Bifidobacterium lactis BS01 and Lactobacillus acidophilus LA02 supplementation may change the mineral balance in healthy young women

Abstract

Czajeczny D., Kabzińska-Milewska K., Wójciak R.W. 2021. Bifidobacterium lactis BS01 and Lactobacillus acidophilus LA02 supplementation may change the mineral balance in healthy young women. AbstrAct Gut microbiota is involved in the metabolism of calcium, iron, magnesium, selenium, copper, zinc, and silver. Previous research indicates that the mineral status of an organism is associated mostly with the mineral content in the diet, but there is also evidence for probiotic bacteria having an effect on facilitating mineral absorption. However, the effect of probiotic supplemen-tation on the gut microbiota composition is not clear, with some studies pointing towards no effect, or towards individual and strain-specific efficacy. Hair samples were previously established as a biomarker of dietary mineral intake over the previous 6-8 weeks. The aim of this research was to test the hypothesis that prophylactic consumption of Bifidobacterium lactis BS01 and Lactobacillus acidophilus LA02 can impact the mineral status in healthy females. The study utilizes a randomized, single-blind, placebo-control design. 53 healthy females between 19 and 33 years old were enrolled, and 38 completed the trial. A 6-week supplementation with Bi-fidobacterium lactis BS01 and Lactobacillus acidophilus LA02 or placebo was conducted. Participants were asked not to change any of their diet and lifestyle habits during the study. The contents of Ca, Mg, Zn, Cu, and Fe in hair samples were determined by flame atomic absorption spectrometry. The outcome of this study provides evidence that Bifidobacterium lactis BS01 and Lactobacillus acidophilus LA02 strains might be useful for improving the mineral status in healthy people (without dietary intervention), increasing Ca, Mg, Fe, and decreasing Cu concentration in hair, changing the mineral balance. The results support the hypothesis that probiotics might possibly have antidepressant properties.

Full text

Czajeczny D., Kabzińska-Milewska K., Wójciak R.W. 2021.
Bidobacterium lactis BS01 and Lactobacillus acidophilus LA02
supplementation may change the mineral balance in healthy young women.
J. Elem., 26(4): 849-859. DOI: 10.5601/jelem.2021.26.1.2121
Journal of Elementology ISSN 1644-2296
ORIGINAL PAPER
RECEIVED: 24 February 2021
ACCEPTED: 22 October 2021
BIFIDOBACTERIUM LACTIS BS01
AND LACTOBACILLUS ACIDOPHILUS LA02
SUPPLEMENTATION MAY CHANGE THE MINERAL
BALANCE IN HEALTHY YOUNG WOMEN*
Dominik Czajeczny, Karolina Kabzińska-Milewska,
Rafał Wojciech Wójciak
Chair and Department of Clinical Psychology
Poznan University of Medical Sciences, Poland
AbstrAct
Gut microbiota is involved in the metabolism of calcium, iron, magnesium, selenium, copper,
zinc, and silver. Previous research indicates that the mineral status of an organism is associated
mostly with the mineral content in the diet, but there is also evidence for probiotic bacteria
having an effect on facilitating mineral absorption. However, the effect of probiotic supplemen-
tation on the gut microbiota composition is not clear, with some studies pointing towards no
effect, or towards individual and strain-specic efcacy. Hair samples were previously estab-
lished as a biomarker of dietary mineral intake over the previous 6-8 weeks. The aim of this
research was to test the hypothesis that prophylactic consumption of Bidobacterium lactis
BS01 and Lactobacillus acidophilus LA02 can impact the mineral status in healthy females. The
study utilizes a randomized, single-blind, placebo-control design. 53 healthy females between 19
and 33 years old were enrolled, and 38 completed the trial. A 6-week supplementation with Bi-
dobacterium lactis BS01 and Lactobacillus acidophilus LA02 or placebo was conducted. Partic-
ipants were asked not to change any of their diet and lifestyle habits during the study. The
contents of Ca, Mg, Zn, Cu, and Fe in hair samples were determined by ame atomic absorption
spectrometry. The outcome of this study provides evidence that Bidobacterium lactis BS01 and
Lactobacillus acidophilus LA02 strains might be useful for improving the mineral status in
healthy people (without dietary intervention), increasing Ca, Mg, Fe, and decreasing Cu concen-
tration in hair, changing the mineral balance. The results support the hypothesis that probiotics
might possibly have antidepressant properties.
Keywords: hair, minerals, probiotics, supplementation, women.
Dominik Czajeczny, Collegium Stomatologicum, Poznan University of Medical Sciences,
Poznań, 60-812, Poland, Tel: +48 723 343 803, e-mail: d.czajeczny@gmail.com
* The study has been supported by the Poznan University of Medical Sciences grant for young
scientist.

850
INTRODUCTION
The gastrointestinal tract is a natural habitat for many microbial species
(Hu, Wang et al. 2016), including up to 1000 species of bacteria (Qin et al.
2010). The gut microbiota can be considered to be a bacterial organ located
inside the host’s organism. It complements human biology, allowing us to
take advantage of bacteria’s genetic and metabolic attributes, thus playing
an important role in our functioning (BäckHed et al. 2005). Gut bacteria pre-
vent pathogenic colonization by competing for shared nutrients and niches,
and also inuence the host’s immune responses (kamada et al. 2013). Altera-
tions in gut microbiota and associated increased gut permeability (which
triggers an immune response) are now widely accepted as relevant to the
etiology, course, and treatment of many neuropsychiatric disorders (LecLercQ
et al. 2014). The development of the HPA axis (hypothalamic-pituitary-adre-
nal axis) response is dependent on early gut colonization (Sudo et al. 2004),
and some studies suggest that probiotics might have antidepressant proper-
ties (Liang et al. 2015).
Gut microbiota plays an important role in digestion and metabolism
(BäckHed et al. 2005). It has been linked to the development of obesity,
cardiovascular disease, and metabolic diseases, such as type 2 diabetes
(cLaeSSon et al. 2012, TremaroLi, BäckHed 2012). Studies on both animal
models and humans show that microbiota can affect the energy yield from
food and regulate fat storage (Skrypnik, SuLiBurSka 2018). There is also evi-
dence for probiotic bacteria having an effect on facilitating mineral absorp-
tion (ScHoLz-aHrenS et al. 2007) and a similar effect for prebiotics (which
selectively promote the growth of bacteria species in the gut) (ScHoLz-aHrenS,
ScHrezenmeir 2002). A review of studies by Skrypnik and SuLiBurSka (2018)
indicates that gut microbiota is involved in the metabolism of calcium, iron,
magnesium, selenium, copper, zinc, and silver.
The mineral status of an organism is associated with age but depends
mostly on the mineral content in the diet (Wójciak et al. 2004). An Iranian
study on 238 females reported normal iron status for only 49.8% of the sub-
jects (SHamS et al. 2010). Data from Poland indicate that dietary iron intake
in young adult females (aged 19-30) provides only slightly above 50% of the
recommended daily allowance (Wójciak et al. 2004).
A 2020 study by WiLLemSe et al. (2020) reported that 42% of pregnant
women subjected to the study had a calcium intake below the estimated
average requirement of 800 mg/day. Despite the frequent use of food supple-
ments containing calcium in the studied population (64.8% women at
8 weeks of gestation), such products do not provide sufcient amounts
of calcium to make up for a decient diet, median calcium content of 120.0
(60.0-200.0 mg/day). Due to the reported prevalence of mineral-decient
diets in females across the globe (SuLiBurSka 2011), the ability of probiotics
to facilitate mineral absorption might be essential in the improvement of the

851
mineral status in women. The functioning of an organism is related not only
to the content of minerals but also to the balance between them. SuLiBurSka
et al. (2011) argue that the proportions between zinc and copper are espe-
cially important because of the antagonistic interaction between them at the
absorption and transport stages.
Probiotic products are the fastest-growing group of dietary supplements
worldwide (cHampagne et al. 2018). They have become increasingly popular
pharmacy and grocery items and are widely used in different areas of medi-
cine and nutrition (adamS 2015). Despite the claimed health benets of such
products, in most countries, food supplements are considered food. Therefore,
they are not tested for efcacy or even safety before entering the market
(czajeczny et al. 2020a). The effects of probiotic supplementation on human
health are still debated, with some data indicating that probiotic supplemen-
tation might not be a reliable way to change the gut microbiota composition
(zmora et al. 2018). BenTon et al. ( (2007) argue that probiotics might be effec-
tive only in clinical populations where there is room to grow. In our previous
study, probiotic supplementation did not impact healthy females’ anthropo-
metric measures (czajeczny et al. 2020a).
The aim of this research was to test the hypothesis that prophylactic
consumption of probiotic bacteria can impact the mineral status in healthy
females.
MATERIAL AND METHODS
Participants
53 female participants were recruited via internet ads and posters on the
university campus. During an initial interview, a written informed consent
and general health information were obtained from the participants. Parti-
cipants with: 1) gastroenteric, 2) endocrine, 3) neurological, or 4) psychiat-
ric disorders, 5) antibiotic treatment up to 3 months prior to the supple-
mentation, and 6) current probiotic supplementation were excluded from
the study. 38 participants (20 in the supplementation and 18 in the placebo
group) completed the study. The most common reason for leaving the study
was an antibiotic treatment during the supplementation period. Other rea-
sons included withdrawal of consent, and in one case – the onset of a psy-
chiatric disorder. The characteristics of the research group are presented in
Table 1.
Study protocol
The study protocol was previously described in another publication
(czajeczny et al. 2020a) The study protocol was approved by the Poznan
University of Medical Sciences Bioethics Committee (No. 1070/16, 05.01.2017).

852
Hair samples were collected twice - at baseline and after treatment.
They were taken by one researcher in an effort to minimize discrepancies
between collecting techniques. Participants were provided one probiotic sup-
plement or placebo capsule daily for 6 weeks, as recommended by the supple-
ment’s manufacturer. A second meeting was scheduled at the convenience
of the participants but no later than 7 days after taking the last capsule.
Participants were asked not to change any of their diet and lifestyle habits
during the study. They were instructed to immediately contact a researcher
in case any side effects of supplementation occurred. No participants repor-
ted any side effects of either supplement or placebo (czajeczny et al. 2020a).
Supplementation
Bidobacterium lactis BS01 (2 109 CFU) and Lactobacillus acidophilus
LA02 (2 109 CFU) bacteria in the form of a probiotic supplement were used
in this study. Placebo was prepared using empty capsules (similar in size
and colour to supplement capsules) and maltodextrin as a ller (STeenBergen
et al. 2015). Both products had the same taste, colour, and smell, and were
provided to participants in ziplock bags. Participants were blinded to whether
they received probiotic or placebo capsules.
Assessment of metal concentrations in hair
Previous publications by other authors described the preparation of hair
samples and the determination of minerals in the hair, as well as reference
values for hair elements (cHojnacka et al. 2010, SuLiBurSka 2011). Hair sam-
ples, taken from six different points of the occipital scalp (about 0.5 g, 1.0 cm
from the skin), were washed three times in unionized detergent, deionized
water, acetone, and deionized water again, then dried to a dry mass (at 105°C).
Wet mineralization in a nitric acid environment (65%, supra pure, Merck)
using the Ethos Easy microwave mineralizer (Milestone Srl) was conducted.
After proper dilutions, the contents of Ca, Mg, Zn, Cu, and Fe in the hair
samples were determined by ame atomic absorption spectrometry using an
iCE3500 spectrophotometer (ThermoFisherScientic). The accuracy of the
method was veried with certied reference material (NCS DC 73347 human
hair). Standards recovery was 99.6-102.9%. For details of the analysis see
Table 1
Research group details
Variable Placebo Supplementation
Age (years) mean ± SD
Range
Median
23.06±3.11
20–29
23
23.47±4.19
19–31
24
BMI (kg m-2) mean ± SD
Range
Median
22.01±2.42
18.65–28.07
21.42
23.67±5.56
18.65–29.93
22.38

853
Wojciak (2019). The reference values established on the basis of previous
research by the authors (Wojciak et al. 2004, 2010, 2019) and other authors’
research (SuLiBurSka et al. 2015), were as follows: Ca – 600-1000, Mg – 40-60,
Zn – 160-200, Cu – 10-20, Fe – 10-20 µg g-1 d.m.
Statistical analysis
The normality of distributions was tested with the Shapiro-Wilk test.
The hair mineral concentration distribution was shown to deviate from nor-
mality. The Wilcoxon test was used to determine the differences between
means before and after supplementation. The χ2 test was used to compare
data distributions against normative / reference values. The data were pre-
sented using basic descriptive statistics: arithmetic mean, standard devia-
tion, range, and median. All analyses were performed using the Statistica
ver. 13.3 statistical program at a signicance level of 0.05.
RESULTS AND DISCUSSION
The results in this study are presented in Tables 2 and 3. Table 2 con-
tains data on hair mineral concentrations in placebo and supplementation
groups before and after probiotic treatment. In the placebo group, changes in
mean Ca, Mg, Zn, Cu, and Fe concentrations in hair samples were not signi-
cant. In the supplementation group, mean concentrations of Ca, Mg, and Fe
signicantly increased after the probiotic treatment. The mean concentration
of Cu signicantly decreased after the probiotic treatment, and the change
in the mean concentration of Zn after the probiotic treatment was not signi-
cant. All of the differences between groups in terms of mean concentrations
of minerals in hair samples at baseline (before treatment) were not signi-
cant, indicating successful randomization.
Table 3 presents the percentage distribution of participants according
to hair mineral reference values (RVs). No signicant changes (Ca, Mg, Zn,
Cu, Fe) in distributions according to RVs were observed in the placebo group.
In the supplementation group, signicant changes of distributions
according to RVs were observed for Ca, Mg and Fe. The percentage of partic-
ipants <RVs for Ca changed from 31% to 6%. A general shift towards >RVs
was observed. The percentage of participants <RVs for Mg changed from 13%
to 6%. A general shift towards >RVs was for Mg was also observed. The dis-
tribution of Fe RVs changed towards >RVs (from 25% >RVs pre-treatment
to 63% >RVs post-treatment). The distribution of Cu RVs shifted towards
<RVs, but this change was not statistically signicant.
In both the supplementation and placebo groups, no participants were
below RVs for Fe. The presented study investigated the effects of prophylac-
tic Bidobacterium lactis BS01 and Lactobacillus acidophilus LA02 supple-

854
mentation on the mineral status in healthy, young females. The main aim
of the study was to assess whether prophylactic consumption of probiotic
supplementation can impact the mineral concentrations in hair.
The outcome of this study provides evidence that Bidobacterium lactis
BS01 and Lactobacillus acidophilus LA02 supplementation affects the mine-
ral status in healthy females, increasing the calcium, magnesium, iron while
decreasing the copper concentrations in hair. The probiotic treatment also
affected the distribution of participants according to RVs. Calcium, magne-
sium, and iron distributions were shifted towards RV and >RV after the pro-
biotic treatment. No signicant changes were observed in the placebo group
in both mean mineral concentrations in hair and percentage distribution
according to RVs.
The diets of females around the world are low in calcium, magnesium,
and iron (SuLiBurSka 2011). Despite the commonly reported iron deciency
among adolescent and adult females (aLzaHeB aL-amer 2017, aLSHeikH 2018),
no participants in this study were <RVs for iron concentration in hair. In the
authors’ previous study (SuLiBurSka 2011), 4% of females aged between
19 and 30 (age group similar to this study) were <RVs for iron. A signicant
increase in iron concentrations in hair after the probiotic treatment suggests
Table 2
Hair mineral concentrations in the placebo and the supplementation group (µg g-1 d.m.)
Minerals Placebo Supplementation
before after before after
Ca
mean±SD
range
median
975.8±308.8
475.8–1623.87
985.9
1003.4±285.0
(480.9–1524.8)
986.5
1077.6±578.7
(369.4–2286.1)
986.9
1424.3±505.5
(402.8–2560.8)
1375.4
Statistic p0.1402 0.0005
Mg
mean±SD
range
median
60.22±27.79
23.85–117.79
55.43
57.37±25.86
22.81–129.95
56.03
52.75±11.58
25.04–72.58
54.25
59.64±13.59
26.38–79.32
60.39
Statistic p0.3137 0.0008
Zn
mean±SD
range
median
231.8±73.9
143.3–415.3
210.7
221.8±68.3
138.5–402.8
207.2
243.5±94.2
143.6–556.6
222.5
245.8±53.3
166.8–383.1
242.0
Statistic p0.1280 0.9204
Cu
mean±SD
range
median
21.55±9.66
4.93–36.27
21.44
22.85±10.84
5.14–39.84
19.04
22.55±18.53
3.46–63.90
12.58
18.27±15.97
1.64–56.93
11.98
Statistic p0.1084 0.0149
Fe
mean±SD
range
median
22.82±7.20
13.07–37.58
19.71
23.03±7.90
13.50–36.56
20.64
17.95±3.71
12.88–26.50
18.10
20.82±4.32
14.25–30.99
20.71
Statistic p0.8313 0.0002

855
that it may be useful for improving the iron status in iron-decient indivi-
duals even without iron supplementation or dietary interventions (pedLar
et al. 2018). Iron deciency has been associated with depressive symptoms
(HideSe et al. 2018). Improvement of the iron status might be one of the
mechanisms of hypothesized effect of a probiotic on mood. Other mechanisms
involve changes in immune response and hypothalamic-pituitary-adrenal
HPA axis activity. These mechanisms were further discussed in our previous
article (czajeczny et al. 2020b).
Magnesium decits have also been associated with the development
of depression in both human and animal studies (Wang et al. 2018). A 2017
study (BamBLing et al. 2017) reported decreased depressive symptoms
in patients with poor previous SSRI treatment outcomes after an 8-week
treatment with a combination of Lactobacillus acidophilus, Bidobacterium
bidum, Streptoccocus thermophiles ( total CFU of 2 1010), and magnesium
orotate (1600 mg) divided into two daily doses. The study did not compare
Table 3
Percentage distribution of subjects according to reference values (RVs) for hair minerals (%)
Specication Placebo Supplementation
before after before after
Ca
<RVs 6 6 31 6
RVs 47 47 19 6
>RVs 47 47 50 80
Statistic (χ2, p) (0.00, 1.0000) (34.12, 0.0000)
Mg
<RVs 18 18 13 6
RVs 41 47 56 44
>RVs 41 35 31 50
Statistic (χ 2, p)(0.88, 0.6431) (8.48, 0.0144)
Zn
<RVs 12 12 6 0
RVs 29 24 25 25
>RVs 59 65 69 75
Statistic (χ 2, p)(0.67, 0.7136) (3.84, 0.1465)
Cu
<RVs 12 12 31 44
RVs 29 41 31 25
>RVs 59 47 38 31
Statistic (χ2, p)(3.42, 0.1813) (3.61, 0.1648)
Fe
<RVs 0 0 0 0
RVs 53 47 75 38
>RVs 47 53 25 63
Statistic (χ 2, p)(0.72, 0.3961) (29.30, 0.0000)

856
the effects of probiotics and magnesium supplementation separately; howe-
ver, another study (TarLeTon et al. 2017) reported attenuated depressive
symptoms after just 2 weeks of magnesium chloride (248 mg of elemental
magnesium per day) supplementation, and the results of this study suggest
that probiotic consumption alone might improve magnesium absorption,
potentially affecting depressive symptoms associated with magnesium decit.
This outcome further supports the hypothesis that probiotics might have
antidepressant properties (maroTTa et al. 2019) and might improve mineral
absorption when combined with mineral supplements, improving their efcacy.
In this study, 31% of the supplementation group participants were <RVs
for calcium before the probiotic treatment. This percentage dropped to 6%
after the treatment, and the mean calcium concentration in hair improved
signicantly in the supplementation group. Calcium bioavailability depends
not only on the source but also the age, transit time, the amount of calcium
ingested, intestinal content, and type of diet. Higher content of phytate, oxa-
late, and dietary bre in the diet, along with higher pH (alkaline condition),
can interfere with calcium absorption (duBey, paTeL 2018). Probiotics pro-
duce short-chain fatty acids, which increase the solubility of available calci-
um (duBey, paTeL 2018). A study on mice with Lactobacillus plantarum NTU
102 fermented soy milk showed that through the production of enzyme
phytase, probiotic treatment could increase the release of the depressed cal-
cium and increase calcium availability at the site of absorption (cHiang, pan
2011).
The observed decrease of the mean copper concentrations in hair after
the probiotic treatment is in line with the previously reported inverse corre-
lation of copper with calcium, magnesium, iron, and zinc levels in hair.
This can be explained by the interactions between minerals at the stage
of transport and absorption (SuLiBurSka 2011).
In this study, no effect of probiotic treatment on zinc levels in hair was
observed, but a recent in-vitro study reported a 2% increase in zinc bioacces-
sibility and a 4% increase in iron bioaccessibility after fermenting Uapaca
kirkiana (indigenous fruit tree found in the miombo ecological zone in
sub-Saharan Africa) fruit pulp with Lactobacillus rhamnosus yoba strain
(cHaWafamBira et al. 2020). The authors argue that promoting probiotic foods
might help improve nutrition in poor populations in sub-Saharan Africa.
CONCLUSIONS
The outcome of this study provides evidence that Bidobacterium lactis
BS01 and Lactobacillus acidophilus LA02 strains might be useful for improv-
ing the mineral status in healthy people. The reported increase in mineral
concentrations in hair might be an effect of improved mineral absorption and
transportation. It is important to note, however, that more is not always

857
better and the optimal functioning of an organism is related not only to the
content of minerals but also to the balance between them (SuLiBurSka 2011).
The multitude of bacterial strains used in probiotic products and combi-
nations of probiotics with prebiotics, mineral supplements etc., make it dif-
cult to draw general conclusions on the effects of probiotics on the mineral
status and other health aspects. A meta-analysis by mcfarLand et al. (2018)
found strong evidence that the efcacy of probiotics is both strain-specic
and disease-specic. Strains used in this study were benecial for mineral
status but not for anthropometric measures ( czajeczny et al. 2020a).
Authors’ contribution
Dominik Czajeczny: funding acquisition, conceptualization, methodo-
logy, investigation, formal analysis, writing – original draft preparation,
writing – reviewing and editing,
Karolina Kabzińska-Milewska: conceptualization, investigation,
writing – reviewing and editing,
Rafał Wojciech Wójciak: conceptualization, methodology, formal analy-
sis, supervision.
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