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The International Arabic Journal

of Antimicrobial Agents ISSN 2174-9094

Survival and growth of antibiotic

resistant bacteria in treated
wastewater and water distribution
system and their implication in
human health: A review
Abstract
Multiple antibiotic resistant bacteria (MARB) and antimicrobial drugs
enter the environment via wastewater, especially from hospitals and
pharmaceutical plants, and through agricultural runoff, leading to contamination of surface and groundwater. This is a serious problem in
arid regions such as Oman where wastewater is recycled for irrigation and recharging aquifers. Treatment with chlorine does not completely remove bacteria from wastewater or prevent their re-growth
in downstream distribution systems. MARB can infect humans via
contaminated food and drinking water, or directly from the environment. Agricultural runoff and sewage, either treated or untreated,
are also the main sources of MARB in coastal seawater. It is necessary to use antibiotics more prudently in medicine, treat wastewater
more effectively, eliminate the discharge of untreated waste into the
environment, and curtail the profligate use of antibiotics as growth
promoters for livestock.

2014
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doi: 10.3823/758

Saif N. Al-Bahry1,
I.Y. Mahmoud I.Y.2,
J.R.Paulson3,
S.K. Al-Musharafi4
1Department of Biology
College of Science
Sultan Qaboos University
Muscat, Sultanate of Oman
2Department of Biological Sciences and
Chemistry
University of Nizwa
Nizwa, Sultanate of Oman
3Department of Chemistry
University of Wisconsin-Oshkosh
Oshkosh, WI 54901 USA
4Department of Applied Biotechnology
Sur, College of Applied Sciences
Sur, Sultanate of Oman

Corresponding author:
Prof. Saif N. Al-Bahry

 snbahry@squ.edu.om

Keywords: Antibiotic resistance, bacteria, survival and growth, human

health.

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The International Arabic Journal of Antimicrobial Agents

ISSN 2174-9094

Wastewater treatment and

survival of antibiotic resistant
bacteria
It is clear that antibiotic-resistant bacteria can be
detected in wastewater treatment plants. Treatment
of sewage can reduce the number of both sensitive and resistant bacteria significantly. However,
as will be discussed in the next section, not even
chlorination is sufficient to eliminate these bacteria
completely[1-2]. In short, the current methods used
for treatment of sewage effluent do not remove all
organic matter and pathogenic microbes. Sewage
treatment plants are the main sources of antibiotics
and MARB released to the environment, is a serious
public health concern [3].
The occurrence of multiple antibiotic-resistant bacteria in treated wastewater has been reported in
other studies. Antibiotic-resistant strains of intestinal
microflora, originating not only in humans but also
in domestic and agricultural animals, find their way
to sewers and sewage treatment plants [1-2, 4]. The
highest resistance to various drugs has been found
in E. coli strains isolated from the main sewage
treatment plants receiving effluents from three sewage sources in southern Austria. The most frequent
resistance rates were found in E. coli isolatesfrom
a sewage treatment plant receiving municipal sewage and sewage from a hospital [5]. The susceptibility of Acinetobacter spp isolates from upstream
and downstream of the hospital and pharmaceutical sewage treatment plant discharge points was
studied. The results revealed that hospital effluents
affected the prevalence of oxytetracycline resistance
only. On the other hand, the wastewater discharge
from pharmaceutical sewage treatment plant was
increased both single- and multiple-antibiotic resistance among Acinetobacter spp isolates [6].
A major problem facing water suppliers is the deterioration of bacteriological quality of the water
being distributed [7]. Since wastewater treatment

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processes and disinfection systems do not inactivate the whole microbial population, the surviving
microorganisms can adapt to the conditions in the
distribution system and start multiplying [1, 8-9].
Hence, it is meaningful to analyze treated water
in terms of microbial populations and the factors
influencing their growth.
The microorganisms found in a water distribution
network can either be indigenous, including those
growing in pipelines [10], or exogenous bacteria
such as fecal coliforms, which are introduced and
transported in water from the treatment plant [910, 11]. The latter group may potentially include
pathogenic bacteria carrying resistance genes. The
viability of coliform bacteria in water distribution
systems is used as an indicator for the presence
of potential pathogens, including opportunistic microbes [8]. The presence of these bacteria in water
occurs as a result of complex interactions among
various environmental factors [12]. These factors
include disinfection effectiveness, physicochemical
parameters and the quality of the water source [1,
9, 13]. Re-growth in the distribution system is stimulated by high content of organic matter in the water,
as shown by the linear relationship between bacterial level and organic concentration [12].

Antibiotic resistance,
heavy metals and chlorine
disinfection
Some sewage treatment plants in Oman receive industrial wastes that contain high concentrations of
heavy metals. In many cases, these heavy metals are
found in the treated sewage effluent and sludge at
concentrations exceeding maximum permissible levels
[14-16]. It is noteworthy that bacterial isolates from
waste streams contaminated with heavy metals have
also been found to be resistant to antibiotics. For example, microbial isolates from pig manure containing
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The International Arabic Journal of Antimicrobial Agents

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high concentrations of zinc and copper were found

to be highly resistant to antibiotics including piperacillin and doxycycline [17]. Other investigators have
reported that MARB have common survival mechanisms for resistance to antibiotics and heavy metals
[18-20]. Some antibiotic resistant bacteria such as
Enterobacter, Pseudomonas, Aeromonas, Kluyvera,
Klebsiella, Pasteurella, Serratia and Salmonella spp
isolated from treated sewage effluents use essential
heavy metals for their survival, and that these bacteria are also resistant to chemical disinfection [1].
Chlorine is the most widely used chemical disinfectant in wastewater treatment [21] because of its
potency in its uncombined form and because it is
effective against both bacteria and viruses, even at
low concentrations [8]. Chlorine acts on bacterial
cells by disrupting cell membranes, coagulating enzymes and nucleic acids, subsequently leading to a
reduction or cessation in metabolic activity [8, 22].
Chlorine has been shown to cause fatal physiological injury to coliforms [23].
Tertiary treatment of wastewater with chlorine
contributes greatly to the removal of most bacteria
from treated effluent, including fecal coliforms [5].
Tertiary treatment should be able to eliminate both
antibiotic-resistant and -sensitive pathogens, but this
is not usually the case. As has been demonstrated
in a number of studies, some bacteria overcome the
chlorine treatment and survive to create subsequent
public health problems. In particular, MARB isolated
in Oman have been shown to resist the chlorination
process and remain viable in tertiary treated sewage effluents from hospitals and industries [2,24].
It has been shown that MARB from sewage treatment plants treating waste from industrial sources
are more resistant to higher chlorine concentrations
than those from hospital sources [25]. It has been
reported that water taken from the Gomti River in
India used for human consumption still has MARB,
even after chlorination [26].
The disinfection efficiency during treatment plays an
important role in the maintenance of water quality
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in the effluent [7]. However, even if the majority of

bacteria are eliminated, those that survive re-grow
in the downstream distribution system. MARB were
isolated from drinking water in distribution systems
and household storage tanks [13]. Other investigators reported extensive growth in chlorinated sewage effluents of fecal and non-fecal coliforms [27].
It has been shown that coliforms survived chlorination in a treated water distribution system and that
the maintenance of 1-2 mg/mL free chlorine was
insufficient to eradicate the growth of coliforms in
the distributed water [7]. Enumeration of bacteria
in effluent from distribution lines used for irrigation
showed that treated sewage had the lowest counts
immediately after chlorination, but that microbial
re-growth increased significantly while chlorine
concentration decreased drastically at the end of
the line and that isolates were resistant to several
antibiotics [1].
The mechanisms by which bacteria develop resistance to chlorine include: (i) modification of cell
surface structures which may lead to increased aggregation or clumping of cells in situ, (ii) formation
of resistant endospores, (iii) microbial adhesion to
pipe surfaces or to suspended particulate matter
such as detritus or clay particles, and (iv) extrusion of
protective extracellular capsular or slime layers [12].
Another factor in the survival and growth of bacteria
downstream from disinfection is the loss of potency
of the chlorine. The effect of chlorine as a function
of time has been examined [21] and shows that
immediately following chlorination, there is a rapid
inactivation of E. coli found in the treated wastewater sample, but that five minutes after addition of
chlorine there was little or no inactivation of E. coli.
This rapid change results from the fact that chlorine
is highly reactive against organic matter [12] and is
rapidly converted from a free to a combined form
due to the presence of exogenous organic matter
in most water treatment systems [21]. Temperature
also affects the biocidal activity of chlorine. At low
temperature chlorine activity decreases [28].

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ISSN 2174-9094

Spread of resistant bacteria

through recycling and reuse of
wastewater
The process of wastewater treatment ideally removes pathogenic organisms from the water and
either removes organics and solids or changes them
into forms that are compatible with the environment. Recycled treated wastewater is either returned to surface waters or reused and this has the
benefit of reducing water demand, specifically in
arid regions [12, 16, 24, 29-30].
Coliform bacteria including E. coli are used as indicators of pathogenic bacteria of enteric origin in
treated water used for irrigation. Routine microbiological analyses of treated wastewater in Oman
have revealed that E .coli is present in numbers exceeding the permitted Omani standards. Therefore
this wastewater poses a threat of contamination to
both groundwater and coastal water. E. coli isolatesfrom the wastewater treatment plant were resistant to several antibiotics commonly used to treat
infections in humans. This presents a public health
problem due to the potential difficulty in treating
infections caused by this bacterium and other antibiotic-resistant pathogens that might be present
[1]. Although antibiotic resistance may be present in
bacteria which are not considered primary pathogens, they remain a threat to public health due to
possibilities of transmittance of resistance to other
microorganisms, especially human pathogens [31].

Antibiotic resistance in the

aquatic environment
As discussed above, there is strong evidence that
antibiotics and antibiotic-resistant bacteria find their
way into the environment. Indeed, resistance to antibiotics in bacteria from different environments is
increasing substantially and becoming a worldwide
concern [1, 32-33]. The profile of antibiotic-sensitive

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bacteria differs significantly from that of the preantibiotic era, with more and more environmental
samples being reported to contain bacteria resistant
to antibiotics [34]. Animals from the wild are exposed to antibiotic residues and bacteria with antibiotic resistance genes and consequently multiple
antibiotic resistances have been found in almost all
species of bacteria that inhabit humans, domestic
animals and wildlife. Antibiotic-resistant bacteria
from sewage effluents have been found to contaminate underground water and this has had a great
impact on terrestrial and aquatic wild life [2, 32-36].
Antibiotic-resistance in the aquatic environment has
received little attention, despite the fact it is a major
problem, with large numbers of resistant bacteria
being found in these ecosystems. Antibiotic-resistant
bacteria have been reported in mammals, birds, turtles and fish. High-level resistance to aminoglycosides
in environmental isolates of enterococci from aquatic
habitats was reported [34]. The overuse of antibiotics, agriculture runoff and coastal development has
resulted in an increase in antibiotic-resistant bacteria isolated from marine habitats. Unfortunately, the
coastal environment has been used as a dumping
ground for sewage and other waste products [36].
As a result, the environment has become a reservoir
for resistant bacteria and provides a return path for
antibiotic resistance genes in bacteria that can infect
both humans and animals [37]. In particular, marine
flora and fauna are exposed to antibiotic residues
and to MARB [1, 32-33, 36, 38-39]. Bacterial isolates
from fish in Chile, contained significantly high rate
of MARB. In Oman, antibiotic-resistant bacteria were
isolated from fish feeding near the dumping sites of
sewage effluent, strongly suggesting that infection
of fish by antibiotic-resistant bacteria is directly related to the treated wastewater exposure [2].
Polluted sewage effluents though agricultural runoff
may also be the source of antibiotic-resistant bacteria isolated from wild sea turtles. MARB have been
isolated from eggs and cloacal fluid of the green
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The International Arabic Journal of Antimicrobial Agents

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turtles, Chelonia mydas [36, 40]. Microbial isolates

from cloacae of the loggerhead turtle (Carettacaretta), had similar high level of MARB [38]. MARB were
isolated from eggs and oviductal fluid, an indication
of contaminated effluents encountered by the sea
turtles during migration and in the feeding areas
near their nesting grounds [24, 36, 38, 40].
Antibiotic resistant bacteria are also associated
with aquaculture. The release of sewage effluents
into seawater is one possible route for transferring
antibiotic-resistant bacteria to aquaculture. It was
demonstrated high levels of individual and multiple
antimicrobial resistance within several groups of
bacteria, including flavobacteria and aeromonads,
associated with aquacultural environments [39].

Antibiotic resistant bacteria

as bio-indicators of aquatic
environmental pollution
The spread of MARB into the aquatic environment
is a serious issue. Antibiotics and MARB enter the
environment via routes as discussed above. Therefore, effluent pollution can be detected by the presence of MARB or antimicrobial agents. The presence of MARB in the aquatic environment has been
investigated by many workers [2, 24, 32, 36, 38-42].
These studies have shown that many aquatic and
marine habitats exposed to antibiotic residues have
developed a significant MARB presence. In short,
the presence of MARB in aquatic habitats can be
used as a bioindicator of pollution [2, 24, 36,42]. In
one application of this concept MARB were isolated
from soil and snails in a pond contaminated with
treated sewage effluent from industrial and residential sources [40]. In another example, the presence
of MARB in tissues of fish caught near the outlet
of a sewage treatment plant, which is a clear indication of treated sewage effluent contaminating
coastal areas [2].
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MARB as bioindicators of pollution from contaminated effluents is an attractive and valuable point,
particularly in the case of ocean pollution. Due to
the low concentrations of pharmaceutical pollutants
in seawater, they are difficult and expensive to detect using current methodologies, whereas detection of MARB is comparatively easy. In addition, it
may not be feasible to survey for the presence of
pharmaceutical compounds in many localities. The
use of MARB in marine animals, such as sea turtles,
as bio-indicators is probably more practical and can
provide an integrated assessment of the extent of
contamination along the turtles migratory routes
[24, 41].
In summary, these investigations induce deep concerns about the dissemination of resistance to antibiotics in marine wildlife. However, they also suggest
that the presence of antibiotic-resistant bacteria in
marine animals such as the green turtle, can be
used for monitoring the degree of pollution in the
turtles feeding grounds along the seashore and in
the wide geographical regions where they migrate.

Implications for human health;

Spread of antibiotic resistant
bacteria to humans from the
environment.
The spread of MARB among pathogenic and commensal bacteria is a global health concern. Each
year worldwide about 17 million people die from
infectious diseases, most of which are caused by
bacteria [43]. The Centers for Disease Control has
stated that in the United States more than two million people are sickened and 23,000 die each year
as a result of antibiotic-resistant infections [44]. Antibiotic resistance can lead to increases in human
and domestic animal health care costs as well as
increased mortality and morbidity [45]. Consumption of contaminated water or food consequently
leads to gastrointestinal tract by various bacterial,

The International Arabic Journal of Antimicrobial Agents

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including E. coli [46]. Antimicrobial resistance in E.

coli is of particular concern because it is the most
common Gram-negative pathogen in humans, the
most common cause of urinary tract infections and
a common cause of both community and hospitalacquired bacteremia. Moreover, the transfer of antibiotic resistance determinants from E. coli to normal
flora of gastrointestinal tract has been reported [47].
Due to the fact that consumption of contaminated
food has been considered the main route of transmission of drug resistance, relatively little attention
has been paid to other routes by which antibiotic
resistance can be disseminated, such as natural water, wastewater and soil environments [48]. Nevertheless, it is clear that MARB in the environment
have serious implications for human health. Not
only can MARB spread to humans from animals, as
previously described, they can also spread from the
environment to humans.
Once established in the environment, resistant
bacteria can infect humans either directly, via reinfection by way of meat, crop or potable water
[9, 49-51].
One major route for transmission of drug resistant
strains to humans involves soil microorganisms,
which are the main producers of antibiotics. The use
of drugs in agriculture adds to their accumulation
in the soil and contributes further to the selection
of soil microbes that carry resistance genes. Such
genes may subsequently be acquired by non-soil
microbes, which can infect animals [52] and thence
humans.
Reservoirs of antibiotic-resistant bacteria are found
not only in domesticated animals but also in wild
animals. Those isolated from wild animals living in
close proximity to human activities are more often
resistant to antibiotics than those isolated from animals living in remote areas. This is a serious concern
because in recent years about 75% of new human
diseases have originated in wildlife (zoonoses) [53].
Surface water contamination with fecal-derived
bacteria, is a health concern. However, groundwa-

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ter contamination is also a serious health problem

[45]. In Ontario, most rural families rely on about
500,000 private wells [54]. About 10% - 34% of
these wells are not within the drinking water standards associated with a high risk of gastrointestinal
illness [55]. Regardless the risks of antimicrobialresistant E. coli in potable water, only a few studies
have been conducted on this topic. MARB in soil
or in water used for irrigation may cause crop contamination [51-56]. It was reported that fresh vegetable crops such as lettuce are important sources
of E. coli outbreaks in humans, although outbreaks
resulting from contaminated meat are more deadly
[51]. A recent study has shown that in the Jordanian
retail markets, fresh leafy vegetables were not contaminated with any type of common diarrheagenic
pathogens, but they were associated with few percentage of multiple antibiotic-resistant E. coli [56]. In
Jordan also, Pseudomonas aeruginosa with relatively similar common antimicrobial resistance pattern
and serotypes were isolated form feces of patients
and in drinking water sources [57].

Antibiotics and MARB in

the environment: Possible
remedies
In Oman, efforts are made to show why and how
MARB arise and why MARB in the environment
is a serious problem. It was reported that better
health care practices and more stringent regulations
should be implemented in order to control the usage of antibiotics and to stop the emergence and
dissemination of multiple resistant strains which are
comparatively similar to the global concerns [2, 4,
41-42].
We suggest the following four major strategies to
reduce the spread of MARB:
(1) E liminate the release of untreated sewage into
the environment;
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The International Arabic Journal of Antimicrobial Agents

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(2) Use antibiotics more prudently in medicine;

(3) Improve sewage treatment technologies to more
efficiently remove antibiotics and MARB and
(4) Curtail the use of antibiotics as growth promoters in food animals.
With regard to points 1 and 2, dumping of raw sewage into rivers, lakes and coastal areas is a serious
health hazard, whether or not antibiotic-resistant
bacteria are present. It should be self-evident that
universal application of sewage treatment would be
a very good thing, though obviously it may be politically and economically difficult to achieve, especially
in less developed countries. Second, antibiotics need
to be more carefully utilized in medicine and veterinary medicine. Greater awareness on the part of
both health professionals and the public of the risks
of improper use and disposal of antimicrobial drugs
will be crucial to decrease the abuse of antibiotics
and to minimize their release, and the release of resistant bacteria, into the environment. In the United
States, it is promising that recent reports from the
Centers for Disease Control and Prevention [44] and
recent actions by the Food and Drug Administration
[58] have gotten wide coverage in the news media
which may help to make the public more aware of
the seriousness of the problem.
The third step toward solving the problem concerns
the effectiveness of wastewater treatment. The
main objective of sewage treatment is to remove
pollutants and produce environmentally safe water
for disposal or recycling and sludge that is suitable
for reuse as fertilizer. The treatment procedures include physical, chemical, and biological processes.
However, it is clear that current methods for the
treatment of sewage are not adequate, since both
antibiotics and resistant bacteria can be found in
the effluents.
Some new technologies that have potential for
more efficient waste treatment are essential. Note
that an important part of sewage water purification
in the future will be monitoring the influence of the
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process on the antimicrobial susceptibility profiles of

bacterial indicators that could spread to the environment and to humans [59].
Reverse osmosis for the treatment of municipal
sewage effluent has been available for several decades [60]. Reverse osmosis has the advantages
that it can produce clean water from chlorinated,
filtered, secondary sewage effluent on a large scale
[61] and the recovery rate for reclaimed water can
reach 98% [62]. However, even though reverse osmosis produces more environmentally acceptable
water than conventional sewage treatment plants,
several obstacles currently make its use impractical.
These obstacles include membrane fouling, pH of
the feed effluent, the high cost of reverse osmosis membranes and the economics related to high
energy-input [61-62].
Nanotechnology for water reclamation may play an
important role in the future for water and food security [63]. Several nanotechnology procedures and
applications have been tested for their efficacy in
treating contaminated effluents. New membranes
are being introduced that involve the use of catalysts made of nanomaterials for the breakdown
of toxic compounds in water. These nanomaterials
include zeolites and carbon compounds, bimetallic nanoparticles and mixed oxides [64]. Emerging
nanotechnology applications to wastewater treatment may therefore replace inefficient conventional
methods. Photodialysis is one of the emerging technologies whereby light sensitive organic matter and
microbes can be treated [32, 65].
Photo-catalysis was used effectively to degrade certain antibiotics and other pharmaceuticals in aqueous environment using combination of titanium
oxide and ultraviolet light. However, the presence
of organic compounds inhibits photo-catalytic degradation of some antimicrobial compounds such as
sulfamethoxazole [65]. Also, frequency and light
intensity are important factors in photodecomposition. Photodecomposition is not effective in turbid water, sewage, sewage pipes and soil [32]. This

The International Arabic Journal of Antimicrobial Agents

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technology may be improved by combining the

composite photo-catalytic membranes and nanomembrane separation technologies [66].
The fourth major step needed to reduce MARB in
the environment concerns the use of antibiotics as
growth promoters in chickens, fish, cattle and other
food animals. The use of antibiotics as feed additives for food animals should be phased out, because it is ultimately detrimental to human health.
Another reason to curtail or eliminate the use of
antibiotics in this way is that as resistant strains arise
and are selected, the drugs will inevitably become
less effective. A decline in the growth-promotion
response of pigs to antimicrobial agents, and this
decline was associated with the presence of bacteria having increased resistance to the agents that
were used [67]. In Denmark, it has been possible to
reduce the usage of antimicrobial agents for foodanimals significantly and in general this has led to
decreases in the prevalence of resistance [68]. It has
been noted that when the antibiotics are not used
at all, resistance is generally not observed. E. coli
isolates from chickens in Jamaica were not resistant
to gentamycin because it is not used in livestock
there [69].
In general, Europe has been quicker to adopt limitations on the use of antibiotics as growth promoters than the United States [70]. However, in the
United States some progress is being made. Though

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tenaciously opposed by farmers and pharmaceutical manufacturers, the Food and Drug Administration (FDA) prohibited the use of fluoroquinolones
in poultry in 2005 and has recently adopted some
restrictions on the use of cephalosporins [58, 70].
Although these steps have been criticized as inadequate [71], there is hope that with increased awareness of the seriousness of the problem [44], further
progress will be forthcoming.

Conclusion
MARB and other pollutants are rapidly increasing
in aquatic and terrestrial habitats at an alarming
rate. It is clear that strategies must be developed
and implemented internationally to avoid dumping
residues of various antibiotics and other pharmaceuticals directly into the environment. Stringent sets
of rules and regulations will be required to prevent
direct sewage drainage into the aquatic and terrestrial habitats. Examination of these effluents for
the presence of MARB, heavy metals and other
contaminants would reflect the effectiveness of the
waste treatment. Since MARB are relatively easily
detected, this means that the presence of MARB
in wildlife and environmental samples can be used
as a biological indicator to monitor the degree of
environmental pollution.

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The International Arabic Journal of Antimicrobial Agents

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