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Prevalence and susceptibility of multiple antimicrobial-resistant Escherichia coli in the Factory Creek watershed, Sumter County, Alabama.

ABSTRACT

The purpose of this research was to determine (i) the prevalence of antimicrobial-resistant Escherichia coli from cattle and surface water in the Factory Creek watershed in Sumter County, and (ii) the susceptibility levels of commonly used antimicrobial agents against E. coli isolated from within the Factory Creek watershed. Factory Creek, which begins southeast of Emelle, AL and travels approximately 14.92 miles to its confluence with the Tombigbee River north of Epes, AL, drains 88 [mi.sup.2] of pastures and forests in Sumter County and is considered a sub-watershed of the Upper Tombigbee River Basin. E. coli from the Factory Creek watershed were assayed for antibiotic resistance using the disc diffusion method with the following classes of antimicrobial agents: aminoglycosides, carbacephems, cephalosporins (1st, 2nd, and 3rd generation), macrolides, penicillins, polypeptides, quinolones, sulfonamides, and tetracyclines. The isolates generated 21 distinct antimicrobial resistance profiles, 2 of which accounted for the majority (53%) of the isolates. Factory Creek isolates displayed 2 unique profiles, while the cattle isolates displayed 18 unique profiles. Overall, the correlation between Factory Creek isolates and cattle isolates was strong, R(19)=0.672, p<0.001; however, the correlation was entirely dependent upon one shared antimicrobial resistance profile which accounted for 75% of the Factory Creek isolates and 25% of the cattle isolates. The results of this study show that 100% of the E. coli recovered from Factory Creek water samples and 75% of the E. coli recovered from cattle were categorized as resistant to the antimicrobial agents tested, confirming concerns about the lack of effectiveness of commonly used antimicrobial agents.

INTRODUCTION

Antimicrobial agents are naturally occurring, semi-synthetic and synthetic compounds with antimicrobial activity that are used in human and veterinary medicine to prevent and treat infections and for growth promotion in food animals. The growth-promoting effects of antimicrobial agents were first discovered in the 1940s when chickens fed by-products of tetracycline fermentation were found to display increased growth rates (Stokestad et al., 1949). Since then, many antimicrobial agents have been found to improve average daily weight gain and feed efficiency in livestock in a variety of applications (Preston, 1987). Whereas some growth-promoting effects are mediated through alterations of the normal intestinal microbiota resulting in more efficient digestion of feed and metabolism of nutrients, others are mediated through the immune system release resulting from suppression of non-resistant pathogens (Gaskins, 2002, Wierup, 2001).

Antimicrobial resistance is as ancient as antimicrobial agents, as it protects both antimicrobial-producing microbes from their own products and competitor microbes from antimicrobial attack in nature. All antimicrobial agents can select for microbes displaying spontaneous resistance as well as mutants that have acquired resistance by transfer from other microbes. These resistant variants can become dominant and spread in host-animal populations with differing clinical implications depending on the characteristics of specific antimicrobial agents. Nevertheless, even low-level resistance, consisting of diminished antimicrobial potency within the clinically susceptible range, may be a first step towards clinical resistance. These considerations have always been important in definitions of rational antimicrobial therapy, and have been re-emphasized by recent calls for prudent therapy in human and veterinary medicine (Levy, 1984). In Europe, this has led to the precautionary banning of several antimicrobial growth promoters (Phillips et al., 2004), a practice which in turn required the increased use of therapeutic antimicrobial agents (Casewell et al., 2003) to prevent the epidemic spread of animal disease and to protect animal welfare.

Most of the antimicrobial resistance studies reported in the literature have examined pathogenic bacteria, such as Salmonella and enterotoxigenic Escherichia coli, or bacteria isolated from clinical cases (Orden, 2000). From record surveillance of these studies, the United States FDA has found that clinical antimicrobial resistance is higher for antimicrobial agents that have been in use longer (FDA, 2010). However, a growing number of antimicrobial resistance studies of non-clinical bacteria collected from environmental sources suggest that the incidence of drug-resistance traits is increasing in commensal bacteria (Institute of Medicine, 1999; Aarestrup et al., 2008). Additionally, it has been shown that strains of E. coli that are found in water and livestock can serve as vectors that pass on antimicrobial resistance to human commensal bacteria (Chaslus-Dancla et al., 1989). For example, apramycin is an aminoglycoside that was introduced in France as a veterinary antimicrobial in the early 1980s. Plasmid-born resistance to apramycin was detected soon after in cattle E. coli, found to transfer to cattle Salmonella (Hunter et al., 1992), and then detected in human E. coli and Salmonella typhimurium (Chaslus-Dancla et al., 1986, Chaslus-Dancla et al., 1989). The possibility of passing more antimicrobial resistance traits from animal bacteria to human bacteria is a serious, ongoing concern (Casewell, 2003).

The purpose of this research was to determine (i) the prevalence of antimicrobial-resistant E. coli from cattle and surface water in the Factory Creek watershed in Sumter County, and (ii) the susceptibility levels of commonly used antimicrobial agents against E. coli isolated from within the Factory Creek watershed. This study was the first to investigate environmental antimicrobial susceptibility in the Factory Creek watershed.

MATERIALS AND METHODS

Study site

Factory Creek (Hydrologic Unit Code 12: 031601060702, latitude: 32.7026333, longitude: - 88.114189) begins southeast of Emelle, AL and travels approximately 14.92 miles to its confluence with the Tombigbee River north of Epes, AL (Fig. 1). The Factory Creek watershed drains 88 mi2 of pastures and forests in Sumter County and is considered a sub-watershed of the Upper Tombigbee River Basin. In accordance with the Clean Water Act of 1972, the Alabama Department of Environmental Management (ADEM) designated Factory Creek with the "Fish and Wildlife" use category, indicating that the water should be of sufficient quality to support fish and wildlife and incidental human contact (CFR, 2000; CFR, 2003).

Sample collection

A reference database of local E. coil antimicrobial resistance profiles was generated from the Factory Creek watershed using previously described methods (Burnes, 2003; Burnes, 2010). E. coil were collected from fresh cattle feces for comparison to E. coil collected from an existing water quality monitoring site at the confluence of Factory Creek and the Tombigbee River (Fig. 1). All samples were placed on ice and returned to the laboratory and processed within 6 hours. Fecal samples were suspended (1 gram/100m1), serially diluted in FC Buffer (3x[10.sup.-4]M [H.sub.2]KP[O.sub.3], 2x[10.sup.-3]M Mg[Cl.sub.2]*6[H.sub.2]0, pH 7.2+/-0.1), and then processed identically to water samples. E. coil were isolated from all samples using ColiScan EasyGel plates (Micrology Labs, Inc., Goshen, Indiana) according to the manufacturer's instructions.

Antimicrobial susceptibility testing

Susceptibility testing was done using the disc diffusion method on Mueller-Hinton agar (Sigma-Aldrich, St. Louis, MO) according to CLSI methods for E. coil (Clinical and Laboratory Standards Institute, 2006). Zones of growth inhibition were measured and interpreted for 19 antimicrobial agents (Sigma-Aldrich, St. Louis, MO) (Table 1). The inhibition zone measurements were interpreted as resistant (R) or susceptible (S) according to CLSI Interpretive Standards for Enterobacteriaceae (Clinical and Laboratory Standards Institute, 2006). These antimicrobial agents were chosen from each commercially available class of antimicrobial agents known to be effective against E. coli.

Table 1. Antimicrobial agents used in this study

                                                    Zone Diameter
                                                         (mm) (3)

Antimicrobial   Code  Disc Potency  Drug Class        Susceptible
Agent                       ug (2)                  [greater than
                                                     or equal to]

Amikacin        AN              30  Aminoglycoside             17

Cefazolin       CZ              30  1st GC (1)                 18

Cefotaxime      CTX             30  3rd GC                     21

Cefoxitin       FOX             30  2nd GC                     26

Ceftazidime     CAZ             30  3rd GC                     18

Ceftriaxone     CRO             30  3rd GC                     21

Cefuroxime      CXM             30  2nd GC                     18

Cephalothin     CF              30  1st GC                     18

Clindamycin     CC               2  Lincosamide                21

Colistin        CL              10  Polymyxin                  11

Doxycyline      D               30  Tetracycline               16

Furazolidone    FX             100  Nitrofuran                  -

Imipenem        IPM             10  Carbapenem                 16

Minocycline     MI              30  Tetracycline               19

Nalidixic Acid  NA              30  Quinolone                  19

Nitrofurantoin  F/M            300  Nitrofuran                 17

Novobiocin      NB              30  Aminocoumerin              22

Oxacillin       OX               1  Penicillin                 13

Polymyxin B     PB             300  Polymyxin                  19

Tobramycin      NN              10  Aminoglycoside             15

                   Interpretive
                      Standards

Antimicrobial   Resistant [less
Agent             than or equal
                            to]

Amikacin                     14

Cefazolin                    14

Cefotaxime                   15

Cefoxitin                    19

Ceftazidime                  14

Ceftriaxone                  13

Cefuroxime                   14

Cephalothin                  14

Clindamycin                  14

Colistin                      8

Doxycyline                   12

Furazolidone                  -

Imipenem                     13

Minocycline                  14

Nalidixic Acid               13

Nitrofurantoin               14

Novobiocin                   17

Oxacillin                    10

Polymyxin B                  15

Tobramycin                   12

(1) GC (Generation Cephalosporin). (2) Disc Potency for
polymyxin B is reported in Units. (3) No CLSI standards
exist for clindamycin or oxacillin against E. coli;
instead, the standards against Staphylococcus are
reported. No CLSI standards exist for furazolidone;
it is included to improve discriminant analysis.


RESULTS

A total of 40 E. coli isolates, consisting of 32 isolates from cattle and 8 from Factory Creek, were collected from the Factory Creek watershed for analysis. All of the Factory Creek isolates and 75% of the cattle isolates displayed resistance to all of the antimicrobial agents tested (Fig. 2 and Table 2). Cattle isolates showed the least resistance (56.25%) to the antimicrobial Imipenem (Ipm). All isolates were resistant to the antimicrobial agents cefazolin (CZ), cefotaxime (CTX), cephalothin (CF), doxycycline (D), nalidixic Acid (NA), and oxacillin (OX). The isolates generated 21 distinct antimicrobial resistance profiles, 2 of which accounted for the majority (53%) of the isolates (Table 3). Factory Creek isolates displayed 2 unique profiles, each containing 1 isolate (12.5% of FC isolates), while the cattle isolates displayed 18 unique profiles, with one profile containing 7 isolates (22% of cattle isolates) and the other 17 profiles each including 1 isolate (3% of cattle isolates). Overall, the correlation between Factory Creek isolates and cattle isolates was strong, R(19)=0.672, p<0.001. However, the correlation was dependent upon the two groups of isolates sharing only one antimicrobial susceptibility profile that accounted for 75% of the Factory Creek isolates and 25% of the cattle isolates.

Table 3. Antimicrobial resistance profiles of E. coli isolates

                                                  Source

Antimicrobial resistance profile           Factory Creek  Cattle

AnCzCtxFoxCazCroCxmCfCcClDMiNaOxOaPbNn                 -       7
AnCzCtxFoxCazCroCxmCfCcClDIpmMiNaOxOaPbNn              6       8
AnCzCtxFoxCazCroCxmCfCcClDIpmMiNaOxOaNn                -       1
AnCzCtxFoxCroCxmCfCcClDIpmNaOxOaPb                     -       1
AnCzCtxFoxCroCxmCfCcDIpmMiNaOxOaPbNn                   -       1
AnCzCtxFoxCazCfCcClDIpmMiNaOxOaPbNn                    -       1
AnCzCtxFoxCazCxmCfCcClDIpmMiNaOxOaPbNn                 -       1
AnCzCtxFoxCazCxmCcClDIpmMiNaOxOaPbNn                   -       1
AnCzCtxFoxCxmCfCcClDMiNaOxOaNn                         -       1
CzCtxFoxCazCroCxmCfCcDIpmMiNaOxOaPbNn                  -       1
AnCzCtxFoxCroCxmCfCcCIDMiNaOxOaPbNn                    -       1
AnCzCtxFoxCazCroCxmCfCcClDMiNaOxOaPb                   -       1
AnCzCtxFoxCroCxmCfCcCIDIpmMiNaOxOaPbNn                 -       1
AnCzCtxCazCxmCfCcClDMiNaOxOaPbNn                       -       1
AnCzCtxFoxCxmCfCcClDMiNaOxOaPbNn                       -       1
AnCzCtxFoxCazCxmCcClDlDmMiNaOxOaPbNn                   -       1
AnCzCtxFoxCroCxmCfCcClDIpmMiNaOxOaPbNn                 -       1
CzCtxFoxCazCxmCfCcClDIpmMiNaOxOaPb                     -       1
AnCzCtxFoxCroCxmCfCcClDIpmMiNaOxOaNn                   -       1
AnCzCtxFoxCazCroCxmCfCcClDIpmMiNaOxPbNn                1       -
AnCzCtxFoxCxmCfCcClDIpmMiNaOxOaPbNn                    1       -


DISCUSSION

This antimicrobial resistance surveillance study consisted of collecting 40 E. coli isolates from the Factory Creek watershed and testing for the prevalence of resistance to 19 antimicrobial agents (Table 2). The strongest antimicrobial resistance seen in cattle was to the antimicrobial agents Cephalothin, Cefazolin, Nalidixic Acid, Oxicillin, Doxycycline, and Cefotaxime. Oxicillin and doxycyline are in the drug classes penicillins and tetracyclines, respectively, and are very widely used because of their relatively low price, availability, and regulatory acceptance (Salauze et al., 1990). Tetracycline, in particular, has been widely used in veterinary therapy and to promote feed efficiency in animal production systems since its approval in 1948 (Tadesse et al., 2012). The lowest resistance to an individual antimicrobial agent seen in isolates from either category was in cattle, of which 56% were resistant to Imipenem. Imipenem is in the drug class carbapenem and is highly restricted in use. The two groups of isolates shared one antimicrobial resistance profile (AnCzCtxFoxCazCroCxmCfCcC1DIpmMiNa0x0aPbNn, Table 3), which accounted for 75% of the Factory Creek isolates and 25% of the cattle isolates. This linkage may explain the origins of part of the bacteria in the Factory Creek watershed and will be the focus of future studies. The results of this study show that 100% of the isolates recovered from Factory Creek water samples and 75% of the isolates recovered from cattle feces were categorized as resistant to the antimicrobial agents tested. The antimicrobial resistance prevalences and resistance levels found in E. coli from the Factory Creek watershed are cause for concern for the potential overuse of antimicrobial agents in the environment.

These results are in concordance with a similar antimicrobial resistance surveillance study showing that farm animals display significant resistance to some antimicrobial agents, including neomycin, streptomycin, tetracycline, ampicillin, and sulfisoxazole (Sayah et al., 2005). The tetracyclines are allowed to be used for growth promotion for swine, poultry, and cattle; livestock species (swine, poultry, cattle) that are routinely exposed for extended periods to subtherapeutic doses of antimicrobial agents exhibited a significantly higher prevalence of resistance than the species (horses) that are typically exposed only to therapeutic doses for brief periods (Bogaard et al., 2001). In addition to antimicrobial agent use for growth promotion or disease prevention, the use of these agents for disease treatment contributes to the exposure of enteric bacteria in affected hosts.

Resistance was found in this study to nalidixic acid, a member of the drug class quinolones. The use of quinolones has been restricted since the 1990s, following the rapid emergence of resistance to quinolones after the introduction of enrofloxacin into poultry production in Europe (WHO, 1998). Chromosomal mutations confer resistance to quinolones (Prescott et al., 2000), and the development of resistance to one agent results in cross-resistance to other quinolones. In the United States, quinolone use is prohibited in food animals except for the treatment of acute pneumonia in beef cattle, and currently the Center for Veterinary Medicine of the U.S. Food and Drug Administration is working to ban the use of enrofloxacin in poultry production in the United States (USFDA, 2004). In addition to restrictions on their use, quinolones were introduced into clinical medicine only 20 years ago, making them relatively new antimicrobial agents, and animal populations do not have a long history of exposure to these drugs compared to the history of exposure to other agents, such as penicillin or tetracycline.

Other studies have also shown an alarming prevalence of multi-drug resistance in E. coli isolates from agricultural animals in Africa (Mitema et al., 2001), Europe (Bywater et al., 2004), and North America (USFDA, 2008). Contact between cattle and/or their manure, or their consumption of foods of animal origin, have been suggested to be the primary methods of distribution of antimicrobial resistance from agricultural animals into human populations (Helmuth and Hensel, 2004). Within cattle manure, for example, E. coli is a predominant species of bacteria (Nuru, 1972) and exposure of other animals to antimicrobial-resistant bacteria in the farm environment can facilitate transfer of antimicrobial resistance (Khachatryan, 2004). Research supports the theory of antimicrobial resistance escalation, such that "the selective pressure from the use of antimicrobial agents at sub therapeutic levels in dairy cattle could result in the selection of those strains that contain genes for antimicrobial resistance" (Molbak, 2004). Researchers suggest that the use of antimicrobial agents in food animals should follow prudent use guidelines to minimize the selection and spread of resistant bacteria (Wierup, 2001), especially with on-farm and slaughter cattle, which have been shown to be carriers of multi-drug resistant E. coli (Threlfall et al., 2000). Additionally, the routine screening of animal and human commensal E. coli could facilitate the study of current and prospective concerns related to the emergence of antimicrobial-resistance (Chaslus-Dancla et al., 1986). Such calls for action have been heeded in warnings from the Danish National Center for Antimicrobials and Infection Control, including the following:

(1) the use of antimicrobial agents regarded as critically or highly important for use in humans should be avoided or minimized in food animals, to preserve the efficiency of these antimicrobial agents for treatment of infection in humans, and

(2) the widespread, non-human, use of these critically or highly important antimicrobial agents creates a reservoir of resistant bacteria that may add to the burden of antimicrobial resistance in humans (Hammerum, 2009).

It is clear that measures are needed to minimize the effects that these resistant bacteria could have on human health.

This study provides the first measurements from Factory Creek of the prevalence of E. coli and its resistance levels to common antimicrobial agents. These findings will aid in determining whether the E. coli present in Factory Creek constitute a potential concern for human health. Ongoing studies will apply these findings to the investigation of temporal changes in E. coli populations in Factory Creek as well as possible origins of E. coli contamination. As continued research reveals the mechanisms, transfer, and evolution of antimicrobial resistance, environmental monitoring studies such as this one provide a clearer understanding of the state of antimicrobial resistance in our environment.

ACKNOWLEDGMENTS

This study was supported by a grant from the Soil and Water Conservation Commission, Sumter County, Alabama.

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Alysia K. Shaw and Brian S. Burnes

Natural Science and Mathematics Department University of West Alabama, Livingston, Alabama

Correspondence: Brian S. Burnes (bburnes@uwa.edu)
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