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

156 Thiele-Bruhn J. Plant Nutr. Soil Sci. 2003, 166, 145±167
Degradation of antibiotics is governed by their molecular
composition. Macrolides and penicillins are targets for fast
degradation in soil (Gavalchin and Katz, 1994; Midtvedt,
2001). The intense transformation of sarafloxacin (Marengo
et al., 1997) and virginiamycin (Weerasinghe and Towner,
1997) yielded numerous metabolites of minor concentration
(< 10 %) and followed first order kinetics. In the presence of
wood rotting fungi, FQs are inactivated through metabolism at
the amine-position of the molecule while the heterocyclic ring
is very persistent (Wetzstein, 2001). Thus, the xenobiotic
fluorine moiety of FQs is quickly eliminated and the resulting
metabolites exhibit no or strongly reduced antibiotic potential
(Wetzstein et al., 1997). From the group of SAs, sulfadimethoxine
is possibly demethylated in sediments (Samuelsen
et al., 1994).
However, fixation of antibiotic compounds to surfaces or in
pores of the soil matrix may effectively protect them from
biodegradation (Samuelsen et al., 1992; Gavalchin and Katz,
1994) without alterations to their molecular structure (Halling-
Sùrensen et al., 2002b). Consequently, bioavailable concentrations
possibly decline below a threshold concentration
for the initiation of biological degradation (Alexander, 1999).
Thus, even compounds like TCs, which are reactive in
standard solutions, persist in the soil for several months (van
Gool, 1993; Höper et al., 2002). In aquatic sediments, no or
only minor degradation of FQs, TCs, and SAs was
determined over a period of 180 days (Samuelsen et al.,
1994; Hektoen et al., 1995). Besides of the physicochemical
properties of the antibiotics, the extent and kinetics of
degradation are also considerably affected by temperature
(Gavalchin and Katz, 1994) and adsorption to soil (Weerasinghe
and Towner, 1997) (Tab. 4). For the FQ enrofloxacin,
it was shown that unspecific adsorption to SOM reduced
degradation, although it was not completely stopped (Martens
et al., 1996; Wetzstein et al., 1997).
The products of biodegradation may still exhibit antimicrobial
potential, as it was found for several metabolites of FQs
(Weerasinghe and Towner, 1997; Marengo et al., 1997;
Wetzstein et al., 2000). Furthermore, the decline in
concentration of TCs and various antibiotics of other
structural classes was not always mirrored by a decline in
microbial toxicity (Halling-Sùrensen et al., 2002b, 2003). For
example, tylosin Awas converted to the antibiotic tylosin B in
acidic medium, whereas in neutral and alkaline medium,
tylosin Aaldol was detected along with a number of polar
decomposition products which were less bioactive (Halling-
Sùrensen et al., 2003).
Generally, the degradation of most xenobiotics is faster and
more complete under aerobic as compared to anaerobic
conditions. Correspondingly, degradation of oxytetracycline,
tylosin, sulfadiazine, streptomycin, metronidazole, and olaquindox
in activated sludge, soil and surface water was
similar or slightly lower under anaerobic as compared to
aerobic conditions, while ciprofloxacin was not degraded
under anaerobic conditions (Ingerslev et al., 2001; Halling-
Sùrensen et al., 2003; Tab. 5). Additionally, Ingerslev and
Halling-Sùrensen (2000) demonstrated that acclimation of
degrading organisms occurs in soil, when degradation times
for SAs declined dramatically after respiking the soil with the
same or a similar antibiotic.
5.4 Effects on soil organisms and plants
Pharmaceutical antibiotics are designed to affect mainly
microorganisms. Hence, the toxic dose for microorganisms is
often several magnitudes smaller than for higher organisms
(Wollenberger et al., 2000). Accordingly, dose related effects
on soil microorganisms were determined (Herron et al., 1998;
Pfeiffer et al., 1998). Selected results are listed in Tab. 6.
Effects and effective doses vary with time (Thiele and Beck,
2001). When a Gleyic Podzol was incubated with tetracycline,
the metabolic quotient was significantly affected by a
concentration of 10 lg kg ±1 after 8 weeks (Höper et al.,
2002). After 16 weeks, effects were significant only at an
initial concentration of 10 mg kg ±1 . Some antibiotics inhibit
microorganisms (Colinas et al., 1994; Thiele and Beck,
2001), while others promote their growth and activity (Patten
et al., 1980; Hossain and Alexander, 1984). Antibiotics like
streptomycin and cycloheximide are generally used to
selectively inhibit growth of bacteria and fungi in soil
experiments. Consequently, other pharmaceutical antibiotics
cause changes in the composition of the indigenous soil
microbial population as well (Ingham and Coleman, 1984; Mc
Cracken and Foster, 1993). In this manner, even small
extractable concentrations of oxytetracycline and sulfapyridine
produced longer lasting significant effects (Thiele and
Beck, 2001).
In contrast, species of soil fauna were not affected by even
excessive doses of antibiotics (Gomez et al., 1996; Herron et
al., 1998; Baguer et al., 2000). While no effects of selected
antibiotics on enchytreids and springtails were observed at
environmentally relevant concentrations, the anthelmintic
ivermectin significantly increased the mortality of springtails
(Jensen et al., 2001b). Also, anthelmintics can change the
fauna in and underneath cow-pats and hamper the dung
decomposition (Madsen et al., 1988; McCracken and Foster,
1993) and inhibit nematodes (Tomlinson et al., 1985) and
earthworms (Gunn and Sadd, 1994; Tab. 6)
The effects of antibiotics on organisms are essentially
influenced by their bioavailability that depends on the soil
properties, the availability of nutrients, and the presence of
root exudates (da Gloria Britto de Oliveira et al., 1995; Herron
et al., 1998). Multivalent cations inhibit the antibiotic potential
of TCs and FQs (Froehner et al., 2000). First results
confirming the reduction of antibiotic potency due to sorption
and degradation in soils were published by Jefferys (1952).
Degradation products of tylosin, sulfadiazine, streptomycin,
ciprofloxacin, and olaquindox showed no significant potency
in a soil bacterial assay (Halling-Sùrensen et al., 2003).
However, a transformation of pharmaceuticals does not
necessarily yield a decline in their antibiotic potential. Various
metabolites of TCs still exhibited bacterial toxicity in sewage
sludge and soil (Halling-Sùrensen et al., 2002b).
The period over which antibiotics are effective depends on
their persistence (Samuelsen et al., 1994). The antibiotic
potential can increase with time (Dojmi di Delupis et al., 1992)