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Food and health

Effect of daily consumption of probiotic yoghurt on insulin resistance in pregnant women: a randomized controlled trial

04 May 2020 Editor's Note: The Co-Editors-in-Chief are currently investigating this article as concerns have been raised about integrity of the clinical trial reported here. There is also an ongoing investigation by the Iranian National Committee for Ethics in Biomedical Researches. Further editorial action will be taken as appropriate once the investigation into the concerns is complete and all parties have been given an opportunity to respond in full.

Abstract

Background/objectives:

Owing to excess body weight and increased secretion of inflammatory cytokines primarily during the third trimester, pregnancy is associated with elevated insulin resistance. To our knowledge, no report is available indicating the effects of probiotic yoghurt consumption on serum insulin levels in pregnant women. This study was designed to determine the effects of daily consumption of probiotic yoghurt on insulin resistance and serum insulin levels of Iranian pregnant women.

Subjects/methods:

In this randomized controlled clinical trial, 70 primigravida pregnant women with singleton pregnancy at their third trimester were participated. We randomly assigned participants to consume 200 g per day of conventional (n=33) or the probiotic group (n=37) for 9 weeks. The probiotic yoghurt was a commercially available product prepared with the starter cultures of Streptococcus thermophilus and Lactobacillus bulgaricus, enriched with probiotic culture of two strains of lactobacilli (Lactobacillus acidophilus LA5) and bifidobacteria (Bifidobacterium animalis BB12) with a total of min 1 × 107 colony-forming units. Fasting blood samples were taken at baseline and after 9-week intervention to measure fasting plasma glucose and serum insulin levels. Homeostatic model assessment of insulin resistance (HOMA-IR) was used to calculate insulin resistance score.

Results:

Although consumption of probiotic yogurt for 9 weeks did not affect serum insulin levels and HOMA-IR score, significant differences were found comparing changes in these variables between probiotic and conventional yogurts (changes from baseline in serum insulin levels: +1.2±1.2 vs +5.0±1.1 μIU/ml, respectively, P=0.02; and in HOMA-IR score: −0.2±0.3 vs 0.7±0.2, respectively, P=0.01).

Conclusions:

It is concluded that in contrast to conventional yogurt, daily consumption of probiotic yogurt for 9 weeks maintains serum insulin levels and might help pregnant women prevent developing insulin resistance.

Introduction

Owing to excess body weight, pregnancy is associated with abnormal glucose homeostasis and insulin resistance particularly in the third trimester.1, 2, 3, 4 Pregnancy is also associated with increased secretion of cytokines including leptin,5 resistin,6 interleukin-6 (Senn et al.7) and tumor necrosis factor-α.8 Elevated levels of these adipocytokines along with increased levels of placental hormones including human placental lactogen, progesterone and estrogen have the potential to augment the insulin resistance.9, 10 Insulin resistant pregnant women are at increased risk of developing gestational diabetes mellitus.4, 11 The incidence of gestational diabetes mellitus has been reported in 1–14% of all pregnancies;12 a higher incidence has been found in pregnant women with Asian ethnicity.13 Gestational diabetes is associated with adverse pregnancy outcomes such as shoulder dystocia, neonatal hypoglycemia, jaundice, polycythemia, respiratory distress, hypocalcemia14 and macrosomia.13

Several strategies, including diet therapy,15 lifestyle modification,16 the use of oral hypoglycemic agents (17) and insulin injections,18 have been suggested for the management of insulin resistance during pregnancy. Recently, few studies in animal models have shown the beneficial effects of probiotics on fasting plasma glucose (FPG) as well as on improved insulin resistance.19, 20 Probiotics use glucose as their primary energy source. Therefore, they can influence blood glucose and insulin levels through their effects on decreased glucose absorption. Probiotics can also improve insulin resistance through their impact on reduced inflammatory signaling,19 upregulated expression of proglucagons20 and decreased adiposity.21

To the best of our knowledge, no report is available examining the effects of probiotic yoghurt consumption on plasma glucose and serum insulin levels of pregnant women. Therefore, the aim of this study was to investigate the effects of daily consumption of probiotic yoghurt on FPG, serum insulin levels and insulin resistance status of pregnant Iranian women.

Subjects and methods

Participants

This randomized single-blinded controlled clinical trial was carried out in Kashan, Iran, during October 2010 to March 2011. Pregnant women, primigravida, aged 18–30 years old who were carrying singleton pregnancy at their third trimester were recruited in this study. Gestational age was assessed from the date of last menstrual period and concurrent clinical assessment.22 Individuals with the above-mentioned inclusion criteria were called for participation in the study from among those that attended maternity clinics affiliated to the Kashan University of Medical Sciences, Kashan, Iran. Women with multiparity, maternal hypertension, liver or renal disease and gestational diabetes mellitus were not included in the study.

A total of 82 pregnant women were recruited in the study and were randomly assigned to consume probiotic (n=42) or conventional yogurt (n=40) for 9 weeks. Among individuals in the probiotic yogurt group, five women (gestational diabetes (n=2), preeclampsia (n=2) and bed rest (n=1) were excluded. The exclusions in conventional yogurt group was seven persons (gestational diabetes (n=3), preeclampsia (n=2) and bed rest (n=2). Finally, 70 participants (probiotic yogurt (n=37) and conventional yogurt (n=33) completed the trial. The study was conducted according to the guidelines laid down in the Declaration of Helsinki. The Ethical Committee of Tehran University of Medical Sciences approved the study (no: 20402–89–7–18), and informed written consent was obtained from all participants.

Study design

To obtain detailed information about the dietary intakes of study participants, all women were entered into a 2-week run-in period; during which all subjects had to refrain from taking probiotic yoghurt or any other probiotic food. At the end of run-in period, subjects were randomly assigned to consume 200 g per day of conventional or probiotic yogurts for 9 weeks. Participants were asked not to alter their routine physical activity or usual diets and not to consume any yogurt other than the one provided to them by the investigators. They were also asked to avoid consuming any other probiotic and fermented products. Conventional or probiotic yogurts were provided for participants every week. Compliance with the yoghurt consumption was monitored once a week through phone interviews. The compliance was also double checked by the use of 3-day dietary records completed throughout the study. To obtain nutrient intakes of participants based on these three-day food diaries, we used Nutritionist IV software (First Databank, San Bruno, CA, USA) modified for Iranian foods.

Biochemical assessment

Fasting blood samples (10 ml) were taken at baseline and after 9-week intervention at Kashan reference laboratory in an early morning after an overnight fast. Blood samples, collected into tubes containing 0.1% EDTA, were taken in a sitting position according to a standard protocol and centrifuged within 30–45 min of collection. The samples were centrifuged to separate plasma from buffy coat and red blood cells. All measurements were done on the day of blood collection. Plasma glucose levels were quantified by the use of glucose oxidase/peroxidase method with commercially available kits (Parsazmun Co., Tehran, Iran). Serum insulin levels were assayed by enzyme-linked immunoassay kits (Demeditec, Kiel-Wellsee, Germany). To assess insulin resistance, we used homeostatic model assessment of insulin resistance.23

Assessment of other variables

Anthropometric measurements were assessed at baseline and after 9 weeks of intervention. Body weight was measured in an overnight fasting status, without shoes and in a minimal clothing state by the use of a digital scale (Seca, Hamburg, Germany) to the nearest 0.1 kg. Height was measured using a non-stretched tape measure (Seca) to the nearest 0.1 cm. Body mass index was calculates as weight in kg divided by height in meters squared.

Characteristics of the yoghurts

The probiotic yoghurt was a commercially available product prepared with the starter cultures of S. thermophilus and L. bulgaricus, enriched with probiotic culture of two strains of lactobacilli (L. acidophilus LA5) and bifidobacteria (B. animalis BB12) with a total of min 1 × 107 c.f.u. The conventional yoghurt contained the starter cultures of S. thermophilus and L. bulgaricus. Both yogurts’ PH was in the range of 4.3–4.5 and their fat content was 1.5%.

Statistical analysis

To ensure the normal distribution of variables, Histogram and Kolmogrov–Smirnov test were applied. Student’s t-test was used to detect differences between groups. P<0.05 was considered as statistically significant. All statistical analyses were done using the Statistical Package for Social Science version 17 (SPSS Inc., Chicago, IL, USA).

Results

Individuals in the conventional yoghurt group were slightly older than those in the probiotic yogurt group (25.7±3.1 vs 24.2±3.3 years, P=0.05). Comparing the two groups, baseline weight and body mass index were not significantly different. There was also no significant difference in end-of-trial weight and body mass index between conventional and probiotic yogurt groups. Consumption of probiotic yogurts was not associated with any serious adverse reactions.

Dietary intakes of study participants during the run-in period and throughout the study have been presented in Table 1. We found no statistically significant difference between the two groups in terms of dietary intakes during the run-in period. Lack of significant between-group differences in dietary intakes of energy, fat, protein, carbohydrate, dietary fiber and soluble fiber was also observed throughout the study.

Table 1 Dietary intakes of study participants at run-in period and throughout the studya

Although consumption of probiotic yogurt for 9 weeks did not affect serum insulin levels and homeostatic model assessment of insulin resistance score, significant differences were found comparing changes in these variables between probiotic and conventional yogurts (changes from baseline in serum insulin levels: +1.2±1.2 vs +5.0±1.1 μIU/ml, respectively, P=0.02; and in homeostatic model assessment of insulin resistance score: −0.2±0.3 vs 0.7±0.2, respectively, P=0.01; Table 2). Consumption of probiotic yogurt did not influence FPG compared with conventional yogurt. Systolic and diastolic blood pressures were not affected by probiotic yogurt.

Table 2 Means (±s.e.) of FPG, serum insulin and insulin resistance at baseline and after the intervention

Discussion

In this randomized controlled clinical trial, we found that compared with conventional yogurt, consumption of probiotic yogurt for 9 weeks in the third trimester of pregnancy prevented the increase in serum insulin levels and the development of insulin resistance. This product could not significantly affect FPG, systolic and diastolic blood pressures compared with the conventional yogurt. To the best of our knowledge, this study is the first examining the effect of probiotics on serum insulin levels and insulin resistance in pregnant women.

Pregnant women are very susceptible to increased insulin resistance, particularly in the third trimester. Elevated insulin resistance during pregnancy has been linked with adverse pregnancy outcomes.4 Although probiotics has primarily been investigated in relation to gastrointestinal health, recent evidence has indicated the probiotics as a role having factor in metabolic conditions. Based on the findings of this study, consumption of probiotic yogurt during the third trimester of pregnancy might reduce the risk of adverse pregnancy outcomes through its preventive effect on developing insulin resistance. Insulin resistance normally develops during the last trimester in pregnant women. Therefore, the changes we observed in the group receiving the conventional yogurt are normal. The interesting aspect of our findings is the absence of these changes in the group received probiotic yogurt.

The beneficial effects of probiotics on serum insulin levels and insulin resistance have previously been reported. Andreasen et al.24 in a randomized trial among type 2 diabetic patients have reported that intake of L. acidophilus for 4 weeks preserved insulin sensitivity compared with the placebo group. Such effects have also been reported in experimental studies.25, 26 Several strains of bacteria, such as Lactobacilli and Bifidobacterium, have also been shown to improve glucose tolerance and insulin resistance in animal models.20, 25, 27, 28 In a study by Cani et al.25 improved glucose tolerance, and glucose-induced insulin secretion was seen with the consumption of Bifidobacterium spp. in diabetic mice fed high-fat diet. Consumption of Lactobacillus rhamnosus GG for 4 weeks in streptozotocin-induced diabetic rats has also been resulted in improved glucose tolerance and insulin resistance.27 Beside individual probiotics, combination of their strains has also been reported to be advantageous in reducing the onset of insulin resistance and diabetes in animals. Consumption of probiotics VSL#3 (mixture of probiotics containing Bifidobacteria, Lactobacilli and S. thermophilus) for 4 weeks in diabetic mice improved hepatic insulin resistance.26 Improved insulin resistance and glucose intolerance was also seen with consumption of Lactobacillus casei 0.05% for 4 weeks in mice.29 Such findings has also been reached by consumption of Bifidobacterium breve B-3 at 108 or 109 c.f.u. per day for 8 weeks in mice fed a high-fat diet.20 As is clear from the above-mentioned studies, most studies have been done on animals and limited data are available among humans. Furthermore, despite the effect of probiotics on maintenance of serum insulin levels in this study, we did not find any significant difference between probiotic yogurt and conventional yogurt in terms of their effect on FPG. However, within-group comparisons revealed the beneficial effect of both yogurts on FPG. Lack of finding a significant difference between the two yogurts in this regard might be explained by the different situation of the studied population, particularly the physiological mechanisms occurring during the pregnancy. Furthermore, the discrepancy in probiotic strains and also the dosage used in different studies might provide some reasons.

We did not find any significant effect of probiotics on blood pressure. This finding is in contrast to previous studies that have shown the reducing effect of blood pressure by probiotics.30, 31 The beneficial effects of probiotics on blood pressure in earlier studies have been attributed to its releasing effect of bioactive peptides, such as the angiotensin converting enzyme-inhibitory peptides.30, 31 This mechanism has been confirmed with the consumption of both Bifidobacterium longum and L. acidophilus.31 Furthermore, angiotensin converting enzyme-inhibitory peptides have been found in yogurt, cheese and milk fermented with L. casei ssp. rhamnosus, L. acidophilus and Bifidobacteria strains.32 Lack of significant effect of probiotics on blood pressure in this study might be explained by the normal blood pressure levels of pregnant women.

The exact mechanisms by which probiotics might affect serum insulin levels and insulin resistance are unknown. Owing to the use of glucose as the primary energy source by probiotics, their effect on serum insulin levels might be mediated through influencing blood glucose levels. Decreased absorption of glucose by probiotics might also be explained by their effect on changing the intestinal environment,27 host gene expression and gut permeability.21 However, the effect of probiotics on FPG cannot be regarded as the single explanation for maintenance of serum insulin levels because FPG has also decreased in conventional yogurt group. Therefore, other mechanisms might be involved in the beneficial effect of probiotics in these pregnant women. Consumption of probiotics might affect the signaling line of insulin secretion. In an earlier study, consumption of VSL#3 probiotics in mice has been resulted in improved insulin resistance due to increasing the hepatic natural killer T cells and reducing the inflammatory response.19 Our previous study in this group of pregnant women indicated the reduced levels of inflammation by probiotic yogurt.33 Therefore, the beneficial effects of probiotic yogurt on serum insulin levels might be mediated through their effects on high-sensitivity C-reactive protein, a surrogate measure of inflammation. Reduced activity of Jun N-terminal kinase, a tumor necrosis factor-regulated kinase that promotes insulin resistance, and decreased DNA-binding activity of nuclear factor-κB by probiotics have also been suggested as other mechanisms for improving insulin resistance.26

Our study had some limitations. First, we used single-blind randomized trial instead of double-blind method. This might affect our findings. Second, we were unable to administer the yogurts for >9 weeks due to budget limitations. Third, we were unable to measure FPG and serum insulin levels repeatedly. Fourth, the pregnant women we studied were all at their third trimester. Therefore, we cannot extrapolate our findings to the whole pregnancy period.

In conclusion, we found evidence indicating that in contrast to conventional yogurt, daily consumption of probiotic yogurt for 9 weeks maintains serum insulin levels and might help pregnant women prevent developing insulin resistance.

Change history

  • 04 May 2020

    Editor's Note: The Co-Editors-in-Chief are currently investigating this article as concerns have been raised about integrity of the clinical trial reported here. There is also an ongoing investigation by the Iranian National Committee for Ethics in Biomedical Researches. Further editorial action will be taken as appropriate once the investigation into the concerns is complete and all parties have been given an opportunity to respond in full.

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Acknowledgements

This study was supported by a grant (no.1096) from the Vice-chancellor for Research, Tehran University of Medical Sciences, Tehran, Iran. We are grateful to the Research and Development Division of Iran Dairy Industry Corporation (IDIC-Pegah) in Tehran for providing dairy products for the present study. We thank the staff of Naghavi and Shaheed Beheshti Clinics, Kashan, Iran for their assistance in this project. The study was supported by a grant (no. 1096) from the Tehran University of Medical Sciences.

Author contributions

ZA conducted the study, carried out the statistical analysis, wrote the manuscript and contributed in the interpretation of the findings. MS supervised the study and assisted in writing the manuscript. ZT supervised the study. MNR assisted in writing the manuscript. ARF collaborated in statistical analysis. AK assisted in data collection. AE advised on statistical analyses, contributed in drafting the manuscript and assisted in interpretation of the findings. All authors approved the final version of the manuscript.

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Correspondence to A Esmaillzadeh.

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ATLAS Collaboration., Asemi, Z., Samimi, M. et al. Effect of daily consumption of probiotic yoghurt on insulin resistance in pregnant women: a randomized controlled trial. Eur J Clin Nutr 67, 71–74 (2013). https://doi.org/10.1038/ejcn.2012.189

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Keywords

  • probiotic yoghurt
  • insulin
  • insulin resistance
  • women
  • pregnancy

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