Journal of Environmental Management 222 (2018) 409–419

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Journal of Environmental Management

journal homepage: www.elsevier.com/locate/jenvman

Review

Recent progress and perspectives in biotrickling filters for VOCs and odorous T
gases treatment
Hao Wua, Huayu Yana, Yue Quana, Huazhang Zhaob, Nanzhe Jianga, Chengri Yina,∗
a
Key Laboratory of Natural Resources of Changbai Mountain and Functional Molecules, Ministry of Education, Department of Chemistry, Yanbian University, Yanji
133002, China
b
Department of Environmental Engineering, Peking University, The Key Laboratory of Water and Sediment Sciences, Ministry of Education, Beijing 100871, China

A R T I C LE I N FO A B S T R A C T

Keywords: Pollution caused by volatile organic compounds (VOCs) and odorous pollutants in the air can produce severe
Air pollution control environmental problems. In recent years, the emission control of VOCs and odorous pollutants has become a
Biofilm crucial issue owing to the adverse effect on humans and the environment. For treating these compounds, bio-
Biotrickling filter trickling filter (BTF) technology acts as an environment friendly and cost-effective alternative to conventional air
Deodorization
pollution control technologies. Besides, low concentration of VOCs and odorous pollutants can also be effectively
Microbial analysis
removed using BTF systems. However, the VOCs and odorants removal performance by BTF may be limited by
VOCs
the hydrophobicity, toxicity, and low bioavailability of these pollutants. To solve these problems, this review
summarizes the design, mechanism, and common analytical methods of recent BTF advances. In addition, the
operating conditions, mass transfer, packing materials and microorganisms (which are the critical parameters in
a BTF system) were evaluated and discussed in view of improving the removal performance of BTFs. Further
research on these specific topics, together with the combination of BTF technology with other technologies,
should improve the removal performance of BTFs.

1. Introduction
Air pollution and health are closely related and a series of adverse
health effects especially mortality and morbidity owing to cardiovas-
cular and respiratory diseases are closely associated with the current-
day concentrations of ambient air pollutants (Hoek et al., 2013). It has
been reported that outdoor air pollution leads to 3.3 million (95%
confidence interval [1.61, 4.81]) premature deaths per year worldwide,
predominantly in Asia (Jerrett, 2015). Odorous pollutants and volatile
organic compounds (VOCs) are common and typical outdoor air pol-
lutants. They have adverse effects on the social and physical environ-
ment, and create disproportionate disease burdens in less affluent seg-
ments of the society (Garcia et al., 2015). Thus, air pollution problems
caused by the emission of odorous pollutants and VOCs not only
threaten public health, but also deteriorate personal welfare
(Balasubramanian et al., 2012). VOCs can adversely affect both short-
and long-term health of humans and animals. They are involved in the
formation of photochemical smog, ozone and respirable suspended
particulates in the atmosphere, and contribute to sharp declines in crop
yields and destruction of forests and ecosystems (Yang et al., 2010b).
VOCs are organic compounds, including alkanes, aromatics, olefins,
halocarbons, esters, aldehydes, ketones, etc., with a boiling point ran-
ging from 50 °C to 260 °C (Kim, 2011; Zhang et al., 2018). Furthermore,
as a common environmental problem, emission of odorous pollutants is
not only a public health concern, but also a threat to personal comfort
(Leuch et al., 2008). The main components of odorous pollutants are (1)
nitrogen-containing compounds (including inorganic compounds such
as NH3 and NOX, and amines such as methylamine, dimethylamine, and
trimethylamine) (Han et al., 2016; Wan et al., 2011b); (2) sulfur-con-
taining compounds (including inorganic compounds such as H2S and
SO2, and organosulfur compounds such as methyl mercaptan, ethyl
mercaptan, dimethyl sulfide, and dimethyl disulfide) (Chung et al.,
2010; Lebrero et al., 2012b; Montebello et al., 2013; Shammay et al.,
2016); and (3)VOCs (including aromatic, aliphatic and chlorinated
hydrocarbons, fatty acids, aldehydes, terpenes and ketones) (Munoz
et al., 2010; Xue et al., 2013). In addition to their potent offensive
smell, VOCs and odorous gases also result in acute toxic and chronic
long-term health effects (Kim, 2011; Zhang and Tay, 2015). Therefore,
air pollution caused by VOCs and odorous gas need to be immediately
solved.
In recent years, to improve air quality and reduce or eliminate air
pollution caused by VOCs and odorous gases, various technologies have

∗
Corresponding author.
E-mail address: cryin@ybu.edu.cn (C. Yin).

https://doi.org/10.1016/j.jenvman.2018.06.001
Received 21 November 2017; Received in revised form 19 May 2018; Accepted 1 June 2018
0301-4797/ © 2018 Elsevier Ltd. All rights reserved.
H. Wu et al.
been developed. Among them, the common methods used can be
grouped into three categories: physical technologies, which usually
include condensation, adsorption, water scrubbers; chemical technolo-
gies, which mainly include chemical scrubbers, thermal oxidation,
catalytic oxidation, and ozonation; and biological technologies such as
biofilters (BF), bioscrubbers, and biotrickling filters (BTFs) (Wan et al.,
2011a). Despite the effectiveness of physical–chemical methods in de-
stroying VOCs and odorous gases, the disadvantages of high cost and
secondary pollution are characteristic of these techniques. For some
applications of physical–chemical methods, the concentration of waste
gas should be relatively high, otherwise economic benefits are un-
achievable (Khan and Kr. Ghoshal, 2000). However, the concentration
of waste air contaminated by VOCs and odorous gases is usually from
low to moderate, but the volumes are high. Furthermore, owing to the
limitation of technology and production process, the use of VOCs and
other odorous volatile compounds cannot be completely prohibited.
Thus, VOCs and odorous gas pollution cannot be eliminated soon, and
the use of conventional methods such as adsorption, condensation, and
incineration for the treatment of low concentrations of VOCs and
odorous gases may not be economical (Singh et al., 2010b).
Biotechnologies are currently recognized as the best available
methods for the treatment of low and moderate concentrations of waste
gases containing odorous pollutants and VOCs because they are cost-
effective and environment-friendly, when compared with other phy-
sical and chemical technologies (Ryu et al., 2011). These processes
usually use bioreactors that play a very important role in the control of
VOCs and odorous gases. Bioreactors have been found to be cost-ef-
fective for treating off-gases with low concentrations of VOCs
(usually < 3 g/m3) and can achieve 99% odor reduction for some
pollutants (Groenestijn and Kraakman, 2005).
Though a number of different configurations exist, the main types of
conventional air-phase bioreactors include BF, BTF, and bioscrubber.
The characteristics of these bioreactors are shown in Table 1 and Fig. 1.
The basic differences among the reactors exist in the environment of the
microorganisms (suspended or fixed), and the state of the liquid (flow
or stationary). As indicated in Fig. 1A, in the BF system, the filter bed is
usually made of organic material such as soil, peat, straw, compost, or
other suitable substrate. The amount of nutrient supply is strongly
correlated with the characteristics of the waste air. As the packing
material used in BF systems usually contains microorganisms as well as
lots of nutrients for the growth of microorganisms, additional supply of
microorganisms and nutrients are not necessary for the treatment of
odor problems. However, supply of some extra nutrients may enhance
the biodegradation of VOCs (Wahman et al., 2007). Occasionally, water
must be sprayed onto the packing bed to maintain high moisture con-
tent, and leachate can be recirculated to the BFs to avoid wastewater
generation. Generally, the pollutant gases flow through the porous
packing media, and are degraded by microorganisms. The BF systems
have the advantages of cost effectiveness, and almost no secondary
pollution. However, some disadvantages include difficulty in moisture
and pH control, clogging of the medium due to particulate matter and
abundant biomass, and medium deterioration.
As shown in Fig. 1B, bioscrubber systems consist of two subunits,
one is an absorption unit and the other is a bioreactor unit. Gaseous and
liquid phases flow counter-currently within the bioscrubber column.
The waste gases are first cleaned by absorption and the clean gases are
released at the top of the column. Pollutants in the aqueous solution are
Table 1
Characteristics of three types of bioreactors.
Bioreactor type Microorganisms Water phase
Biofilter Fixed Stationary
Biotrickling filter Fixed Dis- or continuously flowing
Bioscrubber Suspended Flowing
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Journal of Environmental Management 222 (2018) 409–419
Fig. 1. Schematic view of conventional bioreactors. A: biofilter (BF); B: bio-
scrubber; C: biotrickling filter (BTF).
degraded by appropriate microbial strains suspended in the aqueous
solution. The bioscrubber systems have the advantages of operational
stability, adequate control of operation parameters (pH, nutrients), low
pressure drop, and minimum space requirement. The disadvantages of
bioscrubbers include the ability to treat only readily soluble VOCs and
odorous pollutants having low Henry coefficient. Furthermore, bio-
scrubbers generate excess sludge and liquid waste that have to be
treated.
In BTF systems (Fig. 1C), waste gas being treated is carried through
a packed bed, which is continuously or intermittently irrigated with an
aqueous solution containing essential nutrients required by the biolo-
gical system. Microorganisms from an external source are inoculated on
the surface of the packing material and form a biofilm. Pollutants are
initially absorbed by an aqueous film that surrounds the biofilm and are
then degraded by the biofilm. The BTF system has the advantages of
low operating and capital costs, lower pressure drop during long-term
operation, and capability to intensively treat acidic degradation pro-
ducts of VOCs and acidic odorous gases (Lebrero et al., 2012a). How-
ever, BTFs are relatively complex in construction and operation and
accumulate excess biomass (Mudliar et al., 2010).
Comparison of BFs, BTFs, and bioscrubbers revealed that BTFs have
better capacity in treating recalcitrant VOCs and acidic or alkaline
compounds. Moreover, water management is the major advantage of
BTFs, when compared with the BF systems, allowing defined control of
pH, nutrient supply, and removal of toxic metabolites, thus achieving
higher pollutants elimination rates (Seignez et al., 2004). Besides, when
compared with bioscrubbers, BTFs exhibit rapid biodegradation of
pollutants owing to enrichment of pollutants with extracellular poly-
meric substances acting as surfactants, resulting in large numbers of
immobilized microorganisms coming into contact with the pollutants.
Although the construction and operation of a BTF may be complex, as a
typical form of biological treatment technology these systems have
succeeded in treating many kinds of pollutants (Balasubramanian et al.,
2012). Thus, when combining this benefit with its cost effectiveness,
BTF technology is an attractive option for controlling VOCs and odor
emissions from various industrial processes (Zehraoui et al., 2012).
However, some limitations in BTF processes (such as excess biomass
accumulation, low mass transfer rate, etc.) may affect the pollutant
removal performance of BTFs. In a BTF system, the design, operating
condition, mass transfer, packing materials and microorganisms are
critical influences during BTF processes (Fig. 2) and can significantly
affect the removal of gaseous pollutants.
Many methods have been investigated for enhancing the removal
performance of BTFs, such as pollutant pretreatment, fungal BTF, sur-
factant addition, and other techniques. Essentially, these methods are
designed to optimize the critical parameters of BTFs. Thus, examination
of these critical parameters is necessary, because they are the founda-
tion for utilizing BTFs and improving the pollutant removal perfor-
mance.
H. Wu et al.
Fig. 2. Critical parameters of biotrickling filter (BTF) systems for the removal of
volatile organic compounds (VOCs) and odorous pollutants.
To optimize and solve the problems that still exist in the BTF sys-
tems, this review attempts to provide an overview of concepts and
perspectives related to BTFs, along with details on their configuration
and design, mechanism of operation, mass transfer, packing materials
and analysis of microbial communities, and future needs to improve
their performance in treating VOCs and odors. The review will provide
researchers a better understanding about the BTF technology and help
to improve the design and process parameters of BTF systems to achieve
high VOCs and odorous pollutants removal.
2. BTF mechanisms and limitations
A BTF system for VOCs and odorous gas removal is usually a com-
plex combination of different physicochemical and biological phe-
nomena. As the vapor passes through the BTF bed, contaminants and
nutrients are transferred to the microorganisms, where cellular meta-
bolism breaks down the chemicals into simpler components. As shown
in Fig. 3, microorganisms are immobilized on the surface of the packing
material and the surface of biofilms is covered by a water phase. The
VOCs and odorous pollutants in the contaminated air first need to be
transferred to the water phase layer, and then moved to microbial cells
in the biofilm where they are ultimately degraded by the microorgan-
isms.
Initially, the vapor-phase contaminants and any nutrients needed
for microbial growth (oxygen, nitrogen, and phosphorus, etc.) must be
dissolved in the water phase surrounding the biofilm. The pollutant
vapors and oxygen are transported in humid air or directly into the
water phase by concentration gradient differences, and this process is
indicated as mass transfer (Kraakman et al., 2011; Lebrero et al.,
Fig. 3. Diffusion, reaction limitations, and processes of biodegradation within a
biotrickling filter (BTF) system.
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Journal of Environmental Management 222 (2018) 409–419
2012a). Subsequently, biodegradation reactions occur, during which
the dissolved contaminants are assimilated and degraded by the biofilm
through conversion to CO2 or other poorly volatile intermediates with
simple chemical structures. In the presence of nutrients, the energy
released by the oxidation of these contaminants is utilized by the mi-
croorganisms to form a biofilm. In a BTF, the biodegradation effect is
controlled both by mass transfer of gaseous pollutants from air to bio-
film (diffusion limitation) and by the biodegradation reactions (reaction
limitation) (Li et al., 2012). In a previous study (Wu et al., 2016b), the
relationship between elimination capacities (EC) and inlet load (IL) was
discussed at three empty bed retention times (EBRT). When IL was
fixed, longer EBRT meant the gaseous pollutant characteristics were a
high inlet concentration and low total flow rate. In this case, the water
phase surrounding the biofilm was saturated by gaseous pollutants;
thus, the degradation reaction was controlled by the reaction limita-
tion. At shorter EBRT, the gaseous pollutant characteristics were a high
total flow rate and low inlet concentration. Under these conditions, the
gaseous pollutant exited the BTF without adequate contact with the
water phase; thus, the degradation was controlled by diffusion limita-
tion (Wu et al., 2016b).
The actual biodegradation of target contaminants occurs within the
biofilm, and the formation of secondary metabolites is possible. If
formed, secondary metabolites will undergo the same simultaneous
diffusion, biodegradation, and sorption processes as the primary pol-
lutants. Finally, the end products (such as CO2) after microbial de-
gradation are transferred to gas phase or forms carbonate in aqueous
phase by VOC oxidation (Cheng et al., 2016a). However, if the sec-
ondary metabolites show higher toxicity than the original pollutants,
their formation will stop the biodegradation processes, for example,
production of p-benzoquinone during the biodegradation of chlor-
ophenol or 4-chloronitrobenzene, and accumulation of tert-butyl al-
cohol during the transformation of methyl tert-butyl ether (MTBE)
(Purswani et al., 2011; Skiba et al., 2002).
For effective BTF treatment, the contaminants must be biodegrad-
able and non-toxic or have low toxicity to BTF. The most successful
pollutant removal using BTFs has been achieved for low molecular
weight and highly soluble organic compounds with simple bond
structures. Compounds with complex bond structures usually require
more energy, which, sometimes, is not always available to the micro-
organisms, and as a result, little or no biodegradation of these com-
pounds occurs. It must be noted that organic compounds such as al-
cohols, aldehydes, ketones, and some simple aromatics have excellent
biodegradability; phenols, chlorinated hydrocarbons, PAHs, and highly
halogenated hydrocarbons show moderate to slow degradation; and
certain anthropogenic compounds may not biodegrade at all unless
some additional factors, such as necessary enzymes, are added. Table S1
lists some contaminants and their biodegradability in the BTF systems
(Devinny et al., 1999b).
3. Operation of BTFs
3.1. Design of BTFs
The design and operating conditions, along with packing materials
and mass transfer can significantly affect the removal performance of a
BTF. A common BTF design consists of a column and packing beds. The
column of a laboratory- or pilot-scale BTF is usually made of glass or
plastics (Hernandez et al., 2013; Singh et al., 2010a). Due to the
transparency of plastics such as Plexiglas®, these materials make it easy
to observe the changes in the BTF. However, industrial-scale BTFs are
commonly made of steel, fiberglass reinforced plastics or polymer
(Chen et al., 2014b).
The filter bed in a BTF system consists of packing material and
microorganisms. The packing material provides support for the growth
of microorganisms and contributes to pollutant sorption to ensure
adequate residence time for the degradation of gaseous pollutants.
H. Wu et al.
Thus, packing materials are considered as one of the core factors of the
BTF systems. The main function of packing material is to promote
contact between the contaminants and microorganisms, thereby al-
lowing the generation of a stable aggregate (Gutierrez-Acosta et al.,
2012). The packing beds in a BTF can be arranged in a single layer or
multiple layers (Kennes and Thalasso, 1998). Single-layer packing bed
BTF can save more space, whereas multiple-layer packing beds can aid
BTFs to generate lower pressure drop. Furthermore, when compared
with the single-layer packing bed systems, multiple-layer packing beds
present higher VOCs and odorous gas removal rates.
In a BF system, the flow mode (up-flow or down-flow) is important
owing to the possibility of drying of medium, which may affect the mass
transfer. Several studies have indicated that in a BTF system, which
mainly operates in a discontinuous irrigation mode, the choice of flow
can be counter-current or co-current for liquid and gaseous phases, with
little influence on the treatment (Cox and Deshusses, 1999; Mudliar
et al., 2010). However, this may not be true at all times, for example,
sulfide formation is related to the sulfide/oxygen ratio in biogas de-
sulfurization. In addition, because of the formation of free ammonia
and free nitrite, the N/O ratio is altered, resulting in the inhibition of
ammonia removal by the BTFs (Vadivelu et al., 2007). The nutrient
solution stored in a nutrient tank can be intermittently or continuously
recirculated by using a pump and sprayed onto the top of the BTF.
Below each layer of medium, a perforated plate (carrier plate) prevents
the column packing from falling off, while simultaneously ensuring that
gas and water can pass through easily.
3.2. Parameters during operating period
The results of treatment performance in a BTF can be illustrated
using EBRT (s), RE (%), EC (g/m3h) and IL (g/m3h). The EBRT is the
relative measure of how long gas is retained within the packing
medium; this parameter critically affects the treatment performance of
a BTF (Rene et al., 2010a). The IL is the pollutant mass applied to a BTF
per unit volume of medium per unit time. The parameter RE is the
measure of pollutant removal efficiency and is expressed as a percen-
tage of the initial pollutant that is removed. The EC is defined as the
pollutant mass removed per unit volume of medium per unit time and it
represents how much pollutant mass can be removed under a given
condition. The EBRT, IL, RE and EC can be calculated using Eq. (1)–(5):
Vbed
Empty bed retention time, EBRT =
Q (1)
C (Kraakman et al., 2011). As contaminated air flows through the packing
Inlet load, IL = ⎛ in ⎞ ∗Q
⎜ ⎟
⎝ Vbed ⎠ (2)
C − Cout ⎞
Removal efficiency, RE = ⎛ in
⎜ ∗100%
⎟
⎝ Cin ⎠ (3)
C − Cout ⎞
Elimination capacity, EC = ⎛ in ⎜ ∗Q ⎟
⎝ Vbed ⎠ (4)
or
C − Cout ⎞ C C − Cout ⎞
EC = ⎛ in
⎜ ∗ Q= ⎛ in ⎞ ∗Q∗ ⎛ in
⎟ ⎜ ⎟ ⎜ = IL∗RE
⎟
⎝ Vbed ⎠ ⎝ Vbed ⎠ ⎝ Cin ⎠ (5)
where Q is the gas flow rate (m /h), Vbed is the packing medium volume
3
of the BTF (m3), and Cin and Cout are the inlet and outlet concentrations
of the gas pollutant (g/m3 or mg/m3), respectively. In some studies,
pollutant concentrations are reported in ppmv. The conversion of mass
concentration to volumetric concentration at room temperature (25 °C)
can be achieved by using the ideal gas law, shown by Eq. (6) (Iranpour
et al., 2005).
24776∗Concentration (g/m3)
Concentration (ppmv) =
Molecular weight of pollutant (g/mol) (6)
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Journal of Environmental Management 222 (2018) 409–419
Sometimes, the concentration of odorous gases can be evaluated by
the sense of smell. The odor concentration of a single odorant can be
determined using Eq. (7).
Odorous gases concentration
Odor concentration =
Odor threshold value (7)
where odorous gases concentration is the actual concentration of a
certain odorant (g/m3 or mg/m3), and odor threshold value is the
lowest concentration of the odorant that is perceivable by the human
sense of smell. However, in measuring environmental odors, which are
generally complex mixtures of compounds, the threshold cannot be
expressed as the concentration of the mixture, instead, the threshold
can only be expressed as dilution-to-threshold ratios, and D/T means
dilution to threshold ratio (V/V) (Cha, 1998; Huang and Guo, 2018).
The unit of OU/m3 can be used to establish the odor index and odor
concentration (Gostelow et al., 2001). The main pain panel calibration
gas used is n-butanol, which produces 1 OU/m3 at a certain dilution
rate. In general, the result of odorant sample measurement can be
significantly affected by the dilution system, sample presentation, pa-
nelist selection, training, panel size, as well as panelist olfactory acuity
(Cha, 1998).
Mineralization is the term used to describe the complete bio-
conversion of a target compound to biomass, CO2, water and possibly
inorganic salts or acids. In aerobic biodegradation, VOCs are ultimately
degraded to CO2, and water by microorganisms, and the energy (ATP)
generated during this process is utilized by the microorganisms for
biomass production. Thus, the CO2 production rate may provide valu-
able information about the performance of a BTF. The mineralization
degree of organic pollutants denotes the amount of organic C being
converted to CO2 (Vert et al., 2012), and also reflects the degradation
level of VOCs. For example, the mineralization degree of CO2 can be
calculated as shown in Eq. (8). In addition, for accurate quantification
of mineralization levels, the C levels fixed in the biomass should also be
taken into consideration.
mole of CO2 produced
CO2 % = ∗100%
Mole of C in VOCs consumed (8)
4. Mass transfer in BTFs
As shown in Fig. 4, mass transfer in BTF systems consists of gas-
liquid and liquid-biofilm transfer, and is frequently assumed to be a
balance of the two processes at the interfaces of the two phases
bed, pollutant vapors, oxygen, and other molecules can be transferred
to the trickling water phase or directly to the biofilm (Cox and
Deshusses, 1998). The mass transfer rate for pollutants from air to
water phase in the BTFs is related to Henry's law constant of pollutants.
As the contact between the microorganisms and pollutants occurs after
VOC diffusion into the liquid film, the liquid flow and cyclic frequency
of trickling liquid are critical parameters for mass transfer. The pH, salt,
or metabolite concentration can be controlled by the trickling liquid to
guarantee a favorable environment for microorganisms to metabolize
pollutants. When the water membrane surrounding the microorganisms
is saturated by pollutants, liquid solution can dilute the pollutant con-
centration and decrease the diffusion limitation (Wu et al., 2016b). The
trickling liquid also supplies nutrients for the growth of microorgan-
isms, and usually contains N, P, and trace elements. Besides, the VOCs
in waste gas usually serve as the C source to be metabolized by mi-
croorganisms (Cheng et al., 2016a). However, sometimes other C
sources need to be added into the nutrient solution to act as co-meta-
bolism substrates to promote the removal of odorants and VOCs. For
example, toluene, methane, phenol, and methanol can make tri-
chloroethylene (TCE) more bioavailable and have been proved to be
good primary C sources during TCE removal in BTFs (Chheda and
Sorial, 2017). Furthermore, co-metabolites may help stimulate the
H. Wu et al.
Fig. 4. Mass transfer and the function of surfactants during the biodegradation
of biotrickling filter (BTF) system. The truck icon denotes factors that can
promote mass transfer, such as added surfactants.
release of substrate-oxidizing enzymes that assist the catalytic trans-
formation of target pollutants along with the primary substrates
(Suttinun et al., 2012).
Owing to the removal mechanism, BTFs are more adapted for the
elimination of water soluble VOCs. However, many VOCs are hydro-
phobic (such as ethane, pentane, hexane, and cyclohexane) or moder-
ately hydrophobic (including TCE, chlorobenzene, BTEX, styrene, etc.)
(Henry coefficient Hc = Cg/Cl, ranging from 0.1 to 70) (Cheng et al.,
2016a), and thus, the main rate-limiting factor might be the transpor-
tation of hydrophobic VOCs from the gas phase to the liquid and biofilm
phase (Hassan and Sorial, 2010). To lower the mass transfer limitations,
some hydrotropic agents should be added into the reactor.
Fig. 4 indicates that the addition of mass transfer factor can promote
the process of mass transfer. To increase the solubility of hydrophobic
VOCs, the addition of surfactants is a common choice. Surfactants are
commonly classified as (1) anionic surfactants; (2) cationic head
groups; (3) zwitterionic (amphoteric) surfactants; and (4) nonionic
surfactants. They are usually organic compounds that are amphiphilic
owing to their hydrophobic tails and hydrophilic heads (Rosen, 2012).
When diffusing into water, surfactants get adsorbed at the interfaces
between air and water. In the case of water mixed with organic phase,
surfactants are adsorbed at the interface between the organic phase and
aqueous phase. As a result, the water-insoluble hydrophobic group
extends out of the bulk water phase into the air or organic phase,
whereas the water-soluble head group remains in the water phase (Hu
et al., 2013).
Surfactants make the hydrophobic compounds more bioavailable in
the BTFs by reducing the mass transfer resistance between the gas phase
and liquid (or solid) phase (Yang et al., 2010a). Ramirez et al. (2012)
reported that when Brij-35 (a non-ionic surfactant) was added, the
methane conversion doubled with respect to that of BTFs without
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Journal of Environmental Management 222 (2018) 409–419
surfactant. Due to the low water solubility and high vapor pressure of
some VOCs (such as styrene), removal by typical wet-scrubbing pro-
cesses is difficult. Song et al. (2012) reported that by adding Triton X-
100, the RE of their BTF under three different inlet loads increased from
87% to 96%, 70%–92%, and 50%–82%, respectively.
Although surfactants can promote mass transfer during the removal
process of VOCs and other waste gases, some problems occur with their
use. Some surfactants themselves are contaminants of water and air,
and some are toxic to humans and microorganisms, and may lead to
several serious diseases (Fabrega et al., 2014). Also, most surfactants
with low concentration can act as a carbon resource for some micro-
organisms. Thus, excessive metabolism of surfactants by microorgan-
isms may decrease the metabolism of VOCs and other odorants, re-
sulting in a decrease in the treatment performance of a BTF. Thus,
finding new surfactants and novel methods of surfactant usage is es-
sential to improve the VOC removal performance of BTFs. Wang et al.
(2013) used Zn2+ combined with non-ionic surfactant Tween-20 to
remove ethylbenzene in a BTF; as a result, RE was increased and ex-
cessive biomass was removed.
Recently, the use of biosurfactants in the biodegradation of VOCs
and odorants has attracted much attention because these natural
compounds have advantages over synthetic surfactants, including being
more environment friendly, less toxic, and more biodegradable (Zhou
et al., 2011). Biosurfactants are surface-active substances synthesized
by living cells, especially by bacteria or other microorganisms. To en-
hance mobilization and bioavailability of hydrophobic compounds,
biosurfactants have been extensively studied. Some popular microbial
biosurfactants include emulsan produced by Acinetobacter calcoaceticus
(Foght et al., 1989), sophorolipids produced by several yeasts belonging
to Candida and the Starmerella clade (Kurtzman et al., 2010), and
rhamnolipids produced by Pseudomonas aeruginosa (Li et al., 2014). Tu
et al. (2015) indicated that the biosurfactant saponins can considerably
enhance the n-hexane removal performance of a BTF and decrease the
biomass accumulation rate in the packing bed. Rhamnolipids consists of
one or two hydrophilic rhamnose molecules (Rha-) and up to three
molecules of hydrophobic hydroxyl fatty acids, and stimulate the de-
gradation of some VOCs such as hexadecane, octadecane and phenan-
threne by P. aeruginosa (Li et al., 2014). If present in the liquid phase,
rhamnolipids are expected to solubilize VOCs within the micelle
structure (or cause the biofilm surface to become more hydrophobic, or
both), and decrease the surface and interfacial tensions between gases,
liquids and biofilms, thereby increasing the availability of VOCs to the
bacterial cells (Li et al., 2014).
5. Packing materials in BTFs
5.1. Classification of packing materials used in BTFs
The packing materials used for VOCs and odorant removal in BTFs
can be typically divided into three categories: inorganic, organic and
mixed materials. Some traditional inorganic packing materials usually
come directly from nature such as perlite and lava. Their shape may be
irregular but these natural materials have good surface properties.
Other inorganic packing materials (such as ceramic or Raschig rings)
can be synthesized, and a foaming agent is sometimes used to improve
porosity and surface area of these materials (Lee et al., 2013). Although
the inorganic packing materials require the addition of mineral nu-
trients, they have the advantage of uniform structure and size, which
reduces compaction and allows better airflow distribution (Ortiz et al.,
2003).
Initially, organic packing materials used in early BTFs were similar
to those used in BFs, such as soil, peat and wood chips. Subsequently, a
variety of synthetic organic packing materials, such as plastic pall rings,
rubber particles, and other materials have been applied in the BTF or
other systems (Park et al., 2011). These kinds of organic packing ma-
terials have smooth surface and do not contain pore structure.
H. Wu et al. Journal of Environmental Management 222 (2018) 409–419

Table 2
Removal of commonly found VOCs and odorous compounds in BTFs.
Packing material Waste air composition Performance
Pollutant Conc. (mg/m3) EBRT (s) RE (%) EC (g/m3h) Reference
Odorous N and S compounds
PU and organism-suspend H2S 300–650 53–79 65–100 39.95 Chen et al. (2016b)
PU Methyl mercaptan 20–25 7–50 47.8–100 < 17.28 (Lebrero et al., 2012b)
Maifanite/ceramic Dimethyl disulfide < 25 123 100 19.0/16.6 Chen et al. (2016a)
Perlite Nitro-benzene 100–300 24 80–90 13.1 Oh and Bartha (1997)
Structured plastic tube Ammonia 9.6 1.2 82 24 Melse et al. (2012)
Ceramic particle Aniline 10–60 42–166 42–100 6.9–12.2 Li et al. (2012)
Chlorinated VOCs
Lava rock TCE 53.6–337.1 202.5 20.8–92.2 1.7–2.6 Quan et al. (2017)
PUF cube Chlorobenzene 200–800 20–75 < 91.6 < 117 Zhou et al. (2016)
Ceramic material Chlorobenzene 100–1750 15–60 < 96 < 95 Zilli and Nicolella (2012)
Non-chlorinated VOCsr
Ceramsite Toluene 384–8420 8–128 98.86 234.23 Sun et al. (2013)
Ceramsite Methyl acrylate 75.3–7234 200–400 40–100 < 8.39 Wu et al. (2016b)
Pall ring Styrene 500–1200 60–120 95 70–110 Zamir et al. (2015)
Perlite Acetone 10–8900 17.1–137 75.6 < 257 Rene et al. (2010b)
Plastic and PU Isopropanol 298–1095 14–160 > 80 30.11–59.25 Pérez et al. (2013)
PU Hexane 600 7.5–30 56.8–91.3 < 99.8 Tu et al. (2015)
Lava rock Formaldehyde 100 72–108 > 80 15–43 Prado et al. (2008)

However, owing to their special shape and strength, they can maintain
more biomass and increase the contact area of gas and liquid to improve
the removal performance of BTFs. For example, when compared with a
Raschig ring, the different structure and shape of the Pall ring improved
the gas-liquid distribution and utilization of the inner surface of the
ring, thus, increasing the performance by more than 50% and reducing
the pressure drop at least by half. In recent years, new organic packing
materials (such as polyurethane foam) have been developed that have
the advantages of both good surface properties and special shapes
(Hernandez et al., 2013). These novel materials are not only able to
maintain or intercept more microorganisms, but also adsorb the pol-
lutant molecules (Singh et al., 2010b).
Packing materials (inorganic or organic) that can operate in BTFs
for long periods are called inert packing materials. In general, inert
packing materials are the most commonly used in BTFs (Cox and
Deshusses, 1998). Mixed packing material can be described as the
combination of natural organic packing material and inert packing
material in a BTF, or as a single packing material that has different
components. Mixed packing material can be used to minimize bed
compaction and avoid clogging. Chen et al. (2016b) achieved high RE
and EC of H2S from air using a two-layer BTF packed with activated
carbon-loaded polyurethane in the upper layer and modified organism-
suspended fillers in the lower layer.
5.2. Characteristics of packing materials in BTFs
As one of the core factors in BTF systems, packing materials must
satisfy some requirements such as optimal environmental conditions for
microbial activity, adequate area to sustain growth and activity of mi-
croorganisms, optimal particle size to prevent high bed pressure drop,
and ability to resist compaction to avoid high bed pressure drop and
allow uniform air flow distribution through the bed. Many factors (such
as specific surface area, moisture holding capacity, density and ten-
dency to compact, adsorption properties and nutrient supply) de-
termine the characteristics of a packing material to be used in a BTF
system (Dorado et al., 2010). Good packing materials must have spe-
cific physicochemical properties such as high porosity, high surface
area, good mechanical resistance and water retention capacity to
guarantee microbial growth and biofilm adhesion (Kim and Deshusses,
2008). Furthermore, good water-holding capacity (40%–80% by weight
for organic packing materials) of the packing material is necessary, and
in most cases 40%–80% of porosity or void volume can ensure both gas
plug flow and low pressure drop. For bulk packing materials, the par-
ticles should be relatively small (diameter of 1–5 cm) to ensure large
surface area for both pollutants mass transfer and microbial im-
mobilization (Devinny et al., 1999a; Kennes and Thalasso, 1998). It
must be noted that owing to the inertness of the packing materials, the
adsorption of pollutants is usually minimal in the BTFs. However, if the
concentration of the contaminants does not reach a high level, biode-
gradation cannot occur. Therefore, good packing material should ac-
cumulate relatively high concentrations of pollutants to ensure biode-
gradation occur. Moreover, liquids should be uniformly distributed on
the surface of the packing material and air should easily flow through
the packing material. Besides, low-cost and recyclable sources should
also be considered when selecting packing materials for BTF systems.
Although nutrients are always externally provided in the BTFs, the
packing material should also contain some nutrients that can promote
biofilm formation and microbial metabolism (Hernandez et al., 2010).
In addition, in a BTF, the packing bed can be either randomly filled
with small packing materials or with specifically designed structured
packing materials (Dorado et al., 2015; Montebello et al., 2014). Dif-
ferent packing structures have varied surface areas and void space be-
tween the packing bed, which influence the mass transfer and removal
performance of the BTF systems. San-Valero et al. (2014) reported that
the structured packing material (specific surface area and mass transfer
coefficient of 410 m3m-2 and 175 h−1, respectively) exhibited a higher
mass transfer coefficient, when compared with that presented by two
types of random packing materials (348 m3m-1, 130 h−1, respectively,
and 207 m3m-1, 130 h−1, respectively) in a series of BTFs to treat iso-
propanol. These results also indicated that a high specific surface area
could improve the mass transfer in BTFs. Similarly, with a high specific
surface area, the structured packing material can also exhibit a higher
mass transfer, which could be attributed to the effect of different flow
paths within the packing materials. However, a significant decrease in
mass transfer may occur when clogging develops in the structured
packing material. Conversely, random packing materials could more
readily promote channeling than structured packing materials. Thus, a
mixed packing bed, with upper layer packed with structured packing
material and lower layer packed with bulk packing material may be a
good strategy to improve the mass transfer in BTF systems. Table 2
summarizes the biodegradation of a wide range of pollutants in BTFs
and the packing materials used, operation conditions, and removal
performance. It can be noted from the table that many odorous com-
pounds and VOCs can be efficiently removed by BTFs with suitable
packing materials.
Sometimes packing materials can act as the link between BTF
technology and other technologies. Wu et al. (2018) reported the use of
a self-made conductive packing material in a BTF to treat toluene waste

414
H. Wu et al.
gas, and analyzed the influence of applied voltage on toluene removal
performance and microbial community. Their findings indicated that
during the biodegradation process an electrical potential difference
could be generated between the bottom and top of the packing bed
without external voltages, and that the potential difference decreased
with increasing total flow rate. However, application of an external
voltage was found to significantly change the bacterial community.
Some researchers have used coke, which is also electrically conductive,
as a packing material to combine BTF technology with microbial fuel
cell (MFC) technology. In their BTF-MFC system, a graphite rod and
porous coke were used as the anode, and a polyvinyl alcohol membrane
electrode assembly was used as the cathode to form an electric circuit,
with both the anode and cathode connected with titanium wire (Wu
and Lin, 2016). This BTF-MFC not only removed ethyl acetate with high
efficiency, but also continuously generated electricity and ensured ef-
fective use of chemical energy in waste gas (Wu et al., 2016a). Thus,
combining BTF with other technologies could also be a possible way of
developing new packing material. In addition, development of new
packing materials in BTF systems that can chemically react with air
pollutants, such as the Fe-C packing materials used in wastewater
treatment (shown in Fig. S1 in Supplementary Data) is also an attractive
option (Li et al., 2011; Wang et al., 2016) and needs further in-
vestigation. The electrochemical reaction between the packing mate-
rials and pollutants could promote the biodegradation of refractory
pollutants and enhance the removal performance of BTFs.
6. Microorganisms in BTFs
The removal performance of VOCs and odor pollutants by BTF
systems is not only significantly affected by the physicochemical
properties of the pollutants, but also by the microorganisms (Cheng
et al., 2016a; Cox and Deshusses, 1998; Zehraoui et al., 2012). In BTF
processes, ensuring adequate supply of nutrients to the microorganisms
is essential to support their growth. The microbial growth is controlled
by nutrients in trickling liquid, temperature, pH, O2 content, and
moisture, and the optional conditions are listed in Table 3 (Schiavon
et al., 2016). The microbial community is a critical parameter in BTF
systems. Usually, microbes are the decomposer organisms in the natural
environment and can completely degrade many pollutants. The mi-
crobial species that are present, their population densities, the meta-
bolic transformations they are catalyzing, and their interactions with
their environment and each other are fundamental to BTF operation. To
acquire a better understanding of the relationship between microbial
diversity and the performance of a BTF, knowledge about the structure
and dynamics of microbial communities is required. Thus, the analysis
of the microbial communities that are present in BTFs is important and
necessary.
6.1. Microbial community analysis methods
The analysis of the microbial community in BTFs usually examines
the biofilm on the surface of packing materials. However, as some
species of microorganisms in BTFs are unculturable and the complex
environment in BTFs is difficult to reproduce and simulate outside of
BTFs, the strategy for analyzing biofilm after the culturing and pur-
ification of strains should be limited (Vaz-Moreira et al., 2013). After
culturing, the variety of species of microorganisms may decrease
Table 3
Optimal conditions for the growth of microorganisms in BTFs.
Nutrient Temperature pH O2 content Moisture
C:N:P = 100:5:1 10–40 a
7–8 °C 5–15% 60–80%
a
In general, for heterotrophic species, when removing acid (such as H2S),
the optimal pH should be 1–2.
415
Journal of Environmental Management 222 (2018) 409–419
drastically so that the analytical result does not reflect the actual bio-
film that exists in BTFs. Many biological molecular methods have been
applied to examine biofilms and analyze the microbial community in
BTFs, including fluorescence in situ hybridization (Kristiansen et al.,
2011), polymerase chain reaction-denaturing gradient gel electro-
phoresis (PCR-DGGE) with cloning and sequencing (Wu et al., 2016b),
and high-throughput sequencing (Hu et al., 2016). Of these methods,
PCR-DGGE and high-throughput sequencing appear to be the most
popular (Cheng et al., 2010; Li et al., 2012; Quan et al., 2017; Wu et al.,
2016b).
DGGE is widely applied to evaluate microbial diversity of several
environments, to “profile” complex microbial communities and to infer
the phylogenetic affiliation of the community members (Aguirre et al.,
2018; Perez et al., 2015, 2016; Wei et al., 2015; Wu et al., 2016b). The
experimental workflow and change in DNA during an experiment are
shown in Fig. S2 (Supplementary Data).
High-throughput (formerly “next-generation”) sequencing can si-
multaneously detect tens of hundred to million DNA sequences, and has
many applications in the BTF systems (de Magalhaes et al., 2010; Quan
et al., 2018; Wu et al., 2018). Besides, this technology allows massive-
scale DNA sequencing at a low cost and high speed. Currently, high-
throughput sequencing used in microbial community analysis mainly
includes Illumina® Solexa™ methods, Roche 454 GS FLX System, ABI
SOLiD® (Supported Oligo Ligation Detection), and Life Technologies Ion
Torrent™ (Mardis, 2008; Meyer et al., 2008; Quail et al., 2008). All of
these sequencing platforms have the advantages of high-throughput,
high speed, and low costs (Mason and Elemento, 2012). Similar to
DGGE, these platforms produce sequencing results that can be further
analyzed to obtain diversity indices and some other useful information.
6.2. Microorganisms in BTF systems
The effectiveness of a BTF depends on the ability of the micro-
organisms to biodegrade pollutants (Prachuabmorn and Panich, 2010).
Microorganisms differ in their degradation performance in treating a
particular pollutant. The biofilms in BTFs usually consist of high
numbers of bacteria and low numbers of fungi; thus, most articles focus
on the analysis of bacterial communities (Zhao et al., 2014). Bacteria of
the genera Pseudomonas, Bacillus, Staphylococcus and Rhodococcus are
most often found in BTFs. Pseudomonas has been identified as the
dominant species of the bacterial population in different bioreactors
used to remove nitrogen, H2S and many VOCs (Giri et al., 2014; Li
et al., 2014; Zheng et al., 2016). Bacillus can occur simultaneously
under aerobic nitrification-denitrification conditions, Staphylococcus
can reduce nitrate to nitrite (Cheng et al., 2010), and Rhodococcus has
the ability to metabolize harmful environmental pollutants, including
toluene, naphthalene, herbicides, and other compounds (Baltrenas
et al., 2015).
Although pollutant degradation in BTFs is usually attributed to
bacteria, sometimes, fungi may play an important role. Some studies
have indicated that fungi exhibit a higher VOC removal performance
than bacteria (Cox and Deshusses, 1998; Giri et al., 2014). Moreover,
fungi allow easy absorption of many VOCs from the bulk gas phase
because of their filamentous structures with aerial mycelia and a large
surface area (Kraakman et al., 2011). Meanwhile, the resistance of fungi
to low humidity favors mass transfer of hydrophobic VOCs from the gas
phase to fungal surfaces. Compared with bacteria, fungi can better re-
sist the environments of low humidity and high acidity (Prenafetaboldú
et al., 2008). Therefore, using fungi as the main degradation micro-
organism in BTFs has great potential.
Filamentous fungi belonging to the genera Scedosporium,
Paecilomyces, Cladosporium and Cladophialophora, white-rot fungi and
yeasts of the genus Exophiala are often obtained in BTFs (Repeckiene
et al., 2015). Jin et al. (2007) indicated that a fungi-dominated BTF
showed a good potential to withstand shock loads in the treatment of
alpha-pinene and could rapidly achieve its full performance after a 3–7
H. Wu et al. Journal of Environmental Management 222 (2018) 409–419

Table 4
Studies on the RE, and microbial community of current BTF systems for removing VOCs and odor waste gases.
Contaminant Max RE Microbes type Predominate strain Reference

Hydrogen sulfide 99.8% Bacterial Thiobacillus thioparus Ramirez et al. (2009)

100% Bacterial Thiothrix spp., Thiobacillus denitrificans Zhou et al. (2015)
95% Bacterial Acidithiobacillus thiooxidans, Acidiphilum sp. Montebello et al. (2013)
Ammonia 100% Bacterial Sinorhizobium meliloti, Pseudomonas sp. Cheng et al. (2010)
99% Bacterial Nitrosospira sp., Nitrosomonas sp. Yin and Xu (2009)
NOX 92.3% Bacterial Chelatococcus daeguensis TAD1 Yang et al. (2012)
BTEX (mixed) 96% Bacterial Fungal Pseudomonas putida, Rhodococcus erythropolis, Cladosporium sphaerospermum, etc. Raboni et al. (2017)
Toluene 98% Bacterial Burkholderia sp. strain T3 Sun et al. (2013)
100% Bacterial Bacillus cereus S1 and S2 Li et al. (2008)
Ethylbenzene 90% Bacterial Pseudomonas oleovorans DT4 Chen et al. (2014a)
Chlorobenzene 85% Bacterial Ralstonia pickettii L2 Zhou et al. (2016)
Styrene 95% Fungal Sporothrix variecibatus Rene et al. (2010a)
95% Bacterial Ralstonia eutropha Zamir et al. (2015)
Aniline 100% Bacterial Uncultured bacterium AB185009, etc. Li et al. (2012)
Dimethyl disulfide 100% Bacterial Bacillus cereus GIGAN2 Chen et al. (2016a)
100% Bacterial Pseudomonas putida, Pseudomonas acidovorans, etc. Chung et al. (2010)
Methyl mercaptan 95% Bacterial Dokdonella sp., Thiobacillus denitrificans Lebrero et al. (2012b)
Acetone 75.6% Fungal Sporothrix variecibatus, Sporothrix sp. Rene et al. (2010b)
Isopropanol 90% Bacterial Pseudomonas putida, Pseudomonas sp. Pérez et al. (2013)
Siloxanes 74% Bacterial Pseudomonas aeruginosa S240 Li et al. (2014)
Methyl acrylate 100% Bacterial Variovorax paradoxus, Hyphomicrobium denitrificans, etc. Wu et al. (2016b)
Trichloroethene 90% Bacterial Dehalococcoides strain Popat and Deshusses (2009)
59.2% Fungal Ascomycota strain Quan et al. (2018)

days starvation period. Furthermore, fungi can remove highly con-
centrated VOCs in highly acidic conditions (Zehraoui et al., 2014).
However, fungi also have some drawbacks. Compared to bacteria, fungi
have generally lower metabolic rates that make the start-up periods of
BTFs much longer and their filamentous structure often leads to clog-
ging in BTFs.
Studies on the characteristic of current BTF systems for several ty-
pical VOCs and odor waste gases removal are summarized in Table 4.
To improve the removal performance of BTF, bacteria-dominated BTF
and fungi-dominated BTF can be combined. Cheng et al. (2016b) set up
three different BTFs (bacterial BTF, fungal BTF and bacterial-and-fungal
BTF) to study the difference in the treatment of toluene. The bacterial-
and-fungi BTF reached an RE of 90%, while the RE of the fungal BTF
and the bacterial BTF were 60% and 20%, respectively.
7. Other techniques combined with BTF systems
Combination of a BTF system with other types of treatment can
achieve much better removal performance than the use of BTF system
alone. Some microorganisms can produce different kinds of enzymes
such as monooxygenase, which can enhance the degradation of re-
fractory VOCs to simple molecules (Pant and Pant, 2010). Co-metabo-
lism can help the microorganisms to stimulate the release of substrate
oxidizing enzymes. Quan et al. (2017) used a static magnetic field
combined BTF to treat TCE waste gas and compared this combined
technique to a single BTF. The results indicated improved TCE removal
performance and alteration in the bacterial community under 60 mT of
magnetic field intensity. Magnetic field strengthening can produce si-
milar effects of pollutant removal with the addition of phenol and so-
dium acetate as co-metabolic substrate. Furthermore, different mag-
netic field intensities significantly affected the fungal community in the
BTF systems and improved the abundance of the phylum Ascomycota,
thus increasing the TCE removal rate (Quan et al., 2018). Similar to
using enzymes, pretreatment of refractory VOCs could promote the
metabolism of pollutants by microorganisms. For example, in the
treatment of some aromatic compounds such as styrene and chlor-
obenzene, UV pretreatment is usually used prior to a BTF system (Zhu
et al., 2015). The UV energy can directly convert the hydrophobic and
stable VOCs into water-soluble and easily biodegradable intermediates,
making it an efficient pretreatment step prior to BTF treatment. As a
result, both mass transfer and reaction rate are enhanced by UV
pretreatment because it transforms pollutants into more soluble and
biodegradable compounds. Besides UV, plasma or other photolysis
pretreatment strategies can also be applied (Dobslaw et al., 2017; Wei
et al., 2013; Zeng et al., 2016).
8. Conclusions and perspectives
BTF systems play an important role in the intensive treatment of
VOCs and odorants that occur in large volumes and low concentrations.
Many factors affect the removal performance of VOCs and odorous
pollutants in BTFs. Briefly, the operation of BTF needs suitable inlet
concentration/load and trickling recycling rate to guarantee optimized
mass transfer, nutrient supplementation, and microbial activity.
Packing materials in BTFs should have specific physicochemical prop-
erties and provide an adequate environment for the growth of micro-
organisms and enhance the performance of biological activities.
Superior quality packing materials can also be used in pollutants de-
gradation reactions. As different microorganisms have their own ad-
vantages, it is important to choose a suitable microbial community.
Some enzymes produced by microorganisms can also convert refractory
pollutants to simple and soluble ones, which can enhance the removal
performance.
Moreover, further developments of BTF systems should focus on
innovations that combine a BTF system with other physical, chemical,
and biological technologies. These combinations can not only improve
the pollutant removal performance but also give BTF technology a
function of resource renewal by power generation. Hence, to improve
the performance of BTF systems for removing VOCs and odors, there is
a need for continuous innovation in bioreactor configurations.
Acknowledgments
This work was supported by the National Natural Science
Foundation of China (No. 21662038, No. 21661031).
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://dx.
doi.org/10.1016/j.jenvman.2018.06.001.

416
H. Wu et al.
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