Open Access

Antimicrobial resistance profiles of Shiga toxin-producing Escherichia coli O157 and Non-O157 recovered from domestic farm animals in rural communities in Northwestern Mexico

Antimicrobial Resistance and Infection Control20165:1

DOI: 10.1186/s13756-015-0100-5

Received: 25 September 2015

Accepted: 18 December 2015

Published: 5 January 2016

Abstract

Background

Antimicrobial resistance in Shiga toxin-producing Escherichia coli (STEC) O157 and non-O157 is a matter of increasing concern. The aim of the present study was to investigate the antimicrobial resistance profiles of STEC O157 and non-O157 recovered from feces of domestic farm animals in the agricultural Culiacan Valley in Northwestern Mexico.

Findings

All of the examined STEC strains showed susceptibility to five antimicrobials, ceftazidime, ceftriaxone, ciprofloxacin, nalidixic acid, and trimethoprim-sulfamethoxazole. However, resistance to the four antimicrobials, ampicillin, cephalothin, chloramphenicol, and kanamycin was commonly observed. Interestingly, non-susceptibility to cephalothin was predominant among the examined STEC strains, corresponding to 85 % (22/26) of the O157:H7 from cattle, sheep and chicken and 73 % (24/33) of the non-O157 strains from cattle and sheep. Statistical analyses revealed that resistance to ampicillin was significantly correlated to 38 % (10/26) of STEC O157:H7 strains from multiple animal sources. Another significant correlation was found between serotype, source, and antimicrobial resistance; all of the O20:H4 strains, recovered from sheep, were highly resistant to tetracycline. Multidrug resistance profiles were identified in 42 % (22/53) of the non-susceptible STEC strains with clinically-relevant serotypes O8:H9, O75:H8, O146:H21, and O157:H7.

Conclusions

STEC O157 and non-O157 strains, recovered from domestic farm animals in the Culiacan Valley, exhibited resistance to classes of antimicrobials commonly used in Mexico, such as aminoglycosides, tetracyclines, cephalosporins and penicillin but were susceptible to fluoroquinolones, quinolones, and sulfonamides. These findings provide fundamental information that would aid in the surveillance of antimicrobial resistance in an important agricultural region in Northwestern Mexico.

Keywords

Antimicrobial resistance Antibiotics Domestic farm animals Shiga toxin Escherichia coli O157:H7 Escherichia coli non-O157 Mexico

Introduction

Shiga toxin-producing Escherichia coli (STEC) is a foodborne pathogen and causes severe gastroenteritis, hemorrhagic colitis, and the life-threatening hemolytic-uremic syndrome (HUS) in humans [1]. Serotype O157:H7 has been implicated in most outbreaks [1]; however, other non-O157 serotypes have been associated with severe human infections worldwide [13]. Recently, several reports have documented a significant increase of antimicrobial resistance in STEC O157:H7 and non-O157:H7 strains [4, 5], and antibiotic resistance of E. coli in Mexico has increased over the years [6]. Inappropriate usages of antibiotics for treating human and plant diseases and for promoting food-animal growth are proposed to contribute to antimicrobial resistance among bacteria populations [69]. Moreover, the use of antimicrobials to treat STEC infections is controversial since they can induce Shiga toxin (Stx) production, resulting in HUS in humans [1012]. However, other studies have suggested that if some classes of antimicrobials are administered early during the infection, STEC disease progression to the HUS could be prevented [10, 13, 14].

STEC strains have been recovered from a variety of animals, and cattle are considered the major reservoir for STEC strains [1, 15, 16]. Recent evidence has indicated that small domestic ruminants are also relevant STEC reservoirs [16, 17]. Given that animals act as reservoirs of STEC that could potentially be transmitted to humans, thru direct or indirect contact, or via the food chain, the present study examined antimicrobial susceptibility in STEC O157 and non-O157 strains, recovered from feces of domestic farm animals [16]. The domestic farm animals were raised in small rural communities within the agricultural Culiacan Valley in Northwestern Mexico. The results indicated that STEC O157 and non-O157 strains exhibited resistance to aminoglycosides, tetracyclines, cephalosporins and penicillins, antimicrobials commonly used in Mexico [1820]. However, all examined STEC strains were susceptible to fluoroquinolones, quinolones, and sulfonamides, agents that can induce Stx production [10, 12, 21]. These findings provide fundamental information that would aid in the surveillance of antimicrobial resistance patterns in an important agricultural region in Northwestern Mexico.

Materials and methods

Bacterial strains and growth conditions

A total of 59 STEC O157:H7 and non-O157 strains were isolated from domestic animal feces in small rural farms, near agricultural fields in the Culiacan Valley, Northwestern Mexico [16, 22]. The source, serotype and virulence potential of the tested STEC strains were previously characterized [16, 22]. STEC strains were routinely grown at 37 °C on trypticase soy agar (Bioxon, Mexico City, Mexico) under aerobic conditions.

Antimicrobial susceptibility testing

The Kirby-Bauer disk diffusion method was performed to test 15 antimicrobials, representing 11 distinct classes (see Additional file 1), which are commonly used in Mexico for animal food production and human infection treatments [1820]. Inoculums from each STEC strain were grown aerobically in 5 mL Mueller-Hinton (MH) broth (Bioxon, Mexico City, Mexico) and incubated at 37 °C to reach a turbidity equal to a McFarland 0.5 standard, according to guidelines provided by Clinical and Laboratory Standards Institute (CLSI) [23]. MH agar plates were surface inoculated with each STEC culture using sterile cotton swabs, and antimicrobial paper disks (BD Diagnostics, Mexico City, Mexico) were placed on surface of inoculated MH agar plates. After incubation at 37 °C for 16–18 h, the diameter of the zone of microbial growth inhibition around the antimicrobial disk was measured in millimeters. E. coli ATCC 25922 (American Type Culture Collection, Manassas, VA) was used as a positive control for antimicrobial susceptibility. The minimum inhibitory concentration (MIC) was then determined according to the interpretive criteria established by CLSI to classify the STEC strains as sensitive, intermediate, or resistant to the tested antimicrobial agent [23].

Statistical analysis

Statistical differences were determined by performing the Fisher’s exact test with the R Statistical Software (version 3.0.1; R Foundation for Statistical Computing, Vienna, Austria) [24]. A p-value ≤ 0.01 was considered statistically significant.

Results

Susceptibility to all tested 15 antimicrobials was observed in 3 % (1/26) of the O157:H7 cattle strains and 15 % (5/33) non-O157 from cattle and sheep. All of the examined STEC strains showed susceptibility to five antimicrobials, CAZ, CIP, CRO, NAL, and SXT (Tables 1 and 2), and approximately 90 % of the tested STEC strains showed susceptibility to AMC, AMK, CFP, GEN, IPM and TET. By contrast, non-susceptibility to the four antimicrobials, AMP, CEF, CHL, and KAN was commonly observed, and in particular, non-susceptibility to CEF, including intermediate and resistant categories, was predominant among the examined STEC strains, corresponding to 85 % (22/26) of the O157:H7 (Table 1) and 73 % (24/33) of the non-O157 strains (Table 2). Resistance to AMP was significantly correlated to 38 % (10/26) of the O157:H7 strains (p-value = 0.0107). A statistically significant correlation was found between serotype, source, and antimicrobial resistance; all of the O20:H4 strains, recovered from sheep, were resistant to TET (p-value = 0.0001), accounting for 75 % (3/4) of the TET resistant STEC strains. No other correlation was found for other non-O157 serotypes and antimicrobials tested.
Table 1

Antimicrobial MIC Values of STEC O157:H7 strains examined in this study

Serotype

Strain

Sourcea

Antimicrobial MIC Values (μg/mL)

AMC

AMK

AMP

CAZ

CEF

CFP

CHL

CIP

CRO

GEN

IPM

KAN

NAL

SXT

TET

O157:H7

RM8744

Cattle

≤8/4

≤ 16

≤ 8

≤ 4

≥ 32b

32c

16c

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8753

Sheep

≤ 8/4

32c

≤ 8

≤ 4

≥ 32b

≤ 16

16c

≤ 1

≤ 1

≤ 4

≤ 1

32c

≤ 16

≤ 2/38

≤ 4

RM8754

Cattle

≤ 8/4

≤ 16

≤ 8

≤ 4

≤ 8

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8759

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≥ 32b

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8767

Cattle

≤ 8/4

≤ 16

≤ 8

≤ 4

16c

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8768

Cattle

≤ 8/4

≤ 16

≤ 8

≤ 4

≥ 32b

≤ 16

16c

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8769

Cattle

≤ 8/4

≤ 16

≤ 8

≤ 4

≤ 8

≤ 16

16c

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8771

Cattle

≤ 8/4

≤ 16

≤ 8

≤ 4

≤ 8

≤ 16

16c

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8781

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

16c

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

32c

≤ 16

≤ 2/38

≤ 4

RM8920

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

16c

≤ 16

16c

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8921

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≥ 32b

≤ 16

16c

≤ 1

≤ 1

≤ 4

≤ 1

32c

≤ 16

≤ 2/38

≤ 4

RM8922

Cattle

≤ 8/4

≤ 16

≤ 8

≤ 4

16c

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM9450

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≥ 32b

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM9451

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

16c

≤ 16

≥ 32b

≤ 1

≤ 1

≤ 4

≤ 1

≥ 64b

≤ 16

≤ 2/38

≥ 16b

RM9452

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≥ 32b

≤ 16

16c

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM9453

Sheep

≤ 8/4

32c

≤ 8

≤ 4

≥ 32b

≤ 16

16c

≤ 1

≤ 1

≤ 4

≤ 1

32c

≤ 16

≤ 2/38

≤ 4

RM9454

Cattle

≤ 8/4

≤ 16

≥ 32b

≤ 4

16c

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM9455

Cattle

≤ 8/4

≤ 16

≥ 32b

≤ 4

16c

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM9456

Cattle

≤ 8/4

≤ 16

≥ 32b

≤ 4

16c

≤ 16

16c

≤ 1

≤ 1

≤ 4

≤ 1

32c

≤ 16

≤ 2/38

≤ 4

RM9457

Cattle

≤ 8/4

≤ 16

≥ 32b

≤ 4

16c

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM9458

Chicken

≤ 8/4

≤ 16

≥ 32b

≤ 4

16c

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM9459

Chicken

≤ 8/4

≤ 16

≥ 32b

≤ 4

16c

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM9460

Cattle

≤ 8/4

≤ 16

≥ 32b

≤ 4

16c

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM9461

Cattle

≤ 8/4

≤ 16

≥ 32b

≤ 4

16c

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM9462

Cattle

16/8c

32c

≥ 32b

≤ 4

16c

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

32c

≤ 16

≤ 2/38

≤ 4

RM9463

Sheep

≤ 8/4

≤ 16

≥ 32b

≤ 4

≤ 8

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

aDomestic animal samples were collected from distinct regions in the Culiacan Valley, Sinaloa, Mexico [16]

bMIC value in bold indicates resistance to the tested antimicrobial, according to CLSI guidelines [23]

cMIC value indicates an intermediate susceptibility to the tested antimicrobial, according to CLSI guidelines [23]

Table 2

Antimicrobial MIC Values of STEC non-O157 strains examined in this study

Serotypea

Strain

Sourceb

Antimicrobial MIC Values (μg/mL)

AMC

AMK

AMP

CAZ

CEF

CFP

CHL

CIP

CRO

GEN

IPM

KAN

NAL

SXT

TET

O8:NT

RM8766

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≤ 8

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

O8:H19

RM8772

Cattle

≤ 8/4

32d

≤ 8

≤ 4

16d

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

32d

≤ 16

≤ 2/38

≤ 4

RM8773

Cattle

≤ 8/4

≤ 16

≤ 8

≤ 4

≤ 8

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8774

Cattle

≤ 8/4

≤ 16

≤ 8

≤ 4

16d

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8775

Cattle

≤ 8/4

≤ 16

≤ 8

≤ 4

≥ 32c

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

32d

≤ 16

≤ 2/38

≤ 4

RM8776

Cattle

≤ 8/4

≤ 16

≤ 8

≤ 4

≥ 32c

≤ 16

≥ 32c

≤ 1

≤ 1

≤ 4

≤ 1

32d

≤ 16

≤ 2/38

≤ 4

O15:NT

RM8747

Cattle

≥ 32/16c

≤ 16

≥ 32c

≤ 4

≥ 32c

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

O20:H4

RM8749

Sheep

≤ 8/4

≤ 16

≥ 32c

≤ 4

16d

≤ 16

≥ 32c

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≥ 16c

RM8750

Sheep

≤ 8/4

≤ 16

16d

≤ 4

≥ 32c

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≥ 16c

RM8751

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

16d

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

32d

≤ 16

≤ 2/38

≥ 16c

O73:NT

RM8748

Cattle

≤ 8/4

≤ 16

≤ 8

≤ 4

16d

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

O73:H4

RM8745

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≥ 32c

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

32d

≤ 16

≤ 2/38

≤ 4

RM8746

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≥ 32c

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

32d

≤ 16

≤ 2/38

≤ 4

O75:H8

RM8752

Sheep

≤ 8/4

≤ 16

16d

≤ 4

≥ 32c

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

32d

≤ 16

≤ 2/38

≤ 4

RM8760

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≤ 8

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8763

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≤ 8

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8764

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≤ 8

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8765

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

16d

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

32d

≤ 16

≤ 2/38

≤ 4

RM8778

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≥ 32c

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

32d

≤ 16

≤ 2/38

≤ 4

RM8779

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

16d

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8780

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≤ 8

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8923

Cattle

≤ 8/4

≤ 16

≤ 8

≤ 4

16d

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

32d

≤ 16

≤ 2/38

≤ 4

RM8929

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

16d

≤ 16

16d

≤ 1

≤ 1

≤ 4

≥ 4c

32d

≤ 16

≤ 2/38

≤ 4

RM8930

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

16d

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

32d

≤ 16

≤ 2/38

≤ 4

RM13865

Cattle

≤ 8/4

≤ 16

≥ 32c

≤ 4

16d

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

32d

≤ 16

≤ 2/38

≤ 4

O111:H8

RM8755

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

16d

≤ 16

≤ 8

≤ 1

≤ 1

≥ 16c

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8916

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≥ 32c

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

O146:H8

RM8762

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≤ 8

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

O146:H21

RM8756

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≤ 8

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8757

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

≤ 8

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

RM8758

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

16d

≤ 16

16d

≤ 1

≤ 1

≤ 4

≤ 1

32d

≤ 16

≤ 2/38

≤ 4

RM8761

Sheep

≤ 8/4

≤ 16

≤ 8

≤ 4

16d

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

≤ 16

≤ 16

≤ 2/38

≤ 4

O168:NT

RM8917

Cattle

≤ 8/4

≤ 16

≤ 8

≤ 4

16d

≤ 16

≤ 8

≤ 1

≤ 1

≤ 4

≤ 1

32d

≤ 16

≤ 2/38

≤ 4

aNT, Non-typeable H-antigen

bDomestic animal samples were collected from distinct regions in the Culiacan Valley, Sinaloa, Mexico [16]

cMIC value indicates resistance to the tested antimicrobial, according to CLSI guidelines [23]

dMIC value indicates an intermediate susceptibility to the tested antimicrobial, according to CLSI guidelines [23]

Correlation analysis of non-susceptibility to more than one antimicrobial, belonging to different classes, indicated that 37 % (22/59) of the examined STEC strains exhibited resistance to both the aminoglycoside KAN and to the 1st generation-cephalosporin CEF, resulting in a statistically significant correlation (p-value = 0.0001) (Tables 1 and 2). Other observations were that 93 % (14/15) and 80 % (24/30) of the AMP and CHL non-susceptible strains, respectively, also showed non-susceptibility to CEF; however, these associations were not found to be statistically significant. The analyses revealed 19 distinct antimicrobial resistant profiles, and 12 were classified as multidrug resistant profiles (Table 3), indicating non-susceptibility to more than 3 agents in different classes [25]. These multidrug resistance profiles were observed in 42 % (22/53) of the non-susceptible STEC strains with clinically-relevant serotypes O75:H8, O146:H21, O8:H9, and O157:H7 (Table 3). The analysis also revealed that a particular antimicrobial resistance profile was not significantly correlated with animal source or STEC serotype.
Table 3

Antimicrobial resistance profiles identified in the STEC O157 and non-O157 from different animal sources

STEC Serotypes (n)a

Sourcesb

Resistance Profile

O157:H7 (1)

Sheep

AMP

O146:H21 (1), O157:H7 (4)

Sheep Cattle

CEF

O75:H8 (3), O146:H21 (1), O157:H7 (2)

Sheep Cattle

CHL

O157:H7 (7)

Cattle, Chicken

AMP, CEF

O8:H19 (1), O73:NT (1), O75:H8 (1), O111:H8 (1), O157:H7 (3)

Sheep, Cattle

CEF, CHL

O111:H8 (1)

Sheep

CEF, GEN

O157:H7 (1), O73:H4 (1), O75:H8 (1), O168:NT (1)

Sheep, Cattle

CEF, KAN

O75:H8 (2)

Sheep, Cattle

AMP, CEF, KAN

O20:H4 (1)

Sheep

AMP, CEF, TET

O157:H7 (1)

Cattle

CEF, CFP, CHL

O8:H19 (2), O73:H4 (1), O75:H8 (3), O146:H21 (1), O157:H7 (1)

Sheep, Cattle

CEF, CHL, KAN

O20:H4 (1)

Sheep

CEF, KAN, TET

O157:H7 (1)

Cattle

AMP, CEF, CHL, KAN

O20:H4 (1)

Sheep

AMP, CEF, CHL, TET

O75:H8 (1)

Sheep

CEF, CHL, KAN, IPM

O157:H7 (1)

Sheep

CEF, CHL, KAN, TET

O15:NT (1)

Cattle

AMC, AMP, CEF, CHL

O8:H19 (1), O157:H7 (2)

Sheep, Cattle

AMK, CEF, CHL, KAN

O157:H7 (1)

Cattle

AMC, AMK, AMP, CEF, KAN

aNT, Non-typeable H-antigen

bDomestic animal samples were collected from distinct regions in the Culiacan Valley, Sinaloa, Mexico [16]

Discussion

Many factors have been proposed to contribute to antimicrobial resistance in enteric bacterial pathogens, such as the inappropriate prescription and use of antibiotics in the public, private, and agricultural sectors [69]. Moreover, data from surveillance programs in Mexico have reported an apparent increase in antimicrobial resistance of E. coli over the years [6, 18]. In the present study, resistance to antimicrobials, belonging to classes commonly utilized in Mexico [1820], was investigated in zoonotic STEC. The STEC strains were recovered from domestic farm animals in small rural communities that were adjacent to the agricultural Culiacan Valley, where the primary purpose of raising livestock is for local consumption [16]. The findings of this study provide a better understanding of resistance to antimicrobial agents in an important agricultural region in Mexico and will aid in the development of efficient and targeted intervention strategies.

The results from the present study demonstrated that zoonotic STEC O157 and non-O157, recovered from the Culiacan Valley, were resistant to antimicrobials belonging to classes such as aminoglycosides, beta lactams, carbapenem, cephalosporins, phenicols, and tetracyclines. In particular, resistance to CEF, a 1st-generation cephalosporin, was prominently detected in 78 % (46/59) of the tested STEC O157 and non-O157 strains. Interestingly, the present study has demonstrated for the first time a significant correlation for AMP resistance in O157:H7 and TET resistance in O20:H4 zoonotic STEC strains recovered from Northwestern Mexico. In agreement with published findings on STECs recovered from foods in this geographical region [18], susceptibility was observed for sulfonamides, quinolones and fluoroquinolones in the recovered STEC strains. These agents have been found to induce Stx production in STEC strains [10, 21], potentially increasing the risk of HUS. However, all STEC strains were susceptible to the 3rd-generation cephalosporin CRO, which does not promote Stx production [21].

Classification of multidrug-resistance, based on recently published criteria [25], was observed in 42 % (22/53) of the non-susceptible STEC strains, harboring serotypes associated with human illness [2]. Multidrug resistance profiles, described in the present study, included classes of antimicrobials commonly used in Mexico, such as aminoglycosides, tetracyclines, cephalosporins, and penicillins [1820], and these findings highlight the need for surveillance of the antimicrobial resistance patterns in enteric bacterial pathogens. Future work is aimed at further dissecting the genetic elements contributing to the acquisition and dissemination of the antimicrobial resistance genes in STEC strains recovered from agricultural regions in Northwestern Mexico.

Abbreviations

AMC: 

Amoxicillin – clavulanic acid

AMK: 

Amikacin

AMP: 

Ampicillin

CAZ: 

Ceftazidime

CEF: 

Cephalothin

CFP: 

Cefoperazone

CHL: 

Chloramphenicol

CIP: 

Ciprofloxacin

CLSI: 

Clinical and Laboratory Standards Institute

CRO: 

Ceftriaxone

GEN: 

Gentamicin

HUS: 

Hemolytic uremic syndrome

IPM: 

Imipenem

KAN: 

Kanamycin

MDR: 

Multi-drug resistant

MH: 

Mueller-Hinton

MIC: 

Minimum inhibitory concentration

NAL: 

Nalidixic acid

STEC: 

Shiga toxin-producing Escherichia coli

Stx: 

Shiga toxin

SXT: 

Trimethoprim-sulfamethoxazole

TET: 

Tetracycline

Declarations

Acknowledgments

This work was supported by the U.S. Department of Agriculture, Agricultural Research Service CRIS project number 5325-42000-047 and by a Postgraduate Studies Scholarship from The National Council of Science and Technology in Mexico (CONACyT grant #234885) to BAAL. The authors would like to thank Lucía Tamayo and Célida Martínez (CIAD in Culiacan, Sinaloa, Mexico) for excellent technical assistance.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Faculty of Chemical and Biological Sciences (FCQB), The Autonomous University of Sinaloa (UAS)
(2)
U.S. Department of Agriculture/Agricultural Research Service, Western Regional Research Center, Produce Safety and Microbiology Research Unit
(3)
Centro de Investigación y Asistencia en Tecnología y Diseño del Estado de Jalisco (CIATEJ)
(4)
Research Center in Food & Development (CIAD), Food Safety National Research Laboratory (LANIIA)

References

  1. Gyles CL. Shiga toxin-producing Escherichia coli: an overview. J Anim Sci. 2007;85(13 Suppl):E45–62. doi:10.2527/jas.2006-508.View ArticlePubMedGoogle Scholar
  2. Hussein HS. Prevalence and pathogenicity of Shiga toxin-producing Escherichia coli in beef cattle and their products. J Anim Sci. 2007;85(13 Suppl):E63–72. doi:10.2527/jas.2006-421.View ArticlePubMedGoogle Scholar
  3. Smith JL, Fratamico PM, Gunther NW. Shiga toxin-producing Escherichia coli. Adv Appl Microbiol. 2014;86:145–97. doi:10.1016/b978-0-12-800262-9.00003-2.View ArticlePubMedGoogle Scholar
  4. Colello R, Etcheverría AI, Di Conza JA, Gutkind GO, Padola NL. Antibiotic resistance and integrons in Shiga toxin-producing Escherichia coli (STEC). Braz J Microbiol. 2015;46(1):1–5. doi:10.1590/s1517-838246120130698.PubMed CentralView ArticlePubMedGoogle Scholar
  5. Pickering LK. Antimicrobial resistance among enteric pathogens. Semin Pediatr Infect Dis. 2004;15(2):71–7. doi:10.1053/j.spid.2004.01.009.View ArticlePubMedGoogle Scholar
  6. Murillo Llanes J, Varon J, Félix JSV, González-Ibarra FP. Antimicrobial resistance of Escherichia coli in Mexico: how serious is the problem? J Infect Dev Ctries. 2012;6(2):126–31. doi:10.3855/jidc.1525.PubMedGoogle Scholar
  7. Amábile-Cuevas CF. Antibiotic resistance in Mexico: a brief overview of the current status and its causes. J Infect Dev Ctries. 2010;4(3):126–31. doi:10.3855/jidc.427.View ArticlePubMedGoogle Scholar
  8. McManus PS, Stockwell VO, Sundin GW, Jones AL. Antibiotic use in plant agriculture. Annu Rev Phytopathol. 2002;40:443–65. doi:10.1146/annurev.phyto.40.120301.093927.View ArticlePubMedGoogle Scholar
  9. Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, et al. Global trends in antimicrobial use in food animals. Proc Natl Acad Sci U S A. 2015;112(18):5649–54. doi:10.1073/pnas.1503141112.PubMed CentralView ArticlePubMedGoogle Scholar
  10. Bielaszewska M, Idelevich EA, Zhang W, Bauwens A, Schaumburg F, Mellmann A, et al. Effects of antibiotics on Shiga toxin 2 production and bacteriophage induction by epidemic Escherichia coli O104:H4 strain. Antimicrob Agents Chemother. 2012;56(6):3277–82. doi:10.1128/aac.06315-11.PubMed CentralView ArticlePubMedGoogle Scholar
  11. Smith KE, Wilker PR, Reiter PL, Hedican EB, Bender JB, Hedberg CW. Antibiotic treatment of Escherichia coli O157 infection and the risk of hemolytic uremic syndrome. Minnesota Pediatr Infect Dis J. 2012;31(1):37–41. doi:10.1097/INF.0b013e31823096a8.View ArticlePubMedGoogle Scholar
  12. Zhang X, McDaniel AD, Wolf LE, Keusch GT, Waldor MK, Acheson DW. Quinolone antibiotics induce Shiga toxin-encoding bacteriophages, toxin production, and death in mice. J Infect Dis. 2000;181(2):664–70. doi:10.1086/315239.View ArticlePubMedGoogle Scholar
  13. Corogeanu D, Willmes R, Wolke M, Plum G, Utermöhlen O, Krönke M. Therapeutic concentrations of antibiotics inhibit Shiga toxin release from enterohemorrhagic E. coli O104:H4 from the 2011 German outbreak. BMC Microbiol. 2012;12:160. doi:10.1186/1471-2180-12-160.PubMed CentralView ArticlePubMedGoogle Scholar
  14. Shiomi M, Togawa M, Fujita K, Murata R. Effect of early oral fluoroquinolones in hemorrhagic colitis due to Escherichia coli O157:H7. Pediatr Int. 1999;41(2):228–32. doi:10.1046/j.1442-200X.1999.4121038.x.View ArticlePubMedGoogle Scholar
  15. Ferens WA, Hovde CJ. Escherichia coli O157:H7: animal reservoir and sources of human infection. Foodborne Pathog Dis. 2011;8(4):465–87. doi:10.1089/fpd.2010.0673.PubMed CentralView ArticlePubMedGoogle Scholar
  16. Amézquita-López BA, Quiñones B, Cooley MB, Leon-Felix J, Castro-Del Campo N, Mandrell RE, et al. Genotypic analyses of Shiga toxin-producing Escherichia coli O157 and non-O157 recovered from feces of domestic animals on rural farms in Mexico. PLoS One. 2012;7(12):e51565. doi:10.1371/journal.pone.0051565.PubMed CentralView ArticlePubMedGoogle Scholar
  17. La Ragione RM, Best A, Woodward MJ, Wales AD. Escherichia coli O157:H7 colonization in small domestic ruminants. FEMS Microbiol Rev. 2009;33(2):394–410. doi:10.1111/j.1574-6976.2008.00138.x.View ArticlePubMedGoogle Scholar
  18. Canizalez-Román A, González-Nuñez E, Vidal JE, Flores-Villaseñor H, León-Sicairos N. Prevalence and antibiotic resistance profiles of diarrheagenic Escherichia coli strains isolated from food items in Northwestern Mexico. Int J Food Microbiol. 2013;164(1):36–45. doi:10.1016/j.ijfoodmicro.2013.03.020.View ArticlePubMedGoogle Scholar
  19. Homedes N, Ugalde A. Mexican pharmacies and antibiotic consumption at the US-Mexico border. South Med Rev. 2012;5(2):9–19.PubMed CentralPubMedGoogle Scholar
  20. Wirtz VJ, Dreser A, Gonzales R. Trends in antibiotic utilization in eight Latin American countries, 1997-2007. Rev Panam Salud Publica. 2010;27(3):219–25. doi:10.1590/S1020-49892010000300009.View ArticlePubMedGoogle Scholar
  21. McGannon CM, Fuller CA, Weiss AA. Different classes of antibiotics differentially influence Shiga toxin production. Antimicrob Agents Chemother. 2010;54(9):3790–8. doi:10.1128/aac.01783-09.PubMed CentralView ArticlePubMedGoogle Scholar
  22. Amézquita-López BA, Quiñones B, Lee BG, Chaidez C. Virulence profiling of Shiga toxin-producing Escherichia coli recovered from domestic farm animals in Northwestern Mexico. Front Cell Infect Microbiol. 2014;4:7. doi:10.3389/fcimb.2014.00007.PubMed CentralView ArticlePubMedGoogle Scholar
  23. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; 24th informational supplement. Wayne: CLSI Document M100-S24; 2014.Google Scholar
  24. Mehta CR, Patel NR. Algorithm 643. FEXACT: a FORTRAN subroutine for Fisher’s exact test on unordered r×c contingency tables. ACM Trans Math Softw. 1986;12(2):154–61. doi:10.1145/6497.214326.View ArticleGoogle Scholar
  25. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268–81. doi:10.1111/j.1469-0691.2011.03570.x.View ArticlePubMedGoogle Scholar

Copyright

© Amézquita-López et al. 2016

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