Food Chemistry 239 (2018) 1151–1159

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Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem

Magnesium enriched lactic acid bacteria as a carrier for probiotic ice

cream production
Małgorzata Góral a,⇑, Katarzyna Kozłowicz b, Urszula Pankiewicz a, Dariusz Góral b
a
Department of Analysis and Food Quality Assessment, Faculty of Food Science and Biotechnology, University of Life Sciences, Skromna 8, 20-704 Lublin, Poland
b
Department of Refrigeration and Food Industry Energetics, Faculty of Production Engineering, University of Life Sciences, Doświadczalna 44, 20-280 Lublin, Poland

a r t i c l e i n f o a b s t r a c t

Article history: The following strains of bacteria: Lactobacillus rhamnosus B 442, Lactobacillus rhamnosus 1937, and
Received 20 April 2017 Lactococcus lactis JBB 500 were enriched with magnesium ions using Pulsed Electric Fields. The poten-
Received in revised form 10 July 2017 tially probiotic strains were added to the mixture in the DVS process and applied for the production of
Accepted 11 July 2017
ice cream which were then analyzed physicochemically and microbiologically. Results showed that addi-
Available online 13 July 2017
tion of bacteria enriched with magnesium did not change chemical parameters of the ice cream and did
not affect the freezing process, meltability, and hardness. No significant differences were noted in colour
Keywords:
of the samples. The ice cream with addition of bacteria enriched with magnesium had higher adhesive-
Ice cream
Magnesium
ness. The results of viability determination showed that the total number of microorganisms in the ice
Bioaccumulation cream was higher than in the starter cultures. Viability of the bacteria enriched with magnesium in
Lactic acid bacteria the obtained ice cream was lower in comparison to the control samples.
PEF Ó 2017 Elsevier Ltd. All rights reserved.

1. Introduction which in turn leads to reduction of mineral salts absorption by

Magnesium plays an important role in a proper functioning of
human body. It influences functioning of heart, brain and skeletal
muscles. This element it is a cofactor of enzymatic reactions, par-
ticipates in carbohydrates metabolism and enhances synaptic plas-
ticity affecting learning and memory abilities (Rylander, 2014). It
participates in the synthesis of DNA and RNA and oxidative phos-
phorylation. Magnesium plays a key role in the active transport of
calcium and potassium ions through cell membranes. About 99% of
all magnesium is found in bones, muscles and soft tissues. Between
50% and 60% occur as substrates of the hydroxyapatite bone min-
eral surface. The rest is located in the skeletal muscles and soft tis-
sues. The magnesium content and its bioavailability in bones
decreases with age. Intracellular concentration of the element var-
ies in the range 5–20 mmol
l1 (Gröber, Schmidt, & Kisters, 2015).
According to FAO/WHO (2004), the daily recommended intake
of magnesium for males is 260 mg and for women is 220 mg. The
studies proved that about 60% of U.S. population shows deficit of
this element. According to De Baaij, Hoenderop, and Bindels
(2015) intensification of agriculture, among others, is responsible
for this phenomenon. Monoculture farming causes soil depletion
⇑ Corresponding author at: University of Life Sciences, Skromna Street 8, 20-704
Lublin, Poland.
E-mail address: sd-779@student.up.edu.pl (M. Góral).
plants. Processing of food commodities also causes decrease of
vitamin and minerals contents in food (Chaudhary, Sharma, &
Bansal, 2010). Magnesium deficiency increases a risk of heart dis-
eases, high blood pressure, lithiasis and depression (Derom,
Sayón-Orea, Martínez-Ortega, & Martínez-González, 2013). Sup-
plementation of diet with magnesium ions may be a solution for
this problem. The most frequently used method is pharmacological
supplementation, however the bioavailability of these prepara-
tions is low (De Nicola & Walker, 2009). The studies showed that
magnesium in the form of magnesium citrate is absorbed only in
_
4% (Ostrózka-Cieślik, Dolińska, & Ryszka, 2015). Metal ions can also
be delivered as complexes with proteins. Living organisms widely
used in the food industry, such as lactic acid bacteria or yeast, can
incorporate elements into their cellular structures becoming a
source of minerals in the human diet (De Nicola & Walker, 2009).
Therefore, it seems to be reasonable to supply magnesium ions
in the form of easily absorbed protein complexes produced by
bacteria.
Probiotic lactic acid bacteria (LAB) are responsible for mainte-
nance of intestinal microflora, prevent inflammations and protect
against gastrointestinal tract disorders (Parvez, Malik, Kang, &
Kim, 2006). Additionally, they are involved in immune response
of the organism and potentially prevent against colon cancer
(Xing et al., 2016). LAB can be used for production of probiotic
ice cream because of their pro-health properties and suitable type

http://dx.doi.org/10.1016/j.foodchem.2017.07.053
0308-8146/Ó 2017 Elsevier Ltd. All rights reserved.
1152 M. Góral et al. / Food Chemistry 239 (2018) 1151–1159
of carrier (yoghurt). pH of ice cream is higher than that of tradi-
tional fermented dairy products which is beneficial for LAB (Akin
& Dasnik, 2015). Moreover, consumers eagerly reach for this pro-
duct as it can be stored for long time without loss of physicochem-
ical and organoleptic quality (Mohammadi, Mortazavian,
Khosrokhavar, & da Cruz, 2011). It is worth mentioning that intro-
duction of lactic acid bacteria to ice cream does not decrease gen-
eral quality of this product (Ranadheera, Evans, Adams, & Baines,
2013). Adequate survival of probiotics, however, requires opti-
mization of each stage of the production process (Cruz, Antunes,
Sousa, Faria, & Saad, 2009). Probiotics can be introduced into ice
cream in the free state or in the form of microcapsules. In the first
case the ice cream mixture is blended with the fermented milk
base or it is directly inoculated (before freezing) with bacteria.
Introduction of the inoculum can cause total or partial fermenta-
tion of the mixture or it does not participate in the fermentation
process at all. It depends on the expectations for the final product
(Soukoulis & Tzia, 2008). Fermented probiotic ice creams, unlike
unfermented ones, are characterized by significant physicochemi-
cal changes. Inoculum size, fermentation conditions, pH and bacte-
rial strain influence, among others, viscosity of the product (Di
Criscio et al., 2010).
The above statements show that ice cream with addition of
potentially probiotic bacteria can be regarded as functional food
which has beneficial effect on human body. Moreover, magnesium
introduced to foodstuffs in an easily absorbed form eliminates
effects of its deficiency.
The aim of the work was to investigate the possibility of enrich-
ment of ice cream made from natural yoghurt produced under lab-
oratory conditions with potentially probiotic lactic acid bacteria
(Lactobacillus rhamnosus and Lactococcus lactis species) containing
magnesium ions. Moreover, the effect of bacteria addition on the
selected physicochemical properties of ice cream was studied.
2. Materials and methods
2.1. Ingredients for ice cream production
The following ingredients were used to prepare the ice cream:
sterile milk containing 3.2% of fat (Mlekopol, Poland), skimmed
milk powder (SM Gostyń, Poland), cream containing 36% of fat
(SM Łowicz, Poland), sugar, vanilla flavour (Delecta, Poland), inulin
(Agnex, Białystok) and emulgator E 471 (Fooding, Shanghai).
2.2. Bacterial strain and culture condition
Three strains of bacteria: Lactobacillus rhamnosus B 442, Lacto-
bacillus rhamnosus 1937, Lactococcus lactis JBB 500 from the collec-
tion of Department of Biotechnology, Human Nutrition and Science
of Food Commodities, University of Life Sciences in Lublin, Poland
were used in the experiment. For the preparation of inoculum and
culture medium the following components were used: MRS broth
(Btl) 58.937 g/L, Tween 80 (Biochemica, ICI, USA) 1 mL/L, agar
(DIFCO, Detroit, MI, USA) 15 g/L, NaCl 80 g/L and MgCl2  6 H2O
(POOCH, Gliwice, Poland) in concentration of 400 lg Mg2+/mL
medium.
2.3. Preparation of culture
Bacteria were passaged three times in MRS broth and incubated
at 37 °C (for Lactobacillus rhamnosus strains) and 30 °C (for Lacto-
coccus lactis JBB 500). Then inoculum was prepared by transferring
3 mL of bacteria to 57 mL of sterile medium in 500-mL Erlenmeyer
flasks. Flasks were incubated at 37 °C and 30 °C for 48 h. The
obtained inoculum (5 mL) was transferred into 85 mL of sterile
medium (sterilization at 121 °C and 0.5 atm for 20 min) placed in
Erlenmeyer flasks. An 10-mL aliquots of magnesium chloride at
400 lg Mg2+/mL medium concentration was added to each flask
(except of the control samples K1, K2, K3). Then the culture was
incubated at 37 °C and 30 °C for 24 h. Cultures were treated with
pulsed electric field (PEF) for 15 min at pulse width 20 ls, electric
field strength 2.0 kV/cm, at the field frequency of 1 Hz using a lab-
oratory electroporator (except of the control samples K1, K2, K3).
Then the cultures were incubated for 20 h. Biomass was cen-
trifuged (15 min, 3000 rpm, 1467g), supernatant was discarded,
and cells were rinsed three times with sterile 0.9% saline
(Songtummin & Leenanon, 2016).
2.4. Preparation of ice cream
The bacteria cultures were added to ice cream during its pro-
duction in a DVS process (Direct Vat Set) (Cruz et al., 2009). Each
strain, in amount of 4.5%, was cultured in sterile milk for 24 h at
respectively, 37 °C (Lactobacillus rhamnosus B 442 and Lactobacillus
rhamnosus 1937) and 30 °C (Lactococcus lactis JBB 500). The fer-
mented milk was added to the prepared ice cream mixture (cream
15%, skimmed milk powder 15%, sugar 10%, emulgator 0.2%, inulin
4.7% and vanilla flavour) in amount of 55%. The mixtures were pre-
pared in traditional way by weighing of ingredients according to
the prescription, thorough mixing and aeration. Simultaneously,
the control samples of ice cream containing bacteria not supple-
mented with magnesium were produced (K1, K2, and K3). Each
type of ice cream with added bacteria was produced in three differ-
ent repetitions.
2.5. Freezing process
Freezing was performed in an ice cream maker (Ariete Galatiera
Compact, Italy) until the ice cream temperature was 6 °C. Tem-
perature was recorded at every minute interval (twice) using a
temperature mini data logger (Kimo KT 20, Germany). On the basis
of the recorded data the freezing curves were plotted and the cryo-
scopic temperature was determined using Microsoft Office Excel
2007 (Rahman et al., 2002). Then the samples were placed in plas-
tic containers and hardened at 30 °C for 24 h (chest deep freezer,
Whirlpool). Physicochemical analyses were carried out after
lyophilization of the samples, 48 h of storage at 30 °C (liofilizator
LABCONCO 64132, USA).
2.6. Determination of magnesium concentration
Bacteria biomass was lyophilized and mineralized in a MARS
microwave oven (CEM Corporation). Samples were prepared as fol-
lows: about 0.1 g of lyophilizate was transferred to a tube and 3 ml
of HNO3 was added. Then the samples were mineralized at 200 °C
for 20 min. The obtained solutions were cooled down, transferred
to 25 mL measuring flasks and topped up with deionized water.
Concentration of magnesium ions in L. rhamnosus B 442, Lactobacil-
lus rhamnosus 1937, Lactococcus lactis JBB 500 cells was determined
using an electrothermal atomic absorption spectrophotometer (ET-
AAS, VARIAN AA 280 FS) according to PN-EN 15505:2009 (2009).
2.7. Determination of magnesium and calcium concentration in ice
cream
The analysis was carried out according to the methodology
described in the Section 2.6. with modification of the sample
weight (0.5 g) and volume of HNO3 (5 mL).

2.8. Physiochemical analysis ice cream
All measurements were carried out in triplicate. The dry mat-
ters of ice cream were determined by drying samples at
130 ± 1 °C for 3 h (AOAC, 2000). Fat content was determined
according to AOAC (2000) applying extraction in a Soxhlet
apparatus (Tecator Soxtec System HT 1043 extraction unit, Gemini,
Apeldoorn), and protein content was assayed according to
Kjeldahl method (AOAC, 2000). Ash content was analyzed accord-
ing to PN-67/A-86430/Az2 (2002). Carbohydrates were calculated
as the difference between 100% and the sum of the percentages
of water, protein, total lipid (fat) and ash (US Department of
Agriculture, Agricultural Research Service, Nutrient Data
Laboratory, 2016).
2.9. Determination of melting time, melting resistance and melting
rate
In order to determine the melting time a cooled metal ring in a
form of a cone (stored at 30 °C for 24 h; 35 mm in height, 35 mm
in upper diameter, 25 mm in lower diameter, volume – 30 ml) was
driven into a sample. In the following step, the ice cream samples
were removed from a ring, transferred on a funnel with a mesh and
then placed in a controlled temperature chamber at 25 °C. Time of
melting was measured until the first drop appeared (Jasinska,
Trzcinski, Dmytrów, & Mituniewicz-Malek, 2012).
Melting resistance was determined according to the methodol-
ogy employed by Silva Junior and Lannes (2011) modifying the
sample size and melting time. It was determined by measuring
the dripped volume for 25 min every 5 min since the samples were
placed in a controlled temperature chamber. The data recorded
were used to determine the melting rate (mL/min). The analyzes
were performed in 3 replications.
2.10. Texture measurements
The evaluation of textural properties of ice cream: hardness and
adhesiveness was performed according to the methodology of
Tiwari, Sharma, Kumar, and Kaur (2015) adapted to the test
requirements recommended by Brookfield Engineering Laborato-
ries. The penetration test with chamber for backward extrusion
were determined on LFRA texture analyzer (Brookfield Engineering
Laboratories, Inc., Middleboro, Massachusetts). The chamber was
filled with ice cream at temperature of 6 °C. Hardness was
defined as a maximal force (N) required to push a probe into the
sample on a half of its height. Adhesiveness was determined on
the basis of a force recorded during withdrawal of a probe from
the sample. The following parameters were assumed for analysis:
probe diameter – 12 mm, chamber diameter – 30 mm, probe rate
during penetration – 0.2 mm/s, and pressure force – 0.2 N (Tiwari
et al., 2015). The analyzes were performed in 6 replications.
2.11. Colour determination
Colour of ice cream was determined using a colorimeter LOVI-
BOND CAM-SYSTEM 500 (The Tintometer Ltd., Amesbury, UK)
and expressed in CIE – L⁄a⁄b system where L⁄ – lightness of ice
cream (1–100), a⁄ – redness (+100) and greenness (100),
b⁄ – yellowness (+100) and blueness (100). The measurements
were performed in triplicate. The total colour difference (DE) was
calculated using the equation below (1):
rffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
 2 
DE ¼ Lsample  Lcontrol þ asample  acontrol þ bsample  bcontrol
M. Góral et al. / Food Chemistry 239 (2018) 1151–1159 1153
The values for background colours were: L⁄ = 91.8; a⁄ = 0.4;
⁄
b = 0.4 (Tiwari et al., 2015). The analyzes were performed in
10 replications.
2.12. Viability determination
Total number of microorganisms was determined by plate dilu-
tion method according to PN-EN ISO 7218:2008 (2008). Colonies of
microorganisms were diluted 8 and 9 times with 0.8% sterile saline
solution. Then 1 cm3 of each was taken and placed in Petri dishes in
two replicates. The diluted bacteria were flooded with sterile liquid
agar. Cultures were incubated for 48 h at 37 °C (for Lactobacillus
rhamnosus strains) and 30 °C (for Lactococcus lactis JBB 500). The
Petri dishes with two consecutive dilutions on which grew from
30 to 300 colonies were selected for reading. The total number of
microorganisms (L) in 1 cm3 of the sample was calculated accord-
ing to the formula (2):
C
L¼
d ð2Þ
ðN1 þ 0:1N2 Þ
C – sum of colonies on all dishes selected for counting,
N1 – number of dishes from the first calculated dilution,
N2 – number of dishes from second calculated dilution,
d – dilution ratio corresponding to the first (lowest) dilution.
2.13. Statistic analysis
The test of Shapiro-Wilk was applied to verify if data followed a
normal distribution. Significant differences between particular
groups were found using the Student t-test applied to compare
independent samples in pairs, and variance analysis (ANOVA)
was used for more than two groups. Detailed analysis was based
on Tukey’s confidence intervals. The Pearson’s correlation coeffi-
cients were used to evaluate linear relationships between vari-
ables. All statistical tests were carried out at significance level of
a = 0,05. Statistical processing of results was performed using R
program version 3.1.2 and Statgraphics 5.0.
3. Results and discussion
3.1. Magnesium concentration in bacterial cells
Magnesium is essential for many biochemical processes taking
place in the cells of microorganisms. It is recommended for supple-
mentation of media used for lactic acid bacteria (LAB) culturing
and it has no negative influence on bacterial cells. Magnesium
plays an important role in synthesis of proteins, DNA and sub-
stances binding to a cell membrane (Watanabe, van der Veen, &
Abee, 2012). The strains selected for ice cream production were
characterized by the highest accumulation of this element (in con-
centration of 400 lg Mg2+/mL medium) at the optimal PEF param-
eters. The cultures treated with PEF at magnesium concentration in
medium: 10, 40, 100, 200, 600, 800, 1000 lg/mL showed lower
accumulation of this element.
The conducted experiments showed that pulsed electric field
affected accumulation of magnesium in the bacterial cells. The
highest concentration of this element, that is 4.28 mg Mg2+/g d.
m., was noted for L. rhamnosus B 442. The strains L. rhamnosus
1937 and L. lactis JBB 500 accumulated, respectively, 1.97 mg
Mg2+/g d.m. and 1.86 mg Mg2+/g d.m. Concentration of Mg in the
cells was higher than in the control cultures, respectively, 6-fold
for L. rhamnosus B 442, 2-fold for L. lactis JBB 500 and about 2-
2  2
 
fold for L. rhamnosus 1937.
Roman, Gniewosz, and Mantorska (2009) reported that Mg con-
ð1Þ tent in the L. brevis biomass cultured in the medium supplemented
1154 M. Góral et al. / Food Chemistry 239 (2018) 1151–1159
with magnesium sulfate contained 1.67–2.69 mg Mg/g d.m., and in
the case of L. plantarum – 1.35–2.31 mg Mg/g d.m. Whereas
Gniewosz, Chlebowska-Smigiel, Lipinska, Krasniewska, and
Rapacka (2014) who studied the influence of addition of lactic acid
bacteria containing increased amount of Mg to dough on, among
others, its level in bread noted that accumulation of this element
was in the range from 23.66 mg Mg/100 g d.m. of bread (prepared
with addition of S. cerevisiae and L. plantarum) to 26.56 mg
Mg/100 g d.m. of bread (prepared with addition of S. cerevisiae
and L. brevis). The authors supplemented medium with 1.25 g/
dm3 of hydrated magnesium acetate.
The results of this study showed that pulsed electric fields has a
positive effect on magnesium accumulation in the cells. Concentra-
tion of Mg2+ in the cells of Lactobacillus rhamnosus B 442 was over
2-fold higher than the average content obtained by Roman et al.
(2009) and over 17-fold higher than that noted by Gniewosz
et al. (2014). The studies conducted by Pankiewicz, Sujka,
Włodarczyk-Stasiak, Mazurek, and Jamroz (2014) also confirmed
the effect of PEF on accumulation of elements in the cells of
microorganisms. Concentration of magnesium in the Saccha-
romyces cerevisiae cells treated with PEF was higher by 0.47 mg
Mg2+/g d.m. than in the control culture which was not
electroporated.
3.2. Magnesium and calcium concentration in ice cream
The interaction of magnesium and calcium ions is well known.
It has been shown that Mg2+ inhibit calcium absorption in the duo-
denum, and Ca2+ ions inhibit magnesium absorption in the ileum.
In people with idiopathic hypercalciuria and renal Ca stone disease,
dietary supplementation with magnesium ions reduces the
absorption of calcium ions in favor of magnesium ions, whereas
Mg2+ deficiency increases enterocyte content of Ca (Areco et al.,
2015). However, studies on the effect of magnesium on calcium
absorption are not unequivocal. Fine, Santa Ana, Porter, and
Fordtran (1991) observed that increasing content of Mg2+ in the
diet did not affect the absorption of Ca. While Dolińska,
Mikulska, and Ryszka (2009) believe that magnesium ions have a
positive influence on the absorption and calcium management of
the body. Magnesium deficiency is also listed as a risk factor for
osteoporosis.
The study showed that the concentration of magnesium in
magnesium-enriched ice cream ranged from 23.02 mg/100 g ice
cream to 31.29 mg/100 g ice cream and was 30–50% higher than
in the control samples which contained from 18.08 mg/100 g ice
cream to 19.26 mg/100 g ice cream. Calcium content varied from
108.42 mg/100 g ice cream to 113.89 mg/100 g ice cream (samples
with addition of magnesium) and from 107.97 mg/100 g ice cream
to 111.26 mg/100 g ice cream (control samples) (Fig. 3). The high-
est content of both elements was found in the ice cream produced
with addition of L. rhamnosus B 442 enriched with magnesium ions
with the use of PEF.
Yangılar (2015) showed that calcium and magnesium content
in ice cream with 1% peel green banana was 1723 mg/kg and
193 mg/kg, respectively. Erkaya, Dağdemir, and Sßengül (2012)
reported that contents of these elements in selected samples of
ice cream with cape gooseberry were, respectively, 1832.5 mg/kg
and 167.25 mg/kg.
3.3. Physicochemical characteristics of ice cream
Freezing of food is a physical process with lowering of their
temperature below the freezing point of a material. A temperature
decreasing inhibits metabolic processes occurring in products as
well as slows down the rate of microbiological changes. One of
the most important parameters of freezing is the cryoscopic tem-
perature. Its values allow to evaluate, among others, water activity
which affects physicochemical properties of products. A proper
freezing conditions guarantee high quality of the manufactured
ice cream (Góral & Kluza, 2009).
The cryoscopic temperature (Tcr) of the ice cream determined
on the basis of the freezing curves (Fig. 1a; Fig. 1b; Fig. 1c)
amounted to 3.5 °C for most of the samples. Only the control
samples (K1) and the samples of ice cream produced with addition
of L. rhamnosus B 442 enriched with magnesium had Tcr = 4°C.
According to the expectations, addition of magnesium did not
influence the cryoscopic temperature of the obtained ice cream.
Muse and Hartel (2004) reported that values of Tcr determined
for ice cream produced with the addition of three types of sweet-
ener and three levels of the emulsifier were in the range from
1.8 °C to 4.6 °C. On the other hand, Alvarez, Wolters,
Vodovotz, and Ji (2005) noted values of Tcr ranging from 4.68 °C
to 5.42 °C. These differences, however, had no influence on sen-
sory evaluation of ice cream. The values of Tcr obtained in this
study were in accordance with the data cited in the literature
(Alvarez et al., 2005; Muse & Hartel, 2004).
No statistically significant effect of genius, species and strain of
the studied bacteria as well as addition of magnesium on the con-
tents of fat, dry mass, water and carbohydrates in ice cream was
observed (Table 1). Concentrations of the mentioned constituents
were: 5.12–5.64% for fat, about 41% for dry mass and 26.52–
27.48% for carbohydrates. Similar values of fat content (5.77–
5.90%) were reported by Vardar and Öksüz (2007) who analyzed
the strawberry ice cream enriched with bacteria of genius Lacto-
coccus and Lactobacillus acidophilus. However, they noted lower
dry mass content (27.91–29.29%) than that noted in this study.
Ayar, Siçramaz, Öztürk, and Öztürk Yilmaz (2017) reported that
the probiotic ice cream manufactured with addition of L. aci-
dophilus and B. animalis subsp. Lactis. contained 1.13–1.83% of
ash and 3.07–4.03% of protein. In this study the lowest contents
of protein and ash were noted, respectively, for the control sample
K3 with addition of L. lactis JBB 500 (6.95%) and the sample con-
taining bacteria of this strain enriched with magnesium (1.72%).
3.4. Characteristics of melting and texture of ice cream
Melting is an important factor influencing quality of ice cream.
The melting rate of ice cream is affected by many factors, including
total solids, sizes of the ice crystals, sizes and number of fat glob-
ules. These parameters depend on composition of ice cream mix-
tures (Muse and Hartel (2004)). The values of the melting time
determined in this study were much lower than those reported
in the literature. The shortest melting time was noted for the ice
cream with L. rhamnosus 1937 (the control sample K2) and the
longest – for the ice cream containing L. rhamnosus B 442 (the con-
trol sample K1) (Table 2). The melting rate ranged from 0.78 ml/
min to 1.03 ml/min. The control sample with L. rhamnosus B 442
showed the highest melting resistance. It may be caused by a
low participation of stabilizer in the ice cream mixture which binds
water molecules and consequently retards melting. Akin, Akin, and
Kirmaci (2007) noted that values of the first dripping time and the
complete melting time were in the ranges, respectively, 1780 s
(15% sugar without inulin)- 2058 s (21% sugar supplemented with
2% inulin) and 4806 s (21% sugar, without inulin)- 5313 s (18%
sugar supplemented with 2% inulin).
Correlation was observed between melting of ice cream and its
hardness. The samples with the lowest melting rate had the high-
est hardness. The Pearson’s correlation coefficient calculated for
this relationship amounted to 0.976, which indicates a strong
negative correlation. The higher hardness of ice cream the lower
the melting rate. Hardness of the studied ice cream oscillated
between 0.32 N and 4.63 N (Table 3). Values obtained for the ice
 M. Góral et al. / Food Chemistry 239 (2018) 1151–1159 1155

Fig. 1. The freezing curves plotted on the basis of temperature recorded every 1 min during ice cream production.

cream with L. rhamnosus B 442 differed significantly from those
noted for the samples containing other strains. The ice cream man-
ufactured with addition of L. rhamnosus B 442, both the samples
supplemented with magnesium and the control samples, were
characterized by high values of hardness (from 2.72 N to 4.73 N).
The lowest hardness (0.32 N) was noted for the control ice cream
K2 containing L. rhamnosus 1937. Supplementation with magne-
sium had a significant effect on adhesiveness of ice cream. The
ice cream containing bacteria enriched with magnesium had
higher adhesiveness than the control samples (K1, K2, K3). The dif-
ferences were as follows: 2.31 Ns, 4.04 Ns, and 0.16 Ns, respec-
tively, for L. rhamnosus B 442, L. rhamnosus 1937, and L. lactis JBB
500.
Di Criscio et al. (2010) reported that hardness of the ice cream
produced with addition of L. rhamnosus and L. casei ranged from
4.60 N to 6.86 N. The results obtained by Tiwari et al. (2015) were
1156 M. Góral et al. / Food Chemistry 239 (2018) 1151–1159

Table 1
Chemical composition (mean ± standard deviation) of the L. rhamnosus B 442 (control K1 – without addition of magnesium), L. rhamnosus 1937 (control K2 – without addition of
magnesium), and L. lactis JBB 500 (control K3 – without addition of magnesium) with magnesium ions in 100 g of final product, after lyophilization, 48 h of storage at 30 °C.

Ice cream with strains of bacteria Fat [%] Protein [%] Ash [%] Dry matter [%] Water [%] Carbohydrates [%]

x±SD
L. rhamnosus B 442 5.19 ± 0.53a 7.49 ± 0.06bc 1.73 ± 0.01ab 41.61 ± 0.15a 58.39 ± 0.15a 27.20 ± 0.68a
L. rhamnosus B 442 (K1) 5.54 ± 0.36a 7.57 ± 0.08c 1.84 ± 0.02b 41.47 ± 0.33a 58.51 ± 0.33a 26.52 ± 0.40a
L. rhamnosus 1937 5.37 ± 0.44a 7.47 ± 0.07bc 1.78 ± 0.01ab 41.92 ± 0.33a 58.08 ± 0.33a 27.30 ± 0.62a
L. rhamnosus 1937 (K2) 5.44 ± 0.03a 7.47 ± 0.09bc 1.85 ± 0.07b 41.71 ± 0.13a 58.29 ± 0.13a 26.96 ± 0.19a
L. lactis JBB 500 5.12 ± 0.25a 7.29 ± 0.08b 1.72 ± 0.003a 41.61 ± 0.10a 58.39 ± 0.10a 27.48 ± 0.31a
L. lactis JBB 500 (K3) 5.64 ± 0.30a 6.95 ± 0.05a 1.74 ± 0.02ab 41.76 ± 0.18a 58.24 ± 0.18a 27.44 ± 0.48a
a,b,c
Means in the same column indicated by different letters were significantly different (P value < 0.05).

Table 2
Melting time, rate and resistance (mean ± standard deviation) of the L. rhamnosus B 442 (control K1 – without addition of magnesium), L. rhamnosus 1937 (control K2 – without
addition of magnesium), and L. lactis JBB 500 (control K3 – without addition of magnesium) with magnesium ions in ice cream samples, after 48 h of storage at 30 °C.

Ice cream with strains of bacteria Melting time Melting rate [ml/min] Melting resistance [ml]
First drop [min] After 5 min After 10 min After 15 min After 20 min After 25 min After 25 min

x±SD
L. rhamnosus B 442 4.0 ± 0.3b 0.09 ± 0.009a 0.38 ± 0.02b 0.42 ± 0.02b 0.60 ± 0.02b 0.87 ± 0.01b 21.8 ± 0.2b
L. rhamnosus B 442 (K1) 4.2 ± 0.2b 0.07 ± 0.008a 0.27 ± 0.02a 0.36 ± 0.02a 0.48 ± 0.05a 0.78 ± 0.01a 19.2 ± 0.2a
L. rhamnosus 1937 2.1 ± 0.07a 0.43 ± 0.05c 0.50 ± 0.0c 0.56 ± 0.02c 0.86 ± 0.02c 1.03 ± 0.02d 25.8 ± 0.6d
L. rhamnosus 1937 (K2) 1.9 ± 0.2a 0.27 ± 0.05b 0.47 ± 0.05bc 0.61 ± 0.02c 0.85 ± 0.04c 1.02 ± 0.04 cd 25.5 ± 0.7 cd
L. lactis JBB 500 2.2 ± 0.06a 0.27 ± 0.05b 0.50 ± 0.04c 0.61 ± 0.02c 0.89 ± 0.03c 1.02 ± 0.02 cd 25.5 ± 0.4 cd
L. lactis JBB 500 (K3) 2.2 ± 0.1a 0.17 ± 0.05ab 0.38 ± 0.02b 0.57 ± 0.04c 0.83 ± 0.04c 0.97 ± 0.01c 24.2 ± 0.2c
a,b,c,d
Means in the same column indicated by different letters were significantly different (P value < 0.05).

Table 3 rhamnosus 1937 and magnesium had porous structure and more
Hardness and adhesiveness (mean ± standard deviation) of the L. rhamnosus B 442 intensive colour in the center of the sample. There were no statis-
(control K1 – without addition of magnesium), L. rhamnosus 1937 (control K2 –
without addition of magnesium), and L. lactis JBB 500 (control K3 – without addition
tically significant differences in DE between the samples contain-
of magnesium) with magnesium ions in the final product, after 48 h of storage at ing the bacteria supplemented with magnesium and the
30 °C. respective control samples. The differences in the results obtained
Ice cream with strains of bacteria Hardness [N] Adhesiveness [Ns]
for the ice cream with magnesium and the control samples ranged
from 0.00 to 0.55. Addition of magnesium and application of vari-

x ± SD
ous strains for ice cream production did not have a significant
L .rhamnosus B 442 2.72 ± 0.69bc 2.95 ± 0.38ab effect on colour parameters. According to Tiwari et al. (2015) var-
L. rhamnosus B 442 (K1) 4.63 ± 1.40c 0.64 ± 0.09c
ious levels of inulin caused differences in colour of ice cream in the
L. rhamnosus 1937 0.62 ± 0.13ab 4.34 ± 1.34a
L. rhamnosus 1937 (K2) 0.32 ± 0.03a 0.30 ± 0.12c range from 3.6 to 7.
L. lactis JBB 500 0.55 ± 0.17a 1.04 ± 0.26bc
L. lactis JBB 500 (K3) 0.55 ± 0.08a 0.88 ± 0.15c
a,b,c
Means in the same column indicated by different letters were significantly dif- 3.6. Viability determination
ferent (P value < 0.05).
The results of cells viability in the medium ranged from
2.9
109 cfu/ml to 1.29
1011 cfu/ml (Fig. 2a). Significant differences
similar. They varied from 2.6 kg (ice cream without inulin) to in viability were noted among the control cultures. The highest via-
4.9 kg (ice cream with 6% addition of stabilizer). bility among all the tested samples was noted for Lactococcus lactis
Hardness is affected by many factors such as: overrun, ice crys- JBB 500 (1.29
1011 cfu/ml) treated with PEF and the lowest – for
tal size, ice phase volume, and extent of fat destabilization. Prod- the control sample K3.
ucts containing more large ice crystals are harder than these Application of PEF caused an increase in viability of bacteria
with lower number of large ice crystals. A good example can be from each of the investigated strains. The results were higher in
creamy ice cream which contains small ice crystals and has low comparison to the control samples by, respectively, 9.35
109 cfu/
hardness (Muse & Hartel, 2004). ml for L. rhamnosus B 442, 4.56
1010 cfu/ml for L. rhamnosus 1937
and 1.26
1011 cfu/ml for L. lactis JBB 500. No statistically significant
3.5. Colour of ice cream differences in this parameter were noted for bacteria from the
strains L. rhamnosus 1937 and L. lactis JBB 500 enriched with
Colour of ice cream is one of the basic attributes affecting con- magnesium.
sumer product choice. In this connection the effect of addition of Analysis of viability showed that the total number of bacteria in
different bacterial strains and magnesium ions on ice cream colour ice cream was higher than in the starter culture. It ranged from
was investigated. Table 4 presents the results of colour 2.9
109 cfu/ml to 1.29
1011 cfu/ml (Fig. 2b). The higher results were
determinations. noted for the control cultures (K1, K2, K3) which were not
The values of L⁄, a⁄, and b⁄ were in the range, respectively, supplemented with magnesium and not treated with PEF. The
92.20–92.80, 0.40–1.2, and 4.57–7.50. There were no statistically differences in viability between the control and the sample
significant differences in these parameters between surface of containing enriched bacteria were, respectively, 9.35
109 cfu/ml
the samples and their interior. The ice cream with addition of L. (L. rhamnosus B 442), 4.56
1010 cfu/ml (L. rhamnosus 1937) and
 M. Góral et al. / Food Chemistry 239 (2018) 1151–1159 1157

Table 4
Colour values (mean ± standard deviation) of the L. rhamnosus B 442 (control K1 – without addition of magnesium), L. rhamnosus 1937 (control K2 – without addition of
magnesium), and L. lactis JBB 500 (control K3 – without addition of magnesium) with magnesium ions in ice cream samples, after lyophilization, 48 h of storage at 30 °C.

Ice cream with strains of bacteria L* a* b* DE


x ± SD
Center Surface Center Surface Center Surface Center Surface
L. rhamnosus B 442 92.90 ± 0.33a 92.77 ± 0.38a 0.40 ± 0.00a 1.20 ± 0.00a 6.70 ± 0.00a 4.83 ± 0.38a 0.00a 0.35a
L. rhamnosus B 442 (K1) 92.90 ± 0.33a 92.53 ± 0.29a 0.40 ± 0.00a 1.20 ± 0.00a 6.70 ± 0.00a 5.10 ± 0.00a – –
L. rhamnosus 1937 92.53 ± 0.29a 92.20 ± 0.33a 0.40 ± 0.00a 1.20 ± 0.00a 6.97 ± 0.75a 4.57 ± 0.75a 0.55a 0.35a
L. rhamnosus 1937 (K2) 92.67 ± 0.33a 92.43 ± 0.00a 0.40 ± 0.00a 1.20 ± 0.00a 7.50 ± 0.00a 4.83 ± 0.38a – –
L. lactis JBB 500 92.80 ± 0.65a 92.77 ± 0.19a 0.40 ± 0.00a 1.20 ± 0.00a 6.43 ± 0.75a 5.37 ± 0.38a 0.53a 0.27a
L. lactis JBB 500 (K3) 92.80 ± 0.45a 92.77 ± 0.19a 0.40 ± 0.00a 1.20 ± 0.00a 6.97 ± 0.75a 5.63 ± 0.38a – –
a
Means in the same column indicated by different letters were significantly different (P value < 0.05).

Fig. 2. Influence of magnesium addition and bacterial strain on viability of the potentially probiotic bacteria: (a) In the starter cultures after 20 h of culturing. (b) In the ice
cream after 48 h of storing. Means with the same letters are not highly significantly different (P < 0.05; n = 6).

1.26
1011 cfu/ml (L. lactis JBB 500). All the differences were statisti-
cally significant.
Viability of probiotic bacteria depends on strain, technology of
production, temperature, time of storage, and product composition
(Champagne, 2009). According to the recommendation of the
International Dairy Federation the probiotic products should con-
tain at least 107 cfu/mL of lactic acid bacteria or 106 cfu/mL of bifi-
dobacteria (Champagne, Gardner, & Roy, 2005). Most often
viability of microorganisms in probiotic food ranges from 107 cfu/
g to 108 cfu/g (Champagne, 2009). According to Jayamanne and
Adams (2006), the levels of lactobacilli of 107- 109 cfu/g may be
necessary to elicit anti-diarrhoeal effects. Also the present Brazilian
1158 M. Góral et al. / Food Chemistry 239 (2018) 1151–1159
Fig. 3. The contents of calcium and magnesium in ice cream produced with addition of L. rhamnosus B 442, L. rhamnosus 1937 and L. lactis JBB 500 enriched with magnesium
with the use of PEF. K1, K2, K3 – control samples with addition of a particular bacteria strain and not supplemented with magnesium. Means with the same small or large
letters are not highly significantly different (P < 0.05; n = 12).
legislation requires for probiotic food the minimum quantity of
viable cells in the range 108 – 109 cfu via the daily dose of the pro-
duct (ANVISA, 2008).
Gniewosz et al. (2014) in their studies on the cultures of
selected strains of bacteria enriched with magnesium obtained via-
bility in the range 1.15
109 cfu/ml–2.52
109 cfu/ml. Supplementa-
tion of medium with magnesium did not reduce viability of
bacteria compared to the control cultures.
Chiquetti et al. (2016) reported that viability of Lactobacillus aci-
dophilus La-5 in ice cream amounted to 107 cfu/g, independently on
time of storing. Whereas the results obtained by Mohammadi et al.
(2011) for L. acidophilus and B. bifidum were as high as, respec-
tively, 1.5
108 cfu/ml and 2.5
108 cfu/ml. Determination was car-
ried out immediately after freezing of the ice cream previously
subjected to fermentation. After 17 weeks of storing at 29 °C via-
bility decreased by, respectively, 4
106 and 1
107 cfu/ml.
Magarinos, Selaive, Costa, Flores, and Pizarro (2007) also observed
a decrease in viability of Lactobacillus acidophilus La-5 and Bifi-
dobacterium animalis subsp. Lactis Bb-12 in the ice cream in com-
parison to the mixture. The number of microorganisms dropped
from 3.01
107 cfu/g to1.3
107 cfu/g to after freezing and storing at
25 °C for 60 days.
The results of viability determination presented in this study
are higher than those cited in the literature. It may be due to the
high participation of bacteria in milk (4.5%), selection of the strains
resistant to elevated contents of magnesium in the medium and
application of PEF. Viability of bacteria in ice cream was in agree-
ment with the requirements for probiotic food (Champagne, 2009).
4. Conclusions
The application of pulsed electric fields enhanced accumulation
of magnesium in the cells of selected bacterial strains (in compar-
ison to the control cultures K1, K2, and K3). Thoroughly selected
parameters of the process contributed also to the increase of viabil-
ity of microorganisms. According to the expectations, addition of
magnesium ions did not influence the physicochemical parameters
for most of the ice cream samples. Only adhesiveness of the exam-
ined samples was significantly higher. Both magnesium concentra-
tion in the bacterial cells and the strain of bacteria had no
significant effect on the ice cream colour. Viability of bacteria in
the ice cream was higher than in the starter cultures. The total
number of bacteria was in agreement with the requirements for
probiotic food. The results demonstrated that potentially probiotic
bacteria of strains L. rhamnosus B 442, L. rhamnosus 1937 and L. lac-
tis JBB 500 are good carriers for magnesium. Owing to this property
they can be used for production of ice cream supplemented with
magnesium in the form of easily absorbed metalloproteins.
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