Mycotoxins

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Introduction

Mycotoxins and food Mycotoxins are naturally occurring, toxic


safety chemicals which can be produced by fungi
infecting agricultural crops during the
growth, drying and subsequent storage of the
crop. If eaten, they can produce toxic effects
in human and animals.
David Atkins and Human reactions to mycotoxins have been
recorded since ancient times. Throughout the
Julie Norman Middle Ages, when rye bread was the staple
diet of many Europeans, there were numerous
outbreaks of ergot poisoning when it appears
that “the staff of life became the sceptre of
death”. Symptoms included hallucination,
manic depression, gangrene, abortion,
decreased fertility and could lead to painful
The authors convulsive death. The poisonings have been
David Atkins and Julie Norman are joint Head of Food linked to the production of the mycotoxin
Contaminants Division of MAFF and the Department of ergot by contamination of the cereal by the
Health’s Joint Food Safety and Standards Group, London, fungi Claviceps purpurea. It is now believed by
UK. some historians that ergot played a major role
in limiting the population of Europe during
Abstract the Middle Ages, with population growth only
A review of the food safety implications of crops contami- increasing significantly in the mid-eighteenth
nated by mycotoxins. Each of the most important mycotox- century as a result of the introduction of
ins, aflatoxins, ochratoxin A, and patulin, are described wheat and potatoes as dietary staples (Smith
individually with details of national and international et al., 1994).
safety evaluations and the UK’s controls to protect con- Mycotoxin contamination of food and
sumer safety. The state of play of EC proposals to har- feeds remains a world-wide problem. The
monise national laws on mycotoxins is also described. United Nation’s Food and Agriculture
Consumer perceptions of risk from these natural toxicants
Organisation has estimated that as much as 25
are assessed. Mycotoxins present a potential threat to
per cent of the world’s food is significantly
consumer safety. Continued vigilance is necessary to
contaminated (Smith et al., 1994). Countries
ensure that regulatory and advisory limits are complied
of the European Community (EC) are some-
with. MAFF surveys regularly check the foods most at risk
what less at risk than the populations of less
of contamination and where a problem is unearthed,
developed countries because of the generally
consumers and industry are alerted as soon as possible
high standards of major food suppliers and
through rapid publication procedures. Subsequent
retailers, and also because of relatively tight
monitoring of the situation ensures that effective action is
regulatory controls which deter import of the
taken to protect consumer safety.
most contaminated material. As a conse-
quence, the most contaminated material is
probably consumed by those populations,
such as some of the producer countries them-
selves, which may not benefit from this level of
consumer protection.
Although many mycotoxins have been
identified by the scientific literature, these
have been found mostly under laboratory
conditions. Only a relatively small number
have been shown to occur naturally in food
and animal feed at sufficiently high levels and
frequency of occurrence to be of concern.
Nutrition & Food Science
Number 5 · September/October 1998 · pp. 260–266 The main mycotoxins of interest at present
© MCB University Press · ISSN 0034-6659 are:
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Mycotoxins and food safety Nutrition & Food Science
David Atkins and Julie Norman Number 5 · September/October 1998 · 260–266

• aflatoxins, the need to control consumer exposure to


• ochratoxin A, individual mycotoxins is summarised below.
• fumonisins,
• patulin, Aflatoxins
• moniliformin, Aflatoxins are produced predominantly by
• sterigmatocystin, two species of mould, Aspergillus flavus and
• tricothecenes and Aspergillus parasiticus. They are a group of
• zearalenone. difuranocoumarin derivatives of which 18
This list may increase as more assessments are types have been identified. The main ones are
made of toxicology and implications for con- B1, B2, G1, G2, and M1. They are found in a
sumer safety. wide variety of foodstuffs including nuts,
To protect consumers, the Ministry of cereals, dried fruit and milk. However, the
Agriculture, Fisheries and Food (MAFF) growth of these mould species are not
regularly checks food for mycotoxins. These favoured by the temperatures and humidity of
surveys, first reported in 1980 (MAFF, most EC countries and therefore products
1980), have identified the foods most at risk imported from third countries with hot and
of contamination problems, which have been humid climates present the major sources,
subsequently dealt with through regulation or either directly through contaminated nuts and
figs, or indirectly through contaminated
codes of practice and advice. For both aflatox-
animal feeding stuffs. When cattle consume
ins and patulin, consumer exposure has been
feed contaminated by aflatoxin B1, it is
reduced substantially by this action and by
metabolised to aflatoxin M1 and appears in
subsequent follow-up surveys. Details of these
the milk.
results and MAFF’s other work on mycotox-
All aflatoxins are acutely and chronically
ins can be found in the publications listed in
toxic, although to varying degrees. Aflatoxin
Appendix.
B1 is considered to be among the most potent
carcinogens known and has been linked
UK regulation of mycotoxins epidemiologically with cases of human liver
cancer in a number of developing countries.
As with all food chemical contaminants, the
However, even in these cases the picture is not
general provisions of the Food Safety Act
clear, since the role of other factors such as
(HMSO, 1990) offer consumer protection
Hepatitis B must be considered in the disease
against the gross contamination of food by
process. It is therefore extremely difficult to
mycotoxins. In addition, aflatoxins, which of
assess the level of risk to most consumers in
all the mycotoxins are generally considered to
the EC who experience occasional low levels
present the greatest threat to food safety, are
of exposure. Because of the profound toxicity
specifically regulated in the UK (HMSO, in animals, most regulators have followed the
1992). Throughout the world, this group is precautionary principle and have insisted on
the most highly regulated of the mycotoxins extremely low limits which are as low as can
since they are not only animal carcinogens, be practically achieved. It is no surprise that
but are generally recognised to be human the European Community has begun with
carcinogens as well. aflatoxins in its task of harmonising its laws on
World-wide, many advisory bodies con- mycotoxins.
cerned with food safety, including the World The COT concluded, in the light of
Health Organisation’s Joint Expert Commit- evidence of animal carcinogenicity and
tee on Food Additives (JECFA) and the probable human carcinogenicity, that
European Community’s Scientific Committee aflatoxins in food should be reduced to the
for Food (SCF), have assessed the risk from lowest level that is technologically achievable
mycotoxins and have advocated controls to (MAFF, 1980). Following subsequent advice
reduce consumer exposure. In the UK, the from the FAC (MAFF, 1980), in 1992 the
control of mycotoxins has been based on Aflatoxins in Nuts, Nut Products, Dried Figs and
expert advice from the Committee on Toxicity Dried Fig Products Regulations (HMSO, 1992)
of Chemicals in Food, Consumer Products set limits of 4µg/kg (microgram per kilogram
and the Environment (COT) and the Food or part per billion – ppb) for total aflatoxins in
Advisory Committee (FAC). Their advice on food ingredients and finished products for
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Mycotoxins and food safety Nutrition & Food Science
David Atkins and Julie Norman Number 5 · September/October 1998 · 260–266

consumers, and 10µg/kg for products desig- findings (Food Surveillance Information Sheet,
nated for further processing to reduce the No. 130 – see Appendix).
aflatoxin levels before sale or
incorporation into a product for human Patulin
consumption. Subsequent surveys (listed in Patulin is a low molecular weight hemiacetal
Appendix) have shown that the advice of the lactone possessing wide spectrum antibiotic
COT and FAC and the consequent regulation properties which was at one time evaluated as
have reduced the exposure of UK consumers a treatment for the common cold. It is pro-
to aflatoxins. Further consumer protection is duced by a number of species of Aspergillus
offered by the Feeding Stuffs Regulations and Penicillium. Most commonly and
which, through maximum limits for aflatoxin importantly it is associated with Penicillium
B1 in animal feed, ensure that consumers are expansum, a common storage rot of apples,
not exposed to unacceptable levels of the toxic peaches, pears, bananas, apricots, cherries
metabolite, aflatoxin M1, in milk. and grapes. A series of extensive MAFF
surveys (Appendix) has shown that the major
Ochratoxin A dietary source in the UK is from apple juice
Ochratoxins are a group of structurally related following the use of moulding or
derivatives of isocoumarin linked to L-pheny- damaged fruit. Since patulin is largely
lalanine of which ochratoxin A is the most destroyed by fermentation, cider is not a
common. A range of fungal species from the significant source of the toxin.
genera Aspergillus and Penicillium is able to Patulin is considered to be mutagenic,
produce ochratoxin A. Contamination is most although it may not be carcinogenic. It has also
commonly associated with cereals, pulses and been found from animal trials to have adverse
coffee. Unlike aflatoxins, the organisms which effects on the developing foetus and can cause
produce ochratoxin A can thrive in the immunotoxic, neurotoxic and adverse affects
temperatures and humidity commonly found on the gastrointestinal tract. The UK currently
in temperate countries. has an advisory maximum level of 50µg/kg for
Ochratoxin A has been linked with kidney patulin in apple juice. This level was agreed by
damage in pigs and in humans has been asso- the FAC in 1992 following advice from the
ciated with a chronic progressive kidney COT that levels be reduced to the lowest
disease (Balkan endemic nephropathy), pre- technologically achievable (MAFF, 1993).
dominantly affecting women, which may lead Following further surveillance reports in 1993,
to death (Krugh, 1980). Ochratoxin A 1994 and 1995 (see Appendix), the FAC
appears to be an animal carcinogen, but there reconfirmed this level in 1995, but because of
is uncertainty over its status as a human car- its concerns that the advisory level is not fully
cinogen. The COT concluded in 1992 that effective in removing grossly contaminated
ochratoxin A is a genotoxic carcinogen and apple juice from the food supply, it recom-
advised that levels in food should be reduced mended that officials should seek to have a
to the lowest level that is technologically specific limit included in future EC regulation
achievable (MAFF, 1993). of mycotoxins (MAFF and DH, 1995).
The FAC considered the implications of
the COT’s advice for the UK food supply in
EC regulation
1992 and published its opinion in a statement
in Food Surveillance Paper, No. 36 (MAFF, In the course of initial discussions, the
1993). It requested that surveillance of EC Commission suggested a number of
ochratoxin A in UK-produced cereals and mycotoxins for future Community regulation,
animal feeding stuffs should continue with the but decided to defer consideration of all but
aim of developing a plan to reduce ochratoxin aflatoxins, pending the outcome of a safety
A contamination to the lowest level techno- review of ochratoxin A and patulin by the
logically achievable. However, it did not at EC’s Scientific Committee for Food (SCF).
this time advocate regulation. The FAC This move was supported by most Member
recently reviewed its position and advocated States, since of all the mycotoxins, aflatoxins
EC regulation (see below) and specifically are considered to present the clearest toxic
advised that a limit be sought for dried vine hazard. Aflatoxins are also the most widely
fruits in the light of the recent MAFF survey controlled mycotoxin by current national
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Mycotoxins and food safety Nutrition & Food Science
David Atkins and Julie Norman Number 5 · September/October 1998 · 260–266

regulations and therefore provide the greatest be included in this amending regulation, but
impetus for harmonisation. will not make a formal proposal until the EC’s
The current EC proposals set limits for Scientific Committee for Food (SCF) has
aflatoxin B1 (2µg/kg) and total aflatoxins completed its review of ochratoxin A. It seems
(4µg/kg) in edible nuts, dried fruit and for likely that the Commission will propose limits
cereals and cereal products intended for direct of 5µg/kg for cereals, coffee and dried vine
human consumption or as an ingredient in fruits. The EC Commission also stated that
foodstuffs. A higher limit of 5µg/kg B1 and unless alternatives are suggested, the sam-
10µg/kg total aflatoxins is proposed for edible pling plan for ochratoxin A will be the same as
nuts and dried fruit subject to further that for aflatoxins.
treatment before consumption; and a level of The EC Commission has also proposed to
0.05µg/kg for M1 in milk. In addition, return to a consideration of patulin once the
specifically for groundnuts subject to further SCF has completed its review. Most Member
treatment before consumption, higher limits States with regulations or advisory levels
of 8µg/kg B1 and 15µg/kg total aflatoxins are appear to favour 50µg/kg in fruit juices or just
proposed. These proposals, although similar apple juice. It is likely therefore that the EC
to the current UK regulations (HMSO, Commission will propose a harmonised limit
1992), will extend the range of commodities along these lines.
covered to include cereals, dried fruit other Although ochratoxin A and patulin are the
than figs and milk, which although not most likely candidates for EC Commission
considered in the UK to present important proposals, it is possible that the current
sources of aflatoxins, will nonetheless offer toxicological study of fumonisins in the USA
in principle a broader range of consumer may raise potential human health problems,
protection. requiring regulatory intervention. In the
The procedures for sampling and analysis future, with increased knowledge about other
are described by an associated draft Directive. mycotoxins and their implications for food
There are concerns about the unduly onerous safety, the EC may need to expand the scope
nature of the proposed sampling plan. It is of its regulation.
less practical than the sampling plan in the
current UK regulations, and may result in a Risks from contaminated foods entering
decreased level of enforcement testing with the UK from other EC Member States
reduced protection for UK consumers. How- Recent EC action imposing a temporary ban
ever, Member States (MS) will have until 31 on Iranian pistachio nuts (MAFF and DH,
December 2000 to implement the sampling 1998) has raised a number of concerns about
directive and during the intervening period the relative effectiveness of surveillance
regular meetings will be held to discuss testing regimes throughout the Community
changes which may be required in the light of and the potential for contaminated foods to
any difficulties identified. be brought to the UK market from other EC
The documents have now been finalised at ports without further testing. The UK has a
EC Working Group level following the con- long history of mycotoxin surveillance and
sideration and comment by representatives of statutory sampling and testing procedures,
the World Trade Organisation. The proposals which is not the case for all EC Member
will go to the EC’s Standing Committee on States.
Foodstuffs for adoption, probably in June Current UK regulations apply to com-
1998, with the regulation coming into force modities when imported and subsequently to
shortly afterwards. Most Member States are food ingredients and final foods at retail. This
likely to vote in favour of the proposed regula- dual level of protection will continue to be the
tion. case when there are EC regulations. When
produce is imported through another EC
EC action on other mycotoxins Member State and brought to the UK, it is
The EC Commission proposes to include possible to test further at the port of entry,
ochratoxin A in a future regulation. At the and subsequently up to the point of retail,
Working Group meeting on 10 November without contravention of Community free
1997, the Commission sought advice from trade rules. Nonetheless, it is easier to test and
Member States on which commodities should control imports of food from third countries
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Mycotoxins and food safety Nutrition & Food Science
David Atkins and Julie Norman Number 5 · September/October 1998 · 260–266

when they are imported directly into the UK, situation. Both committees have
usually in large batches, through the ports of recommended that a further survey should be
entry designated by current UK regulations carried out as a matter of priority to check on
(HMSO, 1992). Realistically, this trade will the effectiveness of this action. As well as
continue, but the proposed EC regulation will seeking the opinions of the COT and the
tighten up the current entry requirements of FAC, MAFF informed the industry of their
many EC Member States for foods subject to individual results and held a meeting with
aflatoxin contamination and will reduce the them, consumers and health and enforcement
chances of contaminated material entering organisations. Industry was asked to take
the UK market. action to reduce the level of contamination in
The EC’s Food Control Working Group is dried vine fruits. Subsequently, industry came
currently reviewing the general issue of third forward with a plan of action to improve the
country imports of non-animal origin via the situation including test procedures for
annual Co-ordinated Sampling Programme. ochratoxin A, both in producing countries
In 1998 this programme will focus on the and on import. In addition, a code of practice
sampling of peanuts and pistachios for afla- is being developed to ensure that all dried vine
toxin contamination and the results will be fruits sold in the UK are as free from
available to the Working Group in 1999. mycotoxins as possible.
MAFF has also communicated the survey
MAFF’s mycotoxin surveillance results to other EC Member States and to the
programme EC Commission. The EC Commission has
been asked to consider a regulatory limit for
To protect consumer safety, MAFF has a
ochratoxin A in vine fruits when regulatory
broad programme of surveys on mycotoxins
proposals on ochratoxin A are made in the
which was first reported in 1980 in Food
near future. MAFF will carry out a follow-up
Surveillance Paper, No. 4. Further results from
survey in 1998 to check that the action being
this programme have been subsequently
taken by industry has been effective.
reported in further Food Surveillance Papers
(Nos 18 and 36) and by a range of Food
Surveillance Information Sheets (Appendix).
’…Mycotoxins present a potential threat
to consumer safety. Continued
Recent mycotoxin surveys
vigilance is necessary to ensure that
The most recently reported survey looked at
raw materials and foods comply with
levels of aflatoxins and OA in a number of
regulatory and advisory limits…‘
commodities. The results of this survey of 313
UK retail foods and 153 UK cereal samples
have been published as Food Surveillance
Information Sheet, No. 130 (Appendix). A survey of ochratoxin A in the 1997 UK
Aflatoxins were not detected in any of the cereal harvest at intake to cereal stores and
samples analysed. Ochratoxin A, was not following storage is currently being under-
detected in 75 per cent of samples. However, taken and will be completed in 1998. It is
27 samples were found to contain ochratoxin possible that conditions during the 1997
A at concentrations above 4µg/kg. These growing season, coupled with the damp
samples were predominantly dried vine fruits harvest, were particularly favourable for the
(raisins, currants and sultanas) indicating a production of ochratoxin A in cereals. A
possibly widespread problem with these survey of the human exposure to ochratoxin A
commodities. is also being conducted. This will correlate
Expert committee advice was sought on dietary intakes of ochratoxin A with concen-
the significance of these results for consumer trations in plasma and urine. Results from
safety. The FAC (MAFF and DH, 1997a) has these surveys will be used to support the UK
endorsed the COT advice (MAFF and DH, negotiating line in the forthcoming EC
1997a) confirming that ochratoxin A should negotiations on proposed limits for ochratoxin
be reduced to the lowest level that is techno- A. In addition, two studies are under way to
logically achievable and recommended that develop statistically meaningful but practical
industry take immediate action to remedy this sampling plans for mycotoxins.
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David Atkins and Julie Norman Number 5 · September/October 1998 · 260–266

Two other surveys have been undertaken to Mycotoxins present a potential threat to
examine respectively the concentrations of consumer safety. Continued vigilance is
sterigmatocystin and moniliformin in a range necessary to ensure that raw materials and
of UK foods. The results of these surveys will foods comply with regulatory and advisory
be published in 1998. A survey of UK dietary limits.
exposure to sterigmatocystin has not been MAFF surveys regularly check the foods
possible until recently due to a lack of reliable most at risk of contamination and where a
analytical methods.
problem is unearthed, consumers and indus-
During 1998, in addition to the follow up
try are alerted as soon as possible through the
survey on ochratoxin A, it is also planned to
rapid publication procedures (MAFF and
carry out a further survey of directly produced
DH, 1997b). Subsequent monitoring of the
apple juice for patulin. The results of this
survey will be taken to the FAC in the situation ensures that effective action is taken
Autumn when it will reassess its current to protect consumer safety.
position on the advisory level in preparation
for any future EC regulatory proposals. References

Hayward, A.C.D. (1997), “Consumer perceptions”, in


Consumer perceptions of risk from Tennant, D. R. (Ed.), Food Chemical Risk Analysis,
mycotoxins Blackie, London.
Several UK studies have been performed into HMSO (1990), Food Safety Act 1990, HMSO, London.
consumer perceptions of relative risk from HMSO (1992), Aflatoxins in Nuts, Nut Products, Dried Figs
food related hazards. These have been and Dried Fig Products Regulations 1992, S.I.
summarised in a recent publication No. 3236.
(Hayward, 1997). In 1971, the following Krogh, P. (1980), “Ochratoxins: occurrence, biological
order of public priorities were reported: food effects and causal role in disease”, in Eaker, D. and
additives, pesticide residues, environmental Wadstrom, T. (Eds), Natural Toxins , Pergamon Press,
contaminants, nutritional problems, micro- Oxford, pp. 673-80.
biological hazards, and natural toxicants. MAFF (1980), “Survey of mycotoxins in the United King-
Although subsequent studies have reported dom”, Food Surveillance Paper, No. 4, HMSO.
reduced levels of concern about food MAFF (1993), “Mycotoxins: third report”, Food Surveil-
additives and have revealed new concerns lance Paper, No. 36, HMSO.
about BSE and novel foods and processes, MAFF and DH (1995), “FAC advice patulin in apple juice”,
natural toxicants, including mycotoxins, Food Safety Information Bulletin, No. 67, p 3,
appear to remain a relatively low priority of November, MAFF London. Tel: 0345 573012.
concern. MAFF (1997), Natural Toxicants in Our Food, Foodsense
These findings appear to reflect personal Booklet PB 1265, available from Foodsense, London.
responses to natural based risks, which seem Tel: 0645 556000.
responsible for the generally low priority also MAFF and DH (1997a), “Ochratoxins A and aflatoxins”,
given to microbiological risk. However, it Food Safety Information Bulletin, No. 90, November,
may also reflect a lack of knowledge about MAFF, London, pp. 10-12. Tel: 0345 573012.
mycotoxins and their potential for harm. MAFF and DH (1997b), “Surveillance results releasing
MAFF publications on mycotoxins have brand names new policy”, Food Safety Information
been aimed largely at interested parties rather Bulletin, No. 88, September, MAFF, London,
than the lay reader, through publications such pp. 1, 18-20. Tel: 0345 573012.
as Food Surveillance Papers and Food MAFF and DH (1998), “Iranian pistachios ban on
Surveillance Information Sheets (plus imports lifted”, Food Safety Information Bulletin,
associated Bulletin articles); see Appendix. No. 93, MAFF, London, February, p. 13. Tel: 0345
However, a MAFF Food Sense Booklet – 573012.
natural toxicants in our food – is available Smith, J.E., Lewis, C.W. et al. (1994), Mycotoxins in
which covers mycotoxins and offers advice Human Nutrition and Health, European Commission
to consumers on avoiding risks from DG XII, Science Research and Development, EUR
contaminated foods (MAFF, 1997). 16048 EN.
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David Atkins and Julie Norman Number 5 · September/October 1998 · 260–266

Appendix: Food Surveillance Papers and information sheets on mycotoxins

No. Title/subject area Date Bulletin


16 Patulin in Apple Juice: 1993 Survey October 1993 42
22 Aflatoxins in Herbs and Spices January 1994 45
24 More on Patulin in Apple Juice February 1994 46
28 Surveillance of UK Cereals for Ochratoxin A May 1994 49
29 Survey of Apple Products for Patulin May 1994 49
36 1994 Survey of Apple Juice for Patulin September 1994 53
37 Survey of “Ethnic Foods” for Mycotoxins September 1994 53
45 Aflatoxin Contaminaion of Peanut Butter and Peanuts November 1994 55
48 Surveillance of UK Cereals of Ochratoxin A January 1995 57
56 Aflatoxin Contamination of Peanut Butter and Peanuts February 1995 58
61 Surveillance for Fumonisins in Maize-Based Foodstuffs May 1995 61
63 Survey of Fruit Juices and Tomato Products for Patulin June 1995 6264
64 Survey of Aflatoxin M1 in Retail Milk and Milk Products June 1995 62
73 Surveillance of Ochratoxin A in Retail Coffee Products September 1996 65
74 1995 Survey of Apple Juice for Patulin September 1995 71
80 Surveillance of Ochratoxin A in Green (Unroasted) Coffee Beans March 1996 71
81 Aflotoxin Surveillance of Retail and Imported Nuts, Nut
Products, Dried Figs and Fig Products March 1996 71
86 Surveillance of Fumonisins in Foodstuffs April 1996 72
95 Ochratoxin A in Cereals and Flour, and Carry-over into
Retail Processed Foods October 1996 77
97 1996 Survey of Apple Juice for Patulin October 1996 77
130 Survey of Aflatoxins and Ochratoxin A in Cereals and
Retail Products November 1997 89
4 Survey of Mycotoxins in the United Kingdom
(Food Surveillance Paper, HMSO) 1980
18 Mycotoxins (Food Surveillance Paper, HMSO) 1987
36 Mycotoxins: Third Report (Food Surveillance Paper, HMSO) 1993
Note: Publications are available from Publicity and Information Section, Room 303b, Ergon House c/o Nobel
House, 17 Smith Square, London SW1P 3JR. Also on MAFF’s Website at http://www.maff.gov.uk/food/
infsheet/intro.htm

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