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489
Food Safety in China: Science, Technology, Management and Regulation, First Edition.
Edited by Joseph J. Jen and Junshi Chen.
© 2017 John Wiley & Sons Ltd. Published 2017 by John Wiley & Sons Ltd.
29
29.1 The Present Situation for Fruit and Vegetable Safety,
Domestic and Abroad
Fruits and vegetables play important roles in human nutrition and health, particularly
as sources of vitamin C, thiamine, niacin, pyridoxine, folic acid, minerals, and dietary
fiber. Moreover, many different organizations (WHO, FAO, USDA, EFSA) recommend
increases in fruit and vegetable consumption to help reduce the risk of cardiovascular
diseases and cancer [1]. Therefore, the market for fresh fruit and vegetable produce has
continually grown over the past decade around the world. With increases in consump-
tion of fresh produce, food safety issues are obviously becoming a public concern.
According to the CDC’s Food-borne Outbreak Online Database (food tool;
http://wwwn.cdc.gov/foodborneoutbreaks/), the number of food-borne outbreaks
per year in the US has gradually decreased since 1998. Nonetheless, the number of
produce‐associated outbreaks still remains high, ranging from 23 to 60 per year dur-
ing 2004–2012, without a clear trend over this period of time [2]. There were obvious
increases in 2006 (57 outbreaks), 2008 (51 outbreaks), and 2011 (60 outbreaks).
Moreover, 49 of the produce‐associated outbreaks (13%) reported during the years
2004–2012 were multi‐state outbreaks. Norovirus was the main cause of produce‐
associated outbreaks (59% and mainly linked to salad), followed by Salmonella (18%),
which was the leading pathogen in multi‐state outbreaks and was responsible for the
majority of sprouts‐associated outbreaks. However, in the summer of 2011, a multi‐
state outbreak of listeriosis linked to whole cantaloupes from Jensen Farms, Colorado,
caused 147 infection cases, 33 deaths, and 1 fetal loss in 28 states [3]. This outbreak is
considered to be the largest listeriosis outbreak on record and also the largest recent
outbreak due to any pathogen in the US [4].
For the EU, based on the EFSA national zoonoses country reports (https://www.efsa.
europa.eu/en/biological‐hazards‐data/reports), the number of outbreaks linked to
fresh produce per year ranged from 10 to 42 in 2004–2012 with no discernible pattern
emerging. However, there were substantial increases in 2006 (29 outbreaks), 2009
(34outbreaks), and 2010 (44 outbreaks) [2]. The share of produce‐associated outbreaks
The Importance of Food Safety for Fruits and Vegetables
Xiaosong Hu1, Fang Chen1, Pan Wang1 and Zhao Chen2
1 College of Food Science and Nutritional Engineering, China Agricultural University, Beijing, China
2 Department of Biological Sciences, Clemson University, SC, USA
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490
increased from 4.4% in 2009 to 10% in 2010 [5]. Norovirus was the most common
pathogen for produce‐associated outbreaks (53% and mainly linked to berries), fol-
lowed by Salmonella (20%), which was consistent with the situation in the US. In
May2011, German health authorities began to investigate an outbreak of a novel patho-
gen, Shiga‐toxin‐producing Escherichia coli (STEC) O104:H4 [6], which caused the
highest number of hemolytic‐uremic syndrome (HUS) cases associated with a single
outbreak. The final case count was 4075 cases (908 HUS cases) and 50 deaths in 16
countries. Initially, German health authorities made wrong assessments of the likely
strain of E. coli and also incorrectly linked the pathogen to Spanish cucumbers [7]. The
traceback investigations by the EFSA finally identified fenugreek seeds imported from
Egypt as the source. This outbreak led to negative economic impacts on Spanish vegeta-
ble growers, highlighting challenges in investigating outbreaks caused by rare patho-
gens and with international trade involved [8].
With respect to Canada, the number of reported food‐borne outbreaks during 1975–
1995 varied significantly from year to year [9]. Fresh‐fruit‐associated outbreaks in 1985
showed 21 and 55 incident and case reports, respectively, but with no documented
cases in 1993. In Australia, fresh produce accounted for 4% of food-borne outbreaks
during 2001–2005 [10].
Compared to Western countries, China does not have many outbreaks due to fresh
produce since the Chinese do not eat as much raw produce as Westerners and thus have
less chances of exposure to produce pathogens. However, chemical contamination can
occur at any stage from farm to fork [11]. Water pollution, heavy metals in the environ-
ment, excessive use of pesticides, and chemical fertilizers have directly resulted in several
food safety incidents over the past few years in China. Chemical residues within fruits and
vegetables have become the most important health risk. According to statistics from the
Ministry of Health, in 2006, there were as many as 326 incidents of food poisoning caused
by excessive pesticide residues in China, with a total number of 2974 people poisoned (66
people died). In 2014, the corresponding data showed 160 incidents of food poisoning,
with a total number of 5657 people poisoned (110 people died) (Table 29.1). Moreover,
intentional adulteration has occurred in fruit and vegetable products such as fruit juice.
China has made great efforts to improve food safety. The Food Safety Law of the PRC was
promulgated in 2009. According to statistics in 2009–2014 from the Ministry of Agriculture,
more than 95% of the fruit and vegetable samples passed supervision inspections
(Figure29.1). In 2006, the Agricultural Product Quality and Safety Law and the Organization
Law of Farmer Special Economic Cooperation were approved to guide the implementation
and supervision of the quality and safety of agricultural products. In terms of the adminis-
tration of quality and safety of agricultural products, China’s government carried out a
strategy of “separate supervision and regulation in each section.” In addition, various certi-
fications, such as ISO22000, GAP, GMP, and HACCP have developed rapidly.
29.2 Pre-Harvest Routes for Fresh Produce Contamination
in Soils
China is the world’s largest fruit and vegetable processing country [1, 12]. In 2014, the
cultivation areas for fruits and vegetables in China were 1237.14 and 2140.48 million hec-
taresand the production amounted to 26 142.24 and 76 005.48 million tons, respectively
Table 29.1 A list offactors causing food poisoning inChina from2010–2014.
Reason for poisoning
Number of cases Number of people poisoned Number of people dead
2010 2011 2012 2013 2014 2010 2011 2012 2013 2014 2010 2011 2012 2013 2014
Microbial 81 78 56 49 68 4585 5133 3749 3359 3831 16 14 16 1 11
Chemical 40 30 21 19 14 682 730 395 262 237 48 57 19 26 16
Toxic animals, plants and mushrooms 77 53 72 61 61 1151 1543 990 718 780 112 51 99 79 77
Unknown 22 28 25 23 17 965 918 1551 1220 809 8 15 12 3 6
Total 220 189 174 152 160 7383 8324 6685 5559 5657 184 137 146 109 110
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492
(Figure 29.2) [13]. However, hazardous compounds in environment and input residues in
agricultural production have become a public concern on health risk.
29.2.1 Environmental Contaminants
Serious heavy metal contamination events have taken place since the 1950s in China,
with more frequent occurrences coming in recent years. Metals are selectively concen-
trated by crops. In particularly, leafy vegetables are more responsive to trace elements
2009 2010 2011 2012 2013 2014
95.0
95.5
96.0
96.5
97.0
97.5
98.0
98.5
Vegetables
Fruit
Qualified rate (%)
Figure 29.1 Pass (qualified) rate (%) for fruit and vegetable quality and safety tests in China.
2004 2005 2006 2007 2008 2009 2010 2011 2012 2013
0
10000
20000
30000
40000
50000
60000
70000
80000
Output (million tons)
vegetable
fruit
Figure 29.2 Changes in fruit and vegetable output from 2004 to 2013.
29 The Importance ofFood Safety forFruits andVegetables 493
in soil, such as cadmium and lead. Ni, Yang, and Long [14] found that cadmium accu-
mulation in crops was linearly related to the level of cadmium in soil. For leafy vegeta-
bles, the increase was exponential. It has been documented that nearly 50% of the mean
ingestion of cadmium and lead from food involves fruits, vegetables, and cereals [15].
Therefore, accumulation of metals in leafy vegetables not only affect food quality, but
are also have present a potential hazard to human health by way of the food chain.
Many surveys have shown heavy metal contamination on crops to be caused by sew-
age irrigation due to the impending water shortage in China. The emission of industrial
wastewater has increased with the rapid economic growth and population increase
since the 1970s. The emission of sewage (urban and rural sewage) is greater than 60
billion tons every year, with urban sewage treatment rates reaching 77.5% in 2010,
although it is less than 10% in rural areas. With increasing wastewater emissions, sew-
age irrigation has become an effective measure to alleviate the shortage of water
resources and increase agricultural production [16]. However, sewage contains a large
number of potentially hazardous materials, including persistent organic pollutants, and
heavy metals [17]. Intake of vegetables containing high concentrations of metals has
caused detrimental health risks, such as osteoporosis and cardiovascular disease, to the
consumer, especially children [18]. In 2013, for the first time, the government prohib-
ited the application of sewage with heavy metals and/or persistent organic pollutants
for irrigation [19]. However, policy implementation is challenging, especially in the
North China Plain as a result of the lack of availability of good quality water.
29.2.2 Chemical Inputs inAgricultural Production
Fruit and vegetable protection provided by the use of pesticides have made a signifi-
cant contribution to growth in agricultural productivity. The total consumption of
fertilizers and pesticides has increased linearly over time, with usage doubling over the
past two decades [20]. Although grain yield grew in the same period, total production
has increased only by a quarter, with a yield reduction between 1999 and 2003. After
2003, the government has implemented a series of policies, such as subsidies for seeds,
fertilizers, and pesticides, and abolition of the agricultural tax. It was found that usage
of pesticides and fertilizers was positively correlated with grain yield and this correla-
tion after 1999 was stronger and of a higher magnitude than before 1999. Due to lim-
ited availability of arable land, it is necessary to increase the yield per unit area through
the increase of chemical inputs. Although farmers could use fewer pesticides to get
higher yields with the implementation of an integrated pesticide management (IPM)
program [21], the current production of grain still greatly relies on the use of pesticides
and fertilizers.
29.2.2.1 Fertilizers
China is a large consumer of chemical fertilizers. China’s grain yield increased 1.7‐fold
over the past three decades and chemical fertilizer use increased by 3.9 times, with an
average annual growth rate of 12.9%. The total fertilizer consumption was 430.0 kg/ha
in 2012 [20], whereas the internationally recognized maximum safe usage of fertilizers
is 225.0 kg/ha [22]. However, over the same period, many countries have taken meas-
ures in order to control and reduce the consumption of nitrogen and phosphorus ferti-
lizers. Chemical fertilizer use has been reduced by approximately 30–50% in Western
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494
European countries since the 1980s. In 2010, the consumption of nitrogen and
phosphorus fertilizers were 278.4 and 134.5 kg/ha in China, and only 70.7 and 23.9 kg/ha
in the United States [21]. Nitrate is a potential hazard because it can be reduced to
nitrite endogenously in plants. This nitrite may result in methemoglobinemia and can
react with amines or amides to form a variety of N‐nitroso compounds (NOCs), which
are potential human carcinogens [23].
Moreover, the utilization efficiencies are 30–40%, 10–20%, and 35–50% for nitrate,
phosphate, and potash, respectively, which are much lower than in developed countries,
where the nitrate use efficiency can be as high as 70–80%. Up to half the nitrogen
applied in China is lost by volatilization, and another 5–10% by leaching. A large num-
ber of surveys have indicated that there is a higher nitrate or nitrite content in drinking
water in higher cancer incidence areas [24]. Control of nitrate content in drinking water
could effectively reduce the incidence of cancer in Linzhou City in Henan Province [25].
In recent years, China’s environmental protection policy has paid attention to the
reduction of ammonia nitrogen emissions. This has led to increases in measures that
convert ammonia nitrogen into nitrate nitrogen in wastewater treatment plants before
discharge into environment. These measures may cause more severe nitrate nitrogen
pollution.
29.2.2.2 Pesticides
Pesticide residues in the vegetable and fruit sectors is more serious than it is in other
sectors. It is the most important concern for consumers. China is the largest pesticide
consumer in the world [20]. The total amount of pesticide applied was 1.78 million
tons in 2011, which has increased by 2.3 times since 1991, with an average annual
growth rate of 11.7%. At the same time, the efficiency of pesticides is only about 30%
in China, while it is 50–60% in developed countries [26]. Thus, pesticide residues
inagricultural products have become one of the biggest consumer health concerns in
China. In recent years, the Chinese government has addressed pesticide production
and use issues largely through its regulatory power. The production and use of some
high‐toxic and high‐residue pesticides has been prohibited. The data showed that the
overall level of contamination decreased and that the percentage of pesticide residues
over prescribed limits declined year by year, from 0.7% in 2003 to 0.5% in 2009. The use
of pesticides in agricultural production is tending to be more scientific, reasonable,
and feasible.
Pesticide residue testing by firms and sample testing by the government are the two
screenings that alleviate potential food safety risks. The Food Safety Law of the People’s
Republic of China, promulgated on November 1, 2006, explicitly requires that firms
engaged in agricultural production should test pesticide residues themselves or through
third‐party testing organizations. Therefore, pesticide residue testing has become one of
the effective measures for food safety control. Nevertheless, the pesticide residue testing
system in China is not perfect. Furthermore, it is not sufficient to completely solve food
safety problems by just testing for pesticide residues. Creating a traceability system that
helps to quickly identify faulty products is of great necessity to firms. To date, a number
of firms in China have established sales account systems, and it is now possible to trace
firms that provide faulty products. Production records that contain inputs and produc-
tion management measures, and are recorded by farmers are needed to further and more
accurately trace exact responsibility to the appropriate subjects. In addition, one of the
29 The Importance ofFood Safety forFruits andVegetables 495
main problems in first‐stage product processing is the inappropriate use of chemical
preservatives, which can be effectively traced by establishing production records. Hence,
in this chapter we are also looking at the establishment of production records as a food
safety control practice.
29.3 Post-Harvest Routes for Fresh Produce Contamination
Mechanical injury induced by cutting (lettuce, apple, and pear), shredding (carrot, cab-
bage), dicing (tomato), or peeling (carrot, orange) during harvesting operations occurs
for fresh‐cut produce. These operations create surfaces upon which enteric pathogens
can more easily attach. Cut surfaces of produce also release large amounts of nutrient‐
laden liquids that are readily utilized by the attached microbes.
29.3.1 Pathogens Associated withFruits andVegetables
A number of mechanisms have been advocated as contributing to adhesion of enteric
pathogens to food surfaces, including: extracellular polymeric substances; the presence
or absence of fimbriae; cell surface hydrophobicity; divalent cationic bridges; and bacte-
rial surface charge. Unfortunately, conclusive evidence for the contribution of these
factors is absent due to differences in response by pathogens to attachment and the
heterogeneous nature of the various surfaces investigated, as well as the dramatic differ-
ences in cell surface composition between different types of produce.
Fresh‐cut fruits and vegetables harbor a wide variety of microorganisms, such as
bacteria, yeasts, and fungi that cause spoilage (Table 29.2) [27]. An estimated 80–90%
of bacteria are Gram‐negative, predominantly Pseudomonas and Enterobacteriaceae
species. Lactic acid bacteria are part of the normal flora of fruits and vegetables and are
associated with spoilage organisms, causing unpleasant odors. Yeasts and molds are
present in smaller numbers than bacteria, but, when present in high numbers, they can
contribute to spoilage of fermented products and the development of soft rot.
According to epidemiological surveys, fresh‐cut fruits and vegetables can also harbor
pathogenic bacteria capable of causing human infections, such as Listeria monocy-
togenes, Salmonella spp., and Escherichia coli O157:H7 [28]. Many factors can contrib-
ute to the contamination of fresh and fresh‐cut products with pathogens. Pre‐harvest
contamination of fruits and vegetables can occur via animals, insects, water, soil, dirty
equipment, and human handling. Post‐harvest manipulation, wash water, workers,
Table 29.2 Common human pathogens existing infresh fruits andvegetables.
Categories Specific microorganisms
Pathogenic bacteria in soil Clostridium botulinum, Listeria monocytogenes
Pathogenic bacteria in faeces Salmonella, Shigella, Escherichia coli O157:H7
Pathogenic parasites Cryptosporidium, Cyclosporiasis
Pathogenic viruses Hepatitis A virus, Enterovirus, Norwalk‐like virus
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496
packing materials, process equipment, and transportation vehicles are also potential
sources of contamination.
Due to the occasional presence of pathogens on fruits and vegetables, several out-
breaks associated with the consumption of these products have been reported. For
example, melons, tomatoes, pears, watermelons, strawberries, mangoes, grapes, spin-
ach, and lettuce have been implicated in outbreaks caused by Salmonella spp. and E. coli
O157:H7 [29]. L. monocytogenes has been implicated in outbreaks linked to contami-
nated lettuce, broad‐leaved endive, broccoli, radishes, cabbages, potatoes, cucumbers,
and melons [30].
29.3.2 Survival andGrowth ofPathogens onFresh Produce During Storage
In general, enteric pathogens are often capable of surviving on produce over the
period of distribution. The fate of enteric pathogens on produce during storage is
dependent on the storage conditions, including temperature, relative humidity, gase-
ous composition of the atmosphere, nutrient availability, and presence of competitive
bacteria or antimicrobial compounds. In addition, damage to the product often
enhances survival and growth of contaminated pathogens. For example, lettuce tissue
from heads dropped six feet incurred survival or growth of E. coli O157:H7 ˜0.5 log
greater than in undamaged tissue when stored at ambient temperature for 4 hours,
followed by 48 hours of storage at 4 °C. Slicing methods that shear or tear the tissue
also led to consistently higher E. coli and L. innocua counts on packaged vegetables
(carrots, and iceberg and butterhead lettuces) during storage than slicing manually
with a razor. Biological damage is also of concern as it often leads to enhanced sur-
vival or growth of enteric pathogens. For example, produce that has been affected by
soft rot is more conducive to growth of Salmonella than non‐diseased produce [31].
Nevertheless, significant differences in survival of L. monocytogenes strains occurred
in coleslaw, with most strains exhibiting decreases in population during storage at
8°C. However, populations of serotype 1/2a strain 269 increased on coleslaw during
storage at 8 °C [32].
29.3.3 Packaging Technology
Modern methods of storage, including physical methods, chemical methods, and bio-
logical methods, such as low‐temperature storage, controlled atmosphere storage,
radiation storage, chemical antisepsis, antagonistic storage of microbes and their meta-
bolic products, genetic engineering technology, and so on. These methods can maintain
the freshness of fruits and vegetables to some extent, but not completely (Table 29.3).
Modified atmosphere packaging (MAP) of fresh products consists of altering the
atmosphere inside the package by the natural interaction between the respiration rate
of the product and the transfer of gases. The desired atmosphere can be created using
either active or passive modified atmosphere packaging. Active MAP is based on the
displacement or replacement of gases in the package, or the use of gas scavengers or
absorbers to establish a desired mixture of gases, while passive MAP is based on the use
of a specific packaging film, in which a desired atmosphere develops naturally due to the
product’s respiration and the diffusion of gases through the film [33].
MAP is used for various types of products, and the specific mixture of gases in the
packaging in each case depends on the product type, the packaging materials, and the
29 The Importance ofFood Safety forFruits andVegetables 497
storage temperature. If the permeability (for O2 and CO2) of the packaging film is
adapted to the product respiration, an equilibrium modified atmosphere is established
in the package and the shelf‐life of the product increases.
In addition, temperature control is also very important to an effective MAP system.
Temperature strongly affects the respiration rate and the permeability of gases through
packaging films, allowing atmosphere changes to occur inside the packaging [35].
Furthermore, storage temperature is one of the most important factors in the survival
and growth of pathogens on fresh‐cut fruits and vegetables. Maintaining produce tem-
perature at or below 4 °C throughout the cold chain is essential for microbial safety.
During fruit and vegetable processing, the intracellular components released from bro-
ken cells may enhance bacterial growth. Therefore, specific measures and interventions
should be implemented to minimize the risk of infection associated with the consumption
of contaminated fresh‐cut fruits and vegetables. Nowadays, MAP in combination with
Table 29.3 Potential damage existing inthemethods ofstorage andpreservation[34].
Methods Potential Damage
Low‐
temperature
storage
Different fruits and vegetables have certain ranges of endurance of low
temperature. If the temperature is too far out of the range, it will change the
nutrition and shape of the products and affect the food safety. This is called
low‐temperature damage.
Controlled
atmosphere
storage
This kind of damage is caused by different proportions of gas components,
which would destroy the sensory properties of fruits and vegetables, accelerate
the loss of nutrients, and even produce substances harmful to human health.
This damage also contributes to the multiplication of some anaerobic bacteria
on fruits, threatening the safety of fruit and vegetable products.
Hypobaric
Storage
Each kind of fruit and vegetable has a certain endurance limit for low pressure
preservation. If the pressure were beyond the limit, the nutrition and quality
would be damaged.
Radiation
storage
A range in radiation amount is an important factor affecting fruit and vegetable
nutrition and quality. A relatively low amount of radiation should be chosen to
process fresh fruits and vegetables, otherwise, lots of nutrients would be lost,
with the fruits and vegetables becoming soft under radiation.
Chemical
antisepsis
An inappropriate solvent concentration not only cannot maintain the quality of
fruits and vegetables, but will accelerate deterioration.
Antagonistic
storage
The inducing effects of antagonistic microorganisms will definitely change
physiological metabolism of fruits and vegetables, such as inducing some
secondary metabolites to resist disease, enzymes for defense, and structural
resistance.
Storage with
bionic
preservatives
The researches about the inhibitory effects of natural products on pathogenic
bacteria have always been done in culture media, but practice has shown that to
obtain the inhibitory concentration acquired in culture media from
experiments, the amount of preservative should be multiplied in practical
application.
Genetic
engineering
Modifying, silencing, or altering the expression activity of some genes may
change physiological processes and the quality of fruits and vegetables.Whether
it is safe to eat genetically modified fruits and vegetables is a problem needing
an urgent solution.
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498
refrigeration can be used as a mild preservation technique to enhance the safety of
minimally processed products. However, the effect of MAP on microorganisms can vary,
depending mainly on the storage conditions and the type of product.
29.3.4 Transportation
Currently, the supply of fruit and vegetable products in China is still stuck in the tradi-
tional mode of storage and transportation, as cold‐chain logistics are not well devel-
oped. In 2012, there were 0.3 million refrigerated carriers in China, while in America
and Japan the number was 2 million and 1.2 million, respectively [36]. The ratio of
refrigerated carriers to freight vehicles in China is only 0.3%, while in America the ratio
is 0.8–1.0%, and Germany and other developed countries have a ratio around 2–3%.
Every year, the amount of perishable goods transported by railway in China is about
100 million tons, but only 25% of the total products are transported in refrigerated
trains. The total amount of refrigerated vehicles used for highway transportation is only
0.4 million and the amount of perishable goods transported by refrigerator cars occu-
pies less than 20%. China has over 200 refrigerated transportation ships, with a total
capacity of 1 million tons, however only 1% of the total products are transported by
waterway. With the exception of export fruits and vegetables transported under refrig-
eration, domestic fruits and vegetables are generally transported at ambient tempera-
ture (Table 29.4).
Compared to the increasing output of fresh produce, the cold chain logistics of fruits
and vegetables in China are very deficient, thus developing these is still a most impor-
tant and pressing task for China.
29.4 Global Perspective
For the control of food safety of fruits and vegetables, a worldwide traceability system has
been implemented. We have emphasized that agricultural production is the source and
the most critical stage as a result of the transmission of food safety problems along a sup-
ply chain. The inappropriate use of fertilizers and pesticides and agro‐ecological environ-
mental pollution results in chemical and microbiological contamination of fresh produce
at source. Thus, food safety control practices at the production stage essentially involve
three aspects: (i) environmental inspection, (ii) input, and (iii) production management.
Table 29.4 Cold-chain circulation andtransportation amounts from2010 to2014 inChina [37].
Year
Amount of production
(billion tons)
Amount of cold-chain
circulation (billion tons)
Amount of cold-chain
transportation (billion tons)
2010 8.65 0.51 1.38
2011 9.07 0.66 1.60
2012 9.50 0.85 1.85
2013 9.86 1.13 2.14
2014 10.00 1.46 2.47
29 The Importance ofFood Safety forFruits andVegetables 499
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