JEMAT, 2020, Vol 8, No 1, 50-57

JOURNAL OF ENVIRONMENTAL MICROBIOLOGY

AND TOXICOLOGY
Website: https://journal.hibiscuspublisher.com/index.php/JEMAT
JEMAT VOL 8 NO 1 2020
SEM of Durio zibethinus

Biodegradation of Carbofuran; A Review

Fazillah Ariffin1 and Sukirah Abdul Rahman2*
1
School of Fundamental Sciences (PPSA), Universiti Malaysia Terengganu (UMT),
21030 Kuala Terengganu, Terengganu, Malaysia.
2
Biotechnology Research Centre,Persiaran Mardi - UPM, Mardi,
43400 Serdang, SelangorSelangor, Malaysia.

*Corresponding author:

Sukirah Abdul Rahman

Biotechnology Research Centre,
Persiaran Mardi - UPM,
Mardi, 43400 Serdang,
Selangor,
Malaysia.
Email: sukirah@mardi.my

HISTORY ABSTRACT
Pesticides are substances used for the destruction or control of pest. They include insecticides,
Received: 24th June 2020
Received in revised form: 28th June 2020
herbicides, fungicides, rodenticides rats and mice, molluscides and others. Carbofuran is an
Accepted: 1st July 2020 insecticide that is very toxic pesticide often used to control pests in agricultural areas. Its usage
is still being reported despite worldwide efforts to ban the pesticides. Reported deaths and illness
KEYWORDS due to indiscriminate and excessive use of carbofuran is still being reported in developing and
pesticides third world countries prompting the call of more research on isolating microorganisms that are
biodegradation
carbofuran
able to completely mineralize this toxic pesticide. The presence of toxic carbofuran in various
bioremediation soil types that can persist for many months can be remediated via the use of carbofuran-degrading
Malaysia microorganisms which is a more feasible and economical methods of remediation compared to
various physicochemical methods. The aim of this review is to highlight the toxicity of
carbofuran, especially in the Malaysian perspective and the current body of knowledge on
carbofuran-degrading microorganisms that are able to remediate this toxic threat.

INTRODUCTION In the developing countries, particularly in North America,

Western Europe and Japan, pesticides have come to play an
Pesticides may be of the broad-spectrum type that kills a wide extremely important role in the maintenance of high agriculture
range of organisms or the selective type, which destroys only one productivity. Despite the uses of pesticides, about 35% of the
organism or a few specific organisms. In the early part of this crops are lost from pests, diseases and weeds. Worldwide FAO
century the increase in world population resulted in a greater estimates that an average of 38% of the cotton crop is saved from
demand for food. It has led to a substantial increase in the destruction by pests through the effective use of pesticides.
production and use for agrochemical such as pesticides and However, pesticides have been known to affect a number of non-
fertilizers [1–7]. target organisms. Many experts have approximated that only a
small percentage roughly about 0.1% of the pesticides used on
Pesticides are very known to contribute significantly in crops get to their target pests and most 99% of the utilized
reducing losses and thereby increasing food production and pesticides have an effect on non-target organisms [8,10–16].
quality. Past trend indicates that most of the pesticides used in the
developing countries have frequently been employed in the A good example is the decline in paddy field fish
control of vectors of human disease and on industrial export populations due to increased pesticide usage, causing severe
crops. Roughly one thousand pesticide preparations are utilized economic hardship and nutritional deficiencies among the poorer
around the world today. The yearly globally agriculture paddy farmers. The rice growing areas of central Thailand,
utilization of pesticides has been approximated to be in the order farmers use the food irrigation method where when they drain the
of five million tons and approximately seventy percent is utilized water from the rice paddies into the rivers and canals, carrying
in farming and the rest by public health agencies and government pesticides residues to nearby agricultural farms. In December
departments for vector control and for household goals [5,6,8,9]. 1982, this practice resulted in the complete destruction of the
aquaculture industry in central Thailand. Over US$10 million
worth of fish were killed and about 5 million kilograms of fish

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were lost due to pesticides poisoning. This affected people build up into food chains many years after their use in soil [28].
throughout the country because fish is a major source of cheap Pesticides range of motion is important for pest management. For
protein [17]. Pesticides induced chronic toxicity is emerging as a instance, particular pre emergence herbicides used on the soil
public health concern including cancers, reproductive surface area must shift several inches into the soil to arrive at the
impairment and irreversible neurotoxicity. According to the germinating weed seeds. There are actually five processes that
World Health Organization (WHO), over half a million people may shift pesticides including runoff, volatilization, leaching,
are poisoned each year by pesticides and five thousand of the physical removal and absorption. Due to its good water solubility
victims die [18]. (351 mg/L at 25 oC), carbofuran is comparatively mobile in soil
and in surface runoffs and is expected to partition into the water
Toxicology of Pesticides in General from soil [31]. As an example, it is estimated that carbofuran,
Pesticides (whether insecticides, herbicides or fungicides) by which is widely utilized in paddy soil remains in the water at
their nature and purpose are poisons. Even if their amount is about 54% and in soil of about 46%.
minimal in comparison to that of silt, their impact on the
environment may be considerable. Since 1962, the use of Pesticides Degradation
pesticides in the Unites States has increased more than two-fold. During pesticides degradation, some of the metabolites can also
It now endangers groundwater quality in most of the States [19]. become more toxic than the original compound. The vast
Recently, concern about effects of pesticides on human health majority of pesticides residues in the environment are turned into
and on the ecosystem began to move beyond cancer. It appears non-active or less poisonous or harmful chemical substances by
that some chlorinated hydrocarbon pesticides exert a multitude means of primarily chemical degradation, photo degradation and
of toxic effects. These pesticides are neurotoxic, mutagenic and microbial degradation [4,6,32–38].
teratogenic. They exert toxic effects on the reproductive system
and suppressed the immune system. These compounds act by Chemical Degradation
mimicking or inhibiting estrogen receptors. It also affects Chemical degradation of pesticides is a degradation process
women’s health but also believed to be responsible for a decrease which do not include living organisms. Examples of chemical
in sperm count and a rise in testicular cancer in human as well as degradation of carbofuran include oxidation-reduction,
abnormal sexual development in some wildlife species [20]. hydrolysis and ionization which can be generally associated with
pH. Just about the most common pesticides breakdown is
Pesticides in Soil hydrolysis, a degradation process in which the pesticides interact
Soil in the environment consist of numerous ecosystems where with water. It might happen in both acid and alkaline conditions.
recycling of organic matter occurs. Soil microflora which consist As soil pH gets to be highly acidic or alkaline, microbial activity
of bacteria, fungi, protozoa and algae play a major role in nutrient generally reduces, but such circumstances may lead to elevated
cycle. This is because of the capability of using the organic matter chemical degradation [4,6,32,33,38].
as a source of nutrient. Examples of these process are .
nitrification, denitrification and carbon mineralization [21–27].
Hydrolysis
Several studies have shown that pesticides behavior in soil The most crucial reaction involves hydrolysis, which is the
are influenced by the absorption, motility and degradation splitting of a bond in a molecule by way of its reaction with a
process. Adsorption of pesticides to soil particle is a vital course water molecule. Usually a compound is modified in a hydrolytic
of action impacting on their migratory conduct in numerous soil reaction by the replacing of chemical groups of the substance
environments. The characteristics absorption and desorption and with a hydroxyl group. The hydrolytic reactions are generally
the mobility of the pesticides 2,4-D, lindane, paraquat and catalyzed through the reactions of hydrogen or hydroxide ions
glyphosate in the soils of two Malaysian agriculture show and therefore the reaction rate is firmly determined by the pH of
variability in absorption and desorption properties [28]. In the the environment. A number of functional groups that are prone
research, it was observed that the absorption-desorption to this hydrolytic reactions include lactones, carboxylic acids
attributes and leaching behavior of the above pesticides ester, amides, epoxides, carbamates, phosphoric- and sulfonic
demonstrated little variations from the results documented in acids esters [4,6,38–40].
soils from other areas of world. The inclination of these .
pesticides to be absorbed by soil particles differs with their
chemical and physical qualities. Absorption of paraquat in soil Oxidation –Reduction (Redox)
was very fast and binds tightly to the soil particle especially in Oxidation –Reduction (Redox) reactions involve the transfer of
clay and loam [29]. electrons from the reduced species to oxidized species. It has
been shown that mixed function oxidase (MFO) enzymes are
Pesticides absorption-desorption characteristics are capable of catalyzing aromatic hydroxylation, dealkylation,
measured by partition coefficient. Research carried out to the deamination, desaturation, expoxidation and N-or-S oxidation.
mobility of carbofuran in two soil types demonstrated only slight Several of these mechanisms occur sequentially to form
variations between adsorption coefficients. The study degradation products. For example, the reaction of N-
demonstrates that carbofuran exhibited a Kd value of 22.4 in clay dealkylation can occur at the carbamate amine. The oxidative
loam (OC content 53%, pH 8.6) and a Kd value of 19.9 in silt metabolic of the ring hydroxylation is important in the
loam (OC content 18%, pH 8.4). Therefore, higher adsorption of metabolism of carbaryl and carbofuran. In this process it
carbofuran occurs in the presence of a greater organic matter probably proceeds through epoxidation to the hyroxy compound
[30]. and then to the keto and eventually to ring cleavage. Some
compounds in which redox reactions have been observed to be
The absorption pesticides in soil are very important because important include mercury, toxaphene and DDT [41,42].
it can lead to environmental problems. Pesticides that do not bind
to the soil particle will be degraded to produce less toxic Ionization
metabolites while in comparison, adsorbed pesticides will The hydrogen ions in the water body determine the fate of toxic
continue to be in the surroundings for a number of years and may organics which are possibly acids or bases. The hydrogen ion

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concentration influences the ionic species of many compound diseases to people and animal [6,36,58,74–76]. At the moment,
including pesticides. For example, the ionized species of an the effective use of pesticides is in depth and agriculture,
organic acid is to a much lesser degree absorbed by sediments horticulture, vector control and forestry and livestock production
than its neutral form [43]. are the reason for the highest usage. The pesticide market in
Malaysia is increasing over the years with herbicides still
Photo degradation accounting for the highest rate at 75 % followed by insecticides
The breakdown of pesticides by light especially sunlight is called at 16 percent, fungicides at 5.4% and rodenticides at 3.5 % [77].
photo degradation. It is a degradation process where energy in The insecticides are used in Malaysia mainly for vegetables, rice,
the form of photons smashes the bonds in a molecule (USEPA, cocoa, fruits, oil palm and tobacco. The major insecticides used
1987). It can demolish pesticides on vegetation, on the soil are BHC, endosulfan, chlorpyrifos, carbofuran and carbaryl in
surface as well as in the air. Normally, the factors that affect rice fields. The major herbicides used are gyphosate, paraquat,
pesticides photo degradation range from the level of the sunlight, 2,4-D and lindane [78–88].
especially its intensity, qualities of the application sites, the
method of application and the attributes of the pesticides. Mill In Malaysia, the main legal guidelines for the control of
and Mabey (1985) illustrate the types of photolysis reactions pesticides is the Pesticides Act of 1974. Normally the principal
impacting on many different substances such as chloroaromatics, purpose of this act is the control of the production and import of
ketones and aldehydes. pesticide by means of registration and licensing of premises
marketing, storing, selling, labeling and management of the
Research has shown that a quantity of pesticides is broken import of unregistered pesticides for research and academic
down at quantifiable rates of sunlight. Such is the situation that applications [86].
the number of pesticides not broken down by sunlight is very
small. In fact, circumstances can be obtained to which almost all The health impacts of pesticides on human and other
current day herbicides and plant - growth regulators will be organisms in Malaysia are expected to rise as the use of pesticides
decomposed by sunlight. Examples of herbicides that have been in the agriculture area increases. Nowadays, the use of pesticides
proved to be successfully degraded by sunlight involves 2,4-D, in Malaysia is a cause of serious concern. Some pesticides have
MCPA, 2,4,5-T, silvex and bromoxymil [44], simazine, monuron been shown to be toxic to the environment as well as human
and diuron [45]. himself. Between the years 1970 and 1982 there were about one
hundred cases of organophosphate poisoning needing admission
to the University Hospital Intensive Care Unit in Kuala Lumpur
Microbial degradation [2]. Data from the Ministry on pesticides poisoning from 1979 to
The breakdown of pesticides by microorganisms usually results 1986 were associated with the pesticide paraquat with 49.1% of
in the pesticides becoming food source for growth and energy. It the cases are intentional and the remaining 37.8% are accidental.
is now naturally revealed that microorganisms not just break In the paddy field areas in Tanjong Karang, it was reported that
down natural organic materials, but they are also accountable for about 72% of rice farmers experienced poisoning signs and
the the breakdown of many other xenobiotics. These substances symptoms when dealing with pesticides. It has been found that in
include petroleum hydrocarbons, pesticides, and organic these places, proper attire and clothing including googles, shoes
solvents. Transformation of contaminants to less dangerous and respiratory masks were hardly ever worn [89].
materials via biodegradation is highly likely in the case of
mineralization while in under certain situations more often seen The levels of pesticide found in the blood serum of the
under anaerobic transformation, toxic products can also be general Malaysia population are much higher than that of the
produced [46–62]. United States. The total mean DDT concentration in Malaysia
farmers was 0.11 ppm, the level for rubber estate workers was
Microbial degradation as a tool for bioremediation 0.09ppm and the level for the general population was 0.066 ppm.
Basically, the mineralization or total biodegradation of an The impact of this unhealthy trend of excessive pesticides usage
organic molecule for example pesticides in soils is practically in Malaysia will result in adverse effects in the environment and
constantly a result of bacterial activity. As they transform the the wellbeing of the people [81].
organic substrate to inorganic products, the accountable
population utilizes a number of the carbon in the substrate and It was also observed that the high accidental and
turns it to cellular components. Simultaneously, energy is occupational exposure of workers and the general population to
produced, and the populations increase in quantities and biomass pesticides further confirm this unhealthy trend. Estate workers
as they absorb a significant number of the carbon for energy and formed the majority of all pesticide’s poisonings in Peninsular
biomass. Carbofuran, like many other pesticides is a soil- Malaysia. There is a wide use of organophosphorus insecticides
incorporated pesticide which has been confirmed to be affected and rodenticides in the agricultural sector especially in oil palm
by microbial degradation. The majority of pesticides at present is plantations. Problem arise because estate workers are generally
being used and have been found in the biosphere for more than unaware or not made aware of the color coding of these
forty years but a number of these substances are speedily hazardous chemicals.
microbially broken down in soil [60,63–73].
Long term exposure has led to several illnesses such as
pulmonary, eye, skin, and neurological problems [90]. Various
Pesticides contamination in the Malaysian environment factors have contributed to the acute poisoning cases which
Contamination of the Malaysian environment is becoming an include the use of pesticide (by farmers) in concentration in
escalating issue throughout the last one hundred year with the excess of requirements, poor knowledge and understanding of
continuing development of industry and agriculture and with the safe practices in pesticide use, lack of protective clothing suitable
advancement human population. Not long ago, there has been an for tropical climates, the poor maintenance facilities of spray
increase reports of pesticides contamination from the agriculture equipment, giving rise to hazardous contamination and the use of
use of fertilizers and pesticides. In Malaysia, pesticides are pesticide mixture [91].
widely-used to manage pests that damage crops and broadcast

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Carbofuran (C12H15NO3 ) correlate with an increased osmotic fragility of erythrocytes.

Carbofuran (2,3-dihydro-2, 2-dimethyl-7-benzofuranol N [110]. In female Swiss albino mice, the interruption of estrous
methylcarbamate) is a broad-spectrum carbamate acaricide, cycle and follicular toxicity caused by carbofuran exposure has
insecticide and nematicide. It is widely used towards quite a few been documented [111] where the estrous cycle was effected with
unwanted pests of agricultural products including rice, corn and a significant decrease in the duration of each phases of the estrous
on other agriculturally important plants. Carbofuran is utilized to cycle and its number as well as a concomitant significant
manage soil-dwelling and foliar feeding pesky insects for increase in the diestrus phase [112]
example wireworms, corn rootworm, boil weevils, alfalfa weevil,
mosquitoes, white grubs and aphids [3,7,92–94].
Bioremediation
Bioremediation is using microorganisms or plants to clean or
detoxify the environment. It is an option which offers a solution
to detoxify or at least lessen the toxicity of the substances in the
environment. It is a natural process using living organism,
primarily microorganisms to remediate the environment
contaminants into less harmful forms. It is a course of treatment
that employs microorganisms to degrade substance that are
detrimental to human health and environmental surroundings.
Typically, microorganisms make use of organic compounds to
Fig. 1. Chemical structure of carbofuran produce energy and nutrients for their growth. Bioremediation
can happen under aerobic and anaerobic circumstances.
Carbofuran was initially utilized in a commercial sense in 1967
and its particular use is continuing to grow speedily more than In aerobic situation, microorganisms make use of
following years. Its half-life in soil is from thirty to one hundred atmospheric oxygen and will transform numerous organic
and twenty days. In sandy soils, the half- life is approximately pollutants to CO2 and H2O. Whilst under anaerobic condition,
thirty days while the intermediate half-life in loamy soils is about reactions take place solely without molecular oxygen
forty days. Its half-life in muddy soil is about eighty days [94]. [26,27,62,113–120]. Bioremediation can be performed either ex-
Its molecular weight is 221.25 with a melting point of between situ or in-situ. The ex-situ process requires excavation of
150 and 152oC. Under neutral or acidic conditions, it is contaminated soil before they can be treated. While, in the in-situ
comparatively stable but breakdowns rapidly in alkaline media. process, remediation is carried out in the location without
Carbofuran is soluble in water at concentrations of up to 700 excavation or removal of contaminated soil. In the case of in-situ
mg/L in water but in organic solvents its solubility reduces to less bioremediation several successful cases have been reported and
than 30 mg/L [93]. the target pollutants remediated include chlorinated pesticides,
halogenated aliphatics, nitroaromatics, polychlorinated
Sign and symptoms of poisoning biphenyls, and polycyclic aromatics [26,27,62,116–118].
Carbofuran is a highly toxic compound when inhaled and
moderately toxic through dermal absorption. Symptoms of acute Bioremediation can be carried out by four basic techniques.
toxic exposure include nausea, excessive salivation, abdominal To begin with, the microbes may end up being immediately
cramps, vomiting, sweating, weakness, diarrhea, imbalance, employed to degrade pollutants. Secondly, in-situ spiking
breathing difficulty, blurring of vision, increased blood pressure nutrients may be utilized to stimulate the growth of indigenous
and incontinence. The rapidity, with which these symptoms microbes capable of decontamination. Thirdly, cell extracts or
appear, is dependent on the amount of toxicant administered, purified enzyme products of microbial origin could be used for
chemical structure of the toxicant, mode of entry into the body, decontamination. Finally, plants can often be used to eliminate or
biochemistry and physiology of the animal treated [95–101]. transform pollutants. Presently, scientific studies are being
carried out on the utilization of microorganisms to break down
Mode of action cholinesterase inhibition by carbofuran chemicals.
Generally speaking, carbofuran successfully manages insects by
means of its action on as an anticholinesterase activity. Methods and resources for the design of new microbes are
Acetylcholinesterase (AchE) inhibition by carbofuran is already been created. Included in this are the design of regulated
substantially studied in the past years. In both invertebrates and gene expression circuits that limit catabolic activities and the
vertebrates, carbofuran act by suppressing the enzyme assemblage of gene blocks coding for chosen metabolic modules
acetylcholinesterase (AchE), which is an enzyme important for to produce new metabolic routes. As with many chemicals,
regular nerve functionality inside the peripheral and central pesticides are subject to both biotic and abiotic transformation
nervous systems. Cholinesterases are the enzymes that carry out process. Many of the abiotic transformations result in partial
neuromuscular and interneuron transmission and switch on degradation to products that can be further degraded by
various intracellular reactions in a number of tissues and cell microorganisms. Hydrolytic reactions are the most significant
varieties [102–107]. Death can happen consequently coming abiotic transformations. The reactions can be base or acid and
from asphyxiation resulting from extreme activation in nerves occurred through interactions surface, reactive organic
due to the buildup of acetylcholine at the nerve synapses of the compounds and inorganics metal such as Cu2+ [26,27,62,113–
central nervous system and resulting in the subsequent failure of 120].
the respiratory process [31,96,108,109].
Carbofuran-degrading microorganisms
Other effects of carbofuran toxicity Carbamates and organophosphates are currently, the most
Organophosphate and organocarbamate pesticides including employed insecticides for indoor and agricultural purposes. Even
carbofuran can cause oxidative stress in erythrocytes. As the though they are biodegradable, they display neurotoxicity in
erythrocytes harbor polyunsaturated fatty acids and hemoglobin, mammals. Carbofuran, a class of carbamates is usually applied at
they are prone to oxidative stress where the latter increase may the time of planting to control numerous insects in various

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agricultural plants. It is important that the carbofuran persist in Hydrolase activity was determined to be optimum at pH 8.5 and
the soil for 3-5 weeks after planting to control the feeding larvae 37oC [137].
[98,101,121–125]. Microbial deterioration of this compound
continues to be analyzed and the effectiveness of carbofuran in In conclusion, carbofuran, an important pesticide has many
the field is diminished and reapplication needs to be carried out uses in agricultural and nonagricultural purposes. Bioremediation
as a result of the phenomenon of increased microbial can provide a cost-effective method compared to existing
degradation. It was suggested that bacteria contained in the area physicochemical methods provided that a suitable
have the ability to make use of the bacteria as a substrate for microorganism can be found to completely mineralize carbofuran
growth [98,123–125]. completely. The purified enzyme shows diverse substrate
specificity and stability conditions also varied considerably.
It has become increasingly possible to isolate microorganisms Novel carbofuran-degrading enzymes need to be isolated and
that are capable of degrading xenobiotic and recalcitrant characterized specifically from developing and underdeveloped
compounds from environments polluted with toxic chemicals. countries where carbofuran is still being used despite worldwide
Several microorganisms are responsible for the metabolism ban.
pesticides in soil. The degradation of several carbamates
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