Water Air Soil Pollut: Focus (2008) 8:395404

DOI 10.1007/s11267-007-9148-4

Modeling Biodegradation of Nonylphenol

Kauser Jahan & Ral Ordez &
Ravi Ramachandran & Shira Balzer &
Michael Stern

Received: 19 February 2007 / Accepted: 1 August 2007 / Published online: 31 October 2007
# Springer Science + Business Media B.V. 2007

Abstract Nonylphenol is the primary breakdown environment. The validity of applying each model to
product of nonylphenol ethoxylates, a certain class of the biodegradation of nonylphenol was analyzed by
nonionic surfactants. Nonylphenol has been found to computing the R2 values of each equation.
be toxic to aquatic organisms and has been suspected
of being harmful to humans due to its xenoestrogenic Keywords Biodegradation . Kinetics . Nonylphenol .
properties. Although there are known releases of Electrolytic respirometry . Nonionic surfactants
nonylphenol to the environment, there is a lack of data
describing the extent of biodegradation. This study Nomenclature
thus focuses on much needed information on the A Arrhenius Frequency Factor (s1)
biodegradation kinetics of nonylphenol. Oxygen up- Ea Activation Energy (kJ/mol)
take, cell growth and nonylphenol removal data were kd decay coefficient (h1)
collected using batch reactors in an electrolytic kT reaction rate at temperature T, C
respirometer. Nonylphenol removal, cell growth and k20 reaction rate at temperature 20C
substrate removal rates were modeled by the Monod, Ks half-velocity constant (mg/L)
Haldane, Aiba, Webb, and Yano equations. The dif- Ki Haldane inhibition coefficient (mg/L)
ferential equations were solved by numerical integra- OX Cumulative Oxygen Uptake (mg/L)
tion to simulate cell growth, substrate removal, and R Universal Gas Constant (kJ/mole. K)
oxygen uptake as a function of time. All models S substrate concentration (mg/L)
provided similar results with the Haldane model t time
providing the best fit. The values of the kinetic T temperature C
parameters and the activation energy for nonylphenol X cell concentration (mg/L)
were determined. These values can be used for Y cell yield
predicting fate and transport of nonylphenol in the YOX oxygen consumption coefficient
YOX,d oxygen consumption coefficient for
K. Jahan (*) : R. Ramachandran : S. Balzer : M. Stern
endogenous respiration
Rowan University,
Glassboro, NJ 08028, USA
e-mail: [email protected] Greek Symbols
Specific growth rate (h1)
R. Ordez
University of Dayton, m Maximum specific growth rate (h1)
Dayton, OH 45469, USA Temperature activity coefficient
396 Water Air Soil Pollut: Focus (2008) 8:395404

1 Introduction OH
Alkylphenol ethoxylates (APEs) are nonionic surfac-
tants made up of a branched chain ethylene oxide to
produce an ethoxylate chain (Ahel et al. 1994a;
1994b). The main alkylphenol ethoxylates used in
industry are nonylphenol (NPE) and octylphenol
(OPE). Nonionic surfactants, such as APEs, have been H19 C 9
shown to increase solubility and dispersion of poorly Fig. 1 Structure of nonylphenol
soluble hydrocarbons and oils thereby enhancing
desorption and bioavailability. They function as emul-
sifiers, wetting agents and dispersants. Nonylphenol are soluble in water; the shorter chain NPEs are in-
ethoxylates comprise about 80% of the worldwide soluble in water; particularly NP.
surfactant market volume (Giger et al. 1984). Formu-
lating products that commonly contain NPEs include 1.1 Nonylphenol
those used for fiber sizing, spinning, weaving, fabric
dyeing, herbicides, and cosmetics, scouring and NP is a lipophilic organic micropollutant and is a
washing. Materials also likely to contain NPEs are problem in wastewater treatment, sewage sludge,
water based paints, inks and adhesives (Corvini et al. surface waters and sediments (Chang et al. 2007).
2006). In the household market, APEs are used Nonylphenol has a log Kow value of 4.48 which
mainly in laundry detergents and hard-surface contributes to its tendency to bioaccumulate. It is
cleaners. There are many other significant sources of suspected of having estrogenic effects, including
NPEs including textile manufacturing, pulp and paper contributing to the feminization of male fish in sewage
production and recycling, and some pesticide formu- outflows (Tanghe et al. 1998; Topp and Starratt 2000).
lations (Talmage 1994). This suspicion is based in part on evidence that
There is an abundance of literature that indicates nonylphenol can bind to human estrogen receptors,
that NPEs can be biologically degraded in sewage stimulate human breast cancer cell growth, and induce
treatment plants and in natural environments (Brunner the expression of the egg protein vitellogenin in fish
et al. 1988; Ahel et al. 1996; Naylor 1995; Yuan et al. (Naylor 1995). The evidence of estrogenic effects has
2004; Johnson et al. 2005; Cheng et al. 2006; Hseu intensified concern over environmental and human
2006). Most of these articles have focused on the fate health effects. Throughout northern Europe a voluntary
of NPEs and their metabolites. Researchers have ban on APE use in household cleaning products began
indicated that the major biodegradation product of in 1995 and restrictions on industrial applications
NPEs is nonylphenol (NP). They have further identi- followed by the year 2000 (Ahel et al. 1994a).
fied that NP is much more persistent than the parent Many researchers over the years have investigated
compound and can mimic estrogenic properties. NP the biodegradation of NP under various conditions.
has a phenolic ring and an attached lipophilic linear Banat et al. (2000) reported results of aerobic
nonyl chain or, more usually, branched nonyl group. treatment under thermophilic conditions of sewage
The structure of NP is presented in Fig. 1. sludge artificially contaminated with 4-NP. Experi-
NP has been identified to be approximately ten ments were carried out using three parallel laboratory-
times more toxic than its ethoxylate precursor (Brunner scale batch reactors operating with blank, 50 and
et al. 1988). Brunner et al. (1988) indicated that 100 mg/l of 4-NP concentration. For the two studied
biodegradation of NPEs is accomplished by stepwise concentrations, up to 66% NP reduction was achieved
shortening of the ethoxylate chain. This produces a at a specific air flow rate of 16 L/h and a thermophilic
complex mixture of compounds that can be divided into temperature of 60C, within 10 days of operation. The
three main groups: short-chain ethoxylates, nonylphe- presence of 4-NP has minor effect on the rate of
noxy carboxylic acids, and nonylphenol. As the chain sludge oxidation and the nitrogen and phosphorous
gets shorter, the molecule becomes less soluble. The content in the sludge. Chang et al. (2007) investigated
nonylphenoxy carboxylic acids and longer chain NPEs the effects of various factors on the aerobic degrada-
Water Air Soil Pollut: Focus (2008) 8:395404 397

tion of NP in sewage sludge. NP (5 mg/kg) degra- 2 Materials and Methods

dation rate constants calculated were 0.148 and
0.224 day1 and half-lives were 4.7 and 3.1 days, 2.1 Respirometric Studies
respectively. The optimal pH value for NP degradation
in sludge was 7.0 and the degradation rate was An N-CON electrolytic aerobic respirometer (NCON
enhanced when the temperature was increased Cheng Systems Co. Inc., Crawford, GA) with adjustable
et al., (2006) investigated the biodegradation of nonyl- temperature controlled water baths was used for this
phenol monoethoxylate (NP1EO) and nonylphenol study. Acclimated cultures capable of degrading nonyl-
(NP) by aerobic microbes in sediment samples phenol were developed using wastewater from the
collected at four sites along the Erren River in southern Mullica Hill wastewater treatment plant located in New
Taiwan. Aerobic degradation rate constants and half- Jersey. The acclimated cultures were grown at the
lives for NP (2 g g1) ranged from 0.007 to 0.051 day1 temperature the experiments were to be carried out.
and 13.6 to 99.0 days, respectively; for NP1EO (2 g g1) Enrichment of bacteria capable of degrading nonyl-
the ranges were 0.0060.010 day1 and 69.3115.5 days. phenol was accomplished in batch reactors containing
Aerobic degradation rates for NP and NP1EO were nonylphenol as the sole carbon source. The culture was
enhanced by shaking and increased temperature. acclimated to nonylphenol through repeated transfers
Levels of nonylphenol in the environment, as into fresh autoclaved nutrient buffer media, thereby
reported by Tanghe et al. (1998), are presented in ensuring that at least 99% of the bacteria used in the
Table 1. experiments were involved in the biodegradation of
While there is an abundance of literature focusing nonylphenol.
on the fate of NPEs and NP, very few studies have Nonylphenol with 98.0% purity was obtained from
focused on the biodegradation kinetics of NP. Staples et Fluka (Fluka, Milwaukee, WI). The analytical stan-
al. (1999) reported that 62% of NP was biodegraded in dard of NP with 98.0% purity was purchased from
28 days using the OECD 301F method. However NP Aldrich Chemical Co. (Milwaukee, WI). All other
required more than 10 days to undergo 1060% solvents were purchased from Sigma Chemical Co.
biodegradation. The researchers reported a half life of (St. Louis, MO). Nonylphenol concentrations of 30, 90,
20 days for NP at 22C. However this was not a and 150 mg/L were used for this study. HACH BOD
detailed study of biodegradation kinetics. As such a nutrient buffer pillows (HACH Chemical Company,
study of the biodegradation kinetics of NP was under- Loveland, CO) were used for the growth media. The
taken. The research objectives for this study were to respirometer was set at a constant temperature of 20C
for conducting experiments with various NP concen-
& Develop a mixed culture capable of biodegrading
trations. Separate trials were conducted at 15, 20, and
nonylphenol;
30C to determine the effects of temperature on the
& Conduct batch biodegradation experiments under
biodegradation kinetics of nonylphenol at a concentra-
varying temperatures and concentrations of nonyl-
tion of 30 mg/L. NP and cell concentrations were
phenol using respirometry;
measured at certain intervals by extracting samples
& Model experimental data to determine the biodeg-
from the reactors that were equipped with side arms
radation kinetics; and
with septa for sample collection. NP was measured
& Determine the activation energy for nonylphenol.
using a Hewlett Packard 1100 HPLC according to the
method outlined by Giger et al. (1984). Cell mass was
Table 1 Reported nonylphenol levels in the environment measured as protein by the method of Lowry et al.
Surface water Ahel et al. (1996) <0.1 to 180 g NP/L (1951). Literature indicates that dry cell mass is twice
the protein concentration. As such cell mass was
Sewage Brunner et al. (1988 ) 1 g NP/kg dry matter calculated by doubling the protein concentrations.
sludge and Giger et al. (1984) in sewage sludge Controls without NP and cells only were maintained
Secondary Ahel et al. (1994a) 2.244 g NP/L
to determine oxygen uptake due to endogenous cell
effluents Blackburn et al. (1999) Up to 330 g NP/L
Groundwater Barber et al. (1988) 1 g NP/L growth. Abiotic degradation of NP was also assessed
Ahel et al. (1996) 7.2 g NP/L by maintaining controls with NP only. All experiments
were conducted in duplicates.
398 Water Air Soil Pollut: Focus (2008) 8:395404

2.2 Modeling NP Biodegradation Table 2 Substrate-inhibition models

Source Model Equation

Biodegradation kinetics play an important role in the
fate of synthetic organic chemicals in both natural and Monod (1949) m mSK
max S
s (1)
mmax S
laboratory environments. As a consequence, predic- Haldane (1930) m 2 (2)
SKs SK
mmax S 1KS
i

tion of the fate of such chemicals requires quantifica- Webb (1963) m 2 (3)
SKs KS
mmax1
 S
tion of their biodegradation rates (Brown et al. 1990). Yano et al. (1966) m (4)
SKs S


S2
K1 1KS
Determination of the parameters describing biodegra- Aiba et al. (1968) m mmax Se
K1

(5)
SKs
dation was once a tedious and labor-intensive under-
taking. However, it is now possible to determine
biodegradation parameters by oxygen uptake data Arrhenius equation for cell growth rate m is pre-
collected automatically from batch reactors using sented below:
electrolytic respirometry. The principles of aerobic
mm Ae
RT
Ea
respirometry have been described in details by Grady
and his coworkers (Dang et al. 1989; Gejlsbjerg et al.
The above mentioned models were used to analyze
2003 ; Grady et al. 1989; Smets et al. 1996). The key
the experimental data obtained for NP removal, cell
advantage of using respirometric data for estimation
growth and oxygen consumption. Equations used to
of substrate biodegradation kinetics is the fact that
describe the removal of nonylphenol (S), cell growth
substrate removal, cell growth and oxygen consump-
(X) and oxygen uptake (OX) with time are presented
tion are all stoichiometrically linked.
below:
The most widely used expressions for biodegra-
dation kinetics is the Monod equation which is dS 1 dX

7
applicable to non-inhibitory substrates (Monod dt Y dt
1949). This model has been further modified for
inhibition and a number of models have been dX
proposed for substrate inhibition. Inhibition is defined mX
kd X 8
dt
as the interference of enzyme activity that affects
reaction rates. In biological treatment biodegradation
dOX
rates can be impacted tremendously due to the Yox mX Yox;D kd X 9
dt
inhibitory nature of external compounds. Many of
m S
where: m SKms S2 and the inhibition factor is SKi
2
the toxic compounds in the environment are in fact
Ki
enzyme inhibitors (Bailey and Ollis 1986). Depending These modeling equations have been used by other
on the impact of the inhibitor on the biochemical researchers for modeling pentacholophenol and phen-
reaction, inhibition can be classified as competitive, anthrene biodegradation kinetics (Klecka and Maier
un- or non competitive, feedback or as substrate 1985; Jahan et al. 1998). Kinetic coefficients related
inhibition. Competitive inhibition can be overcome by to cell growth (endogenous decay coefficient kd, half-
increasing substrate concentration. Non competitive velocity constant Ks, inhibition constant Ki, maximum
inhibition is irreversible. Substrate inhibition occurs specific growth rate m, and maximum yield coeffi-
when concentrations of the substrate itself become cient Y) were determined by developing and imple-
inhibitory to the biochemical reaction. menting a MATLAB mathematical model (Shah et
The Monod model and the modified model for al. 2003). The MATLAB function ode15s, which
inhibition by various researchers are presented in implements a variation of the Runge-Kutta numerical
Table 2. method, was used to solve the differential equations.
Biodegradation rates are also impacted by tempera- The MATLAB function lsqnonlin was used to
ture. The Arrhenius model has been used extensively perform nonlinear optimization to determine the pa-
in biological and engineering literature over limited rameters in the kinetic model that best match the
temperature ranges (Onysko et al. 2000) in quantify- experimental data sets. The model predictions were
ing the effect of temperature on reaction rates. The compared to the experimental oxygen uptake data, NP
Water Air Soil Pollut: Focus (2008) 8:395404 399

removal and cell growth and the process was repeated reactor data were statistically different when com-
until the best agreement was obtained between the pared to the control results. Moreover there was no
simulated and observed values. The routine mini- lag or acclimation period observed in all experiments.
mized the residual sum of the squares error (RSSE) This was due to the use of acclimated mixed cultures.
between the experimental and observed values. Initial cell mass added in all reactors was 5.0 mg/L.
The Monod model did not represent any of the
2.3 Statistical Analyses experimental data adequately. As such the four
different inhibition models were used to model the
Statistical data analyses were conducted to determine experimental data.
if the data for oxygen uptake in the presence of Initial estimates of cell growth rate were obtained
nonylphenol were statistically different from the from separate batch studies conducted at 20C. These
control data. Data for the 110 day duration was fitted were conducted to determine cell growth rate and
by linear regression for each curve to obtain the slopes cell yield Y from the slope of the straight line plots of
of the regression lines. The significance of the ln X versus time and X versus S, after the acclimation
difference of the slopes between the control and the period. Initial values of m, Ks and Ki were deter-
NP reactors was tested using a paired t-test (Crow et al. mined using nonlinear regression on S and m using
1960). A null hypothesis that states that the difference MATLAB. The values obtained for m, Ks and Ki
between the slopes of the regression lines is zero was were 0.14 h1, 387 mg/L and 290 mg/L respectively.
tested by comparing the t value obtained to the A cell yield value Y of 0.8 was obtained and used in
critical t value selected at a significance level of the modeling studies. YOX values were estimated to be
2%. If t experimental exceeded the critical t around 2.5 from total oxygen uptake and total NP
value, the null hypothesis is rejected and the dif- concentrations. Model sensitivity analyses were con-
ference between the data is significant at the 2% ducted to see which kinetic parameters impacted the
significance level. shape of the oxygen uptake, cell growth and substrate
removal curves drastically. The parameters that
appeared significant included m, Ks, YOX, Y and Ki.
3 Results and Discussion The endogenous decay coefficients kd and YOX,d did
not impact the curves significantly and were assumed
No oxygen uptake and cell growth were observed in to be 0.005 and 0.008 h1.
the control reactors that received cells only. Abiotic The average results of NP removal, cell growth and
degradation of NP was also not observed. All NP oxygen uptake for 30 mg/L NP at 20C is presented
Fig. 2 Oxygen uptake,
cell growth and NP removal
for 30 mg/L nonylphenol
at 20C
400 Water Air Soil Pollut: Focus (2008) 8:395404
Fig. 3 Oxygen uptake at 400
various NP concentrations
at 20C 350

300

O 2 Uptake (mg/L)
250

200 30 mg/L
90 mg/L
150
150 mg/L
100 Model Oxygen Uptake

50

0
0 5 10 15 20
Time (Days)

in Fig. 2 while the results of reactors containing NP at substrate inhibition which occurs at high substrate
a concentration of 30, 90, and 150 mg/L at 20C are concentrations. It is primarily caused by more than
shown in Fig. 3. one substrate molecule binding to an active site meant
The lines in Figs. 2 and 3 represent the Haldane for just one, often by different parts of the substrate
model predications for the experimental data. The molecules binding to different sub-sites within the
Haldane model adequately represented the experi- substrate binding site. If the resultant complex is
mental data at 20C. inactive this type of inhibition causes a reduction in
It is evident from Fig. 3 that NP biodegradation the rate of reaction, at high substrate concentrations.
was still evident at high concentrations and toxic The results of NP biodegradation at various
effects were not noted for the concentrations of NP temperatures are presented in Fig. 4. It is evident that
used in this study. Similar plots were obtained for all the biodegradation was much slower at lower tempera-
data sets and each set was modeled with the four tures. NP biodegradation has also been shown to be
select models. temperature dependent in other studies (Tanghe et al.
The kinetic parameters obtained for the selected 1998; Banat et al. 2000; Manzano et al. 1999). Tanghe
inhibition models are presented in Table 3. et al. (1998 ) indicated that NP added at concentrations
It is evident from Table 3 that the modeling results of 8.33 mg/L was almost totally removed and bio-
do not vary significantly from each other. Since the degraded when the reactors were operated at 28C. By
Haldane model yielded an R2 value of 0.9744 it was lowering the temperature from 28C to 1015C,
used for further data analyses. The optimum Haldane elimination capacities decreased drastically. Chang et
model kinetic coefficients at 20C were close to the al. (2007) also indicated that the NP degradation rate
values reported earlier from the batch studies. The was enhanced when temperature was increased.
Haldane model (Bailey and Ollis 1986) is a special The biodegradation kinetic parameters for tempera-
case of uncompetitive inhibition and is termed as ture studies for 30 mg/L of NP were also modeled by

Table 3 Regression statistics and parameter estimates for various inhibition models

Temp (C) Model m (h1) Ks (mg/L) Ki (mg/L) K (mg/L) R2 Value

20 Aiba et al. 0.0800 345.00 349.09 0.9403

20 Haldane 0.1291 340.10 260.27 0.9744
20 Webb 0.0700 349.39 348.92 562.11 0.9720
20 Yano et al. 0.0755 348.58 347.47 515.92 0.9719
Water Air Soil Pollut: Focus (2008) 8:395404 401
Fig. 4 Oxygen uptake at
90
various temperatures for
30 mg/L NP
80
70

O 2 U ptake (m g/L)
60
Temp 15oC
50
Temp 20oC
40
30 Temp 30oC

20 Model Oxygen
10 Uptake

0
0 10 20 30 40
Time (Days)

the Haldane model and the biodegradation kinetic tion energy is defined as the energy, in excess over the
parameters were determined. These values are pre- ground state, which must be added to an atomic or
sented in Table 4. molecular system to allow a particular process to take
The table clearly indicates that the growth rate m place (Bailey and Ollis 1986). It is typically denoted
is a function of temperature and NP concentration. as Ea and has units of kJ (kilojoules). Fast reactions
Increase in NP concentration led to decrease in m. usually have a small Ea; those with a large Ea proceed
This implies that nonylphenol is inhibitory and that a slowly. Ea is independent of temperature and concen-
higher concentration of the compound is a greater trations. Arrhenius proposed the following relation-
hindrance to growth. ship between reaction rate (k), temperature (T in
Figure 5 shows the graph of the natural log of the Kelvin) and activation energy Ea:
growth rates for nonylphenol concentrations of
30 mg/L plotted as a function of the difference k Ae
Ea =RT
between the temperature at which the experiment A is a pre-exponential factor or simply the prefactor
was conducted and 20C. and R is the universal gas constant. The units of the
By substituting the values on this graph into the pre-exponential factor A are identical to those of the
Q10 rule equation for reaction rates rate constant and will vary depending on the order of
kT k20 DT
20 10 the reaction.
The Arrhenius plot, as shown in Fig. 6, provides
a (theta) value of 1.06 was calculated. This is values for the activation energy (Ea) and the Arrhenius
within the accepted range of 1.011.07, with 1.04
being a typical value for biological activity (Metcalf Table 4 Kinetic parameter values at varying temperatures
and Eddy 1991). Although Onysko et al. (2000) had using the Haldane model
reported a similar temperature dependency for both Ki Temperature (C) NP (mg/L) m (h1) Ks (mg/L) Ki (mg/L)
and Ks for phenol, this was not evident for our
nonylphenol studies. More experiments on tempera- 15 30 0.080 1,000 2
ture effects may have to be conducted to obtain the 20 30 0.129 340 260
impact of temperature on Ki and Ks. 30 30 0.200 340 260
20 90 0.104 340 260
Attempts were also made to determine the activa-
20 150 0.075 340 260
tion energy for nonylphenol biodegradation. Activa-
402 Water Air Soil Pollut: Focus (2008) 8:395404
Fig. 5 Growth rate versus 0
temperature for NP at
30 mg/L
-0.5

y = 0.0586x - 2.1571
2
R = 0.9521

ln Growth Rate
-1

-1.5

-2

-2.5

-3
-6 -4 -2 0 2 4 6 8 10 12
o
Temperature (T-20) C

frequency factor (A). These were determined to be A= nonylphenol concentration. The Monod model did not
4.7x106 h1 and Ea =42.7 kJ/mole. adequately describe the biodegradation of nonylphe-
Since there are no existing values of Ea and A nol. The Haldane, Webb and Yano inhibition models
reported for nonylphenol, the nonylphenol activation were found to adequately describe the experimental
energy was compared to values reported for phenol. data at different nonylphenol concentrations and
Values of Ea for phenol were reported as 39.0, 28.4 different temperatures. The Aiba model also described
and 61.6 kJ/mole (Onysko et al. 2000). the kinetics well, but with more deviation from the
actual data values. Values of activation energy of
nonylphenol are similar to the ones reported for
4 Conclusions phenol in literature. Results of this study provide
much needed insight into the values of the biodegra-
This study indicates that nonylphenol is biodegrad- dation kinetic parameters that can be used for
able and its biodegradation is temperature dependant. predicting fate and transport of nonylphenol in the
The cell growth rate decreased with an increase in environment.

Fig. 6 Arrhenius plot for 0

nonylphenol
-0.5 slope = - E a /R
intercept=lnA
-1
y = -5136.2x+ 15.379
2
R = 0.9573
ln m

-1.5

-2

-2.5

-3
0.00325 0.0033 0.00335 0.0034 0.00345 0.0035

o
1/T K
Water Air Soil Pollut: Focus (2008) 8:395404 403

Acknowledgements This work has been funded by a grant Dang, J. S., Harvey, D. M., Jobbagy, A., & Grady Jr., C. P. L.
(DUE no. 0097887) provided by the National Science (1989). Evaluation of biodegradation kinetics with respi-
Foundation and Rowan University. However, this study has rometric data. Research Journal of the Water Pollution
not been subjected to the Foundations peer and administrative Control Federation, 61, 17111721.
review and therefore may not necessarily reflect the view of the Gejlsbjerg, B., Madsen, T., & Andersen, T. T. (2003).
agency, and no official endorsement should be inferred. Comparison of biodegradation of surfactants in soils
and sludgesoil mixtures by use of 14C-labelled com-
pounds and automated respirometry. Chemosphere, 50(3),
321331.
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