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The use of advanced oxidation processes in the degradation of the pesticide chlorpyrifos
and reduction of microbial contamination on apples
The use of advanced oxidation processes in the degradation of the pesticide chlorpyrifos and
reduction of microbial contamination on apples
Jordan Ho Advisors:
University of Guelph, 2019 Dr. Keith Warriner
Dr. Ryan Prosser
A method based on Advanced Oxidation Process (AOP) was validated for the degradation of
chlorpyrifos on apples and inactivating Escherichia coli O157:H7, along with Aspergillus niger
spores. AOP generates free-radicals using UV-C light (at 254 nm), hydrogen peroxide, and
ozone. The use of gaseous ozone alone was ineffective in chlorpyrifos degradation and was
therefore excluded from AOP use. Response surface methodology (RSM) was used to find that
the degradation of chlorpyrifos was primarily dependent on UV-C dose and hydrogen peroxide
temperature but not hydrogen peroxide concentration. The maximal degradation of chlorpyrifos
on apples was achieved through an AOP treatment applying 68.4 kJ/m2 UV dose and 1.22% v/v
H2O2 at 66°C that resulted in a 47% reduction (92µg) of the pesticide with < 0.004 µg
accumulation of chlorpyrifos-oxon. The same treatment supported a >6.56 log CFU reduction in
E. coli O157:H7 and >6.56 log CFU reduction of A. niger spores.
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ACKNOWLEDGEMENTS
First, I’d like to thank my advisor Dr. Keith Warriner for taking me on as a graduate student, a
cautionary tale I’m sure he would not repeat. Thanks for these two years, I’ve learned a lot in the
field of food safety and enjoyed every minute of it. I also learned, more than I wanted, about how
the world of academia works which is why I would hate to pursue a PhD degree! Too much
politics and drama, although entertaining as a spectator, it doesn’t seem fun as a participant. I’d
also like to thank my committee members Dr. Ryan Prosser and Dr. David Lubitz for helping me
develop my presentation skills during my committee presentations as well as helping me edit this
thesis. I hope you both well wishes and I couldn’t have asked for a better committee.
Thank you everyone in my lab, especially Fan, Mahdiyeh, and Joanna for helping me out with my
experiments. Next, I’d like to thank my friends and family for their support, especially Emma,
Jesse, Nick, and Siva. Special thanks to Andrew Green for helping answer any questions I had
about microbiology and life too maybe. Also special thanks to Katherine Katie Kathy Petker, and
Dr. Shane Walker for not throwing a toaster at me for my constant annoyance. May WW continue
again someday even though I am no longer there.
Lastly, thank you OMAFRA Agri-Food and Innovation for funding this project along with Clean
Works Corp. for their donation of equipment and consultancy.
iv
TABLE OF CONTENTS
ABSTRACT ............................................................................................................................................... ii
ACKNOWLEDGEMENTS ........................................................................................................................... iii
TABLE OF CONTENTS .............................................................................................................................. iv
LIST OF TABLES ....................................................................................................................................... vi
LIST OF FIGURES ....................................................................................................................................viii
LIST OF ABBREVIATIONS ......................................................................................................................... xi
Chapter 1: Introduction and Literature Review ........................................................................................ 1
Future work ........................................................................................................................................... 72
Table 2. Different types of insecticides and their mechanism of action. Sourced from (NPIC, 2019). ...... 7
Table 3. Produce with the highest and lowest pesticide residues scores. Adapted from Environmental
Working Group. ...................................................................................................................................... 8
Table 4. Produce-linked foodborne outbreaks of Escherichia coli O157:H7 in North American between
1996 and 2018. Modified from (Green, 2018). ....................................................................................... 16
Table 5. Reduction of pesticide residues on produce by current washing treatments. .............................. 22
Table 6. Degradation of pesticides using AOPs and individual processes. .............................................. 29
Table 7. Oxidation potential of reactive species. Adapted from Parsons (2004). ..................................... 31
Table 8. Contamination and waste products treated with AOP technologies with pesticides and
microorganisms highlighted. Modified from Vogelpohl (2003). ............................................................. 32
Table 9. RSM trials (20) using various test parameters of UV-C dose (kJ/m2), temperature (°C) and
concentration (%) of hydrogen peroxide. ............................................................................................... 42
Table 10: Six center point replicate trials determining the replicability and precision of the experimental
method. Arranged from lowest to highest reduction corrected with the average (n=177) positive control
recovery of 89.4%. The standard deviation between reductions was 3.6 µg. ........................................... 43
Table 11. RSM trials with amount of CPY reduction (µg) observed using various test parameters of UV-C
dose (kJ/m2), temperature (°C) and concentration (%) of hydrogen peroxide. Reduction from each trial
was corrected using the average positive control recovery of 89.4% (n=177). ........................................ 58
Table 12: Six center point replicate trials determining the replicability and precision of the experimental
method. Arranged from lowest to highest reduction corrected with the average (n=177) positive control
recovery of 89.4%. The standard deviation between reductions was 3.6 µg. ........................................... 59
vii
Table 13. ANOVA analysis table of the linear model indicating that values lower than P < 0.05 are
significant. In this case, UV-C dose and H2O2 temperature are significant whereas H2O2 concentration
was not significant. * indicates P < 0.05................................................................................................. 59
Table 14. Q-ToF analysis of CPY-O on apple skins spiked with CPY. It can be observed that apple skin
samples treated with AOP produced the by-product CPY-O while samples spiked with CPY but not
treated with AOP had concentrations below the limit of detection. ......................................................... 66
Table 15. Log count reduction of Escherichia coli O157:H7 and Aspergillus niger spores inoculated onto
apple peel sections then treated with UV-C (at 254 nm), hydrogen peroxide (1.22% v/v at 66C) or a
combination of UV-C and hydrogen peroxide ........................................................................................ 70
viii
LIST OF FIGURES
Figure 1. Bioaccumulation of the pesticide DDT throughout the food chain. Modified from Penn State
Figure 11. Photolysis reaction of ozone when exposed to UV-C light at 254 nm. One oxygen molecule
and hydroxyl radical is produced. Modified from Spartan Environmental Technologies, LLC. ............... 35
Figure 12. Response surface methodology design with center points and star points. Modified from Stat-
Ease, Inc. ............................................................................................................................................... 37
Figure 13. Schematic diagram (A) and photograph (B) of the advanced oxidation process reactor used for
chlorpyrifos degradation and microbial inactivation. .............................................................................. 40
Figure 14. Schematic (A) and photograph (B) of ozone chamber treatment of CPY spiked apple skins. . 47
Figure 15. Calibration curve of chlorpyrifos-oxon standards ranging in concentrations from 0.01 – 0.31
µg/mL. Concentrations of 0.16 and 0.31 µg/mL were removed due to low accuracy. R2 value = 0.9993. 50
Figure 16. 3D surface graph of different interaction effects of an advanced oxidation process for
degrading CPY on apples. CPY was introduced onto apple peel and treated with various combinations of
hydrogen peroxide and UV dose with the decrease in pesticide levels being recorded. The plots illustrate
UV dose and H2O2 temperature (A), UV dose and H2O2 concentration (B) & H2O2 concentration and
H2O2 temperature (C). ........................................................................................................................... 62
Figure 17. Predicted vs actual reduction of CPY table and graph illustrating the accuracy of the RSM
model in predicting CPY degradation under known conditions. ............................................................. 63
Figure 18. Graph of CPY reduction using only UV radiation with a linear trend line (orange line).
Reductions were calculated using HPLC analysis. A R2 value of 0.982 was calculated using 5 data points
of varying UV doses (kJ/m2) and CPY reduction (µg). ........................................................................... 64
x
Figure 19. Log counts of Escherichia coli O157:H7 and Aspergillus niger spores. *<2.3 CFU/mL is the
limit of enumeration. All treatments are determined to be statistically significant for both organisms. .... 70
xi
LIST OF ABBREVIATIONS 2,4-D…………………………………………………...…………2,4-Dichlorophenoxyacetic acid
Warriner, 2008). It is thought that the free radicals generated on the surface of the sample can
access microbes shielded from UV-C by surface structures. It is possible that the proportion of
free radicals required to inactive microbes is less than that needed for CPY oxidation. The results
suggest that hydrogen peroxide makes a greater contribution to antimicrobial action of AOP,
while photo-oxidation by UV-C makes a greater contribution to the degradation of CPY, and it
can be enhanced by temperature. In this respect, the optimum AOP treatment parameters
70
identified in this study can collectively act to reduce microbial and chemical hazards in fresh
produce.
Figure 19. Log counts of Escherichia coli O157:H7 and Aspergillus niger spores. *<2.3 CFU/mL is
the limit of enumeration. All treatments are determined to be statistically significant for both
organisms.
Table 15. Log count reduction of Escherichia coli O157:H7 and Aspergillus niger spores inoculated
onto apple peel sections then treated with UV-C (at 254 nm), hydrogen peroxide (1.22% v/v at
66C) or a combination of UV-C and hydrogen peroxide.
Microbe Treatment Log CFU/Sample
Initial
Loading
Post-Treatment LCR
Escherichia coli
O157:H7
Control
(Non-treated)
8.590.52
H2O2 (1.22% v/v) <2.30* >6.56a
UV-C (69 kJ/m2) 2.690.41 5.890.41b
71
UV-C + H2O2(69
kJ/m2 and 1.22%
v/v)
<2.30* >6.56a
Aspergillus
niger
Control
(Non-treated)
6.980.35
H2O2 (1.22% v/v) 5.320.40 1.650.40a
UV-C (69 kJ/m2) <2.30* >4.68b
UV-C + H2O2 (69
kJ/m2 and 1.22%
v/v)
<2.30* >4.68b
Mean values for each of the test microbes, followed by the same letter are not significantly
(P>0.05) different.
*Limit of enumeration = 2.30 log CFU/Sample
4. Conclusions
This study found that the use of AOPs involving UV radiation at 254 nm and hydrogen peroxide
were successful in degrading the pesticide chlorpyrifos (CPY) on the surface of apple skins. An
HPLC analysis method and recovery method for determining residual CPY levels on apples was
shown to be effective and accurate with an average positive control recovery of 89.4% 3.8%
(n=177). Through multiple ozone fumigation trials, it was shown that ozone gas was incapable of
degrading CPY on apple skins after 30 minutes of exposure in an enclosed space. A set of
experiments designed using RSM showed that hydrogen peroxide concentration is an
insignificant factor in degrading CPY while UV radiation and hydrogen peroxide temperature
were significant factors. When using the optimized treatment parameters of 68.4 kJ/m2 UV dose
and 1.22% v/v H2O2 at 66°C, an average degradation of 94 µg (47% of the initial concentration)
(n = 9) was observed. However, it was shown that UV radiation on its own was more effective
than when used in combination with hydrogen peroxide; a UV dose of 64 kJ/m2 alone produced
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an average CPY degradation of 141 µg (n = 9). Although degradation of CPY was observed, Q-
ToF analysis showed that CPY degradation resulted in the production of chlorpyrifos-oxon
(CPY-O), the active and more toxic form of CPY. Treatment of 10 µg/mL CPY with optimized
degradation parameters resulted in the production of 0.004 µg (0.02 µg/mL) CPY-O. The spike
amount used in this study was 1000 times the MRL for CPY on apples in Canada of 0.01 µg/mL
which suggests that the production of CPY-O from treated apples with CPY concentrations near
the MRL would be minimal and not pose a significant risk to human health. Decreasing the
contact distance between the UV lamp source and apple skin surface resulted in the UV dose
being increased due to an increased UV intensity, thus reducing the treatment time required for
the same effect. AOP treatment was also successful in reducing microbial colonies of both the
pathogen E.coli O157:H7 and A. niger. Despite being insignificant in degrading CPY, the
addition of hydrogen peroxide is useful for treating microbial contamination, and was significant
in reducing E.coli O157:H7 to below the limit of enumeration (2.30 log CFU/sample).
Future work
This study focused only on the treatment of apples, which have a relatively smooth surface
compared to most other fruits and vegetables. Different types of produce should be tested with
the AOP to determine its effectiveness in reducing CPY and microbial contaminants. Other types
of insecticides besides CPY should be tested as well including: carbamates, organochlorides,
phenylpyrazole, pyrethroids, neonicotinoids, and ryanoids. Other types of pesticides can also be
tested such as fungicides, bactericides, and especially herbicides, which are the most widely used
type of pesticide in the world. Modern day pesticide analysis involves testing for multiple
pesticide residues at the same time. A known concentration pesticide solution containing
multiple pesticides should be spiked onto apple skin samples and analyzed using triple-quad LC-
73
MS-MS in order to determine the degradation of multiple pesticides at the same time rather than
using HPLC to determine the degradation of a single pesticide as performed in the current study.
Other future work of interest may be to use AOP to treat lower CPY spike concentrations, down
to 0.01 µg/mL (maximal residue limit on apples in Canada). It may also be worth investigating
how to obtain a higher UV dose in order to decrease treatment time, which will impact the rate of
food production.
Different microbial organisms can also be tested on apples or different types of produce
including: salmonella and if possible, viruses. UV-C radiation has been known to inactivate
viruses as well as bacteria and molds (Tseng & Li, 2007; Watanabe et al., 2010)
74
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