Water Air Soil Pollut (2011) 214:163–174
DOI 10.1007/s11270-010-0412-2
Occurrence and Environmental Fate of Veterinary
Antibiotics in the Terrestrial Environment
Kwon-Rae Kim & Gary Owens & Soon-Ik Kwon &
Kyu-Ho So & Deog-Bae Lee & Yong Sik Ok
Received: 2 November 2009 / Accepted: 23 March 2010 / Published online: 20 April 2010
# Springer Science+Business Media B.V. 2010
Abstract A wide variety of veterinary antibiotics
(VAs) has been detected in environmental water
samples, and this is of potential environmental
concern due to their adverse effects. In particular,
the potential for development of antibiotic-resistant
bacteria has raised social concerns leading to
intensive investigation regarding the influence of
antibiotics on human and ecosystem health. One of
the main sources of antibiotic effluence to the
environment is livestock manures that often contain
elevated levels of VAs that survive normal digestive
procedures following medication in animal hus-
bandry because unlike human waste, waste gener-
ated on farms does not undergo tertiary wastewater
K.-R. Kim (*) : S.-I. Kwon : K.-H. So : D.-B. Lee
Climate Change and Agroecology Division,
Department of Agricultural Environment,
National Academy of Agricultural Science, RDA,
150 Suin-ro, Kwonsun-gu,
Suwon 441-707, Republic of Korea
e-mail: Kimkr419@korea.kr
G. Owens
Centre for Environmental Risk Assessment
and Remediation, University of South Australia,
Mawson Lakes,
Adelaide, SA 5095, Australia
Y. S. Ok
Department of Biological Environment,
Kangwon National University,
Chuncheon 200-701, Korea
treatment, and consequently, the concentration of
antibiotics entering the environment is expected to
be larger from farming practices. Animal feed is
often supplemented with VAs to promote growth
and parasite resistance in the medicated animals,
and this practice typically resulted in higher use of
VAs and consequential excretion from livestock
through urine and feces. The excretion rate varied
depending on the type of VA used with around 75,
90, and 50–100% being excreted for chlortetracy-
cline, sulfamethazine, and tyolsin, respectively. The
excreted VAs that initially present in livestock
manures were degraded more than 90% when
proper composting practice was used, and hence,
this can be employed as a management strategy to
decrease VA environmental loads. The reduction of
VA concentrations during composting was mainly
attributed to abiotic processes rather than biotic
degradation. The VAs released to soils by the
application of manure and manure-based composts
can be degraded or inactivated to various degrees
through abiotic process such as adsorption to soil
components. Depending on the antibiotic species
and soil properties, residues can be transferred to
groundwater and surface water through leaching
and runoff and can potentially be taken up by
plants.
Keywords Antibiotics . Chlortetracycline .
Sulfamethazine . Tylosin . Degradation . Fate
164
1 Introduction
The concern regarding environmental exposure to
antibiotics has consistently grown since several
antibiotics were first detected in river water in the
UK more than two decades ago (Watts et al. 1982).
This resulted in many countries in the European
Union (EU) and the USA initiating monitoring
programs for the characterization of antibiotic distri-
bution in the environment and studies of their
environmental impact (Sarmah et al. 2006). In the
USA, a nationwide survey of pharmaceutical com-
pounds revealed that a number of antibiotics were
detected in 27% of 139 rivers at concentrations up to
0.7 µg L−1 (Kolpin et al. 2002). Among a number of
potential sources for this antibiotic effluence, land
application of livestock manure containing residual
veterinary antibiotics (VAs) appeared to be the
dominant pathway for the release of antibiotics to
the environment (Baguer et al. 2000).
Antibiotics are widely used in livestock production
for disease prevention and growth promotion (Aust et
al. 2008), with significant quantities of antibiotics
used as a feed supplement for growth enhancement of
food animals (Halling-Sorensen et al. 1998; Kumar et
al. 2005a). Although the inclusion of VAs in feed for
growth promotion was banned in the European Union
in 1998 (CEC 1998a, b), it is still a common practice
in other countries such as Canada, Korea, and the
USA (Sarmah et al. 2006). A significant portion of
the VAs given to livestock may be excreted with urine
or feces (Aust et al. 2008), and the consequential
treatment of soils with these wastes as an alternative
organic fertilizer could result in environmental con-
tamination. Given that VAs are often found to be
recalcitrant after excretion (Bouwman and Reus 1994;
Dolliver et al. 2008), many previous investigations
(Burkhardt et al. 2005; Kay et al. 2005c) have shown
that VAs can spread to the groundwater and the
surface water by infiltration and runoff, respectively.
Sustained elevated levels of antibiotics in the envi-
ronment may contribute to the development of
antibiotic-resistant microbial populations (Witte
1998) since even very low quantities of antibiotics
encourage the selection of antibiotic-resistant bacteria
(Khachatourians 1998; Hirsch et al. 1999; Boxall et
al. 2003). In addition, some of these antibiotics may
even cause serious allergies or may be toxic to
humans at significant concentrations (Patterson et al.
Water Air Soil Pollut (2011) 214:163–174
1995; Kumar et al. 2005a). The current information
regarding the implications of VAs on the terrestrial
environment and impacts on human health is still
limited. Thus, a wide range of investigations to
elucidate the influence of antibiotics on humans and
the environment is required to establish safe manage-
ment protocols for antibiotics usage and treatments.
To this end, the current paper reviews previous
studies to identify current knowledge gaps and
encourage further research, especially in Korea, on
areas specifically requiring attention. This review
covers (1) the amount of VAs used worldwide, (2)
estimated concentrations in livestock manure in
Korea, (3) the degradation and fate of VAs in the
environment, and (4) the transfer of VAs to plants.
The data reviewed mainly focused on three antibiotic
families including tetracyclines (TCs), sulfonamides,
and macrolides. These three families were chosen
because these were the VAs prioritized for environ-
mental risk studies in Korea based on use and
potential to reach the environment (Seo et al. 2007)
and they also constituted almost 60% of the total
amount of VAs used worldwide and are therefore
representative of the common issues associated with
VAs.
2 Worldwide Usage
The worldwide variation in the total amounts of VAs
used in different countries is shown in Table 1. Due to
the difficulty in collecting information on the total
amount used in individual stock farms, most countries
simply provided the amount sold as an estimate of the
amount used. At 11,148 tons year−1, the USA was the
biggest consumer of VAs followed by Korea at
1,533 tons year−1 (Table 1). These usage rates were
significantly higher than Australia and many EU
countries (Table 1), and this was attributed to not
only high numbers of livestock in both the USA and
Korea but also the common agricultural practice of
using VAs as feed supplements for growth promotion
in both countries. This was also well evidenced by the
calculation of the VAs used per head of livestock in
each country (Table 1). The EU prohibition on the use
of VAs as feed supplements for growth enhancement
in 1998 resulted in significant reduction in VA
consumption in European countries. Thus, with the
exception of the large amount of VAs used for pig
Water Air Soil Pollut (2011) 214:163–174 165

Table 1 Worldwide variation in the total amount (tonnes) of veterinary antibiotics used and the amount used (grams) per livestock
heada with country

Country Head (×1,000) Amount used (tonnes) Reference

Cattle Pig Poultry Cattle Pig Poultry Total

Australia 4,500 700 80,700 – – – 932 JETACAR 1999

Denmark 1,107 25,785 121,735 11 (9.9) 93 (3.6) 0.4 (0.003) 104.4 DANMAP 2005
Korea 1,819 8,962 109,628 112 (62) 831 (93) 335 (3.1) 1,278 KFDA 2006
Norway 930 802 3,646 – – – 6 NORM/NORM-VET 2005
Sweden – – – – – – 16 SAV 2005
UK 10,378 4,851 159,323 7 (0.7) 281 (58) 20 (0.12) 308 VMD 2006
USA 29,000 92,600 780,000 1,675 (58) 4,694 (51) 4,779 (6.1) 11,148 Benbrook 2002
a
The values in parenthesis are the amount of veterinary antibiotics used per head (grams head−1 )

(58 g head−1) in the UK, VA usage in Europe was
generally low. In contrast, no ban on VA use in the
USA and Korea has been imposed, and growth
promotion antibiotics are still widely used. However,
Korea is currently moving to limit the use of growth
promotion antibiotics and planning to cease the use of
growth promotion antibiotics feed additives by 2012.
Comparison of the total amount of VAs used
among the three different stock animals indicated that
the highest amounts of VAs were used for pig
followed by poultry (Table 1). This is related to the
type of livestock breeding. For effective production,
pigs are raised very densely in a limited space, and
such animal husbandry practices are likely to be the
cause of decreased immunity and higher infection
rates among pigs, driving the usage of antibiotic
treatments. Among the antibiotic families reviewed,
in most countries, tetracyclines were the most
commonly used antibiotics followed by sulfonamides
and macrolides (Table 2). For instance, these three
antibiotic groups accounted for approximately 90% of
the total antibiotics used in the UK, whereas in Korea
and Denmark, these three groups accounted for more
than 50% of total antibiotic usage.
3 Environmental Release
Although veterinary antibiotics can occur naturally in
the environment, the majority of VAs causing envi-
ronmental concerns is solely of anthropogenic origin.
The primary routes of environmental release are via
application of urine and manures from medicated
animals directly to land or via manure that has been
composted and then applied to land.
3.1 Excretion Rate and Concentrations in Manure
Since pharmaceutical antibiotic compounds are not
optimized in their pharmacokinetics, most VAs fed to
animals are poorly absorbed in the animal gut and
consequently do not accumulate in the subject
(Thiele-Bruhn 2003). Therefore, a substantial amount
of VAs given to animals is excreted with the urine and

Table 2 Variation of the

total amount (tonnes) of Country Amount used (tonne) Reference
three antibiotic families
used with country Total Tetracyclines Sulfonamides Macrolides

Denmark 112 30 (27a) 13 (12) 22 (20) DANMAP 2005

Korea 1,595 723 (45) 237 (15) 59 (4) KFDA 2006
a
The values in parenthesis Norway 6 0.3(5) 1.5 (25) – NORM/NORM-VET 2005
are the percentages of each
VA family used compared Sweden 16.4 1.6 (10) 2.5 (15) 1.0 (6) SAV 2005
to total VAs used in each UK 390 240 (61) 74 (19) 37 (9) VMD 2006
country assumed to be USA 11,148 3,230 (29) – – Benbrook 2002
100%
166
feces (Aust et al. 2008) within a few days of
medication (Winckler and Grafe 2001). Orally applied
tetracyclines were rapidly excreted via feces and
urine. While some individual animals continued to
excrete tetracyclines over a longer period of time
(Winckler and Grafe 2001), in general, for most
animals, 72% of the active ingredients initially
dispensed were recovered in the animal wastes within
2 days of application (Winckler and Grafe 2001).
Veterinary antibiotics commonly found in pig, cattle,
and turkey manures included tetracyclines, tylosin,
sulfamethazine, amprolium, monensin, virginiamy-
cin, penicillin, and nicarbazine (Webb and Fontenot
1975; De Liguoro et al. 2003; Kumar et al. 2004;
2005a) where excretion rates ranged from 65–75, 90,
and 28–100% for chlortetracycline (CTC), sulfame-
thazine (SMZ), and tylosin (TYL), respectively
(Table 3).
Depending on the specific antibiotic, excreted
material may include not only the original antibiotic
but also a significant proportion of both active and
inactive metabolites (Aust et al. 2008). Thiele-Bruhn
(2003) reported that after medication, antibiotics were
mostly excreted as their parent compounds, but that
metabolites might be excreted in some proportion and
were also normally bioactive. Even if antibiotic
metabolites were not bioactive, they can potentially
be transformed back to the bioactive parent com-
pound after excretion (Langhammer 1989). For
instance, glucoronide of N-4-acetylanted sulfametha-
zine was excreted as the SMZ metabolite from pig,
and this compound was converted back to the parent
form in liquid manure (Berger et al. 1986). After
medication, SMZ undergoes conjugation with liver
sugars that inactivates the compound, but on excre-
tion, microbes can rapidly degrade these sugars,
thereby converting the metabolites back into their
original bioactive parent forms (Renner 2002).
Table 3 Antibiotic excretion rate (percentages) via urine and feces after medication
Chlortetracycline Sulfamethazine Tylosin
(CTC) (SMA) (TYL)
(%)
≈65% ≈90% 50–100%
75% – –
– – 28–76%
72% (TCs) – –
Water Air Soil Pollut (2011) 214:163–174
Previous investigation on the distribution of anti-
biotics in manures showed that final residual concen-
trations varied with both the excretion rate and the
total amount fed to the animals. Chlortetracycline was
the most frequently detected compound in manures at
generally higher concentrations than either SMZ or
TYL (Table 4). This was in good agreement with the
amounts used from each antibiotic family in Table 2.
With the exception of one study conducted by
Dolliver et al (2008a), higher concentrations of
antibiotics were observed in pig manure than in either
manure from poultry or cattle. This may be due to the
higher amount of antibiotics used for pig breeding as
described in Table 1. The Dolliver et al (2008a) study
may be at odds with the majority of other studies
because their poultry was medicated with extremely
high amounts of antibiotics, and this consequently
resulted in higher concentrations of antibiotics being
excreted with the manures.
To our knowledge, there are no published data on
VA concentrations in livestock manures from Korea.
Therefore, the concentrations of VA in manure of
each livestock animal in Korea were estimated
(Table 5) using the total amount of manure production
and the total amount of antibiotics used during 2005
and the excretion rate of each antibiotic reported in
the literature. This estimate showed that among the
three different families, the concentration of tetracy-
clines was the highest in all three manures, and
compared to poultry and cattle, pig manure consis-
tently had the highest concentration of each individual
antibiotic. For most antibiotics, these estimated values
were much higher than those reported in the literature
(Table 4), but this may simply be a direct result of the
higher amounts of VAs used in Korea compared to
other countries, as well as dissipation of the anti-
biotics in manure in real samples, which is not
allowed for in this simple calculation.
Reference
(EMEA 1994–2002; Halling-Sorensen et al. 2001; Arikan et al. 2009)
(Montforts 1999)
(Feinman and Matheson 1978)
(Winckler and Grafe 2001)
Water Air Soil Pollut (2011) 214:163–174 167

Table 4 Variation in the

concentration of antibiotic Manure source Antibiotic concentration (µg kg−1) Reference
residues (micrograms per
kilogram) in manure with Tetracyclines Sulfonamides Macrolides
animal type
Pig 119 (CTC) 9,990 (SMZ) 12.4 (TYL) (Aust et al. 2008)
46 (CTC) 20 (SDM) – (Martinez-Carballo et al. 2007)
29 (OCT)
23 (TC)
880 (CTC) – – (Hamscher et al. 2000)
58 (CTC) 87 (SDM) (Xian-Gang et al. 2008)
78 (OCT) 87 (SMX)
81 (TC) 85 (SOD)
Poultry 94.7 (CTC) – – (Bao et al. 2009)
11,900 (CTC) 10,800 (SMZ) 3,700 (TYL) (Dolliver et al. 2008)
The individual compounds 91 (SDM) (Martinez-Carballo et al. 2007)
in each antibiotic group was
given in parenthesis 57 (CTC) 100 (SDM) (Xian-Gang et al. 2008)
62 (OCT) 101 (SMX)
OCT oxytetracycline,
TC tetracycline, SDM 69 (TC) 103 (SOD)
sulfadimidine, SMX Cattle 11 (CTC) – – (Hamscher et al. 2000)
sulfamethoxazole, SOD 208 (CTC) – – (Arikan 2008)
sulfadimethoxine

3.2 Degradation Via Composting
Manure composting is a well-established approach for
the stabilization of nutrients and the reduction of
pathogens and odors in manures (US Composting
Council 2000). Manure composting can also signifi-
cantly decrease the concentrations of VAs excreted in
feces and urines. The residue concentrations of
oxytetracycline (OTC) in feces at 10 days, in
composted manure at 30 days, and in soil after
treatment with composted manure at 140 days after
OTC medication were respectively, 54%, 6.3%, and
<0.23% compared to a control, implying that the
concentrations of antibiotic residues were significantly
reduced during the composting period (De Liguoro et al.
2003). While 60–85% degradation of TYL was
observed in pig manure under anaerobic conditions
within 24 h, almost complete degradation was
observed under aerobic conditions within 12 h
(Kolz et al. 2005). Since TYL is positively charged,

Table 5 Estimated concentrations (milligrams per kilogram) of antibiotic residues in livestock manure in Korea

Antibiotic family Animal type Manure generateda Antibiotics usedb Excretion ratec (%) Estimated conc.
(tonne year−1) (tonnes year-−1) (mg kg−1)

Macrolides Cattle 16,676,949 2.5 50–100 0.07–0.14

Pig 14,363,192 30.1 50–100 1.05–2.1
Poultry 4,349,489 5.4 50–100 0.62–1.24
Sulfanomides Cattle 16,676,949 9 90 0.49
Pig 14,363,192 134.7 90 8.44
Poultry 4,349,489 6.7 90 1.39
Tetracyclines Cattle 16,676,949 42.4 65 1.65
Pig 14,363,192 366 65 16.56
Poultry 4,349,489 104.5 65 15.62
a
RDA 2007
b
KFDA 2006
c
Refer to Table 2
168
it does not form complexes with metal ions but can
form strong ionic bounds with the negatively
charged components of manure (Loke et al. 2002).
In many other studies, the reduction of VA concen-
trations during composting has been adequately
demonstrated under a variety of different composting
condition (Table 6).
The degradation rate of antibiotics during com-
posting varied depending on the species of antibiotic,
the type of livestock manure, and the composting
conditions. Among the three different manures, the
concentration of CTC in pig manure was reduced the
least by composting, with temperature and composting
period being the most significant factors influencing the
degradation rate of antibiotics (Table 6).
The removal of VAs during manure composting
is mainly due to abiotic processes such as adsorp-
tion and/or degradation rather than biotic processes
(Aust et al. 2008; Arikan et al. 2009; Bao et al.
2009). Tetracyclines generally adsorb strongly to
manure constituents, and this is often attributed to
the high amounts of divalent cations that occur in
manures (Chadwick and Chen 2002) and the ability
of CTC to form chelate complexes with organic
substances (Martin 1979). It has also been suggested
that during composting, more adsorption sites for
VAs are generated (Hartlieb et al. 2003), and
consequently, extractable concentrations of tetracy-
clines and their metabolites decline with time in high
organic matrices such as composts (Arikan et al.
2009). Similar decreasing rates of CTC in cattle
manure were observed from both sterile and non-
sterile manure samples implying that decreased
Table 6 Reduction of antibiotic concentrations in manure during composting
Reduction rate (%) Manure
CTC SMZ TYL
92.6 (94.7) – – Poultry
27.3% (879) – – Pig
99 (11.9) 0 (10.8) 76 (3.7) Poultry
75 (5.9) – – Cattle (Calves)
75–89 (113) – – Cattle
98–99 (113) – – Cattle
40–49 (113) – – Cattle
a
The values in parenthesis represent initial concentrations (milligrams per kilogram).
Water Air Soil Pollut (2011) 214:163–174
concentrations appeared to be entirely due to
temperature-dependent abiotic processes (Arikan et
al. 2009). In addition, microbial population counts
have shown greatly decreased numbers of CTC-
resistant organisms after composting of the CTC-
containing mixture, suggesting that nonextractable
CTC residues are not bioactive (Arikan et al. 2009).
The temperature dependency of the rate of CTC
disappearance in a soil–chicken feces mixture indicated
that 44%, 88%, and 100% of CTC remained in the soil–
chicken feces mixture after 30 days of incubation at
30°C, 20°C, and 4°C, respectively (Gavalchin and
Katz 1994). Abiotic degradation or transformation
studies have demonstrated that at least some portion
of CTC or OTC degradation during composting and
stockpiling may be due to abiotic processes (Rose
and Bygrave 1996; Seborg et al. 2004).
From the information reviewed to date, a well-
managed composting process for livestock manures is
likely to reduce the environmental impact of antibiotics
to a reasonable level and thus enable manure applied to
soils to be used as an alternative organic fertilizer. So far,
there are no guidelines for the levels of contaminants
such as VAs in manure and composts, although there are
clear restrictions on the use of raw manure in organic
farming in the USA (National Organic Program
Regulations) due to the concern of bacterial contamina-
tion such as Salmonella and Escherichia coli (Kumar et
al. 2005b). Therefore, the regulated concentrations for
VA residues in manure-based compost should be
established, and inspection of commercially available
manure-based compost is recommended to mitigate
any potential environmental burden. In addition, it is
Composting conditions Reference
Moisture (60%), aerobic, (Bao et al. 2009)
42 days
Moisture (60%), aerobic, (Bao et al. 2009)
42 days
60°C,10 days (Dolliver et al. 2008)
35°C, 33 days, Anaerobic (Arikan 2008)
55°C, 7 days (Arikan et al. 2009)
55°C, 30 days (Arikan et al. 2009)
25°C, 30 days (Arikan et al. 2009)
Water Air Soil Pollut (2011) 214:163–174
critical to investigate the fate of antibiotics in soils
derived from the applied manure and/or manure-based
composts, since if the degradation of antibiotics was
mainly due to abiotic processes, then antibiotics
dissipated during composting could potentially be
redissolved from the compost after incorporation with
soils.
4 Fate in Soils
4.1 Concentration in Soil
The concentration of antibiotics in soils can be
elevated by repeated application of either fresh
livestock manure or manure-based compost (Winckler
and Grafe 2001; Hamscher et al. 2002). Depending on
the concentration of CTC and TYL in any specific pig
manure, the application of pig manure at a rate of
approximately 50,000 L ha−1 (equivalent to an
application rate of 168 kg ha−1 N) can result in final
applied rates of up to 387 g of CTC and 202 g of TLY
per hectare (Kumar et al. 2005a,b). In addition, from
the concentration of OTC in the manure and the
quantity of manure applied (96 tons ha−1), a plowing
depth (45 cm), and a soil density (1.5 kg L−1), a final
concentration of 12 μg kg−1 of OTC in plowed soil
was predicted (De Liguoro et al. 2003), which was in
good agreement with the level (<10 μg kg−1) actually
found. Moreover, it was estimated that the residual
concentrations of antibiotics in agricultural soils
ranged from 450–900 μg kg−1 for TCs and 13–
67 μg kg−1 for macrolides (Thiele-Bruhn 2003).
Many researchers have directly analyzed antibiotic
residues in soils following livestock manure applica-
tion, and the results are presented in Table 7. Of
course, if antibiotics are not effectively degraded after
release to soils, they could potentially be accumulated
Table 7 Concentration
(micrograms per kilogram) Tetracyclines Sulfonamides
of selected antibiotics in
soils 52 (CTC) 72 (SMZ)
86.2 (CTC) – –
93 (CTC) 4.5 (SMZ)
20–30 (CTC) – 50 (TYL)
The individual compounds – 11 (SDM)
in each antibiotics group is 7 (CTC) – –
given in parenthesis
199 (TC)
ND not detected
169
in concentrations significantly higher than the
values presented in Table 7. The monitoring of
antibiotic concentrations in soils under conventional
land farming fertilized with manure for 2 years
showed that the average concentrations of tetracy-
cline, chlortetracycline (Hamscher et al. 2002), and
sulfadimidine (Hoper et al. 2002) were 199, 7, and
11 μg kg−1, respectively.
The European Union has initially proposed that
when total concentrations of pharmaceutical com-
pounds exceed 10 μg kg−1 soil, further evaluation
of a specific compound should be considered
(Spaepen et al. 1997; Kuhne et al. 2000). However,
the 10 μg kg−1 concentration appeared to have been
set arbitrarily, as knowledge about the concentra-
tions that were relevant in the environment at that
time and the potential impact on crops in the field
was lacking (Jjemba 2002). Consequently, recent
research conducted by the International Cooperation
on Harmonisation of Technical Requirements for
Registration of Veterinary Medicinal Products provided
a more robust rationale for selecting the environmental
antibiotic concentrations of concern and proposed that
the total concentration in soil should not exceed
100 μg kg−1 (VICH 2000), as at this level, ecotoxicity
tests with veterinary medical products registered in the
USA showed no effects on earthworms, microbes, or
plants.
4.2 Interaction with Soils
Only recalcitrant antibiotics will have significant
opportunities to interact with soils. Since veterinary
antibiotics released to soils through livestock manure,
were degraded primarily by abiotic process rather
than biotic processes, such antibiotics were not
readily biodegradable (Gartiser et al. 2007; Bao et
al. 2009). This was also evidenced by Kreuzig and
Macrolides Reference
ND (TYL) (Aust et al. 2008)
(Hamscher et al. 2000)
– (Pawelzick et al. 2004)
(Halling-Sorensen et al. 2005)
– (Hoper et al. 2002)
(Hamscher et al. 2002)
170
Holtge (2005) who found that only 1% of the initially
applied sulfadiazine was mineralized and 82%
remained in a nonextractable form after a 102-day
incubation. The extent of antibiotic adsorption to soils
depends on the antibiotic species present and soil
properties including pH, organic matter content, and
the concentration and type of divalent cations present
(Rabolle and Spliid 2000).
Chlortetracycline strongly binds to soil constitu-
ents and may accumulate in the soil environment
(Hamscher et al. 2002), while SMZ persists in the
environment for prolonged periods and is potentially
leachable (Thiele-Bruhn 2003), and significant
amounts of OTC (95–99%) were bound to the soil
regardless of soil type (Rabolle and Spliid 2000). In
sandy and sandy loam soils, OTC distribution
coefficients (Kd) were 420 and 1,030 L kg−1,
respectively, while Kd values for TYL ranged from
8–11 L kg−1 for sandy soil and 62–128 L kg−1 for
sandy loam soils (Rabolle and Spliid 2000). In other
studies, the Kd of 11 different soils varied from 950
to 7,200 and 10 to 370 L kg−1 for OTC and TYL,
respectively (Ter Laak et al. 2006b), and the Kd for
OTC and TYL increased with increasing soil pH (Ter
Laak et al. 2006a). These results implied that in
general, OTC was more strongly absorbed to soil
than TYL, and antibiotic absorption was mainly
governed by soil pH.
TCs are relatively stable in acidic media but more
unstable under alkaline conditions and form salts in
both media (Halling-Sørensen et al. 2002). TCs form
complexes with chelating agents such as divalent
metal ions and β-diketons and strongly bind to
proteins and silanol groups. Sithole and Guy (1987)
found that sorption of tetracyclines to humic acids
(HAs) varied between 70% and 100% depending on
the pH. They assumed that sorption was caused by
three mechanisms of interaction with the organic
matter: (1) binding to divalent cations, (2) ion
exchange reactions, and (3) hydrogen bonding
between acidic groups in the humic acid and the
polar groups in the tetracycline. The presence of a
large amount of dissolved organic matter (DOM) was
also found to decrease the sorption of OTC to clay,
suggesting that DOM may increase OTC mobility
(Kulshrestha et al. 2004). OTC readily forms very
strong complexes with divalent cations like Mg2+ and
Ca2+ (Lunestad and Goksoyr 1990), and it is therefore
believed that the sorption of OTC to mineral cations
Water Air Soil Pollut (2011) 214:163–174
and organic matter such as humic acids is indicative of
strong binding with the soil matrix (Loke et al. 2002).
Modification of HA by Ca2+ addition increased
tetracycline sorption, suggesting that ternary complex
formation (HA–metal–tetracycline) may be important
at higher concentrations of multivalent metal cations
(Gu et al. 2007).
4.3 Runoff and Leaching from Soils
Antibiotic transport within soils and to groundwater
and surface water can occur by both leaching and
runoff. Surface transport of sulfonamides with runoff
was previously reported and attributed to hindered
infiltration of water into the soil due to surface sealing
by manure and particle-bound transport (Burkhardt et
al. 2005; Kay et al. 2005c; Kreuzig et al. 2005).
Furthermore, as evidenced by the study of Kreuzig et
al. (2005), the manner in which agricultural lands are
cultivated can determine the extent of runoff. In their
study, higher emissions of sulfonamides via runoff,
ranging from 13% to 23% of the initial amount
applied, were observed from manured grassland plots,
compared to arable land where runoff was reduced by
soil cultivation to 0.1% to 2.5%.
Hamscher et al. (2000) detected average concen-
trations of 9.5 μg kg−1 CTC in the upper 10 cm of the
soil from eight fields that had been treated with animal
slurry 2 days before sampling. This concentration
decreased with depth to about 0.7 μg kg−1 below
80 cm (Hamscher et al. 2000). In a subsequent study,
CTC levels between 0.17 and 0.22 μg L−1 were found
in water samples collected at 80- and 120-cm depth by
the same researchers. These studies indicated that the
antibiotics moved through the soil profile and reached
the groundwater. In contrast, some studies reported that
even after repeated application of OTC, residues were
not found below 20 cm in a sandy soil from Florida,
and this was attributed to the presence of higher
percentages of clay and organic matter in the surface
soil where residues of OTC were bound strongly to soil
particles (Gonsalves and Tucker 1977). Recently, TYL
was not detected in soil or leachates 2–120 days after
application of large amounts of TYL dissolved in a
slurry, to undisturbed soil columns and lysimeters (Kay
et al. 2005a,b). These results agreed well with other
studies that reported that TYL and OTC in a slurry
applied to soils posed very little risk of accumulating in
the soil or contaminating groundwater or surface water
Water Air Soil Pollut (2011) 214:163–174
(Blackwell et al. 2007; Blackwell et al. 2009). The
degree of mobility of antibiotics in the environment
can depend on several factors including chemical
properties (water solubility, dissociation constants,
sorption–desorption processes, and partitioning coef-
ficients at various pH), temperature, moisture content
of the soil, the timing of manure application, as well as
prevailing weather conditions (Sarmah et al. 2006).
Soil macropores are largely responsible for the rapid
movement of antibiotics to tile drainage systems and
surface water, while smaller macropores appear to have
a much less significant effect on antibiotic leaching
(Kay et al. 2004). Consequently, Kay et al. (2005a)
suggested that soil tillage prior to manure slurry
application could practically reduce the environmental
risk posed by VAs.
5 Plant Uptake
While the maximum residue level for antibiotics in
animal-based products has been established, there
are currently no regulated values for antibiotics
residues in plant-based products (JEFCA 2006).
This is because of the limited information regarding
antibiotic uptake by plants and the subsequent
influence on human health following ingestion of
plant material containing VAs. .
To our knowledge, only a few studies have been
conducted to investigate antibiotic uptake by plants.
Chlortetracycline was translocated to the above-
ground tissue of green onions, cabbage, and corn
from a CTC-treated soil (Kumar et al. 2005a). In
contrast, none of these plants took up TYL, despite
higher concentrations being applied to the soil and the
lower adsorption coefficient (Kd) of TYL compared to
CTC. This was attributed to the larger molecular
weight of TYL, which is almost double the mass of
CTC, making it unlikely that TYL was taken up by
plants either in mass flow (in the transpiration stream)
or as active uptake (Kumar et al. 2005a). SMZ, which
has a low molecular weight and is not strongly
adsorbed to soil particles, was also taken up by plants
(Dolliver et al. 2007). A plant uptake study of ten
antibiotics to lettuce and carrot from a sandy soil
spiked at a soil antibiotic concentration of 1 mg kg−1
detected florfenicol, levamisole, and trimethoprim in
lettuce leaves at concentrations ranging 6–
170 μg kg−1, whereas enrofloxacin, florfenicol, and
171
trimethoprim were detected in carrot at concentrations
ranging from 2.8–13 μg kg−1 fresh weight (Boxall et
al 2006). Studies of the toxicity of sulfadimethoxine
to plants found that a sulfadimethoxine concentration
of 300 mg L−1 in agar and soil-based laboratory
systems significantly reduced root, stalk, and leaf
growths in millet, pea, corn, and barley (Migliore et
al. 1996). These authors identified bioaccumulation as
the mechanism causing the phytotoxic response since
concentrations as high as 1,000- and 2,000-mg kg−1
sulfadimethoxine were reported in the foliage and root
materials, respectively (Migliore et al. 1996).
6 Conclusion
Veterinary antibiotics are necessary for both increased
efficiency in animal food production and to maintain
the welfare of livestock animals. However, VAs given
to animals as a feed supplement for growth promotion
in excess of the amount necessary for effectiveness
can potentially threaten the environment when they
are excreted by animals through the urine and feces
and subsequently directly or indirectly applied to soils
as a soil amendment. Regulated management in both
the manner of VA use and the treatment of
livestock waste prior to exposure to the environ-
ment is necessary to retard the potential adverse
influence of VAs on the environment. As adopted
in many EU countries, immediate abandonment of
the use of VA supplements in feed would be
necessary to immediately reduce the effluence of
VAs to the environment. However, this would still
leave an environmental burden for recalcitrant VAs
already exposed to the environment, and some
limited use of VAs is likely to continue worldwide.
The adoption of adequate composting processes for
livestock manure is a more effective strategy to
enhance the decline of residue VA concentrations
and will significantly reduce the quantities of VAs
transferred from stock farm to soils.
Previous studies have been limited to a few
selected antibiotic species, and the influence of
antibiotics in general on the environment and human
health is still not fully understood. Further research is
necessary to elucidate (1) the excretion rate of
different antibiotics and their fate during composting,
(2) the environmental activities of antibiotic metabo-
lites, (3) the behavior of VAs at the soil–root interface
172
and the subsequent plant uptake, and potential for
exposure of antibiotics to humans via ingestion of
crops grown in soils treated with livestock manure
and compost.
Acknowledgment This study was supported by the 2009
Post Doctoral Course Program of the National Academy of
Agricultural Science, Rural Development Administration,
Republic of Korea.
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