Evolution of β-lactams, fluroquinolones and colistin resistance and genetic profiles in Salmonella isolates from pork in northern Italy


Submitted: 14 July 2021
Accepted: 15 February 2022
Published: 21 June 2022
Abstract Views: 542
PDF: 242
HTML: 11
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

  • Ilaria Carmosino Food Hygiene Unit, Department of Veterinary Science, University of Parma, Italy.
  • Silvia Bonardi Food Hygiene Unit, Department of Veterinary Science, University of Parma, Italy.
  • Martina Rega Food Hygiene Unit, Department of Veterinary Science, University of Parma, Italy.
  • Andrea Luppi Istituto Zooprofilattico Sperimentale della Lombardia ed Emilia-Romagna, Parma, Italy.
  • Luca Lamperti Food Hygiene Unit, Department of Veterinary Science, University of Parma, Italy.
  • Maria Cristina Ossiprandi Microbiology Unit, Department of Veterinary Science, University of Parma, Italy.
  • Cristina Bacci Food Hygiene Unit, Department of Veterinary Science, University of Parma, Italy.

The European Food Safety Authority and European Centre of Disease Prevention and Control antimicrobial resistance report published in 2021 shows increasing levels of antimicrobial resistance in Salmonella against antibiotics of choice for human salmonellosis (ß-lactams and fluoroquinolones). The aim of the study was to follow the evolution of resistance against some Critical Important Antimicrobials in Salmonella isolates from fresh pork collected in Emilia-Romagna region, northern Italy, over two decades. Emilia-Romagna region is characterized by production of well-known pork derived products, as Parma Ham. The samples were collected in three different periods, ranging from 2000 to 2003, 2012 to 2016 and 2018 to 2021. After serotyping, the isolates were phenotypically tested for resistance to three classes of antibiotics: ß-lactams, fluoroquinolones and polymyxins. End-point polymerase chain reaction (PCR) and PCRReal Time were used for genotypical analyses. The phenotypical resistance to ß-lactams and fluoroquinolones were clearly increasing when comparing the results obtained from isolates collected in the first period (16.7% and 16.7%, respectively) with those of the third period (29.7% and 32.4%, respectively). On the contrary, the resistance to colistin decreased from 33.3% to 5.4%. Genotypically, the 71.4% and 83.3% of the strains harboured ß-lactams and fluoroquinolones genes, respectively, while colistin resistance genes were not detected in the phenotypically resistant strains.


Barilli E, Bacci C, StellaVilla Z, Merialdi G, D’Incau M, Brindani F, Vismarra A, 2018. Antimicrobial resistance, biofilm synthesis and virulence genes in Salmonella isolated from pigs bred on intensive farms. Ital J Food Saf 7:7223. DOI: https://doi.org/10.4081/ijfs.2018.7223

Beloeil PA, Chauvin C, Proux K, Madec F, Fravalo P, Alioum A, 2004. Impact of the Salmonella status of market-age pigs and the pre-slaughter process on Salmonella caecal contamination at slaughter. Vet Res 35:513-30. DOI: https://doi.org/10.1051/vetres:2004028

Bonardi S, 2017. Salmonella in the pork production chain and its impact on human health in the European Union. Epidemiol Infect 145:1513-26. DOI: https://doi.org/10.1017/S095026881700036X

Borowiak M, Baumann B, Fischer J, Thomas K, Deneke C, Hammerl JA, Szabo I, Malorny B, 2020. Development of a novel mcr-6 to mcr-9 multiplex PCR and assessment of mcr-1 to mcr-9 occurrence in colistin-resistant Salmonella enterica isolates from environment, feed, animals and food (2011-2018) in Germany. Front Microbiol 11:80. DOI: https://doi.org/10.3389/fmicb.2020.00080

Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ, 2005. Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63:219-28. DOI: https://doi.org/10.1016/j.mimet.2005.03.018

Carroll LM, Gaballa A, Guldimann C, Sullivan G, Henderson LO, Wiedmann M, 2019. Identification of novel mobilized colistin resistance gene mcr-9 in a multidrug-resistant, colistin-susceptible Salmonella enterica serotype Typhimurium isolate. Mbio 10:e00853-19. DOI: https://doi.org/10.1128/mBio.00853-19

Chen K, Dong N, Chan EW, Chen S, 2019a. Transmission of ciprofloxacin resistance in Salmonella mediated by a novel type of conjugative helper plasmids. Emerg Microbes Infect 8:857-65. DOI: https://doi.org/10.1080/22221751.2019.1626197

Chen K, Chan EWC, Chen S, 2019b. Evolution and transmission of a conjugative plasmid encoding both ciprofloxacin and ceftriaxone resistance in Salmonella. Emerg Microbes Infect 8:396-403. DOI: https://doi.org/10.1080/22221751.2019.1585965

Cuypers WL, Jacobs J, Wong V, Klemm EJ, Deborggraeve S, Van Puyvelde S, 2018. Fluoroquinolone resistance in Salmonella: insights by whole-genome sequencing. Microb Genom 4:e000195. DOI: https://doi.org/10.1099/mgen.0.000195

De Busser EV, Maes D, Houf K, Dewulf J, Imberechts H, Bertrand S & De Zutter L, 2011. Detection and characterization of Salmonella in lairage, on pig carcasses and intestines in five slaughterhouses. Ital J Food Saf 145:279-86. DOI: https://doi.org/10.1016/j.ijfoodmicro.2011.01.009

Directive 2003/99/EC of the European parliament and of the council of 17 November 2003 on the monitoring of zoonoses and zoonotic agents, amending Council Decision 90/424/EEC and repealing Council Directive 92/117/EEC.

Doma AO, Popescu R, Mitulețu M, Muntean D, Dégi J, Boldea MV, Radulov I, Dumitrescu E, Muselin F, Puvača N, Cristina RT, 2020. Comparative evaluation of qnrA, qnrB, and qnrS genes in Enterobacteriaceae ciprofloxacin-resistant cases, in swine units and a hospital from western Romania. Antibiotics (Basel) 9:698. DOI: https://doi.org/10.3390/antibiotics9100698

Elzbieta M, Stefaniuk ST, 2019. Colistin resistance in Enterobacterales strains-A current view. Pol. J. Microbiol 68:417-27. DOI: https://doi.org/10.33073/pjm-2019-055

European Medicine Agency (EMA), Committee for Medicinal Products for Veterinary Use (CVMP), Committee for Medicinal Products for Human Use (CHMP), 2016. Updated advice on the use of colistin products in animals within the European Union: development of resistance and possible impact on human and animal health; EMA: London, UK.

Entervet. 2002. http://entervet.izsvenezie.it

European Food Safety Authority (EFSA); European Centre for Disease Prevention and Control (ECDC), 2021. The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2018/2019. EFSA J 19:e06490. DOI: https://doi.org/10.2903/j.efsa.2021.6490

European Surveillance of Veterinary Antimicrobial Consumption (ESVAC), 2018. Sales of veterinary antimicrobial agents in 31 European countries in 2018. Trends from 2010 to 2018. Tenth ESVAC Report. EMA 10:1-101

Farina, R. and Scatozza, F, 1998. Trattato di malattie infettive degli animali, 2a Edizione, UTET, Torino.

Gunell M, Webber MA, Kotilainen P, Lilly AJ, Caddick JM, Jalava J, Huovinen P, Siitonen A, Hakanen AJ, Piddock LJ, 2009. Mechanisms of resistance in nontyphoidal Salmonella enterica strains exhibiting a nonclassical quinolone resistance phenotype. Antimicrob Agents Chemother 53:3832-6. DOI: https://doi.org/10.1128/AAC.00121-09

Hooper DC, 2001. Emerging mechanisms of fluoroquinolone resistance. Emerg Infect Dis 7:337-41. DOI: https://doi.org/10.3201/eid0702.010239

ISO, 1993. Microbiology of food and animal feeding stuffs. Horizontal method for the detection of Salmonella spp. ISO Norm 6579:1993. International Organization for Standardization, Geneva, Switzerland.

ISO, 2002. Microbiology of food and animal feeding stuffs. Horizontal method for the detection of Salmonella spp. ISO Norm 6579:2002. International Organization for Standardization, Geneva, Switzerland.

ISO, 2017. Microbiology of food and animal feeding stuffs. Horizontal method for the detection of Salmonella spp. ISO Norm 6579:2017. International Organization for Standardization, Geneva, Switzerland.

Istituto Zooprofilattico Sperimentale delle Venezie (IZSVe). https://www.izsvenezie.it/.

Jeon HY, Kim YB, Lim SK, Lee YJ, Seo KW, 2019. Characteristics of cephalosporin-resistant Salmonella isolates from poultry in Korea, 2010-2017. Poult Sci 98:957-65. DOI: https://doi.org/10.3382/ps/pey418

Jiang HX, Song L, Liu J, Zhang XH, Ren YN, Zhang WH, Zhang JY, Liu YH, Webber MA, Ogbolu DO, Zeng ZL, Piddock LJ, 2014. Multiple transmissible genes encoding fluoroquinolone and third-generation cephalosporin resistance co-located in non-typhoidal Salmonella isolated from food-producing animals in China. Int J Antimicrob Agents 43:242-7. DOI: https://doi.org/10.1016/j.ijantimicag.2013.12.005

Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X. 2016. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: A microbiological and molecular biological study. Lancet Infect Dis 16:161-8. DOI: https://doi.org/10.1016/S1473-3099(15)00424-7

Lu X, Zeng M, Xu J, Zhou H, Gu B, Li Z, Jin H, Wang X, Zhang W, Hu Y, Xiao W, Zhu B, Xu X, Kan B, 2019. Epidemiologic and genomic insights on mcr-1-harbouring Salmonella from diarrhoeal outpatients in Shanghai, China, 2006-2016. EbioMedicine 42:133-44. DOI: https://doi.org/10.1016/j.ebiom.2019.03.006

Mąka Ł, Popowska M, 2016. Antimicrobial resistance of Salmonella spp. Isolated from food. Rocz Panstw Zakl Hig 67:343-58.

Min KL, Son ES, Kim JS, Kim SH, Jung SM, Chang MJ, 2018. Risk factors of colistin safety according to administration routes: intravenous and aerosolized colistin. PloS ONE 13:e020758. DOI: https://doi.org/10.1371/journal.pone.0207588

Onseedaeng S, Ratthawongjirakul P, 2016. Rapid Detection of genomic mutations in gyrA and parC genes of Escherichia coli by Multiplex allele specific Polymerase Chain Reaction. J Clin Lab Anal 306:947-55. DOI: https://doi.org/10.1002/jcla.21961

Pelyuntha W, Ngasaman R, Yingkajorn M, Chukiatsiri K, Benjakul S, Vongkamjan K, 2021. Isolation and characterization of potential Salmonella phages targeting multidrug-resistant and major serovars of Salmonella derived from broiler production chain in Thailand. Front Microbiol 12:662461. DOI: https://doi.org/10.3389/fmicb.2021.662461

Pérez-Pérez FJ, Hanson ND, 2002. Detection of plasmid-mediated AmpC -Lactamase genes in clinical isolates by using Multiplex PCR. J. Clin. Microbiol 40:2153-62. DOI: https://doi.org/10.1128/JCM.40.6.2153-2162.2002

Rebelo AR, Bortolaia V, Kjeldgaard JS, Pedersen SK, Leekitcharoenphon P, Hansen IM, Guerra B, Malorny B, Borowiak M, Hammerl JA, 2018. Multiplex PCR for detection of plasmid-mediated colistin resistance determinants, mcr-1, mcr-2, mcr-3, mcr-4 and mcr-5 for surveillance purposes. Eurosurveillance 23:e17-00672. DOI: https://doi.org/10.2807/1560-7917.ES.2018.23.6.17-00672

Regulation (EC) No 2073/2005 of the Commission of 15 November 2005 on microbiological criteria for foodstuff. Official J EU L 338:1-26.

Regulation (EU) No 217/2014 of 7 March 2014 amending Regulation (EC) No 2073/2005 as regards Salmonella in pig carcases. Official J EU L 69/93

Roschansky N, Fischer J, Guerra B, Roesler U, 2014. Development of a Multiplex Real-Time PCR for the rapid detection of the predominant Beta-Lactamase genes CTX-M, SHV, TEM and CIT type AmpCs in Enterobacteriaceae. PloS ONE 9:e100956. DOI: https://doi.org/10.1371/journal.pone.0100956

Scott HM, Acuff G, Bergeron G, Bourassa MW, Simjee S, Singer RS, 2019. Critically important antibiotics: criteria and approaches for measuring and reducing their use in food animal agriculture. Ann N Y Acad Sci 1441:8-16. DOI: https://doi.org/10.1111/nyas.14058

Shigemura H, Sakatsume E, Sekizuka T, Yokoyama H, Hamada K, Etoh Y, Carle Y, Mizumoto S, Hirai S, Matsui M, Kimura H, Suzuki M, Onozuka D, Kuroda M, Inoshima Y, Murakami K, 2020. Food workers as a reservoir of Extended-spectrum-cephalosporin-resistant Salmonella strains in Japan. Appl Environ Microbiol 86:e00072-20. DOI: https://doi.org/10.1128/AEM.00072-20

Sridhar S, Forrest S, Pickard D, Cormie C, Lees EA, Thomson NR, Dougan G, Baker S, 2021. Inhibitory concentrations of ciprofloxacin induce an adaptive response promoting the intracellular survival of Salmonella enterica serovar Typhimurium. mBio 22:e0109321 DOI: https://doi.org/10.1101/2021.05.06.443048

Sun S, Negrea A, Rhen M, Andersson DI. Genetic analysis of colistin resistance in Salmonella enterica serovar Typhimurium. Antimicrob Agents Chemother. 2009 Jun;53(6):2298-305 DOI: https://doi.org/10.1128/AAC.01016-08

Sun J, Zhang H, Liu YH, Feng Y, 2018. Towards understanding MCR-like colistin resistance. Trends Microbiol 26:794-808. DOI: https://doi.org/10.1016/j.tim.2018.02.006

The European Committee on Antimicrobial Susceptibility Testing (EUCAST), 2018. Breakpoint Tables For Interpretation Of Mics And Zone Diameters, Version 8.1. Available online: http://www.eucast.org

Tooke CL, Hinchliffe P, Bragginton EC, Colenso CK, Hirvonen VHA, Takebayashi Y, Spencer J, 2019. Β-Lactamases and β-Lactamase Inhibitors in the 21st Century, Journal of Molecular Biology 431:3472-500. DOI: https://doi.org/10.1016/j.jmb.2019.04.002

Wang J, Stephan R, Karczmarczyk M, Yan Q, Hächler H, Fanning S, 2013. Molecular characterization of bla ESBL-harboring conjugative plasmids identified in multi-drug resistant Escherichia coli isolated from food-producing animals and healthy humans. Front Microbiol 4:188. DOI: https://doi.org/10.3389/fmicb.2013.00188

Wong MH, Yan M, Chan EW, Biao K, Chen S, 2014. Emergence of clinical Salmonella enterica serovar Typhimurium isolates with concurrent resistance to ciprofloxacin, ceftriaxone, and azithromycin. Antimicrob Agents Chemother 58:3752-6. DOI: https://doi.org/10.1128/AAC.02770-13

World Organisation for Animal Health (OIE), 2019. Terrestrial Animal Health Code, 20th ed. World organisation for Animal Health. Paris, France 6:1-6.

Xu Z, Song Q, Li C, Zhan Y, 2019. Characterization of ciprofloxacin-resistant and ESBL-producing Salmonella enteric serotype Derby in Eastern China. BMC Microbiol 19:61 DOI: https://doi.org/10.1186/s12866-019-1434-6

1.
Carmosino I, Bonardi S, Rega M, Luppi A, Lamperti L, Ossiprandi MC, Bacci C. Evolution of β-lactams, fluroquinolones and colistin resistance and genetic profiles in <em>Salmonella</em> isolates from pork in northern Italy. Ital J Food Safety [Internet]. 2022 Jun. 21 [cited 2024 May 11];11(2). Available from: https://www.pagepressjournals.org/ijfs/article/view/9972

Downloads

Download data is not yet available.

Citations