The authors have declared that no competing interests exist.
‡ First authors.
Whole genome sequencing (WGS) has been used as a powerful technology for molecular epidemiology, surveillance, identification of species and serotype, identification of the sources of outbreaks, among other purposes. In Brazil, there is relatively few epidemiological data on
Foodborne diseases have a major impact on the economy and public health worldwide. Non-typhoidal
Among the
In Brazil, there are relatively little epidemiological data on
Epidemiological studies have been crucial to verify the relationship among pathogenic strains isolated from different sources, to elucidate contamination routes and to differentiate strains isolated from outbreaks and sporadic cases. Investigative capabilities have been greatly enhanced with the development and increasing feasibility of WGS as a molecular epidemiological tool [
The use of antimicrobials is not recommended in cases of noninvasive
The extensive use of antimicrobials has led to increasing numbers of non-typhoidal
In previous studies of our group, we typed
In this present work, WGS is used to uncover the diversity of
A total of 90
CFSAN n° | Isolate name | Source | State | Year of isolation | Phenotypic Resistance Profile | Genotypic Resistance Profile (Identity %) | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Aminoglycoside | Tetracycline | Sulphonamide | Trimethoprim | Beta-lactam | Fluoroquinolone | Phenicol | ||||||
CFSAN033848 | STm01 | Human feces | SP | 1983 | AMP-NA-SXT-STR | ― | ― | ― | ― | |||
CFSAN033849 | STm02 | Human feces | SP | 1983 | AMC-AMP-NA-SXT-C-GEN-STR-SUL | ― | ― | |||||
CFSAN033850 | STm03 | Human feces | SP | 1983 | AMP-NA-SXT-C-GEN-STR-SUL | ― | ||||||
CFSAN033851 | STm04 | Human feces | SP | 1983 | AMP-NA-SXT-C-GEN-STR-SUL | ― | ― | |||||
CFSAN033852 | STm05 | Human feces | SP | 1983 | AMP-NA-SXT-C-GEN-STR-SUL | ― | ||||||
CFSAN033853 | STm06 | Human feces | SP | 1983 | ― | ― | ― | ― | ― | ― | ― | ― |
CFSAN033854 | STm07 | Human feces | SP | 1983 | AMP-NA-SXT-C-STR | ― | ― | ― | ||||
CFSAN033856 | STm09 | Human feces | SP | 1984 | AMP-NA-SXT-C-GEN-SUL | ― | ― | |||||
CFSAN033857 | STm10 | Human feces | SP | 1984 | NA-SXT-SUL | ― | ― | ― | ― | ― | ― | |
CFSAN033858 | STm11 | Human feces | SP | 1984 | AMP-NA-SXT-C-GEN-STR-SUL | ― | ― | |||||
CFSAN033859 | STm12 | Human feces | SP | 1984 | NA-GEN-STR-SUL | ― | ||||||
CFSAN033860 | STm13 | Human feces | SP | 1984 | AMP-NA-SXT-C-GEN-SUL | ― | ― | |||||
CFSAN033861 | STm14 | Human feces | SP | 1984 | AMP-NA-SXT | ― | ― | ― | ||||
CFSAN033862 | STm15 | Human feces | SP | 1985 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033863 | STm16 | Human feces | SP | 1985 | NA-SXT | ― | ― | ― | ― | ― | ||
CFSAN033864 | STm17 | Human feces | SP | 1985 | ― | ― | ― | ― | ― | ― | ― | ― |
CFSAN033865 | STm18 | Human feces | SP | 1985 | ― | ― | ― | ― | ― | ― | ― | ― |
CFSAN033866 | STm19 | Human feces | SP | 1986 | AMP-NA-SXT-C-GEN-STR-SUL-CRO | ― | ||||||
CFSAN033867 | STm20 | Human feces | SP | 1986 | NA-SXT-C-TET-STR | ― | ― | ― | ||||
CFSAN033868 | STm21 | Human feces | SP | 1986 | NA-SXT-STR | ― | ― | ― | ― | ― | ||
CFSAN033869 | STm22 | Human feces | SP | 1986 | AMC-AMP-NA-SXT-C-GEN-STR-SUL | ― | ||||||
CFSAN033870 | STm23 | Human feces | SP | 1986 | TET-STR | ― | ― | ― | ― | ― | ||
CFSAN033871 | STm24 | Human feces | SP | 1986 | AMP-NA-SXT-C-GEN-STR-SUL | |||||||
CFSAN033872 | STm25 | Human feces | SP | 1986 | AMP-NA | ― | ― | ― | ― | |||
CFSAN033873 | STm26 | Human feces | SP | 1986 | NA-STR | ― | ― | ― | ― | ― | ||
CFSAN033874 | STm27 | Human feces | SP | 1986 | AMP-NA-SXT-C-GEN-STR-SUL | |||||||
CFSAN033875 | STm28 | Human feces | SP | 1988 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033876 | STm29 | Human feces | SP | 1989 | AMP-STR-SUL | ― | ― | ― | ― | |||
CFSAN033877 | STm30 | Human feces | SP | 1990 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033878 | STm31 | Human feces | SP | 1991 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033879 | STm32 | Human feces | SP | 1992 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033880 | STm33 | Human feces | SP | 1992 | ― | ― | ― | ― | ― | ― | ― | ― |
CFSAN033881 | STm34 | Human feces | SP | 1993 | ― | ― | ― | ― | ― | ― | ― | ― |
CFSAN033882 | STm35 | Human feces | SP | 1995 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033883 | STm36 | Cold chicken | SP | 1995 | STR | ― | ― | ― | ― | ― | ― | ― |
CFSAN033884 | STm37 | Raw pork sausage | SP | 1996 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033885 | STm38 | Human feces | SP | 1997 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033886 | STm39 | Human feces | SP | 1998 | STR | ― | ― | ― | ― | ― | ― | ― |
CFSAN033887 | STm40 | Lettuce | SP | 1998 | STR-SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033888 | STm41 | Raw kafta | SP | 1998 | TET-STR-SUL | ― | ― | ― | ― | ― | ||
CFSAN033889 | STm42 | Human feces | SP | 1999 | TET-STR | ― | ― | ― | ― | ― | ||
CFSAN033890 | STm43 | Human feces | SP | 2000 | TET-STR | ― | ― | ― | ― | ― | ||
CFSAN033891 | STm44 | Blood | SP | 2000 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033892 | STm45 | Raw pork sausage | SP | 2000 | TET-STR-SUL | ― | ― | ― | ― | ― | ||
CFSAN033893 | STm46 | Raw tuscan sausage | SP | 2002 | STR | ― | ― | ― | ― | ― | ― | |
CFSAN033894 | STm47 | Human feces | SP | 2003 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033895 | STm48 | Brain abscess | SP | 2005 | AMP-SXT-STR-SUL | ― | ― | ― | ― | |||
CFSAN033896 | STm49 | Human feces | SP | 2010 | NA | ― | ― | ― | ― | ― | ― | ― |
CFSAN033897 | 702/99 | Final product | SC | 1999 | ― | ― | ― | ― | ― | ― | ― | ― |
CFSAN033898 | 12288/06 | Swine | SC | 2006 | AMP-TET-STR-SUL | ― | ― | ― | ― | |||
CFSAN033899 | 12278/06 | Swine | SC | 2006 | NA-TET-STR-SUL | ― | ― | ― | ― | ― | ||
CFSAN033900 | 12290/06 | Swine | SC | 2006 | TET-STR-SUL | ― | ― | ― | ||||
CFSAN033901 | 12268/06 | Swine | SC | 2006 | AMP-NA-STR-SUL | ― | ― | ― | ||||
CFSAN033902 | 12381/06 | Swine | SC | 2006 | TET-STR-SUL | ― | ― | ― | ― | |||
CFSAN033903 | 5936/06 | Cold chicken | SC | 2006 | STR-SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033904 | 5937/06 | Cold chicken | SC | 2006 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033905 | 5934/06 | Swine | SC | 2006 | NA-TET-GEN-STR-SUL | ― | ― | ― | ― | |||
CFSAN033906 | 5961/06 | Swine | SC | 2006 | TET-GEN-STR-SUL | ― | ― | ― | ― | |||
CFSAN033907 | 5962/06 | Swine | SC | 2006 | TET-STR-SUL | ― | ― | ― | ― | |||
CFSAN033908 | 5929/06 | Poultry | SC | 2006 | TET-SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033909 | 13609/06 | Poultry | SC | 2006 | ― | ― | ― | ― | ― | ― | ― | ― |
CFSAN033910 | 3848/08 | Food | SC | 2008 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033911 | 16238/09 | Ready-to-eat dish | MS | 2009 | AMP-NA-SXT-C-TET-GEN-STR-SUL | ― | ||||||
CFSAN033912 | 16239/09 | Ready-to-eat dish | MS | 2009 | AMP-NA-TET-SUL-CRO | ― | ― | ― | ― | ― | ||
CFSAN033913 | 16240/09 | Ready-to-eat dish | MS | 2009 | AMP-NA-C-TET-STR-SUL-CRO | ― | ― | ― | ― | |||
CFSAN033914 | 16202/09 | Industrialized product | RS | 2009 | TET-SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033915 | 16251/09 | Industrialized product | GO | 2009 | AMP-SXT-C-TET-GEN-SUL | |||||||
CFSAN033916 | 16273/09 | Industrialized product | GO | 2009 | AMP-NA-TET-GEN-SUL | ― | ― | ― | ||||
CFSAN033917 | 17307/09 | Industrialized product | - | 2009 | AMP-NA-SXT-TET-GEN-STR-SUL-CRO | ― | ||||||
CFSAN033918 | 9461/10 | In natura meat | SC | 2010 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033919 | 9479/10 | In natura meat | SC | 2010 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033920 | 7032/10 | Poultry | PR | 2010 | CTX-ATM-FEP-AMP-SXT-TET-STR-SUL-CRO | ― | ― | |||||
CFSAN033921 | 3057/10 | Frozen chicken carcass | PR | 2010 | STR-SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033922 | 6346/10 | Chicken | SP | 2010 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033923 | 5635/10 | Unknown | RS | 2010 | NA | ― | ― | ― | ― | ― | ― | ― |
CFSAN033924 | 9109/10 | Swine | PR | 2010 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033925 | 426/10 | Chicken | SC | 2010 | CTX-FEP-AMP-SUL-CRO | ― | ― | ― | ― | ― | ― | |
CFSAN033926 | 447/10 | Chicken | SC | 2010 | CTX-FEP-AMP-SUL-CRO | ― | ― | ― | ― | ― | ― | |
CFSAN033927 | 2452/11 | Frozen chicken carcass | SP | 2011 | TET-SUL | ― | ― | ― | ― | |||
CFSAN033928 | 6709/11 | Cold chicken | RS | 2011 | AMP-NA-SXT-C-TET-GEN-STR-SUL | |||||||
CFSAN033929 | 948/12 | Raw salad | BA | 2012 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033930 | 1103/12 | Swine (homemade salami) | RS | 2012 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033931 | 1104/12 | Swine (homemade salami) | RS | 2012 | ― | ― | ― | ― | ― | ― | ― | ― |
CFSAN033932 | 3330/12 | Roast beef | SC | 2012 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033933 | 994/13 | Final product sales (animal origin) | SP | 2013 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033934 | 374/13 | Final product sales (animal origin) | SC | 2013 | SUL | ― | ― | ― | ― | ― | ― | ― |
CFSAN033935 |
465/13 | Final product sales (animal origin) | SP | 2013 | AMP-SXT-TET-GEN-STR-SUL | ― | ― | |||||
CFSAN033937 | 622/13 | Final product sales (animal origin) | SC | 2013 | NA | ― | ― | ― | ― | ― | ― | ― |
CFSAN033938 | 583/13 | Final product sales (animal origin) | SC | 2013 | AMP-TET-SUL | ― | ― | ― | ||||
CFSAN033939 | 623/13 | Final product sales (animal origin) | SP | 2013 | AMP-NA-C-TET-STR | ― | ― | ― |
* This genome was the only one that presented the
The genomic DNA extraction methods followed Campioni and Falcão [
All isolates were prepared using the Nextera Sample Preparation Kit (Illumina, San Diego, CA) and then sequenced on Illumina NextSeq (Illumina) for 2 x 151 cycles.
Antimicrobial susceptibility of the 90
In addition to the 90
A total of 39 antimicrobial resistance genes were identified (
Ten distinct aminoglycoside resistance genes were detected including: the most common gene
Five distinct tetracycline resistance genes were detected including: the most common
Only two sulfonamide resistance genes were detected including:
Seven distinct beta-lactam resistance genes were detected including:
Five fluoroquinolone resistance genes were detected including:
Two phenicol genes were detected including:
Only one macrolide resistant gene (
A total of 65 (72.2%) out of 90
A total of 33 (36.7%) out of 90 strains studied presented mutation points in the
CFSAN n° | Isolate Name | CIP E-test | QRDRs mutations | |||
---|---|---|---|---|---|---|
CFSAN033848 | STm01 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033849 | STm02 | Intermediate | Asp(87)→Gly | ― | ― | ― |
CFSAN033850 | STm03 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033851 | STm04 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033852 | STm05 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033853 | STm06 | ― | ― | ― | ― | ― |
CFSAN033854 | STm07 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033856 | STm09 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033857 | STm10 | Intermediate | Asp(87)→Gly | ― | ― | ― |
CFSAN033858 | STm11 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033859 | STm12 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033860 | STm13 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033861 | STm14 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033862 | STm15 | ― | ― | ― | ― | ― |
CFSAN033863 | STm16 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033864 | STm17 | ― | ― | ― | ― | ― |
CFSAN033865 | STm18 | ― | ― | ― | ― | ― |
CFSAN033866 | STm19 | ― | Asp(87)→Gly | ― | ― | ― |
CFSAN033867 | STm20 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033868 | STm21 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033869 | STm22 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033870 | STm23 | ― | ― | ― | ― | ― |
CFSAN033871 | STm24 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033872 | STm25 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033873 | STm26 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033874 | STm27 | Susceptible | Asp(87)→Gly | ― | ― | ― |
CFSAN033875 | STm28 | Susceptible | ― | ― | ― | ― |
CFSAN033876 | STm29 | Susceptible | ― | ― | ― | ― |
CFSAN033877 | STm30 | ― | ― | ― | ― | ― |
CFSAN033878 | STm31 | Susceptible | ― | ― | ― | ― |
CFSAN033879 | STm32 | ― | ― | ― | ― | ― |
CFSAN033880 | STm33 | ― | ― | ― | ― | ― |
CFSAN033881 | STm34 | Susceptible | ― | ― | ― | ― |
CFSAN033882 | STm35 | Susceptible | ― | ― | ― | ― |
CFSAN033883 | STm36 | Susceptible | ― | ― | ― | ― |
CFSAN033884 | STm37 | Susceptible | ― | ― | ― | ― |
CFSAN033885 | STm38 | ― | ― | ― | ― | ― |
CFSAN033886 | STm39 | ― | ― | ― | ― | ― |
CFSAN033887 | STm40 | Susceptible | ― | ― | ― | ― |
CFSAN033888 | STm41 | ― | ― | ― | ― | ― |
CFSAN033889 | STm42 | ― | ― | ― | ― | ― |
CFSAN033890 | STm43 | ― | ― | ― | ― | ― |
CFSAN033891 | STm44 | Susceptible | ― | ― | ― | ― |
CFSAN033892 | STm45 | Susceptible | ― | ― | ― | ― |
CFSAN033893 | STm46 | Susceptible | ― | ― | ― | ― |
CFSAN033894 | STm47 | Susceptible | ― | ― | ― | ― |
CFSAN033895 | STm48 | ― | ― | ― | ― | ― |
CFSAN033896 | STm49 | Intermediate | Asp(87)→Asn | ― | ― | ― |
CFSAN033897 | 702/99 | ― | ― | ― | ― | ― |
CFSAN033898 | 12288/06 | ― | ― | ― | ― | ― |
CFSAN033899 | 12278/06 | Susceptible | Asp(87)→Asn | ― | ― | ― |
CFSAN033900 | 12290/06 | ― | ― | ― | ― | ― |
CFSAN033901 | 12268/06 | Intermediate | Asp(87)→Asn | ― | ― | ― |
CFSAN033902 | 12381/06 | ― | ― | ― | ― | ― |
CFSAN033903 | 5936/06 | ― | ― | ― | ― | ― |
CFSAN033904 | 5937/06 | ― | ― | ― | ― | ― |
CFSAN033905 | 5934/06 | Susceptible | ― | ― | ― | ― |
CFSAN033906 | 5961/06 | ― | ― | ― | ― | ― |
CFSAN033907 | 5962/06 | ― | ― | ― | ― | ― |
CFSAN033908 | 5929/06 | ― | ― | ― | ― | ― |
CFSAN033909 | 13609/06 | ― | ― | ― | ― | ― |
CFSAN033910 | 3848/08 | ― | ― | ― | ― | ― |
CFSAN033911 | 16238/09 | Resistant | Ser(83)→Tyr | ― | ― | ― |
CFSAN033912 | 16239/09 | Intermediate | Asp(87)→Asn | ― | ― | ― |
CFSAN033913 | 16240/09 | Intermediate | Asp(87)→Asn | ― | ― | ― |
CFSAN033914 | 16202/09 | ― | ― | ― | ― | ― |
CFSAN033915 | 16251/09 | ― | ― | ― | ― | ― |
CFSAN033916 | 16273/09 | Intermediate | Ser(83)→Phe | ― | ― | ― |
CFSAN033917 | 17307/09 | Resistant | Ser(83)→Tyr | ― | ― | ― |
CFSAN033918 | 9461/10 | ― | ― | ― | ― | ― |
CFSAN033919 | 9479/10 | ― | ― | ― | ― | ― |
CFSAN033920 | 7032/10 | ― | ― | ― | ― | ― |
CFSAN033921 | 3057/10 | ― | ― | ― | ― | ― |
CFSAN033922 | 6346/10 | ― | ― | ― | ― | ― |
CFSAN033923 | 5635/10 | Intermediate | Asp(87)→Asn | ― | ― | ― |
CFSAN033924 | 9109/10 | ― | ― | ― | ― | ― |
CFSAN033925 | 426/10 | ― | ― | ― | ― | ― |
CFSAN033926 | 447/10 | ― | ― | ― | ― | ― |
CFSAN033927 | 2452/11 | ― | ― | ― | ― | ― |
CFSAN033928 | 6709/11 | Intermediate | Asp(87)→Asn | ― | ― | ― |
CFSAN033929 | 948/12 | ― | ― | ― | ― | ― |
CFSAN033930 | 1103/12 | ― | ― | ― | ― | ― |
CFSAN033931 | 1104/12 | ― | ― | ― | ― | ― |
CFSAN033932 | 3330/12 | ― | ― | ― | ― | ― |
CFSAN033933 | 994/13 | ― | ― | ― | ― | ― |
CFSAN033934 | 374/13 | ― | ― | ― | ― | ― |
CFSAN033935 | 465/13 | ― | ― | ― | ― | ― |
CFSAN033937 | 622/13 | Intermediate | Ser(83)→Tyr | ― | ― | ― |
CFSAN033938 | 583/13 | ― | ― | ― | ― | ― |
CFSAN033939 | 623/13 | Intermediate | Ser(83)→Tyr | ― | ― | ― |
The
The 90
The genomes of one
In this study 90
In this study, 47 (52.2%) strains presented phenotypic resistance to gentamicin and/or streptomycin. Streptomycin is not frequently used to treat
Our results confirm McDermott et al’s. [
The tetracycline resistance genes were found in 32 (35.5%) strains. Interestingly, 2 strains that were phenotypically resistant to tetracycline did not present any known tetracycline resistance genes suggesting a possible alternative mode of resistance. In contrast, seven strains that presented tetracycline resistance genes were phenotypically susceptible. Of these seven, six strains had two tetracycline resistance genes and one strain had only one tetracycline resistance gene. Tetracycline has been used commonly as an antibiotic in swine husbandry [
Cefoxitin resistance has been used to indicate certain types of beta-lactamases production by
Some of the discrepancies observed when a resistance gene is present but no phenotypic resistance in bacterial growth is observed, or when the phenotype is present but no known resistance gene is observed, is likely due to new unidentified resistance genes or mutations conferring resistance in undiscovered genes. Therefore, it is important to study any discrepancy as each represents new ways that bacteria are acquiring resistance as was reported for a new mechanisms discovered for
McDermott and colleagues [
Food isolates were distributed in Clades A and B in relatively similar numbers suggesting that there is more than one subtype in circulation, in foods in Brazil. Human’s isolates were more prevalent in the Clade B suggesting the existence of a prevalent subtype. Genomic and phenotypic testing results suggest clinical strains isolated before the mid-1990s presented more antimicrobial resistance compared to later strains. The diversity and prevalence of resistant genes found in Brazilian
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