Pharmaceutical antibiotic compounds in soils - a review - Susane.info

152 Thiele-Bruhn J. Plant Nutr. Soil Sci. 2003, 166, 145±167
ca. 50 % of red rock crab (Cancer productus) collected after
oxytetracycline application exceeded the US FDAlimit of 0.1
lg g ±1 for seafood (Capone et al., 1996).
The intra-corporal administration of antibiotics inevitably
leads to residual concentrations in excrements. Consequently,
antibiotics are frequently found in dung and manure.
Manure samples from pigs contained up to 3.5 mg kg ±1 of
SAs and up to 4 mg kg ±1 of TCs (Höper et al., 2002;
Hamscher et al., 2002a; Sengelùv et al., 2003). Even larger
concentrations of TCs were determined in dung from beef
cattle and calves (Patten et al., 1980; Höper et al., 2002).
Campagnolo et al. (2002) detected antimicrobial compounds
from a multitude of different classes in all manure samples
taken from eight pig farms, with the single substances often
exceeding 100 lg l ±1 and the sum of all antibiotics
approaching 1000 lg l ±1 . Additionally, surface and groundwater
samples nearby the storage lagoons were often
contaminated with antibiotics. Residual concentrations of
antibiotics were estimated for agricultural soils, ranging for
TCs from 450 to 900 lg kg ±1 (Winckler and Grafe, 2000), for
macrolides from 13 to 67 lg kg ±1 and for FQs from 6 to 52 lg
kg ±1 (Schüller, 1998). In soils under conventional landfarming
fertilized with manure and monitored for two years, average
concentrations of up to 199 lg kg ±1 tetracycline, 7 lg kg ±1
chlortetracycline (Hamscher et al., 2002a), and 11 lg kg ±1
sulfadimidine (Höper et al., 2002) were detected. Contamination
of Swiss river water with veterinary antibiotics pointed to
a runoff or leaching of antibiotics from soil to surface water
(Alder et al., 2001). In contrast, Runsey et al. (1977) detected
no antibiotics in weathered manure on pasture and soil and in
runoff water. Additionally, b-lactams were rarely found in the
environment, most probably due to the fast degradation of the
chemically unstable lactam ring (Alder et al., 2001).
5 Fate of antibiotics in soils
5.1 Sorption and fixation
The antibiotics of different structural classes vary considerably
in their molecular structures and physicochemical
properties (Tab. 2). Some substances are hydrophobic or
non-polar, whereas others are completely water soluble or
dissociate at pH values typical for soils. Thus, distribution
coefficients (K d ) for the adsorption of antibiotics to soil
material and aquatic sediments, e.g. as summarized by Tolls
(2001), vary for SAs from 0.6 to 4.9, for TCs from 290 to
1620, and for FQs from 310 to 6310 (Tab. 4). From the
extractability, Katz and Katz (1983) deduced that the strength
of sorption to soil increases in the following sequence:
oxytetracycline = chlortetracycline £ bacitracin < tylosin <
erythromycin < streptomycin. For most of the antibiotics,
especially the stronger adsorbed TCs and FQs, desorption
hysteresis is strong, and partition coefficients multiply in
desorption experiments (Nowara et al., 1997; Rabùlle and
Spliid, 2000). Yeager and Halley (1990) found that only 50 %
of the adsorbed efrotomycin could be extracted, even with
harsh solvents. However, sorption of antibiotics to soil
minerals is weaker than to soil organic matter (SOM).
Although adsorption of various SAs was stronger to the clay
than to the sand size fraction of a soil, the opposite was true
for the increase of the partition coefficients at the desorption
step (Thiele et al., 2002). As shown for chlortetracycline, the
adsorption of epimers and metabolites of an antibiotic may be
considerably different from that of the parent compound and
in the case of anhydro-chlortetracycline may be even lower
(Tjùrnelund et al., 2000). This is of special importance when
the more mobile metabolite still exhibits antimicrobial activity.
Sorption of pharmaceutical antibiotics is especially influenced
by soil pH (Holten Lützhùft et al., 2000), SOM (Langhammer,
1989; Gruber et al., 1990), and soil minerals (Batchelder,
1982). Pinck et al. (1961a) and Bewick (1979) reported a
much stronger adsorption of aminoglycosides, TCs, and
tylosin to expandable three layer clay minerals than to illite
and kaolinite. Correspondingly, nearly the opposite sequence
was found for the desorption of these antibiotics, while no
release of aminoglycosides was determined (Pinck et al.,
1961b). Similar results were obtained for the adsorption of
these pharmaceuticals and of streptomycin in soils characterized
by the investigated different clay minerals (Pinck et
al., 1961a; Soulides et al., 1962). It is assumed that besides
adsorption, diffusion into porous soil particles also contributed
to the fixation. An interlayer adsorption of antibiotics from
various classes in the presence of montmorillonite was first
described by Pinck et al. (1962). Correspondingly, the strong
adsorption of FQs to soils, especially to clay minerals, was
accompanied by an expansion of the spacing of montmorillonite
(Nowara et al., 1997). The authors proposed
coulombic interactions and the adsorption of anionic
antibiotics via cation bridging to clay minerals as the main
mechanism for FQ adsorption. Thereby, the deprotonated
carboxylic group of FQ-carboxylic acids is fixed to the clay
minerals while the sorption of the decarboxylated derivative is
much smaller.
The sorption and fixation of antibiotics is strongly governed by
the property of numerous compounds to ionize depending on
the pH of the medium (Yeager and Halley, 1990). Octanol/
water coefficients of ionizing compounds change considerably
in a pH range around the acid dissociation constant
(Holten Lützhùft et al., 2000). Electrostatic forces mostly
drive the sorption of these derivatives to charged surfaces of
mineral and organic exchange sites (Williams, 1982; Holten
Lützhùft et al., 2000). The adsorption coefficients (K d )ofSAs
increased from < 1 up to 30 when the soil pH decreased in the
range of 8 to 4 (Boxall et al., 2002; Tolls et al., 2002). This
was related to the ionization of the amphoteric sulfonamides.
Correspondingly, the adsorption of TCs to humic substances
and clay minerals was not only influenced by the pH, but also
by the ionic strength of the medium (Sithole and Guy, 1987a,
b). Oxytetracycline adsorption was 2.5 times greater when
Ca 2+ was sorbed to clay minerals as compared to Na +
(Sithole and Guy, 1987a), because TCs form reversible
complexes with multivalent cations (Wessels et al., 1998).
Chelate complexes of TCs preferentially involve the
tautomeric C-11-C-12 b-diketone system that is formed under
alkalinic conditions from the keto-enol molecule, while with
decreasing pH, the dimethylamino group at C-4 position
becomes increasingly involved (Loke et al., 2002). Sithole
and Guy (1987a, b) proposed three major sorption mechan-