Salmonella Isolated From Raw Chicken Meats at Selected Slaughterhouses in Peninsular Malaysia; Their Antibiotic Resistance Profiles and Biofilm Formation on Nutrient-Limited Media

https://doi.org/10.55230/mabjournal.v53i2.2767

Authors

  • Zuraidah Ismail Department of Food Service and Management, Faculty of Food Science and Technology, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia
  • Nur Naqiyah Azmi Halal Products Research Institute, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia
  • Nor Ainy Mahyudin Department of Food Service and Management, Faculty of Food Science and Technology, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia; Halal Products Research Institute, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia
  • Wan Hasyera Wan Omar Halal Products Research Institute, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia
  • Marina Abdul Rahman Veterinary Public Health Laboratory, Department of Veterinary Services Malaysia, Jalan Nilai Banting, Bandar Baru Salak Tinggi, 43900 Sepang, Selangor, Malaysia
  • Marni Sapar Division of Research and Innovation, Department of Veterinary Services, Federal Government Administration Centre, 62630 Putrajaya, Malaysia

Keywords:

Antibiotic resistance, chicken meat, Salmonella, biofilm formation, slaughterhouse

Abstract

Salmonella is one of the pathogens responsible for foodborne diseases. Antibiotic resistance of Salmonella, particularly multidrug-resistant (MDR) strains have emerged and are becoming more prevalent, which is a very serious issue worldwide. This study sought to determine the antibiotic resistance profiles of Salmonella isolated from raw chicken meats, which were collected at selected slaughterhouses in Peninsular Malaysia and evaluating its biofilm-forming capability on surfaces. Antibiotic resistance of 135 Salmonella isolates against 12 antibiotics were investigated via disk diffusion method. The biofilm-forming ability of the isolates was evaluated by crystal violet staining using two media; a tryptic soy broth (TSB) and a 1/20 TSB with incubation periods of 24 and 48 h at 37 °C. A total of 118 strains of Salmonella showed higher resistance to erythromycin (87.41%), followed by tetracycline (85.19%;); 93 of the isolates (68.88%) were multi-drug resistant. A greater quantity of Salmonella was able to produce biofilm when grown in 1/20-TSB (90.37%) compared to the growth in TSB (88.15%), respectively. The findings in this study showed high prevalence, antibiotic resistance, and the biofilm forming ability of Salmonella strains isolated from raw chicken meats, suggesting that effective measures are required to ensure food safety in the poultry industry.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

Adzitey, F., Rusul, G. & Huda, N. 2012. Prevalence and antibiotic resistance of Salmonella serovars in ducks, duck rearing and processing environments in Penang, Malaysia. Food Research International, 45(2): 947-952. DOI: https://doi.org/10.1016/j.foodres.2011.02.051

Agarwal, R.K., Singh, S., Bhilegaonkar, K.N. & Singh, V.P. 2011. Optimization of microtitre plate assay for the testing of biofilm formation ability in different Salmonella serotypes. International Food Research Journal, 18(4): 1493-1498.

Ariffin, A.S., Mohtar, S. & Baluch, N.H. 2014. Broiler industry with emphasis on short supply chain in Malaysia. Paper presented at the meeting of the 4th International Conference on Technology and Operation Management (ICTOM 04), Kuala Lumpur. August 2014.

Bacci, C., Boni, E., Alpigiani, I., Lanzoni, E., Bonardi, S. & Brindani, F. 2012. Phenotypic and genotypic features of antibiotic resistance in Salmonella enterica isolated from chicken meat and chicken and quail carcasses. International Journal of Food Microbiology, 160(1): 16-23. DOI: https://doi.org/10.1016/j.ijfoodmicro.2012.09.014

Beyene, T., Yibeltie, H., Chebo, B., Abunna, F., Beyi, A.F., Mammo, B., Ayana, D. & Duguma, R. 2016. Identification and antimicrobial susceptibility profile of Salmonella isolated from selected dairy farms, abattoir and humans at Asella Town. Journal of Veterinary Science and Technology, 7(3): 1-7.

Čabarkapa, I., Škrinjar, M., Lević, J., Kokić, B., Blagojev, N., Milanov, D. & Suvajdžić, L. 2015. Biofilm forming ability of Salmonella enteritidis in vitro. Acta Veterinaria, 65(3): 371-389. DOI: https://doi.org/10.1515/acve-2015-0031

Capita, R., Alonso-Calleja, C. & Prieto, M. 2007. Prevalence of Salmonella enterica serovars and genovars from chicken carcasses in slaughterhouses in Spain. Journal of Applied Microbiology, 103(5): 1366-1375. DOI: https://doi.org/10.1111/j.1365-2672.2007.03368.x

Carramiñana, J.J., Rota, C., Agustín, I. & Herrera, A. 2004. High prevalence of multiple resistance to antibiotics in Salmonella serovars isolated from a poultry slaughterhouse in Spain. Veterinary Microbiology, 104(1-2): 133-139. DOI: https://doi.org/10.1016/j.vetmic.2004.08.010

Centers for Disease Control and Prevention. 2013. Antibiotic resistance threats to the United States, 2013. URL http://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf (accessed 10.23.17).

Centre of Disease Control and Prevention (CDC). 2020. National Antimicrobial Resistance Monitoring System for Enteric Bacteria (NARMS): Antibiotic Tested by NARMS. U.S. Food and Drug Administration, Silver Spring.

Chia, T.W.R., Goulter, R.M., McMeekin, T., Dykes, G.A. & Fegan, N. 2009. Attachment of different Salmonella serovars to materials commonly used in a poultry processing plant. Food Microbiology, 26(8): 853-859. DOI: https://doi.org/10.1016/j.fm.2009.05.012

Chmielewski, R.A.N. & Frank, J.F. 2003. Biofilm formation and control in food processing facilities. Comprehensive Reviews in Food Science and Food Safety, 2(1): 22-32. DOI: https://doi.org/10.1111/j.1541-4337.2003.tb00012.x

Chotinun, S., Rojanasthien, S., Unger, F., Tadee, P. & Patchanee, P. 2015. Prevalence and antimicrobial resistance of Salmonella isolated from carcasses, processing facilities and the environment surrounding small scale poultry slaughterhouses in Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health, 45(6): 1392-1398.

CLSI (Clinical and Laboratory Standard Institute). 2015. Performance standards for antimicrobial susceptibility testing-25th Informational Supplement. M100-S25. URL http://file.qums.ac.ir/repository/mmrc/CLSI2015.pdf. (accessed 6.12.17).

Codex Alimentarius Commision (CAC). 2004. General guidelines on sampling. Codex Alimentarius Commision CAC-GL 50. URL http://www.fao.org/uploads/media/Codex_2004_sampling_CAC_GL_50.pdf. (accessed 02.15.21)

Cui, M., Xie, M., Qu, Z., Zhao, S., Wang, J., Wang, Y., He, T., Wang, H., Zuo, Z. & Wu, C. 2016. Prevalence and antimicrobial resistance of Salmonella isolated from an integrated broiler chicken supply chain in Qingdao, China. Food Control, 62: 270-276. DOI: https://doi.org/10.1016/j.foodcont.2015.10.036

Djordjevic, D., Wiedmann, M. & McLandsborough, L. A. 2002. Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Applied Environmental Microbiology, 68: 2950- 2958. DOI: https://doi.org/10.1128/AEM.68.6.2950-2958.2002

Donlan, R.M. 2002. Biofilms: microbial life on surfaces. Emerging Infectious Diseases, 8(9): 881-890. DOI: https://doi.org/10.3201/eid0809.020063

Franco, B.E., Martínez, M.A., Rodríguez, M.A.S. & Wertheimer, A. I. 2009. The determinants of the antibiotic resistance process. Infection and Drug Resistance, 2: 1-11. DOI: https://doi.org/10.2147/IDR.S4899

Gerstel, U. & Römling, U. 2001. Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella Typhimurium. Environmental Microbiology, 3(10): 638-648. DOI: https://doi.org/10.1046/j.1462-2920.2001.00235.x

Gharieb, R.M., Tartor, Y.H. & Khedr, M.H.E. 2015. Non-typhoidal Salmonella in poultry meat and diarrhoeic patients: prevalence, antibiogram, virulotyping, molecular detection and sequencing of class I integrons in multidrug resistant strains. Gut Pathogens, 7(34): 2-9. DOI: https://doi.org/10.1186/s13099-015-0081-1

Ghasemmahdi, H., Tajik, H., Moradi, M., Mardani, K., Modaresi, R., Badali, A. & Dilmaghani, M. 2015. Antibiotic resistance pattern and biofilm formation ability of clinically isolates of Salmonella enterica serotype typhimurium. International Journal of Enteric Pathogens, 3(2): 1-6. DOI: https://doi.org/10.17795/ijep27372

Giaouris, E. & Nesse, L.L. 2015. Attachment of Salmonella spp. to food contact and product surfaces and biofilm formation on them as stress adaptation and survival strategies. In: Salmonella: Prevalence, Risk Factors and Treatment Options. B.H. Christopher (Ed.). Nova Science Publisher, New York. 111-136 pp.

Goncuoglu, M., Ormanci, F.S.B., Uludag, M. & Cil, G.I. 2016. Prevalence and antibiotic resistance of Salmonella spp. and Salmonella Typhimurium in broiler carcasses wings and liver. Journal of Food Safety, 36: 524-531. DOI: https://doi.org/10.1111/jfs.12272

Grant, A., Hashem, F. & Parveen, S. 2016. Salmonella and Campylobacter: Antimicrobial resistance and bacteriophage control in poultry. Food Microbiology, 53: 104-109. DOI: https://doi.org/10.1016/j.fm.2015.09.008

Hood, S.K. & Zottola, E.A. 1997. Adherence to stainless steel by food borne microorganisms during growth in model food systems. International Journal of Food Microbiology, 37(2-3): 145-153. DOI: https://doi.org/10.1016/S0168-1605(97)00071-8

Jackson, B.R., Griffin, P.M., Cole, D., Walsh, K.A., & Chai, S.J. 2013. Outbreak-associated Salmonella enterica serotypes and food commodities, United States, 1998-2008. Emerging Infectious Diseases, 19(8): 1239-1244. DOI: https://doi.org/10.3201/eid1908.121511

Keelara, S., Thakur, S. & Patel, J. 2016. Biofilm formation by environmental isolates of Salmonella and their sensitivity to natural antimicrobials. Foodborne Pathogens and Disease, 13(9): 509-516. DOI: https://doi.org/10.1089/fpd.2016.2145

Kemal, J., Sibhat, B., Menkir, S. & Beyene, D. 2016. Prevalence, assessment, and antimicrobial resistance patterns of Salmonella from raw chicken eggs in Haramaya, Ethiopia. The Journal of Infection in Developing Countries, 10(11): 1230-1235. DOI: https://doi.org/10.3855/jidc.7885

Krumperman, P.H. 1983. Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Applied and Environmental Microbiology, 46(1): 165-170. DOI: https://doi.org/10.1128/aem.46.1.165-170.1983

Lampang, K.N., Chailangkarn, S. & Padungtod, P. 2013. Prevalence and antimicrobial resistance of Salmonella serovars in chicken farm, Chiang Mai and Lamphun province, Northern of Thailand. Chiang Mai Veterinary Journal, 2(2): 85-93.

Majowicz, S.E., Musto, J., Scallan, E., Angulo, F.J., Kirk, M., O'Brien, S.J., Jones, T.F., Fazil, A. & Hoekstra, R.M. 2010. The global burden of nontyphoidal Salmonella gastroenteritis. Clinical Infectious Diseases, 50(6): 882-889. DOI: https://doi.org/10.1086/650733

Manijeh, M., Mohammad, J. & Roha, K.K. 2008. Biofilm formation by Salmonella enteritidis on food contact surfaces. Journal of Biological Sciences, 8(2):502-505. DOI: https://doi.org/10.3923/jbs.2008.502.505

Mariappan V, Vellasamy K.M., Mohamad, N.A., Subramaniam, S. & Vadivelu, J. 2021. OneHealth approaches contribute towards antimicrobial resistance: Malaysian perspective. Frontiers in Microbiology, 12: 718774. DOI: https://doi.org/10.3389/fmicb.2021.718774

Ministry of Health Malaysia (MOH). 2019. Annual health report 2018. Ministry of Health Malaysia, Putrajaya.

Modarressi, S. & Thong, K.L. 2010. Isolation and molecular sub typing of Salmonella Enterica from chicken, beef and street foods in Malaysia. Scientific Research and Essays, 5(18): 2713-2720.

Nair, A., Rawool, D.B., Doijad, S., Poharkar, K., Mohan, V., Barbuddhe, S.B., Kolhe, R., Kurkure, N.V., Kumar, A., Malik, S.V.S. & 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. DOI: https://doi.org/10.1016/j.meegid.2015.08.012

Najwa, M.S., Rukayadi, Y., Ubong, A., Loo, Y.Y., Chang, W.S., Lye, Y.L., Thung, T.Y., Aimi, S.A., Malcolm, T.T.H., Goh, S.G., Kuan, C.H., Yoshitsugu, N., Nishibuchi, M. & Son, R. 2015. Quantification and antibiotic susceptibility of Salmonella spp., Salmonella Enteritidis and Salmonella Typhimurium in raw vegetables (ulam). International Food Research Journal, 22(5): 1761-1769.

Nguyen, H.D.N., Yang, Y.S. & Yuk, H.G. 2014. Biofilm formation of Salmonella Typhimurium on stainless steel and acrylic surfaces as affected by temperature and pH level. LWT - Food Science and Technology, 55(1): 383-388. DOI: https://doi.org/10.1016/j.lwt.2013.09.022

Nidaullah, H., Abirami, N., Shamila-Syuhada, A.K., Chuah, L.O., Nurul, H., Tan, T.P., Zainal Abidin, F.W. & Rusul, G. 2017. Prevalence of Salmonella in poultry processing environments in wet markets in Penang and Perlis, Malaysia. Veterinary World, 10: 286-292. DOI: https://doi.org/10.14202/vetworld.2017.286-292

Nillian, E., Rukayadi, Y. & Radu, S. 2016. Biofilm of antibiotics resistant Salmonella Typhimurium and Salmonella Enteritidis against detergents. Transactions on Science and Technology, 3(2): 319-327.

Parry, C.M. & Threlfall, E.J. 2008. Antimicrobial resistance in typhoidal and nontyphoidal salmonellae. Current Opinion in Infectious Diseases, 21(5): 531-538. DOI: https://doi.org/10.1097/QCO.0b013e32830f453a

Ren, X., Li, M., Xu, C., Cui, K., Feng, Z., Fu, Y., Zhang, J. & Liao, M. 2016. Prevalence and molecular characterization of Salmonella enterica isolates throughout an integrated broiler supply chain in China. Epidemiology and Infection, 144: 1-11. DOI: https://doi.org/10.1017/S0950268816001515

Rincón-Gamboa, S.M., Poutou-Piñales, R.A., & Carrascal-Camacho, A.K. 2021. Antimicrobial resistance of non-typhoid Salmonella in meat and meat products. Foods, 10: 1731. DOI: https://doi.org/10.3390/foods10081731

Sallam, K.I., Mohammed, M.A., Hassan, M.A. & Tamura, T. 2014. Prevalence, molecular identification and antimicrobial resistance profile of Salmonella serovars isolated from retail beef products in Mansoura, Egypt. Food Control, 38(1): 209-214. DOI: https://doi.org/10.1016/j.foodcont.2013.10.027

Shafini, A.B., Son, R., Mahyudin, N.A., Rukayadi, Y. & Tuan Zaizanor, T.C. 2017. Prevalence of Salmonella spp. in chicken and beef from retail outlets in Malaysia. International Food Research Journal, 24(1): 437-449.

Sinde, E. & Carballo, J. 2000. Attachment of Salmonella spp. and Listeria monocytogenes to stainless steel, rubber and polytetrafluorethylene: The influence of free energy and the effect of commercial sanitizers. Food Microbiology, 17(4): 439-447. DOI: https://doi.org/10.1006/fmic.2000.0339

Singh, A.K., Prakash, P., Achra, A., Singh, G.P., Das, A. & Singh, R.K. 2017. Standardization and classification of in vitro biofilm formation by clinical isolates of Staphylococcus aureus. Journal of Global Infectious Diseases, 9(3): 93. DOI: https://doi.org/10.4103/jgid.jgid_91_16

Solomon, E.B., Niemira, B.A, Sapers, G.M. & Annous, B.A. 2005. Biofilm formation, cellulose production, and curli biosynthesis by Salmonella originating from produce, animal, and clinical sources. Journal of Food Protection, 68(5): 906-912. DOI: https://doi.org/10.4315/0362-028X-68.5.906

Stanaway, J.D., Parisi, A., Sarkar, K., Blacker, B.F., Reiner, R.C., Hay, S.I., Nixon, M.R., Dolecek, C., James, S.L., Mokdad, A.H., Abebe, G.A., Ahmadian, E., Alahdab, F., Alemnew, B., Alipour, V., Bakeshei, F.A., Animut, M.D., Ansari, F., Arabloo, J., Asfaw, E.T. et al. (2019). The global burden of non-typhoidal salmonella invasive disease: a systematic analysis for the Global Burden of Disease Study 2017. The Lancet Infectious Diseases, 19(12): 1312-1324.

Stepanović, S., Ćirković, I., Ranin, L. & Švabić-Vlahović, M. 2004. Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Letters in Applied Microbiology, 38(5): 428-432. DOI: https://doi.org/10.1111/j.1472-765X.2004.01513.x

Sukri, A., Zulfakar, S.S., Mohd Taib, I.S., Omar, N.F. & Mohamad Zin, N. 2021. The high occurrence of multidrug-resistant Salmonella spp. isolated from raw chicken meat and contact surfaces at wet market in Malaysia. Sains Malaysiana, 50(12): 3765-3772. DOI: https://doi.org/10.17576/jsm-2021-5012-25

Ta, Y.T., Nguyen, T.T., To, P.B., Pham, D.X., Le, H.T.H., Thi, G.N., Alali, W.Q., Walls, I. & Doyle, M.P. 2014. Quantification, serovars, and antibiotic resistance of Salmonella isolated from retail raw chicken meat in Vietnam. Journal of Food Protection, 77(1): 57-66. DOI: https://doi.org/10.4315/0362-028X.JFP-13-221

Tadesse, D.A., Singh, A., Zhao, S., Bartholomew, M., Womack, N., Ayers, S., Fields, P.I. & McDermott, P.F. (2016). Antimicrobial resistance in Salmonella in the United States from 1948 to 1995. Antimicrobial Agents and Chemotherapy, 60(4): 2567-2571. DOI: https://doi.org/10.1128/AAC.02536-15

Thai, T.H., Hirai, T., Lan, N.T. & Yamaguchi, R. 2012. Antibiotic resistance profiles of Salmonella serovars isolated from retail pork and chicken meat in North Vietnam. International Journal of Food Microbiology, 156(2): 147-151. DOI: https://doi.org/10.1016/j.ijfoodmicro.2012.03.016

Thong, K.L. & Modarressi, S. 2011. Antimicrobial resistant genes associated with Salmonella from retail meats and street foods. Food Research International, 44(9): 2641-2646. DOI: https://doi.org/10.1016/j.foodres.2011.05.013

Thong, K.L., Ngoi, S.T., Chai, L.C. & Teh, C.S.J. 2015. Quinolone resistance mechanisms among Salmonella enterica in Malaysia. Microbial Drug Resistance, 22(4): 259-269. DOI: https://doi.org/10.1089/mdr.2015.0158

Thung, T.Y., Mahyudin, N.A., Basri, D.F., Wan Mohamed Radzi, C.W.J., Nakaguchi, Y., Nishibuchi, M. & Radu, S. 2016. Prevalence and antibiotic resistance of Salmonella Enteritidis and Salmonella Typhimurium in raw chicken meat at retail markets in Malaysia. Poultry Science, 95(8): 1888-1893. DOI: https://doi.org/10.3382/ps/pew144

Van, T.T.H., Moutafis, G., Istivan, T., Tran, L.T. & Coloe, P.J. 2007. Detection of Salmonella spp. in retail raw food samples from Vietnam and characterization of their antibiotic resistance. Applied and Environmental Microbiology, 73(21): 6885-6890. DOI: https://doi.org/10.1128/AEM.00972-07

Vo, A.T.T., van Duijkeren, E., Fluit, A.C., Heck, M.E.O.C., Verbruggen, A., Maas, H.M.E. & Gastraa, W. 2006. Distribution of Salmonella enterica serovars from humans, livestock and meat in Vietnam and the dominance of Salmonella Typhimurium phage type 90. Veterinary Microbiology, 113(1-2): 153-158. DOI: https://doi.org/10.1016/j.vetmic.2005.10.034

Wang, H., Ye, K., Wei, X., Cao, J., Xu, X. & Zhou, G. 2013. Occurrence, antimicrobial resistance and biofilm formation of Salmonella isolates from a chicken slaughter plant in China. Food Control 33(2), 378-384. DOI: https://doi.org/10.1016/j.foodcont.2013.03.030

Yoke-Kqueen, C., Learn-Han, L., Noorzaleha, A.S., Son, R., Sabrina, S., Jiun-Horng, S. & Chai-Hoon, K. 2008. Characterization of multiple-antimicrobial-resistant Salmonella enterica subsp. enterica isolated from indigenous vegetables and poultry in Malaysia. Letters in Applied Microbiology, 46(3): 318-324. DOI: https://doi.org/10.1111/j.1472-765X.2007.02311.x

Zhou, G., Li, L.J., Shi, Q.S., Ouyang, Y.S., Chen, Y.B. & Hu, W.F. 2013. Effects of nutritional and environmental conditions on planktonic growth and biofilm formation of Citrobacter werkmanii BF-6. Journal of Microbiology and Biotechnology, 23(12): 1673-1682. DOI: https://doi.org/10.4014/jmb1307.07041

Published

30-06-2024

How to Cite

Ismail, Z., Azmi, N. N., Mahyudin, N. A., Wan Omar, W. H., Abdul Rahman, M., & Sapar, M. (2024). Salmonella Isolated From Raw Chicken Meats at Selected Slaughterhouses in Peninsular Malaysia; Their Antibiotic Resistance Profiles and Biofilm Formation on Nutrient-Limited Media. Malaysian Applied Biology, 53(2), 55–71. https://doi.org/10.55230/mabjournal.v53i2.2767

Issue

Section

Research Articles

Most read articles by the same author(s)