The Relationship of Antimicrobial Sensitivity and Biofilm Formation of Salmonella spp. Isolated from Broiler Chicken Farms in Biskra, Algeria | ||
| Journal of Applied Veterinary Sciences | ||
| Article 12, Volume 10, Issue 2, April 2025, Pages 98-109 PDF (508.83 K) | ||
| Document Type: Original Article | ||
| DOI: 10.21608/javs.2025.355680.1522 | ||
| Authors | ||
| Hana Nedjma Belabed1; Nouzha Heleili2; Ammar Ayachi* 3; Moussa Chergui1; Omar Bennoune2 | ||
| 1Laboratory of Diversity of Ecosystems and Dynamics of Agricultural Production Systems in Arid Zones (DEDSPAZA).SE/SNV Faculty, University of Mohamed Kheider, Biskra, Algeria | ||
| 2Laboratory of Health, Animal Production and Environment (ESPA), Institute of Veterinary and Agricultural Sciences, University of Batna 1, Batna, Algeria; Department of Veterinary Sciences, Institute of Veterinary and Agricultural Sciences, University of Batna 1, Batna, Algeria | ||
| 3Department of Veterinary Sciences, Institute of Veterinary and Agricultural Sciences, University of Batna 1, Batna, Algeria, Laboratory of Biotechnology of Bioactive Molecules and Cellular Physiopathology (LBBMPC), University of Batna 2, Batna, Algeria | ||
| Abstract | ||
| Salmonella is a pathogen implicated in foodborne illnesses. Antibiotic resistance in Salmonella has emerged and is increasingly prevalent, posing a significant global problem. The current study aimed to study the antimicrobial resistance and biofilm formation capacity of Salmonella spp. isolated from broiler chicken farms in Biskra, Algeria. Two hundred and seventy samples were collected from various sources within broiler chicken farms (fecal matter, cloacal swabs, surface swabs, reservoir water, and water from final dispenser lines). Conventional methods were used to isolate and identify Salmonella species and confirmed using API 20E test strips, and the disk diffusion method was used to perform a sensitivity test, in addition to the crystal violet microtiter plate method to assay the biofilm formation capacity of the isolates. 45 strains isolated with a prevalence of 16.66%. The result of the sensitivity test showed resistance against ampicillin, Ciprofloxacin and tetracycline at 97.78%, 95,56% and 91.11%, respectively. Meanwhile, the third-generation cephalosporins and cefadroxil showed moderate sensitivity. The results also showed a difference in the ability of the isolates to produce biofilms; most of them were weak, medium and non-productive biofilms at a rate of 55.56%, 37.78% and 6.67%, respectively. A negative correlation of a statistically significant relationship between antibiotic resistance and the capacity for biofilm formation in strains of Salmonella was observed. This study revealed a high prevalence of antibiotic resistance of Salmonella strains isolated from broiler chicken farms, indicating the necessity for effective measures to ensure food safety in the poultry industry in Algeria. | ||
| Keywords | ||
| Algeria; Antibiotic resistance; Biofilm formation; Broiler chicken farms; Salmonella spp | ||
| References | ||
|
ABDI, R. D., MENGSTIE, F., BEYI, A. F., BEYENE, T., WAKTOLE, H., MAMMO, B., and ABUNNA, F., 2017. Determination of the sources and antimicrobial resistance patterns of Salmonella isolated from the poultry industry in Southern Ethiopia. BMC infectious diseases, 17, 1-12.www.doi.org/10.1186/s12879-017-2437-2
AGARWAL, R. K., SINGH, S., BHILEGAONKAR, K. N., and SINGH, V. P., 2011. Optimization of microtiter plate assay for the testing of biofilm formation ability in different Salmonella serotypes. International Food Research Journal, 18(4), 1493.
AL-ZENKI, S., AL-NASSER, A., AL-SAFAR, A., ALOMIRAH, H., AL-HADDAD, A., HENDRIKSEN, R. S., and AARESTRUP, F. M., 2007. Prevalence and antibiotic resistance of Salmonella isolated from a poultry farm and processing plant environment in the State of Kuwait. Foodborne pathogens and disease, 4(3), 367-373.https://doi.org/10.1089=fpd.2007.0017
CA-SFM,Vet 2023. Breakpoints Tables for Interpretation of MICs and Zone Diameters. Veterinary recommendations. https://www.sfm-microbiologie.org/wp-content/uploads/2023/06/CASFM_VET2023.pdf.
ARKALI A., and CETINKAYA B., 2020. Molecular identification and antibiotic resistance profiling of Salmonella species isolated from chickens in eastern Turkey. BMC Vet Res. Dec; 16(1), 205.https://doi.org/10.1186/s12917-020-02425-0
ASSOUMY, M. A., BEDEKELABOU, A. P., TEKO-AGBO, A., OSSEBI, W., AKODA, K., NIMBONA, F., and BADA-ALAMBEDJI, R., 2021. Antibiotic resistance of Escherichia coli and Salmonella spp. strains isolated from healthy poultry farms in the districts of Abidjan and Agnibilékrou (Côte d’Ivoire). Veterinary World, 14(4), 1020.www.doi.org/10.14202/vetworld.2021.1020-1027
AYACHI, A., ALLOUI, N., BENNOUNE, O., and KASSAH-LAOUAR, A., 2009. Survey of Salmonella serovars in broilers and laying breeding reproducers in east of Algeria. The Journal of Infection in Developing Countries, 4(02), 103–106.https://doi.org/10.3855/jidc.562
BORGES, K.A., FURIAN, T.Q., SOUZA, S.N., MENEZES, R., TONDO, E.C., SALLE, C.T.P., MORAES, H.L.S. and NASCIMENTO, V.P. 2018. Biofilm formation capacity of Salmonella serotypes at different temperature conditions. Pesq. Vet. Bras. 38(1):71- 76.https://dx.doi.org/10.1590/1678-5150-PVB-4928
BOUGHABA, A., ABERKANE, S., FOURAR, Y. O., and DJEBABRA, M., 2019. Study of safety culture in healthcare institutions: case of an Algerian hospital. International journal of health care quality assurance, 32(7), 1081-1097.https://doi.org/10.1108/IJHCQA-09-2018-0229
BRITO, D. A., OBA, A., PAIÃO, F. G., and FERREIRA, B. L., 2024. Antimicrobial multiresistance and biofilm formation in Salmonella enterica isolated from broiler production chain. Pesquisa Veterinária Brasileira, 44, e07463.https://doi.org/10.1590/1678-5150-PVB-7463
CARRIQUE-MAS, J. J., and DAVIES, R. H., 2008. Sampling and bacteriological detection of Salmonella in poultry and poultry premises: a review. Revue scientifique et technique (International Office of Epizootics), 27(3), 665-677.https://doi.org/10.20506/rst.27.3.1829
CASTRO VARGAS, R.E., HERRERA SANCHEZ,. MP., RODRIGUEZ HERNANDEZ, R., and RONDON BARRAGAN, I.S., 2020. Antibiotic resistance in Salmonella spp. Isolated from poultry : A global overview. Veterinary World, 13(10): 2070-2084. https://www.doi.org/10.14202/vetworld.2020.2070-2084
CIGE, H. Y., OMOTOSHO, O. O., and IBRAHIM, A. M., 2023. Evaluation of Antibiotic Resistance Pattern of Escherichia Coli and Salmonella Species Isolated from Cloaca of Indigenous Chickens in Live-bird Markets in Marodi Jeh Region, Somalia. Journal of Applied Veterinary Sciences, 8(2), 44-54.https://dx.doi.org/10.21608/javs.2023.179843.1200
COSBY, D. E., COX, N. A., HARRISON, M. A., WILSON, J. L., BUHR, R. J., and FEDORKA-CRAY, P. J., 2015. Salmonella and antimicrobial resistance in broilers: A review. Journal of Applied Poultry Research, 24(3), 408-426.https://doi.org/10.3382/japr/pfv038
COURVALAIN, P., and LECLERQ, R. 2012. Antibiogramme. 3rd ed. ESKA, Paris, France, p800.
CWIEK, K., KORZEKWA, K., TABIS, A., BANIA, J., BUGLA-PLOSKONSKA, G., and WIELICZKO, A., 2020. Antimicrobial resistance and biofilm formation capacity of Salmonella enterica serovar Enteritidis strains isolated from poultry and humans in Poland. Pathogens, 9(8), 643.https://doi.org/10.3390/pathogens9080643
DJEFFAL, S., MAMACHE, B., ELGROUD R., HIRECHE, S., and BOUAZIZ O., 2018. Prevalence and risk factors for Salmonella spp. Contamination in broiler chicken farms and slaughterhouses in the northeast of Algeria, Veterinary World, 11(8): 1102.https://doi.org/10.14202/vetworld.2018.1102-1108
EFSA and ECDC, 2020. The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2017/2018. EFSA J. 18(3) :6007. https://dx.doi.org/10.2903/j.efsa.2020.6007
EUCAST, 2024. General technical conditions for diffusion methods Recommendations. V.1.0 Juin.14.http://www.eucast.org
FAKOREDE, C. O., AMISU, K. O., SAKI, M., and AKINYEMI, K. O., 2023. Co-existence of extended-spectrum β-lactamases bla CTX-M-9 and bla CTX-M-15 genes in Salmonella species isolated from febrile and diarrhoeagenic patients in Lagos, Nigeria: a cross-sectional study. European Journal of Medical Research, 28(1), 3.https://doi.org/10.1186/s40001-022-00960-0
PENHA FILHO, R. A. C., FERREIRA, J. C., KANASHIRO, A. M. I., DARINI, A. L. D. C., and BERCHIERI, A., 2016. Antimicrobial susceptibility of Salmonella Gallinarum and Salmonella Pullorum isolated from ill poultry in Brazil. Ciência Rural, 46(3), 513-518.https://doi.org/10.1590/0103-8478cr20150398
FOX, L.K., ZADOKS, R.N., and GASKINS, C.T., 2005. Biofilm production by Staphylococcus aureus associated with Intramammary infection. Vet Microbiol; 107: 295–9.https://doi.org/10.1016/j.vetmic.2005.02.005
GALLOWAY, W. R., HODGKINSON, J. T., BOWDEN, S., WELCH, M., and SPRING, D. R., 2012. Applications of small molecule activators and inhibitors of quorum sensing in Gram-negative bacteria. Trends in microbiology, 20(9), 449-458.www.doi.org/10.1016/j.tim.2012.06.003
GHARAIBEH, M.H., LAFI, S.Q., HABIB-ALLAH, A.M., and ALQUDSI, F.R., 2024. Occurrence, virulence, and resistance genes in Salmonella enterica isolated from an integrated poultry company in Jordan Poultry Science. 103:103733.https://doi.org/10.1016/j.psj.2024.103733
GILBERT, P., ALLISON, D. G., and MCBAIN, A. J., 2002. Biofilms in vitro and in vivo : do singular mechanisms imply cross-resistance ? Journal of applied microbiology, 92.https://doi.org/10.1046/j.1365-2672.92.5s1.5.x
GUECHTOULI, S., MESSAI, C. R., MORSLI, A., HAMDI, T. M., and KHELEF, D., 2024. Isolation, Identification, and Antibiotic Resistance of Salmonella Spp. Strains Isolated from Broilers and Layer Hens in The Central Region of Algeria. Egyptian Journal of Veterinary Sciences, 1-12.www.doi.org/10.21608/EJVS.2024.321538.2379
HABIB, I., MOHAMED, M.Y.I.., LAKSHMI, G.B.., GHAZAWI, A., KHAN M., ABDALLAH, A., and ANES, F., 2024. High prevalence and genomic features of multidrug-resistant Salmonella enterica isolated from chilled broiler chicken on retail sale in the United Arab Emirates. International Journal of Food Microbiology 423-110828.https://doi.org/10.1016/j.ijfoodmicro.2024.110828
HAGRAS, R., MOSTAFA, N. F., SADAT, A., and AWAD, A., 2024. Characterization and antimicrobial susceptibility of Salmonella enterica isolated from broiler chicks. Mansoura Veterinary Medical Journal, 25(4), 2.https://doi.org/10.35943/2682-2512.1243
HASSAN, E. R., and ALHATAMI, A. O., 2019. Antimicrobial susceptibility profile of Salmonella enterica isolated from poultry farms using Vitek-2. Kufa Journal for Veterinary Medical Sciences, 10(1), 105-116.
INIGUEZ-MORENO M., GUTIERREZ-LOMELI M., GUERRERO-MEDINA P.J. and AVILA-NOVOA M.G., 2018. Biofilm formation by Staphylococcus aureus and Salmonella spp. under mono and dual-species conditions and their sensitivity to cetrimonium bromide, peracetic acid and sodium hypochlorite. Braz. J. Microbiol. 49(2) :310- 319.https://dx.doi.org/10.1016/j.bjm.2017.08.002
ISO 6579-1. 2017. Microbiology of food chain- Horizontal method for the detection, enumeration and serotyping of salmonella- Part1: Detection of Salmonella spp.
JIBRIL, A.H., OKEKE, I.N., DALSGAARD KUDIRKIENE, A.E, AKINLABI, O.C., BELLO, M.B., OLSEN, J.E., 2020. Prevalence and risk factors of Salmonella in commercial poultry farms in Nigeria PLoS ONE 15(9): e0238190. https://doi.org/10.1371/journal.pone.0238190
JULIANINGSIH, D., ALVARADO-MARTINEZ, Z., TABASHSUM, Z., TUNG, C., ADITYA A., KAPADIA S., MASKEY, S., MOHAPATRA, A., and BISWAS, D., 2024. Identification of Salmonella enterica biovars Gallinarum 1 and Pullorum and their antibiotic resistance pattern in integrated crop-livestock farms and poultry meats. Access Microbiology,6(9),000775-v6. https://doi.org/10.1099/acmi.0.000775.v3
KAMEL, K., MERGHAD, A., BAROUR, D., GHERISSI, D.E., and KHENENOU, T., 2024. High antimicrobial resistance rates and multidrug resistance in Enterobacteriaceae isolates from poultry in Souk Ahras region, Algeria, Veterinary World, 17(12): 2709–2718. www.doi.org/10.14202/vetworld.2024.2709-2718
LEILA DIB, A., CHAHED, A., LAKHDARA, N., AGABOU, A., BOUSSENA, S., GHOUGAL, K., and GAGAOUA, M., 2019. Preliminary investigation of the antimicrobial and mechanisms of resistance of Enterobacteria isolated from minced meat in the Northeast of Algeria: The case of butchers from Constantine. Integr Food Nutr Metab 6. https://doi.org/10.15761/IFNM.1000273
LEONHARD, M., ZATORSKA, B., MOSER, D., and SCHNEIDER STICKLER, B., 2019.Growth media for mixed multispecies oropharyngeal biofilm compositions on silicone. Biomed Res Int 1–8. https://doi.org/10.1155/2019/8051270
MAGDY, O. S., MOUSSA, I. M., HUSSEIN, H. A., EL-HARIRI, M. D., GHAREEB, A., HEMEG, H. A., and KABLI, S. A., 2020. Genetic diversity of Salmonella enterica recovered from chickens’ farms and its potential transmission to human. Journal of Infection and Public Health, 13(4), 571-576.https://doi.org/10.1016/j.jiph.2019.09.007
MOHAMMED, Y., and DUBIE, T. 2022. Isolation, identification and antimicrobial susceptibility profile of Salmonella isolated from poultry farms in Addis Ababa, Ethiopia. Veterinary Medicine and Science, 8(3), 1166-1173.https://doi.org/10.1002/vms3.762
MUSA, L., TOPPI, V., STEFANETTI, V., SPATA, N., RAPI, M.C., GRILLI, G., ADDIS, M.F., DI GIACINTO, G., FRANCIOSINI, M.P. and PROIETTI, P.C. 2024. High biofilm-forming multidrug resistant Salmonella Infantis strains from the poultry production chain. Antibiotics 13:595.https://dx.doi.org/10.3390/antibiotics13070595
MRIDHA, D., UDDIN, M. N., ALAM, B., AKHTER, A. T., ISLAM, S. S., ISLAM, M. S., and KABIR, S. L., 2020. Identification and characterization of Salmonella spp. from samples of broiler farms in selected districts of Bangladesh. Veterinary world, 13(2), 275.www.doi.org/10.14202/vetworld.2020.275-283
MOGHADAM, M.N., RAHIMI, E., SHAKERIAN, A., and MOMTAZ, H., 2023. Prevalence of Salmonella Typhimurium and Salmonella Enteritidis isolated from poultry meat: virulence and antimicrobial-resistant genes. BMC Microbiology 23:168.https://doi.org/10.1186/s12866-023-02908-8
NAIR, A., RAWOOL, D.B., DOIJAD, S., POHARKAR, K., MOHAN, V., BARBUDDHE, S.B., KOLHE, R., KURKURE, N.V., KUMAR, A., S.V.S., and BALASARAVANAN, T., 2015. Biofilm formation and genetic diversity of Salmonella isolates recovered from clinical, food, poultry and environmental sources. Infection, Genetics and Evolution, 36: 424-433. https://doi.org/10.1016/j.meegid.2015.08.012
NGUYEN, T. K., NGUYEN, L. T., CHAU, T. T. H., NGUYEN, T. T., TRAN, B. N., TANIGUCHI, T., HAYASHIDANI, H., and Ly, K. T. L., 2021.Prevalence and antibiotic resistance of Salmonella isolated from poultry and its environment in the Mekong Delta, Vietnam. Veterinary World, 14(12), 3216-3223.https://doi.org/10.14202/vetworld.2021.3216-3223
OGU, G.I., OKOLO, J.C., IGBORGBOR, F.I., and AKINNIBOSUN, F.I., 2021. Multidrug-resistance and biofilm formation profiles of Salmonella spp. isolated from raw chicken meat. Novel Research in Microbiology Journal, 5(2): 1214-1226.https://doi.org/10.21608/nrmj.2021.164551
O'Toole, G. A. 2011. Microtiter dish biofilm formation assay. Journal of visualized experiments: JoVE, (47), 2437.https://doi.org/10.3791/2437
OUESLATI, W., RJEIBI, M. R., BENYEDEM, H., MAMLOUK, A., SOUISSI, F., SELMI, R., and ETTRIQUI, A., 2021. Prevalence, risk factors, antimicrobial resistance and molecular characterization of Salmonella in Northeast Tunisia broiler flocks. Veterinary Sciences, 9(1), 12.https://doi.org/10.3390/vetsci9010012
PUI, CF., WONG, C., CHAI, L.C., LEE, H.Y., NOORLIS, A., ZAINAZOR, C., TANG, J.Y., GHAZALI, F.M., CHEAHY, K., NAKAGUCHI, Y., NISHIBUCHI, M., and RADU, S., 2011. Multiplex PCR for the concurrent detection and differentiation of Salmonella spp. Salmonella Typhi and Salmonella Typhimurium. Tropical medicine and health, 39(1), 9-15.https://doi.org/10.2149/tmh.2010-20
REGHAIS, A., DROUICHE, A., ZAHI, F., and DEBIECHE, T. H., 2023. Hydrogeochemical evaluation of the Terminal Complex aquifer system in an arid area: a case study from the Biskra region, north-east Algeria. Environmental Earth Sciences, 82(7), 182.https://doi.org/10.1007/s12665-023-10786-6
SAHA, M., and SARKAR, A., Review on multiple facets of drug resistance: a rising challenge in the 21st century. J Xenobiot. 2021 Dec 13; 11(4) :197–214.https://doi.org/10.3390/jox11040013
SAUER, K., STOODLEY, P., GOERES, D. M., Hall-STOODLEY, L., BURMØLLE, M., STEWART, P. S., and BJARNSHOLT, T. (2022). The biofilm life cycle: expanding the conceptual model of biofilm formation. Nature Reviews Microbiology, 20(10), 608-620.https://doi.org/10.1038/s41579-022-00767-0
SHAJI, S., SELVARAJ, R. K., and SHANMUGASUNDARAM, R., 2023. Salmonella infection in poultry: a review on the pathogen and control strategies. Microorganisms, 11(11), 2814.https://doi.org/10.3390/microorganisms11112814
SINGH, R., YADAV, A. S., TRIPATHI, V., and SINGH, R. P., 2013. Antimicrobial resistance profile of Salmonella present in poultry and poultry environment in north India. Food Control, 33(2), 545-548.https://doi.org/10.1016/j.foodcont.2013.03.041
SLEIMAN, A., AWADA, B., MOCADIE, M., SHERRI, N., HARAOUI, L.P., BABY, V., ARAJ, G.F., KANJ, S.S., RIZK,N., MATAR, G.M., and ABOU FAYAD, A.G., 2021. An unequivocal superbug: PDR Klebsiella pneumoniae with an arsenal of resistance and virulence factor genes. JIDC., 15(03): 404-414.https://doi.org/10.3855/jidc.13573
STEPANOVIC, S., ĆIRKOVIC, I., RANIN, L., and S✓ VABIC‐VLAHOVIC, M., 2004. Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Letters in applied microbiology, 38(5), 428-32.https://doi.org/10.1111/j.1472-765X.2004.01513.x
STEPANOVIC, S., VUKOVIC, D., HOLA, V., BONAVENTURA, G. D., DJUKIC, S., ĆIRKOVIC, I., and RUZICKA, F., 2007. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. Apmis, 115(8), 891-899.https://doi.org/10.1111/j.1600-0463.2007.apm_630.x
VOSS-RECH, D., ZIECH, R. E., VAZ, C. S. L., COLDEBELLA, A., KUCHIISHI, S. S., BALZAN, C., and BOTTON, S. A., 2023. Association between antimicrobial resistance and biofilm forming ability of Salmonella enterica serotypes from commercial broiler farms in Brazil. British Poultry Science, 64(2), 224-230.https://doi.org/10.1080/00071668.2022.2136511
WAGHAMARE, R. N., PATURKAR, A. M., VAIDYA, V. M., ZENDE, R. J., DUBAL, Z. N., DWIVEDI, A., and GAIKWAD, R. V., 2018. Phenotypic and genotypic drug resistance profile of Salmonella serovars isolated from poultry farm and processing units located in and around Mumbai city, India. Veterinary world, 11(12), 1682.www.doi.org/10.14202/vetworld.2018.1682-1688
WAJID, M., SALEEMI, M. K., SARWAR, Y., and ALI, A., 2019. Detection and characterization of multidrug‐resistant Salmonella enterica serovar Infantis as an emerging threat in poultry farms of Faisalabad, Pakistan. Journal of applied microbiology, 127(1), 248-261.https://doi.org/10.1111/jam.14282
WANG, X., WANG, H., LI, T., LIU, F., CHENG, Y., GUO, X., and ZHANG, T. 2020. Characterization of Salmonella spp. isolated from chickens in Central China. BMC veterinary research, 16, 1-9.https://doi.org/10.1186/s12917-020-02513-1
WIBISONO, FJ., RAHMANIAR, R.P., SYAPUTRA, D.E., ZURIYA, Z., AZIZ, K.M., IKENG, L.D., EFFENDI, M.H., and BERNARD, A.N., 2023. Risk factors for non-typhoidal Salmonella contamination in chicken meat : A cross-sectional study on traditional markets in Surabaya. Adv Life Sci 10 (2): 282-288.http://dx.doi.org/10.62940/als.v10i2.1793
WORLD HEALTH ORGANIZATION (WHO), 2018. Salmonella (non-typhoidal). Available at:https://www.who.int/news-room/factsheets/detail/salmonella.
YANG, X., HUANG, J., WU Q, ZHANG, J., LIU S., GUO, W., CAI, S., and YU, S., 2015.Prevalence, antimicrobial resistance and genetic diversity of Salmonella isolated from retail ready-to-eat foods in China. Food Control, 60: 50-56.http://www.sciencedirect.com/science/journal/09567135
ZAHLI, R., ANN, K.S., JAMAL, A., JOSÉ, L., COPA, P., AMAJOUD, N., SKALI, S.N., and JUAN, S., 2022. Salmonella spp: Prevalence, antimicrobial resistance and molecular typing of strains isolated from poultry in Tetouan-Morocco, LWT Food Science and Technology 153-112359. https://doi.org/10.1016/j.lwt.2021.112359 | ||
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