Possible impact of treated wastewater discharge on incidence of antibiotic

resistant bacteria in river water

T. Iwane*, T. Urase** and K. Yamamoto***

* Department of Urban Engineering, University of Tokyo, 7-3-1 Hongo, Bunkyo, Tokyo
113-8656, Japan
** Department of Civil Engineering, Tokyo Institute of Technology, 2-12-1 Ookayama,
Meguro, Tokyo 152-
8552, Japan
*** Environmental Science Center, University of Tokyo, 7-3-1 Hongo, Bunkyo, Tokyo
113-0033, Japan

Abstract Escherichia coli and coliform group bacteria resistant to seven

antibiotics were investigated in the
Tama River, a typical urbanized river in Tokyo, Japan, and at a wastewater
treatment plant located on the
river. The percentages of antibiotic resistance in the wastewater effluent were, in
most cases, higher than the percentages in the river water, which were observed
increasing downstream. Since the possible increase in the percentages in the river
was associated with treated wastewater discharges, it was concluded that the river,
which is contaminated by treated wastewater with many kinds of pollutants, is also
contaminated with antibiotic resistant coliform group bacteria and E.coli. The
percentages of resistant bacteria in the wastewater treatment plant were mostly
observed decreasing during the treatment process. It was also demonstrated that the
percentages of resistance in raw sewage are significantly higher than those in the
river water and that the wastewater treatment process investigated in this study
works against most of resistant bacteria in sewage.
Keywords Antibiotic resistance; coliform group; Escherichia coli; river water
quality; the Tama River;
wastewater treatment

Introduction
Reclaimed wastewater is a stable water resource for urbanized rivers in Japan.
There are comprehensive basin-wide sewerage construction programs and effluent
standards aimed to control river water quality (Murakami, 1991). Moreover,
reclaimed wastewater serves as an ornamental and recreational water resource for
small rivers or streams in large cities in Japan. One of the major beneficial uses
of reclaimed wastewater (total volume: approx.
1 ´ 108m3/ year) is environmental water and flow augmentation (32%) (Asano et al.,
1996)
and there are projects to restore river flow with wastewater reuse (Ohgaki and
Sato, 1991). To keep reclaimed wastewater quality high and manage the water
environment, conven- tional water indexes such as BOD and coliform group bacteria
are insufficient. Unregulated pollutants including microorganisms in wastewater and
river water are now of increasing importance. Furthermore, unexamined risks, which
we have few measures to control at present, should be paid attention.
Antibiotic resistance is one of the major problems in today’s medicine and it is
known that bacteria with resistance to antimicrobial agents cause serious
outbreaks. In spite of this clinical concern, however, the significance of
resistant bacteria in water environment is not clear. Genes encoding antibiotic
resistance often transfer from bacterial cells to other cells, occasionally from
commensal bacteria to pathogenic ones. The water environment may, therefore, play a
part in providing resistance genes a field for transfer, as well as providing
resistant bacteria themselves a chance for spread. Antibiotic resistant bacteria or
resistance genes in water environment, consequently, could be one of the unexamined
potential risks, considering outbreaks of bacterial diseases in our community,
although the fates of resist-
ant bacteria or their genes have not been fully understood. The incidence of
antibiotic 91

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resistant bacteria has been surveyed in surface water (Koditschek and Guyre, 1974;
Grabow et al., 1975; Al-Ghazali et al., 1988; Aravanitidou et al., 1997),
wastewater (Sturtevant and Feary, 1969; Sturtevant et al., 1971; Grabow et al.,
1973, 1976; Bell et al.,
1981; Walter and Vennes, 1985; Mezrioui and Baleux, 1994), or both (Bell et al.,
1980,
1983; Niemi et al., 1983; Alcaide and Garay, 1984). Nevertheless, little
information is available on the change in percentages of resistance and the
comparison between antibiotic resistant bacteria and other water quality indexes
along a highly urbanized river which receives a large amount of effluents from
wastewater treatment plants.
In this paper, antibiotic resistant Escherichia coli and coliform group bacteria
were investigated at five sites along the Tama River, which is a typical urbanized
river in Tokyo, Japan, and at a wastewater treatment plant located on the river.
The results were compared with the percentage of resistant bacteria in the Tama
River previously reported by another researcher. Furthermore, the results were
compared with established water quality index or the results of previous studies by
other researchers on other contaminants in the same river to discuss the impacts of
wastewater discharge on the river water quality.

Description of the Tama River

The Tama River is about 130km in reach and flows through the western suburb of
Tokyo and densely populated metropolitan area, pouring into the Tokyo Bay (Fig.1).
Site A, about
53km from the mouth of the river, is at a sluice gate for Tokyo metropolitan water
supply. Downstream from this site, the river flow gathers a large amount of
effluent of treated wastewater or untreated gray water and polluted tributaries.
Site K, about 13km from the mouth, is at a sluice gate for Tokyo metropolitan water
supply that is no longer used because of the deterioration in water quality. There
are nine large scale municipal waste- water treatment plants, to all of which the
activated sludge process is applied. Their efflu- ents were discharged into the
Tama River or its tributaries between sites C and K.
Water quality data (average value) in 1996 at each site indicated in Fig.1 except
site D were obtained from an annual report (Japanese Ministry of Construction,
1998) and are shown in Figs.2 and 3. After the intake for water supply at site A,
the flow volume is largely reduced and gradually recovered mostly by wastewater
discharged from the treatment plants. Downstream from sites E to K, 65~92% of the
volume of the flow at each site was originating from wastewater (Japanese Sewer and
Sewerage Works Association, 1998) dis-
charged from the large-scale treatment plants upstream (Fig.2). BOD, COD, SS and
col-
92 Figure 1 The Tama River

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Figure 2 Volume of treated wastewater in the flow of the Tama River

Figure 3 BOD, COD, SS and coliform group count along the Tama River

iform group bacterial counts at sites E to K were considerably higher than those at
A to C (Fig.3).
In this survey, river surface water samples were collected at five sites; A, D, G,
I and K, between April and December 1998. During the same period, three types of
sewage samples; the influent, the treated (before chlorination) and the
effluent (after chlorination), were taken from the T-Wastewater Treatment Plant
located between sites C and D (Fig.1). In the influent of this plant, yearly
average values of BOD, COD, SS and coliform count were respectively 210mg/ l,
140mg/ l, 179mg/ l and 320000CFU/ ml; in the effluent,
2.2mg/ l, 11.0mg/ l, 3mg/ l and 160CFU/ ml (Japanese Sewer and Sewerage
Works Association, 1998). Samples were cooled and processed within four hours from
collection.

Materials and methods

E.coli isolation and antibiotic sensitivity testing
E.coli isolates were obtained from river samples of sites A and I (carried out four
times) and from all sewage samples (carried out three times). Samples were properly
diluted with phosphate buffer and streaked onto plates of chromogenic selective
(CHRO) agar (Chromocult Coliform Agar; Merck). This agar medium contains two kinds
of chro- mogenic substances which can detect activities of two enzymes (b-D-
Galactosidase and b- D-Glucuronidase) to examine both coliform group bacteria and
E.coli (Manafi et al.,
1991). The plates were incubated overnight at 44.5°C and fifty purple colonies for
each sample were randomly isolated as E.coli strains for antibiotic sensitivity
testing.
The strains isolated as described above were tested for their sensitivity to seven
antimi- crobial agents by the disk diffusion method with Muller-Hinton broth/agar
(Difco) and Tri- disk (Eiken-kagaku), which was a plastic strip with three disks
containing different amounts of the same antibiotic (Acar and Goldstein, 1996).
Broth culture of the tested strains was spread over an agar plate and seven plastic
strips for each antibiotic were placed on each plate. After overnight incubation at
37°C, the susceptibility of the organisms to each antibiotic was determined by the
presence of growth inhibition around the disks. No growth inhibition around all
three disks (resistant to the largest amount) was scored as resistance.
Antimicrobial agents employed and their largest amounts of each strip were as
follows:
ampicillin, 20µg; cephalothin, 30µg; kanamycin, 30µg; gentamicin, 10µg;
tetracycline
30µg; chloramphenicol 30µg; nalidixic acid 15µg. Two hundred isolates for each
river sam- ple and 150 isolates for each sewage sample were tested.

93

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Enumeration of antibiotic resistant coliform group bacteria
The total counts of coliform group bacteria and the counts of coliform group
bacteria resist- ant to ampicillin or tetracycline were measured for all river
surface water (carried out twice) and for all sewage samples (carried out three
times). Properly diluted samples were plated with CHRO agar or desoxycholate (DESO)
agar (Eiken-kagaku) and the same agar media supplemented with ampicillin
(concentration: 32µg/ ml) or tetracycline (16µg/ ml). After overnight incubation at
37°C, colonies were counted in quadruplicate. On the CHRO agar plates, purple and
red colonies were determined to be coliform group bacteria. The percentages of
resistant bacteria were calculated as the ratio of the counts on agar plates with
antibiotic to the counts on plates with no supplements.

Results
Percentages of resistant bacteria in the T-Wastewater Treatment Plant
Figure 4 shows the percentage of E.coli strains resistant to one or more
antimicrobial agents of seven employed or specifically resistant to ampicillin and
tetracycline respectively, in sewage samples of the T-Wastewater Treatment Plant.
22.0% in the influent, 14.7% in the treated (before chlorination) and 14.0% in the
effluent (after chlorination) were found to be resistant to at least one antibiotic
tested. 14.0% and 14.7% in the influent, 7.3% and 8.0% in the treated and 7.3% and
6.7% in the effluent were resistant to ampicillin and tetracycline respectively.
Figures 5 and 6 show the percentages of coliform group bacteria resistant to
ampicillin or tetracycline which were measured with two types of agar media (mean
value). 5.1% of coliform bacteria on DESO agar in the effluent, 18.5% in the
treated and 30.1% in the efflu- ent were resistant to ampicillin. 12.9% in the
influent, 21.3% in the treated and 13.9% in the effluent were ampicillin-resistant
on CHRO agar. Percentages of tetracycline-resistance were 16.9% in the influent,
9.9% in the treated and 8.7% in the effluent on DESO agar;
1.5%, 0.6% and 0.1% on CHRO agar.

Percentages of resistant bacteria in the Tama River

Figure 7 shows the percentage of E.coli strains resistant to one or more
antibiotics or specif- ically resistant to ampicillin and tetracycline in the Tama
River water samples (sites A and I). 9.5% and 13.0% from sites A and I were
respectively resistant to at least one antibiotic tested. 3.0% from site A and 5.5%
from site I were resistant to ampicillin. 6.5% from site A and 8.0% from site I
were resistant to tetracycline.
Figures 8 and 9 show the percentages of coliform group bacteria resistant to
ampicillin or tetracycline. At site A, 5.6% (DESO) and 6.8% (CHRO) of coliform
group bacteria were resistant to ampicillin; 0.0% of coliform group bacteria on
both agar media were resistant to
tetracycline. On the other hand, at the rest of the sites (D, G, I and K), 11.8% to
29.4%

Figure 4 Percentage of resistant E.coli in the

94 T-Plant
Figure 5 Percentage of ampicillin-resistant coliform group bacteria in the T-Plant

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Figure 6 Percentage of tetracycline-resistant coliform group bacteria in the T-

Plant
Figure 7 Percentage of resistant E.coli in the Tama
River

Figure 8 Percentage of ampicillin-resistant coliform Figure 9 Percentage of

tetracycline-resistant
group bacteria in the Tama River
coliform group bacteria in the Tama River

(DESO) or 10.5% to 31.0% (CHRO) were resistant to ampicillin; 1.4% to 6.8% (DESO)
or
0.1% to 1.1% (CHRO) were resistant to tetracycline.

Discussion
Decrease in the percentage of resistance in the T-Wastewater Treatment Plant
As shown in Fig.4, decrease in the percentage of antibiotic resistant E.coli
through the treatment process was observed. This result agrees with the findings in
our previous study (unpublished) on a wastewater treatment plant in Tokyo
Metropolitan area (not located on the Tama River) that the percentage of resistance
to one or more antibiotics of the seven was
23.0% in the influent and 18.8% in the treated. Furthermore, the values of the
percentages in the influent in this paper are comparable to those of ampicillin-
(14.0%), and tetracy- cline-resistance (15.5%) in the influent obtained from the
previous study. Therefore, it can be concluded that these values of resistant
E.coli percentage are likely in raw sewage in Tokyo and that percentage of
antibiotic resistant E.coli in raw sewage is considerably higher than in river
water.
On the other hand, the percentage of ampicillin-resistant coliform group bacteria
(Fig.5) was found to be increasing through the process, while that of resistance to
tetracycline (Fig.6) was decreasing. The treatment process possibly selects
bacterial species which are generally resistant to ampicillin compared to other
coliform group bacteria. The percent- ages of tetracycline-resistance on DESO agar
were rather higher than those on CHRO agar, although the reason is not known.
It is uncertain whether the wastewater treatment process induces selection which
prefers antibiotic resistant bacteria or it works against them, although there have
been some researches conducted on wastewater treatment plants. Mezrioui and Baleux
(1994) report- ed that the percentage of antibiotic resistant E.coli increased
during treatment in an aerobic lagoon, while there was no significant change
observed in an activated sludge process. Bell
et al. (1983) reported that, in short-term retention lagoons and mechanical
treatment plants, 95

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there was an overall reduction in the percentage of fecal coliforms resistant to
more than one antibiotic. However, they also found an overall increase in the
percentage of resistance in long-term retention lagoons. It can be considered that
the treatment system or its opera- tional conditions might affect the fates of
resistant bacteria or resistance genes.

Impacts of discharged wastewater on the Tama River

As shown in Fig.7, the percentage of resistant E.coli was observed increasing from
site A to I. The percentages of both ampicillin- (Fig.8), or tetracycline-resistant
(Fig.9) coliform group bacteria at sites D, G, I and K, which are contaminated by
treated wastewater, also become higher than those at site A. Furthermore, the
percentage of resistance in the effluent from the T-Wastewater Treatment Plant was
much higher than that in river surface water at site A, and also higher than that
at the rest of the sites in many cases. Thus, it can be con- cluded that the
increase in the percentage of antibiotic resistant bacteria in the river water
downstream was associated with discharges from wastewater treatment plants, in
which not only the total bacterial concentration but also the percentage of
resistance was much higher.

Comparison with a previous research on the Tama River. Antibiotic resistant

bacteria in the Tama River were also investigated by Arai (1991). He counted
coliform group bacteria and heterotrophic (HPC) bacteria resistant to six
antimicrobial agents and two metals at sites A, D, F, I, J and K. Coliform group
bacteria were counted on MacConkey agar and HPC bacteria were counted on Drigalski
agar. Resistant strains were selectively counted on agar plates containing each
chemical agent. The results for bacteria with ampicillin (con- centration: 50µg/
ml) or tetracycline (25µg/ ml) are summarized in Table 1, where our results
(coliform group bacteria on DESO agar) and the percentages of the river flow which
was comprised by wastewater discharged from the treatment plants upstream
(calculated from Fig.2) are shown.

Table 1 Percentage of resistant bacteria in the Tama River tested by Arai (1991)
(®: no data)

Resistance Site A B C D E
F G H I J K

Coliform Ampicillin 5.6% ® ® 11.8% ® ®

29.4% ® 12.0% ® 20.2% (DESO) Tetracycline 0.0% ®
® 3.7% ® ® 6.8% ® 1.4% ® 5.0%
Coliform Ampicillin 10.2% ® ® 12.5% ®
24.7% ® ® 11.9% 23.9% 23.3% Tetracycline 0.0% ® ®
1.0% ® 1.2% ® ® 4.7% 6.4% 4.1%

This study

Arai (1991)
HPC Ampicillin 21.1% ® ® 27.4% ® 28.2%
® ® 16.7% 29.5% 19.4% Tetracycline 4.4% ® ®
5.1% ® 6.6% ® ® 5.0% 4.9% 5.0%

Wastewater percentage 0% 0% 0% ®* 77% 66% 71% 92%

85% 77% 65% **

*: more than 0%, **: Japanese Ministry of Construction (1998) and Japanese Sewer
and Sewerage Works Association (1998)

The results in Arai’s report are in agreement with our results that the percentage
of antibiot- ic resistant coliform group bacteria was increasing downstream, in
spite of the difference in analytical methods and sampling periods. In the case of
HPC bacteria, the significant increase in the percentage of resistance was not
observed, because the percentage was rela- tively high even at site A. It is
implied that a considerable part of the HPC bacteria from nat- ural sources such as
soil, natural water and so on, is generally resistant to antimicrobial agents. It
is therefore indicated from this comparison that the percentage of antibiotic
resistant bacteria in the coliform group or E.coli reflects contamination by
wastewater in river water.
96

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Comparison of antibiotic resistance with other pollutants. There are some studies
on the Tama River dealing with other chemical pollutants. The results of these
previous reports are summarized in Table 2. Ouyang et al. (1998) found that the
concentrations of most species of metallic elements (chromium, molybdenum and
antimony) increased down- stream, for which environmental water quality standards
or guidelines have already been
established as related to the protection of human health. Their results also
demonstrated
that the increase between sites C and F was specifically attributed to effluents
from waste- water treatment plans and a tributary. In other studies on organic
pollutants, such as chlor- dane (Miyazaki et al., 1986), linear
alkylbenzenesulfonate (LAS) (Nishiyama et al., 1995), galaxolide and tributyl
phosphate (Teraguchi et al., 1996), the concentrations of each at site K were much
higher than at sites upstream. There were similar tendencies for the increase
observed for trihalomethane formation potential (THMFP) (Japanese Environmental
Agency, 1998) and non-purgeable total organic halogen in chlorine-treated river
water (formation potential; NPTOXFP) (Onodera et al., 1992). Sasaki et al. (1996)
measured mutagenicity of river water by the Ames assay with Salmonella typhimurium
YG1024. They detected considerably high mutagenicity at sites J and K, while no
mutagenicity was observed at site A. They also detected Trp-P-1 and Trp-P-2, both
of which are heterocyclic amines, from the river water at site K, and the
mutagenicity of river water was possibly associated with these anthropogenic
chemicals mainly from wastewater. It can be conclud- ed from these reports that the
Tama River is strongly affected by treated wastewater in terms of many pollutants.

Table 2 Results of the investigations on other pollutants in the Tama River (®: no
data)

Site A B C D E F
G H I J K

Cr (µg/ l) 0.59 ® 0.61 ® ®

1.20 ® ® ® ® 1.33 a) Mo (µg/ l)
0.96 ® 1.61 ® ® 1.85 ® ® ® ® 2.14
Sb (µg/ l) 0.30 ® 0.33 ® ®
0.61 ® ® ® ® 0.47
Chlordane (ppt) ® ® ® ® 0.8 ®
4.3 ® 4.4 ® 7.9 b) LAS (µg/ l)
® ® ® ® ® 34.6 ® ® 47.1 ® 62.3
c) Galaxolide (ng/ l) ® ® 10 240 250
190 ® ® ® ® 240 d) Tributyl phosphate (ng/ l)
® ® 9 38 42 70 ® ® ® ®
63
THMFP (µg/ l) 21 ® 17 ® ® ®
® 84 ® 84 89 e) NPTOXFP (µg/ l)
® 121 ® ® 200 ® 181 ® 171 ® 159
f) Mutagenicity
(net revertants/ l) 0 ® 28.5 ® ®
® ® ® ® 715 715 g)

a) Ouyang et al. (1998), b) Miyazaki et al. (1986), c) Nishiyama et al. (1995), d)

Teraguchi et al. (1996)
e) Japanese Environmental Agency (1998), f) Onodera et al. (1992), g) Sasaki et al.
(1996)

The major origin of these pollutants is a wastewater effluent judging from the fact
that more than 65% flow volume is from treatment plants downstream from site D in
this river. Nevertheless, the extent of the increase in the concentration varied,
depending on the pollu- tants. The concentrations of metallic elements in Table 2
became twice downstream com- pared to those at site A. THMFP at site K was observed
to be 5 times as large as that at site C. The concentration of galaxolide at site E
was 25 times as large as that at site C. On the other hand, the percentage of
ampicillin-resistant coliform group bacteria at site G on DESO agar was 5.3 times
as large as that at site A in our research. When the total count of coliforms
(Fig.3) is taken into account, the concentration of coliform group bacteria resist-
ant to ampicillin at site G is calculated to be 38 times larger. Furthermore, the
percentage of tetracycline-resistant coliform group bacteria was under the
detection limit at site A, like mutagenicity in Table 2, while more than 6.0% were
detected to be resistant downstream in
our research as well as in Arai’s report.
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Conclusions
Escherichia coli and coliform group bacteria resistant to seven antibiotics were
investigat- ed in the Tama River, a typical urbanized river in Tokyo, Japan, and at
a wastewater treat- ment plant located on the river. It was concluded from our
results that the river, which is contaminated by treated wastewater with many kinds
of pollutants, is also contaminated with antibiotic resistant coliform group
bacteria and E.coli. The percentages of antibiotic resistance in the treated
wastewater effluent were mostly higher than the percentages in the river water,
which were observed increasing downstream due to discharges from the waste- water
treatment plants. For example, 5.6% of coliform group bacteria in the upper reaches
were ampicillin-resistant on desoxycholate agar, while 29.4% were resistant in the
lower reaches. The percentages of resistance in the wastewater treatment plant were
observed decreasing during the treatment process in most cases. The percentage of
E.coli isolates resistant to one or more antibiotics in the effluent was less than
two-thirds of that in the influent. Only the percentage of ampicillin-resistant
coliform group bacteria was found to increase. Our results also demonstrated that
the percentages of resistance in raw sewage are significantly higher than in the
river water and that the wastewater treatment process inves- tigated in this study
works against most of resistant bacteria in sewage.

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