:699Y706. 10. Salmeron J, Manson JE, Stampfer MJ, et al. Dietary fiber, glycemic load, and risk of nonYinsulin-dependent diabetes mellitus in women. JAMA. 1997;277:472Y477. 11. Salmeron J, Ascherio A, Rimm EB, et al. Dietary fiber, glycemic load and risk of NIDDM in men. Diabetes Care. 1997;20:545Y550.
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Low GI Diet and Gestational DM in Asians
12. Liu S, Willett WC, Salmeron J, et al. A prospective study of dietary glycemic load, carbohydrate intake, and risk of coronary heart disease. Am J Clin Nutr. 2000;71:1455Y1461.
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22. Xie X, Guo W, eds. Obstetrics and Gynecology. 8th ed. Beijing, China: Peoples Health Publishing House; 2013.
14. Moses RG, Barker M, Winter M, et al. Can a low-glycemic index diet reduce the need for insulin in gestational diabetes mellitus? A randomized trial. Diabetes Care. 2009;32:996Y1000. 15. Gunderson EP. Gestational diabetes and nutritional recommendations. Curr Diab Rep. 2004;4:377Y86. 16. Grant SM, Wolever TM, O’Connor DL, et al. Effect of a low glycaemic index diet on blood glucose in women with gestational hyperglycaemia. Diabetes Res Clin Pract. 2011;91:15Y22. 17. Louie JC, Brand-Miller JC, Moses RG. Carbohydrates, glycemic index, and pregnancy outcomes in gestational diabetes. Curr Diab Rep. 2013;13:6Y11. 18. Louie JC, Markovic TP, Perera N, et al. A randomized controlled trial investigating the effects of a low-glycemic index diet on pregnancy outcomes in gestational diabetes mellitus. Diabetes Care. 2011;34:2341Y2346. 19. Hu ZG, Li W, Feng CS. A correlation study between glycemic index and breakfast foods in Guangdong residents. J Trop Med. 2011;1:82Y84. 20. Hu ZG, Li W, Zhou XY, et al. The glycemic index of mixed staple food. Guangdong Med J. 2013;7:1032Y1035.
23. Foster-Powell K, Holt SH, Brand-Miller JC. International table of glycemic index and glycemic load values: 2002. Am J Clin Nutr. 2002;76:5Y56. 24. Diabetes and Nutrition Study Group (DNSG) of the European Association for the Study of Diabetes (EASD). Recommendations for the nutritional management of patients with diabetes mellitus. Diabetes Nutr Metab. 1995;8:186Y189. 25. Carbohydrates in human nutrition. Report of a Joint FAO/WHO Expert Consultation, Rome, April, 14Y18, 1997. FAO Food and Nutrition Paper 66. Rome, Italy: Food & Agriculture Organization of the United Nations (FAO), 1998. 26. American Diabetes Association. Nutrition Recommendations and Interventions for Diabetes: a position statement of the American Diabetes Association. Diabetes Care. 2007;30(suppl 1):S48YS65. 27. Sun JQ, Shen XH, Chen XF. Glycemic index of foods and prevention and treatment of diabetes mellitus. Parenter Enteral Nutr. 2005;12:311Y314. 28. Brand-Miller JC. Postprandial glycemia, glycemic index, and the prevention of type 2 diabetes. Am J Clin Nutr. 2004;80:243Y244. 29. Ge Q, Lin J, Zhang BF, et al. Observation of nutritional therapy using glycemic index and food exchange for type 2 diabetes mellitus. J Clin Exp Med. 2008;12:5Y6.
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