Differences in antimicrobial resistance of Salmonella spp. isolated from humans, animals and food products in Kazakhstan

PDF
DOI: https://doi.org/10.12681/jhvms.28498
Keywords:
Salmonella Paratyphi One Health salmonellosis zoonoses
R RYCHSHANOVA
Institute of Applied Biotechnology, Kostanay State University, Kazakhstan
M RUZAUSKAS
Veterinary Academy, Kaunas, Lithuanian University of Health Sciences
G CHUZHEBAYEVA
Institute of Applied Biotechnology, Kostanay State University, Kazakhstan
R MOCKELIUNAS
Veterinary Academy,Kaunas, Lithuanian University of Health Sciences
N MAMIYEV
Institute of Applied Biotechnology, Kostanay State University, Kazakhstan
M VIRGAILIS
Veterinary Academy,Kaunas, Lithuanian University of Health Sciences
P SHEVCHENKO
Institute of Applied Biotechnology, Kostanay State University, Kazakhstan
R SIUGZDINIENE
Veterinary Academy, Kaunas, Lithuanian University of Health Sciences
L ANSKIENE
Veterinary Academy, Kaunas, Lithuanian University of Health Sciences
A MENDYBAYEVA
Institute of Applied Biotechnology, Kostanay State University, Kazakhstan
Abstract

The aims of this study were twofold: 1. to isolate Salmonella spp. from different sources in Kazakhstan, to determine their serovars and resistance profiles and 2. to evaluate similarities in antimicrobial susceptibility of Salmonella spp. isolated from humans, animals and food products. From the10 212 samples tested Salmonella spp. Were isolated in 47 cases. The predominant serovar isolated from humans and food products was S. Enteritidis. Although different animal species were tested the Salmonella spp. were isolated mainly from chickens and ducks. S. Enteritidis and S. Typhimurium were the most prevalent serovars in raw poultry meat. The most frequent resistances were those to nalidixic acid, ampicillin and tetracycline. Human isolates demonstrated lower resistance compared to animal and food isolates. The genes encoding antimicrobial resistance in human isolates in most cases were absent except for some isolates which harboured tet, sul, stre and bla TEM genes encoding resistance to the oldest antimicrobial classes. The situation in animals and food products was less beneficial as besides different genes, integrons associated with the horizontal gene transfer were detected. The findings suggest that antimicrobials in animal sector should be used more strictly, paying attention to critically important antimicrobials for humans and possible horizontal transfer of pathogens and their genetic determinants.

Article Details
  • Section
  • Research Articles
Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Authors who publish with this journal agree to the following terms:

· Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.

· Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.

· Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.

Downloads
Download data is not yet available.
References
Ammar AM, Abdeen EE, Abo-Shauma UP, Fekry E, Kotb Elmahallawy E (2019) Molecular characterization of virulence and antibiotic resistance genes among Salmonella serovars isolated from broilers in Egypt. Lett Appl Microbiol68:188-195.
Andino A, Hanning I (2015)Salmonella enterica: survival, colonization, and virulence differences among serovars. Sci World J 2015:520179.
AsadollahiP, AkbariM, Soroush S, Taherikalani M, Asadollahi K, Sayehmiri K (2012) Antimicrobial resistance patterns and their encoding genes among Acinetobacter baumannii strains isolated from burned patients. Clin Infect Dis38:1198-1203.
Bert F, Branger C, Lambert-Zechovsky N (2002) Identification of PSE and OXA β-lactamase genes in Pseudomonas aeruginosa using PCR-restriction fragment length polymorphism. J Antimicrob Chemother 50:11-18.
Celenza G, Pellegrini C, Caccamo M, Segatore B, Amicosante G, Perilli M (2006) Spread of blaCTX-M-type and blaPER-2 β-lactamase genes in clinical isolates from Bolivian hospitals. J Antimicrob Chemother 57:975-978.
Chaney WE, Agga GE, Nguyen SV, Arthur TM, Bosilevac JM, Dreyling E, Rishi A, Brichta-Harhay D (2017) Rapid detection and classification of Salmonella enterica shedding in feedlot cattle utilizing the roka bioscience atlas Salmonella detection assay for the analysis of rectoanal mucosal swabs. J Food Prot80:1760-1767.
Chen CH, Huang CC (2013)Risk factor analysis for extended-spectrum β-lactamase-producing Enterobacter cloacae bloodstream infections in central Taiwan. BMC Infect Dis 13:417.
Christabel M, Budambula N, KiiruJ, Kariuki S (2012) Characterization of antibiotic resistance in environmental enteric pathogens from Kibera slum in Nairobi-Kenya. Afr J Bacteriol Res4:46-54.
CLSI (2019) Performance Standards for Antimicrobial Susceptibility Testing. 29th ed. CLSI supplement M100. Wayne, P. A.: Clinical and Laboratory Standards Institute. DarMA, AhmadSM, Bhat SA, Ahmed R, Urwat U, MumtazPT, Bhat SA, Dar TA, Shah RA, Ganai NA (2017) Salmonella typhimurium in poultry: a review. World Poultry Sci J 73:345-354.
DioneMM, IkumapayiUN, SahaD, MohammedNI, GeertsS, IevenM, AdegbolaRA, AntonioM (2011)Clonal differences between non-typhoidal Salmonella (NTS) recovered from children and animals living in close contact in the Gambia. PLoS Negl Trop Dis5:e1148.
Dyson ZA, Klemm EJ, Palmer S, Dougan G (2019) Antibiotic resistance and typhoid, Clin Infect Dis 68 :165-170.
Ekdahl K, de Jong B, Wollin R, Andersson Y (2005)Travel-associated non-typhoidal salmonellosis - geaographical and seasonal differences and serotype distribution. Clin Microbiol Infect 11:138-144.
Eng SK, Pusparajah P, Ab Mutalib NS, Ser HL, Chan KG, Lee,LH (2015) Salmonella: A review on pathogenesis, epidemiology and antibiotic resistance. Front Life Sci8:284-293.
European Centre for Disease Prevention and Control. Facts about typhoid and paratyphoid fever. Interactive https://www.ecdc.europa.eu/en/typhoid-and-paratyphoid-fever/facts. Accsessed: 26-03-2020.
Evangelopoulou G, Kritas S, Christodoulopoulos G, Burriel A R (2015)The commercial impact of pig Salmonella spp. infections in border-free markets during an economic recession. Vet World 8:257-272.
Frana TS, CarlsonSA, Griffith RW (2001) Relative distribution and conservation of genes encoding aminoglycoside-modifying enzymes in Salmonella enterica serotype Typhimurium phage type DT104. Appl Environ Microbiol 67:445-448.
Galimand M, Courvalin P, Lambert T (2003) Plasmid-Mediated High-Level Resistance to Aminoglycosides in Enterobacteriaceae Due to 16S rRNA Methylation. Antimicrob Agents Chemother47:2565-2571.
Gibreel A, Sköld O (1998)High-level resistance to trimethoprim in clinical isolates of Campylobacter jejuni by acquisition of foreign genes (dfr1 and dfr9) expressing drug-insensitive dihydrofolate reductases. Antimicrob Agents Chemother 42:3059-3064.
Goldstein C, Lee MD, Sanchez S, Hudson C, Phillips B, Register B, Grady M, Liebert C, Summers AO, White DG, Maurer JJ (2001) Incidence of class 1 and 2 integrases in clinical and commensal bacteria from livestock, companion animals, and exotics. Antimicrob Agents Chemother45:723-726.
Gutema FD, Agga GE, Abdi RD, De Zutter L, Duchateau L,Gabriël S (2019) Prevalence and serotype diversity of Salmonella in apparently healthy cattle: Systematic review and meta-analysis of published studies, 2000-2017. Front Vet Sci6:102.
Hasman H, Mevius D, Veldman K, Olesen I, Aarestrup FM (2005) β-lactamases among extended-spectrum β-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. J Antimicrob Chemother 56:115-121.
Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DM, Jensen AB, Wegener HC, Aarestrup FM (2011) Global monitoring of Salmonella serovar distribution from the World Health Organization global foodborne infections network country data bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog Dis 8:887-900.
Holt RA, Newton H (1948) The occurrence of Salmonella blegdam in Louisiana. J Lab Clin Med 33:1115-1158.
Hooper DC (2001) Emerging mechanisms of fluoroquinolone resistance. Emerg Infect Dis 7:337-341.
Hudzicki J (2009) Kirby-Bauer disk diffusion susceptibility test protocol. ASM Microbe Libr, URL (https://www.asm.org/getattachment/2594ce26-bd44-47f6-8287-0657aa9185ad/Kirby-Bauer-Disk-Diffusion-Susceptibility-Test-Protocol-pdf.pdf). (accessed 26.03.2020).
ISO 6579-1:2017. Microbiology of the food chain - Horizontal method for the detection, enumeration and serotyping of Salmonella - Part 1: Horizontal method for the detection of Salmonella spp. International Organization for Standardization, Geneva, Switzerland.
Keyes K, Hudson C, Maurer JJ, Thayer S, White DG, Lee MD (2000) Detection of florfenicol resistance genes in Escherichia coli isolated from sick chickens. Antimicrob Agents Chemother44:421-424.
Kihlstrom E, Andaker L (1985)Inability of gentamicin and fosfomycin to eliminate intracellular Enterobacteriaceae. J Antimicrob Chemother 15:723-728.
Kirk M, Ford L, Glass K, Hall G (2014) Foodborne illness, Australia, circa 2000 and circa 2010. Emerg Infect Dis 20:1857-1864.
Lanz R, Kuhnert P, Boerlin P (2003) Antimicrobial resistance and resistance genes determinants in clinical Escherichia coli from different animal species in Switzerland. Vet Microbiol91:73-84.
Liljebjelke KA, Hofacre CL, White DG, Ayers S, Lee MD, Maurer JJ (2017) Diversity of antimicrobial resistance phenotypes in Salmonella isolated from commercial poultry farms. Front Vet Sci 4:96.
Liu JH, Deng YT, Zeng ZL, Gao JH, Chen L, Arakawa Y,Chen ZL (2008) Coprevalence of plasmid-mediated quinolone resistance determinants QepA, Qnr, and AAC(6′)-Ib-cr among 16S rRNA methylase RmtB-producing Escherichia coli isolates from pigs. AntimicrobAgents Chemother 52:2992-2993.
Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu LF, Gu D, Ren H, Chen X, Lv L, He D, Zhou H, Liang Z, Liu, JH, Shen J (2015) 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, S1473-3099(15)00424-7.
Lynch MF, Blanton EM, Bulens S, Polyak C, Vojdani J, Stevenson J, Medalla F, Barzilay E, Joyce, K, Barrett T, Mintz ED (2009) Typhoid fever in the United States, 1999-2006. JAMA 302:859-865.
LynchM, PainterJ, WoodruffR, BradenC (2006)Surveillance for foodborne-disease outbreaks - United States, 1998-2002. MMWR Surveill Summ10:1-42.
Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O’Brien SJ, Jones TF, Fazil A, Hoekstra R M (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50:882-889.
MąkaŁ, Maćkiw E, Ścieżyńska H, Popowska M (2015)Occurrence and antimicrobial resistance of Salmonella spp. isolated from food other than meat in Poland.Ann Agric Environ Med AAEM22:403-408.
Marks F, von Kalckreuth V, Aaby P, Adu-Sarkodie Y, El Tayeb MA, Ali M, Aseffa A, Baker S, Biggs HM, Bjerregaard-Andersen M, et al. (2017) Incidence of invasive salmonella disease in sub-Saharan Africa: a multicentre population-based surveillance study. Lancet Glob Health 5:e310.
Maynard C, Fairbrother JM, Bekal S, Sanschagrin F, Levesque RC, Brousseau R, Masson L, Larivière S,Harel J (2003) Antimicrobial resistance genes in enterotoxigenic Escherichia coli O149:K91 isolates obtained over a 23-year period from pigs. Antimicrob Agents Chemother 47:3214-3221.
Mshelbwala FM, Ibrahim NDG, Saidu SNA, Azeez AA, Akinduti PA, Kwanashie CN, Kadiri AKF, Muhammed M, Fagdamila IO, Luka PD (2017) Motile Salmonella serotypes causing high mortality in poultry farms in three Sauthwestern States of Nigeria. Vet Rec Open 4:e000247.
Narváez-Bravo C, Rodas-González A, Fuenmayor Y, Flores-Rondon C, Carruyo G, Moreno M, Perozo-Mena A, Hoet AE (2013)Salmonella. on feces, hides and carcasses in beef slaughter facilities in Venezuela. Int J Food Microbiol 166:226-230.
Navia MM, Ruiz J, Cespedes SJ, Vila J (2003)Detection of dihydrofolate reductase genes by PCR and RFLP. Diagn Microbiol Infect Dis 46:295-298.
Odumosu BT,Akintimehin AR (2015)Occurrence of extended-spectrum beta-lactamase producing Enterobacteriaceae isolates in communal water sources in Ogun State, Nigeria.Afr J Clin Exp Microbiol16:28-32.
Ojdana D, Sacha PB, Wieczorek P, Czaban B, Michalska A, Jaworowska J, Jurczak A, Poniatowski B, Tryniszewska E (2014)The occurrence of blaCTX-M, blaSHV, and blaTEM genes in extended-spectrum β-Lactamase-positive strains of Klebsiellapneumoniae, Escherichia coli, and Proteus mirabilis in Poland. Int J Antibiot :93584.
Pagani L, Dell’Amico E, Migliavacca R, D’Andrea MM, Giacobone E, Amicosante GER, Rossolini GM (2003)Multiple CTX-M-Type extended-spectrum β-lactamases in nosocomial isolates of Enterobacteriaceae from a hospital in northern Italy. J Clin Microbiol 41:4264-4269.
Pande VV, Devon RL, Sharma P, McWhorter AR, Chousalkar KK (2016) Study of Salmonellatyphimurium infection in laying hens. Front Microbiol7: 203.
PerretenV, BoerlinPA (2003) New sulfonamide resistance gene (sul3) in Escherichia coli is widespread in the pig population of Switzerland. Antimicrob Agents Chemother47:1169-1172.
Robicsek A, Strahilevitz J, Sahm D, Jacoby GA,Hooper DC (2006)qnrprevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob Agents Chemother 50:2872-2874.
Ruzauskas M, Siugzdiniene R, Klimiene I, Virgailis M, Mockeliunas R, Vaskeviciute L, Zienius D (2014) Prevalence of methicillin-resistant Staphylococcus haemolyticus in companion animals: a cross-sectional study. Ann Clin Microbiol Antimicrob13:56.
Sandvang D, Aarestrupp FM (2009)Characterization of aminoglycoside resistance genes and Class 1 integrons in porcine and bovine gentamicin-resistant Escherichia coli.Microb Drug Resist6:19-27.
SeputieneV, Povilonis J, Ruzauskas M, Pavilonis A, Suziedeliene E (2010) Prevalence of trimethoprim resistance genes in Escherichia coli isolates of human and animal origin in Lithuania. J Med Microbiol59:315-322.
SwansonSJ, SniderC, BradenCR, BoxrudD, WunschmannA, RudroffJA, LockettJ,SmithKE (2007)Multidrug-resistant Salmonella enterica serotype Typhimurium associated with pet rodents. N Engl J Med356:21-28.
Thong KL, Bakeri SA, Lai KS, Koh YT, Taib MZ, Lim VKE, Yasin RM (2004) Molecular subtyping of Salmonella enterica serovar Tshiongwe recently isolated in Malaysia during 2001-2002. Southeast Asian J Trop Med Public Health 35:92-96.
Tietjen M, Fung DYC (1995)Salmonellae and food safety. Crit Rev Microbiol 21:53-83.
Tirado C, Schmidt K (2001) WHO surveillance programme for control of foodborne infections and intoxications: preliminary results and trends across greater Europe. World Health Organization. J Infect43:80-84.
Vassort-Bruneau C, Lesage-Descauses M, Martel JL, Lafont JP, Chaslus-Dancla E (1996) CAT III chloramphenicol resistance in Pasteurella haemolytica and Pasteurella multocida isolated from calves. J Antimicrob Chemoth38: 205-213.
Xavier BB, Lammens C, Ruhal R, Kumar-Singh S, Butaye P, Goossens H, Malhotra-Kumar S (2016) Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Belgium. Euro Surveill. 21:pii=30280.
Yan JJ, WuJJ, Ko WC,Tsai SH, ChuangCL, Wu HM, Lu YJ, Li JD (2004) Plasmid-mediated 16S rRNA methylases conferring high-level aminoglycoside resistance in Escherichia coli and Klebsiella pneumoniae isolates from two Taiwanese hospitals. J Antimicrob Chemother 54:1007-1012.
Zhang L, Fu Y, Xiong Z, Ma Y, Wei Y, Qu X, Zhang H, Zhang J, Liao M (2018)Highly prevalent multidrug-resistant Salmonella from chicken and pork meat at retail markets in Guangdong, China.FrontMicrobiol9:2104.