Antibiotic Resistance and Gene Transfer Studies        2009 -- 1946   (161+ papers)

These studies show antibiotic resistant bacterial research has been in progress since 1946.
EPA's Mark Meckes documented 28 years ago that UV light disinfection  in a wastewater
treatment plant amplified antibiotic resistance in bacteria released to the environment. EPA
is also aware that chlorine create antibiotic resistance in water treatment plants. Yet, these
studies do not seem to be in EPA's data based. Of course, EPA doesn't seem to be aware
that 30 gram negative bacteria enumerated in the coliform test cause about half of all
hospital acquired infections, but it still promotes the spreading of these bacteria as near as
can be to humans and animals.

Japanese scientists were the first to really focus on antibiotic resistance in bacteria. The
trend has been to focus on misuse of drugs by doctors and farmers as the cause of the
growing multi-drug resistant epidemic. However, bacteria exposed to chemicals, drugs and  
metals also develop double resistance. Research has documented the amplification of
antibiotic resistant bacteria in the sewage treatment plants as well as drinking water
treatment plants and the human or animal gut

When the Family Enterobacteriaceae (enteric bacteria) was chosen in 1914 to represent
potential human fecal contamination in the Coliform test for water by the Public Health
Service, only one member of the Family, Bacillus coli (E. coli)  was known to cause disease
and grow at an elevated temperature of 46 deg. C. (114.8 deg. F). This
 bacteria in a
stressed state was chosen to represent the confirmation of human fecal contamination by
what is now referred to as the fecal coliform test.

As the research studies show, the transfer of genetic material between members of the
Family Enterobacteriaceae was readily achieved in the laboratory. Since Fred Griffith's
1928 experiment documenting a dead toxin producing bacteria could combine with a live
nontoxin producing bacteria to produce disease, E. coli has become the work horse of the
recombinant DNA industry.  In the beginning scientists used penicillin to search out mutant
bacteria with the resistant gene to work with. Later, scientists inserted resistant genes to
confirm DNA transfer in newly created chimera bacteria as well as in genetically engineered
crops. Today, at least 30 members of Family Enterobacteriaceae (coliform) produce toxins
to create disease in humans.

Human and animal exposure to recombinant antibiotic resistant bacteria may be through
treated sewage sludge biological solids (biosolids) used as a fertilizer, treated sewage
effluent (reclaimed-recycled water) used for irrigation of food crops and treated drinking
The Rise of Antibiotic-Resistant Infections

2009 -- Mechanisms of Infectious Disease • Fall 2009, Lecture 2
2010 --
Propensity of activated sludge to amplify or attenuate tetracycline resistance genes
and tetracycline resistant bacteria: A mathematical modeling approach
The overall goal of this study was to quantify the propensity of the activated sludge (AS)
process at three wastewater treatment plants (WWTP) to amplify or attenuate tetracycline
resistant bacteria (TRB) and tetracycline resistance genes (TRG). Accordingly, the
abundance and fraction of TRB and seven TRG in different unit operations of these WWTP
were analytically measured and modeled using a mass balance approach widely used for
AS design. Based on the model, the AS process of the different WWTP neither amplified nor
attenuated the TRB and TRG fractions. Of the TRG tested, the ribosomal protection genes,
tet(O) and tet(W) were the most abundant, along the treatment train of the WWTP, on all
sampling dates and sampling locations. Significant amounts of TRB and TRG were
discharged in the effluent streams. Notably, in selected samples, the fraction of TRB
increased in response to ultraviolet disinfection of treated wastewater compared to
chlorination. This study therefore implicates wastewater treatment processes as significant
point sources of tetracycline resistance determinants to the environment, and provides a
mathematical basis to compute the production capacity of these determinants in the AS

2009 --  Prevalence of Antibiotic Resistance in Drinking Water Treatment and Distribution
The occurrence and spread of antibiotic-resistant bacteria (ARB) are pressing public health
problems worldwide, and aquatic ecosystems are a recognized reservoir for ARB. We used
culture-dependent methods and quantitative molecular techniques to detect and quantify
ARB and antibiotic resistance genes (ARGs) in source waters, drinking water treatment
plants, and tap water from several cities in Michigan and Ohio. We found ARGs and
heterotrophic ARB in all finished water and tap water tested, although the amounts were
small. The quantities of most ARGs were greater in tap water than in finished water and
source water. In general, the levels of bacteria were higher in source water than in tap
water, and the levels of ARB were higher in tap water than in finished water, indicating that
there was regrowth of bacteria in drinking water distribution systems. Elevated resistance to
some antibiotics was observed during water treatment and in tap water. Water treatment
might increase the antibiotic resistance of surviving bacteria, and water distribution systems
may serve as an important reservoir for the spread of antibiotic resistance to opportunistic
Applied and Environmental Microbiology, September 2009, p. 5714-5718, Vol. 75, No. 17

2009 -- Antibiotic Resistant Bacteria Found In Fertilizer
Acta Veterinaria Scandinavica 2009, 51:24

2009 -- Antibiotic resistance genes in water environment
Abstract  The use of antibiotics may accelerate the development of antibiotic resistance
genes (ARGs) and bacteria which shade health risks to humans and animals. The emerging
of ARGs in the water environment is becoming an increasing worldwide concern. Hundreds
of various ARGs encoding resistance to a broad range of antibiotics have been found in
microorganisms distributed not only in hospital wastewaters and animal production
wastewaters, but also in sewage, wastewater treatment plants, surface water, groundwater,
and even in drinking water. This review summarizes recently published information on the
types, distributions, and horizontal transfer of ARGs in various aquatic environments, as well
as the molecular methods used to detect environmental ARGs, including specific and
multiplex PCR (polymerase chain reaction), real-time PCR, DNA sequencing, and
hybridization based techniques.
Applied Microbiology and Biotechnology, Volume 82, Number 3 / March, 2009

2009 -- Occurrence and Antibiotic Resistance of Escherichia coli O157:H7 in a Watershed
in North-Central Indiana
Published in J Environ Qual 38:997-1004 (2009)

2009 -- Staphylococcus aureus, MRSA, methicillin, β-lactam, SCCmec, spa typing, Panton
Valentine leukocidin, PVL, antibiotic resistance, antibiogram
parentRecord=diva2:211479&searchId=null&pid=diva2:217651 http://en.scientificcommons.

2009 -- Antibiotic susceptibility of thermo-tolerant Escherichia coli 2 isolated from drinking
water of Khairpur City, Sindh, Pakistan.
Pak J Biol Sci. 2009 Apr 15;12(8):648-52.

2009 -- Wastewater treatment contributes to selective increase of antibiotic resistance
among Acinetobacter spp.
The occurrence and spread of multi-drug resistant bacteria is a pressing public health
problem. The emergence of bacterial resistance to antibiotics is common in areas where
antibiotics are heavily used, and antibiotic-resistant bacteria also increasingly occur in
aquatic environments. The purpose of the present study was to evaluate the impact of the
wastewater treatment process on the prevalence of antibiotic resistance in Acinetobacter
spp. in the wastewater and its receiving water. During two different events (hightemperature,
high-flow, 31 °C; and low-temperature, low-flow, 8 °C), 366 strains of Acinetobacter spp.
were isolated from five different sites, three in a wastewater treatment plant (raw influent,
second effluent, and final effluent) and two in the receiving body (upstream and downstream
of the treated wastewater discharge point). The antibiotic susceptibility phenotypes were
determined by the disc-diffusion method for 8 antibiotics, amoxicillin/clavulanic acid (AMC),
chloramphenicol (CHL), ciprofloxacin (CIP), colistin (CL), gentamicin (GM), rifampin (RA),
sulfisoxazole (SU), and trimethoprim (TMP). The prevalence of antibiotic
resistance in Acinetobacter isolates to AMC, CHL, RA, and multi-drug (three antibiotics or
more) significantly increased (pb0.01) from the raw influent samples (AMC, 8.7%; CHL,
25.2%; RA, 63.1%; multi-drug, 33.0%) to the final effluent samples (AMC, 37.9%; CHL,
69.0%; RA, 84.5%; multi-drug, 72.4%), and was significantly higher (pb0.05) in the
downstream samples (AMC, 25.8%; CHL, 48.4%; RA, 85.5%; multi-drug, 56.5%) than in
the upstream samples (AMC, 9.5%; CHL, 27.0%; RA, 65.1%; multi-drug, 28.6%). These
results suggest that wastewater treatment process contributes to the selective increase of
antibiotic resistant bacteria and the occurrence of multi-drug resistant bacteria in aquatic
Science of the Total Environment 407 (2009) 3702–3706

2009 -- Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease
in sub-Saharan Africa have a distinct genotype
Genome Res. 2009. 19: 2279-2287

2009 -- Co-selection of Mercury and Antibiotic Resistance in Sphagnum Core Samples
Dating Back 2000 Years
Geomicrobiology Journal, 26:238–247, 2009

2009 -- Characterization of metal and antibiotic resistance in bacterial population isolated
from a Copper mining industry
IJIB, 2009, vol. 6, No. 2, 57

2009 -- Resistance Variations of Third Generation of Cephalosporins in Some of the
Enterobacteriaceae Members in Hospital Sewage
Int. J. Agri. Biol., 11: 93–96

2009 -- Vancomycin resistant enterococci (VRE) in Swedish sewage sludge

2009 -- Tetracycline Resistance Genes and Tetracycline Resistant Lactose-Fermenting
Enterobacteriaceae in Activated Sludge of Sewage Treatment Plants
Environ. Sci. Technol., 2009, 43 (10), pp 3455–3460

2009 -- Screening for antibiotic-resistant bacteria in drinking water
European Commission, Environment DG Jun. 15, 2009

2009 -- A seasonal study of the mecA gene and Staphylococcus aureus including methicillin-
resistant S. aureus in a municipal wastewater treatment plant
Water Research Volume 43, Issue 4, March 2009, Pages 925-932
23999569995% 23942072%

2009 -- Release of the Final Report of the Advisory Committee on Animal Uses of
Antimicrobials and Impact on Resistance and Human Health - Canada

2008 -- A seasonal study of the mecA gene and Staphylococcus aureus including methicillin-
resistant S. aureus in a municipal wastewater treatment plant
water research 4 3 ( 2 0 0 9 ) 9 2 5 – 9 3 2

2008 -- Detection of Resistance to Macrolides in Thermotolerant Campylobacter Species by
Fluorescence In Situ Hybridization
Journal of Clinical Microbiology, November 2008, p. 3842-3844, Vol. 46, No. 11

2008 -- Heavy Metal Tolerance in Stenotrophomonas maltophilia
PLoS ONE 3(2): e1539.

2008 -- Characterization of Antimicrobial Resistance and Class 1 Integrons in
Enterobacteriaceae Isolated from Mediterranean Herring Gulls (Larus cachinnans)
Microbial Drug Resistance. June 2008, 14(2): 93-99.

2008 -- Prevalence and Mechanisms of Broad-Spectrum β-Lactam Resistance in
Enterobacteriaceae: a Children's Hospital Experience
Antimicrobial Agents and Chemotherapy, November 2008, p. 3909-3914, Vol. 52, No. 11

2008 -- Prevalence of Silver Resistance in Bacteria Isolated from Diabetic Foot Ulcers and
Efficacy of Silver-Containing Wound Dressings
OWM, VOLUME: 54, Issue Number: 3 (March 2008)

2007 -- Multiple Antimicrobial Resistance in Plague:
PLoS ONE 2(3): e309.

2007 -- Toxicogenomic Response to Chlorination Includes Induction of Major Virulence
Genes in Staphylococcus aureus
Environ. Sci. Technol. 2007, 41, 7570-7575

2007 -- Antimicrobial Drug–Resistant Escherichia coli from Humans and Poultry Products,
Minnesota and Wisconsin, 2002–2004

2007 -- Extended-Spectrum -Lactamases (ESBLs), Food, and Caphalosporin Use in Food

2007 -- Elimination of Indicators (TC, FC, FS) and Enterobacteriaceae Family Bacteria
During the Sewage Treatment Process
Polish Journal of Natural Science, Volume 22, Number 2 / June 2007

2007 -- Novel Tetracycline Resistance Determinant Isolated from an Environmental Strain of
Serratia marcescens
Appl Environ Microbiol. 2007 April; 73(7): 2199–2206.

2007 -- Novel Method for Rapid Assessment of Antibiotic Resistance in Escherichia coli
Isolates from Environmental Waters by Use of a Modified Chromogenic Agar
Appl Environ Microbiol. 2007 April; 73(7): 2224–2229.

2006 -- Municipal Wastewater Treatment: A Novel Opportunity to Slow the Proliferation of
Antibiotic-Resistant Bacteria?

2006 -- Frequency of transferable multiple antibiotic resistance amongst coliform bacteria
isolated from a treated sewage effluent in Antofagasta, Chile

2006 -- Serogroups of Escherichia coli from Drinking Water

2006 -- Frequency of transferable multiple antibiotic resistance amongst coliform bacteria
isolated from a treated sewage effluent in Antofagasta, Chile

2006 -- Antibiotic Resistance Genes as Emerging Contaminants: Studies in Northern
Environ. Sci. Technol., 2006, 40 (23), pp 7445–7450

2006 -- Lead, tin, and multiple antibiotic resistant Pseudomonas spp. isolated from polluted
Toxicity Assessment, Volume 2 Issue 4, Pages 377 - 386

2005 -- Persistence of Resistant Staphylococcus epidermidis after Single Course of
Emerging Infectious Diseases, Vol. 11, No 9, Nov 2005; p. 1389

2005 -- Environmental Contamination with Vancomycin-Resistant Enterococci from Hospital
Sewage in Portugal

2005 --
Plasmid Donor Affects Host Range of Promiscuous IncP-1ß Plasmid pB10 in an
Activated-Sludge Microbial Community
Horizontal transfer of multiresistance plasmids in the environment contributes to the growing
problem of drug-resistant pathogens. Even though the plasmid host cell is the primary
environment in which the plasmid functions, possible effects of the plasmid donor on the
range of bacteria to which plasmids spread in microbial communities have not been
investigated. In this study we show that the host range of a broad-host-range plasmid within
an activated-sludge microbial community was influenced by the donor strain and that
various mating conditions and isolation strategies increased the diversity of transconjugants
detected. To detect transconjugants, the plasmid pB10 was marked with lacp-rfp, while rfp
expression was repressed in the donors by chromosomal lacIq. The phylogeny of 306
transconjugants obtained was determined by analysis of partial 16S rRNA gene sequences.
The transconjugants belonged to 15 genera of the - and -Proteobacteria. The phylogenetic
diversity of transconjugants obtained in separate matings with donors Pseudomonas putida
SM1443, Ralstonia eutropha JMP228, and Sinorhizobium meliloti RM1021 was significantly
different. For example, the transconjugants obtained after matings in sludge with S. meliloti
RM1021 included eight genera that were not represented among the transconjugants
obtained with the other two donors. Our results indicate that the spectrum of hosts to which
a promiscuous plasmid transfers in a microbial community can be strongly influenced by the
donor from which it transfers
Applied and Environmental Microbiology, September 2005, p. 5309-5317, Vol. 71, No. 9

2005 -- Antibiotic resistance of bacteria in raw and biologically treated sewage and in
groundwater below leaking sewers
Abstract  More than 750 isolates of faecal coliforms (>200 strains), enterococci (>200
strains) and pseudomonads (>340 strains) from three wastewater treatment plants (WTPs)
and from four groundwater wells in the vicinity of leaking sewers were tested for resistance
against 14 antibiotics. Most, or at least some, strains of the three bacterial groups, isolated
from raw or treated sewage of the three WTPs, were resistant against penicillin G, ampicillin,
vancomycin, erythromycin, triple sulfa and trimethoprim/sulfamethoxazole (SXT). Only a few
strains of pseudomonads or faecal coliforms were resistant against some of the other tested
antibiotics. The antibiotic resistances of pseudomonads, faecal coliforms and enterococci
from groundwater varied to a higher extent. In contrast to the faecal coliforms and
enterococci, most pseudomonads from all groundwater samples, including those from non-
polluted groundwater, were additionally resistant against chloramphenicol and SXT.
Pseudomonads from sewage and groundwater had more multiple antibiotic resistances than
the faecal coliforms or the enterococci, and many pseudomonads from groundwater were
resistant to more antibiotics than those from sewage. The pseudomonads from non-polluted
groundwater were the most resistant isolates of all. The few surviving faecal coliforms in
groundwater seemed to gain multiple antibiotic resistances, whereas the enterococci lost
antibiotic resistances. Pseudomonads, and presumably, other autochthonous soil or
groundwater bacteria, such as antibiotic-producing Actinomyces sp., seem to contribute
significantly to the gene pool for acquisition of resistances against antibiotics in these
Applied Microbiology and Biotechnology, Volume 69, Number 1 / November, 2005

2004 -- Vancomycin-resistant Staphylococcus aureus--New York, 2004.
MMWR Morb Mortal Wkly Rep.  2004; 53(15):322-3

2004 -- Human intestinal bacteria as reservoirs for antibiotic resistance genes
TRENDS in Microbiology Vol.12 No.9 September 2004

2004 -- Antibiotic multiresistance plasmid pRSB101 isolated from a wastewater treatment
plant is related to plasmids residing in phytopathogenic bacteria and carries eight different
resistance determinants including a multidrug transport system.
Microbiology. 2004 Nov;150(Pt 11):3613-30

2004 -- Increased frequency of drug-resistant bacteria and fecal coliforms in an Indiana
Creek adjacent to farmland amended with treated sludge
Canadian Journal of Microbiology, Volume 50, Number 8, 1 August 2004 , pp. 653-656

2003 -- Bacteria learn antibiotic resistance in the sludge
The sludge in wastewater treatment plants could be where bacteria 'learn' to overcome
antibiotics through a natural process of genetic engineering, which might explain the rapid
evolution of multidrug-resistant strains.
A natural genetic engineering device called the integron allows diverse species of Gram-
negative bacteria to exchange and accumulate entire libraries of useful genes. The process
is central to the evolution of antibiotic resistance, say microbiologists, and wastewater
treatment plants, where different bacteria and antibiotics congregate, could be where the
exchange is occurring.
Bacteria residing in the sludge of a municipal water treatment plant contain integron-specific
DNA sequences, says Alfred Pühler, a microbiologist at the University of Bielefeld in
Germany. Such sequences are virtually absent from soil samples, he says, so their
presence in this environment indicates that sludge is "a specific location where genes are
coming together and being distributed."

2003 -- Antibiotic resistance of E. coli in sewage and sludge
The aim of the study is the evaluation of resistance patterns of E. coli in wastewater
treatment plants without an evaluation of basic antibiotic resistance mechanisms.
Investigations have been done in sewage, sludge and receiving waters from three different
sewage treatment plants in southern Austria. A total of 767 E. coli isolates were tested
regarding their resistance to 24 different antibiotics. The highest resistance rates were
found in E. coli strains of a sewage treatment plant which treats not only municipal sewage
but also sewage from a hospital.
Among the antimicrobial agents tested, the highest resistance rates in the penicillin group
were found for Ampicillin (AM) (up to 18%) and Piperacillin (PIP) (up to 12%); in the
cephalosporin group for Cefalothin (CF) (up to 35%) and Cefuroxime-Axetil (CXMAX) (up to
11%); in the group of quinolones for Nalidixic acid (NA) (up to 15%); and for
Trimethoprime/Sulfamethoxazole (SXT) (up to 13%) and for Tetracycline (TE) (57%).
Median values for E. coli in the inflow (crude sewage) of the plants were between 2.0×104
and 6.1×104 CFU/ml (Coli ID-agar, BioMerieux 42017) but showed a 200-fold reduction in
all three plants in the effluent. Nevertheless, more than 102 CFU E. coli/ml reached the
receiving water and thus sewage treatment processes contribute to the dissemination of
resistant bacteria in the environment.
Water Research
Volume 37, Issue 8, April 2003, Pages 1685-1690

2003 -- Antimicrobial, heavy metal resistance and plasmid profile of coliforms isolated from
nosocomial infections in a hospital in Isfahan, Iran
African Journal of Biotechnology Vol. 2 (10), pp. 379-383, October 2003

2003 -- Long-Term Persistence of Resistant Enterococcus Species after Antibiotics To
Eradicate Helicobacter pylori
Ann Intern Med, September 16, 2003 vol. 139 no. 6 483-487

2003 -- Trends in Antimicrobial Susceptibilities among Enterobacteriaceae Isolated from
Hospitalized Patients in the United States from 1998 to 2001
Antimicrobial Agents and Chemotherapy, May 2003, p. 1672-1680, Vol. 47, No. 5

2003 -- Antimicrobial Resistance Markers of Class 1 and Class 2 Integron-bearing
Escherichia coli from Irrigation Water and Sediments

2003 -- genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance
Nature 426, 306-310 (20 November 2003)

2003 -- Significance of antibiotics in the environment
Pharmaceuticals are designed to stimulate a physiological response in humans, animals,
bacteria or other organisms. During the past decade, concern has grown about the adverse
effects the use and disposal of pharmaceuticals might potentially have on human and
ecological health.
Research has shown that after passing through wastewater treatment,
pharmaceuticals, amongst other compounds, are released directly into the environment.1
The selection and development of antibiotic-resistant bacteria is one of the greatest
concerns with regard to the use of antimicrobials.2–5 In a report by the House of Lords, it is
stated that: ‘resistance to antibiotics and other anti-infective agents constitutes a major
threat to public health and ought to be recognized as such more widely than it is at present’.
4 Therefore, the European Union (EU) recommends the prudent use of antimicrobial agents
in human medicine.2 With respect to the causes of resistance, the focus is on the use of
antimicrobials in hospitals, by medical practitioners, i.e. in prescriptions2 and in animal
husbandry. ‘...Coordination between human, veterinary and environment sectors should be
ensured and the magnitude of the relationship between the occurrence of antimicrobial
resistant pathogens in humans, animals and the environment should be further clarified...’.2
However, very little is known about their contribution to the level of bacterial resistance in
the environment and its significance. Also, surprisingly, little is known about the extent of
environmental occurrence, transport, and ultimate fate and effects of pharmaceuticals in
general, as well as of antibiotics in particular.1
Journal of Antimicrobial Chemotherapy (2003) 52, 5-7

2002 -- Mechanisms of antibiotic resistance in bacterial biofilms
International Journal of Medical Microbiology, Volume 292, Issue 2, 2002, Pages 107-113

2002 -- Occurrence and reservoirs of antibiotic resistance genes in the environment
January 2002 - Volume 13 - Issue 1 - pp 15-27

2002  -- Multiple Mechanisms of Antimicrobial Resistance in Pseudomonas aeruginosa: Our
Worst Nightmare?
Clinical Infectious Diseases 2002;34:634–640

2002 -- The fate of antibiotic resistance marker genes in transgenic plant feed material fed
to chickens

2002 -- Antibiotic resistance in soil and water environments.
Seven locations were screened for antibiotic-resistant bacteria using a modified agar
dilution technique. Isolates resistant to high levels of antibiotics were screened for r
plasmids. Low-level resistance (25 micro g x ml(-1)) was widespread for ampicillin, penicillin,
tetracycline, vancomycin and streptomycin but not for kanamycin. Resistant populations
dropped sharply at high antibiotic levels, suggesting that intrinsic non-emergent
mechanisms were responsible for the multiple drug resistance exhibited at low doses. Dairy
farm manure contained significantly (P < 0.01) more (%) resistant bacteria than the other
sites. Bacteria isolated from a dairy water canal, a lake by a hospital and a residential
garden (fertilized by farm manure) displayed resistance frequencies of 77, 75 and 70%,
respectively. Incidence of tetracycline resistance was most prevalent at 47-89% of total
bacteria. Out of 200 representative isolates analyzed, Pseudomonas, Enterococcus-like
bacteria, Enterobacter and Burkholderia species constituted the dominant reservoirs of
resistance at high drug levels (50-170 micro g x ml(-1)). Plasmids were detected in only 29%
(58) of these bacteria with tetracycline resistance accounting for 65% of the plasmid pool.
Overall, resistance trends correlated to the abundance and type of bacterial species
present in the habitat. Environmental reservoirs of resistance include opportunistic
pathogens and constitute some public health concern.
Int J Environ Health Res. 2002 Jun;12(2):133-44.

2001 -- Occurrence and Diversity of Tetracycline Resistance Genes in Lagoons and
Groundwater Underlying Two Swine Production Facilities
Applied and Environmental Microbiology, April 2001, p. 1494-1502, Vol. 67, No. 4

2001 -- The Use of Antibiotic Resistance Markers to Develop Biotech Crops

2000 -- Antibiotic resistance trends in enteropathogenic bacteria isolated in 1985-1987 and
1995-1998 in Barcelona.
Antimicrob Agents Chemother. 2000 May;44(5):1140-5

1999 -- Antimicrobial susceptibility of Enterobacteriaceae isolated from vegetables
J Antimicrob Chemother. 1999 Apr;43(4):503-9.

1998 -- Emergence of Multidrug-Resistant Salmonella enterica SerotypeTyphimurium
DT104 Infections in the United States
NEJM, Volume 338:1333-1339, Number 19, May 7, 1998

1998 -- The Challenge of Antibiotic Resistance
Scientific American March 1998

1998 -- Antibiotic Resistance in Acinetobacter spp. Isolated from Sewers Receiving Waste
Effluent from a Hospital and a Pharmaceutical Plant

1997 -- Association of multiple-antibiotic-resistance profiles with point and nonpoint sources
of Escherichia coli in Apalachicola Bay
Appl. Environ. Microbiol., 07 1997, 2607-2612, Vol 63, No. 7

1994 -- Plasmids designed to alter the antibiotic resistance expressed by insertion
mutations in Bacillus subtilis, through in vivo recombination.

1994 -- Transfer of multiple drug resistance plasmids between bacteria of diverse origins in
natural microenvironments.
Plasmids harboring multiple antimicrobial-resistance determinants (R plasmids) were
transferred in simulated natural microenvironments from various bacterial pathogens of
human, animal, or fish origin to susceptible strains isolated from a different ecological niche.
R plasmids in a strain of the human pathogen Vibrio cholerae O1 E1 Tor and a bovine
Escherichia coli strain were conjugated to a susceptible strain of the fish pathogenic
bacterium Aeromonas salmonicida subsp. salmonicida in marine water. Conjugations of R
plasmids between a resistant bovine pathogenic E. coli strain and a susceptible E. coli strain
of human origin were performed on a hand towel contaminated with milk from a cow with
mastitis. A similar conjugation event between a resistant porcine pathogenic E. coli strain of
human origin was studied in minced meat on a cutting board. Conjugation of R plasmids
between a resistant strain of the fish pathogenic bacterium A. salmonicida subsp.
salmonicida and a susceptible E. coli strain of human origin was performed in raw salmon on
a cutting board. R plasmids in a strain of A. salmonicida subsp. salmonicida and a human
pathogenic E. coli strain were conjugated to a susceptible porcine E. coli strain in porcine
feces. Transfer of the different R plasmids was confirmed by plasmid profile analyses and
determination of the resistance pattern of the transconjugants. The different R plasmids
were transferred equally well under simulated natural conditions and under controlled
laboratory conditions, with median conjugation frequencies ranging from 3 x 10(-6) to 8 x 10
(-3). The present study demonstrates that conjugation and transfer of R plasmids is a
phenomenon that belongs to the environment and can occur between bacterial strains of
human, animal, and fish origins that are unrelated either evolutionarily or ecologically even
in the absence of antibiotics. Consequently, the contamination of the environment with
bacterial pathogens resistant to antimicrobial agents is a real threat not only as a source of
disease but also as a source from which R plasmids can easily spread to other pathogens
of diverse origins.
Appl Environ Microbiol. 1994 November; 60(11): 4015-4021

1992 -- Transferable antibiotic resistance among thermotolerant coliforms from rural
drinking water in India.
Epidemiol Infect. 1992 Aug;109(1):113-20.

1991 -- Evaluation of an Escherichia coli Host Strain for Enumeration
of F Male-Specific Bacteriophages
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, May 1991, p. 1301-1305 Vol. 57, No. 5

1990 -- Behavior of drug resistant fecal coliforms and R plasmids in a wastewater treatment
Nippon Koshu Eisei Zasshi. 1990 Feb;37(2):83-90.

1990 -- Resistance to metal ions and antibiotics in Escherichia
cob isolated from foodstuffs
J . Med. Microbiol. - Vol. 32 (1990) 223-226

1989 -- Factors Mecting Conjugal Transfer of Plasmids Encoding Mercury
Resistance from Pure Cultures and Mixed Natural Suspensions of Epilithic
Journal of General Microbiology (1989), 135, 409-424

1988 -- The occurrence of antibiotic resistant coliforms in the waste water of a water
treatment plant]
Zentralbl Mikrobiol. 1988;143(6):415-23.

1988 -- Plasmid-Mediated Heavy Metal Resistances
Annual Review of Microbiology, Vol. 42: 717-743 (Volume publication date October 1988)

1986 -- Conjugative Transfer of Staphylococcal Antibiotic Resistance Markers in the
Absence of Detectable Plasmid DNA

1987 -- Characterization of the herbicide-resistance gene bar from Streptomyces
The EMBO Journal vol.6 no.9 pp.2519-2523, 1987

1986 -- The survival of antibiotic-resistant escherichia coli in an activated sludge plant

1986 -- Coincident plasmids and antimicrobial resistance in marine bacteria isolated from
polluted and unpolluted Atlantic Ocean samples.
Appl Environ Microbiol. 1986 June; 51(6): 1285-1292

1985 -- Large Plasmids Associated with Virulence in Shigella Species Have a Common
Function Necessary for Epithelial Cell Penetration

1985 -- Occurrence of multiple-antibiotic-resistant enteric bacteria in domestic sewage and
oxidation lagoons.
Appl Environ Microbiol. 1985 Oct;50(4):930-3

1985 -- Biochemical identification of new species and biogroups of Enterobacteriaceae
isolated from clinical specimens.
J Clin Microbiol. 1985 Jan ;21 (1):46-76 3881471

1984 -- Association of metal tolerance with multiple antibiotic resistance of bacteria isolated
from drinking water.
Appl Environ Microbiol. 1984 June; 47(6): 1238-1242

1984 -- Effect of chlorination on antibiotic resistance profiles of sewage-related bacteria.
Appl Environ Microbiol. 1984 June; 47(6): 1238-1242

1984 -- R-Plasmid Transfer in Salmonella spp. Isolated from Wastewater
and Sewage-Contaminated Surface Waters

1984 -- Transferable resistance to gentamicin and other antibiotics in Enterobacteriaceae
isolates from municipal wastewater.

1983 -- Comparison of Epidemiological Markers Used in the Investigation of an Outbreak of
Methicillin-ResistantStaphylococcus aureus Infections
JOURNAL OF CLINICAL MICROBIOLOGY, Aug. 1983, P. 395-399, Vol. 18, No. 2

1983 -- A Cryptic Plasmid from Shigella sonnei
Journal of’ General Microbiology (1983), 129, 15 13 -1 525. Printed in Great Brituin.

1983 -- Antibiotic Resistance Among Different Species of Fecal Coliforms Isolated from
Water Samples

1983 -- Influence of sewage treatment and urbanization on selection of multiple resistance
in fecal coliform populations.
Appl Environ Microbiol. 1983 July; 46(1): 227-232

1983 -- A chimaeric antibiotic resistance gene as a selectable marker for plant cell

1982 -- The persistence of drug resistant Escherichia coli in the intestinal flora of healthy
broiler chicks.
J Hyg (Lond). 1982 Oct;89(2):269-78.

1982 -- Effect of UV light disinfection on antibiotic-resistant coliforms
in wastewater effluents.
Appl Environ Microbiol. 1982 February; 43(2): 371–377.

1982 -- Antibiotic-Resistant Bacteria in Drinking Water

1982 -- R-plasmid transfer in a wastewater treatment plant.
Appl Environ Microbiol. 1982 December; 44(6): 1395-1403

1982 -- Transposon-Mediated Multiple Antibiotic Resistance in Acinetobacter Strains
ANTIMICROBIAL AGENTS AND CHEMOTHERAPY, Aug. 1982, p. 323-329, Vol. 22, No. 2

1982 -- In Situ Studies with Membrane Diffusion Chambers of Antibiotic Resistance Transfer
in Escherichia coli

1982 -- R-Plasmid Transfer in a Wastewater Treatment Plant

1982 -- Selection of antibiotic-resistant standard plate count bacteria during water treatment.
Appl Environ Microbiol. 1982 August; 44(2): 308-316

1981 -- R factors in coliform-fecal coliform sewage flora of the prairies and Northwest
Territories of Canada.
Coliform and fecal coliform populations found in the raw sewages and final sewage effluents
of the prairie provinces and the Northwest Territories were examined for antibiotic
resistance and the possession of R factors. It was determined that 8.91% of the total
coliform and 10.80% of the fecal coliform populations carried R factors. The following
numbers of combinations of R determinants were found: 39 in the Escherichia coli
population, 6 in the Citrobacter population, 20 in the Enterobacter populations, 10 in the
Klebsiella populations, and 11 in the Aeromonas populations. The maximum number of R
determinants transferable simultaneously was seven; organisms with R factors containing
determinants for chloramphenicol usually contained determinants for ampicillin. Of the
coliform and fecal coliform populations, 2 to 4% were resistant to chloramphenicol in some
provinces, and from 17 to 30% of the populations were resistant to three or more antibiotics.
It was calculated that coliforms containing R factors in the raw sewage reached population
levels of 1.5 X 10(7)/100 ml, and fecal coliforms containing R factors reached population
levels of 8.6 X 10(5) ml. Final effluent discharges to the receiving environment contained R
factor-containing coliform and fecal coliform populations of 3.1 X 10(4)/100 ml and 5.8 X 10
(2)/100 ml, respectively. The incidence of bacteria containing R factors in sewage appears
to be increasing with time, and their removal from sewage before discharge to the receiving
environment is desirable. Consideration of data on bacteria with R factors should be made
in future water quality deliberations and in discharge regulations.
Appl Environ Microbiol. 1981 August; 42(2): 204–210

1981 -- Antibiotic-resistant bacteria in drinking water.
Appl Environ Microbiol. 1981 August; 42(2): 277-283

1981 -- An R plasmid of broad host-range, coding for resistance to nine antimicrobial
agents endemic in Gram-negative nosocomial isolates.
J Med Microbiol. 1981 Nov;14(4):371-80.

1981 -- R-Plasmid Transfer to and from Escherichia coli Strains Isolated from Human Fecal
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, Apr. 1981, p. 959-966 Vol. 41, No. 4

1980 -- R-Plasmid Transfer Frequencies from Environmental Isolates of Escherichia coli to
Laboratory and Fecal Strains
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, Oct. 1980, p. 756-764, Vol. 40, No. 4

1980 -- Antibiotic Resistance and Its Transfer Among Clinical and Nonclinical Klebsiella
Strains in Botanical Environments
Appl Environ Microbiol. 1980 January; 39(1): 97–104.

1980 -- Antibiotic and metal resistance in "Escherichia coli" strains isolated from the
environment and from patients (author's transl)]
Ann Sclavo. 1980 Mar-Apr;22(2):212-26.

1980-- Functional expression in yeast of the Escherichia coli plasmid gene coding for
chloramphenicol acetyltransferase (chloramphenicol resistance/Saccharomyces cerevisiae
transformation/heterologous gene expression)

1980 -- Conjugative Transfer of Multiple Antibiotic Resistance Markers in Streptococcus

1980 -- Spread and transfer of plasmid resistance in Escherichia coli
Antibiotiki. 1980 Jun;25(6):429-32.

1. MED. MICROBI0L.-VOL. 12 (1979)

1979 -- Expansion of the Host Range of Coliphage P1 and Gene Transfer from Enteric
Bacteria to Other Gram-Negative Bacteria

1978 -- Antibiotic Resistance Patterns of Gram-Negative Bacteria Isolated from
Environmental Sources
Funded by: US Army Medical Research and Development Command , Fort Detrick,
Frederick, Maryland


1978 -- Drug-Resistance and Enterotoxigenic Plasmids in Enteropathogenic Bacteria With
Special Reference to Clinical Isolates of San Lazaro Hospital*

1977 -- Mercury Resistance and R Plasmids in Escherichia coli Isolated from Clinical
Lesions in Japan
ANTIMICROBIAL AGENTs AND CHZMOTHERAPY, June 1977, p. 999-1003, Vol. 11, No. 6

1977 --  Replication and expression of plasmids from Staphylococcus aureus in Bacillus
subtilis (DNA/genetic transformation/molecular cloning/biohazards)
Proc. Nat!. Acad. Sci. USA Vol. 74, No. 4, pp. 1680-1682, April 1977

1976 -- Antibiotic Resistance Among Coliform and Fecal Coliform
Bacteria Isolated from Sewage, Seawater, and Marine
ANTIMICROBIAL AGENTS AND CHEMOTHERAPY, June 1976, p. 879-884, Vol. 9, No. 6

1976 -- Arizona hinshawii infections. New cases, antimicrobial sensitivities, and literature
Ann Intern Med. 1976 Nov;85(5):587-92.

1975 -- Antibiotic Resistance Plasmids of Staphylococcus aureus and Their Clinical
BACTEROLOGICAL REVIEWS, Mar. 1975, p. 1-32, Vol. 39, No. 1

1975 -- Epidemiology of Antibiotic and Heavy Metal Resistance in
Bacteria: Resistance Patterns in Staphylococci Isolated from
Populations in Iraq Exposed and Not Exposed to Heavy Metals
or Antibiotics
Vol. 7, No. 5

1974 -- Genome construction between bacterial species in vitro: replication and expression
of Staphylococcus plasmid genes in Escherichia coli.

1974 -- Replication and transcription of eukaryotic DNA in Escherichia coli.

1974 -- Patent application for Recombinant Plasmid Chimera by Cohen and Boyer

1974 -- R Factor Transfer in Rhizobium leguminosarum
Journal of General Microbiology 84 (1974), 188-198;

1973 -- Construction of Biologically Functional Bacterial Plasmids In Vitro
(R factor/restriction enzyme/transformation/endonuclease/antibiotic resistance)

1973 -- Aminoglycoside Antibiotic-Inactivating Enzymes in Actinomycetes Similar to Those
Present in Clinical Isolates of  Antibiotic-Resistant Bacteria (streptomyces/origin of R-

1972 -- Nonchromosomal Antibiotic Resistance in Bacteria: Genetic Transformation of
Escherichia coli by R-Factor DNA*
(CaCI2/extrachromosomal DNA/plasmid)

1972 -- Transfer Among Erwinia spp. and Other Enterobacteria of Antibiotic Resistance
Carried on R Factors -- UC Davis

1971 -- Incidence of Infectious Drug Resistance Among Fecal Coliforms Isolated from Raw
The study reveals that a few coliform are  
E. coli,   Citrobacter group or the Klebsiella- Enterobacter group
while a few fecal coliform are   
E. coli, Citrobacter or Klebsiella- Enterobacter group.
Citrobacter causes drug-resistant hospital acquired urinary tract infections among others
(personal observation)
K. pneumoniae is second only to E. coli as a urinary tract pathogen and a superbug. Of the
34 patients infected at Tisch Hospital in Brooklyn, NY in 2000,
half died.
Enterobacter: several species cause opportunistic infections of the urinary tract as well as
other parts of the body.

1970 -- Genetic Mapping of Antibiotic Resistance in Markers
Bacillus subtilis*

1970 -- Intergeneric Transfer of a -Lactamase Gene between Ps. aeruginosa and E. coli

1970 -- Non-Chromosomal Antibiotic Resistance in Bacteria, III :* Isolation of the Discrete
Transfer Unit of the R-Factor RI
Proceedings of the National Academy of Sciences Vol. 67, No. 2, pp. 510-516, October 1970

1969 -- Incidence of Infectious Drug Resistance Among Lactose-Fermenting Bacteria
Isolated from Raw and Treated Sewage
APPuE MICROBIOLOGY, Nov. 1969, p. 918-924 VoL 18, No. 5

1969 -- R-factor Gene Expression in Gram-negative Bacteria
J . gen. Microbiol. (1969), 55, 109-120

1969 -- Drug Resistance and R Factors in the Bowel Bacteria of London Patients before
and after Admission to Hospital
British Medical Journal, 1969, 2, 407-411

1968 -- R (Transmissible Drug-resistance) Factors in Salmonella typhimurium: Pattern of
Transduction by Phage P22 and Ultraviolet-protection Effect
Journal of General Microbiology 53 (1968), 109-123; DOI 10.1099/00221287-53-1-109

1967 -- Drug Resistance of Enteric Bacteria IX. Distribution of R Factors in Gram-negative
Bacteria from Clinical Sources
J Bacteriol. 1967 April; 93(4): 1242-1245

1966 -- Drug Resistance of Enteric Bacteria
VI. Introduction of Bacteriophage P1CM into Salmonella typhi and Formation
of PldCM and F-CM Elements
JOURNAL OF BACTERIOLOGY, May, 1966, Vol. 91, No. 5


J. BACTERIOL. VOI,. 86, 1963

J Bacteriol. 1962 July; 84(1): 9–16

1962 -- Transduction of the transmissible drug-resistance factors by bacteriophage Plkc.
Japan. J. Exptl. Med. 32:139-147.

J. BACTERIOL. VtOL. 84, 1962

1961 -- Episome-mediated transfer of drug resistance in Enterobacteriaceae. III.
Transduction of resistance factors.
J. Bacteriol. 82:202-209.

1961 -- Studies on the mechanism of transfer of drug-resistance
in bacteria. IX. Influence of temperature and pH on resistance-transfer. [In Japanese]
Med. Biol. (Tokyo) 60:42-44.

1961 -- Episomic transfer between Salmonella typhosa and Serratia marcescens.
Genetics 46:703-706.

1961 -- On the drug-resistance of enteric bacteria. 5. Mechanisms of
the transmission of the drug-resistance between Shigella and E. coli. [In Japanese] Japan.
J. Bacteriol. 16:6-16.


1960 -- "Resistance transfer factor", an episome in Enterobacteriaceae.
Biochem. Biophys.Res. Commun. 3:660-665.

1960 -- Transduction of lactose-utilizing ability among strains of E. coli and S. dysenteriae
and the properties of the transducing phage particles.
Virology 12:348- 390.

1960 -- On the drug-resistance of enteric bacteria. 2. Transmission of
the drug-resistance among Enterobacteriaceae.Japan.
J. Exptl. Med. 30:289-299.

1959 -- Mechanism of development of resistance in shigella. Medicine of Japan in 1959. [In
Proc. 15th Gen.Meeting of the Japan Med. Assoc. 5:299- 305.

1959 -- Characteristics of a high frequency of recombination (Hfr) strain of Salmonella
typhosa compatible with Salmonella, Shigella and Escherichia species.
Proc. Natl. Acad. Sci. U.S. 45:1752-1757.

1959 -- Hybridization of Salmonella species by mating with Escherichia toll,
Science, 1959, 130, 566

1959 -- Genetic recombination between Escherichia coli and Salmonella typhimurium.
Proc. Natl. Acad. Sci. U.S. 45:976- 984.

1958 -- Recombination ability of Escherichia coli K-12 protoplast.
Nature 182:456-457.

1957 -- The role of the Krebs cycle in conjugation in Escherichia coli K-12.
J. Gen. Microbiol. 16:120-135.

1957 -- Hybridization between Escherichia coli and Shigella,
J. Bact., 1957, 74, 461

1956 -- Conjugation and genetic recombination in Escherichia coli K-12.
Cold Spring Harbor Symp. Quant. Biol. 21:141-162.

One of the most interesting experiments was performed by Rolf Freter,  Stritch School of
Medicine and Graduate School, Loyola University, in 1956. He found that by feeding mice
antibiotics it was possible rid the intestinal tract's normal E. coli flora  and thereby create
long term asymptomatic infections by feeding the mice streptomycin-resistant strains of
Shigella flexneri or Vibrio cholerae.  The most unusual finding was that upon introducing a
streptomycin-resistant strain of E. coli  into the intestinal tract  Shigella flexneri or Vibrio
cholerae were quickly eliminated.

1956 -- Drug-sensitivity of the Shigella strains isolated in 1955.
[In Japanese]
J. Japan. Assoc. Infectious Diseases 30:403-404

1956 -- Linear inheritance in transductional clones.
Genetics 41:845-871.

1955 -- The relationship of bacteriophage to antigenic changes in group E salmonellas.
J. Bacteriol. 69:571-579.

1954 -- Mendelian and non-Mendelian inheritance of streptomycin resistance in
Chlamydomonas reinhardi.
Proc. Natl. Acad. Sci. U.S. 40:356-363.

J Bacteriol. 1953 January; 65(1): 27–36.

First mention of viable bacteria with no growth (VBNC)
1953 -- The Integration of Research on the Nutrition and .Metabolism of Micro -organisms
The Inaugural Marjory Stephenson Memorial Lecture
Journal of General Microbiology. 9 , 151-173.

GENETICS3 7 : 720 November 1952.

Journal of Bacteriology, 1952, VOL. 64

Cold Spring Harb …, 1951

1951 --  Streptomycin resistance: a genetically recessive mutation.
J. Bacteriol. 61:549-550.


1950 -- Studies on nutritionally deficient bacterial mutants isolated by
means of penicillin.
Experientia 6:41-50.

1948 -- Isolation of biochemically deficient mutants of bacteria by penicillin
Journal of the American Chemical Society, 1948

Journal of BACTERIOLOGY, Vol. 63, No. 6, June, 1047 673 - 684


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Jim Bynum, VP
Help for Sewage Victims

Coliform exhibit optimum
growth in  the 20-37° C range
(68 - 98.6°F).  Total Coliform
are gram negative members of
the Family Enterobacteriaceae
that ferment lactose at 98.6°F
to produce gas and/or acid
within 48 hours. Other
of the Family
take a longer time to ferment

Fecal coliform exhibit minimal
growth at an elevated
temperature. They are a few
thermotolerant members of the
Family Enterobacteriaceae that
ferment lactose at 112.1°F  to
produce gas and/or acid within
48 hours.

E. coli and Klebsiella are the
primary fecal coliform that
exhibit less than 5% growth
rate at the elevated
temperature. They act as
opportunistic pathogens when
they are introduced into body
locations where they are not
normally found, especially if
the host is debilitated or

While there may be some
non-pathogenic strains, the
International Escherichia and
Klebsiella Centre (WHO) has a
collection of approximately
60,000 E. coli strains, most of
which are clinical isolates.
Clinical isolates means they
are pathogens associated with
disease.  About half of the
hospital acquired infections
are caused by the coliform