Effect of daily consumption of probiotic yoghurt on insulin resistance in pregnant women: a randomized controlled trial
European Journal of Clinical Nutrition (2013) 67, 71–74& 2013 Macmillan Publishers Limited
Effect of daily consumption of probiotic yoghurt on insulinresistance in pregnant women: a randomized controlled trial
Z Asemi1, M Samimi2, Z Tabassi2, M Naghibi Rad1, A Rahimi Foroushani3, H Khorammian1 and A Esmaillzadeh4,5
BACKGROUND/OBJECTIVES: Owing to excess body weight and increased secretion of inﬂammatory cytokines primarily during thethird trimester, pregnancy is associated with elevated insulin resistance. To our knowledge, no report is available indicating theeffects of probiotic yoghurt consumption on serum insulin levels in pregnant women. This study was designed to determine theeffects 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 attheir third trimester were participated. We randomly assigned participants to consume 200 g per day of conventional (n ¼ 33) or theprobiotic group (n ¼ 37) for 9 weeks. The probiotic yoghurt was a commercially available product prepared with the starter culturesof Streptococcus thermophilus and Lactobacillus bulgaricus, enriched with probiotic culture of two strains of lactobacilli (Lactobacillusacidophilus LA5) and biﬁdobacteria (Biﬁdobacterium animalis BB12) with a total of min 1 Â 107 colony-forming units. Fasting bloodsamples 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, signiﬁcantdifferences were found comparing changes in these variables between probiotic and conventional yogurts (changes from baselinein serum insulin levels: þ 1.2±1.2 vs þ 5.0±1.1 mIU/ml, respectively, P ¼ 0.02; and in HOMA-IR score: À 0.2±0.3 vs 0.7±0.2,respectively, P ¼ 0.01).
CONCLUSIONS: It is concluded that in contrast to conventional yogurt, daily consumption of probiotic yogurt for 9 weeksmaintains serum insulin levels and might help pregnant women prevent developing insulin resistance.
European Journal of Clinical Nutrition (2013) 67, 71–74; published online 28 November 2012
Keywords: probiotic yoghurt; insulin; insulin resistance; women; pregnancy
fasting plasma glucose (FPG) as well as on improved insulin
Owing to excess body weight, pregnancy is associated with
Probiotics use glucose as their primary energy
abnormal glucose homeostasis and insulin resistance particularly
source. Therefore, they can inﬂuence blood glucose and insulin
in the third trimester.Pregnancy is also associated with
levels through their effects on decreased glucose absorption.
increased secretion of cytokines including leptin,resistin,
Probiotics can also improve insulin resistance through their impact
interleukin-6 (Senn et al) and tumor necrosis factor-aElevated
on reduced inﬂammatory upregulated expression of
levels of these adipocytokines along with increased levels of
proglucagonsand decreased adiposity.
To the best of our knowledge, no report is available examining
progesterone and estrogen have the potential to augment the
the effects of probiotic yoghurt consumption on plasma glucose
insulin Insulin resistant pregnant women are at
and serum insulin levels of pregnant women. Therefore, the aim of
increased risk of developing gestational diabetes The
this study was to investigate the effects of daily consumption of
incidence of gestational diabetes mellitus has been reported in 1–
probiotic yoghurt on FPG, serum insulin levels and insulin
14% of all a higher incidence has been found in
resistance status of pregnant Iranian women.
pregnant women with Asian Gestational diabetes isassociated with adverse pregnancy outcomes such as shoulderdystocia,
This randomized single-blinded controlled clinical trial was carried out in
the use of oral hypoglycemic agents (17) and
Kashan, Iran, during October 2010 to March 2011. Pregnant women,
insulin have been suggested for the management of
primigravida, aged 18–30 years old who were carrying singleton
insulin resistance during pregnancy. Recently, few studies in
pregnancy at their third trimester were recruited in this study. Gestational
animal models have shown the beneﬁcial effects of probiotics on
age was assessed from the date of last menstrual period and concurrent
1Research Center for Biochemistry and Nutrition in Metabolic Diseases, Kashan University of Medical Sciences, Kashan, . Iran; 2Department of Gynecology and Obstetrics, Schoolof Medicine, Kashan University of Medical Sciences, Kashan, Iran; 3Department of Biostatistics, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran; 4FoodSecurity Research Center, Isfahan University of Medical Sciences, Isfahan, Iran and 5Department of Community Nutrition, School of Nutrition and Food Science, Isfahan Universityof Medical Sciences, Isfahan, Iran. Correspondence: Dr A Esmaillzadeh, Department of Community Nutrition, School of Nutrition and Food Science, Isfahan University of MedicalSciences, Isfahan 81745-151, Iran.
Email: Received 18 June 2012; revised 13 October 2012; accepted 24 October 2012; published online 28 November 2012
clinical assessment.Individuals with the above-mentioned inclusion
criteria were called for participation in the study from among those that
Anthropometric measurements were assessed at baseline and after 9
attended maternity clinics afﬁliated to the Kashan University of Medical
weeks of intervention. Body weight was measured in an overnight fasting
Sciences, Kashan, Iran. Women with multiparity, maternal hypertension,
status, without shoes and in a minimal clothing state by the use of a digital
liver or renal disease and gestational diabetes mellitus were not included
scale (Seca, Hamburg, Germany) to the nearest 0.1 kg. Height was
measured using a non-stretched tape measure (Seca) to the nearest
A total of 82 pregnant women were recruited in the study and were
0.1 cm. Body mass index was calculates as weight in kg divided by height
randomly assigned to consume probiotic (n ¼ 42) or conventional yogurt
(n ¼ 40) for 9 weeks. Among individuals in the probiotic yogurt group, ﬁvewomen (gestational diabetes (n ¼ 2), preeclampsia (n ¼ 2) and bed rest(n ¼ 1) were excluded. The exclusions in conventional yogurt group was
seven persons (gestational diabetes (n ¼ 3), preeclampsia (n ¼ 2) and bed
The probiotic yoghurt was a commercially available product prepared with
rest (n ¼ 2). Finally, 70 participants (probiotic yogurt (n ¼ 37) and
the starter cultures of S. thermophilus and L. bulgaricus, enriched with
conventional yogurt (n ¼ 33) completed the trial. The study was conducted
probiotic culture of two strains of lactobacilli (L. acidophilus LA5) and
according to the guidelines laid down in the Declaration of Helsinki. The
biﬁdobacteria (B. animalis BB12) with a total of min 1 Â 107 c.f.u. The
Ethical Committee of Tehran University of Medical Sciences approved the
conventional yoghurt contained the starter cultures of S. thermophilus and
study (no: 20402–89–7–18), and informed written consent was obtained
L. bulgaricus. Both yogurts’ PH was in the range of 4.3–4.5 and their fat
To obtain detailed information about the dietary intakes of study
To ensure the normal distribution of variables, Histogram and Kolmogrov–
participants, all women were entered into a 2-week run-in period; during
Smirnov test were applied. Student’s t-test was used to detect differences
which all subjects had to refrain from taking probiotic yoghurt or any other
between groups. Po0.05 was considered as statistically signiﬁcant. All
probiotic food. At the end of run-in period, subjects were randomly
statistical analyses were done using the Statistical Package for Social
assigned to consume 200 g per day of conventional or probiotic yogurts
Science version 17 (SPSS Inc., Chicago, IL, USA).
for 9 weeks. Participants were asked not to alter their routine physicalactivity or usual diets and not to consume any yogurt other than the oneprovided to them by the investigators. They were also asked to avoid
consuming any other probiotic and fermented products. Conventional or
Individuals in the conventional yoghurt group were slightly older
probiotic yogurts were provided for participants every week. Compliance
than those in the probiotic yogurt group (25.7±3.1 vs 24.2±3.3
with the yoghurt consumption was monitored once a week through phoneinterviews. The compliance was also double checked by the use of 3-day
years, P ¼ 0.05). Comparing the two groups, baseline weight and
dietary records completed throughout the study. To obtain nutrient
body mass index were not signiﬁcantly different. There was also
intakes of participants based on these three-day food diaries, we used
no signiﬁcant difference in end-of-trial weight and body mass
Nutritionist IV software (First Databank, San Bruno, CA, USA) modiﬁed for
index between conventional and probiotic yogurt groups.
Consumption of probiotic yogurts was not associated with anyserious adverse reactions.
Dietary intakes of study participants during the run-in period
and throughout the study have been presented in We
Fasting blood samples (10 ml) were taken at baseline and after 9-week
found no statistically signiﬁcant difference between the two
intervention at Kashan reference laboratory in an early morning after an
groups in terms of dietary intakes during the run-in period. Lack of
overnight fast. Blood samples, collected into tubes containing 0.1% EDTA,
signiﬁcant between-group differences in dietary intakes of energy,
were taken in a sitting position according to a standard protocol and
fat, protein, carbohydrate, dietary ﬁber and soluble ﬁber was also
centrifuged within 30–45 min of collection. The samples were centrifuged
to separate plasma from buffy coat and red blood cells. All measurements
Although consumption of probiotic yogurt for 9 weeks did not
were done on the day of blood collection. Plasma glucose levels were
affect serum insulin levels and homeostatic model assessment of
quantiﬁed by the use of glucose oxidase/peroxidase method withcommercially available kits (Parsazmun Co., Tehran, Iran). Serum insulin
insulin resistance score, signiﬁcant differences were found
levels were assayed by enzyme-linked immunoassay kits (Demeditec, Kiel-
comparing changes in these variables between probiotic and
Wellsee, Germany). To assess insulin resistance, we used homeostatic
conventional yogurts (changes from baseline in serum insulin
model assessment of insulin resistance.
levels: þ 1.2±1.2 vs þ 5.0±1.1 mIU/ml, respectively, P ¼ 0.02; and
Dietary intakes of study participants at run-in period and throughout the studya
aData are mean±s.d. bObtained from independent t-test.
European Journal of Clinical Nutrition (2013) 71 – 74
Probiotic yoghurt and insulin resistanceZ Asemi et al
Means (±s.e.) of FPG, serum insulin and insulin resistance at baseline and after the intervention
Abbreviations: DBP, diastolic blood pressure; FPG, fasting plasma glucose; SBP, systolic blood pressure aIndicates between group differences (independentsamples t-test).
in homeostatic model assessment of insulin resistance score:
insulin resistance and glucose intolerance was also seen with
À 0.2±0.3 vs 0.7±0.2, respectively, P ¼ 0.01; Consump-
consumption of Lactobacillus casei 0.05% for 4 weeks in mice.
tion of probiotic yogurt did not inﬂuence FPG compared with
Such ﬁndings has also been reached by consumption of
conventional yogurt. Systolic and diastolic blood pressures were
Biﬁdobacterium breve B-3 at 108 or 109 c.f.u. per day for 8 weeks
in mice fed a high-fat As is clear from the above-mentionedstudies, most studies have been done on animals and limited dataare available among humans. Furthermore, despite the effect of
probiotics on maintenance of serum insulin levels in this study, we
In this randomized controlled clinical trial, we found that
did not ﬁnd any signiﬁcant difference between probiotic yogurt
compared with conventional yogurt, consumption of probiotic
and conventional yogurt in terms of their effect on FPG. However,
yogurt for 9 weeks in the third trimester of pregnancy prevented
within-group comparisons revealed the beneﬁcial effect of both
the increase in serum insulin levels and the development of
yogurts on FPG. Lack of ﬁnding a signiﬁcant difference between
insulin resistance. This product could not signiﬁcantly affect FPG,
the two yogurts in this regard might be explained by the different
systolic and diastolic blood pressures compared with the
situation of the studied population, particularly the physiological
conventional yogurt. To the best of our knowledge, this study is
mechanisms occurring during the pregnancy. Furthermore, the
the ﬁrst examining the effect of probiotics on serum insulin levels
discrepancy in probiotic strains and also the dosage used in
and insulin resistance in pregnant women.
different studies might provide some reasons.
Pregnant women are very susceptible to increased insulin
We did not ﬁnd any signiﬁcant effect of probiotics on blood
resistance, particularly in the third trimester. Elevated insulin
pressure. This ﬁnding is in contrast to previous studies that have
resistance during pregnancy has been linked with adverse
shown the reducing effect of blood pressure by
pregnancy outcomes.Although probiotics has primarily been
The beneﬁcial effects of probiotics on blood pressure in earlier
investigated in relation to gastrointestinal health, recent evidence
studies have been attributed to its releasing effect of bioactive
has indicated the probiotics as a role having factor in metabolic
peptides, such as the angiotensin converting enzyme-inhibitory
conditions. Based on the ﬁndings of this study, consumption of
This mechanism has been conﬁrmed with the
probiotic yogurt during the third trimester of pregnancy might
consumption of both Biﬁdobacterium longum and L. acidophilus.
reduce the risk of adverse pregnancy outcomes through its
Furthermore, angiotensin converting enzyme-inhibitory peptides
preventive effect on developing insulin resistance. Insulin
have been found in yogurt, cheese and milk fermented with L.
resistance normally develops during the last trimester in
casei ssp. rhamnosus, L. acidophilus and Biﬁdobacteria strains.
pregnant women. Therefore, the changes we observed in the
Lack of signiﬁcant effect of probiotics on blood pressure in this
group receiving the conventional yogurt are normal. The
study might be explained by the normal blood pressure levels of
interesting aspect of our ﬁndings is the absence of these
changes in the group received probiotic yogurt.
The exact mechanisms by which probiotics might affect serum
The beneﬁcial effects of probiotics on serum insulin levels and
insulin levels and insulin resistance are unknown. Owing to the
insulin resistance have previously been reported. Andreasen
use of glucose as the primary energy source by probiotics, their
et al.in a randomized trial among type 2 diabetic patients
effect on serum insulin levels might be mediated through
have reported that intake of L. acidophilus for 4 weeks preserved
inﬂuencing blood glucose levels. Decreased absorption of glucose
insulin sensitivity compared with the placebo group. Such effects
by probiotics might also be explained by their effect on changing
have also been reported in experimental Several
the intestinal environment,host gene expression and gut
strains of bacteria, such as Lactobacilli and Biﬁdobacterium, have
permeability.However, the effect of probiotics on FPG cannot
also been shown to improve glucose tolerance and insulin
be regarded as the single explanation for maintenance of serum
resistance in animal models.In a study by Cani et al.
insulin levels because FPG has also decreased in conventional
yogurt group. Therefore, other mechanisms might be involved in
secretion was seen with the consumption of Biﬁdobacterium spp.
the beneﬁcial effect of probiotics in these pregnant women.
in diabetic mice fed high-fat diet. Consumption of Lactobacillus
Consumption of probiotics might affect the signaling line of
rhamnosus GG for 4 weeks in streptozotocin-induced diabetic rats
insulin secretion. In an earlier study, consumption of VSL#3
has also been resulted in improved glucose tolerance and insulin
probiotics in mice has been resulted in improved insulin resistance
Beside individual probiotics, combination of their
due to increasing the hepatic natural killer T cells and reducing the
strains has also been reported to be advantageous in reducing the
inﬂammatory Our previous study in this group of
onset of insulin resistance and diabetes in animals. Consumption
pregnant women indicated the reduced levels of inﬂammation by
probiotic Therefore, the beneﬁcial effects of probiotic
Biﬁdobacteria, Lactobacilli and S. thermophilus) for 4 weeks in
yogurt on serum insulin levels might be mediated through their
diabetic mice improved hepatic insulin resistance.Improved
effects on high-sensitivity C-reactive protein, a surrogate measure
European Journal of Clinical Nutrition (2013) 71 – 74
of inﬂammation. Reduced activity of Jun N-terminal kinase, a
10 Kirwan JP, Hauguel-De Mouzon S, Lepercq J, Challier JC, Huston-Presley L et al.
tumor necrosis factor-regulated kinase that promotes insulin
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randomized trial instead of double-blind method. This might
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affect our ﬁndings. Second, we were unable to administer the
Gestational diabetes mellitus manifests in all trimesters of pregnancy. Diabetes
yogurts for 49 weeks due to budget limitations. Third, we were
unable to measure FPG and serum insulin levels repeatedly.
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European Journal of Clinical Nutrition (2013) 71 – 74
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