Title


Indonesian Journal of Environmental
Management and Sustainability
e-ISSN:2598-6279 p-ISSN:2598-6260

Research Paper

Bioremediation Techniques for contaminated Land: Focusing on Land

Contaminated by Petroleum Hydrocarbon Pollutants

Wahyu Dian Silviani1

1Faculty of Mathematics and Natural Science, University of Mataram, Jl. Majapahit no. 62 Mataram

*Corresponding author e-mail: silviani.wahyu@gmail.com

Abstract
Oil spills on land is one of major environmental issues. The spills have been known to affect not only environment but also
human health. Certain bioremediation techniques, biostimulation, bioaugmentation, and land farming, have been widely
applied to solve the problem. Approaches using these methods, over the years, have given varying result and rate of success.
Generally, biostimulation and bioaugmentation are preferred since they are more practical and cost effectives compared to
land farming. However, geographical structure of subsurface and competition among indigenous microorganism are of major
concerns when applying biostimulation. For bioaugmentation, the ability of the new engineered microorganisms to survive the
new environment and to find its way to the pollutant are also big challenges. Therefore, finding the best bioremediation
methods that effectively can degrade oil spill must be done carefully. In this paper, advantages, disadvantages, and limitation
of the methods when applied will be discussed.

Keywords
Biostimulation, Bioaugmentation, Land Farming, Oil Spill

Received: 21 August 2020, Accepted: 26 September 2020

https://doi.org/10.26554/ijems.2020.4.3.70-77

1. INTRODUCTION

Land contaminated by petroleum hydrocarbon is one of
environmental problems that have been long causing serious
impacts to both environment and human. Numerous cases
of oil spills containing petroleum hydrocarbons on land have
been reported consistently from many countries in the world.
Newer cases usually occur in oil producing countries, such
as in Mexico where 1284 Ha of soil is contaminated [1]. In
Nigeria, over 13 million tonnes of oil has been spilled in
Niger Delta and contaminating food chain in the area (Sam
and Zabbey, 2018). Similar cases are also reported in Libya
Alzien et al. (2019), Kuwait Mostagab et al. (2018), Iraq
(Arbili and Karpuzcu, 2018). Various methods, like chemical
and mechanical treatment methods have been developed
over the years to find the best way to deal with the problem
(Okoh et al., 2019). However, the outcome of those methods
applications is often environmentally unsustainable and not
cost effective. As a result, alternative methods which are
more economically and environmentally sustainable are pre-
ferred. Bioremediation is one of them (Okoh et al., 2019).
This method utilizes microbes, plants, and earthworms abil-
ity to degrade various types of contaminants Sinha et al.
(2009). The method is economically profitable since the

treatment cost is generally lower compared to other treat-
ment methods Megharaj et al. (2011). Another advantage
of the method is it does solve the contamination problem
permanently, unlike the conventional method which usually
moves the problem to other places Gordon et al. (2018).
This method also does not harm environment for there
is no involvement of hazardous chemical (Perelo, 2010a).
Simple maintenance and “applicable over large areas” are
other factors that make bioremediation more attractive to
be implemented (Perelo, 2010b). In this review, focus of
the discussion will be on bioremediation techniques that
utilize microorganisms that already live in the soil. The
techniques are biostimulation, bioaugmentation, and land
farming. The techniques will be discussed using land con-
taminated by petroleum hydrocarbon pollutant cases. This
review will be divided into three parts of discussion. The
first part will discuss both environmental and health im-
pacts of petroleum pollutants on soil. It will be followed by
discussion of bioremediation methods that could work to
resolve the contamination of petroleum hydrocarbon on land.
Advantages and disadvantages of each proposed treatment
will be discussed in this part. Lastly, a conclusion of this
review is presented.

https://doi.org/10.26554/ijems.2020.4.3.70-77


Wahyu Dian Silviani Indonesian Journal of Environmental Management and Sustainability, 4 (2020) 70-77

2. RESULTS AND DISCUSSION

2.1 Environmental and health effects of petroleum
hydrocarbon pollutants

2.1.1 Environmental effects
Impacts that petroleum hydrocarbon spills caused to the
environment is profound. The impacts may vary depend-
ing on the amount and types of petroleum hydrocarbon
contaminating the land (Baker, 1970). External factors,
such as time of spills as well as weathering degree, also
determine level of damage petroleum hydrocarbon left on
soil (Baker, 1970). Once petroleum hydrocarbon contam-
inates soil, it can damage soil properties, chemically and
physically (Wang et al., 2013). According to Sutton et al.
(2012), the presence of petroleum hydrocarbon stimulates
formation of anaerobic environment in soil (Sutton et al.,
2012). This can happen because petroleum hydrocarbons
are able to smother soil particles by preventing soil pores
from getting air diffusion (Sutton et al., 2012). Furthermore,
the hydrocarbons film can also be formed when oil is spilled
on the soil (Gordon et al., 2018). In addition, the presence
of petroleum hydrocarbon also increases oxygen demand
needed by microorganisms to decompose the oil (de Jong,
1980). This could lead to the decrease number of microbial
community that presents in the soil (Sutton et al., 2012).
Petroleum hydrocarbon spills also causes soil pH rise from
acidic to alkaline (Yu et al., 2020). All of these factors
result in the decrease of concentration level of important
nutrients for plants, such as phosphorus and nitrogen, while
there is possibility of concentration level of toxic compound
such as Mn increases de Jong (1980). Eventually, this could
deteriorate soil physical properties and fertility, adversely
harming plants living on the soil. Real example of this case
is when crude oil spilled in Arctic region (Raisbeck and
Mohtadi, 1974). Growing tissue in this area was entirely
dead and various plants and trees, like sedge and mosses,
could not recover as well (Raisbeck and Mohtadi, 1974). De
Jong also finds that cereal yield decreases significantly when
oil contaminated wheat field in Moose Jaw, Saskatchewan,
Canada (de Jong, 1980). For the cereal case, the decrease
of yield specifically happened because other than factors
mentioned previously; oil also prevents water from being
taken up by wheat (de Jong, 1980).

2.1.2 Health effects
Studies over the years have found that petroleum hydrocar-
bon spills indeed cause negative impacts to human health.
For example, spilled petroleum hydrocarbon on land, after
contaminating top soil (Gay et al., 2010), is highly possible
to find its way to enter groundwater which often is source
of drinking water (Duffy et al., 1980). On top of that, the
spills could contaminate air and live stock as well (Gay et al.,
2010). All these possibilities lead to the greater chance for
human’s health to be affected. A number of serious ill-
nesses have been recorded in some areas which are exposed
to spilled petroleum hydrocarbon. Palinkas finds that the

impacts of the spills on the psychosocial environment are
just as bad as the impacts on the environment (Palinkas
et al., 1993). People, who were exposed to the spills, were
found to have higher possibility, up to 3.6 and 2.9 times
to have generalized anxiety disorder and post-traumatic
stress disorder (PTSD) respectively (Palinkas et al., 1993).
Studies by Lyons et al. reports that people live in the area
contaminated by crude oil spills are associated with “higher
depression and anxiety, self reported headache, and worse
mental health” (Lyons et al., 1999). Other studies by Camp-
bell et al., Morita et al., and Janjua et al. also presents
similar findings in which oil spills do worsens psychological
condition of people who are exposed to the spills [Campbell
et al. (1994), Morita et al. (1999), Janjua et al. (2006)].

In addition to psychological condition, physical illnesses
also are a threat in the oil contaminated places. Studies done
by Zock et al. (2007). and Rodriguez-Trigo et al. show that
people exposed to petroleum hydrocarbon may have higher
chance to experience lower respiratory tract symptoms [Zock
et al. (2007), Rodŕıguez-Trigo et al. (2010)]. People aged
between 40 and 60 have higher chance to suffer from stomach
and skin cancer (Gay et al., 2010). Children under 10 years
old are found to have higher chance to suffer hematopoietic
cancers and leukemia as well (Gay et al., 2010). This could
be because petroleum hydrocarbon exposure to human body
could induce the increase of genotoxic effects, a damaging
effect on DNA/RNA (Pérez-Cadah́ıa et al., 2008). Miscar-
riage rates are also found more significant in the area that is
close to the contamination area Gay et al. (2010). Sam and
Zabbey (2018) also notes other numerous health illnesses
human could suffer from oil contamination, such as genetic
mutation and reproductive defects, birth defects, and many
other diseases (Sam and Zabbey, 2018).

2.2 Bioremediation technique
Basically bioremediation is an effort to enhance hydrocarbon-
degrading microorganisms’ activities in soil so the rates of
natural degradation could increase to significant higher rates
(Atlas and Cerniglia, 1995). The method is believed to be
environmentally friendly, for in the right circumtances, even-
tually, majority petroleum hydrocarbon spilled on the soil
will be degraded by the microorganism. The degradation
process provides energy they need to grow and to reproduce
(Xu et al., 2018). Some examples of native microorganism
that have been identified in oil contaminated soil and are po-
tential to be used for degradation process are Acetobacteria,
Plantomycetes, Bacteriodetes, Actinobacteria, Chloroflexi,
Pseudomonas, Collimonas sp, Rhodococcus coprophilus, No-
cardioides albus, and Rhodococcus erythropolis [Peng et al.
(2015), Saadoun et al. (2008), Hamamura et al. (2006)].

However, generally, the number of these indigenous mi-
croorganisms that naturally exist in soil is less than 1% of
total microbial communities (Atlas and Cerniglia, 1995). As
a result the rate of natural degradation process by these
microorganisms is very low, especially when the amount of

© 2020 The Authors. Page 71 of 77



Wahyu Dian Silviani Indonesian Journal of Environmental Management and Sustainability, 4 (2020) 70-77

petroleum that needs to be degraded is high. There is possi-
bility that the number of the indigenous microorganisms to
increase, up to 10%, with the presence of bigger oil amount
(Atlas and Cerniglia, 1995). Nonetheless, the percentage
increase does not always directly translate into higher degra-
dation rate by the microorganism for the ratio of the oil
and the microorganism will be still too low. In addition,
bioremediation process always depends on various factors
supporting microorganism functions, including site charac-
teristics, moisture content, temperature, nutrients, redox
potential, oxygen content, contaminant bioavailability and
contaminant concentrations (Adams et al., 2015). There-
fore, various techniques have been developed to increase
the natural degradation rates of the hydrocarbon-degrading
microorganisms. Below, a more detailed discussion of three
bioremediation methodologies, biostimulation, bioaugmen-
tation, and land farming are provided.

2.2.1 Biostimulation
Biostimulation is one of in situ bioremediation processes.
This method tries to increase the indigenous microorganism
activities by adding nutrient Benyahia and Embaby (2016),
water, acceptors or donors of electron (Megharaj et al., 2011),
and oxygen (Malina and Zawierucha, 2007). Generally,
nutrient is the one that most often added. The addition of
nutrient is important, especially N since it works as limiting
nutrient (Agamuthu et al., 2013) during bioremediation.
Nutrition addition is also needed since with the increase
number of carbon from petroleum contaminant, nutrient
concentration in the soil will also deplete faster (Margesin
and Schinner, 2001). This means less source of food for
the microorganism. Less source of food means less enzyme
production that is needed to degrade the contaminants
(Vidali, 2001). According to Atlas, this method successfully
increases rate of biodegradation up to three to five times
compared to without the addition of nutrients (Atlas and
Cerniglia, 1995). In addition, Tyagi et al. (2010). report a
better result in which degradation rate increases up to 96%
when nutrient, biosolid and commercial fertilizer, are added
Tyagi et al. (2010). Tangahu et al. also report that the use of
another commercial fertilizer, NPK, manged to reduce total
petroleum hydrocarbon value from 8,37% TPH to 4.23%
(Tangahu et al., 2017). However, unwanted side effects, such
as euthropication, could occur. Nonetheless, this method has
been proven successful to enhance microorganism activities
to break down hydrocarbon pollutants faster (Megharaj
et al., 2011), such as for Alaskan Oil Spill in Alaska in 1989
(Atlas and Cerniglia, 1995).

The main advantage of having this method implemented
is because bioremediation process utilizes the indigenous
microorganisms that are already compatible with their en-
vironment and evenly distributed “within the subsurface”
(Adams et al., 2015). Moreover, nutrients added in this
method could be from both organic and inorganic sub-
stances (Tyagi et al., 2010), meaning more options available

to produce the nutrients. On the other hand, the main
challenge when implementing this method is it relies heavily
on geological structure of subsurface where the indigenous
microorganisms live (Jayaprakash et al., 2019). This factor
should not be overlooked as the geology structure will affect
whether the additives could reach the microorganisms or not.
For example, impermeable and tight subsurface, like clays,
will be a constraint to distribute the additives evenly in the
contaminated area (Adams et al., 2015). Another challenge
is the additives might not only promote indigenous microor-
ganisms’ growth that can degrade petroleum hydrocarbon
pollutants, but also other microorganisms which have noth-
ing to do with the biodegradation process (Adams et al.,
2014). As a consequence, a competition between these two
types of microorganisms often could not be avoided.

2.2.2 Bioaugmentation
This is a bioremediation process that utilizes non-indigenous
microorganisms that is known to have the ability to break
down the contaminants (Megharaj et al., 2011). The mi-
croorganisms come from either genetically modified microor-
ganisms or isolated microorganisms from the contaminated
areas (Tyagi et al., 2010). The addition of these microor-
ganisms also aims to increase contaminant biodegradation
rate (Abdulsalam and Omale, 2009). The reason is be-
cause there is possibility that the indigenous microorganism
species that are available in the contaminated area cannot
degrade the complex mixtures of petroleum hydrocarbon
pollutant since metabolic capacities of the microorganisms
is different one from another (Tao et al., 2017). Another
reason is because the indigenous species might not work
optimally due to stress triggered by the petroleum hydrocar-
bon contaminants (Adams et al., 2015). The low number of
the indigenous microorganisms could be the factor as well
(Adams et al., 2015). Therefore, the introductions of the
non-indigenous species could be a support to the indigenous
species which could lead to the increase of biodegradation
rate (Perelo, 2010a). In order for this method to be suc-
cessful, the non-indigenous species must able to degrade the
petroleum hydrocarbon contaminant and make this process
faster than natural decontamination rate (Perelo, 2010b).
The non-indigenous species should also able to survive the
new harsh environment and compete with the indigenous
species, as well as able to find its way to the contaminants
(Adams et al., 2015).

This method works well to degrade petroleum contami-
nant having complex mixtures. With the addition of more
microorganisms groups or consortia, the wider the range of
hydrocarbon substrates that could be degraded. Usually one
group of microorganism can only degrade limited type of
hydrocarbon substrates (Adams et al., 2015). For instance,
Alcanivorax degrade linear alkanes Harayama et al. (2004)
and Mycobacterium degrade alfalfa (Shi et al., 2020). In
addition, it is possible to choose exactly the right microor-
ganisms that can work optimally to break down appropriate

© 2020 The Authors. Page 72 of 77



Wahyu Dian Silviani Indonesian Journal of Environmental Management and Sustainability, 4 (2020) 70-77

petroleum pollutants since nowadays the microorganisms are
studied well first before they are applied (Shi et al., 2020).
Tao et al. (2017). report that a consortium consisting mainly
“Burkholderials order (98.1%) for degrading crude oil” [2017].
Another study cited in Tyagi et al. (2010) give similar result
in which the use of a microbial consortium degrades diesel
oil completely. However, this method also has limitations.
Vidali notes that usually non-indigenous microorganism
fails to compete with the indigenous microorganism, lead-
ing to the failure of developing sufficient populations that
can degrade the contaminant (Vidali, 2001). Vidali also
highlights the fact that soil that has been long exposed to
biodegradable organic waste, including petroleum, usually
has indigenous microorganisms that can effectively degrade
the waste (Vidali, 2001). This means, for such a case, the
addition of non-indigenous microorganisms will be futile.
Another challenge of using non-indigenous and engineered
microorganism is there are many aspects that have yet to
be fully understood when the microorganisms are released
to the environment (Benjamin et al., 2019).

2.2.3 Land farming
This method is a simple bioremediation technique which
requires the excavation of contaminated soil (Vidali, 2001).
After the contaminated soil is excavated the soil is spread on
a thin surface (Dzionek et al., 2016). This soil then tilled or
plowed time to time to prompt the biodegradation process
aerobically (Pavel and Gavrilescu, 2008). By doing this,
it is expected that indigenous microorganism that already
exist in the contaminated soil could work on degrading the
contaminants (Vidali, 2001). To stimulate activities of the
indigenous microorganism, nutrients and minerals are added
as well (Wang et al., 2016). The addition of additives in
this method making this method is not that different from
biostimulation method, except this method is conducted not
in the original contaminated sites.

In practice, this method usually is only to treat super-
ficial soil (Dzionek et al., 2016). Soil must be graded and
cleared first before treatment using this method is run, ac-
cording to The US Environmental Protection Agency (EPA).
This is done by building treatment system, placing leachate
collection and installing vapor treatment facilities (Pavel
and Gavrilescu, 2008). Land farming could be an effective
solution for contaminated land located in the remote areas
which are far away from residential areas, for soil having
“low concentration of volatile compound”, and for area that
can manage all potential emission to water, air, and land
(EPA, 2014). To implement this method properly there are
a lot of factors that must be considered, including concen-
tration, volume and characteristic of the contaminants, area
and duration for treatment, and criteria of remediation to
be achieved (EPA, 2014). As a result, this method would
be more costly when it is done properly relative to other
in situ bioremediation techniques (Vidali, 2001). However,
nowadays, this method is quite popular as it works well for

contaminants with low concentration (Dzionek et al., 2016)
and cost for maintenance, monitoring and clean-up liabilities
is not as expensive as it was in the past (Vidali, 2001).

2.3 Overall evaluation
Generally, in situ bioremediation process is more preferred
than ex situ process. The reason is usually because cost
needed for in situ treatment is lower than that of ex situ
(Vidali, 2001). There will be no excavation fee for in situ
methodologies as the treatment is conducted on site. More-
over, on site treatment could prevent the spread of pollu-
tants to other areas because there is no excavation as well
as transportation process. Considering these factors, among
the three methods discussed, biostimulation and bioaug-
mentation are the more desirable option compared to land
farming. Biostimulation is also well preferred since US EPA
has recognised it as an effective method to be implemented
in the field (Malina and Zawierucha, 2007). Ex situ method
such as land farming is difficult to apply when the area
contaminated by petroleum is wide and deep and located
in non-remote area. Thus, it can be said that in situ treat-
ments are more beneficial in term of practicality and cost
effectiveness.

For biostimulation and bioaugmentation cases, both
methods are effective in their own way. There are many
factors that can affect the final result of these methods.
Numerous studies have been done over the years using these
methods which give various results from time to time. For
example, a study carried out by Bento et al. which aims to
compare bioremediation techniques, biostimulation, bioaug-
mentation, and natural attenuation, to remediate soil con-
taminated by diesel oil, shows that the three treatments give
different result after 12 weeks of incubation (Perelo, 2010b).
Soils used in this study come from California and Hong
Kong. Bioaugmentation works the best for soil from Long
Beach, California, with the degradation rate is up to 72.7%
in the light (C12–C23). Biostimulation, however, does not
give better result or even an equivalent result like bioaug-
mentation according to (Perelo, 2010b). Other studies using
bioaugmentation to degrade petroleum contaminant gives
varying result of total petroleum hydrocarbon (TPH) re-
moval from 32% to 83% (Adams et al., 2015). This indicates
that other factors play a significant role in determining the
final result of TPH removal.

On the other hand, a study by Xu and Lu indicates that
biostimulation is a better choice for bioremediation of soil
contaminated by crude oil (Xu and Lu, 2010). They find that
biostimulation treatment gives up to 61% of TPH removal.
Wu et al. also reports that biostimulation promotes 60%
TPH removal compared to 34% of bioaugmentation (Wu
et al., 2016). Similar findings is also revealed by Haleyur
et al., Wu et al., and Ortega et al. with removal efficiency
of 99%, 28%, and 49-62% respectively using biostimulation
technique [Haleyur et al. (2019), Wu et al. (2019), Ortega
et al. (2018)]. According to Adams et al., other biostimu-

© 2020 The Authors. Page 73 of 77



Wahyu Dian Silviani Indonesian Journal of Environmental Management and Sustainability, 4 (2020) 70-77

lation studies that use TPH removal rate to measure the
success of bioremediation process also show a promising re-
moval rate with TPH removal from 25% up to 100% (Adams
et al., 2015).

Because biostimulation and bioaugmentation techniques
give varying result, an approach to combine biostimulation
and bioaugmentation to achieve better result is proposed
by (Sun et al., 2012). Sun et al. (2012). finds that dry soil
containing 375 mg of total PAH in each kg could be cleaned
more effectively using combination of these two techniques
(Sun et al., 2012). It was found that 43.9% of total PAH and
55% of 4-6 ring-PAH can be degraded using the combination
techniques. This is far higher than degradation rate when
using biostimulation and bioaugmentation separately (Sun
et al., 2012). Safdari et al. (2018). also report combina-
tion of biostimulation and bioaugmentation gives highest
TPH degradation rate (89,7±0.3%) compared to individ-
ual treatment (Safdari et al., 2018). However, other study
carried out by Abdulsalam and Omale give opposite result.
In their study, they measure TPH removal in soil which is
contaminated by motor oil (Abdulsalam and Omale, 2009).
Concentration of the oil is 40.000 ppm. They found that
combination of biostimulation and bioaugmentation gives a
little bit lower TPH removal rate (65.2±0.25%) compared
with biostimulation TPH removal rate (69.2±0.05%).

Based on the various result given by bioaugmentation
and biostimulation above, it is clear that there are various
factors that affect the final result of these two techniques.
Concentration of contaminants is one of them. Contami-
nants concentration in each study is different. Adams et al.
(2015). points out that when contaminant concentration still
can be tolerated by microorganisms, biodegradation process
will be more optimum and faster (Adams et al., 2015). But
when the concentration of contaminants is beyond “micro-
bial tolerable limit” the rates of biodegradation will be slower
and will take longer times to finish (Adams et al., 2015).
Other factors, such as soil characteristic, scale of studies,
length of studies as well as various different controls applied
during studies will definitely affect how well biodegradation
process proceed (Perelo, 2010b). Thus, comparing result
of bioaugmentation and biostimulation directly cannot be
done without the same condition of study. Comparing one
study result with others also should be done carefully by
observing factors and parameters affecting the studies.

2.4 Limitations
Due to many benefits bioremediation offers, this methodol-
ogy seems like a promising way to resolve land contamination
because of petroleum hydrocarbon. However, this method
still has its own limitations. One of them is there is no
clear bench-marking value that can be used as a standard to
determine whether a bioremediation process is a success or
not (Megharaj et al., 2011). Different studies gives different
TPH removal rate. Some gives impressive number, up to
90% but there are other studies that give less than 50% of

TPH removal rate. Furthermore, every study uses different
contaminant concentration and length of study. Therefore,
it is hard to compare the success of one study to others. If
there was a definite number to measure the efficacy of biore-
mediation technique, for example a success is when TPH
removal rate is X% for every Y ppm of contaminants in Z
days, it would be easier to determine goals and process that
need to be done to achieve such results. Another limitation
is lack of understanding regarding contaminants bioavail-
ability (Megharaj et al., 2011). This is an important factor
that still needs better understanding. Once pollutants enter
soil, there will be sorption process, precipitation and com-
plexation processes that determine how the pollutants will
interact with soil. Sorption process by soil will determine
pollutants’s “susceptibility to microbial degradation”, there-
fore affecting how effective the process of bioremediation
will run (Megharaj et al., 2011). The next limitation is lack
of knowledge of whether there will be impacts in the future
from the addition of nutrients and genetically-engineered
microorganisms to the soil (Benjamin et al., 2019). The
knowledge of how the addition of nutrients and genetically-
engineered microorganisms will affect ecology in the future
is yet fully understood. Having this kind of knowledge ful-
filled will be a great advantage in improving bioremediation
techniques in the future.

3. CONCLUSIONS

In conclusion, bioremediation technique is one of promising
the solutions that can be applied to remedy land contami-
nated by petroleum hydrocarbon. There are two types of
bioremediation, in situ and ex situ. Both of these methods
have been proven to be more environmentally friendly and
more cost effective to solve the problem compared to techni-
cal and chemical methods. However, when in situ and ex
situ methods are compared, currently in situ methods are
thought as the better methodology. That is why methodol-
ogy such as biostimulation and bioaugmentation are widely
used in the studies that aim to degrade petroleum hydro-
carbon pollutants. Using these two methodologies will save
more money for operational cost as well as will prevent pos-
sibilities of pollutants to spread. However, there are many
factors that need to be considered in order to achieve best
result of TPH removal when applying biostimulation and
bioaugmentation techniques. These factors include contami-
nant concentration and characteristics, length of study, soil
condition, and many other factors. These factors also make
contribution to the fact that result achieved using biostimu-
lation should not be compared directly to result achieved
using bioaugmentation. In addition taking into account
these factors, to get the best rates of TPH removal, limita-
tions of bioremediation methodologies, such as the absence
of bench-mark value to measure the success of TPH removal,
the lack of understanding of contaminant bioavailability and
fate of additives and genetically-engineered microorganisms
added to the soil should be recognized as well.

© 2020 The Authors. Page 74 of 77



Wahyu Dian Silviani Indonesian Journal of Environmental Management and Sustainability, 4 (2020) 70-77

REFERENCES

Abdulsalam, S. and A. B. Omale (2009). Comparison of
biostimulation and bioaugmentation techniques for the
remediation of used motor oil contaminated soil. Brazilian
Archives of Biology and Technology, 52(3); 747–754

Adams, G., P. Tawari-Fufeyin, and E. Igelenyah (2014).
Bioremediation of spent oil contaminated soils using poul-
try litter. Research Journal in Engineering and Applied
Sciences, 3(2); 124–130

Adams, G. O., P. T. Fufeyin, S. E. Okoro, I. Ehinomen, et al.
(2015). Bioremediation, biostimulation and bioaugmen-
tion: a review. International Journal of Environmental
Bioremediation & Biodegradation, 3(1); 28–39

Agamuthu, P., Y. Tan, and S. Fauziah (2013). Bioremedia-
tion of Hydrocarbon Contaminated Soil Using Selected
Organic Wastes. Procedia Environmental Sciences, 18;
694–702

Alzien, S. A., R. Azzam, and H. Weiß (2019). Rehabilita-
tion of sites contaminated with petroleum hydrocarbon
by using sustainable remediation approach in lower and
middle-income countries: Libya as a case study. Technical
report, Lehrstuhl für Ingenieurgeologie und Hydrogeologie

Arbili, M. M. and M. Karpuzcu (2018). Effect of Crude Oil
Contamination on physical and Chemical Properties of
Soil of Tarjan Refineries Erbil Province - North of Iraq.
Polytechnic Journal, 8(2)

Atlas, R. M. and C. E. Cerniglia (1995). Bioremediation of
Petroleum Pollutants. BioScience, 45(5); 332–338

Baker, J. M. (1970). The effects of oils on plants. Environ-
mental Pollution (1970), 1(1); 27–44

Benjamin, S. R., F. de Lima, and A. K. Rathoure (2019). Ge-
netically Engineered Microorganisms for Bioremediation
Processes. In Biotechnology. IGI Global, pages 1607–1634

Benyahia, F. and A. Embaby (2016). Bioremediation of
Crude Oil Contaminated Desert Soil: Effect of Biostim-
ulation, Bioaugmentation and Bioavailability in Biopile
Treatment Systems. International Journal of Environ-
mental Research and Public Health, 13(2); 219

Campbell, D., D. Cox, J. Crum, K. Foster, and A. Riley
(1994). Later effects of grounding of tanker Braer on
health in Shetland. BMJ, 309(6957); 773–774

de Jong, E. (1980). The effect of a crude oil spill on ce-
reals. Environmental Pollution Series A, Ecological and
Biological, 22(3); 187–196

Duffy, J., E. Peake, and M. Mohtadi (1980). Oil spills on
land as potential sources of groundwater contamination.
Environment International, 3(2); 107–120

Dzionek, A., D. Wojcieszyńska, and U. Guzik (2016). Nat-
ural carriers in bioremediation: A review. Electronic
Journal of Biotechnology, 23; 28–36

EPA, N. (2014). Best Practice Note: Landfarming. New
South Wales Environment Protection Authority, Sydney,
Australia

Gay, J. C., M. A. Whitman, M. J. Thyden, and O. C.

Shepherd (2010). The health effects of oil contamination:
a compilation of research

Gordon, G., I. Stavi, U. Shavit, and R. Rosenzweig (2018).
Oil spill effects on soil hydrophobicity and related proper-
ties in a hyper-arid region. Geoderma, 312; 114–120

Haleyur, N., E. Shahsavari, S. S. Jain, E. Koshlaf, V. B.
Ravindran, P. D. Morrison, A. M. Osborn, and A. S. Ball
(2019). Influence of bioaugmentation and biostimulation
on PAH degradation in aged contaminated soils: Response
and dynamics of the bacterial community. Journal of
Environmental Management, 238; 49–58

Hamamura, N., S. H. Olson, D. M. Ward, and W. P. Inskeep
(2006). Microbial Population Dynamics Associated with
Crude-Oil Biodegradation in Diverse Soils. Applied and
Environmental Microbiology, 72(9); 6316–6324

Harayama, S., Y. Kasai, and A. Hara (2004). Microbial com-
munities in oil-contaminated seawater. Current Opinion
in Biotechnology, 15(3); 205–214

Janjua, N. Z., P. M. Kasi, H. Nawaz, S. Z. Farooqui, U. B.
Khuwaja, N. ul Hassan, S. N. Jafri, S. A. Lutfi, M. M.
Kadir, and N. Sathiakumar (2006). Acute health effects
of the Tasman Spirit oil spill on residents of Karachi,
Pakistan. BMC Public Health, 6(1)

Jayaprakash, K., M. Govarthanan, R. Mythili, T. Selvanku-
mar, and Y.-C. Chang (2019). Bioaugmentation and Bios-
timulation Remediation Technologies for Heavy Metal
Lead Contaminant. Microbial Biodegradation of Xenobi-
otic Compounds; 24

Lyons, R. A., J. M. Temple, D. Evans, D. L. Fone, and S. R.
Palmer (1999). Acute health effects of the Sea Empress
oil spill. Journal of Epidemiology & Community Health,
53(5); 306–310

Malina, G. and I. Zawierucha (2007). Potential of Bioaug-
mentation and Biostimulation for Enhancing Intrinsic
Biodegradation in Oil Hydrocarbon-Contaminated Soil.
Bioremediation Journal, 11(3); 141–147

Margesin, R. and F. Schinner (2001). Bioremediation
(Natural Attenuation and Biostimulation) of Diesel-Oil-
Contaminated Soil in an Alpine Glacier Skiing Area. Ap-
plied and Environmental Microbiology, 67(7); 3127–3133

Megharaj, M., B. Ramakrishnan, K. Venkateswarlu,
N. Sethunathan, and R. Naidu (2011). Bioremediation
approaches for organic pollutants: A critical perspective.
Environment International, 37(8); 1362–1375

Morita, A., Y. Kusaka, Y. Deguchi, A. Moriuchi,
Y. Nakanaga, M. Iki, S. Miyazaki, and K. Kawahara
(1999). Acute Health Problems among the People Engaged
in the Cleanup of the Nakhodka Oil Spill. Environmental
Research, 81(3); 185–194

Mostagab, H. D., M. Senosy, A. A. Rashed, and M. E.
Salem (2018). The Impact of Hydrocarbon Pollution on
Soil Degradation Using GIS Techniques and Soil Charac-
terization in Burgan Oil field, South Kuwait. Journal of
Environmental Protection, 09(06); 699–719

Okoh, E., Z. R. Yelebe, B. Oruabena, E. S. Nelson, and O. P.

© 2020 The Authors. Page 75 of 77



Wahyu Dian Silviani Indonesian Journal of Environmental Management and Sustainability, 4 (2020) 70-77

Indiamaowei (2019). Clean-up of crude oil-contaminated
soils: bioremediation option. International Journal of
Environmental Science and Technology, 17(2); 1185–1198

Ortega, M. F., D. E. Guerrero, M. J. Garćıa-Mart́ınez,
D. Bolonio, J. F. Llamas, L. Canoira, and J. L. R. Gallego
(2018). Optimization of Landfarming Amendments Based
on Soil Texture and Crude Oil Concentration. Water, Air,
& Soil Pollution, 229(7)

Palinkas, L. A., J. S. Petterson, J. Russel, and M. A. Downs
(1993). Community patterns of psychiatric disorders after
the Exxon Valdez oil spill. American Journal of Psychia-
try, 150(10); 1517–1523

Pavel, L. V. and M. Gavrilescu (2008). OVERVIEW OF EX
SITU DECONTAMINATION TECHNIQUES FOR SOIL
CLEANUP. Environmental Engineering and Management
Journal, 7(6); 815–834

Peng, M., X. Zi, and Q. Wang (2015). Bacterial Community
Diversity of Oil-Contaminated Soils Assessed by High
Throughput Sequencing of 16S rRNA Genes. International
Journal of Environmental Research and Public Health,
12(10); 12002–12015

Perelo, L. W. (2010a). In situ and bioremediation of organic
pollutants in aquatic sediments. Journal of hazardous
materials, 177(1-3); 81–89

Perelo, L. W. (2010b). Review: In situ and bioremediation
of organic pollutants in aquatic sediments. Journal of
Hazardous Materials, 177(1-3); 81–89

Pérez-Cadah́ıa, B., B. Laffon, V. Valdiglesias, E. Pásaro, and
J. Méndez (2008). Cytogenetic effects induced by Prestige
oil on human populations: The role of polymorphisms
in genes involved in metabolism and DNA repair. Mu-
tation Research/Genetic Toxicology and Environmental
Mutagenesis, 653(1-2); 117–123

Raisbeck, J. and M. Mohtadi (1974). The environmental
impacts of oil spills on land in the arctic regions. Water,
Air, and Soil Pollution, 3(2); 195–208

Rodŕıguez-Trigo, G., J.-P. Zock, F. Pozo-Rodŕıguez, F. P.
Gómez, G. Monyarch, L. Bouso, M. D. Coll, H. Verea,
J. M. Antó, C. Fuster, et al. (2010). Health changes in
fishermen 2 years after clean-up of the Prestige oil spill.
Annals of internal medicine, 153(8); 489–498

Saadoun, I., M. J. Mohammad, K. M. Hameed, and
M. Shawaqfah (2008). Microbial populations of crude
oil spill polluted soils at the Jordan-Iraq desert (the Badia
region). Brazilian Journal of Microbiology, 39(3); 453–456

Safdari, M.-S., H.-R. Kariminia, M. Rahmati, F. Fazlol-
lahi, A. Polasko, S. Mahendra, W. V. Wilding, and T. H.
Fletcher (2018). Development of bioreactors for compar-
ative study of natural attenuation, biostimulation, and
bioaugmentation of petroleum-hydrocarbon contaminated
soil. Journal of Hazardous Materials, 342; 270–278

Sam, K. and N. Zabbey (2018). Contaminated land and wet-
land remediation in Nigeria: Opportunities for sustainable
livelihood creation. Science of The Total Environment,
639; 1560–1573

Shi, K., Q. Zhang, J. Xue, X. Chen, Y. Chen, Y. Qiao,
Y. Yang, and J. Sun (2020). Study on the degradation
performance and bacterial community of bioaugmentation
in petroleum-pollution seawater. Journal of Environmen-
tal Chemical Engineering, 8(4); 103900

Sinha, R. K., D. Valani, S. Sinha, S. Singh, and S. Herat
(2009). Bioremediation of contaminated sites: a low-
cost nature’s biotechnology for environmental clean up
by versatile microbes, plants & earthworms. Solid waste
management and environmental remediation; 978–1

Sun, G.-D., Y. Xu, J.-H. Jin, Z.-P. Zhong, Y. Liu, M. Luo,
and Z.-P. Liu (2012). Pilot scale ex-situ bioremediation
of heavily PAHs-contaminated soil by indigenous microor-
ganisms and bioaugmentation by a PAHs-degrading and
bioemulsifier-producing strain. Journal of Hazardous Ma-
terials, 233-234; 72–78

Sutton, N. B., F. Maphosa, J. A. Morillo, W. A. Al-Soud,
A. A. M. Langenhoff, T. Grotenhuis, H. H. M. Rijnaarts,
and H. Smidt (2012). Impact of Long-Term Diesel Contam-
ination on Soil Microbial Community Structure. Applied
and Environmental Microbiology, 79(2); 619–630

Tangahu, B. V., L. Vyatrawan, R. Nurmalasari, and F. Pi-
rade (2017). Bioremediation of Oil Contaminated Soil
by Biostimulation Method Using NPK Fertilizer. OALib,
04(11); 1–8

Tao, K., X. Liu, X. Chen, X. Hu, L. Cao, and X. Yuan
(2017). Biodegradation of crude oil by a defined co-culture
of indigenous bacterial consortium and exogenous Bacillus
subtilis. Bioresource Technology, 224; 327–332

Tyagi, M., M. M. R. da Fonseca, and C. C. C. R. de Carvalho
(2010). Bioaugmentation and biostimulation strategies
to improve the effectiveness of bioremediation processes.
Biodegradation, 22(2); 231–241

Vidali, M. (2001). Bioremediation. An overview. Pure and
Applied Chemistry, 73(7); 1163–1172

Wang, S.-Y., Y.-C. Kuo, A. Hong, Y.-M. Chang, and C.-M.
Kao (2016). Bioremediation of diesel and lubricant oil-
contaminated soils using enhanced landfarming system.
Chemosphere, 164; 558–567

Wang, Y., J. Feng, Q. Lin, X. Lyu, X. Wang, and G. Wang
(2013). Effects of crude oil contamination on soil physical
and chemical properties in Momoge wetland of China.
Chinese Geographical Science, 23(6); 708–715

Wu, M., W. A. Dick, W. Li, X. Wang, Q. Yang, T. Wang,
L. Xu, M. Zhang, and L. Chen (2016). Bioaugmenta-
tion and biostimulation of hydrocarbon degradation and
the microbial community in a petroleum-contaminated
soil. International Biodeterioration & Biodegradation,
107; 158–164

Wu, M., J. Wu, X. Zhang, and X. Ye (2019). Effect of bioaug-
mentation and biostimulation on hydrocarbon degrada-
tion and microbial community composition in petroleum-
contaminated loessal soil. Chemosphere, 237; 124456

Xu, X., W. Liu, S. Tian, W. Wang, Q. Qi, P. Jiang, X. Gao,
F. Li, H. Li, and H. Yu (2018). Petroleum Hydrocarbon-

© 2020 The Authors. Page 76 of 77



Wahyu Dian Silviani Indonesian Journal of Environmental Management and Sustainability, 4 (2020) 70-77

Degrading Bacteria for the Remediation of Oil Pollution
Under Aerobic Conditions: A Perspective Analysis. Fron-
tiers in Microbiology, 9

Xu, Y. and M. Lu (2010). Bioremediation of crude oil-
contaminated soil: Comparison of different biostimulation
and bioaugmentation treatments. Journal of Hazardous
Materials, 183(1-3); 395–401

Yu, Y., Y. Zhang, N. Zhao, J. Guo, W. Xu, M. Ma, and
X. Li (2020). Remediation of Crude Oil-Polluted Soil by

the Bacterial Rhizosphere Community of Suaeda Salsa
Revealed by 16S rRNA Genes. International Journal of
Environmental Research and Public Health, 17(5); 1471

Zock, J.-P., G. Rodŕıguez-Trigo, F. Pozo-Rodŕıguez, J. A.
Barberà, L. Bouso, Y. Torralba, J. M. Antó, F. P. Gómez,
C. Fuster, and H. V. and (2007). Prolonged Respira-
tory Symptoms in Clean-up Workers of thePrestigeOil
Spill. American Journal of Respiratory and Critical Care
Medicine, 176(6); 610–616

© 2020 The Authors. Page 77 of 77


	INTRODUCTION
	RESULTS AND DISCUSSION
	Environmental and health effects of petroleum hydrocarbon pollutants
	Environmental effects
	Health effects

	Bioremediation technique
	Biostimulation
	Bioaugmentation
	Land farming

	Overall evaluation 
	Limitations

	CONCLUSIONS