Environmental pollution is a serious problem that can cause sicknesses, fatality, and biological contaminants such as bacteria, which can trigger allergic reactions and infectious illnesses. There is also evidence that environmental pollutants can have an impact on the gut microbiome and contribute to the development of various mental health and metabolic disorders. This study aimed to study the antibiotic resistance and virulence potential of environmental Pseudomonas aeruginosa (P. aeruginosa) isolates in slaughterhouses. A total of 100 samples were collected from different slaughterhouse tools. The samples were identified by cultural and biochemical tests and confirmed by the VITEK 2 system. P. aeruginosa isolates were further confirmed by CHROMagar™ Pseudomonas and genetically by rpsL gene analysis. Molecular screening of virulence genes (fimH, papC, lasB, rhlI, lasI, csgA, toxA, and hly) and antibiotic resistance genes (blaCTX-M, blaAmpC, blaSHV, blaNDM, IMP-1, aac(6')-Ib-, ant(4')IIb, mexY, TEM, tetA, and qnrB) by PCR and testing the antibiotic sensitivity, biofilm formation, and production of pigments, and hemolysin were carried out in all isolated strains. A total of 62 isolates were identified as P. aeruginosa. All P. aeruginosa isolates were multidrug-resistant and most of them have multiple resistant genes. blaCTX-M gene was detected in all strains; 23 (37.1%) strains have the ability for biofilm formation, 33 strains had virulence genes, and 26 isolates from them have more than one virulence genes. There should be probably 60 (96.8%) P. aeruginosa strains that produce pyocyanin pigment. Slaughterhouse tools are sources for multidrug-resistant and virulent pathogenic microorganisms which are a serious health problem. Low-hygienic slaughterhouses could be a reservoir for resistance and virulence genes which could then be transferred to other pathogens.

Branch of Biotechnology Department of Biology College of Science Mustansiriyah University POX 10244 Baghdad Iraq

Branch of Microbiology Department of Biology College of Science Mustansiriyah University POX 10244 Baghdad Iraq

Department of Bacteriology Immunology and Mycology Faculty of Veterinary Medicine Suez Canal University Ismailia 41522 Egypt

Department of Biology College of Science Princess Nourah Bint Abdulrahman University P O Box 84428 Riyadh 11671 Saudi Arabia

Department of Dentistry Al Rasheed University College Baghdad Iraq

Department of Medical Microbiology and Immunology Faculty of Medicine Assiut University Assiut Egypt

Department of Microbiology and Immunology Faculty of Pharmacy Deraya University Minya Egypt

Department of Pharmacology and Therapeutics Faculty of Veterinary Medicines Damanhour University Damanhour 22511 Egypt

Departmentt of Physics College of Science University of Mosul Mosul Iraq

See more in PubMed

Adetunde LA, Glover RLK, Oliver AWO, Samuel T (2011) Source and distribution of microbial contamination on beef and Chevron in Navrongo. Kassena Nankana District of Upper East Region in Ghana. J Anim Prod Adv 1:21–28

Algammal AM, Mabrok M, Sivaramasamy E, Youssef FM, Atwa MH, El-Kholy AW, Hetta HF, Hozzein WN (2020) Emerging MDR-Pseudomonas aeruginosa in fish commonly harbor oprL and toxA virulence genes and blaTEM, blaCTX-M, and tetA antibiotic-resistance genes. Sci Rep 10:1–12 DOI

AL-Jubori SS, AL-kadmy IM, JassimAl-Ani Z (2016) Emergence of multidrug resistance (MDR) Acinetobacterbaumannii isolated from Iraqi hospitals. Adv Environ Biol 10:265–276

Al-Kadmy IMS, Ali ANM, Salman IMA, Khazaal SS (2018) Molecular characterization of Acinetobacter baumannii isolated from Iraqi hospital environment. New Microbes New Infect 21:51–57 PubMed DOI

Allen L, Dockrell DH, Pattery T, Lee DG, Cornelis P, Hellewell PG, Whyte MKB (2005) Pyocyanin production by Pseudomonas aeruginosa induces neutrophil apoptosis and impairs neutrophil-mediated host defenses in vivo. J Immunol 174:3643–3649 PubMed DOI

Alum EA, Urom SMOC, Ben CMA (2016) Microbiological contamination of food: the mechanisms, impacts and prevention. Int J Sci Technol Res 5:65–78

Auda IG, Al-Kadmy IM, Kareem SM, Lafta AK, A’Affus MHO, Khit IAA, Al Kheraif AA, Divakar DD, Ramakrishnaiah R (2017) RAPD-and ERIC-based typing of clinical and environmental Pseudomonas aeruginosa isolates. J AOAC Int 100(2):532–536 PubMed DOI

Aziz SN, Abid SA, Al-Alak SK, Kadmy IA, Rheima AM (2022) Spread of ESβL-producing Escherichia coli and the anti-virulence effect of graphene nano-sheets. Arch Microbiol 204:1–8 DOI

Bakhtiary F, Sayevand HR, Remely M, Hippe B, Hosseini H, Haslberger AG (2016) Evaluation of bacterial contamination sources in meat production line. J Food Qual 39:750–756 DOI

Barbhaiya HB, Rao KK (1985) Production of pyoverdine, the fluorescent pigment of Pseudomonas aeruginosa PAO1. FEMS Microbiol Lett 27:233–235 DOI

Behravesh CB, Williams IT, Tauxe RV (2012) Emerging foodborne pathogens and problems: expanding prevention efforts before slaughter or harvest. In Improving food safety through a one health approach: workshop summary. National Academies Press (US)

Bintsis T (2017) Foodborne pathogens. AIMS Microbiol 3:529 PubMed DOI PMC

Bintsis T (2018) Microbial pollution and food safety. AIMS Microbiol 4:377 PubMed DOI PMC

Capita R, Cordero J, Molina-González D, Igrejas G, Poeta P, Alonso-Calleja C (2019) Phylogenetic diversity, antimicrobial susceptibility and virulence characteristics of Escherichia coli isolates from pigeon meat. Antibiotics 8:259 PubMed DOI PMC

Carniel E (2001) The Yersinia high-pathogenicity island: an iron-uptake island. Microbes Infect 3:561–569 PubMed DOI

Cotar AI, Chifiriuc MC, Dinu S, Pelinescu D, Banu O, Lazãr V (2010) Quantitative real-time PCR study of the influence of probiotic culture soluble fraction on the expression of Pseudomonas aeruginosa quorum sensing genes. Roum Arch Microbiol Immunol 69:213–223 PubMed

Cramer N, Klockgether J, Wrasman K, Schmidt M, Davenport CF, Tümmler B (2011) Microevolution of the major common Pseudomonas aeruginosa clones C and PA14 in cystic fibrosis lungs. Environ Microbiol 13:1690–1704 PubMed DOI

Desvaux M, Dalmasso G, Beyrouthy R, Barnich N, Delmas J, Bonnet R (2020) Pathogenicity factors of genomic islands in intestinal and extraintestinal Escherichia coli. Front Microbiol 2065

Dobrindt U, Hochhut B, Hentschel U, Hacker J (2004) Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2:414–424 PubMed DOI

Doulgeraki AI, Ercolini D, Villani F, Nychas G-J (2012) Spoilage microbiota associated to the storage of raw meat in different conditions. Int J Food Microbiol 157:130–141 PubMed DOI

El-Baky A, Rehab M, Masoud SM, Mohamed DS, Waly NGFM, Shafik EA, Mohareb DA, Elkady A, Elbadr MM, Hetta HF (2020) Prevalence and some possible mechanisms of colistin resistance among multidrug-resistant and extensively drug-resistant Pseudomonas aeruginosa. Infect Drug Resist 13:323 DOI

El-Fouly MZ, Sharaf AM, Shahin AAM, El-Bialy HA, Omara AMA (2015) Biosynthesis of pyocyanin pigment by Pseudomonas aeruginosa. Int j Recent Res Appl Stud 8:36–48

Elmaraghy N, Abbadi S, Elhadidi G, Hashem A, Yousef A (2019) Virulence genes in Pseudomonas aeruginosa strains isolated at Suez Canal University Hospitals with respect to the site of infection and antimicrobial resistance. Int J Clin Microbiol Biochem Technol 2:8–19 DOI

Farhan SM, Ibrahim RA, Mahran KM, Hetta HF, Abd El-Baky RM (2019) ‘Antimicrobial resistance pattern and molecular genetic distribution of metallo-β-lactamases producing Pseudomonas aeruginosa isolated from hospitals in Minia. Egypt’, Infect Drug Resist 12:2125–2133 PubMed DOI

Freeman DJ, Falkiner FR, Keane CT (1989) New method for detecting slime production by coagulase negative staphylococci. J Clin Pathol 42:872–874 PubMed DOI PMC

Gajic I, Kabic J, Kekic D, Jovicevic M, Milenkovic M, Culafic DM, Trudic A, Ranin L, Opavski N (2022) Antimicrobial susceptibility testing: a comprehensive review of currently used methods. Antibiotics 11:427 PubMed DOI PMC

Gal-Mor O, Brett Finlay B (2006) Pathogenicity islands: a molecular toolbox for bacterial virulence. Cell Microbiol 8:1707–1719 PubMed DOI

Hetta HF, Ramadan YN, Al-Harbi AI, Ahmed E, Battah B, Abd Ellah NH, Zanetti S, Donadu MG (2023) Nanotechnology as a promising approach to combat multidrug resistant bacteria: a comprehensive review and future perspectives. Biomedicines 11

Kao C-Y, Chen C-A, Liu Y-F, Hsiu-Mei Wu, Chiou C-S, Yan J-J, Jiunn-Jong Wu (2017) Molecular characterization of antimicrobial susceptibility of Salmonella isolates: first identification of a plasmid carrying qnrD or oqxAB in Taiwan. J Microbiol Immunol Infect 50:214–223 PubMed DOI

Karami N, Wold AE, Adlerberth I (2017) Antibiotic resistance is linked to carriage of papC and iutA virulence genes and phylogenetic group D background in commensal and uropathogenic Escherichia coli from infants and young children. Eur J Clin Microbiol 36:721–729 DOI

Kareem SM, Al-Kadmy IMS, Al-Kaabi MH, Aziz SN, Ahmad M (2017) Acinetobacter baumannii virulence is enhanced by the combined presence of virulence factors genes phospholipase C (plcN) and elastase (lasB). Microb Pathog 110:568–572 PubMed DOI

Kiani S, Momtaz H, Serajian AA, Tajbakhsh E (2016) Detection of integrons in Acinetobacter baumannii strains isolated from the nosocomial infections of Ahvaz city and their relation with the resistance pattern. Int J Med Lab 3:50–63

Klockgether J, Cramer N, Wiehlmann L, Davenport CF, Tümmler B (2011) Pseudomonas aeruginosa genomic structure and diversity. Front Microbiol 2:150 PubMed DOI PMC

Kurioka S, Liu PV (1967) Effect of the hemolysin of Pseudomonas aeruginosa on phosphatides and on phospholipase C activity. J Bacteriol 93:670–674 PubMed DOI PMC

Laverty G, Gorman SP, Gilmore BF (2014) Biomolecular mechanisms of Pseudomonas aeruginosa and Escherichia coli biofilm formation. Pathogens 3:596–632 PubMed DOI PMC

Lerma L, Leyre NB, del Carmen M, Muñoz C, Gálvez A, Abriouel H (2014) Antibiotic multiresistance analysis of mesophilic and psychrotrophic Pseudomonas spp. isolated from goat and lamb slaughterhouse surfaces throughout the meat production process. Appl Environ Microbiol 80:6792–6806 DOI

Liao C-H, Hsueh P-R, Jacoby GA, Hooper DC (2013) Risk factors and clinical characteristics of patients with qnr-positive Klebsiella pneumoniae bacteraemia. J Antimicrob Chemother 68:2907–2914 PubMed DOI PMC

Magiorakos A-P, Srinivasan A, Carey RB, Yehuda Carmeli ME, Falagas CGG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18:268–281 PubMed DOI

Makharita RR, El-Kholy I, Hetta HF, Abdelaziz MH, Hagagy FI, Ahmed AA, Algammal AM (2020) Antibiogram and genetic characterization of carbapenem-resistant Gram-negative pathogens incriminated in healthcare-associated infections. Infect Drug Resist 13:3991–4002 PubMed DOI PMC

Mathee K, Narasimhan G, Valdes C, Qiu X, Matewish JM, Koehrsen M, Rokas A, Yandava CN, Engels R, Zeng E (2008) Dynamics of Pseudomonas aeruginosa genome evolution. Proc Natl Acad Sci 105:3100–3105 PubMed DOI PMC

Mertz AW, Koo OK, O'Bryan CA, Morawicki R, Sirsat SA, Neal JA, Crandall PG, Ricke SC (2014) Microbial ecology of meat slicers as determined by denaturing gradient gel electrophoresis. Food Control 42:242–47

Moretro T, Solveig L, Even H (2013) Bacteria on meat abattoir process surfaces after sanitation: characterisation of survival properties of Listeria monocytogenes and the commensal bacterial flora. Adv Microbiol

Muhsin EA, Said LA, Al-Jubori SS (2022) Correlation of type 1 and type 3 Fimbrial genes with the type of specimen and the antibiotic resistance profile of clinically isolated Klebsiella pneumoniae in Baghdad. Al-Mustansiriyah Journal of Science 33(3):1–11 DOI

Nageeb WM, Hetta HF (2022) The predictive potential of different molecular markers linked to amikacin susceptibility phenotypes in Pseudomonas aeruginosa. PLoS ONE 17:e0267396 PubMed DOI PMC

Olsén A, Wick MJ, Mörgelin M, Björck L (1998) Curli, fibrous surface proteins of Escherichia coli, interact with major histocompatibility complex class I molecules. Infect Immun 66:944–949 PubMed DOI PMC

Percival SL, Williams D, Cooper T, Randle J (2014) Biofilms in infection prevention and control: a healthcare handbook (Academic Press)

Reeves PP, and L Wang (2002) Pathogenicity islands and the evolution of pathogenic microbes

Roy PH, Tetu SG, Larouche A, Elbourne L, Tremblay S, Ren Q, Dodson R, Harkins D, Shay R, Watkins K (2010) Complete genome sequence of the multiresistant taxonomic outlier Pseudomonas aeruginosa PA7. PLoS ONE 5:e8842 PubMed DOI PMC

Sallman RS, Hussein SS, Ali MR (2018) ERIC-PCR typing, RAPD-PCR fingerprinting and quorum sensing gene analysis of Pseudomonas aeruginosa isolated from different clinical sources. Al-Mustansiriyah Journal of Science 29(2):50–62 DOI

Sansonetti P (1993) Pseudomonas aeruginosa as an opportunistic pathogen: Campa, M., Bendinelli, & M. Friedman, H. 1 vol.(15, 5× 23, 5 cm), 419+ xx pages. Plenum Press, New York, 1993. In.: Elsevier Masson

Schmidt H, Hensel M (2004) Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev 17:14–56 PubMed DOI PMC

Xavier DE, Picão RC, Girardello R, Fehlberg LCC, Gales AC (2010) Efflux pumps expression and its association with porin down-regulation and β-lactamase production among Pseudomonas aeruginosa causing bloodstream infections in Brazil. BMC Microbiol 10:1–7 DOI