Food Control 32 (2013) 99e104

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Food Control
journal homepage: www.elsevier.com/locate/foodcont

Biosorption of patulin from apple juice by caustic treated waste cider yeast
biomass
Caixia Guo, Tianli Yue*, Yahong Yuan, Zhouli Wang, Yaodong Guo, Ling Wang, Zhao Li
Northwest A&F University, College of Food Science and Engineering, No. 28 Xinong Road, Yangling 712100, China

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 10 August 2012
Received in revised form
24 October 2012
Accepted 3 November 2012

Waste cider yeast is a natural by-product generated through the production of fermentable beverages. In
this work, the biosorption of patulin (PAT) from apple juice using waste cider yeast was investigated. The
yeast cells were treated with caustic, ethanol and heats. Among the treatments, the highest PAT uptake
(58.29%) was obtained with the caustic treated waste yeast. The effects of pH and initial concentration of
PAT were assessed. The results showed that the adsorption percentage of PAT increased simultaneously
with the increase of pH and approached equilibrium at pH 4.5. The removal of PAT increased with
decreasing of toxin levels. The experimental data were analyzed using the Langmuir and Freundlich
equations. It has been observed that the adsorption equilibrium was best described by the Langmuir
model. The Langmuir constants were qmax (mg/g) 8.1766 and b (L/mg) 0.0640. In packed bed column
studies, it was found that Ca-alginate gel was a good biosorbent for PAT removal and immobilized caustic
treated yeast particles in the gel increased the biosorption capacity of the gel.
2012 Elsevier Ltd. All rights reserved.

Keywords:
Waste cider yeast
Patulin
Biosorption
Adsorption isotherms
Calcium alginate
Immobilized

1. Introduction
Patulin (PAT) is a toxin secondary metabolite produced by
several fungal species of Penicillium, Aspergillums and Byssochlamys
lu, 2005; Harrison, 1988). This mycotoxin
(Gkmen, Acar, & Sariog
can be found in a number of fruits, including apples, pears, grapes,
apricots, strawberries, blueberries and peaches, and frequently
occurs in commercial fruit juices especially apple juice (Drusch,
Kopka, & Kaeding, 2007). It causes a signicant healthy and
economic impact. Symptoms of PAT consumption include agitation,
convulsions, edema, ulceration, intestinal inammation and vomiting (Magan & Olsen, 2004). Chronic health effects of PAT include
genotoxicity, immunotoxicity and neurotoxicity in rodents, while
its effects on humans are not clear yet (Wouters & Speijers, 1996,
pp. 337e402). Therefore, FAO/WHO have established a provisional
maximum tolerable daily intake (PMTDI) for patulin of 0.4 mg/kg
body weight/d (FAO/WHO, 1995). Additionally, in 2003, the European Union established maximum permitted levels of PAT in fruit
juices at 50 mg/kg (Commission regulation, 2003).
Many traditional approaches including clarication, ltration
and chemical addition have been developed to remove PAT from
food stuffs (Dali, Deschamps, & Richard-Forget, 2010). However,

* Corresponding author. Tel./fax: 86 29 87092492.

E-mail address: yuetl305@nwsuaf.edu.cn (T. Yue).
0956-7135/$ e see front matter 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.foodcont.2012.11.009

most of these approaches are not widely available due to high cost,
chemical hazards during processing, impact on the environment, or
practical difculties involved in detoxication process (GonzlezOsnaya, Soriano, Molt, & Maes, 2007; SantAna, Rosenthal, & de
Massaguer, 2008). Recently, more and more attention was paid
on biosorbent due to its low cost. It has been reported that a wider
variety of microorganisms, including lactic acid bacteria (LAB),
Gluconobacter oxydans and Saccharomyces cerevisiae, were capable
of reducing PAT (Hatab, Yue, & Mohamad, 2012; Ricelli, Baruzzi,
Solfrizzo, Morea, & Fanizzi, 2007; Topcu, Bulat, Wishah, & Boyac,
2010; Yue, Dong, Guo, & Worobo, 2011). Among the microorganisms used, signicant biosorption of patulin has been observed by S.
cerevisiae (Yue et al., 2011). In addition, it is easy to get from
fermentation industry as a by-product, which is the source of
different functional groups such as carboxyl, amine, hydroxyl,
phosphate and sulfonate. These functional groups have been reported to be responsible for mycotoxin binding (Hatab et al., 2012;
Niderkorn, Morgavi, Pujos, Tissandier, & Boudra, 2007).
The aim of this study was to test and compare different treated
waste cider yeast (S. cerevisiae) for their capacity to absorb PAT. Two
adsorption models, the Langmuir model and the Freundlich equation were applied to the experimental data obtained for caustic
treated yeast biomass and correlations were found for these
models. In addition, calcium alginate with and without immobilized caustic treated yeast biomass were also tested for PAT removal
in a packed bed bioreactor.

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C. Guo et al. / Food Control 32 (2013) 99e104

2. Material and methods

2.4. Isotherm models

2.1. Biomass and PAT solution

The isotherms were obtained using a similar procedure as for

the biosorption experiments previously mentioned. Tests were run
for 36 h, time enough to reach the equilibrium. The biosorption
capacity of adsorbent for PAT was investigated in different initial
concentrations of PAT (10, 50, 100, 200, 300 mg/L). The biosorption
isotherms are described by the well-known adsorption isotherm
models of Langmuir and Freundlich respectively.
The Langmuir model isotherm based on monolayer adsorption
is expressed as follows (Langmuir, 1918):

Waste cider yeast slurry, generated in the production of apple

cider, was kindly provided by the Fermentation Lab at the College of
Food Science and Engineering of Northwest A&F University (Yangling, China).
Standard stock solution of PAT at concentration of 200 mg/mL
was prepared in ethyl acetate and stored at 40  C. Test solutions
was prepared by evaporative removal (40  C/15 min) of the organic
solvent from a PAT standard solution followed by dissolution of the
PAT in sterile commercial apple juice (Hengxing company, Baoji,
China) known to be free from PAT.
2.2. Physical and chemical treatments of yeast cells
Heat treated cells were prepared by mixing 10.0 g of waste yeast
with 100 mL of distilled water and heating the resultant solution in
a water bath (100  C, 1 h) and an autoclave (121  C, 15 min). Caustic
treated cells were prepared by mixing 10.0 g of waste yeast with
100 mL of 1 M NaOH and sterilizing the resultant solution at 121  C
for 15 min. Ethanol treated cells were prepared by mixing 10.0 g of
waste yeast with 100 mL of 700 g/L ethanol solution for 20 min.
After treatments, yeast cells were collected by centrifugation
(3600 g; 10min) and washed several times with distilled water to
remove excess reagent. All the treated cells were freeze-dried
at 54  C for 26 h by a vacuum freeze-dryer (MCFD5505, SIM
International Group Co. Ltd.). The dried biomass was grounded and
screened through a set of sieves to get different geometrical sizes
100e120 mesh. This produced a uniform material and the biomass
was stored in desiccators for future use.
2.3. Biosorption experiments
The adsorption experiments of PAT were investigated in apple
juice by caustic treated waste yeast. The powdered yeast (0.5 g) was
transferred into a 100 mL sterile conical ask containing 40 mL PAT
test solution. The control was prepared without the addition of
adsorbents. The control and test solutions were placed on a shakerincubator (CertomatWR, B. Braun, Melsungen, Germany) at
120 rpm, 29  C for 24 h. Then the mixture was centrifuged at 3600
g for 20 min. The concentration of PAT in supernatant apple juice
was measured respectively by HPLC.
The effect of pH on biosorption was investigated in the pH range
from 2.5 to 5.5. The pH value was adjusted by 1 M NaOH or 1 M HCl.
The effect of initial PAT concentration was conducted in the range of
10e300 mg/L. Further experiments were proceeded to investigate
the effect of contact time, during which samples were harvested at
1, 5, 10, 20, 30 and 40 h. All adsorption experiments were performed in triplicate and mean values reported.
PAT adsorption capacity (q) was determined as following
equation:


Co  Cf V=m

where q (mg/g) is the amount of PAT adsorbed on the per-unit

weight of adsorbent in adsorbing process; Co and Cf (mg/L) are the
initial and nal PAT concentrations; V (L) is the volume of reaction
solution and m is the weight of the adsorbent.
The removal ratio of PAT adsorption from apple juice is calculated as follows:

Removal efficiency% Co  Ct =Co  100

Ce
Ce
1


qe
qm bqm
where qe (mg/g) is the amount of PAT adsorbed on the per-unit
weight of adsorbent in adsorbing equilibrium; Ce (mg/L) is the
equilibrium concentration of PAT; qm (mg/g) is the monolayer biosorption capacity of the solution and b (L/mg) is the Langmuir
adsorption equilibrium constant relating the free energy and
afnity of adsorption.
Another essential factor of the Langmuir isotherm is RL, which
can be calculated according to the following equation:

RL

1
1 bCo

Where Co (mg/L) is the highest PAT concentration.

The Freundlich isotherm based on sorption on a heterogeneous
surface is expressed as follows (Freundlich, 1906):

1
lnqe lnKF lnCe
n
where KF is a constant relating the biosorption capacity and n is an
empirical parameter relating the biosorption intensity, which varies with the heterogeneity of the materials.

2.5. Biosorbent immobilization

Sodium alginate (2 g) was dissolved in hot distilled water
(60 mL) with constant stirring to avoid lumps formation. On cooling
to room temperature, 4.0 g dried waste yeast homogenized in
distilled water (25 mL) was added under stirring condition to form
a uniform mixture and volume was made to 100 mL. This mixture
was added dropwise to 1000 mL of 1% CaCl2 through a nozzle. The
gel beads (diameter 3e4 mm) were kept overnight at 4  C in CaCl2
for completion of gelation process. The beads were repeatedly
washed with distilled water and stored at 4  C in distilled water
prior to use as the biosorbent. Blank alginate beads (2% w/v)
without biosorbent were also prepared.

2.6. Column studies

Continuous biosorption experiments were carried out using
jacketed pyrex column reactor packed with Ca-alginate beads. The
inner diameter and height of column are 1.1 cm and 20 cm,
respectively. Apple juice containing 200 mg/L of PAT was pumped
upward with a peristaltic pump through the column packed with
Ca-alginate beads. The ow rate of the PAT solution was 2 mL/min.
The samples of PAT solutions from the down-stream of column
were collected at different intervals of volume passed and were
analyzed until equilibrium was reached in the column.

C. Guo et al. / Food Control 32 (2013) 99e104

2.7. Sample extraction and PAT determination

80

The method of AOAC ofcial method (MacDonald, Long, Gilbert,

& Felgueiras, 2000) for the detection and quantication of PAT in
clear and cloudy apple juices was used for the extraction of PAT. In
this method, test apple juice (10 mL) was extracted three times
with 20 mL of ethyl acetate, cleaned up by extraction with 4 mL of
a 1.5% (w/v) sodium bicarbonate solution. The ethyl acetate extract
was passed over a bed of anhydrous sodium sulfate (15 g) and
evaporated to dryness. Then PAT was redissolved in 1 mL of
deionized water, adjusted to pH 4.0 with acetic acid. Highperformance liquid chromatography (HPLC) analysis was performed immediately after ltering all samples through a 0.22 mm
membrane.
PAT in juice samples and standards were determined by HPLC
system (Shimadzu LC-20AD pump, CTO-20A column oven, and
SPD-M20A detector), using an Alltima reversed-phase column C18
(250  4.6 mm I. D., 5 mm particles). A 20 mL sample was injected,
and deionized watereacetonitrile (10:90, v/v) was used as isocratic
mobile phase with a ow rate of 1 mL/min at 30  C. The detection
wavelength was set at 276 nm.

70

101

% PAT adsorbed

60
50
40
30
20
10
0
2.5

3.0

3.5

4.0

4.5

5.0

5.5

pH values
Fig. 2. Effect of pH on biosorption of PAT by caustic treated waste yeast. Initial PAT
concentration in apple juice was 100 mg/L.

2.8. Statistical analysis

All experiments were performed in triplicate, and the data are
presented as means  standard deviation (SD). Data was subjected
to One-way analysis of variance (ANOVA) by using the Statistical
Analysis System (SAS). Statistical signicance was considered to
exist when p < 0.05.
3. Results and discussion
3.1. Effects of pretreatments of waste cider yeast on biosorption
To investigate the effects of different pretreatments on PAT
binding, waste cider yeast was treated with caustic, ethanol and
heats. As shown in Fig. 1, the highest PAT removal percentage
(58.29%) was obtained by caustic treated waste yeast and 44.41% of
PAT binding was obtained with ethanol treated yeast cells. Similar
PAT binding values were obtained by different heat treatments. The

80

amino and carboxyl residues of proteins and peptides in the yeast

cell walls were probably exposed by the caustic treatment so
enhancing PAT-binding to the cells. Thus, the permeability within
the internal structure of waste yeast improved, and more organic
functional groups on waste yeast exposed. According to the reports
of Niderkorn et al. (2007) and Hatab et al. (2012), the amino and
carboxyl groups in microorganisms could be mainly available for
characteristic coordination bonding with mycotoxin. Therefore, the
caustic treated waste yeast with more exposed amino and carboxyl
groups would have a great advantage in adsorbing PAT.

3.2. Effect of pH on biosorption

The pH value of the solution is an important parameter that may
affect binding by changing both the form and the binding sites on
the biomass. The pH value was investigated ranging from 2.5 to 5.5,
as PAT is very stable in aqueous acidic media in the range of pH 2.5e
5.5 (Drusch et al., 2007). The results showed that the biosorption
capacity of PAT increased simultaneously with the increase of pH in

70
10ug/L
50ug/L
100ug/L
200ug/L
300ug/L

100

50
80

40

% PAT adsorbed

% PAT adsorbed

60

30
20

60

40

20

10
0

10

20

30

40

time (h)
Fig. 1. Effects of different pretreatments on the PAT removal of waste cider yeast (1.
Autoclaved yeast; 2. Heat treated yeast; 3. Caustic treated yeast; 4. Ethanol treated
yeast). Initial PAT concentration in apple juice was 100 mg/L.

Fig. 3. Biosorption of PAT by caustic treated waste yeast at different initial PAT
concentrations.

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C. Guo et al. / Food Control 32 (2013) 99e104

Table 1
Parameters for the application of Langmuir and Freundlich models to the biosorption of PAT on caustic treated waste yeast using linear regression.

10

PAT adsorbed (ug/g adsorbent )

Langmuir model

8
7

Freundlich model

b (L/mg)

qm (mg/g)

R2

RL

KF (L/g)

R2

0.0640

8.1766

0.9837

0.0495

2.4795

1.0511

0.9765

6
5

3.3. Effect of initial PAT concentration on biosorption

Biosorption experiments with caustic treated waste yeast were

conducted for apple juice containing 10e300 mg/L PAT at different
time (Fig. 3). The results showed that the binding amount of PAT
increased with contact time, indicating that equilibrium is reached
at about 30 h which is supported by the data in Fig. 3.
The PAT concentration signicantly affected the amount of the
toxin bound. At higher concentrations of PAT the active sites of the
caustic-treated yeast cells would become saturated so optimizing
(or maximizing) the adsorption process. The amount of PAT
removed increased with the initial concentration of toxin. This is in
agreement with that reported by Fuchs et al. (2008) and Mateo
et al. (2010) where the removal of mycotoxin was concentration
dependent, and the removal amount of PAT increased as toxin
levels.

3
2
1
0
0

50

100

150

200

250

Equilibrium concentration(Ce), ug/L

Fig. 4. Adsorption capacities of PAT onto caustic treated waste yeast (per gram) at
different equilibrium concentration (Ce).

solution and approached equilibrium at pH 4.5 (Fig. 2). Several

researches have also investigated the effect of pH on biosorption of
mycotoxin by using different microbial biomass and found similar
results with this study. Ringot et al. (2005) found that optimal
removal of PAT and ochratoxin A by lactic acid bacteria was at pH
5.0. It was explained that the low-pH condition might be responsible for the resistance of PAT adsorption. Zinedine, Faid, and
Benlemlih (2005) showed that more aatoxin B1 removal takes
place at pH 5.5 (than pH 3 or pH 4.5). However, Topcu et al. (2010)
noted that the highest removal of PAT by nonviable cells of
Enterococcus strains occurred at pH below 5, this may be due to the
effect of hydrogen bond interactions on removal of PAT. Haskard,
Binnion, and Ahokas (2000) reported that pH in the range from
2.5 to 8.5 did not affected the binding of AFB1 using Lactobacillus
rhamnosus GG, which may indicate that a cation exchange mechanism was not operating. In general, the effect of pH probably
results from competition for negatively charged binding sites
between toxin and protons (H).

3.4. Adsorption isotherm of PAT

As shown in Fig. 4, the adsorption capacity increased rapidly
with the initial increase in concentration and then slowed as it
approached a maximum. In the design of sorption systems, the
equilibrium sorption isotherms are very important from fundamental point of view. The equation parameters and the underlying
thermodynamic assumptions of these equilibrium models often
provide some insight into both the sorption mechanism and the
surface properties and afnity of the sorbent (Ho, Porter, & McKay,
2002). In order to investigate the sorption isotherm, Langmuir
model and Freundlich equilibrium model were applied.
The experimental isotherm data were tted to Langmuir model
and Freundlich isotherm for nonlinear regression analysis. The t
plots were presented in Fig. 5 and the correlation parameters for
each model were listed in Table 1. The coefcient b in Langmuir

30

2.0
25

1.5
20

In qe

Ce/qe

1.0
15

0.5
10

0.0

-0.5

0
0

50

100

150

Ce

200

-1

In Ce

Fig. 5. Adsorption isotherms of PAT on the caustic treated waste yeast. (A) Langmuir plots for PAT adsorption. (B) Freundlich plots for PAT adsorption.

C. Guo et al. / Food Control 32 (2013) 99e104

103

Ca - alginate

250

Effluent PAT concentration (ug/L)

Ca - alginate + biosorbent
200

150

100

50

0
0

200

400

600

800

1000

1200

1400

1600

Volume (mL)
Fig. 6. Efuent PAT concentration after biosorption with Ca-alginate beads and Ca-alginate beads immobilized with caustic treated waste yeast in a packed bed bioreactor (initial
PAT concentration: 200 mg/L, ow rate: 2 mL/min, room temperature).

equation is a measure of the stability of the complex formed

between PAT and waste biomass. The small b values (0.0640) obtained in this research implied strong binding of PAT to caustic
treated yeast biomass. Maximum PAT uptake capacities of caustic
treated yeast biomass (qmax) were found as 8.1766 mg/g. Moreover,
as reported by Stephen, Chien, Ho, Yang, and Chen (2006) the
Langmuir parameter RL indicates the shape of the isotherm and
nature of biosorption process (RL > 1: unfavorable; RL 1: linear;
0 < RL < 1: favorable; RL 0: irreversible). The RL value was 0.0495,
indicating that biosorption of PAT by caustic treated waste yeast
was favorable. In the case of Freundlich model, the adsorption
features are dened by both KF (mg) and n value, where KF represents the adsorption coefcient and n is related to the effect of
concentration of PAT. KF value obtained in this study was 1.0511 and
n value was 2.4795, respectively. Besides, with the n value between
1 and 10, the biosorption by caustic treated waste yeast was
favorable under studied conditions.
As listed in Table 1, the correlation coefcient of biosorption data
simulated by Langmuir model was 0.9837, a slight higher than
0.9765 by Freundlich one. This implies that the Langmuir model
may be relatively more suitable to predict the adsorption of PAT
onto caustic treated waste yeast. The agreement of the experimental data with the Langmuir model implied that the bisorption
of PAT onto caustic treated waste yeast was considered as monolayer adsorption. Its suggested that waste yeast cell wall played
a very important role on adsorption. This result was consistent with
a number of former researches focusing on the adsorption of
mycotoxin (El-Nezami et al., 2004; Hernandez-Mendoza, Guzmande-Pea, & Garcia, 2009; Piotrowska, 2011). However, Moss and
Long (2002) found that PAT was converted to E-ascladiol and Zascladiol during an alcoholic fermentation of apple juice, not bind
to yeast cells or apple juice sediment.

and without caustic treated yeast biomass were used for biosorption in the same experimental condition. As can be seen from
Fig. 6, the results showed that PAT removal was fast and highly
effective during the initial phase and PAT removal decreased with
the increase of excurrent volume, as a consequence of the
progressive saturation of the binding sites. At the initial phase of
bisorption, Ca-alginate gel with immobilized caustic treated yeast
removed 100% of PAT, and Ca-alginate gel without caustic treated
yeast biomass removed 71.42% of PAT. After collecting 1200 mL of
efuent from the column, the column came to saturation. It can be
concluded that Ca-alginate gel itself is a good biosorbent of PAT and
immobilizing caustic treated yeast particles in the gel increases the
biosorption capacity of the gel.

4. Conclusion
In this study, caustic treated waste cider yeast (S. cerevisiae) has
been successfully used as a biosorbing agent for removal of PAT
from apple juice. The Langmuir adsorption model and Freundlich
equation were used for the mathematical description of the biosorption of PAT onto caustic treated yeast biomass. It was seen that
the adsorption equilibrium data conformed well by the Langmuir
model. Ca-alginate gels with and without biosorbent particles were
used as an immobilization matrix and it was found that Ca-alginate
gel was a good biosorbent for PAT biosorption. Immobilizing caustic
treated yeast biomass in Ca-alginate increased biosorption capacity.
It seems that the use of readily available waste cider yeast biomass
from fermentation industries offers an alternative for the removal
of PAT from apple juice.

Acknowledgments
3.5. Column studies using calcium alginate immobilized biosorbent
For the successful application of biosorption, biomass needs to
be immobilized to increase its mechanical strength, density, reusability and resistance to mechanical environments. In this study,
Ca-alginate gel was chosen for the immobilization experiments as it
is cheaply, abundantly available and nontoxic. Ca-alginate gel with

This study has been supported by China State 12th Five-Year

Plan scientic and technological support scheme (2012
BAK17B06, 2012BAD31B01); National Natural Science Foundation
of China (31071550, 31171721); 948 project of the Ministry of
Agriculture of China (2011-G8-3); Shaanxi SheFa research projects
(2011K17-05-01).

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C. Guo et al. / Food Control 32 (2013) 99e104

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