mahato2021

Toxicon 198 (2021) 12–23
Contents lists available at ScienceDirect
Toxicon
journal homepage: www.elsevier.com/locate/toxicon
Review
Patulin in food: A mycotoxin concern for human health and its

management strategies
Dipendra Kumar Mahato a, Madhu Kamle b, Bharti Sharma c, Shikha Pandhi c, Sheetal Devi d,
Kajal Dhawan e, Raman Selvakumar f, Diwakar Mishra g, Arvind Kumar c, Shalini Arora h,
Namita Ashish Singh i, Pradeep Kumar b, *
a
CASS Food Research Centre, School of Exercise and Nutrition Sciences, Deakin University, Burwood, VIC, 3125, Australia
b
Applied Microbiology Lab., Department of Forestry, North Eastern Regional Institute of Science and Technology, Nirjuli, 791109, Arunachal Pradesh, India
c
Department of Dairy Science and Food Technology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, 221005, Uttar Pradesh, India
d
National Institute of Food Technology Entrepreneurship and Management (NIFTEM), Sonipat, Haryana, 131028, India
e
Department of Food Technology and Nutrition, School of Agriculture Lovely Professional University, Phagwara, 144411, Punjab, India
f
ICAR-Indian Agricultural Research Institute, Pusa Campus, New Delhi, 110012, India
g
Department of Dairy Technology, Birsa Agricultural University, Dumka, 814145, Jharkhand, India
h
Department of Dairy Technology, College of Dairy Science and Technology, Lala Lajpat Rai University of Veterinary and Animal Sciences, Hisar, 125004, Haryana,
India
i
Department of Microbiology, Mohanlal Sukhadia University, Udaipur, 313001, Rajasthan, India
A R T I C L E I N F O A B S T R A C T
Handling Editor: Raymond Norton The mycotoxin patulin is primarily produced as a secondary metabolite by numerous fungal species and pre
dominantly by Aspergillus, Byssochlamys, and Penicillium species. It is generally associated with fungal infected
Keywords: food materials. Penicillium expansum is considered the only fungal species liable for patulin contamination in
Patulin pome fruits, especially in apples and apple-based products. This toxin in food poses serious health concerns and
Food contamination
economic threat, which has aroused the need to adopt effective detection and mitigation strategies. Under
Chemistry
standing its origin sources and biosynthetic mechanism stands essential for efficiently designing a management
Health issues
Management strategies strategy against this fungal contamination. This review aims to present an updated outline of the sources of
patulin occurrence in different foods and their biosynthetic mechanisms. It further provides information
regarding the detrimental effects of patulin on human and agriculture as well as its effective detection, man
agement, and control strategies.
1. Introduction drying, handling, packaging, storage, and distribution facilities are some
of the significant contributors to mycotoxins intensification (Bhat et al.,
Recently food safety is a thriving concern worldwide due to the 2010). Patulin (PAT), a mycotoxin, is a polyketide lactone (4-hydrox
alarming rise of chemical and biological contaminants in the environ y-4H-furo [3,2-c]pyran-2(6H)-one) produced primarily by Penicillium,
ment. Mycotoxins are one such concern and it represents a class of Aspergillus and Byssochlamys species. PAT was found to grow signifi
highly toxic secondary metabolites produced by a certain group of fungi cantly on fruits like apples, pears, and grapes (Joshi et al., 2013). The
(Joshi et al., 2013). These are less volatile, low molecular weight com genus Penicillium with the species Penicillium expansum is the significant
pounds with a profound toxic effect and if ingested it can pose severe PAT producer associated with a severe health concern and economic
health implications in humans (Cunha et al., 2014; Kumar et al., 2017). threat. The mycotoxin is accountable for a common post-harvest disease
The contamination of agricultural and food commodities by filamentous like blue mould rot. Apple amongst the fruit is one of the most suscep
fungal toxins pose serious health concerns. Inadequate harvesting, tible food commodities to PAT mycotoxin.
* Corresponding author.
E-mail addresses: [email protected] (D.K. Mahato), [email protected] (M. Kamle), [email protected] (B. Sharma), shikhapandhi94@
gmail.com (S. Pandhi), [email protected] (S. Devi), [email protected] (K. Dhawan), [email protected] (R. Selvakumar),
[email protected] (D. Mishra), [email protected] (A. Kumar), [email protected] (S. Arora), [email protected] (N.A. Singh),
[email protected] (P. Kumar).
https://doi.org/10.1016/j.toxicon.2021.04.027
Received 25 January 2021; Received in revised form 30 March 2021; Accepted 27 April 2021
Available online 29 April 2021
0041-0101/© 2021 Elsevier Ltd. All rights reserved.
D.K. Mahato et al. Toxicon 198 (2021) 12–23
In many filamentous fungi, environmental factors such as pH, water 3. Chemistry and biosynthesis of patulin
activity, temperature, and nutrient composition may regulate the PAT
biosynthesis mechanism (Vidal et al., 2019). Penicillium expansum is The biosynthetic mechanism for mycotoxin production can be
most prevalent in soil and air with good adaptability to environmental modulated equally by pathway-specific transcription factors and uni
conditions. However, the growth occurs at 25 ◦ C optimal temperature versal regulatory factors (Li et al., 2019a). PAT is a polyketide metab
and 90% relative humidity. Essentially, it grows on the rotting vegeta olite similar to other major mycotoxins like zearalenone, aflatoxins,
tive matter. It can further survive in a wide pH range, and pH from 4.0 to fumonisins and ochratoxins (Kamle et al., 2019; Kumar et al., 2017,
5.0 promotes its spore germination, while the extreme pH such as 2.0 or 2020; Mahato et al., 2019). The organic compound PAT is categorized as
8.0 exerts an inhibitory effect on spore germination (Li et al., 2020). PAT a heat-resistant lactone that cannot be denatured by heat. PAT has a
is soluble in water and various solvents like ethanol, methanol, acetone, molar mass of 154.12 g/mol and a melting point of 110 ◦ C. The
ethyl-acetate etc. It is moderately soluble in sulphuric acid and benzene biosynthetic pathway of PAT production consists of ten steps (Saleh and
and stable in acidic conditions but can be degraded on cooking with Goktepe, 2019). The mechanism of PAT comprised of a sequence of
sulphuric acid (Pleadin et al., 2019). In comparison to raw food, the condensation and redox reactions. PAT is a polymer of acetate and short
presence of PAT in processed food products is rare. Processes such as carboxylates that requires the participation of a multifunctional enzyme
clarification, filtration and enzymatic treatment during the processing of known as polyketide synthases (PKS) (Huffman et al., 2010). The role of
juices and fermentation during winemaking significantly reduce PAT PKS is not solely for the biosynthesis of mycotoxin. Some modification
content. Washing, sorting and grading, and removing spoiled portions enzymes perform an obligatory catalyzing function in various subse
from the fruits can also decrease PAT content (Cunha et al., 2014). quent reactions involved in the biosynthesis route. The genes encoding
The International Agency for Research on Cancer (IARC) has cate these essential enzymes are presented as a cluster on a single chromo
gorized PAT under Group 3 category, which is considered not carcino some as in most of mycotoxin biosynthesis pathway (Snini et al., 2014).
genic. European Commission (EC) and FAO/WHO Joint Expert The biosynthetic mechanism of PAT is initiated by acetyl coenzyme
Committee on Food Additives and Contaminants (JECFA) have estab A (CoA) and malonyl CoA. The enzyme responsible for the first step is 6-
lished the maximum permitted limits and suggested a provisional MSAS. This enzyme is a polyketide synthase (PKS) that brings about the
maximum tolerable daily intake (PMTDI) of 0.4 mg/kg body weight/day conversion of CoA and malonyl CoA to 6-methylsalicylic acid. The
for PAT (Vidal et al., 2019). The maximum critical limits for mycotoxin synthesis mechanism is commenced with an acetyl coenzyme A (CoA)
was set by the European Union for certain fruit and fruit-based products. and 3 units of malonyl CoA, forming a tetraketide. They both condensed
For infant consumption, the limit were 50, 25 and 10 μg of PAT/kg for to give 6-methylsalicylic acid (6-MSA) using 6-methylsalicylic acid
fruit juices, solid apple products, and apple-based products, respectively synthetase (6-MSA synthetase) enzyme. The inhibition of this enzyme
(Tannous et al., 2014). Further, numerous studies have revealed that can serve as a limiting step for retarding PAT production. This enzyme’s
acute PAT intoxication results in ulceration, agitation, convulsions, inactivation is a highly selective step of inhibition. In some species of
oedema, vomiting, and DNA damage in the brain, kidney and liver. P. urticae, this enzyme is found stable at the same reaction conditions
However, the effect of chronic intoxication in rodents was immunotoxic, that lead to the inactivation of 6-MSA synthetase. The next step involves
neurotoxic, genotoxic and teratogenic (Vidal et al., 2019). the transformation of 6-MSA into m-cresol through the activity of 6-
Keeping in view, this review tends to provide insights on various MSA decarboxylase.
sources, biosynthesis mechanism and genes responsible for patulin Further, the m-cresol is then transformed to m-hydroxybenzyl
production in food. It also outlines its effect on agriculture products and alcohol via m-cresol 2-hydoxylase. The next step eventually leads to
human health along with its mechanism of toxicity in brief. In addition, gentisaldehyde by two different mechanisms giving either intermediary
it discusses the degradation kinetics of patulin, its detection techniques compounds such as gentisyl alcohol or m-hydroxybenzaldehyde. Some
and management strategies concisely. studies have indicated that both the compounds can be formed, with
hydroxybenzaldehyde being more favourable. The enzymes responsible
2. The primary source of patulin for carrying out these two steps require oxygen and NADPH. As the
gentisaldehyde has been produced, it is then transformed to iso
PAT is a polyketide lactone produced by various fungal species, epoxydon, phyllostine, neopatulin, E-ascladiol and it finally produces
amongst which Penicillium expansum is known as the leading producer. PAT. The transformation from isoepoxydon to phyllostine is attained via
Fruits and vegetables are the most common substrate for the toxin the NADP-dependent isoepoxydon dehydrogenase enzyme. The change
occurrence. It is primarily predominant in apple and apple-based of neopatulin to E-ascladiol is brought via reduction by NADPH. The
products and occasionally in other fruits such as pears, grapes, or product eascladiol formed is then either oxidized to PAT or non-
anges and their derivatives (Saleh and Goktepe, 2019; Vidal et al., enzymatically converted to its isomer Z-ascladiol (Joshi et al., 2013).
2019). The use of overripe fruits serves as the main causative agent of
the fungal contamination and it is observed as brown rot in peaches, 4. Genes responsible for patulin production
banana, apricots, and pineapples. The toxin has not been limited to
spoiled fruits and vegetables but also been detected in visually appealing The biosynthesis pathway for the production of mycotoxins is
fruits. In pome and stone fruits, Penicillium expansum is abundantly enzymatic cascades, wherein the enzymes are triggered successively
found and resulted in blue mould rot in such fruits. The characteristic with the metabolism of newly synthesized product. The association of
wound parasitic fungal mycotoxin, P. expansum, enter the fruits genes form clusters that encode an enzyme which catalyzes various
damaged surface that might be caused due to insects and birds infesta biosynthesis pathway steps (Barad et al., 2016; Li et al., 2019). The PAT
tion, hostile weather conditions or injuries occurred during mechanical biosynthesis pathway entails ten enzymes catalyzed steps with the
harvesting and transportation (Li et al., 2020). Apart from fruits and involvement of a 15 gene cluster. 11 genes are responsible for
fruit-based products, the mycotoxin can also be isolated from cereal and enzyme-catalyzed PAT producing steps, excluding the genes encoding
cereal products such as barley, wheat, bread and cheddar cheese transcription and regulatory factors. The genes PatK, PatH, PatI and
(Babaali et al., 2017). PAT has also been found in seafood such as PatN have been characterized for encoding enzymes 6-methylsalicylic
shellfish wherein the two strains of Penicillium antarcticum have been synthase, m-cresol hydroxylase, m-hydroxybenzyl alcohol hydroxylase
identified from patulin potato dextrose and malt extract agar. Hence, it and isoepoxydon dehydrogenase, respectively (Snini et al., 2014). The
has been recommended that the edible shellfish must be assessed for the biosynthesis cluster of PAT has been initially characterized in Aspergillus
presence of PAT before processing (Wright, 2015). clavatus.
Conversely, the gene cluster was lately recognized in P. expansum,
13
the PAT key producer in apple. PAT gene cluster in P. expansum consists Table 1
of 15 genes assembled in a 41-kb DNA region (Tannous et al., 2014). The occurrence of patulin in foods around the world.
Among these 15 genes, one gene encodes for a putative transcription Food matrix Country Range (μg/ Detection References
factor (PatL), three transporter genes (PatM, PatC, PatA) and genes PatB, kg) technique
PatD, PatE that encodes biosynthetic enzyme GMC oxidoreductase, Apple Brazil 150–267 HPLC-DAD Sylos (1999)
which catalysis the conversion of ascladiol to PAT in the last step. The Pakistan 396 HPLC-UV Hussain et al.
gene PatG encodes a putative decarboxylase that is involved in the (2020)
transformation of 6-methylsalicylic acid to m-cresol. Other genes PatH USA 8.8–417.6 HPLC Harris et al. (2009)
Canada 565 LC Abramson et al.
and PatI encode cytochromes P450 that causes hydroxylation of (2009)
m-cresol and m-hydroxybenzyl alcohol to m-hydroxybenzyl alcohol Argentina 19,622 HPLC Oteiza et al. (2017)
gentisyl alcohol, respectively. The PatJ gene encodes a putative dioxy Portugal 1–70.6 GC–MS Cunha et al. (2014)
genase while the PatK gene encodes a 6-methylsalicylic acid synthase Apple cider South 5–10 HPLC Leggott and
Africa Shephard (2001)
(6-MSAS) belonging to the type I polyketide synthase (PKS) group. On
Belgium 2.8–6.1 HPLC Tangni et al.
the other hand, PatN and PatO genes have been recently recognized, (2003)
with no apparent function shown by the last gene PatF (Tannous et al., Georgia 244–3993 TLC Wheeler et al.
2014). (1987)
Apple jam Pakistan 6 HPLC-UV Hussain et al.
(2020)
5. Occurrence in food Apple juice Spain 10–170 LC Prieta et al. (1994)
Iran 15–285.5 TLC Cheraghali et al.
Patulin is one of the most critical mycotoxins produced by several (2005)
fungal species among all toxic metabolites. In the 1940s, to detect new Saudi 152 HPLC-FD Al-Hazmi (2010)
Arabia
fungal molecules with antibiotic properties, Penicillium griseofulvum and
Italy 5.8–56.4 HPLC Ritieni (2003)
Penicillium expansum were first isolated following Flemings’ discovery of Iran 6–106 HPLC-UV Jalali et al. (2010)
penicillin (Sanzani et al., 2012). PAT occurrence in foods, especially South 5–45 HPLC Leggott and
fruits and vegetables (Table 1), is a significant concern for the world’s Africa Shephard (2001)
food industry. Belgium 2.5–38.8 HPLC Tangni et al.
(2003)
Turkey 2.6–36.8 HPLD-DAD Moukas et al.
6. Effects on agricultural food & GS-MSD (2008)
South 0–1650 HPLC-UV Shephard et al.
Although PAT affects various food products, the common and prev Africa (2010)
South 2.8–8.9 HPLC Cho et al. (2010)
alent toxic effect was observed in apples as studied by various re
Korea
searchers. This might be attributed to the fruit’s physicochemical Pakistan 18 HPLC-UV Hussain et al.
characteristics such as its water activity and pH, which supports the (2020)
growth of P. expansum (Tannous et al., 2016; Zong et al., 2015). Further, Brazil 3–7 LC Iha and Sabino
the crops genetic nature, which determines the wound healing ability (2008)
Spain 2.5–6 LC Marín et al. (2011)
and its susceptibility to infection, also affects PAT production. In a study Tunisia 0–167 HPLC Zaied et al. (2013)
by Janisiewicz et al. (2008), the apple variety Malus sieversii had shown Spain 3–36.5 HPLC Piqué et al. (2013)
resistance towards P. expansum infection. Another incidence of disease Portugal 1.9–45.5 GC-MS Cunha et al. (2014)
was related to the firmness of the fruit wherein the under and over-ripe Malaysia 26.9 HPLC Lee et al. (2014)
Serbia 0.4–65.4 HPLC-UV Torović et al.
fruit had shown a decrease in firmness and an increase in the chance of
(2018)
infection (Vilanova et al., 2014; Wei et al., 2010). Tunisia 4–122.3 HPLC-UV Zouaoui et al.
Awuchi et al. (2019) evaluated the impact of PAT on the cereals (2015)
physical characteristics. The PAT concentration in grains exists in the Iran 50–285 TLC Cheraghali et al.
range recommended by the WHO and the European Union. The results (2005)
Brazil 17 HPLC-DAD Sylos (1999)
showed no difference in the physical aspects of grains. However, PAT Serbia 65.4 HPLC Torović et al.
toxic effect on health demanded its permissible limit, which the regu (2018)
latory authorities have set up that further depends on the type of product Pakistan 0–69.4 HPLC-UV Iqbal et al. (2018)
and geographical location. The European Union has set the maximum Spain 15.0 HPLC Cano-Sancho et al.
(2009)
permitted limit for apple juice and cider to be 50 μg/kg. However, half of
Turkey 19.1–732.8 HPLC-UV Yurdun et al.
this concentration, that is, 25 μg/kg is established for solid apple & TLC (2001)
products and up to 10 μg/kg for the products intended to be consumed Qatar 5.8–82.2 HPLC Hammami et al.
by infants and young children (EC, 2003). In single strength recon (2017)
stituted juices, the maximum concentration is set at 50 g/L by the Codex Iran 100–1000 HPLC-UV Forouzan and
Madadlou (2014)
Alimentarius Commission and US Food and Drug Administration Sweden 50 HPLC Thuvander et al.
(Codex, 2003; FDA, 2001). (2001)
Japan 5.8–56.4 LC-MS Ito et al. (2004)
7. Mechanism of toxicity and health effects of patulin Italy 53.4 HPLC Piemontese et al.
(2005)
Spain 1.5–50.9 GC-MS González-Osnaya
Patulin isolation was carried in 1943, and further, it was used as an et al. (2007)
effective anti-microbial agent against gram-positive and gram-negative Italy 44.89 HPLC-DAD Spadaro et al.
bacteria (Korzybski et al., 2013; Raistrick, 1943). However, after iden (2007)
tifying its toxic effect, it was categorized under Group 3 by the Inter Poland 5–30 HPLC-UV Szymczyk et al.
(2004)
national Agency for Research on Cancer (IARC, 2018). Though there was Turkey 3.2–106.9 HPLC Demirci et al.
insufficient evidence to claim PAT carcinogenic nature, other proven (2003)
harmful impacts were found on health, including immunotoxicity, (continued on next page)
hepatotoxicity, gastrointestinal, and neurological problems (Pal et al.,
14
Table 1 (continued ) Table 1 (continued )

Food matrix Country Range (μg/ Detection References Food matrix Country Range (μg/ Detection References
kg) technique kg) technique
India 205–1839 HPLC-UV Saxena et al. Fruits and by- UHPL-MS/ Vaclavikova et al.
(2008) products MS (2015)
Portugal 1.2–42 HPLC-UV Barreira et al. Grape Argentina 13,808 HPLC Oteiza et al. (2017)
(2010) Grape juice South 5.2–14.5 HPLC Cho et al. (2010)
Apple juice for Spain 0–29.6 CE Murillo-Arbizu Korea
infant et al. (2010) Germany 4.9–5.2 GC-MS Rychlik (2005)
Apple juice China 1.2–3.6 HPLC Wu et al. (2008) Pakistan 39 HPLC-UV Hussain et al.
concentrate Iran 50–148 TLC Cheraghali et al. (2020)
(2005) Grapes must Germany 3.5–80 HPLC-UV Majerus et al.
Iran 8–40 HPLC-DAD Farhadi and Maleki (2008)
(2011) Ginger Ivory 15 HPLC Ake et al. (2001)
Pakistan 328 HPLC-UV Hussain et al. Coast
(2020) Hazelnuts Turkey 16.6–92.4 HPLC Ekinci et al. (2014)
Apple and Brazil 20.7–207.2 HPLC-UV Sargenti and Lychee juice Malaysia 13.1 HPLC Lee et al. (2014)
mixed juice Almeida (2010) Organic baby Italy 13.1–17.7 HPLC Ritieni (2003)
Apple, grape Malaysia 0.5–100 HPLC-DAD Abu-Bakar et al. food
and mango (2014) Marmalade Argentina 17–39 HPLC Funes and Resnik
juice (2009)
Apple juice and Belgium 0-10,000 HPLC-UV De Clercq et al. Pear/Pear Argentina 1749 HPLC Oteiza et al. (2017)
puree (2016a) products Italy 0.79 LC Sarubbi et al.
Apple products Italy 0.4–50 HPLC Beretta et al. (2016)
(2000) Argentina 25 HPLC Funes and Resnik
China 1.2–94.7 HPLC-UV Yuan et al. (2010) (2009)
Apple puree Italy 15.9–16.7 HPLC Ritieni (2003) Peach Turkey 4.3–93.2 HPLC Demirci et al.
Spain 7.7–28.4 GC-MS González-Osnaya (2003)
et al. (2007) Peach Argentina 24 HPLC Oteiza et al. (2017)
Spain 17.6 HPLC Cano-Sancho et al. Pineapple Pakistan 0–460.3 HPLC-UV Iqbal et al. (2018)
(2009) Pineapple juice Malaysia 33.7 HPLC Lee et al. (2014)
Argentina 22–221 HPLC Funes and Resnik Ivory 14.42 HPLC Ake et al. (2001)
(2009) Coast
Pakistan 99 HPLC-UV Hussain et al. Passion fruit Ivory 16.60 HPLC Ake et al. (2001)
(2020) juice Coast
Apricot Argentina 16 HPLC Oteiza et al. (2017) Red globe Pakistan 0–520 HPLC-UV Iqbal et al. (2018)
Baby food South 5–20 HPLC Leggott and grapes
Africa Shephard (2001) Semi-hard Italy 15–460 HPLC Pattono et al.
Italy 0.7 HPLC Piemontese et al. cheese (2013)
(2005) Strawberry Turkey 3.2–572 HPLC Demirci et al.
Spain 9.6 HPLC Cano-Sancho et al. (2003)
(2009) Poland 5–100 HPLC-DAD Sadok et al. (2018)
Portugal 5.7 HPLC-UV Barreira et al. Strawberry Czech >0.5 UHPL-MS/ Vaclavikova et al.
(2010) juice MS (2015)
Italy 4.83–23.62 LC Bonerba et al. Tomato Portugal 21.29 GC-MS Cunha et al. (2014)
(2010) Belgium 13–39 UPLC Van de Perre et al.
Bell peppers Belgium 4 UPLC Van de Perre et al. (2014)
(2014) Pakistan 0–520.5 HPLC-UV Iqbal et al. (2018)
Blackcurrant Denmark 683 HPLC/TLC Larsen et al. (1998) Tomato Italy 7.15 LC Sarubbi et al.
and cherry products (2016)
fruit juice Single strength Argentina 1750 HPLC Oteiza et al. (2017)
Black mulberry Turkey 6.8–157.4 HPLC Demirci et al. pulp
(2003) Wheat Canada 6.8–12.7 TLC Harwig et al.
Barley Canada 1.8–4.4 TLC Harwig et al. (1977)
(1977) Wheat and Spain 22,400 HPLC Lopez-Diaz and
Branded mixed India 21–70 HPLC-UV Saxena et al. barley Flannigan (1997)
juice (2008) White mulberry Turkey 32–426 HPLC Demirci et al.
Corn Canada 2.4–4.4 TLC Harwig et al. (2003)
(1977)
Clear apple Romanian 0.7–50.5 HPLC Oroian et al.
juice (2014) 2017; Vidal et al., 2019). Consequently, kidneys, immune system and
Cherry Turkey 5.6–113.3 HPLC Demirci et al. intestinal tissues were most affected (de Melo et al., 2012). Studies
(2003)
Cereal-based Portugal 0–4.5 RP-HPLC Assunção et al.
regarding the toxicity mechanism of PAT has considered being liable for
foods (2016) the damage of the oxidative pathway. It involves forming certain
Clear apple Portugal 310 HPLC Gaspar and Lucena sulfhydryl-containing compounds, leading to an increase in the con
Juice (2009) centration of reactive oxygen species (ROS) inside the cell. ROS reacts
Conventional Belgium 10.2 HPLC Baert et al. (2006)
with bioactive compounds and causes systemic oxidative damage that
apple juice Italy 1.2–4.5 HPLC Versari et al.
(2007) ultimately results in various cellular deformities and diseases (Finkel
Concentrated Argentina 13,808/ HPLC Oteiza et al. (2017) and Holbrook, 2000; Fliege and Metzler, 2000; Puel et al., 2010).
juice/pulp 708 Various researches have indicated the occurrence of apoptosis
Dried longans China 194.3/ HPLC-UV Ji et al. (2017) because of oxidative stress. Zhong et al. (2017) showed that mitochon
(seedless)/ 276.9
figs
drial dysfunction due to ROS and decrease in enzymes and compounds
Dried apple South 10–50 HPLC-DAD Katerere et al. like catalase, superoxide dismutase and glutathione results in apoptosis
rings Africa (2008) in HEK293 cells. Similar results have been found due to oxidative stress
Czech 1.3–415.2 by PAT toxicity Zhang et al. (2015). Studies suggested that PAT induced
15
apoptosis involves Endoplasmic Reticulum (ER) stress and activation of Barrett, 2005).
the mitochondrial pathway for apoptosis (Hetz, 2012). A disturbance In another study by Diao et al. (2019), apple juice was treated with
causes ER stress during the homeostasis of ER, which activates the ozone and evaluated in reducing PAT concentration. The fourfold
mitochondrial pathway during extreme conditions. Besides, PAT acti decrease in PAT concentration was observed when apple juice was
vates proteins such as GRP78 (a stress marker), CHOP (a transcription exposed to the ozone gas for about 15 min. An elaborative study was
factor to induce apoptosis) and also specific pro-apoptotic proteins such done by Scaccabarozzi et al. (2020) where the effect of long-term stor
as caspases 3, 6, 7, 9, p53 and others (Lu et al., 2017; Schröder and age, heating and high-pressure processing was evaluated on the reduc
Kaufman, 2005; Tabas and Ron, 2011; Zhong et al., 2017). tion of PAT. The author used tomato products like puree, paste, pulp,
Autophagy is also induced as a toxic effect of PAT. It involves the ketchup and juice for this particular study. Artificial contamination of
degradation of cytoplasmic proteins and specific organelles. This effect the samples was carried out, and PAT levels were assessed for six
is confirmed by the over-presence of autophagy markers such as LC3-II months. The result showed a significant reduction in toxin level for all
and LC31 and the degradation of a protein P62 (Lee et al., 2012). the products. A Maximum decrease was observed in tomato paste after a
Moreover, specific signalling pathways essential for cell growth and month of storage at 25 ◦ C, followed by tomato puree, wherein the
replication (transcription, translation) are also affected, and cell survival reduction was up to 98%. It might be due to the unstable nature of the
is also inhibited. Similarly, the effect of ROS has also been reported by toxin or the action of free radicals generated due to L-ascorbic acid
various researchers (Loos et al., 2014; Yang et al., 2018). Yang et al. degradation. Similar observations have also been made by other re
(2018) studied the impact of the toxin on HepG2 cells. It was found that searchers in apple products (Baert et al., 2007b; Drusch et al., 2007).
autophagy occurs by the inhibition of the ROS-Akt1-mTOR pathway. With an increase in the length of heat treatment, a progressive decrease
Another study by Sun et al. (2018) confirmed wherein HepG2 cells in toxin levels was observed but no significant decline occurred when
exposed to the toxin were also treated with an autophagosome inhibitor. the products were processed using high-pressure processing. In contrast,
The results showed a decline in PAT toxicity, indicating autophagy. other studies showed a considerable reduction when the pressure and
Oxidative damage caused by PAT also results in genotoxicity which the holding time increased simultaneously. For example, Avsaroglu et al.
causes mutagenicity, modification of DNA-bases, inter-strand cross- (2015) assessed the impact of pulsed-high hydrostatic pressure (p-HHP)
links, thus ultimately damage the DNA strand (de Champdore et al., and HHP (300–500 MPa) at different temperature (30-40 ◦ C) on
2007; De Ruyck et al., 2015; Schumacher et al., 2006). The enzyme different concentration of PAT (5, 50 and 100 ppb). the study concluded
activity of RNA polymerase and aminoacyl tRNA synthetases was also that both the processing treatments were adequate. Still, p-HHP was
inhibited (de Melo et al., 2012). The detrimental toxin effect was also more efficient at a lower concentration of toxin, and to degrade the
reported to hinder intestinal permeability and modulate tight junctions higher concentration of PAT, a higher level of HHP was found more
(Mohan et al., 2012). When the intestine gets exposed to the toxin, the useful.
intestinal epithelial cells were affected first. Singh et al. (2018) evalu Another method to degrade PAT is the use of ultraviolet radiation. A
ated the mechanism by which intestinal toxicity was induced by PAT study by Dong et al. (2010) revealed the potential of UV radiation in
exposure. The Wistar rats were orally treated with 100 μg/kg body lowering the mycotoxin level without any measurable changes in the
weight of PAT for three consecutive days. The results showed a signifi product’s quality. Though, other studies indicate that the effect was
cant rise in the level of Prostaglandin E2 (PGE2) and cyclooxygenase 2 more pronounced in juice due to the turbidity present in cider, which
(COX-2) in the serum of rats. It was found to be associated with restricts radiation passage and reduces the toxin breakdown rate.
inflammation and proliferation of cells in the intestine. Filtration and clarification processes are found useful to remove
turbidity (Assatarakul et al., 2012). Table 2 enlists the potential of
8. Effects of processing on patulin different processing techniques employed on food products to reduce
PAT concentration.
PAT neurotoxic and mutagenic potential demanded certain food
processing operations resulted in decreased mycotoxins levels (Welke 9. Effects of environmental factors on PAT production
et al., 2009). Moreover, management at pre-processing steps can also
reduce the degree of contamination (Ioi et al., 2017). It includes man The growth of fungus and PAT production occurs in a temperature
agement of storage conditions of farm produce, where the main objec range of 0-24 ◦ C with a minimum water activity of 0.99 (Mandappa
tive is to prevent fungus growth. Therefore, modified atmospheric et al., 2018). The development and colonial morphology of P. expansum
conditions for storage and application of fungicides like benzimidazole are affected by temperature, and so is PAT production. As observed from
and fludioxonil are some of the practical options (Errampalli, 2004; literature, the fungus can grow well at 0 ◦ C or below, and higher growth
Rosenberger, 2003). The application of high CO2 atmosphere and and toxin production were found at a storage temperature of 20–25 ◦ C
polyethylene packaging resulted in a reduction in PAT level, and it also (Gougouli and Koutsoumanis, 2010; Zhong et al., 2018). However, the
controlled rotting in apples (de Souza Sant’Ana et al., 2008; Moodley fungus can produce PAT at a temperature range of 1-20 ◦ C (Garcia et al.,
et al., 2002). 2011). It was studied by Tannous et al. (2016) that the optimal tem
Various processing techniques like clarification, heating, radiation, perature range was 25 ◦ C, wherein the fungus had the shortest lag phase
and high pressure showed an effect on the toxin level. In a study by and colony growth of 8.9 cm at the end of the incubation period. The
Raiola et al. (2012), the impact of thermal processing was evaluated on environmental factors such as gas composition, pH, pressure, water
apple puree and apple juice which was artificially contaminated with activity, and temperature influences apple traits and also have a pro
PAT. The samples were initially pasteurized for 20 min at 80 ◦ C, fol nounced physiological impact on fungi P. expansum that might influence
lowed by cooling for 30 min at 4 ◦ C. In the end, the samples were again the production of PAT (Zhong et al., 2018). The effect of atmosphere and
pasteurized using the same time-temperature combination as earlier. climate is due to the action of the idh gene and at low temperature, this
The results showed a significant reduction of more than 60% in the case gene expression is reduced in turn the rate of PAT production becomes
of juices. The drop in PAT level in juice could be due to several processes low. Different conditions such as controlled atmosphere and stress cause
that have been employed during preparation, such as depectinization, a delay in metabolic reactions but not the complete inhibition of toxin
clarification etc. The method of depectinization uses enzymes respon synthesis in fungus (De Clercq et al., 2016b).
sible for breaking down the pectin, and further processing steps like Similar effects were observed by Coton et al. (2020) when apples
clarification and filtration removes pectin and surrounding proteins were stored in cold and ambient storage. The environmental pH affects
from the liquid. PAT is supposed to be bound to these solid particles and the physiology and pathogenicity of fungus, determining PAT produc
removed during the clarification step (Acar et al., 1998; Root and tion, so the spore germination and growth happens at a low pH range of
16
Table 2 2018), GC-MS (Cunha et al., 2009), and LC-MS (Li et al., 2018b) have
Efficiency of various processing techniques on the level of patulin in food been used for detecting PAT in food. However, these types of equipment
products. require trained personnel to operate (Wu et al., 2018). Moreover, other
Processing Food Processing Reduction References methods based on surface plasmon resonance (Pennacchio et al., 2015),
technique Product parameters in patulin fluorescent resonant energy transfer (Wu et al., 2016) and molecularly
level imprinted polymers (Lucci et al., 2017) are also reported for the
Pasteurization Apple Two phases of Up to 62% Raiola et al. detection of PAT. An alternative to these traditional methods is a
juice and treatment at in juices. No (2012) DNA-based technique, such as real-time quantitative PCR (qPCR). It is
puree 80 ◦ C for 20 min significant
highly sensitive and specific where the mould DNA target can be
with a cooling reduction in
period in the puree detected even in complex mixtures (González-Salgado et al., 2009;
between Mateo et al., 2011). Several qPCR assays have been utilized to detect and
Ozone Apple Ozone Up to 75% Diao et al. quantify PAT besides AFB1 and OTA producing moulds in foods (Gil-
processing juice concentration (2019) Serna et al., 2009; Mayer et al., 2003; Passone et al., 2010; Sardiñas
12 mg/L, Flow
rate 3 L/min,
et al., 2011).
time- 15 min Besides these, immunosensors based on antigen-antibody in
High-pressure Tomato 600 MPa for 10 No Scaccabarozzi teractions were developed for PAT detection (Li et al., 2019b). For
processing products min with significant et al. (2020) example, graphene and its derivatives were utilized in electrochemical
(paste, temperature up reduction
sensors for improved performance (Bahadır and Sezgintürk, 2016;
puree, to 28 ◦ C
juice etc) Shukla et al., 2018). Graphene oxide (GO) provides a large surface area
Pulsed-high Apple 300MPa/50 ◦ C/ More than Avsaroglu with excellent conductivity (Justino et al., 2017). Song et al. (2020)
hydrostatic juice 6 pulses × 50 s 60% et al. (2015) developed an anti-PAT-BSA IgG on a GCE sensor coated with a GO/Au
pressure Holding time- 5 nanocomposite which detected PAT as low as 5 μg/L a minute.
min
The current focus is on immunological or aptamer-based assays for
Ultraviolet Clarified 4.62 J/cm2 50% Tikekar et al.
radiation apple reduction (2014) quick and reliable analysis so that the food industry can have rapid
juice detection methods for “in-house” application (Tomita et al., 2016; Wu
UV radiation Apple 7 passes of More than Dong et al. et al., 2016). The technique like loop-mediated isothermal amplification
cider 14.2mJ/cm2 40% (2010)
(LAMP) is for the enzymatic in vitro amplification of specific DNA se
reduction
after quences with more uncomplicated handling and evaluation methods
seventh pass suitable for low price on-site investigations in the industry (Notomi
et al., 2000). Recently, Frisch and Niessen (2019) have developed a
LAMP assay based on the isoepoxydon dehydrogenase (idh) gene for
3–5 in apples (Zong et al., 2015). McCallum et al. (2002) studied the detecting PAT-producing species, Penicillium, Byssochlamys and Paecilo
effect of temperature on the growth of P. expansum and observed no myces. The assay showed a detection limit of 2.5 pg of purified genomic
influence on PAT production. However, the secretion of PAT occurs at an DNA of P. expansum per reaction (Frisch and Niessen, 2019). Similarly,
ambient pH (3–5) while higher pH negatively affects PAT production. an electrochemical aptasensor based on tetrahedral DNA nanostructures
The reason could be the PAT instability at high pH due to the pepg1 gene (TDNs) and thionine (Thi)-labeled Fe3O4 nanoparticles
present in P. expansum that exhibits acidic pH-specific expression with (Fe3O4NPs)/rGO has been developed for PAT detection ranging from 5
minimum expression at pH > 5 and maximum expression at pH 4 (Li × 10− 8 to 5 × 10− 1 μg mL− 1 and a detection limit of 30.4 fg mL− 1 (He
et al., 2020). Further, Tannous et al. (2016) reported the lowest and the and Lu, 2020). Further, He and Dong (2020) developed an Nb.BbvCI
highest PAT production at pH 2.5 and 4, respectively. The PAT pro powered DNA walking machine with graphene oxide composites
duction decreased when the pH increased from 4 to 7. Further, PacC is (Pt@AuNRs/Fe-MOFs/PEIrGO) and Zr-based frameworks-loaded with
required for the growth of fungal mycelia and virulence in apple. Since methylene blue (MB@Zr-MOFs-cDNA) signal probes for the detection of
the expression of PacC is pH dependant, pH plays an essential role in PAT.
PAT production (Chen et al., 2018). The decrease in the medium pH is
due to the production of organic acids by fungal metabolism, resulted in 11. Masked mycotoxins as a significant concern in detection
extensive fungus growth (Wright, 2015). Further, the amount of organic
acid production affected the medium’s initial pH, thus creating an acidic The “matrix-associated” mycotoxins forms either covalent bonds
environment that also enhances disease progression (Wang et al., 2017). and/or complexes were dissolved or trapped in the matrix, while the
In addition to pH, carbon and nitrogen sources are other critical envi “modified mycotoxins” include both “biologically and chemically
ronmental factors affecting PAT production. It occurs by regulating the modified” forms. “Masked mycotoxins” are, in fact, “biologically
biosynthesis at the transcriptional level where two genes viz, PatL modified” mycotoxins conjugated by plants (Rychlik et al., 2014). These
encoding specific transcription factor and PatK encoding 6-methylsali “modified” forms go undetected by the usual detection techniques
cylic acid synthase, a catalyst enzyme mainly responsible for the first (Berthiller et al., 2013). For example, up to 20% of the PAT in cloudy
step of PAT production, are positively expressed by different concen apple juice is bound, which remain undetected during HPLC-UV analysis
trations of nitrogen (AreA), carbon (CreA) and pH (PacC) (Zong et al., (Baert et al., 2007a). Further, the mycotoxins can occur in conjugated
2015). Another important environmental factor affecting PAT produc (soluble or incorporated into macromolecules) form after metabo
tion is water activity. It was shown that the highest growth rate (0.6 cm lization by fungi, mammals and plants, or during food processing (Ber
per day) of fungus was observed at a water activity of 0.99. It decreases thiller et al., 2009).
as water activity lowers from 0.99 to 0.85 with no significant effect on It is reported that PAT can undergo an attack on a nucleophilic group
fungal growth at 0.95 and 0.99 but lower PAT production at 0.95 such as proteins or small peptides containing cysteine, lysine or histidine
compared to 0.99 (Tannous et al., 2016). residues (Fliege and Metzler, 2000). A covalent bond is hard to break
during extraction, thereby, leading the masked PAT undetected. How
10. Detection techniques ever, PAT harmful effects in mammalian conjugates were unlikely to
occur since they metabolized in the liver and excreted through urine
The traditional chromatography-based detection techniques such as (Galtier, 1998). PAT reacts with cellular nucleophiles such as proteins
HPLC coupled with diode array detection (HPLC-DAD) (Sadok et al., (Fliege and Metzler, 1999) or glutathione (Fliege and Metzler, 2000).
17
The PAT glutathione adduct degrades to L-cysteine conjugate, then upon marine yeast, degraded paulin into less toxic products. In a study by
enzymatic treatment to N-acetyl-L-cysteine derivative and finally elim Tang et al. (2019), it has been shown that orotate phosphoribosyl
inated. Masked mycotoxins can transform back into their parent forms transferase from Rhodotorula mucilaginosa was successfully used for PAT
due to metabolization during food processing, thereby, pose a serious degradation in apple juice with optimum conditions (0.15 g/L orotate
concern for human health (Berthiller et al., 2009, 2011; Kamle et al., phosphoribosyltransferase, 25 ◦ C temperature and 18 h duration),
2019; Kumar et al., 2020; Mahato et al., 2019; Zhang et al., 2019a). Not which resulted in 80% PAT degradation with no significant difference in
much information on masked forms of PAT is reported, so further nutrient profile. The application of porcine pancreatic lipase (PPL)
research is required in foods to reveal their masked forms and the found in microorganisms is a single chain of amino acids used in PAT the
associated health concerns. enzymatic degradation in aqueous solution (Liu et al., 2018). Tang et al.
(2018) had applied immobilized PPL to apple juice, which resulted in
12. Degradation kinetics PAT degradation under optimum conditions (0.03 g/ml immobilized
PPL for 1 mg/ml PAT, 40 ◦ C temperature and 18 h duration). Ngolong
The efforts to mitigate PAT contamination by pre-harvest treatments Ngea et al. (2020) has shown 99% PAT degradation using porcine
(Gacem et al., 2020) and post-harvest treatment such as drying and pancreatic lipase immobilized with calcium carbonate at 30 ◦ C tem
storage have proved little effective in the long run (Ioi et al., 2017). perature when kept for 3 h at pH 5. Candida guilliermondii can grow in
Therefore, detoxification can be achieved by physical, chemical and several PAT concentrations and, at the same time, reduces the PAT
biological processes (Peng et al., 2018). The effective physical tech content by degrading it into E-ascladiol depending upon yeast cell
niques include heat and pulsed light (PL) treatment (Abbasi et al., 2019), viability (Chen et al., 2017). The bacterial strain, E. cloacae subsp. dis
irradiation using UV (Assatarakul et al., 2012), gamma radiations with solvens TT-09, can degrade PAT into a less toxic product called
approx. 67% reduction in PAT at 1.0 kGy dose (Diao et al., 2018a) and E-ascladiol (Xing et al., 2020). It has been demonstrated by Li et al.
adsorption techniques (Erdoğan et al., 2018). The UV irradiation (Zhu (2018a) that PAT can be biologically degraded when incubated with
et al., 2013) and photodegradation of PAT follow first-order kinetics, exo- and endo-enzymes secreted by S. cerevisiae CITCC 93161 cells into
with the solution being more acidic having a faster reaction rate (Ibarz E-ascladiol. The most common byproduct of PAT biodegradation is
et al., 2017). However, these techniques have shown limited degrada E-ascladiol and Z-ascladiol, a new study has shown the byproduct to be
tion effectiveness in addition to non-desired losses and negatively desoxypatulininc acid by Rhodosporidium palugenium (Wright, 2015).
affecting the nutritional and organoleptic properties of products The lactic acid bacteria (LAB), particularly heat-inactivated, have
(Rodríguez-Bencomo et al., 2020). So, new approaches have been higher PAT adsorbing property in aqueous solution due to high specific
analyzed for PAT degradation as they eliminated the drawbacks of surface area and hydrophobicity (Wang et al., 2015). LAB strains such as
previous techniques (Zhang et al., 2019b). Another non-thermal tech Bifidobacterium animalis VM, Bifidobacterium bifidum 6071 and
nique is high hydrostatic pressure (HHP) which has shown a significant L. rhamnosus 6149 were able to degrade 80%, 52.9% and 54.1% PAT in
reduction in PAT concentration e.g. 62% in apple juices and 23% in aqueous solution, and this degradation activity is more at low pH
apple juice concentrates at 800 MPa. It further retains the organoleptic (Muhialdin et al., 2020). Another LAB strain, L. casei YZU01 degraded
and nutritional characteristics of food (Avsaroglu et al., 2015; Hao et al., PAT by extracellular enzymes and also absorbed PAT through the cell
2016). Besides, microwave and ultrasonic waves were also used for PAT wall (Zheng et al., 2020). The spectrum of PAT degradation from yeast
degradation with up to 100% and 69.43% reduction respectively could to LAB has been extended to filamentous fungi, Byssochlamys nivea FF1-2
be achieved under optimum conditions (Diao et al., 2018a). strain, that degrades the 500 μg/ml PAT at 37 ◦ C and pH 3.0–5.0 range
Chemical detoxification involves the degradation of PAT by chem (Zhang et al., 2016). Pichia caribbica degraded PAT by intra and extra
icals, among which the most effective being the ozone (Miller et al., cellular enzymes produced in response to PAT concentration (Zheng
2013). It has been shown by Diao et al. (2018b) that PAT in apple juice et al., 2016). E− and Z-ascladiol were the main intermediate products of
was reduced to 35.22% of original concentration at 7 mg/L ozone PAT degradation by Pichia caribbica which are less toxic and
concentration for 10 min using gaseous ozone. Other chemical com non-poisonous (Zheng et al., 2018). At the molecular level, deletion of
pounds such as ascorbic acid (5% after 3 h and 36% after 44 h), potas PcCRG1, S-adenosylmethionine-dependent methyltransferase, led to a
sium permanganate (99.9%), sulphur compounds (12% after 24 h and decrease, whereas overexpression led to an increase in PAT degradation
90% after two days) also help in the degradation of PAT (Ioi et al., (Wang et al., 2019). These methods have several advantages over
2017). The degradation in ascorbic acid content is shown by the Weibull physical and chemical processes. However, concerns arise regarding the
model and its simplified form in contrast to the zero-order kinetic model uptake of nutrients and metabolite production by these microorganisms
in the absence of ascorbic acid (Kokkinidou et al., 2014). The addition of (Peng et al., 2018).
certain chemicals like calcium D-pantothenate brings about 94.3% PAT
reduction compared to 35.8% reduction when not added (Yazici and 13. Management and control strategies
Velioglu, 2002). Nowadays, metallic nanoparticles such as zinc, silver
and selenium have inhibited mycotoxin production (Afsah-Hejri et al., Patulin contamination can occur in the field before, during and after
2020). ZnO exhibits antifungal activity against P. expansum and restrains harvest while performing storage and packaging activities, so it is
the growth and PAT production in a dose-dependent way (Abd-Elsalam essential to control the contamination while performing such activities.
et al., 2020). The chemical treatments proved to be effective in PAT PAT contamination prevention can be divided into pre-harvest, har
degradation, but it leaves an unknown residue and brings about irre vesting and post-harvest strategies (Kabak et al., 2006).
versible changes which need further studies. Pre-harvest strategies include excellent farm management, applica
Biological degradation involves using microorganisms (yeast, bac tion of fungicides and insecticides, use of fertilizers to maintain mineral
teria and fungi) that degrade the mycotoxins into less toxic products composition, culture management to improve plant vigour, irrigation,
(Gacem et al., 2020). One such example of yeast is Rhodosporidium and cultivar selection (Mandappa et al., 2018). Foliar calcium spraying
kratochvilovae strain LS11 that degraded PAT into desoxypatulinic acid, and use of minimal amounts of nitrogen during the growing season
which is less toxic (Castoria et al., 2011). Biological detoxification in result in the reduction of pre-harvest infection by pathogens and strains
volves two steps: reducing PAT toxicity by detoxification and removing of A. pullulans and Rhodotorula glutinis combined with Bacillus subtilis
PAT from solution by adsorption (Ohadi et al., 2020; Sajid et al., 2019). isolate. It further reduces the chances of post-harvest decay of fruit by
Some yeasts act as biocontrol agents by competing with plant pathogens reducing the size and number of lesions on the wounded apples caused
for nutrients, thus inhibiting their growth (Sperandio et al., 2015). The by P. expansum (Sarrocco and Vannacci, 2018). Other preharvest tech
result of a study by Dong et al. (2015) suggested that Kodameae ohmeri, a niques include crop rotation and crop turnover to reduce inoculation on
18
the field, soil analysis during fertilization before applying fertilizers, and The hygienic conditions of the storage rooms after harvesting also
the use of hybrids resistant to mould infection. Manufacturers should affect the fruit and PAT production and rate of contamination. It can
also be guided by GAP (Good agricultural practices) and GMP (Good determine the spore probability to reach the apple wound, initiation of
management practices) principles so that they can take the necessary colonization, and severity of rot and finally, the amount of apple pulp
preventive measures to reduce the contamination to the lowest level the industry may lose (Morales et al., 2010). This way, maintaining the
(Pleadin et al., 2019). storage facilities and rooms is essential as a post-harvest control strat
During harvest and transportation, there are chances of physical egy. Controlled atmosphere (CA) is the environment with elevated CO2
damage and wounds that give way for P. expansum penetration and levels and decreased O2 levels as compared to normal air. This in com
infection. Reducing wound incidence lowers PAT concentration, for bination with refrigeration extends the shelf life of fruit. It has been
example, 99% damage control resulted in a 70% PAT reduction (Baert shown that prolonged low O2 concentration damages the fungus and
et al., 2012). Hence, it is essential to reduce injuries and physical inhibits primary metabolism (Morales et al., 2007). This has shown a
damage by taking maximum precautions during transportation and reduction in PAT accumulation not only in CA storage but also after
harvesting. Other factors considered while harvesting is picking the fruit ambient storage for subsequent 3 days (Morales et al., 2010).
in dry conditions, keeping them in clean bins, transporting directly to
stores and storing them in cold storage at 1.5–4.0 ◦ C within 18 h of 14. Conclusions and future research
harvest to reduce the mould infection (Kabak et al., 2006). It has also
been shown by Baert et al. (2012) that sorting the fruits stored in a Mycotoxin contamination in the food chain is an inevitable and se
controlled atmosphere by removing the infected apples with lesions is vere concern that has rouse serious food quality and safety concerns
highly effective in reducing PAT concentration because the PAT may worldwide. Numerous studies have revealed that patulin exposure leads
infect the other non-infected tissues and fruits (Paster and Barkai-Golan, to intestinal barrier injury, gastric problems, immunological and
2008). developmental harmful effects. Studies based on animal trial and cell
Post-harvest control strategies include using fungicides, pesticides culture have shown hepatotoxic and genotoxic effects with higher doses
and other biocontrol agents in cold storage, maintaining storage room leading to animal death. There is an escalated need for the development
hygiene along with controlling atmosphere conditions. Fungicides such of protocols that offers a better understanding of patulin as a toxicant to
as benzimidazole are used after the harvesting to prevent the fruit rot in safeguard human from any probable health effects. The systematic
cold storage. Lai et al. (2017) have shown that potassium phosphite surveillance of raw material and final product along with effective
inhibits apple fruit growth and PAT production. However, due to the adoption of preventive tools like Good Agricultural Practice (GAP), the
harmful effects of these chemicals in food and the emergence of a Good Manufacturing Practice (GMP) and the Hazard Analysis and
resistant population, their use has been restricted. The various alterna Critical Control Points (HACCP) stands obligatory to alleviate any
tive treatments such as nitrous oxide, sodium hypochlorite, hydrogen chance of occurrence of patulin contamination from “farm to fork”.
peroxide electrolyzed oxidizing water, copper sulphate, and biocontrol Further emphasis must be put on epidemiological studies and the
yeast have also been suggested (Tannous et al., 2018). In the development of reliable, low-cost, easy to handle and portable detection
post-harvest control strategies, the use of biocontrol agents (BCA) such technologies. Use of microbial control agents and immobilized enzymes
as antagonistic yeast is becoming popular as they persist for a long time for mycotoxin decontamination and degradation can be exploited at a
after treatment and protects the fruit from re-infection (Mahunu et al., commercial level based on their availability for food industries. Further,
2016a). BCA protective effects on apples from P. expansum rot were due the use of genetic engineering for developing crops with improved
to PAT in vitro detoxification and transformation into a less toxic com fungal resistance is an excellent future option.
pound (Castoria et al., 2005). However, the disadvantages include
inconsistency in performance and inability to control latent infections. Credit roles
Therefore, it must be combined with other treatments for better effi
ciency (Paster and Barkai-Golan, 2008). Lima et al. (2011) showed that Pradeep Kumar: Conceptualization; Dipendra Kumar Mahato,
the application of biocontrol yeast R. kratochvilovae isolate LS11, and Madhu Kamle, Bharti Sharma, Shikha Pandhi, Sheetal Devi, Kajal Dha
C. laurentii isolate LS28 combined with CYPR or BOSC raised the control wan, Raman Selvakumar, Diwakar Mishra, Arvind Kumar, Shalini Arora,
of P. expansum rot using the chemical and biological treatments sepa Namita Ashish Singh: Writing-original draft preparation, literature
rately. Another BCA involved in post-harvest management of PAT pro survey, tables preparations. Pradeep Kumar and Dipendra Kumar
duction is the use of Candida sake and Pantoea agglomerans. It effectively Mahato: Writing-Reviewing and Editing.
controlled the growth of P. expansum in the apples during cold storage
(Morales et al., 2008).
Propolis, a resin made by honeybees, has been applied as an anti Declaration of competing interest
fungal agent to inhibit P. expansum growth and PAT production (Silici
and Karaman, 2014). The more recent trends are the use of enhancers The authors declare that they have no known competing financial
that can improve the efficacy of biocontrol agent against P. expansum. interests or personal relationships that could have appeared to influence
Different researchers have suggested the use of certain natural en the work reported in this paper.
hancers in combination with biocontrol agents. In a study, the combined
treatment of yeast P. caribbica and bamboo leaf flavonoid was found as Acknowledgements
an effective biocontrol agent in PAT breakdown in apples (Mahunu
et al., 2018). Similarly, phytic acid (@ 0.2% v/v) in combination with The authors are grateful to the higher authority and the respective
P. caribbica showed significant improvement in the control of P.expan departments, institutions and university.
sum infections in apples (Mahunu et al., 2016b). Likewise, PAT content
reduced by 89.6% compared to the control when R. mucilaginosa was
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Patulin in food: A mycotoxin concern for human health and its

Table 1 (continued ) Table 1 (continued )

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