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Atmospheric Pollution Research xxx (xxxx) xxx–xxx

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Atmospheric Pollution Research


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Phytoremediation of benzene vapors from indoor air by Schefflera arboricola


and Spathiphyllum wallisii plants
Iman Parseha, Hakimeh Teirib, Yaghoub Hajizadehc,∗, Karim Ebrahimpourc
a
Student Research Committee, Department of Environmental Health Engineering, Isfahan University of Medical Sciences, Isfahan, Iran
b
Department of Environmental Health Engineering, School of Health, Shiraz University of Medical Sciences, Shiraz, Iran
c
Environment Research Center, Department of Environmental Health Engineering, Isfahan University of Medical Sciences, Isfahan, Iran

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

Keywords: Benzene is a carcinogenic contaminant. It is therefore important to remove it from the environment. In this
Indoor air study, phytoremediation of benzene from polluted air by two plant species (Schefflera arboricola and
Benzene Spathiphyllum wallisii) was investigated under controlled environment using a Plexiglas chamber. The effect of
Phytoremediation inlet benzene concentrations of 3.6–29.5 μg/m3, and empty bed residence time (EBRT) of 37.5 and 70 s were
Schefflera
tested on the plant efficiency for a period of 36 days. Results showed that the outlet benzene concentration in the
Spathiphyllum
control chamber (plant free) was significantly higher than that in the chamber containing the plants. The
average removal efficiency (RE) at various inlet concentrations including 3.5–6.5, 10.5–16.3, and 25–30 μg/m3
were 97%, 94%, and 91%, respectively. Also, the average RE at EBRTs of 37.5 and 75 min were 93% and 94%
respectively. According to the physiological and morphological tests, no toxicity effects on the plants were found
at these concentrations. It can be concluded that the plant's application is a green and environment-friendly
technology to remove benzene from the polluted indoor air.

1. Introduction and Jantunen, 2001; Jia et al., 2008; Sexton et al., 2007).
Inhalation is account for 95–99% of the benzene exposure. In the
Most people spend about 90% of the day in an indoor environment. United States, daily intake of benzene from the indoor and outdoor air
Thus, indoor air pollution can cause significant adverse health effects. has been estimated between 180 and 1300 μg/day, respectively
Volatile organic compounds (VOCs) are the most important indoor (Krzyzanowski and Cohen, 2008; Sriprapat and Thiravetyan, 2013).
pollutants (Pluschke, 2004). Benzene (CAS number 71-43-2; C6H6; Acute exposure to benzene can cause dizziness, headaches, as well as
molecular weight 78.1 g/mol) is one of the most hazardous VOCs; it is a eye, skin, and respiratory tract irritation. Its chronic exposure can result
monocyclic aromatic hydrocarbon present in both indoor and outdoor in leukemia, and have adverse effects on the developing fetus and re-
air. However, according to some studies, it's concentration in indoor is productive system. The International Agency for Research on Cancer
higher than outdoor (Amagai et al., 2002; Edwards and Jantunen, 2001; (IARC) has categorized the benzene as group 1 carcinogen (known
Schneider et al., 2001). carcinogenic to humans) (IARC, 2004; Wilbur et al., 2007).
Benzene is mainly introduced into the atmosphere through in- There are many physiochemical methods to remove VOCs from
dustrial processes, direct evaporation and automobile exhausts. It also polluted air, including heat treatment, catalytic oxidation, adsorption,
releases to the indoor air through other sources such as tobacco smoke, scrubbing, photocatalytic destruction, thermal combustion, and biolo-
wood burning, building materials and furniture, stored solvents, gical methods (Kumar et al., 2011). Nowadays, it has been proven that
cooking systems, and other human activities (Esplugues et al., 2010; existing methods have no proper capability to remove the indoor air
WHO, 2010). Different studies have measured the concentration of pollutants due to the problems linked to their very low concentrations
benzene in the indoor environment between 3.24 and 32.4 μg/m3 (Guieysse et al., 2008). Phytoremediation, the use of plants to remove
(1–10 ppb) (Brunnemann et al., 1989; Clayton et al., 1999; Kinney pollutants from the environment, is an inexpensive and cost-effective
et al., 2002). Also, the measured indoor levels of benzene in the United technique that is able to remove pollutants at low concentrations
States ranged from 2.6 to 5.8 μg/m3 (Brunnemann et al., 1989; Edwards (Sriprapat and Thiravetyan, 2013). Many studies have been conducted

Peer review under responsibility of Turkish National Committee for Air Pollution Research and Control.

Corresponding author.
E-mail addresses: iparseh97@gmail.com, iman_parseh@hlth.mui.ac.ir (I. Parseh), h_teiri@yahoo.com (H. Teiri), y_hajizadeh@hlth.mui.ac.ir (Y. Hajizadeh).

https://doi.org/10.1016/j.apr.2018.04.005
Received 4 November 2017; Received in revised form 8 April 2018; Accepted 20 April 2018
1309-1042/ © 2018 Turkish National Committee for Air Pollution Research and Control. Production and hosting by Elsevier B.V.

Please cite this article as: Parseh, I., Atmospheric Pollution Research (2018), https://doi.org/10.1016/j.apr.2018.04.005
I. Parseh et al. Atmospheric Pollution Research xxx (xxxx) xxx–xxx

on phytoremediation of VOCs from different environments (air, soil, Table 1


and water) (Alavi et al., 2017; Guieysse et al., 2008; James and Strand, Operational conditions in various phases.
2009; Sriprapat and Thiravetyan, 2013; Suchkova et al., 2014). Plants phase Treatment type EBRT Inlet concentration Operating time
can remove pollutants from the environment through some mechanisms (min) ranges (μg m−3) (days)
such as phytodegradation, phytostabilization, phytovolatilization,
I Control (without 37.5 10.5–16.3 6
phytoextraction, phytofiltration, and rhizodegradation; however, more
plant) 75 10.5–16.3 6
than one may be used by the plant simultaneously. Plants mainly re- II Planted with 37.5 3.6–6.5 3
move VOCs from the polluted air through phytodegradation. Other Schefflera sp. 10.5–16.3 3
mechanisms mainly occur in the soil.(Favas et al., 2014; Alavi et al., 25–29.5 3
2017; Omasa et al., 2012). 75 3.6–6.5 3
10.5–16.3 3
The main objective of this study was to investigate benzene phy-
25–29.5 3
toremediation from polluted air using two ornamental plants including III Planted with 37.5 3.6–6.5 3
Schefflera arboricola and Spathiphyllum wallisii. These plants are popular Spathiphyllum sp. 10.5–16.3 3
and easily available and can tolerate in poor growing conditions. There 25–29.5 3
75 3.6–6.5 3
are insufficient studies on their ability to remove benzene vapor
10.5–16.3 3
(especially at low concentration of < 30 μg/m3) from the air. 25–29.5 3
Therefore, more study is needed in this field.

2. Method and materials south and above the chamber) four times a day over experimental
period using a YF-170 digital light meter (Tenmars electronics co., Ltd,
2.1. Chemicals and plants Taiwan). Average light intensity was 1850 Lux ± 150. Each pot was
watered every two days (100–150 mL of tap water).
All required chemicals including benzene, n-hexylbenzene, and The experimental pots (25 cm height and 20 cm diameter) contained
carbon disulfide (CS2) were obtained from Sigma-Aldrich Company. about 7 kg/pot of a homogeneous mixture of sand (30%), silt (30%),
Sorbent charcoal tubes (Cat. No.: 226-01) used for benzene sampling clay (15%), and humus (25%). There were two plants of Schefflera sp.
was obtained from SKC Company. Schefflera sp. (each pot contained a and three plants of Spathiphyllum sp. in each experimental pot. As
plant having 5 main stems with an average height of 62.1 cm) and shown in Table 1, three various treatments were applied in order to
Spathiphyllum sp. (each pot contained three plants with an average determine the removal efficiency (RE) of the plants and the toxicity
height of 42.5 cm) were purchased from an ornamental flower shop in effects of benzene on the plants: I) Control chamber, the chamber
Isfahan, Iran. Other characteristics of the plants including total leaf without plants exposing with benzene, in order to determine the in-
area, leaf dry weight, and chlorophyll content were shown in Table 2. fluence of abiotic agents including chamber losses, absorption, and
chemical reactions on the outlet benzene concentration; II) the chamber
containing Schefflera sp. and III) the chamber containing Spathiphyllum
2.2. Chamber design and operation
sp. which were exposed to different levels of benzene concentrations.
At first, the Control chamber was operated at benzene concentration
A hard and transparent Plexiglas chamber (84 cm length, 62 cm
ranges of 10.5–16.3 μg/m3 with two different empty bed residence time
width, and 72 cm height) was used for the experiments (Fig. 1). In order
(EBRTs) of 37.5 and 75 min for 12 days. In order to conduct the second
to provide complete mixing of fumigated air, two PC fan (Model: 350
sets of experiments, two planted pots with Schefflera sp. having spacious
XA, 2.03P4) was fixed inside the chamber. The system consisted of
branches with an average areal height of 62.1 cm and soil/root height
three main compartments including i) the chamber containing plants;
of 20 cm (in order to provide sufficient leaf area for optimum air pur-
ii) an air pump connected to a flow meter and impingers system which
ification) were placed inside the chamber. In the third sets of experi-
supplies air, water vapor and benzene vapor with desired concentra-
ments, three planted pots with Spathiphyllum sp. with an average areal
tion; and iii) a sampling apparatus for sample collection from the inlet
height of 42.5 cm and soil/root height of 20 cm were placed in the
and outlet of the chamber that includes vacuum pump, flow meter,
chamber. As show in Table 1, the plants were continuously exposed to 3
solid sorbent tube and connection tubes. Stainless steel and silicone
various ranges of benzene concentrations including Range I: 3.6–6.5,
tubing were used to connect the system compartments. The inside
Range II: 10.5–16.3, and Range III: 25–29.5 μg/m3. Phytoremediation
temperature and relative humidity were held at 21 °C ± 3 and
performance of the plants under different operational conditions was
81% ± 6, respectively. The temperature and relative humidity of the
evaluated during 48 days in 3 separated phases. Operational conditions
chamber were controlled by a digital hygro-thermometer. The light
of each phase including EBRT, benzene concentration, and tests dura-
source was natural with 12 h dark-light cycles. The light intensity was
tion of each phase are signified in Table 1. Among the exposure periods,
measured around the chamber in five directions (west, east, north,
sampling from inlet and outlet of the chamber was performed every
morning and late evening (4 times for each inlet concentration) and the
averages of them were reported. It should be noted that the plant rested
for 24 h before starting the next concentration test.

2.3. Sampling and analytical methods

2.3.1. Benzene measurements


Benzene sampling and analysis were carried out in accordance with
OSHA Method 1005 (Eide, 2002). Samples are collected with
7 cm × 4 mm i. d. × 6 mm o. d. glass sampling tubes packed with two
Fig. 1. Schematic of the experimental setup: (1) air pump, (2) activated carbon sections of charcoal. The front and the back section contain 100 mg and
column, (3) Benzene solution vessel, (4) humidifier vessel, (5) mixing vessel, 50 mg of charcoal, respectively. Air samples at a known rate 0.2–0.9 L/
(6) flow meter, (7) inlet gas sampling port, (8) test chamber, (9) air mixing fan, min for a total sample size of 10–50 L were entered into the charcoal
(10) temperature & humidity sensor, (11) ventilation. tubes. After sampling, the adsorbent tube was removed and sealed with

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I. Parseh et al. Atmospheric Pollution Research xxx (xxxx) xxx–xxx

Table 2
Morphology and physiology changes of the plants during the experiments.
Plant Parameter Unit Before exposure to benzene After exposure to benzene Changes (%)

Schefflera arboricola Plant average height cm 62.1 ± 4 63.2 ± 5.1 1.7


Total Leaf area m2 5.24 ± 1.5 5.3 ± 1.1 1.1
Leaf dry weight (mg/cm2) 4.25 ± 1.3 4.5 ± 1 5.5
Chlorophyll content mg/g 3.22 ± 0.5 3.85 ± 0.3 16.4
Carotenoids mg/g 6.35 ± 1 8.15 ± 1.2 22.1
Spathiphyllum wallisii Plant average height cm 42.5 ± 4.5 43.3 ± 4 1.8
Total Leaf area m2 4.52 ± 1.5 4.6 ± 1.7 1.7
Leaf dry weight (mg/cm2) 3.85 ± 0.4 4.15 ± 0.7 7.2
Chlorophyll content mg/g 2.8 ± 0.2 3.6 ± 0.4 22.2
Carotenoids mg/g 5.4 ± 1.6 7.15 ± 2.5 24.5

EBRT = V / Q (1)

(
RE = 1 − Cout Cin ) × 100 (2)

EC = Q (Cin − Cout )/ SL (3)

where V is chamber volume (m3); Q is the inlet polluted air flow to the
chamber (m3/h); Cin and Cout are the inlet and the outlet concentrations
of benzene (mg/m3), respectively; and SL is the total leaf area (m2) of
the plants in the chamber.

2.5. Statistical analysis

Data were analyzed using the statistical software package (SPSS


Version 16). The significance value was ≤0.05. The mean of the dif-
Fig. 2. The effect of the plants on the RE. ferent tests was compared using some tests including ANOVA, post hoc
(LCD) test, and T-test.
plastic end caps. Then the plastic end caps were removed from the
sample tube and carefully transferred each section of the adsorbent to 3. Results and discussion
separate 2-mL vials. 1.0 mL of extracting solution (CS2 containing
0.25 μ$props_value{literPattern}/mL n-hexyl benzene) was added to 3.1. Influence of the plants on benzene removal
each vial and the vials were immediately sealed with PTFE-lined caps.
The vials were wagged on a shaker for 30 min, then 1.0 μL of the pre- As shown in Fig. 2, the average RE in planted treatments
pared samples were injected to a Gas Chromatograph with DB-1 ca- (93.5 ± 3%) was significantly (p < 0.005) more than its value in the
pillary column (60-m × 0.32 mm i. d and 5.0 μm df) coupled with a unplanted treatment (17 ± 5%). One reason for the removal of ben-
Flame Ionization Detector (GC-FID). Separation was achieved according zene in the unplanted chamber can be photolysis process
to the following program: the initial oven temperature was 60 °C (Mahmoudkhani et al., 2016; Park et al., 2011). Another reason is the
(holding time was 5 min) and increased to 220 °C (final temperature) adsorption of benzene by the chamber walls and the potted soil. Some
with a temperature ramp of 10 °C/min and was held for 14 min. One-μL benzene molecules were adsorbed by the soil and may be broken down
aliquot of the extract was injected in the split-less mode. Each analysis by the soil microorganisms. In this study, this mechanism can be ig-
was duplicated. nored. Because the absorption rate is negligible. It is mostly important
in phytoremediation of polluted soil where microorganisms are directly
contact with pollutants. Therefore, it can be said that a part of the RE in
2.3.2. Morphological and physiological characteristics
planted treatments belonged to the abiotic agents and the potted soil
Some morphological and physiological characteristics of the plants
which may have microbes (control 1). The average RE by Schefflera sp.
including plant height, leaf area, dry weight, chlorophyll content and
was slightly higher than that by Spathiphyllum sp. This may be due to
carotenoid were measured before and after benzene exposure (Table 2).
the higher leaf area of Schefflera sp. (5.2 m2) than Spathiphyllum sp.
Each analysis was duplicated. These parameters were also measured for
(4.5 m2). However, this difference was not significant (p = 0.32). In a
the control plants in the beginning and ending the experiments. Leaf
chamber with high leaf area, the contact between the pollutant and
area was measured by a leaf area meter (ΔT Area meter MK2) (Aydogan
plant increases, so the efficiency increases. Many studies have proven
and Montoya, 2011). The leaves' dry weight was measured by drying
the potential of various plants to remove VOCs from the air (Liu et al.,
them in the oven under 80 ᵒC for 24 h, weighing by an analytical scale
2007; Park et al., 2011; Sangthong et al., 2016; Sriprapat and
and reporting in mg/cm2 of leaf area. Chlorophyll content and car-
Thiravetyan, 2013; Wood et al., 2001). Plants uptake the pollutants
otenoid were determined according to the method of Lichtenthaler and
through their leaves, stomata and cuticles. Once, inside the leaf, pol-
Wellburn (1983). Each analysis was duplicated.
lutant gases diffuse into the spaces between the leaf cells, then they are
absorbed by water films or decomposed through the plant tissues
2.4. Performance evaluation (Noctor et al., 2011; Singh and Tripathi, 2007). Also, phyllosphere
bacteria (bacteria living on the surface of the plants) and endophytic
Phytoremediation performance was evaluated using some para- bacteria (bacteria living in the internal tissue) can detoxify the pollu-
meter such as removal efficiency (RE), empty bed residence time tants via degradation, transformation or sequestration (Weyens et al.,
(EBRT), and elimination capability (EC) which were calculated as 2015). In this study, phyllosphere and endophytic bacteria colonies
follow (Saravanan and Rajamohan, 2009; Hajizadeh et al., 2018): were not assessed; but it can be said that the plants eliminate pollutants

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I. Parseh et al. Atmospheric Pollution Research xxx (xxxx) xxx–xxx

Fig. 3. Influence of the benzene inlet concentration on the RE. Fig. 4. Influence of the benzene inlet concentration on the EC.

a) by phyllosphere and endophytic bacteria or b) by uptake/accumulate tested concentrations are less than the overall elimination capacity of
then degrade/detoxify them. the plants. Teiri et al. (2018) assessed the phytoremediation of for-
maldehyde (as a VOCs) from polluted and found that the EC increased
3.2. Influence of inlet concentration of benzene on the phytoremediation by increasing the inlet formaldehyde concentration. Similar observa-
efficiency tions have been reported for benzene and other VOCs removal by bio-
logical reactors (Abumaizar et al., 1998; Saravanan and Rajamohan,
Fig. 3 illustrates the RE during 36 days of operation (from day 1–18 2009; Hajizadeh et al., 2018).
by Schefflera sp.; from day 19–36 by the Spathiphyllum sp. plant). Ac-
cording to the results, the mean RE at the concentration ranges of 3.3. Influence of the EBRTs on the phytoremediation efficiency
3.5–6.5, 10.5–16.3, and 25–29.5 μg/m3 was 97% ± 1.4, 94% ± 1.5,
and 91% ± 1.8, respectively. These differences were statistically sig- The effects of two different EBRTs (37.5 and 75 min) on the RE of
nificant (p < 0.001). Overall, the RE decreased by increasing the inlet the plants were assessed. In order to reduce the toxic shock of benzene
concentrations. It can't be due to the toxic effect of benzene in this to the plants, EBRT of 90 min was initially applied. As shown in Fig. 5,
concentration ranges because all measured characteristics of the plants the RE increased with increasing EBRT. The mean RE in EBRT of 75 and
including leaf dry weight, chlorophyll and carotenoid contents in- 37.5 min were 94 and 93% respectively (p = 0.2). At low EBRT, it is
creased over time (After exposing to benzene). As shown in Table 2, likely that some benzene molecules leave the chamber without any
there were no significant differences between the morphology and contact with the plants. Therefore the RE decreased by decreasing
physiology characteristic of the plants before and after exposing to EBRT. On the other hands, at high EBRT, the plants have adequate
benzene. This may be due to the fact that benzene at concentration contact time with benzene to adsorb and degrade it. Generally, EBRT is
ranges of 3.6–29.5 mg/m3 had no toxic effect on the plants growth. a major element in the design of biological reactors. The high amount of
There have been no studies done on the toxic effects of benzene on EBRT can increase the contact time with the plants with benzene, re-
Schefflera sp. and Spathiphyllum sp. However, the toxic effect of benzene sulting in increased efficiency. However, high EBRTs will increase space
on living organisms and other plants has been already confirmed and volume requirements, which will increase the investment costs of
(Wilbur et al., 2007). The toxic effect of benzene increases with in- the reactor (Devinny et al., 1998; Prado et al., 2009). Since in this
creasing concentrations. After penetration into the plant, benzene may study, the difference between the RE at EBRTs of 37.5 and 75 s was
travel in the intercellular spaces or the vascular system. As a result, cell negligible, it can be said that the EBRT of 37.5 s is preferable; because it
membranes are damaged, stomata and intercellular space are blocked is more cost-effective than the EBRT of 75 s.
and photosynthesis rates are reduced (Baker, 1970). It has been ob-
served that aromatic compounds at 10% concentration strongly affect 4. Conclusion
plant growth (Cuille and Blanchet, 1958). In the present study, benzene
at the concentration ranges (3.6–29.5 mg/m3) had no toxic effect on the The results showed that Schefflera sp. and Spathiphyllum sp., as or-
plants efficiency. It can be said that a reason for decreasing trend of the namental plants, have a good potential for benzene removal from
RE by increasing the inlet benzene concentrations may be the lack of
sufficient contact of the pollutant molecules with the plants. At high
concentrations, it is likely that some benzene molecules leave the
chamber without any contact with the plants.
Fig. 4 demonstrates the EC of the plants at various inlet con-
centrations. The mean EC in concentration ranges of 3.5–6.5, 16.5 10.5
and 25–30 μg/m3 was 0.4, 1.18, and 2.3 μg/m2 h, respectively. All of
these differences were statistically significant (p < 0.001). In contrast
to RE, EC values increased with increasing concentrations. According to
the results, the relationship between Cin and EC was calculated, as
below:
EC = 0.081 × Cin (4)

When inlet concentration (Cin) increases, the EC increases. This may


be due to contact of more benzene mass with the plants in high Cin than
low Cin. Therefore, at high concentrations, it is likely that more mass of
benzene will be eliminated by the plants. This trend indicates that the Fig. 5. Influence of the EBRTs on the benzene removal efficiency.

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