Tampa BSides - Chef's Tour of Microsoft Security Adoption Framework (SAF)
1568
1. Photodegradation of the Endocrine-Disrupting Chemical 4-Nonylphenol
in Biosolids Applied to Soil
Kang Xia* and Chang Yoon Jeong
Abstract plication of biosolids. 4-Nonylphenol has been fre-
quently detected in a wide range of environmental sam-
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.
There is increasing concern about the environmental fate and im-
pact of biosolids-associated anthropogenic organic chemicals, among ´
ples (Shang et al., 1999; Dachs et al., 1999; Sole et al.,
which 4-nonylphenol (4-NP) is one of the most studied chemicals. 2000; Kolpin et al., 2002; Ferguson et al., 2003). Signifi-
This is primarily because 4-NP is an endocrine disruptor and has cant levels (50–200 g kg 1) of 4-NP have been found
been frequently detected in environmental samples. Due to its high in sediments of rivers that receive surface runoff from
hydrophobicity, 4-NP has high affinity for biosolids. Land application ´
biosolids-amended land (Sole et al., 2000). Marcomini
of 4-NP–containing biosolids could potentially introduce large quanti-
et al. (1989) observed an 80% reduction of 4-NP in the
ties of this chemical into the environment. A laboratory experiment
top 5 cm of soil 30 d after biosolids were spread on the
was conducted to investigate the effect of artificial sunlight on 4-NP
degradation in biosolids applied to soil. When exposed to artificial
soil surface (13.5 dry Mg ha 1 yr 1). The remaining 4-NP
sunlight for 30 d, the top-5-mm layer of biosolids showed a 55% in the soil stayed at a fairly constant level (100 g kg 1)
reduction of 4-NP, while less than 15% of the 4-NP was degraded even 320 d after the application. The levels of 4-NP in
when the biosolids were kept in the dark. Our results indicate that deeper soil profiles were not investigated in the study
sensitized photolysis reaction plays an important role in reducing the by Marcomini et al. (1989). Vikelsøe et al. (2002) investi-
levels of 4-NP in land-applied biosolids. Surface application rather gated 4-NP levels along soil profiles to a depth of 60 cm
than soil incorporation of biosolids could be effective in reducing in a Danish field receiving biosolids application (17 dry
biosolids-associated organic chemicals that can be degraded through Mg ha 1 yr 1) for 25 yr. Even six years after ceasing
photolysis reactions. However, the risks of animal ingestion, foliar biosolids application in this field, they found significant
deposition, and runoff should also be evaluated when biosolids are
concentrations of 4-NP, ranging from 500 to 5000 g
applied on the soil surface.
kg 1, along the soil profiles. Those levels exceeded the
current recommended Danish soil quality criteria of 10
g kg 1 for 4-NP (Jensen et al., 1997). Different from
T he endocrine disruptor 4-NP is one of the major
anaerobic degradation metabolites of nonylphenol
polyethoxylates (NPnEOs), nonionic surfactants that
the study by Marcomini et al. (1989) in which biosolids
were surface-applied, biosolids were incorporated into
soil through conventional cultivation during the applica-
are widely used as industrial detergents, emulsifiers, tion in the field investigated by Vikelsøe et al. (2002).
wetting agents, and dispersing agents (Maguire, 1999; The plow depth was not noted in the study by Vikelsøe
Thiele et al., 1997). Detailed molecular structures for et al. (2002). None of the above-cited studies attempted
4-NP and NPnEOs can be found in a review article by to explore the mechanisms for the transformation of
Maguire (1999). Due to its high hydrophobicity (log 4-NP in soil systems. We hypothesize that biosolids ap-
KOW approximately 4.48, log KOC approximately plication methods may have a significant impact on the
3.97) (Ahel and Giger, 1993; Rolf-Alexander et al., fate of 4-NP in soil.
2002), large quantities of 4-NP are found in biosolids, Surface application and soil incorporation are fre-
which consist of high levels of organic matter. The levels quently used for biosolids disposal in the United States
of 4-NP in biosolids were found to be from a few mg (USEPA, 1999). Compared with soil incorporation, bio-
kg 1 up to several thousand mg kg 1 (Maguire, 1999; solids are exposed to more sunlight and oxygen when
Guardia et al., 2001; Keller et al., 2003; Xia and Pillar, they are surface-applied. Research (Faust and Holgne, ´
2003). Land application of biosolids is one of the most 1987; Pelizzetti et al., 1989; Ahel et al., 1994) has shown
common ways of biosolids disposal and is expected to that under aerobic conditions 4-NP in natural water
increase as other disposal options become more expen- degrades rapidly mainly due to sensitized photolysis
sive or heavily regulated (USEPA, 1999). Given that by dissolved organic matter, while direct photolysis is
the annual production of biosolids in the United States comparatively slow. Sensitized (indirect) photolysis is a
is projected to increase sharply to about 47 million Mg transformation of a given xenobiotic compound initi-
(50% of which will be land-disposed) within the next ated through light absorption by other chemicals present
decade (USEPA, 1999), several thousand Mg of 4-NP in the system. Direct photolysis is a process in which a
could be released to the environment through land ap- given compound undergoes transformation due to its
absorption of light (Schwarzenbach et al., 1993). It is
K. Xia, Department of Crop and Soil Sciences, 3111 Plant Sciences believed that dissolved organic matter–derived organic
Building, University of Georgia, Athens, GA 30602. C.Y. Jeong, De-
partment of Renewable Resources, University of Louisiana, P.O. Box peroxy radicals (ROO·) formed in natural water under
44650, Lafayette, LA 70504. Received 9 Sept. 2003. *Corresponding sunlight can react with 4-NP (Faust and Holgne, 1987;´
author (kxia@uga.edu). Schwarzenbach et al., 1993), a sensitized photolysis reac-
Published in J. Environ. Qual. 33:1568–1574 (2004).
ASA, CSSA, SSSA Abbreviations: HPLC, high performance liquid chromatography;
677 S. Segoe Rd., Madison, WI 53711 USA 4-NP, 4-nonylphenol; NPnEO, nonylphenol polyethoxylate.
1568
2. XIA & JEONG: PHOTODEGRADATION OF ENDOCRINE DISRUPTOR IN SOIL 1569
tion. The half-life of 4-NP in the surface layer of natural num foil, were run simultaneously. One-millimeter headspace
waters was estimated in the range of 0.6 to 29 d (Faust was kept in each cell and air was pumped at a constant rate
´
and Holgne, 1987; Ahel et al., 1994). Research by Peliz- through the headspace to maintain aerobic conditions. The
zetti et al. (1989) demonstrated a complete photocata- outgoing air from each cell was bubbled through a small bottle
containing 10 mL hexane to trap volatilized 4-NP. Every day,
lytic degradation of 4-NP within an hour after it was the hexane in each bottle was collected for analysis of 4-NP.
exposed to UV light (wavelength 340 nm) and TiO2 in Ten milliliters of fresh hexane was immediately added into
water. Although research has shown photodegradation each bottle after the collection. Each collected hexane solution
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.
of 4-NP in aqueous systems, no information has been was evaporated to dryness under N2, redissolved in 0.5 mL
found on how sunlight affects the degradation of 4-NP methanol, then analyzed for 4-NP using high performance
in biosolids that are applied to soil. Photodegradation liquid chromatography (HPLC). The water contents (10%
may contribute to the fast reduction of 4-NP observed weight base) of the samples were monitored by weighing each
by Marcomini et al. (1989) in soils receiving biosolids cell unit daily and kept at their original levels by adding water
through surface application. The objective of the present when needed. For comparison, photodegradation of 4-NP in
study was to use laboratory-constructed soil profiles to a 10-mL solution containing 6.6 mg L 1 4-NP and 5 mg L 1
fulvic acid (International Humic Substances Society Standard
investigate the potential of 4-NP photodegradation in
IS103F) was also investigated under similar experimental con-
biosolids spread on the soil surface, incorporated with ditions as that for biosolids. The carbon concentration in the
soil, and applied below the soil surface. fulvic acid solution was similar to that in typical surface water
´
(Faust and Holgne, 1987). All experiments were run in trip-
Materials and Methods licate.
Biosolids, Compost, and Soil Samples Sample Extraction and Cleanup
Freshly produced biosolids and compost of biosolids were Before extraction for 4-NP and NPnEOs, solid samples
collected from a wastewater treatment plant located in north- taken from each layer of the cell units were freeze-dried and
eastern Kansas. This treatment plant, operated using activated ground to a fine powder. Loss of 4-NP from the samples
sludge systems, serves a city with 150 000 people. It also re- did not occur during freeze-drying and grinding. Freeze-dried
ceives wastewater from several medium-scale industries. The samples (2–5 g) were extracted with hexane and acetone (1:1,
wastewater treatment capacity of the plant is approximately volume ratio) on an accelerated solvent extraction system
4.5 104 m3 d 1 (12 million gallon d 1). The activated sludge (Model 200ASE; Dionex, Sunnyvale, CA) using a single static
is partially dewatered on a belt filter press, producing approxi- cycle (20 min, 100 C, 10 342 kPa [1500 psi]). Water samples
mately 10 000 kg wet biosolids per day. The biosolids produced were extracted for 4-NP with 10 mL hexane using a liquid–
are immediately transferred to lagoons and composted for up liquid extraction method. Extracts of solid samples and water
to two months before they are applied on land. The average samples were then evaporated to dryness under N2 (50 C),
water contents in the biosolids and compost are 85 and 23%, redissolved in 1 mL methanol, and stored at 10 C until analy-
respectively. The biosolids were collected on three different sis. For both solid samples and water samples, 4-tert-butylphe-
days and then composited. Compost samples were collected nol, sublimed (Sigma Chemical, St. Louis, MO) and 2,4,6-
from different compost lagoons and then composited. Biosolids tribromophenol (Sigma Chemical) were used as surrogate
and compost samples were kept frozen until the conduction standard and internal standard, respectively, for quality con-
of 4-NP photodegradation experiments. Soil used for this study trol purposes.
was a Kennebec silt loam (fine-silty, mixed, mesic Cumulic
Hapludolls), an agricultural soil collected from Manhattan, Analysis of 4-Nonylphenol and Nonylphenol Polyethoxylates
KS. The organic matter content of the soil is 2.8%. The soil by High Performance Liquid Chromatography and Gas
consists of (weight percent) montmorillonite (37%), kaolinite Chromatography–Mass Spectrometry
(8%), mica (27%), and montmorillonite-mica (27%).
The concentrations of 4-nonylphenol and NPnEOs were
analyzed, respectively, via reverse phase and normal phase
Experimental Setup
HPLC with a diode array detector (DAD) and a fluorescence
Appropriate amounts of biosolids, compost, or biosolids detector (FLD). The presence of 4-NP and NPnEOs (n
and soil mix (1:1 weight ratio, equivalent to application of 1–4) in each sample was confirmed using gas chromatography
biosolids at a rate of approximately 120 dry Mg ha 1 to the with mass spectrometry detector (GC–MS). Technical-grade
top 1 cm of soil) were distributed homogeneously in the cell 4-NP purchased from Sigma Chemical, pure NP1EO and
shown in Fig. 1. Two types of cells (6- and 11-mm-thick) NP2EO purchased from Ehrenstorfer Labs (Augsburg, Ger-
were constructed. One cell could hold a sample with a 5-mm many), and Surfonic N-95 donated by Mr. Carter Naylor
thickness and the other could hold a sample with a 10-mm (Huntsman Corp., Austin, TX) were used as standards. The
thickness. The cell loaded with a 5-mm-thick sample was Surfonic N-95, with an average of 9.5 ethoxy units, consists
placed on top of a cell, which was loaded with a 10-mm-thick of a mixture of NPnEOs with n 2 to 16 (Keller et al., 2003).
sample to form a cell unit. The two cells were pressed together A Hewlett-Packard (Palo Alto, CA) 1050 HPLC equipped
by fold-back clips placed along the border of the cells. Each with a DAD and a FLD was used for sample analysis. Injec-
cell unit was irradiated with the cell containing a 5-mm-thick tions (5 L) were passed through a 25- L sample loop. The
sample facing the light for 0.5 h, 12 h, 4 d, 10 d, 20 d, and analytical column was kept at 40 C. The DAD was operated
30 d at 25 C in a temperature-controlled growth chamber under the following conditions: signal 277 nm, bandwidth
fitted with lamps simulating the September sunlight radiation 40 nm, and reference 350 nm. Data were collected from
(approximately 2 kWh m 2 d 1) as measured in Manhattan, the FLD at excitation 230 nm, emission 301 nm, and
KS. A sheet of aluminum foil was attached beneath each cell pmtgain 6. A 124- 4-mm LiChrospher 100-RP-18e column
unit to avoid irradiation through the bottom plate by scattering with a particle size of 5 m (Agilent Technologies, Santa
light. Dark controls, cell units completely wrapped with alumi- Clarita, CA) was used for the reverse-phase HPLC. A metha-
3. 1570 J. ENVIRON. QUAL., VOL. 33, JULY–AUGUST 2004
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.
Fig. 1. Schematic diagram for the cell used in the photodegradation study (modified from Balmer et al., 2000). Pyrex glass is adequate for our
experiment in which near-soil-surface sunlight (terrestrial light) (wavelength 290 nm; Schwarzenbach et al., 1993) is of interest. Pyrex glass
does not completely block UV light between 290 and 325 nm. It is more transparent to UV light with wavelength 325 nm than quartz.
nol and water mixture (8:2) was used as the mobile phase at a light exposure and seemed to continue to drop with
flow rate of 1.5 mL min 1. Normal phase HPLC used a 4.6- time. Contrary to what was observed for the top-5-mm
100-mm Hypersil APS column (Agilent Technologies) with a layer, the 4-NP concentrations in the bottom-10-mm
particle size of 5 m. A flow rate of 1.5 mL min 1 was used layer biosolids in the cell units that were exposed to
for the mobile phase (hexane to water to isopropanol ratio
78:2:20, 50:3:47, and 0:3:97 at 0–3, 3–22, and 22–23 min, respec-
tively).
A Hewlett-Packard 6890 Series GC–MS was used to con-
firm the presence of 4-NP and NPnEOs (n 1–4) in the
biosolids and water extracts. The GC–MS used a Model 5972
quadrupole mass selective detector and was operated in the
electron impact mode using helium as the carrier gas (88.9
kPa [12.9 psi]; 1.1 mL min 1). A 30-m 0.25-mm 0.25- m
HP-5MS column was used under the following conditions
(Marcomini et al., 1989; De Voogt et al., 1997). The initial
column temperature was held at 100 C for 0.5 min and then
increased to 320 C at a rate of 10 C min 1. The temperature
was finally maintained at 320 C for 5 min. Injections (1 L)
were in the splitless mode with the injector temperature at
200 C and interface line temperature at 250 C. Published spec-
tra (Stephanou and Ginger, 1982), 4-NP, NP1EO, and NP2EO
standards, and commercial surfactant mixtures were used in
the confirmation of 4-NP and NPnEOs (n 1–4) in the ex-
tractants.
Results and Discussion
The initial concentrations of 4-NP in the biosolids,
compost, and biosolids and soil (1:1) mixture used for
this experiment were 937, 125, and 430 mg kg 1, respec-
tively. Our results suggest that volatilization due to con-
tinuous air flow through each cell during the entire
experimental period was insignificant. Figure 2 shows
that when the cell units were kept in the dark for 30 d
the levels of 4-NP decreased slowly, only about 10 to
15% of the initial concentrations, in the surface- and
bottom-layer biosolids (top 5 mm and bottom 10 mm,
respectively). A rapid decrease was observed for 4-NP Fig. 2. Concentrations of 4-nonylphenol (4-NP) in biosolids in top-
5-mm and bottom-10-mm layers exposed (solid circle) and unex-
in the top-5-mm layer of biosolids when the cell units posed (solid triangle) to artificial sunlight. The term C/Ci is the
were exposed to artificial sunlight. The 4-NP concentra- concentration ratio of 4-NP at each sampling point to its initial con-
tion in this layer dropped about 55% within 30 d of centration.
4. XIA & JEONG: PHOTODEGRADATION OF ENDOCRINE DISRUPTOR IN SOIL 1571
light decreased at the same slow rate as that in the tion, 4-NP may be sorbed tightly onto the organic matter
biosolids that were not exposed to artificial sunlight in biosolids and, therefore, is less available for micro-
(Fig. 2). Similar results were observed for 4-NP in the organisms. Our study has shown a Kd value of approxi-
compost (Fig. 3). Figure 4 shows that artificial sunlight mately 2000 mL g 1 for 4-NP on the biosolids used in
had no effect on the degradation of the parent com- this study. Our observed degradation rates of 4-NP in
pounds (NPnEOs) of 4-NP in the top-5-mm layer of samples that were not exposed to artificial sunlight were
biosolids and, therefore, no new 4-NP was formed in much slower than what have been presented in several
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.
our samples during the experimental period. Our results recent studies in which soil samples, soil and uncontami-
are in agreement with the findings from the study con- nated biosolids mixture samples, or marine sediment
ducted by Ahel et al. (1994), in which significant photol- samples were spiked with 4-NP (Topp and Starratt,
ysis reactions were not detected for NPnEOs. The insig- 2000; Hesselsøe et al., 2001; Gejlsbjerg et al., 2001; Ying
nificant photodegradation of NPnEOs may be due to and Kookana, 2003). The 4-NP reductions varying from
their lack of reactivity with dissolved organic matter– 30 to 95% of original levels within the 30-d period were
derived organic peroxy radicals (ROO·) (Ahel et al., observed in these studies. It has been well-documented
1994). that faster degradation rate is in general observed for
Previous studies have indicated that certain micro- an organic chemical when it is freshly added to a soil
organisms could degrade 4-NP in pure culture when 4-NP matrix than when it is sequestered in a soil due to pro-
was the only carbon and energy source (Tanghe et al., longed chemical–soil contact time (aging) (Hatzinger
1999; Fujii et al., 2000; Vallini et al., 2001). The half- and Alexander, 1995; Kelsey et al., 1997; Alexander,
life of 4-NP in these microbial culture varied from 4 to 2000). During the wastewater treatment processes, 4-NP
7 d. However, in biosolids the role of microorganisms molecules may have moved into sites within the biosolids
may not be as significant as in pure culture because of matrix (an “aging” process) that are not readily accessed
the large quantities of other available carbon sources by microorganisms, resulting in the slower microbial
for microorganisms in biosolids. No information has degradation observed in our study compared with that
been found on whether 4-NP can be cometabolized with observed in the above-cited experiments, which used
the presence of other available carbon sources. In addi- freshly spiked samples.
Our results suggest that sunlight plays an important
role in degrading 4-NP in biosolids. The 4-NP degrada-
tion rate in the top-5-mm layer of biosolids exposed to
artificial sunlight was almost five times as fast as that
in the samples without light exposure. It has been shown
that photolysis depth in soils is only limited to a depth
up to 2 mm (Hebert and Miller, 1990) and, therefore,
artificial light had almost no impact on 4-NP in the
bottom-10-mm layer biosolids. When the biosolids were
incorporated with soil by mixing with soil at 1:1 weight
ratio, 30% of 4-NP was degraded in the top-5-mm layer
within 30 d of light exposure (Fig. 5), a rate slower than
that for the biosolids-only samples (Fig. 2). This may
have been due to the fact that soil particles blocked some
of the light from reaching biosolids particles, resulting in
less photolysis reaction for 4-NP in biosolids. Previous
research has shown sensitized photolysis of 4-NP by
dissolved organic matter in natural waters (Faust and
´
Holgne, 1987; Ahel et al., 1994). Our results shown in
Fig. 6 further prove this reaction. A complete reduction
of 4-NP was achieved within 6 d (144 h) in a solution
containing 5 mg L 1 fulvic acid when the solution was
exposed to artificial sunlight. Although microbial degra-
dation was likely to be retarded due to the strong sorp-
tion and “aging” of 4-NP in biosolids, the association of
4-NP with organic matter microsites in biosolids might
have increased the effectiveness of sensitized photolysis
reaction when the 4-NP–containing biosolids were ex-
posed to light.
Our laboratory study suggests that surface application
of biosolids on soil could be effective in reducing biosol-
Fig. 3. Concentrations of 4-nonylphenol (4-NP) in compost in top- ids-associated organic chemicals that can be degraded
5-mm and bottom-10-mm layers exposed (solid circle) and unex-
posed (solid triangle) to artificial sunlight. The term C/Ci is the
through photolysis reactions. However, since water is
concentration ratio of 4-NP at each sampling point to its initial con- an important factor for the photolysis reaction, wet
centration. rather than dry biosolids should be applied. Surface-
5. 1572 J. ENVIRON. QUAL., VOL. 33, JULY–AUGUST 2004
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.
Fig. 4. Levels of nonylphenol polyethoxylates (NPnEOs) in the top-5-mm layer of biosolids exposed (open triangle) and unexposed (open circle)
to artificial sunlight.
broadcasting on sunny days might be a better approach rapid decrease of 4-NP within 30 d was observed in a
than broadcasting on overcast days. The results from field on which biosolids were thinly spread onto the
the field investigation by Marcomini et al. (1989) sup- surface of the soil at multiple times per year. Sunlight
port the conclusion from our laboratory study. An initial could rapidly degrade 4-NP before it has a chance to
Fig. 5. Concentrations of 4-nonylphenol (4-NP) in soil and biosolids mixture (1:1 weight ratio) in the top-5-mm layer exposed (solid circle) and
unexposed (solid triangle) to artificial sunlight. The term C/Ci is the concentration ratio of 4-NP at each sampling point to its initial concentration.
6. XIA & JEONG: PHOTODEGRADATION OF ENDOCRINE DISRUPTOR IN SOIL 1573
Reproduced from Journal of Environmental Quality. Published by ASA, CSSA, and SSSA. All copyrights reserved.
Fig. 6. Photolysis of 4-nonylphenol (4-NP) in a solution containing fulvic acid at 5 mg L 1. The term C/Ci is the concentration ratio of 4-NP at
each sampling point to its initial concentration.
be incorporated into soil and/or leached down the soil Hesselsøe, M., D. Jensen, K. Skals, T. Olesen, P. Moldrup, P. Roslev,
profile. 4-Nonylphenol was observed to be more persis- G.K. Mortensen, and K. Henriksen. 2001. Degradation of 4-nonyl-
phenol in homogeneous and nonhomogeneous mixtures of soil and
tent when biosolids were incorporated into soils through sewage sludge. Environ. Sci. Technol. 35:3695–3700.
cultivation (Vikelsøe et al., 2002). Jensen, J., H.L. Kristensen, and J.J. Scott-Fordsmand. 1997. Soil qual-
ity criteria for selected compounds. Working Rep. 83. Danish Envi-
Acknowledgments ron. Protection Agency, Copenhagen.
Keller, H., K. Xia, and A. Bhandari. 2003. Occurrence and transforma-
The experiments of this research were conducted at the tion of estrogenic nonylphenol polyethoxylates and their metabo-
Department of Agronomy at Kansas State University. The lites in three northeast Kansas wastewater treatment plants. Period.
research was financially supported by the Kansas Center for Hazard. Toxic Radioactive Waste Manage. 7:203–213.
Agricultural Resources and the Environment (KCARE) and Kelsey, J.W., B.D. Kottler, and M. Alexander. 1997. Selective chemical
the Kansas Agricultural Experiment Station. extractants to predict bioavailability of soil-aged organic chemicals.
Environ. Sci. Technol. 31:214–217.
Kolpin, D.W., E.T. Furlong, M.T. Meyer, E.M. Thurman, S.D. Zaugg,
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