{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T16:19:34Z","timestamp":1792685974123,"version":"4.5.0"},"reference-count":52,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2021,9,9]],"date-time":"2021-09-09T00:00:00Z","timestamp":1631145600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>The burden of antimicrobial use in agricultural settings is one of the greatest challenges facing global health and food security in the modern era. Malaysian poultry operations are a relevant but understudied component of epidemiology of antimicrobial resistance. We aimed to identify the prevalence, resistance patterns, and risk factors associated with Salmonella isolates from poultry farms in three states of East Coast Peninsular Malaysia. Between 8 February 2019 and 23 February 2020, a total of 371 samples (cloacal swabs = 259; faecal = 84; Sewage = 14, Tap water = 14) was collected from poultry operations. Characteristics of the sampled farms and associated risk factors were obtained using semi-structured questionnaires. Presumptive Salmonella spp. isolates were identified based on colony morphology with subsequent biochemical and PCR confirmation. Susceptibility of isolates was tested against a panel of 12 antimicrobials using disk diffusion method. Our findings revealed that the proportion of Salmonella spp.-positive isolates across sample source were as following: cloacal swab (46.3%, 120\/259); faecal (59.5%, 50\/84); in tap water (14.3%, 2\/14); and in sewage sample (35.7%, 5\/14). Isolates from faecal (15.5%, 13\/84), cloacal (1.2%, 3\/259), and sewage (7.1%, 1\/14) samples were significantly resistant to at least five classes of antimicrobials. Resistance to Sulfonamides class (52%, 92\/177) was predominantly observed followed by tetracycline (39.5%, 70\/177) and aminoglycosides (35.6%, 63\/177). Multivariate regression analysis identified intensive management system (OR = 1.55, 95% CI = 1.00\u20132.40) as a leading driver of antimicrobial resistance (AMR) acquisition. A prevalence of resistance to common antimicrobials was recorded for sulfamethoxazole (33.9%), tetracycline (39.5%), and trimethoprim-sulphamethoxazole (37.9%). A close association between different risk factors and the prevalence of AMR of Salmonella strains suggests a concern over rising misuse of veterinary antimicrobials that may contribute to the emergence and evolution of multidrug-resistant pathogen isolates. One Health approach is recommended to achieve a positive health outcome for all species.<\/jats:p>","DOI":"10.3390\/pathogens10091160","type":"journal-article","created":{"date-parts":[[2021,9,9]],"date-time":"2021-09-09T21:36:58Z","timestamp":1631223418000},"page":"1160","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":18,"title":["Antimicrobial Resistance Patterns and Risk Factors Associated with Salmonella spp. Isolates from Poultry Farms in the East Coast of Peninsular Malaysia: A Cross-Sectional Study"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3172-5912","authenticated-orcid":false,"given":"Abdinasir Yusuf","family":"Osman","sequence":"first","affiliation":[{"name":"The Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hatfield AL9 7TA, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4482-9182","authenticated-orcid":false,"given":"Sharifo Ali","family":"Elmi","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Medicine, Universiti Malaysia Kelantan, Pengkalan Chepa, Kota Bharu 16100, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9655-1656","authenticated-orcid":false,"given":"David","family":"Simons","sequence":"additional","affiliation":[{"name":"The Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hatfield AL9 7TA, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linzy","family":"Elton","sequence":"additional","affiliation":[{"name":"Centre for Clinical Microbiology, Department of Infection, Division of Infection and Immunity, University College London, London NW3 2PF, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5980-3460","authenticated-orcid":false,"given":"Najmul","family":"Haider","sequence":"additional","affiliation":[{"name":"The Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hatfield AL9 7TA, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohd Azam","family":"Khan","sequence":"additional","affiliation":[{"name":"Faculty of Veterinary Medicine, Universiti Malaysia Kelantan, Pengkalan Chepa, Kota Bharu 16100, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9225-3678","authenticated-orcid":false,"given":"Iekhsan","family":"Othman","sequence":"additional","affiliation":[{"name":"Jeffrey Cheah School of Medicine and Health Sciences, Monash University Malaysia, Jalan Lagoon Selatan, Bandar Sunway 46150, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5111-5735","authenticated-orcid":false,"given":"Alimuddin","family":"Zumla","sequence":"additional","affiliation":[{"name":"Centre for Clinical Microbiology, Department of Infection, Division of Infection and Immunity, University College London, London NW3 2PF, UK"},{"name":"National Institute for Health Research Biomedical Research Centre, University College London Hospitals, London NW1 2BU, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"McCoy","sequence":"additional","affiliation":[{"name":"Institute of Population Health Sciences, Barts and London Medical and Dental School, Queen Mary University of London, London E1 2AD, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6561-3209","authenticated-orcid":false,"given":"Richard","family":"Kock","sequence":"additional","affiliation":[{"name":"The Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hatfield AL9 7TA, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,9,9]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1038\/nrmicro3439","article-title":"Tackling antibiotic resistance: The environmental framework","volume":"13","author":"Berendonk","year":"2015","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.ijid.2020.09.086","article-title":"Global trends in antimicrobial resistance in animals in low-and middle-income countries","volume":"101","author":"Pires","year":"2020","journal-title":"Int. J. Infect. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"300","DOI":"10.3389\/fvets.2021.652351","article-title":"High, Levels of Antibiotic, Resistance in Isolates, From Diseased, Livestock","volume":"8","author":"Haulisah","year":"2021","journal-title":"Front. Vet. Sci."},{"key":"ref_4","unstructured":"World Health Organization (2011). Tackling Antibiotic Resistance from a Food Safety Perspective in Europe, World, Health Organization Regional Office for Europe."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1086\/650733","article-title":"International collaboration on enteric disease \u201cburden of illness\u201d studies. The global burden of nontyphoidal Salmonella gastroenteritis","volume":"50","author":"Majowicz","year":"2010","journal-title":"Clin. Infect. Dis."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1312","DOI":"10.1016\/S1473-3099(19)30418-9","article-title":"The global burden of non-typhoidal salmonella invasive disease: A systematic analysis for the global burden of disease study 2017","volume":"19","author":"Stanaway","year":"2019","journal-title":"Lancet Infect. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1111\/j.1574-6976.2002.tb00606.x","article-title":"Antimicrobial drug resistance in salmonella: Problems and perspectives in food-and water-borne infections","volume":"26","author":"Threlfall","year":"2002","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Elmi, S.A., Simons, D., Elton, L., Haider, N., Abdel Hamid, M.M., Shuaib, Y.A., Khan, M.A., Othman, I., Kock, R., and Osman, A.Y. (2021). Identification of risk factors associated with resistant escherichia coli isolates from poultry farms in the east coast of peninsular malaysia: A cross sectional study. Antibiotics, 10.","DOI":"10.3390\/antibiotics10020117"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"371","DOI":"10.3201\/eid0303.970316","article-title":"Emerging quinolone-resistant salmonella in the united states","volume":"3","author":"Herikstad","year":"1997","journal-title":"Emerg. Infect. Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"3359","DOI":"10.1128\/JCM.42.7.3359-3362.2004","article-title":"Extended-spectrum-\u03b2-lactamase (tem-52)-producing strains of salmonella enterica of various serotypes isolated in france","volume":"42","author":"Weill","year":"2004","journal-title":"J. Clin. Microbiol."},{"key":"ref_11","unstructured":"Kei, H.M. (2018). Department of statistics malaysia press release. Dep. Stat. Malays. Putrajaya, 5\u20139."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"e316","DOI":"10.1016\/S2542-5196(17)30141-9","article-title":"Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: A systematic review and meta-analysis","volume":"1","author":"Tang","year":"2017","journal-title":"Lancet Planet. Health"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"854","DOI":"10.1038\/s41564-018-0208-5","article-title":"A one-health approach to antimicrobial resistance","volume":"3","author":"Walsh","year":"2018","journal-title":"Nat. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/S0740-0020(95)80072-7","article-title":"Prevalence of salmonella in raw and cooked foods in malaysia","volume":"12","author":"Arumugaswamy","year":"1995","journal-title":"Food Microbiol."},{"key":"ref_15","first-page":"57","article-title":"Multidrug resistance among different serotypes of salmonella isolates from fresh products in indonesia","volume":"19","author":"Kusumaningrum","year":"2012","journal-title":"Int. Food Res. J."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1311","DOI":"10.14202\/vetworld.2019.1311-1318","article-title":"Molecular epidemiology and antimicrobial resistance of salmonella isolates from broilers and pigs in thailand","volume":"12","author":"Phongaran","year":"2019","journal-title":"Vet. World"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1016\/j.ijfoodmicro.2017.12.015","article-title":"Antimicrobial residues and resistance against critically important antimicrobials in non-typhoidal salmonella from meat sold at wet markets and supermarkets in vietnam","volume":"266","author":"Nhung","year":"2018","journal-title":"Int. J. Food Microbiol."},{"key":"ref_18","unstructured":"Ministry of Health Malaysia, and Ministry of Agriculture & Agro-Based Industry Malaysia (2017). Malaysian Action Plan on Antimicrobial Resistance (Myap-Amr) 2017\u20132021."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/AEM.70.1.1-7.2004","article-title":"Characterization of multiple-antimicrobial-resistant salmonella serovars isolated from retail meats","volume":"70","author":"Chen","year":"2004","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1042","DOI":"10.4014\/jmb.0910.10028","article-title":"Characterization of drug-resistant salmonella enterica serotype typhimurium by antibiograms, plasmids, integrons, resistance genes, and pfge","volume":"20","author":"Benacer","year":"2010","journal-title":"J. Microbiol. Biotechnol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"2104","DOI":"10.3389\/fmicb.2018.02104","article-title":"Highly prevalent multidrug-resistant salmonella from chicken and pork meat at retail markets in guangdong, China","volume":"9","author":"Zhang","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-020-70517-w","article-title":"Antimicrobial resistance at the human\u2013animal interface in the Pastoralist, Communities of Kasese, District, South, Western Uganda","volume":"10","author":"Iramiot","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Mohammed Jajere, S., Hassan, L., Zakaria, Z., Abu, J., and Abdul Aziz, S. (2020). Antibiogram profiles and risk factors for multidrug resistance of salmonella enterica recovered from village chickens (gallus gallus domesticus linnaeus) and other environmental sources in the central and southern peninsular malaysia. Antibiotics, 9.","DOI":"10.3390\/antibiotics9100701"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1016\/j.foodres.2017.11.066","article-title":"Genetic relatedness, antimicrobial resistance and biofilm formation of salmonella isolated from naturally contaminated poultry and their processing environment in northern malaysia","volume":"105","author":"Chuah","year":"2018","journal-title":"Food Res. Int."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"576113","DOI":"10.3389\/fvets.2020.576113","article-title":"A cross-sectional study of antimicrobial usage on commercial broiler and layer chicken farms in bangladesh","volume":"7","author":"Imam","year":"2020","journal-title":"Front. Vet. Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"726","DOI":"10.2460\/ajvr.71.7.726","article-title":"Changes in the use of antimicrobials and the effects on productivity of swine farms in Denmark","volume":"71","author":"Aarestrup","year":"2010","journal-title":"Am. J. Vet. Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1080\/10495390600956920","article-title":"Antimicrobial resistance in Scandinavia after a ban of antimicrobial growth promoters","volume":"17","author":"Bengtsson","year":"2006","journal-title":"Anim. Biotechnol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1007","DOI":"10.1086\/433191","article-title":"The routine use of antibiotics to promote animal growth does little to benefit protein undernutrition in the developing world","volume":"41","author":"Angulo","year":"2005","journal-title":"Clin. Infect. Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/S0167-5877(01)00218-5","article-title":"The effect of discontinuing the use of antimicrobial growth promoters on the productivity in the Danish broiler production","volume":"50","author":"Emborg","year":"2001","journal-title":"Prev. Vet. Med."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1089\/10766290152045066","article-title":"The, Swedish experience of the 1986 year ban of antimicrobial growth promoters, with special reference to animal health, disease prevention, productivity, and usage of antimicrobials","volume":"7","author":"Wierup","year":"2001","journal-title":"Microb. Drug Resist."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"j3544","DOI":"10.1136\/bmj.j3544","article-title":"Antimicrobial policy interventions in food animal production in south east asia","volume":"358","author":"Goutard","year":"2017","journal-title":"BMJ"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Coyne, L., Arief, R., Benigno, C., Giang, V.N., Huong, L.Q., Jeamsripong, S., Kalpravidh, W., McGrane, J., Padungtod, P., and Patrick, I. (2019). Characterizing antimicrobial use in the livestock sector in three South, East Asian countries (Indonesia, Thailand, and Vietnam). Antibiotics, 8.","DOI":"10.3390\/antibiotics8010033"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1483637","DOI":"10.1080\/16549716.2018.1483637","article-title":"Antimicrobial resistance in south east asia: Time to ask the right questions","volume":"11","author":"Kakkar","year":"2018","journal-title":"Glob. Health Action"},{"key":"ref_34","first-page":"100084","article-title":"An analysis of national action plans on antimicrobial resistance in southeast asia using a governance framework approach","volume":"7","author":"Chua","year":"2021","journal-title":"Lancet Reg. Health-West. Pac."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1709","DOI":"10.4315\/0362-028x.12-101","article-title":"Molecular characterization of antibiotic-resistant salmonella isolates from retail meat from markets in northern vietnam","volume":"75","author":"Thai","year":"2012","journal-title":"J. Food Prot."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"108790","DOI":"10.1016\/j.ijfoodmicro.2020.108790","article-title":"Prevalence and antimicrobial resistance of retail-meat-borne salmonella in southern china during the years 2009\u20132016: The diversity of contamination and the resistance evolution of multidrug-resistant isolates","volume":"333","author":"Xu","year":"2020","journal-title":"Int. J. Food Microbiol."},{"key":"ref_37","first-page":"6459","article-title":"Global trends in antimicrobial resistance in animals in low-and middle-income countries","volume":"365","author":"Pires","year":"2019","journal-title":"Science"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.ijid.2016.09.016","article-title":"A global antimicrobial conservation fund for low-and middle-income countries","volume":"51","author":"Mendelson","year":"2016","journal-title":"Int. J. Infect. Dis."},{"key":"ref_39","first-page":"317","article-title":"Antimicrobial resistance in 6 malaysian general hospitals","volume":"49","author":"Cheong","year":"1994","journal-title":"Med. J. Malays."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"630","DOI":"10.1126\/science.aba3432","article-title":"Using sewage for surveillance of antimicrobial resistance","volume":"367","author":"Aarestrup","year":"2020","journal-title":"Science"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"6355","DOI":"10.1128\/AEM.02063-14","article-title":"Diversity and antimicrobial resistance of salmonella enterica isolates from surface water in southeastern united states","volume":"80","author":"Li","year":"2014","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"S244","DOI":"10.1086\/381576","article-title":"Chicken consumption is a newly identified risk factor for sporadic salmonella enterica serotype enteritidis infections in the united states: A case-control study in foodnet sites","volume":"38","author":"Kimura","year":"2004","journal-title":"Clin. Infect. Dis."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1940","DOI":"10.3389\/fmicb.2021.689015","article-title":"Reducing the risk of transmission of critical antimicrobial resistance determinants from contaminated pork products to humans in South-East, Asia","volume":"12","author":"Sirichokchatchawan","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"20160137","DOI":"10.1098\/rsbl.2016.0137","article-title":"\u2018Disperse abroad in the land\u2019: The role of wildlife in the dissemination of antimicrobial resistance","volume":"12","author":"Arnold","year":"2016","journal-title":"Biol. Lett."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Razzuoli, E., Listorti, V., Martini, I., Migone, L., Decastelli, L., Mignone, W., Berio, E., Battistini, R., Ercolini, C., and Serracca, L. (2021). Prevalence and Antimicrobial, Resistances of Salmonella spp. Isolated from Wild, Boars in Liguria, Region, Italy. Pathogens, 10.","DOI":"10.3390\/pathogens10050568"},{"key":"ref_46","unstructured":"Wayne, P.A. (2017). Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory, Standards Institute."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1111\/j.1469-0691.2011.03570.x","article-title":"Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance","volume":"18","author":"Magiorakos","year":"2012","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"10969","DOI":"10.1007\/s11356-014-3887-3","article-title":"Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of faecal contamination of water","volume":"22","author":"Titilawo","year":"2015","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1016\/S0140-6736(15)00473-0","article-title":"Understanding the mechanisms and drivers of antimicrobial resistance","volume":"387","author":"Holmes","year":"2016","journal-title":"Lancet"},{"key":"ref_50","first-page":"306","article-title":"Prevalence and antimicrobial susceptibility of Salmonella spp. isolated from snakes in peninsular, Malaysia","volume":"3","author":"Abatcha","year":"2013","journal-title":"J. Vet. Adv."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2105-13-S6-S1","article-title":"Primer-blast: A tool to design target-specific primers for polymerase chain reaction","volume":"13","author":"Ye","year":"2012","journal-title":"BMC Bioinform."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"957","DOI":"10.1111\/zph.12515","article-title":"Factors potentially linked with the occurrence of antimicrobial resistance in selected bacteria from cattle, chickens and pigs: A scoping review of publications for use in modelling of antimicrobial resistance (IAM. AMR Project)","volume":"65","author":"Murphy","year":"2018","journal-title":"Zoonoses Public Health"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/9\/1160\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:59:30Z","timestamp":1760165970000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/9\/1160"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,9,9]]},"references-count":52,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2021,9]]}},"alternative-id":["pathogens10091160"],"URL":"https:\/\/doi.org\/10.3390\/pathogens10091160","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,9]]}}}