Journal of Hazardous Materials 364 (2019) 663–670

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Journal of Hazardous Materials

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Biochar-mediated sorption of antibiotics in pig manure T

a,1 b a,⁎
A.N. Ngigi , Y.S. Ok , S. Thiele-Bruhn
a
Soil Science, University of Trier, Trier, Germany
b
Korea Biochar Research Center, Division of Environmental Science and Ecological Engineering, Korea University, Seoul, Republic of Korea

GRAPHICAL ABSTRACT

ARTICLE INFO ABSTRACT

Keywords: Using manure contaminated with antibiotics as fertilizer is a primary source of soil pollution with antibiotics and
Antibiotics concomitantly with antibiotic resistance genes (ARG). Bioavailable antibiotics trigger further ARG amplification
Biochar during manure storage. Consequently it is aimed to facilitate the immobilization of antibiotics in manure. To this
Pig slurry end, five biochars derived from pine cone (BCP), rice husk, sewage sludge, digestate and Miscanthus were tested
Sorption kinetics
as additional sorbents in liquid pig manure for sulfamethazine, ciprofloxacin, oxytetracycline and florfenicol.
Competitive sorption
Non-linear sorption was best-fit using the Freundlich isotherm (R2 > 0.82) and the pseudo-second-order model
best described sorption kinetics (R2 > 0.94). Antibiotics’ sorption onto manure increased in the order sulfa-
methazine < florfenicol < ciprofloxacin < oxytetracycline. Admixtures of BCP to manure changed the order
to sulfamethazine < oxytetracycline < florfenicol = ciprofloxacin. Generally, with the addition of biochar,
sorption coefficients of florfenicol increased most (by factors > 2.7) followed by sulfamethazine and cipro-
floxacin. Yet, oxytetracycline was mostly mobilized probably due to competitive adsorption. Effects depended on
the proportion of biochar added and the type of biochar, whereby plant-derived biochar exhibited better im-
mobilization of antibiotics. Depending on the type and portion of biochar, admixtures to manure can be used to
lower the mobility and hence bioavailability of fenicols, fluoroquinolones and sulfonamides.

1. Introduction production has led to their frequent detection in different environ-

mental matrices. About 70–90% of the administered antibiotics can be
The continued intensive use of veterinary antibiotics in livestock excreted, primarily through the faeces and urine unchanged or as active

⁎
Corresponding author.
E-mail address: thiele@uni-trier.de (S. Thiele-Bruhn).
1
Present address: Department of Chemistry, Multimedia University of Kenya, Nairobi, Kenya.

https://doi.org/10.1016/j.jhazmat.2018.10.045
Received 3 July 2018; Received in revised form 26 September 2018; Accepted 15 October 2018
Available online 29 October 2018
0304-3894/ © 2018 Elsevier B.V. All rights reserved.
A.N. Ngigi et al.
metabolites [1]. The major route through which veterinary antibiotics
enter the environment is through the application of contaminated
manure as fertilizer onto agricultural land [2]. High concentrations of
antibiotics in animal manure of up to 1420 mg kg‐1 and 66 mg L−1,
respectively, have been reported world-wide for different classes of
antibiotics including sulfonamides (SAs), fluoroquinolones (FQs), tet-
racyclines (TCs) and fenicols (FCs), with resulting concentrations of
more than 0.1 mg kg−1 being reported in agricultural soils for different
antibiotics [3–6]
Antibiotic residues in the environment can cause adverse effects on
soil organisms [7,8] and plants [9]. The interaction of antibiotics and
manure affects soil microbial biomass and structural composition [10].
Adding to the direct adverse effects of antibiotics, these compounds
increase the formation of resistance in bacteria which might even result
in (multi)resistant pathogens with the potential to infect humans and
animals [11,12]. Antibiotic resistance transfer is highly accelerated in
manure [13,14]. Therefore there is need for an improved management
of wastes such as manure containing antibiotic residues [15], thereby
reducing the dissemination of bioavailable veterinary antibiotics and
related antibiotic resistance in manure before addition to soil.
Sorption is a key process controlling mobility, fate, bioavailability
and reactivity of antibiotics in the environment [16]. Biochars are
carbon-rich materials from pyrolysis of biomass that are increasingly
being recognized as potential sorbents for environmental applications
to lower the bioavailability of organic contaminants [17]. Some studies
have demonstrated the potential of biochar to sorb antibiotics [18,19],
and enhanced sorption of antibiotics such as FQs, SAs and TCs in soils
amended with different types of biochar [20–23]. Furthermore, biochar
substrates have other positive effects on manure such as reducing nu-
trient losses upon manure storage and after soil fertilization, and acting
as bulking agents in manure [24–26]. Biochar properties including
surface area, surface charge and porosity vary depending on feedstock
and pyrolysis conditions [27,28]. This in turn determines the sorption
potential of the biochars for antibiotics [29]. Although both plant-based
and biosolids biochars [18,20,22,30] have been used in sorption studies
with antibiotics, addition of biochar has not been tested for its effect on
the sorption of antibiotics that are contained in manure as micro-
pollutants. It is hypothesized that admixtures of biochar to antibiotic
contaminated manure will enhance sorption of antibiotics in manure
and would subsequently lower the formation and spread of resistance
genes in manure and manured soils.
Therefore, as the overall objective of this study, the use of biochar to
enhance sorption of antibiotics in pig slurry was tested using four an-
tibiotics, i.e. sulfamethazine, ciprofloxacin, oxytetracycline, and
Table 1
Molecular structures and formulae, CAS No., molecular weight (MW), pKa, logKOW and water solubility (S) of the investigated antibiotics.
Compound (abbreviation) Molecular structure Formula CAS No.
Sulfamethazine (SMZ) C12H14N4O2S
57-68-1
Ciprofloxacin (CIP) C17H18FN3O3
85721-33-1
Oxytetracycline (OTC) C22H24N2O9
2058-46-0
Florfenicol (FF) C12H14Cl2FNO4S
73231-34-2
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Journal of Hazardous Materials 364 (2019) 663–670
florfenicol which represent major structural classes of antibiotics used
in veterinary medicine. To investigate differences in sorptive proper-
ties, five biochars derived from different substrates were tested with
respect to different concentrations of the antibiotics and biochar, re-
spectively, as well as the sorption kinetics. Due to the high water
content of pig manure, experiments were done using the equilibrium
dialysis method [31,32], where the adsorbents (pig manure or biochar
amended manure) are contained in dialysis membranes.
Sorption data was fitted to the Freundlich, combined Henry and
Langmuir and Toth isotherm models to determine the most appropriate
isotherm model for describing the heterogeneous sorption systems.
Similarly, different sorption reaction kinetics models including pseudo-
first-order, pseudo-second-order and Elovich models [33–35] were used
for describing the kinetics of adsorption of antibiotics onto manure and
biochar amended manure.
2. Materials and methods
2.1. Chemicals
Sorption of veterinary antibiotics in pig slurry and in biochar
amended pig slurry was tested with four compounds: the SA sulfa-
methazine (SMZ), the TC oxytetracycline (OTC), the FQ ciprofloxacin
(CIP), and the FC florfenicol (FF). Sulfapyridine and chloramphenicol
were used as internal standards in LC–MS/MS analysis. All antibiotic
standard compounds were of > 99% purity and purchased from Sigma
Aldrich Vetranal (Taufkirchen, Germany). The chemical structures and
characteristics are shown in Table 1. Antibiotics standards stock solu-
tions of 1 g L−1 were prepared in HPLC-grade methanol (Merck,
Darmstadt, Germany). All other reagents were of analytical grade.
2.2. Manure and biochars
Liquid pig manure was obtained from a conventional pig fattening
and breeding farm in Luxemburg with 11,500 animals. Manure was
collected and stored underneath slatted floors and well-mixed before
sampling. The manure had a pH of 8.1, Eh < −300 mV and 6% dry
matter content. The dry matter comprised 41.3% organic carbon (OC)
and 2.3% total N. Manure was treated with the biocide NaN3 (0.5% w/
w) to avoid biodegradation during sorption experiments.
Biochars used in this study were derived from pyrolysis of (a) plant
substrates, i.e. pine cone (BCP), rice husk (BCR) and Miscanthus sinensis
(BCM), and (b) from fermented biosolids, i.e. sewage sludge (BCS) and
digestate (BCD). The latter was obtained from a renewable biomass
MW (g mol−1) pKa log Kow S (mg L−1)
278.33 2.65/7.65 [59] 0.89 [59] 1500 [59]
331.34 6.09/8.74 [60] 0.28 [61] 30,000 [62]
460.44 3.6/7.5 [63] −1.51 to −1.13 [64] 313 [65]
358.21 9.03 [66] −0.04 [67] Negligible
A.N. Ngigi et al. Journal of Hazardous Materials 364 (2019) 663–670

Table 2
Basic characteristics of biochars used in sorption experiments.
Biochar Source material Pyrolysis temp. pH Total C Total N Total H Total O C/N O/C H/C CEC SSAa

(°C) (%) (%) (%) (%) molar ratio (cmolc kg−1) (m2 g−1)

BCD Digestate 550 9.43 75.63 0.98 1.72 14.92 90.0 0.08 0.27 72.94 27.5 [68,69]b
BCS Sewage sludge 500 8.56 36.90 6.16 2.34 16.44 7.0 0.43 0.76 15.81 26.2 [70]
BCP Pine cone 500 6.77 54.68 1.20 3.02 17.40 53.1 0.08 0.66 6.15 193 [71]
BCR Rice husk 500 10.02 51.54 0.83 1.54 8.84 72.4 0.11 0.36 40.11 24.6 [72]
BCM M. sinensis 850 9.21 74.33 0.43 1.82 14.76 201.6 0.03 0.29 75.59 37.2c [73]

Biochar Source material Na K Ca Mg PO43− Fe Al Cud Mnd Znd

(g kg−1) (mg kg−1)

BCD Digestate 4.44 51.28 1.95 34.74 33.4 4.45 197.7 64.01 0.60 229.0
BCS Sewage sludge 0.01 1.83 0.88 0.38 6.97 81.89 279.1 655.9 0.57 867.0
BCP Pine cone 0.04 0.56 0.45 0.03 0.29 2.75 187.6 29.48 1.47 62.50
BCR Rice husk 0.03 8.12 0.39 1.81 3.15 5.40 208.2 31.41 2.66 50.63
BCM M. sinensis 0.55 17.32 1.20 2.59 2.20 1.30 143.7 36.50 n.d.b 55.25
a
SSA = Specific Surface Area.
b
Oral information.
c
Information from https://www.biochar.ac.uk/.
d
Values represent total extractable ions whereas other element contents represent exchangeable contents.

biogas plant, digesting maize. The BCM and BCD were provided by
PYREG GmbH (Dörth, Germany). BCR was obtained from DAEWON GSI
Co. Ltd. (Korea); BCP and BCS were obtained from the Korea Biochar
Research Center (Korea University, Seoul, Korea). General character-
istics of the biochars are listed in Table 2. Microscopic images of the
biochar materials were recorded with a VHX-6000 digital microscope
(Keyence, Neu-Isenburg, Germany). Images with a magnification of up
to 2000 times were recorded with the objective VH-ZST, those with
higher magnification were done with the objective VH-Z500. Fourier
transform infrared spectroscopy studies were done using a Jasco-4700
FTIR/ATR (Tokyo, Japan) at a wavelength range of 350–4000 cm−1.
Manure and biochars were free from residual contamination with
compounds of the antibiotic classes investigated in this study.
2.3. Sorption of antibiotics in manure
All sorption equilibration experiments were carried out in triplicate,
using dialysis membranes [31,32] (1000 Da molecular weight cut-off,
Merck, Darmstadt, Germany). Prior to sorption experiments, dialysis
membranes were washed in EDTA methanol solution, rinsed with
MilliQ H2O and conditioned with the background electrolyte solution of
0.1 M NaCl. NaCl was used instead of CaCl2 in order to avoid coagu-
lation and precipitation of suspended manure material. A liquid manure
volume equivalent to 0.5 g dry weight was carefully filled into the
dialysis tubes. Membranes with manure were closed with clips and
placed in glass cylinders filled with 250 mL of 0.1 M NaCl solution. The
NaCl solutions were spiked with aliquots of antibiotics standard solu-
tions to achieve final concentrations of 0, 0.2, 0.4, 0.8, 1.2 and 1.6 μg
mL−1, covering concentration ranges typically reported for manure
[36]. Antibiotics solutions were allowed to equilibrate for 48 h at 20 °C
with constant stirring at 120 rpm in the dark. Subsequently, dialysis
membranes were removed from the NaCl equilibrium solutions. Control
samples were prepared, containing only the aqueous solution with
antibiotics and the dialysis membrane and subjected to the same clean-
up procedure as the samples to determine the bias of antibiotic ad-
sorption to the dialysis membranes and losses due to the clean-up
procedure. Recoveries for SMZ and CIP were 98.2 ± 1.6% and
98.8 ± 3.1, respectively. Thus, sorption to dialysis membrane and
losses due to clean-up method were considered negligible. Recoveries
for OTC and FF were 71.3 ± 0.4% and 86.7 ± 4.7, respectively. De-
termined amounts were corrected for the losses for OTC and FF.
For sample clean-up and concentration, 5-mL aliquots of the NaCl
equilibrium solution were solid phase extracted using a strong anion
exchanger cartridge (SAX), Chromabond SB (500 mg in 6 mL volume),
for removal of manure-borne impurities and a hydrophilic-lipophilic
balance cartridge (HLB), Chromabond HR-X (200 mg in 6 mL volume),
for retardation of antibiotics in tandem, both from Macherey-Nagel
(Düren, Germany). The cartridges were conditioned with 3 mL me-
thanol followed by 3 mL 0.1 M NaCl. A 5 mL aliquot of each sample was
passed through the cartridges and cartridges were subsequently rinsed
with 3 mL 0.1 M NaCl. The SAX cartridge was unmounted and the HLB
cartridge rinsed with 3 mL distilled water followed by 3 mL 20% me-
thanol in distilled water and dried by an air-stream for 10 min. Final
elution was done with 2 mL MeOH. The eluate was evaporated using a
rotary evaporator, reconstituted to 1 mL in amber glass vials with
MeOH:MilliQ solution (1:1 v/v) and stored at 4 °C prior to LC–MS/MS
measurement.
The concentrations of antibiotics were determined using a
Shimadzu LC-20 HPLC (Shimadzu, Duisburg, Germany) coupled to an
API 3200 LC-ESI–MS/MS system (Applied Biosystems/MDS Sciex
Instruments, Toronto, Canada). The HPLC consisted of two LC-20 AD
pumps, an autosampler SIL-20 AC, a column oven CTO-10ASvp, and a
system controller CBM-20A Lite. A Sunfire C18, 3.5 μm, 3.0 × 20 mm
chromatographic column was used as stationary phase. The eluent
consisting of 0.1 M HCOOH in water (solvent A) and 0.1 M HCOOH in
methanol (solvent B), was delivered at 1 mL min−1 in a gradient pro-
gram. Sample injection volume was 10 μL. The software Analyst 1.4.2
(Applied Biosystems/MDS Sciex Instruments) was used for assessment
of the analytical data. The quantification of the parent compound was
done by summarizing the signal of the different mass transitions, while
the ratio of two single mass transitions was used for compound iden-
tification. Internal standards (sulfapyridine, chloramphenicol) were
added to the samples at concentrations of 0.1 and 0.5 μg mL−1 as ap-
propriate prior to analysis and external standards of each antibiotic
were used for calibration. The limit of detection of the analytical
method was 5 μg L−1 and the limit of quantification (LOQ) was
10 μg L−1. All data reported here were above the LOQ.
2.4. Sorption experiments with biochar amended manure
In experiment 1, the effect of BCP on sorption of antibiotics at dif-
ferent concentrations was tested. To this end, 5% (w/w) BCP was mixed
with a volume of liquid manure equalling 0.5 g dry mass. The NaCl
solutions were spiked with antibiotics standard solutions and allowed to

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equilibrate.
In experiment 2, the influence of the amount of biochar applied to
manure on the sorption of the antibiotics was tested. This was in-
vestigated by applying different amounts of BCP at 0, 1, 2, 5 and 10% to
liquid manure (w/w of total mass of liquid manure) at a single con-
centration of the different antibiotics of 1.2 μg mL−1. Samples used for
the sorption experiments equalled 0.5 g dry mass.
Experiment 3 aimed at evaluating whether different biochars dif-
ferently affect the sorption of antibiotics in manure. To this end, the five
different biochars, i.e. BCP, BCR, BCS, BCD and BCM, were applied to
manure at two proportions of 5 and 10% (w/w), respectively. The NaCl
solution was spiked at a final antibiotics concentration of 1.2 μg mL‐1.
Experiment 4 was done to determine the sorption kinetics of the
antibiotics to unamended manure and BCP (5% w/w) treated manure.
The solution was spiked with antibiotics at a concentration of
1.2 μg mL−1 and kept in the dark at 20 °C with constant stirring.
Sampling was done at 0, 4, 8, 24, 48 and 72 h, respectively, and the
concentrations of antibiotics remaining in the solution were de-
termined.

2.5. Data evaluation

The adsorbed amount of antibiotics was calculated as the mass

difference between the initial and final determined concentration. To
model heterogeneity of manure and that of biochar-manure admixtures,
the Freundlich isotherm, the two-site sorption isotherm model and the
Toth isotherm were fitted to the adsorption data using the best-fit
method [37–40] (see supplementary information, S1).
For experiments testing single concentrations of antibiotics, the
apparent linear sorption distribution coefficient, Kd (L kg−1), defined as
the ratio between the adsorbed content of a chemical and its con-
centration in the equilibrium solution was calculated as [20]:
Cs
Kd =
Caq
Additionally, the distribution coefficient normalized to the OC
content, KOC, of the sorbent (manure, biochar amended manure) was
evaluated as:
Kd
K OC =
fOC
Different kinetic models including pseudo-first order, pseudo-
second order and Elovich kinetics models were used to investigate the
time-dependent sorption behaviour of the antibiotics onto the sorbent
(Supplementary information) [33,41].
A one-factor ANOVA and Turkey’s post-hoc multiple comparison
tests (p = .05) were used to compare Kd values for the different treat-
ments, using IBM SPSS 22.0 statistical package (IBM Corporation, USA).
3. Results
3.1. Sorption of different antibiotics to manure and BCP amended manure
Sorption of the four antibiotics increased non-linearly with in-
creased antibiotics concentration in both manure and manure amended
with 5% BCP. Data were best fitted by the Freundlich isotherm (Eq. (3))
with R2 > 0.82 and SE ≤0.16 (Fig. 1a and b; Table 3).
log Cs = log Kf + n log Caq,
−1
where Cs (μmol kg ) is the total sorbate content associated with the
sorbent, Caq (μmol L−1) the amount remaining in the solution, Kf the
Freundlich constant (μmol1−1/n L1/n kg−1) and 1/n the measure of
nonlinearity. The treatments resulted in values of the Freundlich ex-
ponent n < 1 except for CIP in BCP amended manure (n = 1.14) and
for FF in manure (n = 1.16). Sorption non-linearity was strongest for
Fig. 1. Linearized Freundlich sorption isotherms for SMZ, CIP, OTC and FF in
(1) manure (a) and in pine cone biochar (BCP, 5%) amended manure (b). Symbols
represent the experimental data and lines represent modelled curve fits.
OTC in manure (n = 0.52).
The coefficients (Kf) of antibiotics’ sorption to manure increased in
the order SMZ < FF < CIP < OTC, ranging from Kf 189.4 for SMZ up
(2) to Kf 2046.9 for OTC. The Kf was significantly and strongly negatively
correlated (r = ‐0.87) with logKow of the different antibiotics. Sorption
coefficients increased in the presence of additional 5% BCP by factors of
1.15 (CIP) to 2.95 (FF), while it declined for OTC (Table 3) so that the
sequence in Kf values was changed to SMZ < OTC < FF = CIP. Fur-
thermore, nonlinearity was changed by addition of BCP, whereby the
nonlinearity exponent (n) decreased for SMZ and FF. In contrast, for
OTC and CIP, both antibiotics exhibiting highest coefficients of sorption
in manure, n was increased in the presence of BCP, so that sorption of
CIP and OTC became linear and more linear, respectively.
3.2. Effects of different amounts of biochar on sorption of antibiotics
Varying the amounts of BCP added to manure (0, 1, 2, 5 and 10%;
w/w) had different effects on the sorption of the different antibiotics
(Fig. 2). For SMZ and FF a clear and significant (p < 0.05) increase in
Kd with addition of 1% BCP and more was found. Yet, additions of ≥2%
BCP did not further increase Kd values. The increase in sorption was
especially strong for FF, where Kd values were about threefold higher in
(3)
BCP amended manure (Table 4), reaching sorption levels of CIP. For
CIP, the effect was different in such a way that sorption steadily in-
creased with higher admixtures of BCP, but effects on Kd of addi-
tions < 5% were not significant. It must be noted that the very low Kd
of CIP in the presence of 2% BCP (Fig. 2) cannot be explained. In
contrast, sorption of OTC declined with additions of up to 5% BCP and
only at 10% BCP the Kd of OTC in manure alone was reached again. The

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Table 3
Coefficients of the Freundlich model fitted to the experimental data on the sorption of antibiotics in manure and in manure with addition of 5% (w/w) of biochar.
SMZ CIP OTC FF

Manure BCP + manure Manure BCP + manure Manure BCP + manure Manure BCP + manure

Kf 189.4 238.9 647.3 751.6 2046.9 679.7 254.5 750.2

n 0.862 0.767 0.843 1.140 0.523 0.864 1.162 0.731
R2 0.868 0.975 0.939 0.948 0.979 0.827 0.869 0.953
SE 0.14 0.06 0.10 0.08 0.06 0.16 0.12 0.08

Fig. 2. Effect of different BCP concentrations added to manure on the linear
adsorption coefficients (Kd) of antibiotics. Bars represent standard deviations
from the mean Kd values of triplicate measurements. The data point with the
grey symbol was not used for the curve fit of CIP data.
Henry constants (Kd) for the antibiotics increased in the order
SMZ < CIP < FF < OTC and SMZ < FF < CIP < OTC at 5% and
10% BCP application, respectively.
3.3. Effects of different biochars on sorption of antibiotics in manure
Overall, the before-mentioned results with BCP were confirmed
with the other biochars (Table 5). While sorption enhancement was
small for SMZ and Kd values increased by a factor of less than 1.7,
effects of biochar admixtures were largest for FF with Kd values in-
creased by factors of 2.7–3.9, with differences between the five bio-
chars. The effect of the relative content of biochar was insignificant for
FF. In contrast, the effect of the relative content of biochar added to
manure on SMZ sorption varied with the type of biochar used. When
5% were added, a yet non-significant mobilization was found with BCD
(also at 10%), BCS, and BCM. Increasing the admixture of BCD and BCP
to 10% had no additional effect on the sorption of SMZ, while it was
significantly higher in the presence of BCS, BCR and BCM.
All biochars rather led to a mobilization of OTC in manure
(Table 5). Depending on the relative content added, sorption coeffi-
cients were significantly reduced in manure-biochar mixtures (5%)
using BCD, BCS, BCR and BCM (factor 0.3–0.9). Addition of 10% bio-
char resulted in significantly higher sorption, yet Kd values were still
significantly smaller compared to manure alone (BCD, BCS, BCR) or at
the same level (BCP, BCM). Also the sorption of CIP clearly depended
on the relative content of biochar admixed to manure. With 5% biochar
addition, Kd values were at about the same level as in manure alone and
even halved in the presence of BCD. However, additions of 10% biochar
led to significantly increased sorption and Kd values increased by fac-
tors of 1.2–2.
Assessing the overall effect of the different biochars (10%) on the
sorption of the four antibiotics in manure, it was found that sorption
increased in the following sequence BCD < manure < BCS
< BCM < BCR < BCP. Hence, sorption was not effectively enhanced
by the two biochars from biosolids but in part even led to mobilization
of CIP (BCD), SMZ and OTC (BCD, BCS). In contrast, plant derived
materials most of all exerted a positive effect. The increase in Kd by the
additions of the biochars was not correlated with most of the para-
meters listed in Table 2b. A significant negative correlation was only
found for the content of PO43− (average of r = −0.5) while the relation
to the contents of monovalent cations (Na+, K+) showed a negative, yet
non-significant trend (data not shown). Normalizing Kd values to the
OC content in the sample yielded KOC values, ranging from 495 to
3087 L (kg OC)−1 (Table S1, Supplementary material). Yet, these data
delivered no further information, especially because the amount of OC
added with 5 and 10% biochar was rather small compared to the OC
content of the manure sample. A Van Krevelen plot of molar O/C and
H/C ratios (Fig. S1) shows that the aromaticity of the biochars in-
creased in the order BCS < BCP < BCR < BCD < BCM. This corre-
sponded with FTIR analyses, where BCS yielded strong signals for
oxygen containing moieties (e.g. phenolic-OH and especially CeOeC
asymmetric stretch and CeO stretch) as well as for hydrogen containing
moieties (e.g. CeH stretching) (Fig. S2). Respective signals were clearly
less for BCM, while skeletal vibrations (500–800 cm−1) also indicating
aromatic C were more pronounced. The O/C ratio was not further re-
lated to the order of Kd values of the antibiotics in biochar amended
manure. However, the H/C ratio of the biochars (Table 2) was strongly
correlated with Kd of CIP and OTC (r = 0.71 and 0.76) while correla-
tion was less or even irrelevant for FF and SMZ, respectively (r = 0.42
and 0.17).
The pH of the equilibrium solutions was altered in the presence of
biochar admixtures and ranged from 7.6 to 8.5 (Table 6). The pH in-
creased in the order BCS < BCP < manure < BCM < BCR < BCD
at the 5% application level and was not substantially different at the
10% application level. The determined pH range largely overlaps with
the pKa values of the tested antibiotics (Table 1), so that the distribution
between neutral and anionic species varied between biochar-manure
mixtures. Hence, pH related effects on the sorption of the antibiotics
were expected. However, the proportion of anionic species and the

Table 4
Henry sorption coefficients (Kd; L kg−1) for antibiotics in manure and BCP-amended manure.
Manure +1% BCP +2% BCP +5% BCP +10% BCP

a* b b ab
SMZ 246.9 ± 37.5 376.0 ± 3.6 372.4 ± 9.4 333.0 ± 40.6 356.1 ± 22.1b
CIP 678.5 ± 48.7a 710.7 ± 31.1ac 512.6 ± 36.2b 733.1 ± 38.4ac 936.5 ± 115.2c
OTC 1337.4 ± 149.0a 1300.9 ± 63.2a 1264.5 ± 53.7a 1229.7 ± 40.5a 1351.7 ± 70.0a
FF 211.2 ± 66.4a 792.4 ± 52.2b 834.1 ± 8.7b 810.4 ± 16.9b 797.1 ± 17.8b

* Values with the same letter are not significantly different (p ≤ 0.05).

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Table 5
Coefficients Kd (L kg−1) for the adsorption of antibiotics in manure without and with addition of 5% and 10% w/w, respectively, of biochar derived from different
substrates.
Antibiotic Manure Biochar added BCD BCS BCP BCR BCM

SMZ 246.9 ± 37.5a* 5% 216.9 ± 9.7a 205.3 ± 10.9a 333.0 ± 40.6b 289.2 ± 33.5bc 233.3 ± 19.1a
10% 217.8 ± 75.2a 255.6 ± 43.3c 356.4 ± 22.1b 407.2 ± 1.4 d 318.3 ± 13.1bc
CIP 678.5 ± 48.7b 5% 372.1 ± 33.8a 742.5 ± 75.2c 733.1 ± 38.4bc 687.8 ± 93.0 b 625.0 ± 166.0 b
10% 823.9 ± 113.0c 1205 ± 177.2df 936.5 ± 115.2e 1225 ± 80.0d 1314 ± 125.5f
OTC 1337 ± 149.0ef 5% 448.6 ± 42.7a 822.9 ± 78.7c 1230 ± 40.5e 695.7 ± 66.1b 622.6 ± 60.1b
10% 731.2 ± 129.8bc 1080 ± 120.7d 1352 ± 70.0f 965.6 ± 23.5d 1097 ± 85.4de
FF 211.2 ± 66.4a 5% 600.4 ± 12.1b 620.0 ± 5.4b 810.4 ± 16.9d 711.4 ± 33.1c 592.2 ± 11.9b
10% 591.3 ± 14.4b 609.1 ± 36.1b 797.1 ± 17.8d 701.0 ± 22.8c 585.2 ± 12.2b

* Statistical significance tested within data of each individual antibiotic; values with the same letter are not significantly different (p ≤ 0.05).

Table 6 4. Discussion
pH of equilibrium solutions of manure and manure-biochar mixtures in 0.1 M
NaCl. Sorption coefficients of the four antibiotics in manure, which varied
Manure biochar added Manure-biochar mixtures widely, corresponded to previously reported data [42–44] and they
were highest (log Kf, 3.3, log Kd 3.1) for OTC. The much stronger
BCD BCS BCP BCR BCM sorption of OTC compared to the other three antibiotics was attributed
a a a a
to the complexation of the highly polar molecule to polar groups of
8.11 1% 7.59
2% a a
8.18 a a manure constituents. Tetracyclines such as OTC are known to form
5% 8.57 7.98 8.08 8.51 8.30 strong complexes with divalent cations such as Mg2+ and Ca2+, which
10% 8.40 8.00 8.27 8.50 8.49 ions are abundant in pig manure (Table 2); these complexes adsorb
a
through cation bridging to organic matter in manure and especially
Missing values indicate combinations that have not been tested.
onto proteins [6,31,42]. Similar bonding mechanisms apply to CIP; the
contained carboxyl, carbonyl and piperazinyl moieties act as electron
sorption coefficients of the individual antibiotics were not significantly donors in formation of strong coordination complexes with divalent
correlated; correlation coefficients (r) ranged between −0.22 and metals ions [45], which explains the observed higher Kf values of CIP
−0.53. relative to FF and SMZ in manure (Table 3). A comparably low sorption
in manure was determined for FF and SMZ. For the SA this is attributed
to electrostatic repulsion by acid functional groups, e.g. from humic
3.4. Sorption kinetics of the antibiotics acids and low-molecular-weight organic acids contained in manure
[23,46–48].
Sorption kinetics of the antibiotics in manure and BCP amended The diverse sorption effects obtained with the ternary mixtures of
manure was best fitted by the pseudo-second-order kinetic model (Figs. antibiotics, biochars and manure were attributed to differences in the
S3 and S4) with R2 ≥ 0.94 for all antibiotics (Table 7) using the line- physicochemical properties of the antibiotics on one hand (Table 1,
arized form of the model (Eq. (4)). [16]) and of the biochars on the other hand. Increased surface area and
t 1 1 sorbent porosity [21,29] played a role in enhancing the sorption of SMZ
= = t and FF. Images from digital microscopy (Fig. S5) showed that BCP and
Ct k2 C2e Ce (4)
BCM comprise plant tissue fragments with the remaining vascular
system providing inner pore space. This is not the case for the fragile
where Ce and Ct are the amount of adsorbate retained at equilibrium
rice husk material and the digested sewage sludge and biogas digestate
and at time t, respectively (μmol kg−1), k2 is the rate constant
materials. Corresponding to our findings, previous studies showed that
(kg μmol−1 h−1) and h the initial sorption rate [33,34]. The value of h
the sorption of SAs to soil was increased by the addition of biochar
decreased with the addition of 5% BCP for FF by a factor of 3, remained
[22,23,49] and a high sorption efficiency for FF (> 99.94%) was ob-
unaffected for OTC (factor 1.0), and increased for CIP and SMZ by
served in pinewood biochars with Freundlich coefficients of up to 2160
factors of 2.0 and 3.8, respectively. FF had the highest sorption rate (k2)
[29]. This agrees with the current study where FF was strongly sorbed
in both manure and BCP amended manure of 33.3 and
(Kd 584–810 L kg−1) upon addition of the five different biochars to pig
11.1 mmol kg‐1 h−1, respectively. There was a strong and positive cor-
manure.
relation between the sorption rate (h) of pseudo-second order kinetics
However, also opposite effects of biochar on sorption of antibiotics
and the sorption nonlinearity in manure (r = 0.50).

Table 7
Pseudo-first-order, pseudo-second-order and Elovich kinetic models constants of antibiotics in manure (M) and BCP-amended manure.
Sample Ce(exp) Pseudo-first-order Pseudo-second-order Elovich model

Ce(cal) (μmol kg−1) k1 (h−1) R2 Ce(cal) (μmol kg−1) k2 (μmol−1 kg h−1) h (μmol kg−1 h−1) R2 α (μmol kg−1 h−1) β R2

SMZ-M 639.60 421.11 0.02 0.879 588.24 4.7 × 10−4 163.93 0.970 203.45 7.6 × 10−3 0.888
SMZ-BCP 817.89 836.56 0.40 0.868 769.23 1.06 × 10−3 625.00 0.948 461.10 6.3 × 10−3 0.750
CIP-M 1029.28 464.62 0.09 0.943 1250.00 2.5 × 10−4 384.62 0.979 543.17 4.0 × 10−3 0.861
CIP-BCP 1041.35 406.16 0.09 0.934 1111.11 6.2 × 10−4 769.23 0.996 601.85 4.1 × 10−3 0.842
OTC-M 731.74 399.30 0.03 0.910 769.23 6.3 × 10−4 370.37 0.992 546.03 7.1 × 10−3 0.696
OTC-BCP 685.35 260.50 0.03 0.645 666.67 9.0 × 10−4 384.62 0.997 427.27 7.2 × 10−3 0.786
FF-M 466.33 66.15 0.03 0.275 454.55 0.16133 3.33 × 104 0.982 486.10 1.1 × 10−2 0.602
FF-BCP 918.32 95.96 0.03 0.345 909.10 0.01344 1.11 × 104 0.999 446.39 4.8 × 10−3 0.633

668
A.N. Ngigi et al.
were determined. Even lowered sorption coefficients were observed for
OTC in all biochar-amended manure. Accordingly, Zhang et al. [50]
reported Koc values for tetracycline on biochar to be lower than those
reported for soil and sediments [51,52]. A mobilization of SMZ was
found at the lowest tested addition level (5%) of BCD, BCS and BCM; an
effect also observed for CIP with several biochars at the 5% addition
level and with all biochars for OTC. The results on sorption rates (h in
second-order kinetic model) were correlated with the non-linearity
coefficient of the Freundlich sorption isotherm, indicating that the ac-
celerated sorption of SMZ and CIP in the presence of BCP went along
with increased non-specific surface sorption, while the increased but
decelerated sorption of FF was probably due to diffusion-controlled
sorption at specific sites.
The decrease in sorption (especially of OTC and CIP) and the lack in
sorption increase at higher additions of biochar to manure (especially of
SMZ and FF) were likely due to a combination of different effects. First,
sorption competition may have occurred. The Kd of OTC sorption to
manure-biochar mixtures was positively correlated with the H/C molar
ratio of biochar. This showed that aromatic sites on biochar were less
preferred for sorption than specific polar sites. Also polar organic
components in manure sorb at polar sites of biochars such as phenol,
amino, alcohol, and enone moieties (see also FTIR spectra in Fig. S2),
thus competing with OTC for the same sorption sites and lowering the
sorption of OTC onto biochar [50]. This was confirmed by decreased
Freundlich exponents (n) for OTC and also CIP upon addition of BCP to
manure (Table 3), indicating decreased sorption heterogeneity. It is
assumed that organic components of the manure interacted with bio-
char, thus blocking sorption sites and available surface area. This may
have resulted in lowered sorption site heterogeneity for the sorption of
antibiotics as it was shown for biochar in soil [20]. However, with in-
creased biochar, there was significant increase in sorption of OTC (but
did not reach the sorption extent found for manure alone), and even
more in sorption of CIP in manure-biochar mixtures. This implies that
the inhibiting factors, which were observed at low biochar concentra-
tion, such as competitive binding, were overcome by the admixture of
additional sorption sites provided by biochar. The dominance of sorp-
tion to polar sites in biochar was not relevant for SMZ and FF which
placed the order of prevalence as OTC > CIP ≫ FF ≫ SMZ. Also the in
general low sorption coefficients for SMZ compared to the other three
compounds are attributed to a competitive binding and blockage of
polar sorption sites in biochar by DOM from pig manure through π-π
interactions as was reported by Lertpaitoonpan et al. [53] for soils.
Further sorption inhibition could have been caused by PO43− that is
known to compete with anionic species of antibiotics for sorption sites.
This was demonstrated for tetracyclines, whereby sorption of the
zwitterion and anionic species was reduced by PO43− [54,55]. The
PO43− content was the only biochar property that was significantly
(negatively) correlated with the sorption coefficients of the antibiotics.
Whereas the presence of Cu2+ enhances the sorption of tetracyclines
[56], the sorption of SMZ is instead lowered [23,47]. Thereby the inner-
sphere complexation of Cu2+ directly competes for the surface O-
functionalities of the biochars, thereby hindering the formation of
charge-assisted H-bonds with SMZ [20]. Sorption reduction was espe-
cially pronounced for the two biochars from biosolids, i.e. BCS and
BCD. As typical for biosolids derived biochar, they contained highest
contents of Cu2+ and PO43−. Additionally, the pH dependent speciation
of the antibiotics (even of FF with pKa 9.03) was altered and sub-
stantially more anionic species were present (Table S2) in the manure-
biochar admixtures with medium alkaline pH of 8–9 (due to alkaline
biochars). It was previously shown that sorption of anionic species of
antibiotics is less compared to other species [57,58], which further
explains the findings of this study.
5. Conclusions
The study showed that antibiotics from different structural classes,
669
Journal of Hazardous Materials 364 (2019) 663–670
i.e. TCs, FQs, SAs and FCs, are very differently sorbed to manure. These
findings can be transferred to other compounds from these structural
classes. Additions of biochar to manure had largely different effects on
the extent, nonlinearity and kinetics of antibiotics’ sorption in manure.
Overall, the strong sorbing antibiotics OTC and CIP were rather mobi-
lized by biochar addition, while the weak sorption of SDZ and FF in
manure was substantially increased by biochar addition. The un-
expected mobilization is explained by sorption competition of biochar
with OTC and CIP for sorption sites on manure constituents and also
due to the pH-increasing effect of biochar addition to manure, leading
to an increase of anionic species that are known to sorb less to sorbates
in alkaline conditions. In addition, ion and especially phosphate com-
petition most likely occurred, which was strongest in biochar derived
from biosolids such as sewage sludge, containing the highest phosphate
content. Hence, biochar from plant material led to better sorption in-
crease than biochar from biosolids. In all cases, the effect on sorption
depended on the relative amount of biochar added to manure.
Admixtures of 2% of the best sorbing biochar from pine cone appeared
to be sufficient for an increased immobilization of SDZ and FF.
However, 10% of biochar or more were required when biochar from
other raw materials was used and to overcome the mobilizing effect on
OTC and CIP that was observed with smaller additions. In total it is
stated that biochar addition to manure is a good way not only to sta-
bilize nutrients in manure but also to reduce the bioavailability of
pharmaceutical antibiotics. This may help to limit adverse effects on the
environment such as the increase and spread of antibiotic resistance
that will be researched in a following study.
Acknowledgements
A.N. Ngigi received funding through a Postdoctoral Fellowship from
the German Academic Exchange Service (DAAD). Laboratory materials
and equipment were provided by Department of Soil Science, Trier
University, Trier, Germany. We thank C. Emmerling, University of
Trier, for providing us with the Miscanthus biochar substrate. We are
grateful to Mrs. K. Wetzel (Keyence, Neu-Isenburg, Germany) for sup-
porting us with the digital microscope and taking the images and we
thank Mr. D. Ondigo of United States International University-Kenya for
acquiring the FTIR spectra.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in the
online version, at https://doi.org/10.1016/j.jhazmat.2018.10.045.
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