Antimicrobial Resistance Profiling of Biofilm Forming Non Typhoidal <i>Salmonella enterica</i> Isolates from Poultry and Its Associated Food Products from Pakistan

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Abstract

Salmonellosis caused by non-typhoidal Salmonella enterica from poultry products is a major public health concern worldwide. This study aimed at estimating the pathogenicity and antimicrobial resistance in S. enterica isolates obtained from poultry birds and their food products from different areas of Pakistan. In total, 95/370 (25.67%) samples from poultry droppings, organs, eggs, and meat were positive for Salmonella. The isolates were further identified through multiplex PCR (mPCR) as Salmonella Typhimurium 14 (14.7%), Salmonella Enteritidis 12 (12.6%), and other Salmonella spp. 69 (72.6%). The phenotypic virulence properties of 95 Salmonella isolates exhibited swimming and/or swarming motility 95 (100%), DNA degrading activity 93 (97.8%), hemolytic activity 92 (96.8%), lipase activity 87 (91.6%), and protease activity 86 (90.5%). The sopE virulence gene known for conferring zoonotic potential was detected in S. Typhimurium (92.8%), S. Enteritidis (100%), and other Salmonella spp. (69.5%). The isolates were further tested against 23 antibiotics (from 10 different antimicrobial groups) and were found resistant against fifteen to twenty-one antibiotics. All isolates showed multiple drug resistance and were found to exhibit a high multiple antibiotic-resistant (MAR) index of 0.62 to 0.91. The strong biofilm formation at 37 °C reflected their potential adherence to intestinal surfaces. There was a significant correlation between antimicrobial resistance and the biofilm formation potential of isolates. The resistance determinant genes found among the isolated strains were bla _TEM-1 (59.3%) , bla _OxA-1 (18%) , bla _PSE-1 (9.5%) , bla _CMY-2 (43%), and ampC (8.3%). The detection of zoonotic potential MDR Salmonella in poultry and its associated food products carrying cephalosporin and quinolone resistance genes presents a major threat to the poultry industry and public health.

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The global burden of nontyphoidal Salmonella gastroenteritis.

Shannon Majowicz, Jennie Musto, Elaine Scallan … (2010)

To estimate the global burden of nontyphoidal Salmonella gastroenteritis, we synthesized existing data from laboratory-based surveillance and special studies, with a hierarchical preference to (1) prospective population-based studies, (2) "multiplier studies," (3) disease notifications, (4) returning traveler data, and (5) extrapolation. We applied incidence estimates to population projections for the 21 Global Burden of Disease regions to calculate regional numbers of cases, which were summed to provide a global number of cases. Uncertainty calculations were performed using Monte Carlo simulation. We estimated that 93.8 million cases (5th to 95th percentile, 61.8-131.6 million) of gastroenteritis due to Salmonella species occur globally each year, with 155,000 deaths (5th to 95th percentile, 39,000-303,000 deaths). Of these, we estimated 80.3 million cases were foodborne. Salmonella infection represents a considerable burden in both developing and developed countries. Efforts to reduce transmission of salmonellae by food and other routes must be implemented on a global scale.

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A modified microtiter-plate test for quantification of staphylococcal biofilm formation.

Srdjan Stepanovic, Dragana Vuković, Ivana Dakić … (2000)

The tube test and the microtiter-plate test are the most frequently used techniques for quantifying biofilm formation, an important indicator for the pathogenicity of staphylococci. The purpose of the present study was to develop a modified microtiter-plate technique for quantification of biofilm formation. This technique involves fixing the bacterial film with methanol, staining with crystal violet, releasing the bound dye with 33% glacial acetic acid, and measuring the optical density (OD) of the solution at 570 nm by using an enzyme immunosorbent assay reader. Biofilm formation of 30 Staphylococcus strains was estimated by the tube test, the standard microtiter-plate test and the modified microtiter-plate test. The modified microtiter-plate test, as a quantitative assay, is superior to the tube test in terms of objectivity and accuracy. It is also superior to the standard microtiter-plate test because it enables indirect measuring of bacteria attached both to the bottom and to the walls of the wells, while in the standard test only the dye bound to the bacteria adhered to the bottom of the wells is spectrophotometrically registered. Highly significant differences between OD values obtained by the standard microtiter-plate test and those obtained by the modified test suggest that large number of bacteria were attached to the walls of the wells. Therefore, the modification of the standard microtiter-plate test by introduction of an additional step of decolorization by acetic acid seems to be a useful improvement of the technique.

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Emergence of an Extensively Drug-Resistant Salmonella enterica Serovar Typhi Clone Harboring a Promiscuous Plasmid Encoding Resistance to Fluoroquinolones and Third-Generation Cephalosporins

Elizabeth J Klemm, Sadia Shakoor, Andrew J Page … (2018)

ABSTRACT Antibiotic resistance is a major problem in Salmonella enterica serovar Typhi, the causative agent of typhoid. Multidrug-resistant (MDR) isolates are prevalent in parts of Asia and Africa and are often associated with the dominant H58 haplotype. Reduced susceptibility to fluoroquinolones is also widespread, and sporadic cases of resistance to third-generation cephalosporins or azithromycin have also been reported. Here, we report the first large-scale emergence and spread of a novel S. Typhi clone harboring resistance to three first-line drugs (chloramphenicol, ampicillin, and trimethoprim-sulfamethoxazole) as well as fluoroquinolones and third-generation cephalosporins in Sindh, Pakistan, which we classify as extensively drug resistant (XDR). Over 300 XDR typhoid cases have emerged in Sindh, Pakistan, since November 2016. Additionally, a single case of travel-associated XDR typhoid has recently been identified in the United Kingdom. Whole-genome sequencing of over 80 of the XDR isolates revealed remarkable genetic clonality and sequence conservation, identified a large number of resistance determinants, and showed that these isolates were of haplotype H58. The XDR S. Typhi clone encodes a chromosomally located resistance region and harbors a plasmid encoding additional resistance elements, including the bla CTX-M-15 extended-spectrum β-lactamase, and carrying the qnrS fluoroquinolone resistance gene. This antibiotic resistance-associated IncY plasmid exhibited high sequence identity to plasmids found in other enteric bacteria isolated from widely distributed geographic locations. This study highlights three concerning problems: the receding antibiotic arsenal for typhoid treatment, the ability of S. Typhi to transform from MDR to XDR in a single step by acquisition of a plasmid, and the ability of XDR clones to spread globally.

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Author and article information

Contributors

Carlos Manuel Franco: Role: Academic Editor

Susana Ferreira: Role: Academic Editor

Journal

Journal ID (nlm-ta): Antibiotics (Basel)

Journal ID (iso-abbrev): Antibiotics (Basel)

Journal ID (publisher-id): antibiotics

Title: Antibiotics

Publisher: MDPI

ISSN (Electronic): 2079-6382

Publication date (Electronic): 28 June 2021

Publication date Collection: July 2021

Volume: 10

Issue: 7

Electronic Location Identifier: 785

Affiliations

[1 ]Atta Ur Rahman School of Applied Biosciences (ASAB), National University of Sciences and Technology (NUST), H-12, Islamabad 44000, Pakistan; mabubakar.asab@ 123456asab.nust.edu.pk (A.S.); saraazim94@ 123456gmail.com (S.A.); amjad.ali@ 123456asab.nust.edu.pk (A.A.); saadia.andleeb@ 123456asab.nust.edu.pk (S.A.)

[2 ]Animal Health Program, Animal Sciences Institute, National Agriculture Research Centre, Park Road, Islamabad 44000, Pakistan; draitzaz786@ 123456gmail.com

[3 ]Department of Biosciences, Faculty of Sciences, COMSATS University Islamabad, Park Road, Islamabad 44000, Pakistan; m.imran@ 123456comsats.edu.pk

Author notes

[* ]Correspondence: a.rahman@ 123456asab.nust.edu.pk

Author information

Amjad Ali https://orcid.org/0000-0002-0486-4661

Abdur Rahman https://orcid.org/0000-0002-0393-5384

Article

Publisher ID: antibiotics-10-00785

DOI: 10.3390/antibiotics10070785

PMC ID: 8300803

PubMed ID: 34203245

SO-VID: 892a0ed6-aa88-408b-b12a-4fe75fe089cd

License:

Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( https://creativecommons.org/licenses/by/4.0/).

Antimicrobial Resistance Profiling of Biofilm Forming Non Typhoidal Salmonella enterica Isolates from Poultry and Its Associated Food Products from Pakistan

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Pakistan Journal of Nuclear Medicine (PJNM)

Most cited references 60

The global burden of nontyphoidal Salmonella gastroenteritis.

A modified microtiter-plate test for quantification of staphylococcal biofilm formation.

Emergence of an Extensively Drug-Resistant Salmonella enterica Serovar Typhi Clone Harboring a Promiscuous Plasmid Encoding Resistance to Fluoroquinolones and Third-Generation Cephalosporins

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