Bioengineering 08 00092 v2

bioengineering
Review
Bioremediation of Agricultural Soils Polluted with Pesticides:
A Review
Carla Maria Raffa and Fulvia Chiampo *
Department of Applied Science and Technology, Politecnico di Torino, Corso Duca degli Abruzzi 24,
10129 Torino, Italy; carla.raffa@polito.it
* Correspondence: fulvia.chiampo@polito.it; Tel.: +39-011-090-4685
Abstract: Pesticides are chemical compounds used to eliminate pests; among them, herbicides are
compounds particularly toxic to weeds, and this property is exploited to protect the crops from
unwanted plants. Pesticides are used to protect and maximize the yield and quality of crops. The
excessive use of these chemicals and their persistence in the environment have generated serious
problems, namely pollution of soil, water, and, to a lower extent, air, causing harmful effects to the
ecosystem and along the food chain. About soil pollution, the residual concentration of pesticides
is often over the limits allowed by the regulations. Where this occurs, the challenge is to reduce
the amount of these chemicals and obtain agricultural soils suitable for growing ecofriendly crops.
The microbial metabolism of indigenous microorganisms can be exploited for degradation since
bioremediation is an ecofriendly, cost-effective, rather efficient method compared to the physical
and chemical ones. Several biodegradation techniques are available, based on bacterial, fungal, or
enzymatic degradation. The removal efficiencies of these processes depend on the type of pollutant
and the chemical and physical conditions of the soil. The regulation on the use of pesticides is strictly
connected to their environmental impacts. Nowadays, every country can adopt regulations to restrict

the consumption of pesticides, prohibit the most harmful ones, and define the admissible concen-
Citation: Raffa, C.M.; Chiampo, F. trations in the soil. However, this variability implies that each country has a different perception
Bioremediation of Agricultural Soils
of the toxicology of these compounds, inducing different market values of the grown crops. This
Polluted with Pesticides: A Review.
review aims to give a picture of the bioremediation of soils polluted with commercial pesticides,
Bioengineering 2021, 8, 92. https://
considering the features that characterize the main and most used ones, namely their classification
doi.org/10.3390/bioengineering8070092
and their toxicity, together with some elements of legislation into force around the world.
Academic Editors: Bruna Matturro
and Marco Zeppilli
Keywords: pesticides; bioremediation; agricultural soil; environmental pollution; sustainable agri-
culture; toxicity; health effects
Received: 6 May 2021
Accepted: 23 June 2021
Published: 2 July 2021
1. Introduction
Publisher’s Note: MDPI stays neutral Soil pollution is a worldwide problem that draws its origins from anthropologic
with regard to jurisdictional claims in and natural sources. Urbanization, industrialization, and food-demand increases have
published maps and institutional affil- required the use of compounds, substances, and chemical agents, which, over the years,
iations.
have brought on the dispersion and accumulation of pollutants in the environment. The
common pollutants present in the soil are heavy metals, polycyclic aromatic hydrocarbons
(PAHs), or pesticides [1].
Pesticides are chemical compounds used to eliminate pests. They are chemical or
Copyright: © 2021 by the authors. biological agents, that weaken, incapacitate, and kill pests. Based on the types of targeted
Licensee MDPI, Basel, Switzerland. pests, the pesticides can be divided into several groups, namely insecticides, herbicides,
This article is an open access article rodenticides, bactericides, fungicides, and larvicides.
distributed under the terms and During the 19th and 20th centuries, the extracts from plants, namely pyrethrins, were
conditions of the Creative Commons
used as insecticides, fungicides, and herbicides. The increase in pesticide use happened
Attribution (CC BY) license (https://
with synthetic chemistry during the 1930s. In this period, inorganic chemicals such as
creativecommons.org/licenses/by/
arsenic and sulfur compounds were applied for crop protection. The arsenic poison was
4.0/).
Bioengineering 2021, 8, 92. https://doi.org/10.3390/bioengineering8070092 https://www.mdpi.com/journal/bioengineering

Bioengineering 2021, 8, x FOR PEER REVIEW 2 of 29
Bioengineering 2021, 8, 92 2 of 29
with synthetic chemistry during the 1930s. In this period, inorganic chemicals such as ar-
with
senicsynthetic
and sulfur chemistry
compoundsduringwerethe 1930s.
applied In for
thiscrop
period, inorganicThe
protection. chemicals
arsenic such poisonas ar-
was
senic
fatal and
to sulfur
insects, compounds
while the sulfurwerewas applied
used as for
a crop protection.
fungicide. At the The arsenic
beginning
fatal to insects, while the sulfur was used as a fungicide. At the beginning of the Second of poison
the was
Second
World
fatal
Worldto War,
War,numerous
insects, while the
numerous pesticides
sulfur was
pesticides wereused
were synthesized,
as a fungicide.
synthesized, mainly
mainly organic
At the chemicals,
beginning
organic chemicals,of the such asas
Second
such di-
dichlorodiphenyltrichloroethane
World War, numerous pesticides(DDT),
chlorodiphenyltrichloroethane (DDT),
were aldrin,and
synthesized,
aldrin, andmainly
dieldrin
dieldrin usedas
organic
used asinsecticides,
insecticides,
chemicals, while
suchwhile
as di-2-
2-methyl-4-chlorophenoxyacetic
chlorodiphenyltrichloroethane
methyl-4-chlorophenoxyacetic(DDT), acid (MCPA)
acid (MCPA)
aldrin, andand 2,4-dichlorophenoxyacetic
dieldrin used as insecticides,
2,4-dichlorophenoxyacetic acid (2,4-D)
while
acid 2-
(2,4-D)
were used as herbicides
methyl-4-chlorophenoxyacetic
were used as herbicides [2]. [2]. acid (MCPA) and 2,4-dichlorophenoxyacetic acid (2,4-D)
were After
used
Afteras 1945, there
therewas
herbicides
1945, [2].a arapid
was rapiddevelopment
developmentofofthe theagrochemical
agrochemicalfield, field,characterized
characterized
by the
by the introduction
After 1945, there of
introduction of many
wasmany insecticides,
a rapid development
insecticides, fungicides, herbicides,
of the herbicides,
fungicides, agrochemicaland other
andfield,
other chemicals,
chemicals,toto
characterized
control
bycontrol pests
the introduction and ensure
pests and ensureof manythe yields of
theinsecticides, agricultural production.
fungicides,production.
yields of agricultural Moreover,
herbicides, and pesticides
pesticidesare
other chemicals,
Moreover, to
are
applied
control in
pestsaquaculture,
and ensure horticulture,
the yields and
of for various
agricultural general
production.household
applied in aquaculture, horticulture, and for various general household applications. Moreover,applications.
pesticides They
are
are alsoare
applied
They used
in also toused
control
aquaculture, vector-borne
horticulture,
to control diseases
vector-borneand for (e.g., malaria
various
diseases and dengue)
general
(e.g., malariahousehold [3]. applications.
and dengue) [3].
TheyFromare 1990 to 2018, there have been registered amounts
From 1990 to 2018, there have been registered amounts of used pesticides[3].
also used to control vector-borne diseases (e.g., malaria of used
and pesticides
dengue) by allbycoun-
all
countries
triesFrom
in thein the
1990 world,
to 2018,
world, especially
there have
especially in Asia
been and
in Asia and
registeredAmerica.
America.amounts The world average
of usedaverage
The world pesticides quantity
by all coun-
quantity has
has in-
increased from 1.55 kg·ha−1 −1 in 1990 to 2.63 kg·ha−1 in 2018, as shown in Figure 1. Looking
tries in the
creased fromworld,
1.55 especially
kg·ha in 1990 in Asia and kg·ha
to 2.63 America. The world
−1 in 2018, as shownaverage quantity
in Figure has in-at
1. Looking
at the types,
creased from fungicides
1.55 kg·haandand
−1 bactericides
inbactericides
1990 to 2.63are are used
kg·ha −1 inmore
2018, than the others
as shown (Figure
in Figure 2).
1. 2).
Looking at
the types, fungicides used more than the others (Figure
the types, fungicides and bactericides are used more than the others (Figure 2).
Figure 1. Pesticides use per area of cropland (data from [4]).

Figure 2. Pesticides use from 1990 to 2016 (data from [4]).

Figure
Figure 2.
2. Pesticides
Pesticides use
use from
from 1990
1990 to
to 2016
2016 (data
(data from
from [4]).
[4]).
There has been no decrease even over the years, and directives have been imple-
There
mented has
Thereinhas
manybeen
been nodecrease
no decrease
countries even
even
around over
over
the the the
world to years,
years, and directives
and directives
reduce the use ofhave haveimplemented
been
pesticides, been imple-
for example,
mented
inthe
many incountries
many countries
Regulation around
(EC) around [5]the
the world
1107/2009 of world
to to reduce
thereduce the use
European theofuse
Union of pesticides,
pesticides,
or the forConvention
example,
for example,
Stockholm the
the
[6],Regulation
Regulation
which (EC) (EC)
focuses 1107/2009
1107/2009
on [5] [5] of
of the
eliminating orthe European
European
reducing Union
Union
of ororganic
or the
persistent the Stockholm
Stockholm Convention
Convention
pollutants (POPs).[6],
To
[6],
whichwhich focuses
focuses on eliminating
on eliminating or reducing
or reducing of persistent
of persistent organic
organic pollutants
pollutants (POPs).
(POPs). To
To this
purpose, the governments have to take measures to eliminate or reduce the release of POPs
into the environment.
When pesticides are used, a part of them remains in the soil, and the accumulation
affects the microorganisms living there. Human exposure can occur through the ingestion
of pesticide-contaminated water and food, the inhalation of pesticide-contaminated air,
and directly from occupational, agricultural, and household use. The pesticides can enter
the human body by dermal, oral, eye, and respiratory pathways [7]. The toxicity of
pesticides depends on the electronic properties and the structure of the molecule, dosage,
and exposure times [8,9].
For these reasons, the residual pesticide concentration present in the soil must be
reduced, and effective remediation techniques must be used to do this. An ecofriendly,
cost-effective, rather efficient method is bioremediation, which is an alternative to more
expensive and toxic approaches, such as chemical and physical methods. In biodegradation,
the removal can be achieved by exploiting the microbial activity of microorganisms. The
microorganisms, primarily bacteria [10], or fungi [11] transform pesticides into less complex
compounds, CO2 , water, oxides, or mineral salts, which can be used as carbon, mineral,
and energy source. In these reactions, the enzymes have an important role since they act as
catalysts [12].
Several techniques are available for the biodegradation of pesticides, which could
develop in aerobic or anaerobic conditions based on types of microorganisms. Moreover,
the bioremediation techniques can be divided into three categories depending on where
the remediation treatment is done, namely in situ, ex situ, or on-site.
In the in situ approach, the treatment is involved in the contaminated zone, and usually,
the process is aerobic. The main in situ techniques are natural attenuation, bioaugmenta-
tion, biostimulation, bioventing, and biosparging. In the ex situ methods, the contaminated
soil is removed from polluted sites and transported to other places for treatment. Bioreac-
tors, composting, landfarming, and biopiles are ex situ treatments. The on-site approach
consists of the treatment of polluted soil on the surrounding site, to say the soil is removed
from its original position but cleaned up in the neighborhood without any impact due to
its transport.
In the literature, several reviews on pesticides have been published in the past years.
Each of them is mainly focused on one topic. However, by this approach, the knowl-
edge of the pesticide sector and its problems is lacking. Table 1 reports a shortlist of
these publications.
Table 1. Reviews on pesticides.
Topic References
Pesticide diffusion in the environment [13,14]
Toxic effects on living organisms [13,15,16]
Legislation [14]
Physical techniques for pesticide degradation [17,18]
Chemical techniques for pesticide degradation [16–18]
Biological techniques for pesticide degradation [17–22]
Microorganisms capable of degrading pesticides [13,19,21–23]
Enzymatic degradation [24]
Economic analysis [17]
Degradation of organochlorine pesticides [14,16]
Degradation of herbicides. [13]
Monitoring of pesticide clean-up [20]
The current review aims to give an overview of the bioremediation of soils polluted
with commercial pesticides, considering the features that characterize the main and most
used ones, namely, their classification and their toxicological issues, together with some
elements of legislation into force around the world.
Bioengineering 2021, 8, 92 4 of 29 4 of 29
Bioengineering 2. Classification
2021, 8, x FOR PEER REVIEW of Pesticides
2. Classification of Pesticides
The pesticides
2. Classification can be classified by different criteria such as chemical classes, func-
of Pesticides
2. Classification
tionalThe pesticides
groups, of Pesticides
mode can be classified
of action, by different criteria such as chemical classes, func-
and toxicity.
The pesticides can be classified by different criteria such as chemical classes, func-
tional groups,
2.The modeof
2. Classification
Classification
pesticides ofPesticides
can action,
be and toxicity.
ofclassified
Pesticides by different criteria such as chemical classes, func-
tional groups, mode of action, and toxicity.
tional groups,
2.1. Classification mode
The pesticides
The of action,
bypesticides
Origin
can canandbe toxicity.
be classified by different
classified by criteria
different such as chemical
criteria such asclasses,
chemical functional
classes, func-
2.1. groups,
Classification
mode
tional by
of Origin
action,
groups, modeand toxicity.
of action, and toxicity.
The pesticides
2.1. Classification can be classified by their origin, namely chemical pesticides and bi-
by Origin
2.1. Classification
The pesticides
opesticides. by Origin
Chemical canpesticides
be classified are by their origin,
generally organic namely
compoundschemical thatpesticides
can have and naturalbi-
The
2.1. pesticides
Classification
2.1.Chemical can
by bebyclassified
Origin
Classification Origin by their origin, namely chemical pesticides and bi-
opesticides.
The
sources pesticides
or by can
chemical pesticides
be
synthesis are
classified generally
by
[7]. their organic
origin,
Biopesticides compounds
namely
are chemical
natural that
substances can have
pesticides
that natural
and
controlbi-
opesticides.
The Chemicalcan
pesticides pesticides
be are generally
classified by their organic
origin, namelycompounds
chemical that can have
pesticides and natural
biopes-
sources
pests byor
opesticides. by The
Chemical
nontoxic pesticides
chemical can
synthesis
pesticides
mechanisms be
are
[25]. classified
[7].generally by their
Biopesticides
organic origin,
arecompoundsnamely chemical
natural substances
that can have pesticides
that control
natural and bi-
sources or
ticides. by chemical
Chemical synthesis
pesticides are [7]. Biopesticides
generally organic are natural
compounds that substances
can have natural thatsources
control
pests
sources by or opesticides.
nontoxic Chemical
mechanisms
by chemical synthesispesticides are generally organic compounds
[25].[7]. Biopesticides are natural substances that control that can have natural
pestsorbybynontoxic
chemical
sources or mechanisms
synthesis
by Chemical[7].
chemical [25].
Biopesticides
synthesis are natural substances that control
[7]. Biopesticides are natural substances that control pests by
pests
2.1.1. by nontoxic
Classification
nontoxic mechanisms
mechanisms by [25]. [25].
Composition
pests
2.1.1. Classification by nontoxic
by Chemicalmechanisms [25].
Composition
2.1.1. With this classification,
Classification by Chemical fourComposition
main groups can be identified: organochlorines, organ-
2.1.1. Classification
2.1.1.
With Classification
ophosphates, byby
this carbamates, Chemical
classification, Chemical
andfour Composition
Composition
main
pyrethrins groups can be identified:
and pyrethroids (Figure organochlorines,
3 and Table 2). organ- The in-
With2.1.1. Classification by
this classification, fourChemical Composition
main groups can be identified: organochlorines, organ-
ophosphates,
WithWiththis carbamates,
this
classification,
formation on carbamates,
the chemicaland and
classification, pyrethrins
four
four main
main
andpyrethrins and
groups
groups pyrethroids
can
can
physical characteristics be identified:
be (Figure
identified: 3 and
organochlorines,
of (Figure
pesticides Table
organochlorines,
is very 2). The
organophos-
useful organ-in-
in de-
ophosphates, With this classification, and pyrethroids
four main groups can be 3 and
identified: Table 2). The
organochlorines, in-
organ-
formation
phates, on
ophosphates,
termining the the
carbamates,chemical
carbamates,
mode ofand andpyrethrins
and
application, physical
pyrethrins characteristics
and pyrethroids
and
precautions (Figure
pyrethroids
that need of pesticides
3(Figure
toand
be Table
3
taken is2).
and very
The useful
Table
during information
2).
the in de-
The
applica-in-
formationophosphates,
on the chemical and physical
carbamates, characteristics
and pyrethrins of pesticides
and pyrethroids is very
(Figure useful
3 and Tablein2).de-The in-
onand
termining
formationthe the
chemical
the mode and
on application
the of physical
chemicalapplication, characteristics
and[26]. precautions
physical of pesticides
that need
characteristics ofistovery usefulisduring
be taken
pesticides invery
determining inthe
the applica-
tion,
termining
mode of
the mode
formation
application,
of the
on rates
application,
chemical
precautions
precautions
and
that
physical
need to
that need
characteristics
be taken
to
during
beoftaken during
pesticides
the
is useful
application,
theand
very applica-
usefulde-in de-
the
tion, and
termining the application
theapplication
modethe rates [26].
of application, precautions that need
tion, and thetermining
rates [26].moderatesof[26].
application, precautions thattoneed
be taken during
to be taken the applica-
during the applica-
tion,application
and the application rates [26].
tion, and the application rates [26]. E.g.: DDT, DDD,
Organochlorines E.g.: DDT, aldrin
DDD,
Organochlorines dieldrin,
E.g.: DDT, DDD,
Organochlorines E.g.: DDT,
dieldrin,E.g.: DDD,
aldrin
DDT, DDD,
Organochlorines dieldrin,
Organochlorines E.g.: HETP, aldrin
dieldrin, aldrin
dieldrin, aldrin
Organophosphates E.g.: HETP,
parathion,
E.g.: HETP,
Organophosphates parathion,
chlorpyrifos
E.g.: HETP,
E.g.: HETP,
Chemical pesticides Organophosphates parathion,
Organophosphates chlorpyrifos
Organophosphates parathion,
chlorpyrifos parathion,
Chemical pesticides E.g.: furadan,
chlorpyrifos
Chemical pesticides Carbamates chlorpyrifos
Chemical Chemical
pesticidespesticides Carbamates E.g.: fenobucarb
sevin, furadan,
E.g.:fenobucarb
furadan,
Carbamates sevin, E.g.: furadan,
E.g.:fenobucarb
furadan,
Carbamates Carbamates sevin, sevin, fenobucarb
Pyrethrin and sevin,
E.g.: fenobucarb
cyfluthrin,
Pyrethrin
pyrethroids and E.g.: cyfluthrin,
bifenthrin, allethrin
Pyrethrin and
Pyrethrin and E.g.: cyfluthrin,
bifenthrin, E.g.: cyfluthrin,
allethrin
pyrethroids
Pyrethrin and E.g.: cyfluthrin,
pyrethroids pyrethroids bifenthrin, allethrin
bifenthrin,
bifenthrin, allethrin
allethrin
Figure 3. Classification of the chemical pesticides. DDT: pyrethroids
dichlorodiphenyltrichloroethane; DDD: dichlorodiphenyldi-
Figure 3. Classification of the chemical pesticides.HETP:
chloroethane; DDT: dichlorodiphenyltrichloroethane;
hexaethyl tetraphosphate. DDD: dichlorodiphenyldi-
Figure 3. Classification of the Figure
chemical
Figure 3. Classification pesticides. DDT:
of3.theClassification dichlorodiphenyltrichloroethane;
chemical pesticides.
of the DDD: dichlorodiphenyldi-
DDT: dichlorodiphenyltrichloroethane;
chemical pesticides. DDT: DDD: dichlorodiphenyldi-
dichlorodiphenyltrichloroethane;
chloroethane;
Figure 3. Classification of the chemical pesticides.
chloroethane;
HETP:
DDT: hexaethyl
chloroethane;
tetraphosphate.
dichlorodiphenyltrichloroethane;
HETP: hexaethyl
HETP: tetraphosphate.
hexaethyl tetraphosphate. DDD: dichlorodiphenyldi- DDD:
dichlorodiphenyldichloroethane;
Table 2. Chemical
chloroethane; composition HETP:
of the
HETP: hexaethyl hexaethyl tetraphosphate.
pesticides.
tetraphosphate.
Table 2. Chemical composition of the pesticides.
Table
Table 2. Chemical 2. composition
GroupChemical composition of the pesticides. Chemical Structure
of the pesticides.
TableTable 2. Chemical
2. Chemical composition
composition ofofthe
thepesticides.
pesticides.
Group Chemical Structure
Group Group
Organochlorines Chemical Chemical Structure
Structure
Group
Group Chemical Structure
Chemical Structure
Organochlorines
Organochlorines
Organochlorines
Organochlorines
Organochlorines
Organophasphates
Organophasphates
Organophasphates
Organophasphates
Organophasphates
Organophasphates
Carbamates
Carbamates
Carbamates
Carbamates
Carbamates
Carbamates
Pyrethrins and
Pyrethrins pyrethroids
and pyrethroids
Pyrethrins and pyrethroids
Organochlorines
Organochlorine pesticides (OCs) are organic compounds, namely hydrocarbon chains
bonded with at least one covalently bonded atom of chlorine (Table 2).
These compounds are widely used in agriculture, especially as insecticides to con-
trol a broad range of insects. The most common organochlorines are dichlorodiphenyl-
trichloroethane (DDT), dichlorodiphenyldichloroethane (DDD), dicofol, dieldrin, lindane,
aldrin, chlordane, endosulfan, isodrin, isobenzan, toxaphene, and chloropropylate [27].
These compounds are lipophilic and are difficult to decompose, thus tending to
bioaccumulate in tissues and remaining in the environment. For their high persistence in
the environment, OCs belong to the class of persistent organic pollutants (POPs). They
may cause damage to living beings, causing mutagenic effects, histopathological effects,
enzyme-inducing and/or enzyme-inhibiting, carcinogenicity, and teratogenicity [28].
For human health, organochlorine exposure may increase the risk of breast cancer [29,30].
Organophosphates
Organophosphates (OPs) are synthetic pesticides, which include phosphoric acid
esters or thiophosphoric acid esters. The general structure is reported in Table 2.
Hexaethyl tetraphosphate (HETP) was the first one synthesized and used as agricul-
tural insecticides. OPs are acutely toxic for insects and other animals, including birds,
amphibians, and mammals. The cause of their toxicity is due to inhibition of the acetyl-
cholinesterase (AChE) in the central and peripheral nervous system [31,32].
The inhibition of this enzyme causes muscarinic and nicotinic effects. Muscarinic
symptoms are linked to the assumption system:
• for inhalation, the symptoms may be cough, expectoration of frothy secretions, chest
tightness, and wheeze, pulmonary edema;
• for ingestion hypersalivation, nausea, vomiting, abdominal cramps, diarrhea, and
tenesmus;
• for eye, miosis, blurred vision, and eye pain.
Nicotinic effects are profuse sweating, fasciculation, progressive flaccidity, and weak-
ness of proximal muscle groups, such as the neck flexors, then the extraocular muscles and
muscles of respiration [33].
Carbamates
Carbamates are compounds derived from carbamic acid. Their chemical structure is
characterized by an amino group bonded with an ester group, as shown in Table 2.
Typically, R1 and R2 are organic radicals or hydrogen. If R2 is hydrogen, it is possible
to understand the target considering the functional group R1 [34]. It is possible to have:
• insecticides, when R1 is a methyl group;
• herbicides, when R1 is an aromatic group;
• fungicides, when R1 is a benzimidazole moiety.
Carbamates are also biocides for industry and household products for the control
of household pests [35]. The common carbamate pesticides are aldicarb, carbofuran,
fenoxycarb, carbaryl, ethienocarb, and fenobucarb [36].
As the organophosphates, carbamates are inhibitors of acetylcholinesterase activity,
and therefore, their toxicity acts on the neurological system [37]. Exposure to carbamate
pesticides increases the risk of non-Hodgkin’s lymphoma in humans since they inhibit
and induce apoptosis of human natural killer (NK) cells and cytotoxic T lymphocytes that
provide defense against tumors [38].
Pyrethrins and Pyrethroids

Pyrethrins are natural insecticides, in which active principle comes from the flowers of
Tanacetum cinerariaefolium, also called Chrysanthemum cinerariaefolium or Pyrethrum cinerari-
aefolium. Their active constituents are esters of 2,2-dimethyl-3-(2-methyl-l-propenyl)-l-
Pyrethrins and Pyrethroids
Pyrethrins are natural insecticides, in which active principle comes from the flowers
of Tanacetum cinerariaefolium, also called Chrysanthemum cinerariaefolium or Pyrethrum cin-
erariaefolium. Their active constituents are esters of 2,2-dimethyl-3-(2-methyl-l-propenyl)-
l-cyclopropanecarboxylic acid (chrysanthemic acid) and of 3-(2-methoxycarbonyl-l-pro-
penyl)-2,2-dimethyl-l-cyclopropanecarboxylic
cyclopropanecarboxylic acid
acid (chrysanthemic acid) and(pyrethric acid). Six types were iden-
of 3-(2-methoxycarbonyl-l-propenyl)-
tified, as shown in Table 2.
2,2-dimethyl-l-cyclopropanecarboxylic acid (pyrethric acid). Six types were identified, as
shown Pyrethroids
in Table 2. are synthetic compounds that are obtained by modifying the chrysan-
themic acid moiety
Pyrethroids areofsynthetic
pyrethrin I and esterifying
compounds the
that are alcohols.byThey
obtained can be the
modifying divided into
chrysan-
themic
[39]: acid moiety of pyrethrin I and esterifying the alcohols. They can be divided into [39]:
• First-generation pyrethroids:
pyrethroids: esters of chrysanthemic acid and one one alcohol,
alcohol, having
having aa
furan ring and terminal side chain moieties.
terminal side chain moieties.
•• Second-generation pyrethroids: they have 3-phenoxybenzyl 3-phenoxybenzyl alcoholsalcohols derivatives
derivatives in in
the alcohol
alcohol moiety
moietyand andhavehavesome
someofofthetheterminal
terminalsidesidechain
chainmoieties
moietiesreplaced
replaced with
witha
dichlorovinyl
a dichlorovinyl oror
dibromovinyl
dibromovinyl substitute
substitute and
and aromatic
aromatic rings.
rings.
Pyrethroids
Pyrethroids are are synthesized
synthesizedto toincrease
increasethe theinsecticidal
insecticidalpower
powerandanddecrease
decreasethethesensi-
sen-
tivity toto
sitivity airair
andandlight,
light,compared
compared toto
the pyrethrins.
the pyrethrins.
Generally,
Generally, in in the
the air,
air, the
the pyrethrins
pyrethrins and
and many
many pyrethroids
pyrethroids are are rapidly
rapidly degraded
degraded by by
sunlight, while they remain for a long time in the soil as they
sunlight, while they remain for a long time in the soil as they bind strongly to bind strongly to it
it [40].
[40].
Pyrethrins
Pyrethrins andand pyrethroids
pyrethroids may may bebe found
found on on leaves,
leaves, fruits,
fruits, and
and vegetables
vegetables since
since they
they are
are
sprayed directly onto crops and plants
sprayed directly onto crops and plants [41]. [41].
The
The pyrethrins
pyrethrins and and pyrethroids
pyrethroids disrupt
disrupt thethe sodium
sodium channels
channels in in the
the axons
axons damaging
damaging
the neurologic system [42]. They are toxic for insects but less harmful
the neurologic system [42]. They are toxic for insects but less harmful to humans. to humans. However,
How-
it was noted that the exposure of these pesticides can have respiratory
ever, it was noted that the exposure of these pesticides can have respiratory effects effects such as
such
cough or upper respiratory irritation after inhalation of dust or aerosol
as cough or upper respiratory irritation after inhalation of dust or aerosol droplets; neu- droplets; neuro-
logical
rologicaleffects
effectssuch
such asasheadache
headacheorordizziness;
dizziness;gastrointestinal
gastrointestinaleffects
effectssuch
suchasasnausea
nausea andand
vomiting; and irritation and/or dermal effects [43]. Pyrethroids may
vomiting; and irritation and/or dermal effects [43]. Pyrethroids may cause cardiovascularcause cardiovascular
problems [44].
problems [44].
2.1.2. Biopesticides
2.1.2. Biopesticides
Biopesticides are pesticides derived from nature (animals, plants, microorganisms,
Biopesticides
and minerals). arecan
They pesticides derived
be divided frommajor
into three natureclasses
(animals, plants,
(Figure microorganisms,
4) based on the type
of active ingredient used, namely, biochemical, plant-incorporated protectants on
and minerals). They can be divided into three major classes (Figure 4) based the type
(PIPs), and
of active ingredient
microbial pesticides.used, namely, biochemical, plant-incorporated protectants (PIPs), and
microbial pesticides.
Biochemical pesticides
Plant incorporated
Biopesticides
protectants (PIPs)
Microbial pesticides
Figure 4.
Figure 4. Classification
Classification of
of biopesticides.
biopesticides.
Biochemical
Biochemical Pesticides
Pesticides
They
They are natural
are natural compounds
compounds thatthat control
control pests
pests by
by nontoxic
nontoxic mechanisms.
mechanisms. They
They can
can
be
be extracted
extracted from
from natural
natural sources
sources or
or synthesized
synthesized to
to have
have the
the same
same structure
structure and
and function
function
as the natural ones [45]. Semiochemicals are chemical compounds emitted by plants
or animals. Pheromones, allomones, kairomones, and attractants are examples of these
compounds. They are connected to the vital functions, such as feeding, mating, and
egg-laying (ovipositing) of the pests [46]. Therefore, acting on their concentration can be
exploited to influence the pest life cycle.
as the natural ones [45]. Semiochemicals are chemical compounds emitted by plant
animals. Pheromones,
as the natural ones [45]. allomones, kairomones,
Semiochemicals and attractants
are chemical compounds are examples
emittedofbythese c
plant
pounds.
animals.They are connected
Pheromones, to the kairomones,
allomones, vital functions, and such as feeding,
attractants are mating,
examples and
of egg-lay
these c
(ovipositing)
pounds. Theyofare the pests [46].toTherefore,
connected acting onsuch
the vital functions, theirasconcentration
feeding, mating, can and
be exploite
egg-la
influence
(ovipositing) the pest
of thelife cycle.
pests [46]. Therefore, acting on their concentration can be exploite
influence the pest life cycle.
Plant-Incorporated Protectants
Plant-Incorporated
The plant-incorporated Protectants protectants (PIPs) can be produced by the plants themse
Plant-Incorporated
whenThe Protectants
the pest feeds on them.
plant-incorporated protectants To force their production,
(PIPs) the plantsby
can be produced can
thebeplants
genetically
themse m
ified introducing
The plant-incorporated
when the pest feeds the gene
protectants acting
on them.(PIPs) on a specific
cantheir
To force be produced pesticidal
production, by the protein
theplants into the
plantsthemselves genetic mate
can be genetically m
when the pest of the
ifiedfeedsplant
on itself.
them.the
introducing InTothis way,
force
gene theon
their
acting plant can synthesize
production,
a specific the plants
pesticidal the toxic
can
protein compounds
beinto
genetically
the geneticfor mat
sele
pests
of the[47].
modified introducing plant the geneInacting
itself. this way, on athe specific
plant canpesticidal
synthesize protein into compounds
the toxic the genetic for sele
material of thepestsplant itself. In this way, the plant can synthesize the toxic compounds for
[47].
selected pests Microbial
[47]. Pesticides
Microbial
MicrobialPesticides
pesticides include living organisms, such as bacteria, fungi, algae, and
Microbial Pesticides
ruses,Microbial
that control the pests.
pesticides Theyliving
include suppress pests either
organisms, suchproducing
as bacteria,toxicfungi,metabolites
algae, and
Microbialcausepesticides
damage include
and living
diseases ororganisms,
preventing such
the as bacteria,
establishment
ruses, that control the pests. They suppress pests either producing toxic metabolites fungi,
of otheralgae, and
microorganisms
viruses, that cause
controldamage
the pests.andTheydiseasessuppress pests either
or preventing theproducing
establishment toxicof metabolites that
other microorganisms
cause damage and diseases or preventing
2.2. Classification by Targets the establishment of other microorganisms [48].
2.2. Classification
Pesticides by Targets
2.2. Classification by Targets can be classified by the roles that they play and the types of pests that t
attack. The main
Pesticides canclasses
beby are insecticides,
classified herbicides, rodenticides, bactericides, and fu
Pesticides can be classified the rolesbythat the they
roles that they
play and play and the
the types of types
pests of pests
that that
cides.
attack. Theclasses
main classes are insecticides, herbicides, rodenticides, bactericides,
they attack. The main are insecticides, herbicides, rodenticides, bactericides, and and fu
cides. Based on their chemical structure, they may interact in a different way with pests
fungicides.
with Based
differenton toxicity.
their chemical structure, they may interact in a different way with pests
Based on their chemical structure, they may interact in a different way with pests and
with different
with different toxicity. toxicity.
2.2.1. Insecticides
2.2.1.Insecticides
2.2.1. Insecticides Insecticidesare chemical and biological compounds that attack and kill insects.
vicides
Insecticides are are specific
Insecticides
chemical are
and insecticides
chemical
biologicaland that target the
biological
compounds larval
compounds
that attacklifeandstage
killof
that an insect.
attack and
insects. kill insects.
Larvi-
vicidesTheseare compounds
specific are
insecticides used in
that agriculture,
target
cides are specific insecticides that target the larval life stage of an insect. the horticulture,
larval life stage forestry,
of an and
insect. gardening
are
These compoundsalso used
Theseare to
compoundscontrol vectors,
are used in
used in agriculture, such as mosquitoes
agriculture,forestry,
horticulture, and
horticulture, ticks, which
forestry,but
and gardening are
andare involve
gardening
spreading
are alsovectors,
also used to control human
used to such and
control animal diseases,
vectors, such
as mosquitoes such as
as mosquitoes
and ticks, dengue [49] and malaria
and ticks,in which
which are involved [50].
spreadingare involve
human and animal The
spreading most-used
human
diseases, suchandinsecticides
asanimal
dengue belong
diseases,
[49] tomalaria
andsuch theasclasses
[50]. of[49]
dengue organophosphates,
and malaria [50].pyrethro
and carbamates.
The most-used Theinsecticides
most-used They act ontothe
insecticides
belong nervous
thebelong
classestoofsystem
the of theofvictims,
classes
organophosphates, causing spasms,
organophosphates,
pyrethroids, resp
pyrethro
and carbamates.tory failure,
They and/or
act on death.
the nervousIn Table
system3, several
of the insecticides
victims,
and carbamates. They act on the nervous system of the victims, causing spasms, resp used
causing in agricultural
spasms, respi- soil are s
ratory failure,marized.
toryand/or
failure, death.
and/or Indeath.
Table 3, In several
Table 3,insecticides used in used
several insecticides agricultural soil aresoil are s
in agricultural
summarized.marized.
Table 3. Classification of the most common insecticides used in agricultural soil.
Table 3. Classification of
Table 3.Classthe most common
Classification of insecticides
the most common used in agricultural
insecticides soil.
used in agricultural soil.
Name Pesticide Chemical Structure Mode of Action
Name Name Pesticide Class
Pesticide Class Chemical Structure
Chemical Structure Mode of Action
Mode of Action
Interaction with sodium ion channels in neurons, ca

Interaction with sodium ion channels in
DDT Organochlorine ing their inactivation,
Interaction which channels
leads to spasms and ev
neurons,with sodium
causing theirion
inactivation,in neurons, ca
DDT DDT Organochlorine
Organochlorine ingwhich
their inactivation, tual
which death.
leads to spasms andleads to spasms and ev
eventual
tual death.
death.
Interference with nerve signaling by

Bioengineering 2021, 8, x FOR PEER REVIEW Interference with nerve signaling by inhibition of8t
Cyfluthrin Cyfluthrin Pyrethroid
Pyrethroid inhibition of the membrane sodium
membrane
Interference sodium
with nerve channel
signaling bysystems.
inhibition of
Cyfluthrin Pyrethroid channel systems.
membrane sodium channel systems.
Interruption of functioning of the

Interruption of functioning of the nervous system, in
Tefluthrin Tefluthrin Pyrethroid
Pyrethroid nervous system, interfering with
fering with
sodium sodium channels.
channels.
Inhibition of cholinesterase prevents the breakdown

Aldicarb Carbamate acetylcholine in the synapse. It leads to respiratory
ure.
Interference with nerve signaling by inhibition of t

λ-cyhalothrin Pyrethroid
Bioengineering 2021, 8, x FOR PEER REVIEW 8
Interruption of functioning of the nervous system, in
Tefluthrin Pyrethroid
Interruption of functioning
fering with sodium of thechannels.
nervous system, in
Tefluthrin Pyrethroid Interruption offering functioning of the nervous system, in
Tefluthrin
Bioengineering 2021, 8, 92 Pyrethroid Interruptionofoffunctioning with
functioningofofthesodium channels.
thenervous 8 of 29system,
nervous system,inin
Tefluthrin Pyrethroid Interruption fering with sodium channels.
Tefluthrin Pyrethroid Interruption of functioning
fering withsodium of the channels.
sodium nervous system, in
Tefluthrin Pyrethroid fering with channels.
Interruption of functioning
fering with sodium of thechannels.
nervous system, in
Tefluthrin Pyrethroid Inhibition ofof
Interruption cholinesterase
functioning prevents
of thechannels.
nervousthe breakdown
system, in
Tefluthrin Pyrethroid fering with sodium
Aldicarb Carbamate Table 3. Cont. Inhibition of fering
acetylcholine cholinesterase
in the with synapse.sodiumprevents
It leads the
to
channels. breakdowf
respiratory
Aldicarb Carbamate Inhibition
acetylcholine of cholinesterase
in the synapse. prevents
ure. It leadsthe breakdown
to respiratory
Inhibition
Inhibition ofofcholinesterase
cholinesterase prevents
prevents the
the breakdown
breakdown
Name AldicarbAldicarb
Carbamate
Pesticide Class
Carbamate Chemical Structure acetylcholine
Inhibition of Mode
acetylcholine
in the synapse.
of
cholinesterase Actionure.It leads
prevents to respiratory
therespiratory
breakdown f
Aldicarb Carbamate acetylcholine ininthe thesynapse.
synapse.
ure. ItItleads
leadstoto respiratory fa
Aldicarb Carbamate Inhibition of cholinesterase
acetylcholine in the synapse. prevents
It leads to therespiratory
breakdownf
Inhibition of cholinesterase ure.
ure. prevents therespiratory
breakdown
Aldicarb Carbamate Inhibition
acetylcholine of
in cholinesterase
the synapse. ure. It prevents
leads to f
Aldicarb Aldicarb Carbamate
Carbamate the breakdown
acetylcholine
Interference in the
with of acetylcholine
synapse.
nerve It
signaling
ure. leads in
by the
to respiratory
inhibition of t
λ-cyhalothrin Pyrethroid synapse. It leads tosodium
respiratory failure.
Interference
membranewith nerve ure.channel
signaling bysystems.
inhibition of t
λ-cyhalothrin Pyrethroid Interference with nerve signaling by inhibition of th
λ-cyhalothrin Pyrethroid membrane
Interferencewith withnerve sodium
nervesignaling channel
signalingby systems.
byinhibition
inhibitionofoftht
λ-cyhalothrin Pyrethroid Interference membrane sodium channel systems.
λ-cyhalothrin Pyrethroid Interference with nerve
membrane sodium signaling
channel bysystems.
inhibition of t
λ-cyhalothrin Pyrethroid membrane
Interference withsodium channel
nerve signaling systems.
by
Interference with nerve
membrane sodium signaling
channel bysystems.
inhibition of t
λ-cyhalothrin
λ-cyhalothrin Pyrethroid
Pyrethroid inhibition of
Interference with thenerve
membrane signaling sodium bysystems.
inhibition of t
Interference with
membrane sodium
sodium channels
channel disrupts the func
λ-cyhalothrin Pyrethroid channel systems.
Permethrin Pyrethroid Interference
of membrane
neurons and with sodium
causes sodium
muscles channel
channels to spasm, systems.
disrupts the func
culminatin
Permethrin Pyrethroid Interference
of neurons and withcauses sodium
paralysis channels
musclesand to disrupts
spasm,
death. the funct
culminatin
Interference
Interference with
withcauses sodium
sodium channels
channels disrupts
disrupts the func
the funct
Permethrin Pyrethroid of Interference
neurons
Interference andwith with sodium
muscles
paralysis
sodium and
channelschannels
todeath.
spasm,
disrupts culminatin
the func
Permethrin
Permethrin Pyrethroid
Pyrethroid ofofneurons
neurons
disrupts and
and the causes
causes
function muscles
muscles
of toto
neurons spasm,
spasm, culminatin
and culminating
PermethrinPermethrin Pyrethroid
Pyrethroid Interference
of neurons and with paralysis
sodium
causes muscles and
channels death.
to disrupts
spasm, the func
culminatin
causes
Inactivation
Interference muscles paralysis
paralysis
to spasm,
of acetylcholinesterase
with sodium and
and death.
death.
culminating
channels by phosphoryla
disrupts the func
Permethrin Pyrethroid of neurons and causes muscles
paralysis to
and death. spasm, culminatin
Terbufos
Permethrin Organophosphate
Pyrethroid ofInactivation
the inand
hydroxyl
neurons paralysis
group
causes and
of death.
serine
muscles present by phosphoryla
atculminatin
the active
paralysis and to spasm,
death.
Terbufos Organophosphate Inactivation
of Inactivation
the hydroxyl of acetylcholinesterase
of group of of
paralysistheserine
enzyme. by by
present
and death.
acetylcholinesterase phosphorylat
at the active
Inactivation
Inactivation ofofacetylcholinesterase
acetylcholinesterase bybyphosphorylati
phosphoryla
Terbufos Organophosphate of the hydroxyl
phosphorylation
Inactivation group of of
the
ofof serine
the
of acetylcholinesterasehydroxyl
enzyme. present group at the active
by phosphorylat
Terbufos Organophosphate
Terbufos Terbufos Organophosphate
Organophosphate of the hydroxyl
of the hydroxyl group group serine
of serine present
present at the at theactive
actives
Terbufos Organophosphate Inactivation
of the serine of
of hydroxyl group of
atthe
acetylcholinesterase
present ofthe enzyme. sitebyofphosphorylat
activepresent
serine at the active
Inactivation of the enzyme.
of the enzyme. by phosphoryla
Terbufos Organophosphate of the hydroxyl the
group enzyme.
of oftheserine
enzyme. present at the active
Terbufos Organophosphate of the hydroxyl
Disruption of nervousgroup of
theserine
of systems enzyme. bypresent at the active
inactivation of ace
Chlorpyrifos Organophosphate of systems
the enzyme.
Disruption of nervous cholinesterase. by inactivation of ac
Chlorpyrifos Organophosphate Disruption of nervouscholinesterase. systems by inactivation of ace
Chlorpyrifos Organophosphate Disruption
Disruption Disruption
ofofnervousof nervous
nervous systems
systems systems
by by
byinactivation
inactivation ofoface
ace
Chlorpyrifos Chlorpyrifos Organophosphate
Chlorpyrifos Organophosphate
Organophosphate cholinesterase.
Disruption of nervous
inactivation systems by inactivation of ace
of acetylcholinesterase.
cholinesterase.
Chlorpyrifos Organophosphate cholinesterase.
Disruption of nervous systems by inactivation of ace
cholinesterase.
Chlorpyrifos Organophosphate Disruption of nervous systems by inactivation of ac
Chlorpyrifos Organophosphate cholinesterase.
cholinesterase.
Methyl-parathion Organophosphate
Disruption of nervous systems by inactivation of ac
cholinesterase.
Methyl-parathion Organophosphate Disruption of nervous
Disruption of nervous systems by inactivation
systems by of ace
Methyl-parathionOrganophosphate
Methyl-parathion Organophosphate Disruption of nervous cholinesterase.
systems byinactivation
inactivationofoface ace
Methyl-parathion Organophosphate
Organophosphate Disruption of nervous
inactivation of systems by
cholinesterase.
acetylcholinesterase.
Methyl-parathion Disruption of nervous systems
cholinesterase. by inactivation of ace
Methyl-parathion Organophosphate cholinesterase.
cholinesterase.
Methyl-parathion Organophosphate Disruption of nervous systems by inactivation of ac
Methyl-parathion Organophosphate cholinesterase.
cholinesterase.
Dimethoate Organophosphate
DisruptionDisruption of nervous
of nervous systems systems
cholinesterase. by
by inactivation of ac
DimethoateDimethoate Organophosphate
Organophosphate Disruption of nervous systems by inactivation of ace
Dimethoate Organophosphate inactivation of acetylcholinesterase.
cholinesterase.
Disruptionofofnervous
Disruption nervoussystems systemsby byinactivation
Dimethoate
Dimethoate Organophosphate
Organophosphate Disruption of nervous cholinesterase.
systems by inactivation of ace
Dimethoate Organophosphate cholinesterase.
cholinesterase.
cholinesterase.
Dimethoate Organophosphate Disruption of nervous systems by inactivation of ac
Dimethoate Organophosphate cholinesterase.
Disruption cholinesterase.
of nervous systems systemsby inactivation
by of ace
Carbofuran Carbofuran Carbamate
Carbamate
inactivation systems by inactivation of ac
of acetylcholinesterase.
cholinesterase.
Carbofuran Carbamate Disruption of nervouscholinesterase. systems by inactivation of ace
Carbofuran Carbamate Disruptionofofnervous
Disruption nervoussystems systemsby byinactivation
Carbofuran
Carbofuran Carbamate
Carbamate Disruption of nervous cholinesterase.
systems by inactivation of ace
Carbofuran Carbamate cholinesterase.
cholinesterase.
cholinesterase.
Carbofuran Carbamate Disruption of nervous systems by inactivation of ac
Carbofuran 2.2.2. Herbicides
2.2.2. Herbicides
Carbamate cholinesterase.
2.2.2.Herbicides
Herbicidesare used to control and remove undesirable plants and weeds. These c cholinesterase.
Herbicides
2.2.2.are used to control and remove undesirable plants and weeds. These
Herbicides
2.2.2.
pounds
compounds2.2.2.
are Herbicides
Herbicides are used
areapplied
mainly
Herbicides
mainly appliedto control and before
in agriculturalremovesoils,undesirableor plants
beforefarming
during and weeds.
farming toThese
maxim c
2.2.2.
poundsHerbicides
Herbicides
are are in
mainly
agricultural
used to control
applied in
soils,
and remove
agricultural
or
soils,
during
undesirable
before orplantstoand
during
maximize
weeds.to
farming These co
maxim
cropHerbicides
crop productivity. productivity.
Herbicides
Herbicides
are Herbicides
areare
used
used also used are
totocontrol
control also
and
inand used
remove
forest inundesirable
forest management
undesirable
management
remove and plants andand
in suburban in
weeds.
andsuburban
Thesecoc
2.2.2.
pounds
crop
Herbicides
are mainly
Herbicides
productivity. applied
are Herbicides
used in agricultural
to controlare and
also soils,
remove
used in before
undesirable
forest orplants
during
plants
management
and
and
weeds.
farming
andweeds.
in toThese
maxim
These
suburban c
urban
pounds
2.2.2.
urban areas.pounds areas.
are mainly
Herbicides
are mainly applied
applied in
in areagricultural
agricultural soils,
soils, before
before or during
or during farming
farming to maxim
to These
maxim
crop
pounds
urban productivity.
Herbicides areHerbicides
are mainly
areas. used to control
applied in are also
and used
remove
agricultural in forest
soils, management
undesirable
before or plants
during and
and in suburban
weeds.
farming to maximca
crop
The modes
crop ofproductivity.
action depend
productivity.
Herbicides Herbicides
on the
Herbicides
are used to chemical
are
control also
also
and used
used
removeininforest
composition, forest
andmanagement
usually,
management
undesirable they
plants and
and
and ininsuburban
involve
weeds. suburban
These ca
urban
pounds
crop areas.
are mainly
productivity. applied
Herbicides in agricultural
are also used soils, before
in forestplant or during
management farming
anddevel- to maxim
in suburban
urban
a plant enzyme
urban or
pounds areas.
a biological
areas. system.
are mainlyHerbicides In
applied inare this way,
agricultural the regular growth and
crop productivity. also used soils, before
in forest or during and
management farming to maxim
in suburban
opments areurban
injured
crop
areas.
or disrupted,
productivity. causing eventual
Herbicides are also plantindeath
used [51].
forest In Table 4, and
management different
in suburban
urban areas.
herbicides used
urbanin agriculture
areas. soil are reported.
Bioengineering 2021,
Bioengineering 2021, 8,
8, xx FOR
FOR PEER
PEER REVIEW
REVIEW 99 of
of 29
29
Themodes
The
The modesof
modes ofaction
of actiondepend
action dependon
depend onthe
on thechemical
the chemicalcomposition,
chemical composition,and
composition, andusually,
and usually,they
usually, theyinvolve
they involve
involve
a The
The
plant modes
modesof
enzyme orofaction
a action depend
depend
biological on onthe
system. the
Inchemical
chemical
this way,composition,
composition,
the regular and
andusually,
plant usually,they
growth involve
theydevelop-
and involve
aaaments
plant
plant
aplant
The
plant
enzyme
enzyme
enzyme
modes
enzyme
are injured
orofaaaaction
or
oror
injured or a
biological
biological
biological system.
system.
system.
depend
biological
or disrupted, on
system.
disrupted, causing
Inthis
In
In
theIn
thisway,
this way,the
way,
chemical
this
causing eventual way,
theregular
the regularplant
regular
composition,
the
eventual plant regular
plant death
plant
plant
and
plant
death [51].
growth
growth
growth
usually,
growth
[51]. In
In Table
and
and
andthey
and
Table 4,
develop-
develop-
develop-
involve
develop-
4, different
different
ments
ments
aments are
are
plantare injured
enzyme oror or disrupted,
aorbiological causing
system. eventual
Ineventual
this plant
way,plant
the death
regular [51]. In Table 94, different
Bioengineering 2021, 8, 92 ments
herbicidesareinjured
injured
used in disrupted,
disrupted,
agriculture causing
soilcausing
are eventual
reported. plant deathplant
death [51]. growth
[51].InInTable and
Table 4, develop-
4,ofdifferent
29
different
herbicides
herbicides
ments
herbicides are used
used in
in
injured agriculture
agriculture
or soil
soil
disrupted, are
are
causing reported.
reported.
eventual plant death [51]. In Table 4, different
herbicidesusedusedininagriculture
agriculturesoil
soilare
arereported.
reported.
herbicides used in agriculture soil
Table 4. Classification of the most common herbicides are reported.
used in agricultural soil.
Table4.
Table
Table 4.Classification
4. Classificationof
Classification ofthe
of themost
the mostcommon
most commonherbicides
common herbicidesused
herbicides usedin
used inagricultural
in agriculturalsoil.
agricultural soil.
soil.
Table 4. Classification
Classification
Table 4.Pesticide of the of the
most most common
common herbicides
herbicides used in used in agricultural
agricultural soil. soil.
Name Table 4.
Table Class
4. Classification
Classification of
of the Chemical
the most
most common Structure
common herbicides
herbicides used
used in agricultural Mode
in agricultural soil. of Action
soil.
Name
Name
Name Pesticide
Pesticide
Pesticide Class
Class
Class ChemicalStructure
Chemical
Chemical Structure
Structure Mode
Mode
Mode of Action
of Action
Name Pesticide Class Chemical Structure ModeofofActionAction
Name Name
Name Pesticide Class
Pesticide Class
Pesticide Class Chemical
Chemical Structure
Structure
Chemical Structure Mode Modeof Action
of Action
DisruptionMode of Action
of shikimic acid pathway
Disruptionof
Disruption
Disruption ofshikimic
of shikimicacid
shikimic acidpathway
acid pathway
pathway
Glyphosate Organophosphate Disruption
Disruption
through inhibitionof shikimic
of shikimic acid pathway
acid
of the enzyme 5-enolpy-
Glyphosate
Glyphosate
Glyphosate Organophosphate
Organophosphate
Organophosphate through
through
through inhibition
inhibition
Disruption
inhibition of
of
of the
the
of shikimic
shikimic enzyme
enzyme
acid 5-enolpy-
5-enolpy-
pathway
Glyphosate Organophosphate Disruption
pathway
through throughof
inhibition ofthe
theenzyme
inhibition
ruvylshikimate-3-phosphate acid
enzyme 5-enolpy-
of pathway
the 5-enolpy-
synthase.
Glyphosate
Glyphosate
Glyphosate Organophosphate
Organophosphate
Organophosphate ruvylshikimate-3-phosphate
ruvylshikimate-3-phosphate
through inhibition of of the
enzyme
through the enzyme
5-enolpyruvylshikimate-3-
inhibition enzyme synthase.
synthase.
5-enolpy-
synthase.
5-enolpy-
ruvylshikimate-3-phosphate synthase.
phosphate
ruvylshikimate-3-phosphate synthase.
synthase.
synthase.
Inhibition of the photosynthetic pathway,
Atrazine Organochlorine Inhibitionof
Inhibition
Inhibition ofthe
of thephotosynthetic
the photosyntheticpathway,
photosynthetic pathway,
pathway,
Atrazine
Atrazine
Atrazine Organochlorine
Organochlorine
Organochlorine Inhibition of
ofthe
specifically
Inhibition photosynthetic
the
thethe photosystempathway,
photosynthetic II.
Atrazine Organochlorine specifically
specifically
Inhibition of
specifically the the photosystem
photosystem
photosynthetic
the II.
II.
pathway,
AtrazineAtrazine
Atrazine Organochlorine
Organochlorine
Organochlorine
Inhibition
pathway, of the
specifically thephotosystem
photosynthetic
specifically
II.
the pathway,
photosystem II.
specifically the
specifically the photosystem II. II.
photosystemphotosystem
II.
Imitation of plant growth hormone auxin

Imitationof
Imitation
Imitation ofplant
of plant growth
plant growthhormone
hormoneauxin
hormone auxin
auxin
Imitation
and of plantgrowth
uncontrolled growth
cell hormone
division auxin
in vascular
2,4-D Organochlorine and
and
and
auxin uncontrolled
uncontrolled
Imitation of
uncontrolled
and
Imitation plant cell
cell
cell
uncontrolled
of plant division
division
growth
division
growthcell in
in
hormone
in
division
hormone vascular
vascular
auxin
vascular
auxin
2,4-D
2,4-D
2,4-D Organochlorine
Organochlorine
Organochlorine and uncontrolled
tissue, leading cell division
to uncontrolled in vascular
growth and
2,4-D 2,4-D Organochlorine
Organochlorine tissue,
tissue,
and leadingto
leading
inuncontrolled
tissue, vascular
uncontrolled
leading to
to uncontrolled
uncontrolled
tissue,
cellleading
division togrowth
growth
in and
and
vascular
2,4-D
2,4-D Organochlorine
Organochlorine
and
tissue, leading
eventuallytouncontrolled
cell division
uncontrolled
death growth
in
growth
of plants. and
vascular
and
eventually
eventually
uncontrolled growth
tissue, eventually
leading death
death
and ofof plants.
plants.
eventually
to uncontrolled
uncontrolled
death growth and
and
tissue, leading to
eventually deathofofplants.growth
plants.
death of plants.
eventually death ofof plants.
plants.
eventually death
Imitationofofplant
Imitation plantgrowth
growthhormone
hormone auxin
Imitationof
Imitation ofplant
plantgrowth
growthhormone
growth hormoneauxin
hormone auxin
auxin
Imitation
and
auxin and of
uncontrolledplant
uncontrolled growth
cell hormone
division
cell auxin
in vascular
division
Dicamba Organochlorine and
and
and uncontrolled
uncontrolled
Imitation
Imitation of plant
uncontrolled
of cell
cell
plantcell division
division
growth
division
growth in
in
hormone vascular
vascular
ingrowth
hormone auxin
vascular
auxin
Dicamba
Dicamba
Dicamba
Dicamba Organochlorine
Organochlorine
Organochlorine
Organochlorine and
tissue, uncontrolled
leading
in vascular to cell division
uncontrolled
tissue, leading to in vascular
and
Dicamba Organochlorine tissue,
tissue, leadingto
leading
and uncontrolled
tissue, uncontrolled
leading to
to uncontrolled
uncontrolled
cell division growth
growth
divisiongrowth
in and
and
vascular
Dicamba
Dicamba Organochlorine
Organochlorine
and
tissue, leading
uncontrolledeventuallytouncontrolled
growth cell
uncontrolled
death
and in
of plants.
eventually
and
vascular
growth and
eventually
eventually
tissue, eventually
leading deathof
death of plants.
of
to uncontrolled
uncontrolled plants.
growth and
and
tissue, leading
deathto
eventuallyof death
death ofplants.
plants. growth
plants.
eventually death
eventually death ofof plants.
plants.
Inhibition of cell
Inhibitionof mitosis, acting on the meri-
Trifluralin Organophosphate Inhibition
Inhibition
Inhibition ofof
of
cellmitosis,
cell
cell
cell
mitosis,acting
mitosis, actingon
acting onthe
on themeri-
meri-
meri-
Trifluralin
Trifluralin
Trifluralin
Trifluralin Organophosphate
Organophosphate
Organophosphate
Organophosphate Inhibition
stems
the and cellmitosis,
oftissues
meristems mitosis, acting
acting
of underground
and tissues on
of onthe
the meri-
organs.
Trifluralin Organophosphate stems
stems and
and
Inhibition
stems oftissues
tissues of
of underground
underground
cell mitosis,
mitosis, acting on organs.
organs.
onorgans.
the meri-
Trifluralin
Trifluralin Organophosphate
Organophosphate stemsand
Inhibition tissues
andof cell
underground
tissues ofofunderground
acting
organs.
underground the meri-
organs.
stems and
stems and tissues
tissues ofof underground
underground organs.organs.
Inhibition
Inhibition of elongases
of elongases andand
thethe geranylgera-
Inhibitionof
Inhibition
Inhibition ofelongases
of elongasesand
elongases andthe
and thegeranylgera-
the geranylgera-
geranylgera-
Metolachlor Organochlorine geranylgeranyl
Inhibition
nyl pyrophosphate pyrophosphate
of elongases and theimportant
cyclases, geranylgera-
in
Metolachlor
Metolachlor
Metolachlor Organochlorine
Organochlorine
Organochlorine nylpyrophosphate
nyl pyrophosphate
pyrophosphate
Inhibition of elongases
elongases cyclases,
cyclases, important
important
andsynthesis
the in
in
geranylgera-
Metolachlor
Metolachlor Organochlorine
Organochlorine nyl
cyclases,
Inhibition
nyl important
of
thepyrophosphate
synthesis cyclases,
in the
and important
the
cyclases,
of long-chain in
geranylgera-
important
fatty acids. in
Metolachlor Organochlorine thepyrophosphate
the
nyl synthesis
synthesis
pyrophosphate oflong-chain
of long-chain
long-chain
cyclases, fatty
fatty acids. in
acids.
important
Metolachlor Organochlorine the
nyltheof long-chain
synthesis
synthesis of fatty acids.fatty
cyclases,
of long-chain acids.in
fattyacids.
important
the synthesis
the synthesis ofof long-chain
long-chain fatty
fatty acids.
acids.
Inhibition of the photosynthetic

Inhibition of the photosynthetic pathway,
Cyanazine
Cyanazine Organochlorine
Organochlorine Inhibition
Inhibition ofthe
of
pathway,
Inhibition of the
the photosynthetic
photosynthetic
specifically pathway,
pathway,
the pathway,
Cyanazine
Cyanazine
Organochlorine
Organochlorine Inhibition of thephotosynthetic
specifically photosynthetic
the photosystem pathway,
II.
Cyanazine Organochlorine specifically
specifically
Inhibition of the
specifically the
photosystem
the
thethe photosystem
II.
photosystem
photosynthetic II.
II.
pathway,
Cyanazine
Organochlorine
Inhibition of
specifically thephotosystem
photosynthetic
photosystem II.
pathway,
II.
specifically the
specifically the photosystem
photosystem II.II.
2.2.3.Rodenticides
2.2.3. 2.2.3. Rodenticides
Rodenticides
2.2.3.
2.2.3. Rodenticides
2.2.3.Rodenticides
Rodenticidesact to kill rodents, such as rats, mice, squirrels, and nutria; all these ro-
Rodenticides
Rodenticides
Rodenticides
Rodenticides
2.2.3. act toact
Rodenticides
Rodenticides killto
act
act torodents,
killrodents,
kill suchsuch
rodents,
rodents, as rats,
such
such as mice,
asrats,
rats,
rats, squirrels,
mice,
mice, andand
squirrels,
squirrels, nutria;
and
and allall
nutria;
nutria; these
all
all thesero-
these ro-
ro-
dents Rodenticides
cancause
cause acttotokill
damage kill rodents,
tocrop,
crop, suchasas
transmit rats,mice,
disease, andsquirrels,
mice, squirrels,
cause andnutria;
ecological nutria;
damage.allthese
these ro-
Rodent
rodents can
dents
dents
dents cause
can
can
can damage
cause damage
damage to crop,
to
to transmit
crop, disease,
transmit
transmit and
disease,
disease, cause
and
and ecological
cause
cause damage.
ecological
ecological Rodent
damage.
damage. Rodent
Rodent
cancause
dentsRodenticides
infestations cause
arisedamage
acta to
damage
in to
wide tocrop,
kill crop, transmit
rodents,
variety such
transmit
of disease,
as
disease,
situations: and
rats, in
mice,
and cause
causeecological
squirrels,
agriculture ecological
soils, damage.
and nutria;
damage.
inside and Rodent
all these ro-
Rodent
around
infestations arise
infestations
infestations
infestations in a wide
arise
arise
arise in
in variety
in aaa wide
wide
wide of situations:
variety
variety
tovariety of
of in agriculture
of situations:
situations:
situations: inand
in
in soils,
agriculture
agriculture inside
soils, and
soils, inside
inside
inside around
and around
and around
around
dents can cause
infestations
buildings,
buildings, in in
sewers, arisedamage
in ainwide
sewers,
in waste waste
dumps,
crop,
variety
dumps,transmit
and/orofand/or
in
disease,
situations:
open in inagriculture
open
areas.
cause
agriculture
areas. soils,
ecological
soils, inside and
damage.
and Rodent
around
buildings,
buildings,
buildings,
infestations insewers,
in
in sewers,
sewers,
arise ain
in
in in wastevariety
waste
waste
wide dumps,
dumps,
dumps, and/or
and/or
ofand/or inopen
in
in
situations: open
open areas.
areas.
areas.
in agriculture soils, inside and around
buildings,
Most in
rodenticides sewers,
act as in waste dumps, and/or in open areas.
buildings, in sewers, in anticoagulants
waste dumps, and/or that interfere
in openwithareas.blood clotting and cause
death due to excessive bleeding. The rodenticide products are baits in block or paste
form [52]. The most common rodenticides are summarized in Table 5.
Most rodenticides act as anticoagulants that interfere with blood clotting and cause
Most rodenticides act as anticoagulants that interfere with blood clotting and cause
deathMost rodenticides
due to act as anticoagulants
excessive bleeding. thatproducts
The rodenticide interfereare
with blood
baits clotting
in block and cause
or paste form
death Most
due rodenticides act as anticoagulants
to excessive bleeding. thatproducts
The rodenticide interfere are
with blood
baits clotting
in block and cause
or paste form
Bioengineering 2021, 8, 92 deathThe
[52]. duemost
Most to excessive
commonbleeding.
rodenticides act The rodenticide
rodenticides thatproducts
are summarized
as anticoagulants are
in Table
interfere baits in block
5. blood
with or
clotting
10 paste
and
of 29 form
cause
death duemost
[52]. The to excessive
commonbleeding. The rodenticide
rodenticides products
are summarized are baits
in Table 5. in block or paste form
[52].
deathThe
duemost commonbleeding.
to excessive rodenticides
The are summarized
rodenticide in Table
products 5. in block or paste form
are baits
[52]. The most common rodenticides are summarized in Table 5.
[52].Table
The 5. Classification
most common of the most common
rodenticides are rodenticides.
summarized
Table 5. Classification of the most common rodenticides.
in Table 5.
Table 5. Classification of the most common rodenticides.
Name PesticideTable
Class 5. Classification of the most
Chemical common rodenticides.
Structure Mode of Action
Name Classification
Table 5.Table
Pesticide Class of the most
Chemical
5. Classification common
of the rodenticides.
Structure
most common rodenticides. Mode of Action
Name Pesticide Class Chemical Structure Mode of Action
Name Pesticide Class Chemical Structure Mode of Action
Name Name Pesticide
Pesticide Class Class ChemicalStructure
Chemical Structure Mode
Mode of Action
of Action
Anticoagulant agent depressing hepatic syn-
Chlorophacinone Organochlorine thesis of prothrombin
Anticoagulant and clottinghepatic
agent depressing factorssyn-
VII,
Chlorophacinone Organochlorine thesis of prothrombin
Anticoagulant agent and clotting
depressing factorssyn-
hepatic VII,
Chlorophacinone Organochlorine IX,Anticoagulant
thesis and
of prothrombin
Anticoagulant agent
X, inducing
agent anddepressing
internal hemorrhage.
clotting
hepatic VII,
Chlorophacinone Organochlorine IX,
thesis and
of
hepatic X, inducing
prothrombin internal
and hemorrhage.
clotting factors VII,
Chlorophacinone
Chlorophacinone Organochlorine
Organochlorine IX,
thesis and X,synthesis
inducingofinternal
of prothrombin
prothrombin
hemorrhage.
and clotting factors VII,
IX,
andand X, inducing
clotting factorsinternal
VII, IX, hemorrhage.
and X,
IX,inducing
and X, inducing internal
internal hemorrhage.hemorrhage.
Inhibition of vitamin K epoxide reductase

Inhibition of vitamin K epoxide reductase
Diphacinone Pyrethroid complex 1, which
Inhibition is anKessential
of vitamin epoxideenzyme for
reductase
Diphacinone Pyrethroid complex
Inhibition1, of
which
Inhibition is anKessential
vitamin
of vitamin epoxide
K epoxideenzyme for
reductase
Diphacinone Pyrethroid complex 1, which
Inhibition activating.
is anKessential
of vitamin epoxideenzyme for
reductase
Diphacinone
Diphacinone Pyrethroid
Pyrethroid reductase
complex activating.
complex
1, which is an1,essential
which isenzyme
an for
Diphacinone Pyrethroid complex 1, which activating.
is an
essential enzyme foressential enzyme for
activating.
activating.
activating.

Anticoagulant
Anticoagulantagent depressing
agent depressinghepatic syn-
Bromadiolone Pyrethroid thesis of prothrombin
Anticoagulant and clottinghepatic
VII,
Bromadiolone Pyrethroid hepatic
thesis synthesis
agent of
of prothrombin
Anticoagulant prothrombin
and clotting
hepatic VII,
Bromadiolone
Bromadiolone Pyrethroid
Pyrethroid IX,
thesis and X, inducing
of prothrombin
Anticoagulant agent internal hemorrhage.
and clottinghepatic
factorssyn-
VII,
Bromadiolone Pyrethroid and
IX,
thesis ofclotting
and factorsdepressing
X, inducing
prothrombin VII,clotting
IX, and
internal
and X,
hemorrhage.
factors VII,
Bromadiolone Pyrethroid IX, and
thesis X, inducing
of prothrombin internal
and hemorrhage.
IX,inducing internalinternal
and X, inducing hemorrhage.
hemorrhage.
IX, and X, inducing internal hemorrhage.
Anticoagulant
Anticoagulantagent depressing
agent depressinghepatic syn-
Difethialone Pyrethroid thesis of prothrombin
Anticoagulant agent and clotting
depressing
hepatic synthesis of prothrombin factorssyn-
hepatic VII,
Difethialone
Difethialone Pyrethroid
Pyrethroid thesis of prothrombin
Anticoagulant and clotting
hepatic VII,
Difethialone Pyrethroid and
IX,
thesis andclotting
X, factors
inducing
of prothrombin
Anticoagulant VII, IX,
internal and X,
hemorrhage.
and clottinghepatic
VII,
Difethialone Pyrethroid IX,inducing
thesis and X, inducing
of prothrombin internal
and hemorrhage.
clotting
internal internal
hemorrhage. factors VII,
Difethialone Pyrethroid IX, and
thesis X, inducing
of prothrombin and hemorrhage.
Inhibition
Inhibition of neurotransmitters,
of glycine glycine as
Strychnine
Strychnine Pyrethroid
Pyrethroid Inhibition of glycine as
neurotransmitters, neurotransmitters,
glycine and as
Strychnine Pyrethroid glycine
Inhibition and acetylcholine.
of glycine neurotransmitters, as
Strychnine Pyrethroid Inhibition ofacetylcholine.
glycine and acetylcholine.
glycine neurotransmitters, as
Strychnine Pyrethroid glycine
Inhibition and acetylcholine.
of glycine neurotransmitters, as
Strychnine Pyrethroid glycine and acetylcholine.
glycine and acetylcholine.
2.2.4. Fungicides
2.2.4. Fungicides
2.2.4. Fungicides
2.2.4.Fungicides
Fungicidesare compounds that kill parasitic fungi or their spores. They permit the
2.2.4. Fungicides
Fungicides are compounds
Fungicides are compoundsthat kill parasitic
that fungi or
kill parasitic theirorspores.
fungi They permit
their spores. the
They permit the
2.2.4. Fungicides
Fungicides are compounds that killoccurring
parasitic fungi orthetheir spores.
foodThey permit the
controlcontrol
of of fungal
fungal
Fungicides
infestations,
infestations,
are compounds
especially
especially occurring
that kill during
parasitic
during
the
fungi whole
or
whole
food
their
control of fungal infestations, especially occurring during the whole food supply. Indeed, supply.
spores.
supply.
Indeed,
They
Indeed,
permit the
control
fungicides of fungal
fungicides
Fungicides
are widely infestations,
are widely
are
applied applied
compounds especially
in the
in the agricultural killoccurring
thatagricultural
parasitic
industry. during
industry.
fungi or
Fungicides the whole
Fungicides
their food
spores.
interfere with supply.
interfere
They Indeed,
with
permit
various vari-
the
control of
fungicides fungal infestations,
are widely applied especially occurring
in the agricultural during the
industry. whole food
Fungicides supply.
interfere Indeed,
with vari-
fungicides
ous
control
biochemical of are
biochemical
fungal
processes widely applied
processes
infestations,
within in
within thethe
especially
the fungal agricultural
fungal
cytoplasm occurring
and industry.
cytoplasm
during
mitochondria.and Fungicides
the whole interfere
mitochondria.
food
They inhibit with
They
supply.
several vari-
inhibit
Indeed,
fungicides
ous biochemicalare widely applied
processes in the
within theagricultural
fungal industry.and
cytoplasm Fungicides interfere
mitochondria. withinhibit
They vari-
enzymes ous biochemical
several enzymes
fungicides
and processes
and
are widely
proteins proteins
involvedappliedwithin
for in the
example the
involved fungal
forthe
agricultural
in cytoplasm
example
lipid in theand
industry.
metabolism, lipidmitochondria.
metabolism,
Fungicides
fungal They
fungal
interfere inhibit
with
respiration, respi-
vari-
ous biochemical
several enzymes processes
and proteins within the fungal
involved cytoplasm
for example in theand lipidmitochondria.
metabolism, They
fungalinhibit
respi-
several
ration, enzymes
and
ous biochemical
and production and
ofproduction proteins
processes
adenosine involved
of adenosine
within
triphosphate for example
triphosphate
the
(ATP)fungal in the
(ATP)
cytoplasm lipidmitochondria.
[53].
and metabolism, fungal respi-
They inhibit
several enzymes
ration, and and proteins
production involved
of adenosine for [53].
example
triphosphate in the[53].
(ATP) lipid metabolism, fungal respi-
ration,
several
Table and
Table 6production
enzymes
6Table
reports reportsand of adenosine
information
proteins
information on
involved
on the most triphosphate
the most
for
common common
example (ATP)in
fungicides. [53].
fungicides.
the lipid metabolism, fungal respi-
ration, and 6production
reports of adenosine
information on thetriphosphate
most common (ATP)fungicides.
[53].
Table
ration, and6production
reports information
of adenosineon the most common
triphosphate (ATP) fungicides.
[53].
Table 6 reports information on the most common fungicides.
Table 6 reports information on the most common fungicides.
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Table 6.
Table
Table 6. Classification
Classification of
of the
themost
most common
common fungicides
fungicides used
used inin agricultural
agricultural soil.
soil.
Table6.6.
Table 6. Table 6. Classification
Classification of the
ofthe most
themost common
most fungicidesfungicides
commonfungicides
fungicides used
usedinin
in agricultural
agricultural soil.
soil.
Table 6.Classification
Classification of
of the most
Classification the mostcommon
of common used
used inagricultural
used in agricultural
common fungicides soil.
agricultural soil.
soil.
Name
Name
Name Pesticide
Pesticide
Pesticide Class
Class
Class Chemical
Chemical
Chemical Structure
Structure
Structure Mode
Mode
Mode of Action
of
of Action
Action
Name Pesticide Class Chemical Structure Mode ofAction
Action
Name Name
Name Pesticide
Pesticide
PesticideClass
ClassClass Chemical
ChemicalStructure
Chemical Structure
Structure Mode
Mode of
of Action
Mode of Action
Inhibition of
Inhibition
Inhibition of enzyme
of enzyme activity
enzyme activity in
activity in fungi
in fungi by
fungi by
by
Inhibitionof
Inhibition ofenzyme
enzymeactivity
activityininfungi
fungiby
by
Mancozeb
Mancozeb Carbamate
Carbamate Inhibition
forming
forming a
a of enzyme
complex
complex
Inhibition of with
with
enzyme activity in fungi by
metal-containing
metal-containing
activity in en-
en-
Mancozeb
Mancozeb
Mancozeb Carbamate
Carbamate
Carbamate forming
forming
forming a
a complex
complex
aacomplex with
with
with metal-containing
metal-containing en-
en-
Mancozeb
Mancozeb Carbamate
Carbamate formingfungi complex
by forming ametal-containing
with
zymes.
zymes.metal-containingen-
complex en-
zymes.
zymes.
zymes.
with metal-containing
zymes.enzymes.
Chlorothalonil
Chlorothalonil
Chlorothalonil Organochloride
Organochloride
Organochloride Reductor
Reductor and
and
Reductor
Reductor and deactivator
deactivator
and
deactivator ofglutathione.
of
deactivator
of glutathione.
of
ChlorothalonilOrganochloride
Chlorothalonil
Chlorothalonil Organochloride Reductor and deactivator of glutathione.
glutathione.
Chlorothalonil Organochloride
Organochloride Reductor
Reductorand
and deactivator
deactivatorofofglutathione.
glutathione. glutathione.
Captan
Captan Captan
Captan Organochloride
Organochloride
Organochloride
Organochloride Reduction
Reduction
Reduction
Reduction of enzymatic
of enzymatic
of enzymatic
of activity.
activity.
activity.
Captan
Captan Organochloride
Organochloride Reduction
Reduction of enzymatic
enzymatic activity.
activity.
Captan Organochloride Reductionofofenzymatic
enzymaticactivity.
activity.
Reaction
Reaction
Reaction andand
and inactivation
inactivation
inactivation ofof
of sulfhydryl
sulfhydryl
Reaction
Reaction
Reaction and
and
sulfhydryl inactivation
andinactivation
inactivation
groups of ofof sulfhydryl
ofsulfhydryl
amino sulfhydryl
Reaction
groups
groups of
of aminoand inactivation
amino acids
acids and
and of sulfhydryl
enzymes,
enzymes, causing
causing
Maneb
Maneb Carbamate
Carbamate groups
groups
groups of
of amino
amino
acidsamino acids
acids
and enzymes, and
and enzymes,
enzymes,
causing causing
causing
Maneb
Maneb
Maneb Maneb Carbamate
Carbamate
Carbamate
Carbamate groupsofof
damage
damage to
to amino
lipid
lipid
acids
acidsand
andenzymes,
metabolism,
metabolism, enzymes, causing
causing
respiration,
respiration, and
and
Maneb Carbamate damage
damage to
damage lipid
damagetotolipid to metabolism,
lipidmetabolism,
lipid respiration,
metabolism,respiration, and
respiration,and
metabolism, and
damage to lipid
production
production ofmetabolism,
of adenosine
adenosine respiration, and
triphosphate.
triphosphate.
respiration,of
production
production
production and
of
of production
adenosine
adenosine
adenosine of
triphosphate.
triphosphate.
triphosphate.
production
adenosine of triphosphate.
adenosine triphosphate.
Creation of
Creation
Creation of chemical
of chemical barrier
chemical barrier between
barrier between the
between the
the
Ziram
Ziram Carbamate
Carbamate Creation
Creation ofchemical
of
Creation chemical
of barrier
barrier
chemical betweenthe
between
barrier the
Ziram
Ziram
Ziram Ziram Carbamate
Carbamate
Carbamate
Carbamate Creation ofplant
chemical
plant and
and aabarrier between the
fungus.
fungus.
Ziram Carbamate between theplant
plant and
and
plant
plant and aafungus.
and
a fungus.
fungus.
a fungus.
plant and a fungus.
Inhibitor of sterol
TebuconazoleOrganochloride
Tebuconazole
Tebuconazole
Tebuconazole Organochloride
Organochloride
Organochloride Inhibitor of
Inhibitor
Inhibitor of sterol
of sterol 14α-demethylase
14α-demethylase
Tebuconazole
Tebuconazole Organochloride
Organochloride Inhibitor
Inhibitor of sterol 14α-demethylase
sterol14α-demethylase
14α-demethylase 14α-demethylase
Tebuconazole Organochloride Inhibitorofofsterol
sterol 14α-demethylase
3. Diffusion
3. Diffusion of of Pesticides
Pesticides into into the the Environment
Environment and and Their
Their Toxicology
Toxicology
3.3.
3. Diffusion Diffusion
of Pesticides
3.Diffusion
Diffusion ofof
of
Pesticides
into theinto
Pesticides
Pesticides
into
into
the
Environment
the
the
Environment
Environmentand Their
Environment
and
and
and
Their
Toxicology
Their
Their
Toxicology
Toxicology
Toxicology
Pesticides aim
Pesticides
Pesticides aim to
aim to prevent,
to prevent, remove,
prevent, remove, and
remove, and control
and control harmful
control harmful pests,
harmful pests, but
pests, but they
but they may
they may be
may be harm-
be harm-
harm-
Pesticides aim to prevent,
Pesticides aim to remove, remove,
prevent, and controland harmful
control pests,
harmful butpests,
they may but be
they harmful
may be
ful
ful to
to Pesticides
the
the environment
environment aim to prevent, and
and human
human remove, andTheir
health.
health. control
Their harmfuluse
excessive
excessive pests,
use can
can but they
give
give high
high may beharm-
harm-
concentra-
concentra-
fulto
to the environment
ful tothetheenvironment
environment
and humanand and
health. human Their health.
excessive Their use excessive
can giveuse use
high can givehighhighconcentra-
concentrations concentra-
ful toof
tions
tions the
of environment
polluting
polluting substances
substances andhumanhuman
in
in the
the
health.
health.Their
environment.
environment. Theirexcessive
excessive
In
In the
the years,
years, usethecan
can
the
give
give high
World
World Health
Health concentra-
Organi-
Organi-
tionssubstances
of polluting
tions ofpolluting
polluting substances
insubstances
the environment. inthe theenvironment.
environment.
In the years, In Inthe
the the
Worldyears,HealththeWorld
World HealthOrgani-
Organization Organi-
tionsofof
zation
zation polluting
ranked
ranked the substances
the pesticides
pesticidestheir
inin the
and
and environment.
reported
reported their
their toxicity
toxicity
years,
In theand
andyears, the
their
their the World
effects
effects on
Health
onHealth
humanOrgani-
human health
health
zation
ranked zation
the ranked
pesticides
ranked the
and
the pesticides
reported
pesticides and
and reported
toxicity
reported and their
theirtheirtoxicity
effects
toxicity and
and on their
human
their effects
health
effects on
on human
[54].
human health
health
[54]. time, several pesticides have been banned in some countries due to their high health
zation
[54].
[54].
Through
ranked the pesticides and reported their toxicity and their effects on human
[54].
[54].Through
toxicity. However, Through
Through at the time,
time,
moment,
time, several
several
several their pesticides
pesticides
production
pesticides have
have
have and been
been banned
banned
usebanned
been in some
in
go on, especially
banned in some countries
some countries
in developing
countries due to
due
due to their
to their
their
Through
Through time,
time,severalseveral pesticides
pesticides have
have been
been bannedand ininsome
some countries
countries due
duetotointheir
their
countries. high
high toxicity.
toxicity.
hightoxicity.
toxicity.However, However,
However,
However,at at
at the
the
at themoment,moment,
moment, their
their
moment, theirproduction production
production
production anduse and use
use go
go
use goon, on,
on, especially
especially
on, especiallyin in de-
in de-
de-
high
high toxicity. However, atthe the moment,their their productionand and usego go on,especially
especially inde- de-
veloping
veloping countries.
countries.
velopingcountries.countries.
veloping
veloping countries.
3.1. Presence and Distribution into the Environment
The 3.1.
3.1. Presencepersist
Presence
pesticides
3.1. Presence and Distribution
and
and Distribution
in the environment
Distribution into the
into
into the Environment
the Environment
and may bioaccumulate and contaminate
Environment
3.1.
3.1.Presence
Presence and
and Distribution
Distribution into
into the
theEnvironment
Environment
the food chain, The
The
The pesticides
pesticides
affecting
pesticides human persist
persist
persisthealth in
in
inthe the
the environment
environment
andenvironment
the the environment and may
and
and may
as
may bioaccumulate
bioaccumulate
a whole. Pesticideand
bioaccumulate and
tends
and contaminate
contaminate
to
contaminate
The
The pesticides
pesticides persist
persist inin the environment
environment and
and may
may bioaccumulate
bioaccumulate and
and contaminate
contaminate
conservethethe
its
thefood food
food chain,
chain,
molecular
foodchain, affecting
affecting
integrity
chain,affecting affectinghuman and human
human chemical,
humanhealth health
health and
and
physical,
healthand andthe the
the environment
environment
and functional
the environmentas as
as aa whole.
whole.
characteristics
asaawhole. Pesticide
Pesticide
whole. Pesticidefor tends
a tends
tends
the
theconserve
food chain, affectinginto human health and theenvironment
environment a whole.Pesticide
asfunctional Pesticide tends
tends
to
to
certain time conserve
after
toconserve
conserveitsbeing its
its molecular
molecular
released
itsmolecular
molecularintegrity integrity
integrity
the
integrityand soiland
and[55].chemical,
chemical,
andchemical,
chemical,physical,physical,
physical,
physical,and and
and functional
andfunctional characteristics
characteristics
functionalcharacteristics
characteristics
totoparameter
conserve its molecular integrity and chemical, physical, andinto functional
for
Thefor
for aa certain
certainthat time
time after
after
can being
bebeing
considered released
released into
tointo the soil
the
evaluate soil [55].
its[55].
persistence the soil characteristics
is the
for aaacertain
certain time
time after
after being
being released
released into
into
intothe
the soil
soil [55].
[55].
half-timefor (t1/2 certain
),
The
The that time
is,
parameter
parameter
Theparameter
parameterthat the after
time that
that being
required
thatcan can
can
canbe
released
be
be for a compound
considered
considered
beconsidered
consideredto
the
to
to soilto [55].
evaluate
evaluate
toevaluate halve
evaluateits its
its its initial
persistence
persistence
itspersistence concentration.
persistenceinto into
into
intothe the soil
the
the soil is
soil is the
is the
the
The
The parameter that can berequired
considered to evaluate its persistence into thesoil
soilisisthe
the
Pesticides
half-time
half-time with (t
(t
half-time(t(t1/21/2 short
1/2
1/2 ),
), that
that half-times
is,
is, the
the time
time accumulate
required and
for
for a
a persist
compound
compound less into
to
to the
halve
halve soil.
its
its By contrast,
initial
initial concentration.
concentration.
half-time
pesticides half-time
with (t
long ),),),half-times
1/2 thatis,
that
that
is,the
is,
thetime
the
timerequired
time
are more
requiredfor
required
foraacompound
for
persistent a
compoundto
compound
and this may
tohalve
to
halveits
halve
increase
itsinitial
its
initialconcentration.
initial
the
concentration.
concentration.
risk to
Pesticides with
Pesticides
Pesticides
1/2 with short
with short half-times
short half-times accumulate
half-times accumulate and
accumulate and persist
and persist less
persist less into
less into the
into the soil.
the soil. By
soil. By contrast,
By contrast,
contrast,
contaminate Pesticides
Pesticides
the environment. with
with short
short half-times
half-times accumulate
accumulate and
and persist
persist less
lessinto
into the
thesoil.
soil. By
By contrast,
contrast,
pesticides
pesticides
pesticideswith with
with
withlong long
long half-times
half-times
longhalf-times
half-timesare are
are
aremoremore
more persistent
persistent
morepersistent
persistentand and
and this
this
andthisthismay may
may increase
increase
mayincrease
increasethe the
the risk
risk
therisk
riskto to con-
to
to con-
con-
pesticides
pesticides
Altogether, theywith canlong half-times
be classified asare more persistent and this may increase the risk tocon-
[56]: con-
taminate
taminate
taminatethe the
the environment.
environment.
theenvironment.
environment.
taminate
taminate the environment.
• nonpersistent Altogether,
Altogether,
pesticides,
Altogether, they
they
theycan can
can
when
can be
be classified
classified
tclassified
1/2 is lower
beclassified as
as [56]:
[56]:
than
[56]: 30 days;
as[56]:
Altogether,
Altogether,they they canbe be classifiedas as [56]:
• moderately persistent, when t1/2 is in the range 30–100 days;

• persistent ones, whent1/2 is higher than 100 days.
Once present in the soil, pesticides may: (1) be adsorbed by soil particles; (2) be
degraded by photochemical, chemical, and microbiological processes; and (3) move from
soil to water.
3.1.1. Adsorption by Soil Particles

Pesticide molecules can be adsorbed physically (Van der Waals forces) or chemically
(electrostatic interactions) on the soil particles. The process can be described with the
adsorption isotherms [57–59]. The adsorption constant is evaluated since it provides
information about solute mobility. If pesticides have a low affinity for adsorption, they
tend to spread more easily into the environment. Several soil parameters influence the
adsorption process, namely soil organic matter content, clay content, clay mineralogy,
and pH.
3.1.2. Degradation Processes

The pesticides can be degraded and transformed into one or more metabolites through
photochemical, chemical, and microbiological processes.
Photodegradation is an abiotic process induced by the absorption of light energy
that leads to the decomposition of the polluting molecules. This process takes place with
more difficulty in the soil, being a heterogeneous system, and it is influenced by soil
properties. For example, photodegradation is more efficient with particles having a large
size and a high specific area since they promote light diffusion [60]. Chemical and biological
degradation occurs by reactions such as hydrolysis, oxidation, reduction, dehydrogenation,
dehalogenation, decarboxylation, and condensation.
In the biodegradation process, pesticides are degraded by microbial organisms through
metabolic or enzymatic action [61]. The evaluation of the kinetics of these reactions gives
information on the persistence of pesticides.
3.1.3. Leaching from Soil to Water

Leaching is the movement of pesticides within the soil. The soluble contaminants are
carried by water downward through permeable soils. This phenomenon is responsible for
the contamination of groundwater.
The extent of leaching is highly dependent on soil properties, pesticide physicochemi-
cal properties, formulation types, distribution of rainfall events or irrigation strategy, and
hydrogeological processes [62].
3.2. Toxicity and Short- and Long-Term Damages

Several studies report the toxic effects on human health associated with the use of
pesticides. Typically, the main routes of human exposure to pesticides are inhalation,
ingestion, and dermal contact. Each compound has its toxicity, but the risk increases with
increasing dosage and exposure time.
The WHO provides guidelines for the classification of pesticides, dividing them into
five categories, and considering the lethal dose 50 (LD50 ) as a benchmark (Table 7) [54].
The LD50 value represents the dose required to kill half the tested population after a
standardized test duration. The substance route can be given dermal and oral.
Table 7. Criteria for classification of pesticides.
LD50 for the Rat

Class
Bioengineering 2021, 8, x FOR PEER REVIEW Characteristics (mg·kg−1 Body Weight) 13 of 29
Oral Dermal
Ia Extremely hazardous <5 <50
Ib
II Highlyhazardous
Moderately hazardous 5–50
50–2000 50–200
200–2000
II
III Moderately hazardous
Slightly hazardous 50–2000
>2000 200–2000
>2000
III Slightly hazardous >2000 >2000
U Unlikely to present acute hazard >5000 >5000
U Unlikely to present acute hazard >5000 >5000
3.2.1. Organochlorines
3.2.1. Organochlorines
Considering the mode of action, the organochlorines damage the nervous systems,
Considering
since theion
they alter the mode of action,
channels. Thethe
mainorganochlorines damage the nervous
effects are hyperexcitability systems,
of brain, convul-
since they alter the ion channels. The main
sions, tremor, hyperreflexia, and ataxia. effects are hyperexcitability of brain, convulsions,
tremor,Organochlorines
hyperreflexia, and ataxia.
have high toxicity and fall into the first classes of WHO classifica-
Organochlorines have high toxicity and fall into the first classes of WHO classification
tion (Figure 5).
(Figure 5).
Figure 5. LD50 (mg·kg−1) of organochlorines for the rat.

Figure 5. LD50 (mg·kg−1 ) of organochlorines for the rat.
ItItwas
wasnoted
notedthat
thatthe
themajor
majorsource
sourcefor
forhuman
humanexposure
exposuretotoorganochlorines
organochlorinesisisfood,
food,
particularly fish products [63]. The OCs are accumulated in fish muscle,
particularly fish products [63]. The OCs are accumulated in fish muscle, and then, theyand then, they
become bioaccessible to humans during gastrointestinal
become bioaccessible to humans during gastrointestinal digestion. digestion.
Significant
Significant concentrations
concentrations of of
OCsOCs were
were found
found on dust
on dust particles.
particles. ThisThis
typetype of exposi-
of exposition
causes cytotoxic effects on human skin, leading to the development of carcinoma [64]. [64].
tion causes cytotoxic effects on human skin, leading to the development of carcinoma
3.2.2.Organophosphates
3.2.2. Organophosphates
Theorganophosphates
The organophosphates (OPs)
(OPs) areare acetylcholinesterase
acetylcholinesterase inhibitors,
inhibitors, which
which leadlead to hav-
to having
high
ing levels of acetylcholine.
high levels The consequence
of acetylcholine. is damage
The consequence to several
is damage organs
to several such as
organs periph-
such as pe-
eral and central
ripheral nervous
and central systems,
nervous muscles,
systems, liver, pancreas,
muscles, and brain.
liver, pancreas, andMost of them
brain. Most belong
of them
tobelong
the first
toclasses
the first(Ia, Ib, and
classes (Ia,II)Ib,
ofand
the II)
WHO classification
of the (Figure 6).(Figure 6).
WHO classification
Bioengineering 8, x8,FOR
2021, PEER
x FOR REVIEW
PEER REVIEW 14 14
of of
29 29
Figure 6.6.6.
Figure LD 50 (mg·kg
LD −1)−
50 (mg·kg of
−1 organophosphates
)1 of forfor
organophosphates rat.
rat.
Figure LD 50 (mg·kg ) of organophosphates for rat.
HighHigh
High doses
doses
doses ofoforganophosphate
of organophosphate
organophosphate cause
cause
cause acute
acute
acute intoxication, which
intoxication,
intoxication, which
which leads
leads
leads totopancreatitis.
to pancreatitis.
pancreatitis.
This
Thisisisisdue
This dueto
due the
toto theAChE-inhibition-induced
the AChE-inhibition-inducedcholinergic
AChE-inhibition-induced cholinergicoverstimulation,
cholinergic overstimulation,which
overstimulation, which
which leads
leadsto
leads toto
increased
increased
increased intraductal
intraductal
intraductal pressure
pressure
pressure andand
and excess
excess
excess pancreatic
pancreatic
pancreatic enzyme
enzyme
enzyme secretion
secretion
secretion [65].
[65].
[65].
InInInthe
the
thelong
long
long term,
term,
term,one
one
oneof
ofofthe
theeffects
effectsofof
of organophosphate
organophosphate
organophosphate poisoning
poisoning
poisoningisisais
aseizure
seizure disor-
disorder.
a seizure disor-
der. Chuang
Chuang et et
al. al.
[66] [66]
havehave
shownshownthat that
the the
risk risk
of of seizure
seizure development
development
der. Chuang et al. [66] have shown that the risk of seizure development is greater in is is
greatergreater
in in pa-
patients
pa-
tients
with
tientswithwith organophosphate
organophosphate
organophosphate poisoning
poisoning than in
poisoning than inin
healthy
than healthy individuals.
individuals.
healthy individuals.
3.2.3.
3.2.3. Carbamates
Carbamates
3.2.3. Carbamates
The
TheThe toxicity
toxicity ofofof
toxicity several
several
several carbamates
carbamates isisis
carbamates such
such asas
as
such toto
to make
make
make them
them
them moderately
moderately
moderately and
and
and slightly
slightly
slightly
hazardous,
hazardous, in
hazardous,ininsomesome cases
somecases unhazardous,
casesunhazardous, as can
unhazardous,asascan be seen
canbebeseen from
seenfrom the
fromthe LD
theLD
LD values
values
5050
50
shown
valuesshown
shownininin
Figure
Figure
Figure 7.
7. 7.
Figure 7.7.7.
Figure LD 50 (mg·kg
LD −1)−
50 (mg·kg of
−1 carbamates
1) of forfor
carbamates rat.
rat.
Figure LD 50 (mg·kg ) of carbamates for rat.
The
The
The carbamates
carbamates
carbamates act
act as
act
asasacetylcholinesterase
acetylcholinesterase
acetylcholinesterase inhibitors
inhibitors
inhibitors and
andandendocrine
endocrine
endocrine disruptors.
disruptors.
disruptors. Ex-
Ex-
Expo-
posure
sure toto
posure carbamates
to carbamates
carbamates causes
causes
causes respiratory
respiratory
respiratory diseases.
diseases.
diseases.
Toxicological
Toxicological
Toxicological experiments
experiments
experiments have
have
haveshown
shown that
thatprenatal
prenatal and
and
prenatal postnatal
postnatal
and postnatal exposure
exposure totocarba-
exposure car-
to car-
bamates
mates
bamates can
can can affect
affect fetal
fetal
affect andand
fetal andchild
child development,
development,
child causing
causing
development, damage
causing damage
to theto
damage tothe
thehippocampus
hippocampus [67,68].
hippocampus
[67,68].
[67,68].
Bioengineering
2021, 8, 8,
92x FOR PEER REVIEW 1515
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2929
It was noted that many fruits and beverages are contaminated by ethyl carbamate, a
It was noted that many fruits and beverages are contaminated by ethyl carbamate, a
carcinogenic chemical causing the development of cancers in various animal species and
carcinogenic chemical causing the development of cancers in various animal species and
rarely in humans. In particular, this pesticide can induce the production of reactive oxy-
rarely in humans. In particular, this pesticide can induce the production of reactive oxygen
gen species, depurination of DNAs, and mitochondrial dysfunction [69,70].
species, depurination of DNAs, and mitochondrial dysfunction [69,70].
3.2.4.Pyrethroids
3.2.4. Pyrethroidsand andPyrethrins
Pyrethrins
Pyrethrinsand
pyrethroids areare
lessless toxic
toxic to mammalian
to mammalian cellscells
and and less persistent
less persistent in thein
the environment than other pesticides. They can damage human
environment than other pesticides. They can damage human health, mainly affecting thehealth, mainly affecting
the nervous
nervous system.
system. The effects
The effects can becan be systemic,
systemic, immunological,
immunological, neurological,
neurological, reproduc-
reproductive,
tive, developmental,
developmental, genotoxic,
genotoxic, and carcinogenic,
and carcinogenic, and [40].
and death deathThe[40]. The neurobehavioral
neurobehavioral func-
functioning
tioning of fetuses
of fetuses and children
and children is damaged
is damaged by theby the exposition
exposition to thesetopesticides,
these pesticides, since
since they
theyan
have have an immature
immature nervous
nervous system,system, and their
and their brainbrain stillto
still has has to grow
grow and and develop
develop [71].[71].
A
A correlation between pyrethroid exposure and the increased risk of
correlation between pyrethroid exposure and the increased risk of diabetes in the adult diabetes in the adult
populationwas
population wasfound
found[72].
[72].
InInFigure
Figure8,8, the
the LD5050 value
valueofofseveral
severalpyrenoids
pyrenoids is shown.
is shown. These compounds
These compounds are more
are
toxictoxic
more thanthan
pyrethrins since
pyrethrins theythey
since are are
synthesized
synthesizedwith thethe
with purpose
purpose of of
increasing
increasingtheir
theirin-
secticidal power.
insecticidal power.
Figure8.8.LD
Figure LD5050(mg ·kg−−11))of
(mg·kg of pyrethroids
pyrethroids for
for rat.
rat.
4. Biological Techniques for Pesticide Removal

4. Biological Techniques for Pesticide Removal
Bioremediation reduces pesticide contamination of agricultural soils by biodegrada-
Bioremediation
tion processes reduces pesticide
via the metabolic activities contamination
of microorganisms.of agricultural soils by
It is an efficient, biodegrada-
cost-effective,
tion processes via the metabolic
and environment-friendly treatment. activities of microorganisms. It is an efficient, cost-effec-
tive,During
and environment-friendly treatment.the microorganisms use the pesticides as cosub-
the bioremediation processes,
strates in their metabolic reactions processes,
During the bioremediation together with the other
microorganisms
nutrients, thususeeliminating
the pesticidesthemas
cosubstrates in their metabolic reactions together with other nutrients,
from the environment. The efficiency of these processes depends on the characteristics of thus eliminating
them fromsuch
pesticides, the as
environment. The efficiency
their distribution, of these processes
their bioavailability, depends
and their on theincharacteris-
persistence soil. It is
necessary to promote the availability of pesticides to microorganisms: this ispersistence
tics of pesticides, such as their distribution, their bioavailability, and their negativelyin
soil. It isbynecessary
affected to promote
the adhesion the availability
of pesticides of pesticides
to soil particles to microorganisms:
and their low water solubilitythis is[73].
neg-
Inatively
addition,affected by the
the soil adhesion of and
characteristics pesticides to soil particles
the environmental and their low
conditions, suchwater
as pH, solubility
water
[73]. Inmicrobial
content, addition, diversity,
the soil characteristics
and temperature,andinfluence
the environmental conditions,
the bioremediation such as pH,
efficacy.
water content, microbial diversity, and temperature, influence the bioremediation effi-
cacy.
4.1. Mechanisms of Microbial Degradation

During biodegradation processes, pesticides are transformed into degradation prod-
ucts or completely mineralized by microorganisms, which use the pollutant compounds as
nutrients for their metabolic reactions. A key role in the biotransformation mechanisms is
carried out by enzymes, such as hydrolases, peroxidases, and oxygenases, that influence
and catalyze the biochemical reactions.
The degradation process of pesticides can be divided into three phases, which can be
summarized in:
• Phase 1: Pesticides are transformed into more water-soluble and less toxic products
through oxidation, reduction, or hydrolysis reactions.
• Phase 2: The Phase-1 products are converted into sugars and amino acids, which have
higher water solubility and lower toxicity.
• Phase 3: Conversion of the Phase-2 metabolites into less toxic secondary conjugates.
The microorganisms involved in the degradation process are bacteria or fungi, which
may generate intra- or extra-cellular enzymes.
The degradation time is a relevant parameter to be assessed when a bioremediation
activity is planned. It is typically interpreted by the first-order model [74], which depends
on the pollutant concentration at the beginning and end of the process. This approach
has limits because several parameters condition the process, such as microbial activity,
temperature, water content, availability, and leaching of pesticide in the soil [61].
4.1.1. Bacterial Degradation

In the years, several bacterial strains were identified as capable of degrading the
pesticides present in the soils. Each bacterium has a specificity that makes it particularly
suitable for a degradative process. The operative conditions, such as temperature, pH,
water content, and types of pollutants, affect the adaptation, development, and role of
a bacterial strain. Moreover, during the degradation process, metabolites can form and
cause additional environmental problems, since they may be more difficult to remove
than the original compound, and this must be considered a drawback. As an example,
chlorpyrifos, an organophosphate used as an insecticide, is hydrolyzed by microorganisms,
and the primary and major degradation product is 3,5,6-trichloro-2-pyridinol (TCP). TCP
has greater water solubility than chlorpyrifos and causes widespread contamination in
soils and aquatic environments. Few microorganisms can degrade the pesticide and its
metabolite and among them the bacterium Ochabactrum sp. JAS2 is capable of hydrolyzing
both compounds [75].
In many cases, the degradation is easier when a bacterial consortium is used compared
to using an isolated pure culture [76,77]. In nature, the bacteria coexist and depend on
each other for their viability. In the metabolic pathways of pesticide degradation, each
bacterium can generate metabolites that may be used as a substrate by others.
4.1.2. Fungal Degradation

The agricultural soils are populated by many fungi, which can be exploited to biode-
grade pesticides. This class of microorganisms includes yeast, molds, and filamentous
fungi. Fungal degradation is promoted by its capacity to produce many enzymes involved
in degradative processes [78]. These microorganisms also can influence the soil properties,
modifying soil permeability, and ion exchange capability.
Fungi can be better degraders than bacteria due to their characteristics, such as
specific bioactivity, growth morphology, and high resistance even at high concentrations
of pollutants.
A common approach is to use both fungi and bacteria to enhance degradation since
fungi can transform pesticides into an easier and accessible form for bacteria [79].
4.1.3. Enzymatic Degradation

Enzymatic biodegradation is due to the enzymes produced during the metabolic
processes of microorganisms or plants. Enzymes are biological macromolecules that can
catalyze biochemical reactions involved in pesticide degradation. These molecules act in
the rate of reaction by lowering the activation energy of the reaction itself [80].
The main metabolic reactions, where they are involved, are oxidation, hydrolysis,
reduction, and conjugation.
• Oxidation, which is the first step of the degradation of pesticides, consists of the
transfer of an electron from reductants to oxidants. Oxygenase and laccase enzymes
may be involved in this reaction. Oxygenases catalyze the oxidation reaction by
incorporating one or two molecules of oxygen; laccases cleave the ring present in
aromatic compounds and reduce oxygen to water and produce free radicals. During
the reaction, heat or energy is generated, and it is utilized by microorganisms for their
metabolic activities.
• Hydrolysis permits the cleavage of bonds of the substrate by adding hydrogen or
hydroxyl groups from water molecules. The pesticide molecules are thus divided into
smaller chain compounds than the original ones. Typical enzymes involved in the
hydrolysis pathways are lipases, esterases, and cellulases. For example, Luo et al. [81]
have identified and cloned an esterase gene from Rhodopseudomonas palustris PSB-S
capable of decomposing several synthetic pyrethroids, such as fenpropathrin, and
tolerates temperature and pH changes. The enzyme is involved in the key step of
hydrolysis, namely the cleavage of the ester bond in the fenpropathrin compound.
• Reduction permits the transformation through reductive enzymes (nitroreductase).
• The conjugation reaction is carried out using existing enzymes, and it is typical
of fungal biodegradation. It involves the addition of exogenous or endogenous
natural compounds to facilitate the mineralization of pesticides. This process includes
reactions such as xyloxylation, alkylation, acylation, and nitrosylation.
Table 8 reports some microorganisms able to degrade widely used pesticides.
Table 8. Microorganisms capable to degrade several pesticides.
Target Pesticide Microorganism References

Chlorpyrifos Ochrobactrum sp. JAS2 [75]
Cypermethrin Bacillus subtilis [82]
DDT Fomitopsis pinicola and Ralstonia pickettii [79]
Insects
Deltamethrin Streptomyces rimosus [74]
Fentopropathrin Rhodopseudomonas palustris PSB-S [81]
Brevibacterium frigoritolerans, Bacillus
Phorate [77]
aerophilus and Pseudomonas fulva
Acetochlor Tolypocladium geodes and Cordyceps [11]
Glyphosate Fusarium [83]
Herbs
Glyphosate and its metabolites Pseudomonas fluorescens [84]
Penoxsulam Aspargillus flavus and Aspargillus niger [85]
Pseudomonas, Rhodobacter, Ochrobactrum,
Epoxiconazole and fludioxonil Comamonas, Hydrogenophaga, Azospirillum, [86]
Fungi
Methylobacillus, and Acinetobacter
Tebuconazole Serratia marcescens [87]
4.1.4. Mineralization
The mineralization process permits the degradation of pesticides into inorganic matter,
namely, carbon dioxide, salts, minerals, and water. The microorganisms use the pesticide
compounds as a source of nutrients.
Also in this case, the degradation is influenced by several factors, such as microbial
species, soil characteristics, and type of pollutants. The mineralization rate depends on the
concentration of microbial community; namely, a decrease in microbial population does
not promote the degradation [88]. For example, chlorothalonil (CTN), an organochlorine
fungicide, is degraded in CO2 , but if the soil microbial community is reduced, several
metabolites can form, which are more toxic, persistent, and mobile than CTN itself. This is
due to the absence of actively-degrading groups or the decrease in soil biodiversity that
leads to low microbial activity.
In glyphosate mineralization, the soil properties influence the mineralization process.
Nguyen et al. [89] have tested agricultural soils, differing for some soil parameters, such as
soil texture, soil organic matter content, pH, and exchangeable ions. By the univariate and
multiple regression analysis, they have found the parameters that influence the glyphosate
mineralization, namely: the cation exchange capacity, determined as the sum of exchange-
able base cations and exchanges acidity (expressed as Al3+ and H+ ); the exchangeable
base cations (expressed as Ca2+ ); and the available form of potassium, determined by
ammonium lactate extraction. The low mineralization of glyphosate in soils with high
exchangeable acidity could be due to either the formation of strong chemical bonds with the
carboxylic or phosphonic acid groups of the glyphosate itself, reducing its bioavailability,
or the toxic effects of exchangeable aluminum to soil microorganisms.
4.1.5. Co-Metabolism
Co-metabolism is the biotransformation, through a series of reactions, of an organic
compound that is not used to support microbial growth. The pesticides are transformed by
microorganisms and enzymes into useful compounds for other biological, chemical, and
physical transformations, and finally degraded thanks to this synergistic effect [90].
In the co-metabolic process, the involved enzymes can be:
• hydrolytic enzymes (esterases, amidases, and nitrilases);
• transferases (glutathione S-transferase and glucosyl transferases);
• oxidases (cytochrome P-450s and peroxidase);
• reductases (nitroreductases and reductive dehalogenases).
Ma et al. [91] have studied the co-metabolic transformation of imidacloprid (IMI), an
insecticide, testing different types of substrates used as an energy source: carbohydrates
and organic acids. P. indica CGMCC 6648 is the tested bacterium, capable of degrading
IMI through the hydroxylation pathway, and forms two metabolites: one olefin and 5-
hydroxy IMI.
4.2. Application of Microbial Remediation

The bioremediation techniques may be carried out in situ, ex situ, or on-site.
In the in situ approach, the treatment is carried out in the contaminated zone, and
typically the process is aerobic. For this, it is necessary to provide oxygen to the soil. The
main in situ techniques are:
• Natural attenuation, which exploits the microflora present in the polluted soil.
• Biostimulation, where the amounts and kind of nutrients to stimulate and promote
the growth of indigenous microorganisms are optimized.
• Bioaugmentation, which is the addition of microbial strains or enzymes into the
polluted soils.
• Bioventing, where oxygen is fed through unsaturated soil zones to stimulate the
growth of indigenous microorganisms capable of degrading the contaminants.
• Biosparging, based on the injection of air under pressure into the saturated soil zone
to increase the oxygen concentration and stimulate the microorganisms to degrade
the pollutant.
These methods are very effective and cheap. Their main advantage is that the polluted
soil is not moved.
Vice versa, in ex situ techniques, the contaminated soil is removed from polluted sites
and transported to the site where the clean-up will occur. The main techniques are:
• Bioreactors, which treat the contaminated soil with wastewater to obtain a slurry and
promote the microbial reactions capable of removing the pollutants.
• Composting, where the contaminated soil is mixed with amendments to promote the
aerobic degradation of the pesticides. Landfarming and biopiles are included in this
technique.
In on-site methods, the soil is removed and processed in the area close to the polluted
site. For example, the landfarming treatment can also be effectuated on-site, reducing the
operation cost comparing to the ex situ approach.
In all bioremediation processes, nutrients, oxygen, pH, water content, and temperature
must be controlled to maximize removal efficiency.
4.2.1. Natural Attenuation

Natural attenuation is a natural process where pollutants are degraded by indigenous
microorganisms present in the soil. The natural processes include biological degradation,
volatilization, dispersion, dilution, radioactive decay, and sorption of the contaminant onto
the organic matter and clay minerals in the soil. For example, Guerin [92] demonstrated
that endosulfan diol and endosulfan sulfate, two metabolites of insecticide endosulfan, are
both mineralized through the microbial activity present in the contaminated soils.
4.2.2. Biostimulation
The biostimulation process consists of the addition of nutrients (nitrogen, phosphorus,
carbon, and oxygen) to promote the growth of the indigenous microorganisms. These
nutrients are essential for the life of microorganisms and allow them to have energy,
microbial population, and enzymes to degrade the pollutants.
Typically, nitrogen and phosphorus are added since they stimulate biodegradation
and increase the diversity of microbial species. Betancur-Corredor et al. [93] have studied
the degradation of DDT, DDD, and DDE, stimulating the microbial population and adding
a surfactant. The number of nutrients supplied must be kept under control throughout the
process, since a reduced or excessive quantity of stimulants could reduce microbial activity
and their diversity.
Baćmaga et al. [94] have studied the degradation of tebuconazole in soil using the
biostimulation process. The tebuconazole negatively influences the enzymatic activity and
microbial proliferation; for this, its concentration in the soil must be reduced. A high con-
centration of pesticides leads to a decrease in the microbial population. The experimental
tests by these authors have evaluated the effects of two different biostimulation substances
(compost and bird droppings) on the remediation process. The results have shown that
both substances had a positive effect on the development of soil microorganisms and
enzymatic activity. The tebuconazole degradation was more intense in the soil fertilized
with bird droppings than with compost.
4.2.3. Bioaugmentation
The bioaugmentation process involves the inoculation of microbial consortia or single
strains into the soil, by augmenting the microbial diversity. In this way, microorganisms
with specific metabolic capabilities promote the biodegradation processes.
The concentration of pesticides in the soils is a parameter that conditions the pro-
cess since high doses of pesticides inhibit the vital functions of soil microorganisms.
Doolotkeldieva et al. studied the bacterial degradation of pesticide-contaminated soils
in dumping zones. In a preliminary study [10], Doolotkeldieva et al. found that several
bacterial strains were present in the studied soils. Then, they tested the degradation of
aldrin, that is a diffused chlorinated hydrocarbon pesticide. The results have demonstrated
that bacteria strains with specific genes (cytochrome P450), namely Pseudomonas fluorescens
and Bacillus polymyxa, were capable of degrading aldrin in a relatively short time. The
selection of specific bacterium, the optimization of soil conditions such as temperature,
pH, and the nutrients available in the soil, were used for the development of the next
experimental tests. In particular, mesocosms were set up with soil contaminated with
several pesticides and inoculated with the microbial consortium [76].
In contaminated soil, the pesticide concentrations can vary at different depths since
the pesticides leach into the subsurface of soil and adsorb on the soil particles, making them
less bioavailable. Odukkathil and Vasudevan [95] have evaluated the bioaugmentation
treatment in an experimental test set up in a glass column with a volume of 4500 cm3 . The
results have shown that the pesticide concentrations in the bottom soil were high, due to
the downward drift of pesticides during the water seepage, whereas the low concentrations
in the central soil could be due to higher microbial activity favoring the degradation.
Application of Natural Attenuation, Biostimulation and Bioaugmentation

Several studies have been conducted to evaluate and compare the biodegradation of
pesticides through natural attenuation, biostimulation, and bioaugmentation strategies.
For example, Bhardawaj et al. [96] have analyzed the biodegradation of atrazine with three
different techniques. Each mesocosm was set up with 100 kg of soil and contaminated with
a concentration of atrazine equal to 300 mg·kg−1 of soil. They have found that despite the
natural attenuation indicating that the soil microbiome possessed an inherent potential for
atrazine biodegradation, the natural process was slow. Conversely, with biostimulation and
bioaugmentation treatments, the atrazine was completely removed after 35 days. Moreover,
the bioaugmentation strategy was more rapid than biostimulation since after 21 days the
pollutant was degraded. Authors recommend this method for the treatment to be fast
and cheap.
The bioremediation of contaminated soils might be more efficient when coupling
bioaugmentation and biostimulation treatments [97]. Raimondo et al. [98] have tested 1
kg mesocosms polluted with lindane at a concentration equal to 2 mg·kg−1 of soil. They
have demonstrated that the removal of lindane increases and the half-life of pesticide can
be reduced using simultaneously bioaugmentation and biostimulation.
4.2.4. Bioventing
Bioventing is an in situ bioremediation technique that promotes the degradation
of organic pollutants adsorbed to the soil. The microbial activity is enhanced by the
introduction of air or oxygen flow, and nutrients into the unsaturated zone of soil through
specifically constructed wells into contaminated soils. The ventilation is light, and it is
necessary to provide the only oxygen needed to sustain microbial activity and avoid the
volatilization of contaminants.
Bioventing can be realized in active or passive mode, with regards to the aeration: in
the first case, the air is driven into the soil with a blower, while, in the passive method,
Bioengineering 2021, 8, x FOR PEER REVIEW 21 the
of 29
gas exchange through the vent wells occurs only by the effect of atmospheric pressure. The
schemes of the two aeration methods are shown in Figure 9.
(a) (b)
Figure9.9.Scheme
Figure Schemeof
ofbioventing
bioventingprocess:
process:(a)
(a)active
activetechnology
technologyand
and(b)
(b)passive
passivetechnology.
technology.
Bioventing remediation may last from 6 months to 5 years, depending on the kind
and concentration of contaminant, biodegradation rates, and characteristics of soil, such
as permeability and water content.
4.2.5. Biosparging
Bioventing remediation may last from 6 months to 5 years, depending on the kind
and concentration of contaminant, biodegradation rates, and characteristics of soil, such as
permeability and water content.
4.2.5. Biosparging
In the biosparging technique, the biodegradation process occurs by stimulating the
indigenous microorganisms through the injection of air in groundwater to increase the
oxygen concentration. The method is similar to bioventing, except that in the biosparging
the air is injected in the saturated zone. This can cause upward movement of volatile
organic compounds to the unsaturated zone to promote biodegradation. Two parameters
that influence the effectiveness of the process are (1) soil permeability, which determines
pollutant bioavailability to microorganisms, and (2) pollutant biodegradability.
4.2.6. Composting
Composting is an approach for the bioremediation of pesticides. It consists of mixing
the contaminated soil with nonhazardous organic amendments to promote the devel-
opment of bacterial and/or fungi population, able to degrade the pesticides through a
co-metabolic pathway.
This approach is particularly indicated when pesticide concentration is low. In com-
posting, the microbial bioaccessibility to the pollutant is crucial. For this reason, it is impor-
tant to control the water content, soil composition, and properties of the added amendment.
In contaminated soils, biochar can be used as an amendment to promote the degrada-
tion processes. Biochar is black carbon produced by the thermal conversions of biomass
under limited oxygen conditions (gasification) or in the absence of oxygen (pyrolysis).
It is characterized by high porosity and a large surface area; these two properties pro-
mote the adsorption of pesticides. Moreover, biochar is a carbon source that stimulates
microbial activity, promoting biodegradation. It has been noted that biochar application
increases the soil water holding capacity and improves aeration conditions in soil [99].
Sun et al. [100] have studied its application for the biodegradation of tebuconazole. This
allowed the immobilization of Alcaligenes faecalis WZ-2, the bacterial strain involved in the
degradation process.
Composting can be carried out with two techniques: landfarming and biopiles.
Landfarming
Landfarming is an aerobic bioremediation process carried out for a long time. Contam-
inated soils are transported to a landfarming zone, incorporated into the soil surface over
large areas, and periodically tilled to aerate the mixture. The kinetics of the degradation
process is slow and may also take years. During the process, leaching and/or volatilization
of toxic compounds (original compound and metabolites) must be controlled or prevented.
To avoid any risk of infiltration, a waterproof cover must be in place on the soil before the
start of the treatment. This treatment is applied especially to soils contaminated with a
mixture of pollutants.
Biopiles
Biopiles are piles of contaminated soil, equipped with a piping system that permits the
aeration. During the process, air or oxygen is sent, and a solution containing nutrients is
applied to the soil surface to stimulate microbial activity. The parameters that influence the
process are water contents, temperature, pH, and concentration of nutrients and oxygen
that must be controlled to enhance biodegradation.
4.2.7. Slurry Bioreactors

In slurry bioreactors, the contaminated soil is mixed with wastewater up to obtain a
slurry with aqueous suspensions between 10% and 30% w·v−1 . The bioreactor can be oper-
ating under aerobic or anaerobic conditions. Baczynski et al. [101] studied the anaerobic
biodegradation of organochlorine pesticides. They used methanogenic granular sludge

as inoculum for anaerobic treatment of soil contaminated by γ-hexachlorocyclohexane,
methoxychlor, o,p’- and p,p’-DDT. The pollutants were removed to a good extent at all
tested temperatures (12, 22, and 30 ◦ C) without a lag phase. Low temperature reduces
the removal rates of pesticides. This might be due to the reduction of desorption rates of
slowly desorbing fractions of these pollutants. In another study [102], the same authors
found that the rapidly desorbing fractions were not a good indicator for the evaluation of
the bioremediation process. Instead, the determination of slowly desorbing fractions can
be better used for this purpose.
4.3. In-Field Applications

At present, few studies report information on real case studies.
Table 9 summarizes some examples. Unfortunately, the findings and results of large-
scale remediation are usually neither published nor widely publicized, limiting the knowl-
edge of experiences on real cases. A similar situation occurs for the costs of the clean-up.
Table 9. Some examples of case studies.
Bioremediation
Pesticides Description References
Technique
Contaminated soil with HCH isomers (>5000 mg·kg−1 )
derived from lindane production was studied in the field for
Hexachlorocyclohexane 11 months, setting up two plots (each 2 m × 10 m). The α-
Landfarming [103]
(HCH) isomers (insecticides) and γ-HCH isomers were decreased by 89 and 82% of the
initial concentration, respectively. The concentration of the
most persistent β-isomer remained essentially unaffected.
Experimental tests were conducted on vineyard plots. In the
crops, an agricultural formulation of pesticides by foliar
spray was applied. After one h of pesticide application,
vines were sprayed with a suspension of four Bacillus
Myclobutanil, tetraconazole,
Bioaugmentation strains. DR-39, CS-126, TL-171, and TS-204 were tested. [104]
and flusilazole.
Residue analysis of field samples showed 87.4 and >99%
degradation of myclobutanil and tetraconazole, respectively,
by the strain DR-39, and 90.8% degradation of flusilazole by
the strain CS-126 after 15−20 days of treatment.
The bioremediation process was studied in 12 experimental
plots, including greenhouse and open field soils. Each plot
(area of 6 m2 ) was inoculated with Stenotrophomonas sp.
Bioaugmentation DDT DDT-1 supplemented with 2% yeast powder. The results [105]
have shown that this microorganism is efficient for DDT
degradation and does not adversely affect soil
microbial activity.
The Borello Property is a 14 acre area treated with soil
amendment to help the indigenous bacteria to metabolize
the pesticides. For the analysis, the area was divided into
Organochlorine pesticides:
zones and in each of them, the soil samples were collected
toxaphene; DDT; DDE; DDD;
Biostimulation from four soil depths (0.5, 1, 1.5, and 2 ft). At the end of the [106]
endosulfan II; γ-chlordane;
test, OCPs were not detected; toxaphene, DDT, and DDE
α-chlordane; dieldrin.
were detected in a single sample; dieldrin was detected in
five samples at concentrations ranging from 1.2 to
1.8 µg·kg−1 .
The Mantegani Property is a 0.8 acre area treated with soil
Organochlorine pesticides: amendment to help the indigenous bacteria to metabolize
toxaphene; DDT; DDE; DDD; the pesticides. High concentrations of DDT and dieldrin
Biostimulation [106]
endosulfan II; γ-chlordane; were present. After treatment, DDT was degraded by 97%
α-chlordane; dieldrin. and dieldrin by 73%, while the concentrations of other
OCPs were below their preliminary remediation goals.
5. Legislation
The necessity of having sustainable food production and a reduction, or even a ban,
of the use of pesticides, has made it so that each country in the world is committed to
implement measures and laws in this regard. Dealing with the topic at the world level, the
Food and Agriculture Organization of the United Nations (FAO) and the World Health
Organization (WHO) have released a pair of updated guidelines on pesticide legislation
and labeling. A code for pesticide legislation has been published in 2020 [107], aiming to
guide governments that seek to review, update, or design national pesticide legislation.
5.1. European Union

In the European Union, the sustainable use of pesticides is ruled by Directive 2009/128/
EC [108]. The aim is to reduce the risks and impacts of these chemicals on health and the
environment.
Moreover, Regulation (EC) 1107/2009 [5] contains the criteria and rules to authorize
the active substances of pesticides and plant protection products (PPPs) and their placement
on the European market. Pesticides cannot be marketed and used if they have not been
previously approved and authorized by this procedure.
The institution which deals to evaluate active substances contained in pesticides is the
European Food Safety Authority (EFSA). EFSA supports the European Commission, the
European Parliament, and the EU member states in taking effective and timely risk man-
agement decisions to ensure the protection of the health and the safety of the food and feed
chain. Each EU member state evaluates and authorizes the products with national laws.
In the member states, Regulation (EC) No. 1107/2009 [5] has been underpinned by
national laws through the formulation of more precise stipulations at the national level.
In particular, the National Action Plans include quantitative objectives, targets, measures,
and timetables, and they are to be reviewed at least every 5 years. The first National
Action Plans were communicated to the Commission in 2012, and a report by the EU
Commission [109] has shown that in 2017 all Member States had plans in place.
5.2. United States of America

In the United States, the regulation and monitoring of pesticides are ruled by three
government agencies:
• The U.S. Environmental Protection Agency (EPA) registers and approves the use of
pesticides and establishes the maximum amounts of residues that are permitted inside
or on food.
• The U.S. Department of Agriculture (USDA) is responsible for the enforcement of
pesticide tolerances primarily in meat, poultry, and certain egg products.
• The U.S. Food and Drug Administration (FDA) is responsible for the enforcement of
pesticide tolerances in other food categories, both domestic and imported ones.
The EPA regulates the use of pesticides considering two federal statutes: (1) the Federal
Insecticide, Fungicide, and Rodenticide Act (FIFRA), enacted in 1947 and updated with
new amendments [110]. It regulates the registration, distribution, and use of pesticides,
including the toxicology, environmental fate, and ecotoxicology and residue chemistry; (2)
the Federal Food, Drug, and Cosmetic Act (FD&C). It establishes tolerances or safe levels
of pesticide residues in raw agricultural commodities. The updated act is FD&C 2021 [111].
The EPA works cooperatively with the state agencies to review pesticide safety data,
register products, educate professional applicators, monitor compliance, and investigate
pesticide problems. State governments develop regulations that are stricter than the federal
regulation given by EPA.
5.3. India
In India, the pesticide regulation was applied for the first time in the insecticide
act [112], by the Ministry of Agriculture, Department of Agriculture and Cooperation in
1968. Since 1971, the insecticide rules [113] have been in force: they regulate the import,
sale, transportation, manufacture, and use of persistent pesticides.
Under this act, all insecticides must be recorded by the Central Insecticides Board
(CIB) and Registration Committee (RC). The CIB and RC scrutinize and periodically review
all pesticides, before authorizing their sale and use. Moreover, they have the authority to
ban environmentally threatened pesticides even after their registration.
5.4. Regulation in Other Countries

The regulations on pesticides in other countries are more recent.
In China, the Ministry of Agriculture is responsible for the enforcement of the Law on
Quality and Safety of Agricultural Products and the Regulation on the Control of Agro-
chemicals. The National Food Safety Standard—Maximum Residue Limits for Pesticides
in Foods [114] was approved in 2012 and updated several times in the following years to
add other maximum residue limits of pesticides in foods, until the current version released
in February 2021 [115].
In Japan, the pesticide regulation is contained in the Food Safety Basic Law, enacted in
2003 [116]. This law sets the principles for developing a food safety regime and defines the
maximum acceptable concentration limits of residual pesticides. A limit of 0.01 mg·kg−1 of
soil applies to compounds for which tolerance limits have not been established.
6. Conclusions
After the Second World War, the use of pesticides and plant protection products
has grown heavily, both in developed and developing countries. Unfortunately, all these
compounds are toxic to different extents and impact human health and the environment.
Moreover, many of them are persistent; that is to say, their degradability is very limited
and occurs for long times.
Soil bioremediation for their removal can be carried out exploiting either specific or
indigenous microorganisms (bacteria and fungi), or enzymatic degradation.
While at a laboratory scale, many findings on soil bioremediation are available in the
literature, few data on real-scale activities can be found. Unfortunately, this is mainly due
to the poor cooperation among research laboratories, local authorities imposing a given
soil clean-up, and companies involved in the sector of bioremediation in soils polluted
with pesticides.
It would be beneficial that more and more this cooperation becomes united, to dissem-
inate the experiences and results. Moreover, the cost data are lacking, too.
As for other pollutants, when required, the pesticide removal must take into account
the chemical and toxicological characteristics of the compounds, without disregarding
the national legislation. To this purpose, it must be outlined that several countries are
still lacking in legislative acts, and this is the main drawback when polluted areas must
be remediated.
Author Contributions: Writing—original draft preparation, C.M.R.; writing—review and editing,

C.M.R. and F.C.; supervision, F.C. Both authors have read and agreed to the published version of
the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: Not applicable.
Conflicts of Interest: The authors declare no conflict of interest.
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bioengineering

Bioengineering 2021, 8, 92. https://doi.org/10.3390/bioengineering8070092 https://www.mdpi.com/journal/bioengineering

Figure 1. Pesticides use per area of cropland (data from [4]).

Figure 2. Pesticides use from 1990 to 2016 (data from [4]).

Table 1. Reviews on pesticides.

Pyrethrins and Pyrethroids

Interaction with sodium ion channels in neurons, ca

Interference with nerve signaling by

Interruption of functioning of the

Inhibition of cholinesterase prevents the breakdown

Interference with nerve signaling by inhibition of t

Imitation of plant growth hormone auxin

Inhibition of the photosynthetic

Inhibition of vitamin K epoxide reductase

Anticoagulant agent depressing hepatic syn-

• moderately persistent, when t1/2 is in the range 30–100 days;

3.1.1. Adsorption by Soil Particles

3.1.2. Degradation Processes

3.1.3. Leaching from Soil to Water

3.2. Toxicity and Short- and Long-Term Damages

Table 7. Criteria for classification of pesticides.

LD50 for the Rat

Figure 5. LD50 (mg·kg−1) of organochlorines for the rat.

4. Biological Techniques for Pesticide Removal

4.1. Mechanisms of Microbial Degradation

4.1.1. Bacterial Degradation

4.1.2. Fungal Degradation

4.1.3. Enzymatic Degradation

Table 8. Microorganisms capable to degrade several pesticides.

Target Pesticide Microorganism References

4.2. Application of Microbial Remediation

4.2.1. Natural Attenuation

Application of Natural Attenuation, Biostimulation and Bioaugmentation

4.2.7. Slurry Bioreactors

biodegradation of organochlorine pesticides. They used methanogenic granular sludge

4.3. In-Field Applications

Table 9. Some examples of case studies.

5.1. European Union

5.2. United States of America

5.4. Regulation in Other Countries

Author Contributions: Writing—original draft preparation, C.M.R.; writing—review and editing,

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