The influence of fasting insulin level in post-gestational diabetes mellitus women receiving low-glycaemic-index diets

Abstract

Post-gestational diabetes mellitus (GDM) women are recommended weight loss to manage increased cardio-metabolic risks. We investigated the effects of lowering diet glycaemic index (GI) on fasting blood glucose (FBG), serum lipids, body weight and composition of post-GDM women with varying fasting insulin levels (INS). Seventy-seven Asian, non-diabetic women with previous GDM (aged 20-40 years, mean BMI: 26.4±4.6 kg m ^-2 ) were recruited. At baseline, 20 subjects with INS <2 μIU ml^-1 and 18 with INS [= or >, slanted]2 μIU ml^-1 received conventional dietary recommendations (CHDR) only. CHDR emphasised energy and fat intake restriction and encouraged increase in dietary fibre intakes. Twenty-four subjects with INS <2 μIU ml^-1 and 15 with INS [= or >, slanted]2 μIU ml^-1 , in addition to CHDR, received low-GI education (LGI). Changes in FBG, serum lipids, body weight and body composition were evaluated. Subjects with INS <2 μIU ml^-1 had similar outcomes with both diets. After 1 year, subjects with INS [= or >, slanted]2 μIU ml^-1 who received LGI education had reductions in FBG and triglycerides. Subjects who received CHDR observed increase in both FBG and triglycerides (P<0.05). Among all subjects, diet GI was lower and dietary fibre intakes were higher in LGI compared with CHDR subjects (all P<0.05). Thus, in Asian post-GDM women with normal/higher INS, adding low-GI education to CHDR improved management of FBG and triglycerides.

Citation: Nutrition & Diabetes (2014) 4, e107; doi:10.1038/nutd.2014.5& 2014 Macmillan Publishers Limited All rights reserved 2044-4052/14

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SHORT COMMUNICATION

The inuence of fasting insulin level in post-gestational diabetes mellitus women receiving low-glycaemic-index diets

RA Ghani1, S Shyam2, F Arshad3, NA Wahab1, K Chinna4, NS Sai5, MYB Nisak6 and NA Kamaruddin1

Post-gestational diabetes mellitus (GDM) women are recommended weight loss to manage increased cardio-metabolic risks.

We investigated the effects of lowering diet glycaemic index (GI) on fasting blood glucose (FBG), serum lipids, body weight and composition of post-GDM women with varying fasting insulin levels (INS). Seventy-seven Asian, non-diabetic women with previous GDM (aged 2040 years, mean BMI: 26.44.6 kg m 2) were recruited. At baseline, 20 subjects with INS o2 mIU ml 1 and 18 with

INS X2 mIU ml 1 received conventional dietary recommendations (CHDR) only. CHDR emphasised energy and fat intake restriction and encouraged increase in dietary bre intakes. Twenty-four subjects with INS o2 mIU ml 1 and 15 with INS X2 mIU ml 1,in addition to CHDR, received low-GI education (LGI). Changes in FBG, serum lipids, body weight and body composition were evaluated. Subjects with INS o2 mIU ml 1 had similar outcomes with both diets. After 1 year, subjects with INS X2 mIU ml 1 who received LGI education had reductions in FBG and triglycerides. Subjects who received CHDR observed increase in both FBG and triglycerides (Po0.05). Among all subjects, diet GI was lower and dietary bre intakes were higher in LGI compared with CHDR subjects (all Po0.05). Thus, in Asian post-GDM women with normal/higher INS, adding low-GI education to CHDR improved management of FBG and triglycerides.

Nutrition & Diabetes (2014) 4, e107; doi:http://dx.doi.org/10.1038/nutd.2014.5

Web End =10.1038/nutd.2014.5 ; published online 17 February 2013

Keywords: gestational diabetes mellitus; glycaemic index; type 2 diabetes mellitus; prevention; fasting insulin; diet

INTRODUCTIONGestational diabetes mellitus (GDM) increases the risk for metabolic syndrome and type 2 diabetes mellitus.1 To attenuate these risks, lifestyle intervention including components of diet, exercise and behavioural changes is recommended to post-GDM women to enable a moderate body weight loss of 710%.1 However, when compared with subjects with similar metabolic risks and glucose tolerance states, women with previous GDM achieve lower weight loss in response to standard recommendations and regain the weight lost rapidly.2 Subjects with hyperinsulinaemia, a condition commonly accompanying GDM, have a greater weight loss when on low-glycaemic-index (GI) diets.3,4 Therefore, we analysed the effect of dietary GI on fasting blood glucose (FBG), serum lipids, body weight and body fat of post-GDM subjects with varying fasting serum insulin levels (INS) during weight loss.

MATERIALS AND METHODSSeventy-seven post-GDM subjects, aged 2040 years (means.d.

30.59 years), without a current diagnosis of diabetes were recruited.

The mean body mass index of the subjects at baseline was26.44.6 kg m 2. Subjects were screened at a minimum of 2 months postpartum and the median duration since the last GDM delivery to the time of screening was 4 months (interquartile range 2). Mean parity among subjects was 2.01.1. Forty-four of the subjects had INS o2 mIU ml 1,

which was below the detectable limits of the automated IMMULITE 2000

Systems, which was used for INS assay. The rest of the subjects had INS X2 mIU ml 1 (range 2.4328.6 mIU ml 1, with a median of 5.7 mIU ml 1).

A fasting insulin value of 2 mIU ml 1 was chosen to be the cutoff to analyse the differential dietary effects, as it was approximately the natural median INS value for our subjects.

Twenty subjects with INS o2 mIU ml 1 (low INS) and 18 with INS X2 mIU ml 1 (normal/high INS) were randomized to a group that only received conventional dietary recommendations (CHDR). CHDR education emphasised restriction of energy and fat intake and encouraged increase in dietary bre intakes. Twenty-four subjects with INS o2 mIU ml 1 (low

INS) and 15 with INS X2 mIU ml 1 (normal/high INS) received low-GI education in addition to CHDR (LGI). A detailed account of the educational intervention used in this study has been published earlier.5 In brief, nutrition education was provided once at the baseline and take-home reference booklets were provided. Quarterly follow-up visits were scheduled. Fortnightly reminders reinforcing concepts of healthy living and motivating subjects to comply with the intervention were sent using email or short messaging services. Compliance was monitored through assessments of dietary intake, physical activity and nutrition knowledge assessment pertaining to the group-specic concepts. Frequency of subject contact was kept similar between groups. Subjects self-reported and calculated adherence to dietary prescription was monitored. Low-GI education taught subjects to choose low-GI options for high-GI staples like bread, rice and so on. A 1500-kcal sample menu used in the two diet groups is presented in Table 1. The differences in FBG, serum lipids, body weight and body fat changes between the two dietary intervention groups among subjects differing in baseline INS were studied.

The study was approved by the Ethics and Review Committees of the institutions involved. Baseline INS was analysed using IMMULITE 2000

1Endocrine Unit, Department of Medicine, Faculty of Medicine, Universiti Kebangsaan Malaysia (National University of Malaysia), Kuala Lumpur, Malaysia; 2School of Post Graduate Studies and Research, International Medical University, Kuala Lumpur, Malaysia; 3Department of Nutrition and Dietetics, International Medical University, Kuala Lumpur, Malaysia; 4Epidemiology and Biostatistics Unit, Department of Social and Preventive Medicine, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia; 5Dietetics Program, School of Healthcare Sciences, Faculty of Health Sciences, Universiti Kebangsaan Malaysia, Kuala Lumpur, Malaysia and 6Department of Nutrition & Dietetics, Faculty of Medicine & Health Sciences, Universiti Putra Malaysia, Serdang, Malaysia. Correspondence: Dr S Shyam, School of Post Graduate Studies and Research, International Medical University, No. 126, Jalan 19/155B, Bukit Jalil, Kuala Lumpur 57000, Malaysia.

E-mail: [email protected] 12 March 2013; revised 23 December 2013; accepted 18 January 2014

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Table 1. Sample menu for the diet groups (B1500 kcal)

Meal Timing (hours)

Sample menu low GI Sample menu high GIa

Breakfast 0700 Whole-grain bread3 slices with baked beansCoffee/tea with 1/2 cup low-fat milk 1 tsp sugar

Tuna whole-meal bread sandwiches3 slices of bread Tea (1 tsp sugar)

Morning snack 1000 1 apple (medium size) 1 slice watermelon (portion size to t a small cup) Lunch 1230 Noodles 1and1/2 cup with chicken or sh (1 match box size)

(or) chappati (60 dia, 2 nos)/ 1/2 cup dhal

Egg1 mediumGreen vegetables salad1 cup Orange1

White rice1and1/2 cup Egg1 medium Baked/steamed sh1 piece Green vegetables salad1 cup Banana1 small

Afternoon snack 1600 3 oatmeal biscuits/high calcium cream crackersLow-fat yoghurt1 small tub

3 Marie biscuitsTea (with 1 tsp sugar)

Dinner 2000 Parboiled/basmati rice1 cup baked chicken/sh 1 piece

(matchbox size)(or) spaghetti with meat sauce (1 cup)

Salad1 cup (use lettuce, cucumber, tomato, chick peas, peas, beans and lemon juice)

White rice1 cupBaked chicken/sh1 piece (matchbox size)

Egg 1 mediumVegetable/salad1cup (lettuce, cucumber, carrot, potato)

aUsed for the conventional dietary recommendations (CHDR) group.

System (Siemens, Healthcare Diagnostics, Deereld, IL, USA). This insulin-automated assay had a coefcient of variation of 3%. Low INS samples were placed in the same category when the test results were duplicated. Blood glucose was measured using Cobas Integra 700 model (Roche Diagnostics, Indianapolis, IN, USA) using the enzymatic reference Hexokinase/G6PD method. Serum lipids were measured using standard enzymatic colorimetric method and low-density lipoprotein was calculated. Body weight was measured in light clothing without footwear using digital weighing scales (Model: BWB-800A, Tanita Corporation, Tokyo, Japan). Body fat was measured using the dual-emission X-ray absorptiometry (DEXA, Model: Delphi, Hologic Systems; Bedford, MA, USA). Dietary analysis was performed using a Malaysian diet intake calculator.6

Statistical analyses were performed using IBM SPSS (version 19, Somers, NY, USA). The statistical signicance standard was set at 5%. Data normality was tested using the ShapiroWilks test. If data points were not normally distributed, statistical analysis was attempted on the natural logarithm of the values to improve the symmetry and homoscedasticity of the distribution. If the transformation was not successful, statistical analysis was carried out using non-parametric tests.

Effect size (ES) statistics were computed to study the magnitude of changes. ES values are typically computed to compare the effects of different treatments.7 ES provides a measure to assess the magnitude of difference between groups that cannot be obtained solely by focusing on P-values.8 P-values are dependent on both the magnitude of difference between groups and the sample size. Therefore, with other factors held constant, increasing the sample size increases the probability of nding a statistically signicant difference.8 ES reported in this study was calculated as the standardized mean difference: that is, as a ratio between the mean change and s.d.of change.8 Individual ES values were calculated for changes in outcomes for each of the two diet groups and compared. ES values between 0.20.5, 0.50.8 and 40.8 were taken to denote small, moderate and large changes in outcomes.7

RESULTS AND DISCUSSIONThe baseline characteristics of subjects randomized to the two diet groups in each INS stratum were comparable (see Table 2). A comparison of the outcome changes in the diet groups among subjects with low and normal/high INS levels is shown in Table 2. Among subjects with low INS, there were no signicant differences in outcomes between the diet groups. After 1 year, normal/high INS subjects in the LGI group had a 2.2% reduction from baseline in FBG ( 0.120.27 mmol l 1), whereas CHDR

subjects had a 3.8% (0.170.32 mmol l 1) increase (P 0.025, see

Table 2). In addition, normal/high INS subjects in the LGI group had a 12% reduction in triglycerides, whereas, in contrast, a 20% increase in triglycerides was noted in the CHDR group ( 0.260.55 vs 0.190.54 mmol l 1, P 0.041, see Table 2).

Changes in other serum lipids were not signicantly different between the diet groups (see Table 2).

Among subjects with baseline INS X2 mIU ml 1, weight loss (LGI vs CHDR: 1.73.8 vs 0.162.9 kg, ES 0.47 vs 0.08,

P 0.361) and changes in total body fat (g) (LGI vs CHDR:

0.372.7 kg, ES 0.14 vs 1.52.8 kg, ES 0.53; P 0.37) were not

signicantly different. These observations suggest benecial effects of low-GI diets in the management of body weight and composition among normal/high INS subjects, although it is emphasised that the study is not statistically powered to evaluate these outcomes. However, these observations are consistent with the 6 months nding from the CALERIE study, which reported that women with postprandial hyperinsulinaemia lost more weight on low-GI diets after 6 months on intervention.4 The observations from this study are also in agreement with the ndings of Ebbeling et al.,9 who showed that subjects with higher insulin levels (X57.5 mIU ml 1 at 30 min after a 75-g dose of oral glucose)

lost signicantly higher amounts of body weight and body fat loss when on low-glycaemic-load diets as compared with conventional low-fat diets. Also, weight regain that is commonly observed after weight loss in trials of duration 46 months was absent among these normal/high-INS Asian subjects in the LGI arm of the current study (see Figure 1). A similar observation was noted among hyperinsulinaemic obese young adults (aged 1835 years) studied in Boston.9

Baseline dietary intakes were similar between groups among all subjects. Among subjects with both INS levels, reported dietary intakes varied signicantly only in terms of diet GI and dietary bre content after intervention (see Table 3). In all subjects, estimated diet GI was lower and reported dietary bre intakes were higher in LGI as compared with CHDR subjects (all Po0.05).

In subjects with low INS, calculated diet GI meanss.d. in the LGI and CHDR groups were 594 and 654, respectively (Po0.001).

Their estimated dietary bre intakes were 123 vs 164 g, respectively (P 0.004). Among subjects with normal/high INS

mean (s.d.) calculated diet GI means (s.d.) in the LGI and CHDR groups were 564 and 626, respectively (Po0.021). Their estimated dietary bre intakes were 135 vs 174 g, respectively (P 0.045).

We acknowledge that 2 mIU ml 1 is very low as a cutoff to suggest fasting hyperinsulinaemia. As published earlier by this research group, data on the normal fasting insulin range for young healthy Malaysian women are currently unavailable.10 A small

Malaysian study found a median fasting insulin level of4.7 mIU ml 1 with a central 95% range of 2.112.1 mIU ml 1 among 30 healthy volunteers (including 12 females).11 This

preliminary study also observed that the range for fasting insulin in their group of Malaysian subjects was lower than the 95% CI of 629 mIU ml 1 typically reported.11 Our study did

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Table 2. Baseline characteristics and outcome changes in diet groups among subjects differing in fasting insulin levels (mean s.d.)

Outcome INSo2 mIU ml 1 INSX2 mIU ml 1

LGI (n 24) CHDR (n 20) P-value LGI (n 15) CHDR (n 18) P-value

Baseline characteristics

Age (years) 31.24.2 31.03.8 0.892 31.55.2 31.85.1 0.863 Parity 2.11.1 2.01.2 0.721 2.11.2 2.21.21.0 0.801` Duration postpartum (months) 4.31.3 7.210.1 0.170 4.51.8 4.41.4 0.801

Weight (kg)

Baseline 61.710.2 57.910.1 0.221 71.111.3 72.110.6 0.807

Change 0.64.3 0.22.7 0.673 1.73.8 0.22.9 0.361

Total body fat (kg)

Baseline 23.26.8 22.36.7 0.673 28.67.2 29.87.1 0.643

Change 1.22.7 1.22.6 0.692 0.42.7 1.32.4 0.368

Trunk fat (kg)

Baseline 10.03.4 9.73.5 0.777 13.13.9 14.34.3 0.433

Change 0.752.1 0.61.5 0.798 0.21.5 0.71.4 0.252

FBG (mmol l 1)

Baseline 4.50.4 4.70.5 0.151 5.00.5 4.90.6 0.553

Change 0.481.2 0.180.32 0.155 0.120.27 0.170.32 0.025

Total-cholesterol (mmol l 1)

Baseline 5.00.98 5.30.81 0.366 5.20.7 5.20.77 0.808

Change 0.090.85 0.180.58 0.704 0.110.73 0.110.76 0.536

Triglyceride (mmol l 1)

Baseline 0.70.2 0.932.8 0.121 1.30.5 1.10.5 0.180

Change 0.160.43 0.080.34 0.075 0.260.55 0.190.54 0.041

HDL cholesterol (mmol l 1)

Baseline 1.50.4 1.50.5 0.744 1.20.3 1.30.2 0.206

Change 0.040.3 0.040.2 0.978 0.10.18 0.010.31 0.283

LDL cholesterol (mmol l 1)

Baseline 3.21.0 3.30.7 0.496 3.40.8 3.30.7 0.726

Change 0.230.66 0.180.41 0.796 0.10.54 0.210.57 0.573

TC:HDL cholesterol

Baseline 3.40.8 3.81.2 0.185 4.51.3 4.01.0 0.186

Change 0.140.43 0.260.37 0.360 0.520.87 0.10.60 0.113

LDL:HDL cholesterol

Baseline 2.20.75 2.40.96 0.279 3.01.1 2.60.79 0.241

Change 0.20.38 0.220.3 0.929 0.380.71 0.160.55 0.326

Abbreviations: CHDR, conventional healthy dietary recommendation group; FBG, fasting blood glucose; HDL, high-density lipoprotein; INS, fasting insulin; LGI, low glycaemic index group; LDL, low-density lipoprotein. Baseline variables were not signicantly different between the diet groups among subjects in both insulin strata. P-values shown are calculated from independent tests for difference between the diet groups, within individual insulin groupings.

demonstrate similarly low fasting INS levels as reported in a small pilot study among Austrian GDM women (n 10), at 3 months

postpartum.12 This study reported a median fasting insulin level of1.63 mIU ml 1.12 Furthermore, lactation is associated with lower levels of INS at 69 weeks postpartum.13 However, in this study, only 12 out of 77 subjects (o16%), recruited at a median of 4 months postpartum, were reportedly breastfeeding.

This study demonstrated signicant lowering of FBG and TG in post-GDM women with baseline fasting insulin 42 mIU ml 1 who

received iso-caloric LGI diets in comparison with those on conventional low-fat diets. These observations are corroborated by earlier ndings that suggest that dietary GI may have varying effects depending on individual metabolic phenotypes.14 As FBG

is considered to be the strongest predictor of development of type 2 diabetes mellitus in women with previous GDM,15

a reduction in FBG by lowering dietary GI may translate to

added clinical benets of lowering diabetes risk among these women with normal or higher insulin levels. Moreover, triglycerides increase cardiovascular disease risk to a higher extent in women than in men.16,17 Therefore, LGI diets may also be considered cardio-protective to post-GDM women with normal to higher insulin levels.

The favourable anthropometric and glycaemic responses to low GI intervention seen in those with higher insulin levels, in comparison with subjects with low baseline insulin levels, could possibly be explained by the exaggerated glycaemic responses to increase in diet GI among high/normal INS subjects as compared with the low INS subjects. Asian subjects known to demonstrate insulin resistance at much lower body weight and waist circumference18 could have exaggerated postprandial glycaemic response to carbohydrate foods even while presenting fasting insulin levels that are typically considered as being normal.

& 2014 Macmillan Publishers Limited Nutrition & Diabetes (2014) 1 5

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Table 3. Dietary intake among subjects after the intervention (means.d.)a

Dietary intake INSo2 mIU ml 1 INSX2 mIU ml 1

LGI CHDR P-value LGI CHDR P-value

Energy (kcal) 1706351 1595298 0.298 1554292 1595442 0.927 Carbohydrate (g) 22146 22155 0.975 18662 20848 0.331 Protein (g) 6815 6013 0.086 7011 6728 0.259 Fat (g) 5917 5111 0.093 5010 5520 0.977 Dietary bre (g) 174 133 0.004 174 135 0.048 Glycaemic index 594 654 o0.001 564 626 0.021

Glycaemic load 13029 14541 0.195 11338 12828 0.244

Abbreviations: CHDR, conventional healthy dietary recommendation group; LGI, low glycaemic index group. Baseline dietary intakes were not signicantly different between the diet groups for subjects in both insulin strata. P-values shown are calculated from independent tests for difference between the diet groups, within individual insulin groupings. aThe values shown are an average of the dietary data obtained using 3-day food records, during the quarterly visits during the 1-year trial period.

Body Weight Changes in Subjects with baseline INS< 2 IU/ml

Body Weight Changes in Subjects with baseline INS> 2 IU/ml

63.0

73.5

Body Weight (Kg)

62.0

71.5

60.0

Body Weight (Kg)

61.0

69.5

67.5

59.0

58.0

65.5

57.0

1 2 3 4 5

1 2 3 4 5

Time

Time

LGI CHDR

LGI CHDR

63.5

Figure 1. Changes in body weight among subjects with varying baseline fasting insulin levels (estimated marginal means, kg). Legend: panel on the left plots weight changes in subjects with baseline fasting insulin o2 mIU ml 1. Panel on the right plots weight changes in subjects with baseline fasting insulin X2 mIU ml 1.

Dotted line shows weight changes in LGI. Smooth line shows weight changes in CHDR. Time points 1, 2, 3, 4 and 5 refer to body weight at baseline, 3, 6, 9 and 12 months after intervention.

Hence, even though a 15% difference in dietary GI between the groups (about 9 units based on baseline GI), thought to have clinical signicance,19 could not be achieved after 12 months of intervention, signicant differences in FBG and TG were seen among subjects with high/normal INS levels. Nevertheless, it is also interesting to observe that much smaller differences in the GI (among the quintiles compared in observational studies), than the10 GI unit difference thought to be of clinical signicance,19,20

show signicant reductions in cardio-metabolic risks.2124

Differences in dietary GI as low as ve units have shown signicant trends for improvements in high-density lipoprotein and hs-CRP.23,25 Lower trends for fasting insulin are seen at around

seven units,22 and lower insulin resistance at three unit differences in GI24 in a few of these observational studies. Furthermore, shorter Asian trials of 6 months duration, achieving a difference in GI of E6 units between groups, have also documented signicant benecial effects in terms of reductions in waist circumference, FBG and glycaemic control in diabetic subjects or those with impaired fasting glucose.26,27 Longer trials lasting until a year have found favourable changes in cardio-metabolic risks in the low GI/GL groups when the difference in GI established between the groups was comparable to the six-unit difference documented in the current study.28,29 A decrease in triglycerides was documented when a seven-unit difference in GI was established among obese young adults.28 Similarly, improvements in insulin sensitivity have been documented when a six-unit GI difference was established between two groups of PCOS women.29 The ndings from this

study therefore extend the application of an existing body of evidence that indicates that low-GI diets may have added benets in cardio-metabolic risk management in hyperinsulinaemic subjects4,9,30 among normal and hyperinsulinaemic Asian subjects.

These ndings lend credence to translational research with practical approaches to lowering dietary GI, when the free-living conditions of the subjects may hamper the achievement of marked diet GI reduction seen in controlled clinical trials. Further investigation of the interaction between insulin levels and response to diet GI is necessary. Such an effort may also help clarify the inconclusive associations reported between GI and risk for chronic diseases.

The small sample size limits generalisation of the results to other populations. Furthermore, INS o2 mIU ml 1 was not quantiable by the assay used. Hence, caution is needed while interpreting these data. Also, the current trial monitored fasting insulin levels and not postprandial insulin, which could have demonstrated more apparently the exaggerated insulin response typical in early pathogenesis of type 2 diabetes mellitus. Nevertheless, an increase in fasting insulin concentration is also associated with hyperinsulinaemia.31

CONCLUSIONThus, in Asian women with a history of GDM, having normal or higher fasting INS, adding low-GI education to conventional dietary guidelines improved management of FBG and triglycerides. More research on the interaction between insulin levels and response to diet GI is necessary.

CONFLICT OF INTEREST

The authors declare no conict of interest.

ACKNOWLEDGEMENTS

This project was funded by an internal research grant (IMU199/2009) from International Medical University, Kuala Lumpur, Malaysia.

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