United States
Environmental Protection
Agency
Environmental Monitoring
and Support Laboratory
P.O. Box 15027
Las Vegas NV 89114
EPA-600/3-79-096
September 1979
Research and Development
&EPA
Benzene Vapor
Depletion in the Presence
of Plants
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RESEARCH REPORTING SERIES
Research reports of the Office of Research and Development, U.S. Environmental
Protection Agency, have been grouped into nine series. These nine broad categories
were established to facilitate further development and application of environmental
technology. Elimination of traditional grouping was consciously planned to foster
technology transfer and maximum interface in related fields. The nine series are:
1. Environmental Health Effects Research
2. Environmental Protection Technology
3. Ecological Research
4. Environmental Monitoring
5. Socioeconomic Environmental Studies
6. Scientific and Technical Assessment Reports (STAR)
7. Interagency Energy—Environment Research and Development
8. "Special" Reports
9. Miscellaneous Reports
This report has been assigned to the ECOLOGICAL RESEARCH series. This series
describes research on the effects of pollution on humans,plant and animal species, and
materials. Problems are assessed for their long-and short-term influences. Investiga-
tions include formations, transport, and pathway studies to determine the fate of
pollutants and their effects. This work provided the technical basis for setting standards
to minimize undesirable changes in living organisms in the aquatic, terrestrial, and
atmospheric environments.
This document is available to the public through the National Technical Information
Service, Springfield, Virginia 22161
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EPA-600/3-79-096
September 1979
BENZENE VAPOR DEPLETION IN THE PRESENCE OF PLANTS
by
Amy J. Cross, James C. McFarlane, and Clyde W. Frank
Monitoring Systems Research and Development Division
Environmental Monitoring and Support Laboratory
Las Vegas, Nevada 89114
ENVIRONMENTAL MONITORING AND SUPPORT LABORATORY
OFFICE OF RESEARCH AND DEVELOPMENT
- U.S. ENVIRONMENTAL PROTECTION AGENCY
LAS VEGAS, NEVADA 89114
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DISCLAIMER
This report has been reviewed by the Environmental Monitoring and Support
Laboratory-Las Vegas, U.S. Environmental Protection Agency, and approved for
publication. Mention of trade names or commercial products does not consti-
tute endorsement or recommendation for use.
Li
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FOREWORD
Protection of the environment requires effective regulatory actions
that are based on sound technical and scientific information. This infor-
mation must include the quantitative description and linking of pollutant
sources, transport mechanisms, interactions, and resulting effects on man
and his environment. Because of the complexities involved, assessment of
specific pollutants in the environment requires a total systems approach
that transcends the media of air, water, and land. The Environmental
Monitoring and Support Laboratory-Las Vegas contributes to the formation
and enhancement of a sound monitoring data base for exposure assessment
through programs designed to:
• develop and optimize systems and strategies for moni-
toring pollutants and their impact on the environment
• demonstrate new monitoring systems and technologies by
applying them to fulfill special monitoring needs of
the Agency's operating programs
This study is designed to determine whether plant systems deplete
atmospheric benzene. Depletion of benzene by Eichhornia crassipes, Beta
vulgaris saccharifera, and Beta vulgaris cicla in soil and water cultures
was observed. This study contributes to the knowledge of biological sinks
as deactivators of carcinogenic materials. Such research aids in the
identification of permissible ambient levels of these compounds.
George,fi. Morgaft'
Director
Environmental Monitoring and Support Laboratory
Las Vegas
iii
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SUMMARY
Three plant species, Eichhornia crassipes in a nutrient hydroponic cul-
ture, Beta vulgaris saccharifera, and Beta vulgaris cicla in soil and in
water cultures, were found to deplete benzene from the air. Following benzene
depletion, plant tissues were extracted and no benzene was detected. This
suggests that benzene was completely utilized within the test system and
that it was degraded to other chemicals.
iv
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INTRODUCTION
Of all the chemicals declared as suspected carcinogens (NIOSH,
Letkiewicz, 1976), benzene is produced in the largest quantities [5 x 109
kilograms (kg) annually (Bertke et al., 1977)]. Among its varied applica-
tions, benzene is used in the manufacture of fuels, industrial solvents,
dyes, polymers, explosives, pesticides, and disinfectants (Gibson, 1968;
Technical Services Division of U.S. EPA, 1976; Fishbein, 1976). It is also
found to occur as a natural product in some raw foods such as avocado
(Jansen and Olson, 1969) other fruits, vegetables, fish, dairy products,
and eggs (Mara and Lee, 1977). It also occurs as a component of cigarette
smoke (Schmeltz and Hoffman, 1976) and is found in canned and irradiated
beef and Jamaican rum (National Cancer Institute, 1977).
Much attention has been given to the sources of environmental contami-
nation by benzene because it is listed in Section 112 of the Clean Air Act.
Several literature reviews and task reports have been undertaken for the
U.S. Environmental Protection Agency in which large volumes of data and
literature were assembled and reviewed (Manning and Johnson, 1977; Mara
and Lee, 1977; Fentiman et al., 1978; and Neher et al., 1977). Benzene
has a high vapor pressure, 100 millimeters (mm) of mercury at 26° C, and
large quantities are lost by volatilization into certain industrial environ-
ments. However, most benzene emissions (81%) are attributed to volatile
losses from gasoline (Bertke et al., 1977).
Despite the large amount of literature describing the production and
release of benzene, little is known about its environmental fate. Available
data indicate that benzene is minimally reactive photochemically. Thus, it
must be assumed that benzene is essentially unchanged chemically in the
atmosphere before reaching receptor sites (Manning and Johnson, 1977) .
Inhalation is the major means of exposure to benzene in animals (Saita,
1973). It has been shown to damage the hematopoietic system resulting in
maladies ranging from anemias to benzene-induced leukemia (Uyeki et al.,
1977; Saita, 1973; Moloney, 1977). The mechanisms involved in these blood
disturbances are unclear, but are likely the result of lymphocyte chromosome
abnormalities (Sawicki, 1977). An unstable metabolite, possibly benzene
oxide, is thought to interact with DNA to initiate this damage (Lutz and
Schlatter, 1977).
Man metabolizes benzene in much the same way as experimental mammals,
primarily involving mixed function oxidases (Marquardt, 1977). In the
mammalian system stable metabolites include phenol, catechol, and muconic
acid (Figure 1) (Gibson, 1971). Certain microorganisms readily oxidize the
benzene ring (Evans, 1963; Gibson, 1971; Marr and Stone, 1961); however,
-------
OH
COOH
COOH
trans, trans
Muconic Acid
3,5-cyclohexadiene
trans 1,2 diol
Mammalian
Pathway
Benzene
H
-OH
' ,
-OH
H
3,5-Cyclohexadiene-
1,2-diol
H
^ O
H
Dioxetane
OH
OH
H
Catechol
3,5-cyclohexadiene
cis 1 ,2 diol
Microbial
Pathway
Benzene Metabolism in Mammals and Soil Microbes,
Adapted from Gibson, 1971; Marrand Stone, 1961.
Figure 1. Benzene metabolism in mammals and soil microbes, adapted from
Gibson, 1971; Marr and Stone, 1961.
-------
these pathways are different from those in mammals (Figure 1) (Gibson, 1971;
Marr and Stone, 1961). For instance, phenol is not an important intermediate
and dioxetane is proposed as an intermediate metabolite (Gibson, 1971).
Pseudomonas aeruginosa and Mycobacterium rhodochrous degrade benzene via 3,5
cyclohexadiene-1,2 diol and catechol to carbon dioxide and water (Marr and
Stone, 1961). Another soil microbe, Pseudomonas putida, degrades benzene by
way of the cis isomer of 3,5 cyclohexadiene-1,2 diol and catechol (Gibson,
1971). Marr and Stone (1961) found that microbes capable of oxidizing ben-
zene were rendered incapable of this oxidation when the benzene was removed.
The inducibility of substrate-specific oxidizing microbes led Rao and Bhat
(1971) to suggest the incorporation of such microbes for the purpose of remov-
ing benzene, and thus detoxifying, waste waters. An alternate use would be
as a biological indicator of aromatic hydrocarbons, or specifically to evalu-
ate the benzene burden of a polluted area (Caparello and LaRock, 1975).
Comparatively little research on benzene degradation in plants is avail-
able. Some reports indicate that plants can metabolize aromatic rings such
as benzene, phenol, toluene, and catechol (Prasad and Ellis, 1978; Jansen
and Olson, 1969). The products of benzene metabolism in plants are reported
to be phenol, muconic acid, and carbon dioxide (Durmishidze et al., 1974;
Jansen and Olson, 1969), suggesting a pathway similar to that in mammals.
Unlike microorganisms, there have been no reports of plants being inducible
to benzene metabolism.
Complete knowledge of the fate of benzene in the environment is important
due to its abundance and carcinogenicity. This study was undertaken to expand
this knowledge by observing benzene depletion rates in plant systems. In addi-
tion, an attempt was made to identify the interactions of benzene with plants.
MATERIALS AND METHODS
Three plant species, Eichhornia crassipes (water hyacinth), Beta vulgaris
cicla (Swiss chard), and Beta vulgaris saccharifera (sugar beet) were studied
in this series of experiments. They were chosen for the convenience afforded
by leaf size and ease of propagation. In addition, water hyacinth has been
found to metabolize phenol (Wolverton and McKown, 1976). Water hyacinth
plants were asexually propagated in Hoaglund nutrient solution in a glass
house. The hyacinths were transplanted to 400 ml of distilled water in the
test vessels (Figure 2) and allowed to grow 10 days prior to study. Three
to 5-week-old Beta plants grown in peat/vermiculite (Jiffy Mix) were rinsed
of all rooting material possible, without damaging the roots, and were placed
in 5 or 10 milliliters (ml) of distilled water in the necks of the smaller
test vessels (Figure 2), and allowed to grow for at least 3 days before
experimentation.
Test vessels for exposing plants to benzene consisted of 0.65-liter
(Beta spp.) or 2.4-liter (Eichhornia) borosilicate glass bottles with short,
2.5-centimeter (cm) diameter, necks. Openings had a Teflon (TFE) lip seal
with a Teflon lined screw-type lid. Each container had a 1-mm diameter
hole in the side and/or top for injecting treatment material and air sampling.
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Injection Hole
2.4 Liter Volume
Water, Root System
-Injection Holes
0.65 Liter Volume
Water, Root System
Figure 2. Microcosms for exposure of Swiss chard, sugar beets, and water
hyacinths.
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These holes were sealed with cellulose acetate tape when not in use. Carbon
dioxide (C02) was added daily to the test vessels to allow photosynthesis.
The desired benzene concentration was achieved by an injection of liquid
benzene with subsequent volatilization within the vessel. The starting con-
centration was verified by gas chromatographic (GC) analysis. Experimental
controls were prepared by injecting benzene into bottles containing the same
volume of water as the test vessels, but with no plants. Benzene loss was
negligible (Appendix 1). A standard benzene concentration was established
by injecting a similar amount of benzene into an empty bottle. Benzene con-
centration was determined by comparing GC signal peak heights of samples to
those of the standards. Depletion rates were determined by performing a
linear regression analysis on the resulting concentrations. Upon dropping
to a zero concentration, the vessels were re-injected with the original
amount of benzene.
After experiments were complete, the plants were extracted by grinding
them in 50% acetonitrile and 50% distilled water with a ceramic mortar and
pestle. This mixture was vacuum-filtered before being extracted with an
equal volume (5 ml/g tissue) of petroleum ether. Some extracts were con-
centrated by evaporation before analysis.
Gas chromatographic analyses were performed on a model 222 Tracer gas
chromatograph with a flame-ionization detector. A 1.8-meter x 2-mm (inside
diameter) glass column was used. For separation of benzene from ether, 10%
Pennwalt-223 plus 4% potassium hydroxide on 80/100 mesh Gas-Chrom packing
was used in the column. Benzene in air samples was separated using a column
packing of 25% diethylene glycol succinate on 60/80 mesh WAW-DMCS Chromosorb.
The carrier gas was helium at a flow rate of 60 ml/minute at the detector.
Detector and injection port temperatures were 265° C and the column tempera-
ture was 150° C.
During these experiments, it became evident that a time lag occurred
between the initial benzene exposure and the maximum benzene depletion rate.
To test the importance of benzene concentration on the depletion rate, plants
were exposed to various benzene concentrations for a predetermined time using
a flow-through exposure system. Four stainless steel cylinders were evacuated
and enough liquid benzene was drawn into them to yield 0, 0.18, 0.27, and
0.61 milligrams per liter (mg/liter) of benzene. Carbon dioxide was added
in the same way to make final concentration of 300 parts per million (ppm).
Finally the cylinders were pressurized to 400 pounds per square inch with
C02~free compressed air. These exposure gases were attached through pres-
sure regulators and a manifold of needle valves and the flow rates were ad-
justed to 10 ml/minute through each test vessel.
Three test vessels were fumigated with each of the different benzene
concentrations for 3 days. The sources were then disconnected and the
benzene depletion rates of each were determined as previously outlined.
A third study was undertaken to determine the depletion rate of benzene
on a larger scale with mature sugar beets. Six-month-old sugar beet plants
grown in 30-cm pots filled with Jiffy Mix were placed in a 2.26-m^ sealed
growth chamber. The C02 concentration was maintained at 300 ppm and benzene
-------
was added daily to reestablish a concentration of 0.6 mg/liter. The benzene
concentration in this chamber was monitored by GC and the depletion rate
calculated from the slope as in the other studies.
Leaf weight and areas were used to confirm uniformity of test plants and
to determine relationships between plant size and depletion rates. Plants
were weighed after blotting,the roots on absorbent paper towels. Leaf area
was obtained with a Li-Cor 0*'portable leaf area meter. Dry weights were
determined after oven-drying the plants for 24 hours at 80° C.
RESULTS AND DISCUSSION
Benzene vapor concentration decreased in the presence of water hyacinth,
sugar beet, and Swiss chard (Figures 3, 4, and 5). This depletion appears
to be a linear phenomenon even when approaching zero concentration. Linearity
suggests that benzene depletion was not limited by gaseous diffusion but by
a rate-limiting reaction site or chemically reactive substrate. Linear re-
gression was used to calculate the slopes and these values are used to de-
scribe the benzene uptake rates.
Data from the initial experiments show typical changes in benzene deple-
tion rates for a series of plants observed at intervals during repeated ben-
zene fumigations (Figure 6). The rate of benzene depletion was determined
repeatedly for up to 25 exposures with some plants. Succeeding rate determi-
nations on the same plant did not always yield the same result. Differences
also occurred between replicates and large differences were evident between
species. For the two Beta species there was a time lag before the rate of
benzene depletion increased. Maximum depletion rates were reached at 16 days
of exposure. The lag period was shorter in the Eichhornia tests. Benzene
depletion was slow the first day but increased rapidly the second and third
days followed by a decline. Experimentation to date has not allowed a con-
clusive explanation for the time lag or for the subsequent decreased absorp-
tion. However, factors suspected in causing this characteristic depletion
pattern include: 1) the deterioration of the epicuticular wax and cuticle
by benzene exposure; 2) the induction of an enzyme system responsible for
the degradation or metabolism of benzene; 3) establishment of a substantial
microbial population which utilizes benzene; 4) and changes in the vigor of
the plants. Current research is directed toward the identification of the
responsible mechanism.
The decreasing rate of benzene depletion coincided with the appearance
of leaf damage. The conditions of the microcosm were not ideal for plant
growth. Maintenance of C02 concentration on only a daily basis, lack of
nutrients, no air turbulence, and high humidity all precluded normal plant
growth. Therefore, the decrease in benzene depletion rates was assumed to
be related to plant deterioration, each species having a different tolerance
to these conditions.
Analysis of petroleum ether extracts of benzene-exposed sugar beet and
water hyacinth plants yielded no benzene in the plants. This indicates that
-------
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Days
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Figure 6. Benzene depletion rates of plant systems during repeated
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benzene was converted to another compound, and not solubilized from the atmo-
sphere by a plant component. This finding parallels the interpretation of the
linear uptake which we suggest indicates chemical or a site-limiting reaction.
The study designed to evaluate the effect of different benzene concentra-
tions on depletion rates indicated a relationship between exposure concentra-
tion during the lag phase and the benzene absorption rate. Although there
was considerable variation in the depletion rates between replicates, the test
vessels exposed to the higher concentrations had faster depletion rates
(Figure 7). The cause of this is unknown, but could be explained by the
induction of an enzyme system, or ingrowth of a microorganism population
that is capable of metabolizing benzene.
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by sugar beet plants.
11
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These studies demonstrate that plant systems may play a major role in
the removal of benzene from the environment. In all studies benzene deple-
tion began after a time lag, the length of which varied with species. The
absorption rate appears to be related to the concentration of the benzene
exposure during the lag phase. Extracts of microcosm components yield no
benzene, suggesting biotransformation of the compound. The component of the
plant system which is responsible for the absorption and biotransformation
of benzene from the atmosphere has yet to be determined, but clearly a sink
exists. The possibility of the absorption of benzene by microorganisms on
and in the plants and soil cannot be overlooked.
REFERENCES
1. Bertke, Thomas J., Terrence Briggs, Leslie Ungars, and David Augenstein,
1977. Atmospheric benzene emissions. PEDCO Environmental Inc.,
Cincinnati, Ohio, EPA 450/3-77-029.
2. Caparello, D. M., and P. A. LaRock, 1975. A radioisotope assay for
quantification of hydrocarbon biodegradation potential in environmental
samples. Microbial Ecology 2:28-42.
3. Durmishidze, S. V., D. Sh. Ugrekhelidze, and A. N. Dzhikiya, 1974.
Assimilation and transformation of benzene by higher plants. Fiziol.
Biokhim. Kul'+Rast 6(3):271-275.
4. Evans, W. C. , 1963. Microbiological degradation of aromatic compounds.
J. of Gen. Micro. 32:177-184.
5. Fentiman, A. F. Jr., R. W. Coutant, G. A. Jungclaus, and C. W. Townley,
1978. Sampling and analysis of benzene in Columbus, Ohio. Battelle:
Columbus, Ohio, Contract No. 68-01-3858.
6. Fishbein, L., 1976. Potential hazards of fumigant residues. Environ.
Health Perspective^ 14:39-45.
7- Gibson, David T., 1968. Microbial degradation of aromatic compounds.
Science 161(3846):1093-1097.
8. Gibson, David T., 1971. The microbial oxidation of aromatic hydrocar-
bons. Chemical Rubber Company Critical Reviews in Microbiology 1:199-
223.
9. Jansen, E. F., and Alfred C. Olson, 1969. Metabolism of carbon-14-
labeled benzene and toluene in avocado fruit. Plant Physiol. 44:786-
787.
10. Letkiewicz, Frank J., 1976. An ordering of the NIOSH suspected carcin-
ogens list. EPA-560/1-76-003, 432 pp.
12
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11. Lutz, W. K., and C. H. Schlatter, 1977. Mechanism of the carcinogenic
action of benzene: Irreversible binding to rat liver DNA. Chemical
Biological Interactions 18:241-245
12. Manning, Justice A., and Richard Johnson, 1977. Atmospheric benzene
emissions. PEDCO Environmental Inc.: Cincinnati, Ohio, Contract No.
68-02-2515.
13. Mara, Susan J., and Shonh S. Lee, 1977. Human exposures to atmospheric
benzene. Stanford Research Institute: Menlo Park, Calif., Contract
No. 68-01-4314.
14. Marquardt, H., 1977- Microsomal metabolism of chemical carcinogens in
animals and man. In: Mohr, U., D. Schmahl, L. Tomatis, eds. Air
Pollution and Cancer in Man. WHO Agency for Research on Cancer, Lyon,
331 PP.
15. Moloney, William C., 1977. Natural history of chronic granulocytic
leukemia. Clinic in Haematology 6_(l):41-53.
16. Marr, Eleanor K., and Robert W. Stone, 1961. Bacterial oxidation of
benzene. J. Bacteriol. 81:425-430.
17. National Cancer Institute, 1977. On occurrence, metabolism, and toxic-
ity including reported carcinogenicity of benzene. Summary report.
Washington, DC.
18. Neher, M. B., G. W. Kinzer, P. R. Sticksel, N. A. Klosterman, and
J. McNulty, 1977- Sampling and analysis for selected toxic substances.
Task Order 1 - sampling and analysis for benzene. Battelle, Columbus,
Ohio, Contract No. 68-01-3420.
19. Prasad, S., and E. E. Ellis, 1978. In vivo characterization of cate-
chol ring cleavage in cell cultures of Glycine max. Phytochemistry 17:
187-190.
20. Rao, B. V., and J. V. Bhat, 1971. Characteristics of yeasts isolated
from phenol- and catechol-adapted sludges. Antonie van Leeuwenhook 37:
303-312.
21. Saita, G., 1973. Benzene-induced hypoplastic anaemias and leukemias.
Blood Disorders Drugs Other Agents:127-146.
22. Sawicki, E., 1977. Chemical composition and potential 'genotoxic1
aspects of polluted atmospheres. In: Mohr, U., D. Schmall, L.
Tomatis, eds., Air Pollution and Cancer in Man. WHO Agency for
Research on Cancer, Lyon, 331 pp.
23. Schemeltz, I., and D. Hoffman, 1976. Formation of polynuclear aromatic
hydrocarbons from combustion of organic matter. Carcinogenesis 2
13
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Comprehensive Survey I., R. Freudenthal, P- Jones eds. Raven Press:
New York, pp. 225-239.
24. Technical Services Division, 1976. Pesticide product information mi-
crofiche: User's guide, 2nd edition: Office of Pesticide Programs,
U.S. Environmental Protection Agency. EPA-540/09-77-010.
25. Uyeki, Edwin M., Ahmed El Ashkar, Don W. Shoeman, and Teresa U. Bisel,
1977. Acute toxicity of benzene inhalation to hemopoietic precursor
cells. Toxicol. Appl. Pharmacol. 40:49-57.
26. Wolverton, B. C., and Mary M. McKown, 1976. Water hyacinths for re-
moval of phenols from polluted waters. Aquatic Botany 2:191-201.
14
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APPENDIX A. Static benzene concentration reached in test vessel containing
water only.
15
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TECHNICAL REPORT DATA
(Please read Instructions on the reverse before completing)
. REPORT NO.
EPA-600/3-79-096
2.
3. RECIPIENT'S ACCESSION NO.
. TITLE AND SUBTITLE
BENZENE VAPOR DEPLETION IN THE PRESENCE OF PLANTS
5. REPORT DATE
September 1979
6. PERFORMING ORGANIZATION CODE
. AUTHOR(S)
Amy J. Cross, James C. McFarlane, and Clyde W. Frank
8. PERFORMING ORGANIZATION REPORT NO.
9. PERFORMING ORGANIZATION NAME AND ADDRESS
Environmental Monitoring and Support Laboratory
Office of Research and Development
U.S. Environmental Protection Agency
Las Vegas, Nevada 89114
10. PROGRAM ELEMENT NO.
1HE775
11. CONTRACT/GRANT NO.
12. SPONSORING AGENCY NAME AND ADDRESS
U.S. Environmental Protection Agency—Las Vegas, NV
Office of Research and Development
Environmental Monitoring and Support Laboratory
Las Vegas, Nevada 89114
13. TYPE OF REPORT AND PERIOD COVERED
Final
14. SPONSORING AGENCY CODE
EPA/600/07
15. SUPPLEMENTARY NOTES
16. ABSTRACT
Three plant species, Eichhornia crassipes in a nutrient hydroponic culture Beta
vulgaris saccharifera, and Beta vulgaris cicla in soil and in water cultures,
were found to deplete benzene from the air. Following benzene depletion, plant
tissues were extracted and no benzene was detected. This suggests that benzene
was completely utilized within the test system and that it was degraded to other
chemicals.
17.
KEY WORDS AND DOCUMENT ANALYSIS
DESCRIPTORS
b.lDENTIFIERS/OPEN ENDED TERMS C. COS AT I Field/Group
Environmental biology
Organic chemistry
Benzene
Air pollution
Eichhornia crassipes
Beta vulgaris saccharife
saccharifera
Beta vulgaris cicla
57H
99A,D
71Q
44G
68A
18. DISTRIBUTION STATEMENT
RELEASE TO PUBLIC
19. SECURITY CLASS (ThisReport)
UNCLASSIFIED
21. NO. OF PAGES
16
20.
llf (T
C J-J-iJL/
22. PRICE
EPA Form 2220-1 (Rev. 4-77) PREVIOUS EDITION is OBSOLETE
US. GOVERNMENT PRINTING OFFICE 197ft 683O91 /22O3
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