Research article

Listeria monocytogenes isolates from Western Cape, South Africa exhibit resistance to multiple antibiotics and contradicts certain global resistance patterns

  • Received: 26 October 2020 Accepted: 04 January 2021 Published: 19 January 2021
  • Food-borne disease outbreaks are common and offer valuable insights into the causes, impacts, and mechanisms underlying food pathogens. This also serves as a good foundation to validate the performance of current best practice control methods, for example antibiotics, that are used in the fight against food pathogens. Listeriosis outbreaks, caused by Listeria monocytogenes, is no exception. In 2018, South Africa experienced the largest global listeriosis outbreak recorded to date. However, despite the scale of this outbreak, information on the bacterium and its resistance towards antibiotics is still severely lacking. Furthermore, until now it remained to be determined whether L. monocytogenes antibiotic resistance patterns in South Africa mirror resistance patterns elsewhere in the world. The aim of this study was therefore to evaluate the efficacy of antibiotics that are currently used against L. monocytogenes. Using the European Committee on Antimicrobial Susceptibility Testing (EUCAST) disc diffusion method, L. monocytogenes isolates (n = 177) from diverse origins in the Western Cape, South Africa (clinical, food, and environment) were tested for susceptibility against five different antibiotics, namely ampicillin, erythromycin, chloramphenicol, gentamicin, and tetracycline. Isolates were collected over a period of two years (2017–2019). All isolates were susceptible to ampicillin, the currently recommended antibiotic, while a large number of isolates were resistant to chloramphenicol, erythromycin, and tetracycline. Also, patterns of resistance observed here are different to patterns observed elsewhere. The findings of this study demonstrate that it is imperative to continuously monitor the efficacy of currently recommended antibiotics, since resistance patterns can quickly develop when such antibiotics are overutilized, and secondly, that it is crucial to assess local antibiotic resistance patterns in conjunction with global patterns, since the latter is not necessarily generalizable to local scales.

    Citation: Rochelle Keet, Diane Rip. Listeria monocytogenes isolates from Western Cape, South Africa exhibit resistance to multiple antibiotics and contradicts certain global resistance patterns[J]. AIMS Microbiology, 2021, 7(1): 40-58. doi: 10.3934/microbiol.2021004

    Related Papers:

  • Food-borne disease outbreaks are common and offer valuable insights into the causes, impacts, and mechanisms underlying food pathogens. This also serves as a good foundation to validate the performance of current best practice control methods, for example antibiotics, that are used in the fight against food pathogens. Listeriosis outbreaks, caused by Listeria monocytogenes, is no exception. In 2018, South Africa experienced the largest global listeriosis outbreak recorded to date. However, despite the scale of this outbreak, information on the bacterium and its resistance towards antibiotics is still severely lacking. Furthermore, until now it remained to be determined whether L. monocytogenes antibiotic resistance patterns in South Africa mirror resistance patterns elsewhere in the world. The aim of this study was therefore to evaluate the efficacy of antibiotics that are currently used against L. monocytogenes. Using the European Committee on Antimicrobial Susceptibility Testing (EUCAST) disc diffusion method, L. monocytogenes isolates (n = 177) from diverse origins in the Western Cape, South Africa (clinical, food, and environment) were tested for susceptibility against five different antibiotics, namely ampicillin, erythromycin, chloramphenicol, gentamicin, and tetracycline. Isolates were collected over a period of two years (2017–2019). All isolates were susceptible to ampicillin, the currently recommended antibiotic, while a large number of isolates were resistant to chloramphenicol, erythromycin, and tetracycline. Also, patterns of resistance observed here are different to patterns observed elsewhere. The findings of this study demonstrate that it is imperative to continuously monitor the efficacy of currently recommended antibiotics, since resistance patterns can quickly develop when such antibiotics are overutilized, and secondly, that it is crucial to assess local antibiotic resistance patterns in conjunction with global patterns, since the latter is not necessarily generalizable to local scales.


    加载中

    Acknowledgments



    This work is based on the research supported in part by the National Research Foundation of South Africa (Grant number 108031 and 115594). The author would like to thank Microchem Lab Services (Pty) Ltd for isolates from food and environmental origin, National Health Laboratory Services (Microbiology Lab, Observatory) for isolates from clinical origin, and Dr. J-H Keet for his assistance in data analysis and statistics.

    Conflict of interest



    All authors declare no conflicts of interest in this paper.

    [1] WHO Food safety, 2019 (2019) .Available from: https://www.who.int/news-room/fact-sheets/detail/food-safety.
    [2] Forsythe SJ (2010)  The Microbiology of Safe Food, Chichester UK: Wiley-Blackwell Pub.
    [3] de Noordhout CM, Devleesschauwer B, Angulo FJ, et al. (2014) The global burden of listeriosis: a systematic review and meta-analysis. Lancet Infect Dis 14: 1073-1082. doi: 10.1016/S1473-3099(14)70870-9
    [4] Lamont R, Sobel J (2011) Listeriosis in human pregnancy: a systematic review. J Perinat Med 39: 227-236. doi: 10.1515/jpm.2011.035
    [5] Montville TJ, Matthews KR, Kniel KE (2012)  Food Microbiology: An introduction Washington, DC: ASM Press. doi: 10.1128/9781555817206
    [6] Li Z, Pérez-Osorio A, Wang Y, et al. (2017) Whole genome sequencing analyses of Listeria monocytogenes that persisted in a milkshake machine for a year and caused illnesses in Washington State. BMC Microbiol 17: 1-11. doi: 10.1186/s12866-016-0921-2
    [7] Smith A, Hearn J, Taylor C, et al. (2019) Listeria monocytogenes isolates from ready to eat plant produce are diverse and have virulence potential. Int J Food Microbiol 299: 23-32. doi: 10.1016/j.ijfoodmicro.2019.03.013
    [8] Wang XM, Lü XF, Yin L, et al. (2013) Occurrence and antimicrobial susceptibility of Listeria monocytogenes isolates from retail raw foods. Food Control 32: 153-158. doi: 10.1016/j.foodcont.2012.11.032
    [9] Fallah AA, Siavash Saei-Dehkordi S, Mahzounieh M (2013) Occurrence and antibiotic resistance profiles of Listeria monocytogenes isolated from seafood products and market and processing environments in Iran. Food Control 34: 630-636. doi: 10.1016/j.foodcont.2013.06.015
    [10] Ziegler M, Kent D, Stephan R, et al. (2019) Growth potential of Listeria monocytogenes in twelve different types of RTE salads: Impact of food matrix, storage temperature and storage time. Int J Food Microbiol 296: 83-92. doi: 10.1016/j.ijfoodmicro.2019.01.016
    [11] Rivera D, Toledo V, Reyes-Jara A, et al. (2018) Approaches to empower the implementation of new tools to detect and prevent foodborne pathogens in food processing. Food Microbiol 75: 126-132. doi: 10.1016/j.fm.2017.07.009
    [12] Pietracha D, Misiewicz A (2016) Use of products containing a phage in food industry as a new method for Listeria monocytogenes elimination from food (Listeria monocytogenes phages in food industry)–a review. Czech J Food Sci 1: 1-8. doi: 10.17221/217/2015-CJFS
    [13] Chibeu A, Agius L, Gao A, et al. (2013) Efficacy of bacteriophage LISTEX ™ P100 combined with chemical antimicrobials in reducing Listeria monocytogenes in cooked turkey and roast beef. Int J Food Microbiol 167: 208-214. doi: 10.1016/j.ijfoodmicro.2013.08.018
    [14] Chen J-Q, Regan P, Laksanalamai P, et al. (2017) Prevalence and methodologies for detection, characterization and subtyping of Listeria monocytogenes and L. ivanovii in foods and environmental sources. Food Sci Hum Wellness 6: 97-120. doi: 10.1016/j.fshw.2017.06.002
    [15] Sosnowski M, Lachtara B, Wieczorek K, et al. (2018) Antimicrobial resistance and genotypic characteristics of Listeria monocytogenes isolated from food in Poland. Int J Food Microbiol 289: 1-6. doi: 10.1016/j.ijfoodmicro.2018.08.029
    [16] CDC Listeria Outbreaks, 2019 (2019) .Available from: https://www.cdc.gov/listeria/outbreaks/index.html.
    [17] Buchanan RL, Gorris LGM, Hayman MM, et al. (2017) A review of Listeria monocytogenes: An update on outbreaks, virulence, dose-response, ecology, and risk assessments. Food Control 75: 1-13. doi: 10.1016/j.foodcont.2016.12.016
    [18] Althaus D, Jermini M, Giannini P, et al. (2017) Local outbreak of Listeria monocytogenes serotype 4b sequence type 6 due to contaminated meat pâté. Foodborne Pathog Dis 14: 219-222. doi: 10.1089/fpd.2016.2232
    [19] Gelbíčová T, Zobaníková M, Tomáštíková1 Z, et al. (2018) An outbreak of listeriosis linked to turkey meat products in the Czech Republic, 2012–2016 T. Epidemiol Infect 146: 1407-1412. doi: 10.1017/S0950268818001565
    [20] Orsi RH, Den Bakker HC, Wiedmann M (2010) Listeria monocytogenes lineages: Genomics, evolution, ecology, and phenotypic characteristics. Int J Med Microbiol 301: 79-96. doi: 10.1016/j.ijmm.2010.05.002
    [21] Lomonaco S, Nucera D, Filipello V (2015) The evolution and epidemiology of Listeria monocytogenes in Europe and the United States. Infect Genet Evol 35: 172-183. doi: 10.1016/j.meegid.2015.08.008
    [22] Manuel CS, Stelten A Van, Wiedmann M, et al. (2015) Prevalence and distribution of Listeria monocytogenes inlA alleles prone to phase variation and inlA alleles with premature stop codon mutations among human, food, animal, and environmental isolates. Appl Environ Microbiol 81: 8339-8345. doi: 10.1128/AEM.02752-15
    [23] Gray MJ, Zadoks RN, Fortes ED, et al. (2004) Listeria monocytogenes isolates from foods and humans form distinct but overlapping populations. Appl Environ Microbiol 70: 5833-5841. doi: 10.1128/AEM.70.10.5833-5841.2004
    [24] Jeffers GT, Bruce JL, McDonough PL, et al. (2001) Comparative genetic characterization of Listeria monocytogenes isolates from human and animal listeriosis cases. Microbiology 147: 1095-1104. doi: 10.1099/00221287-147-5-1095
    [25] Goulet V, King LA, Vaillant V, et al. (2013) What is the incubation period for listeriosis? BMC Infect Dis 13: 11-18. doi: 10.1186/1471-2334-13-11
    [26] Smith AM, Naicker P, Bamford C, et al. (2016) Genome sequences for a cluster of human isolates of Listeria monocytogenes identified in South Africa in 2015. Genome Announc 4: 1-2.
    [27] NICD Division of Public Health Surveillance and Response, Clinical advisory Listeria meningitis, 2017 (2017) .Available from: https://www.nicd.ac.za/wp-content/uploads/2019/03/Listeria-statement_20171025_final.pdf.
    [28] Mateus T, Silva J, Maia RL, et al. (2013) Listeriosis during Pregnancy: A public health concern. ISRN Obstet Gynecol 2013: 851712. doi: 10.1155/2013/851712
    [29] Alonso-Hernando A, Prieto M, García-fernández C, et al. (2012) Increase over time in the prevalence of multiple antibiotic resistance among isolates of Listeria monocytogenes from poultry in Spain. Food Control 23: 37-41. doi: 10.1016/j.foodcont.2011.06.006
    [30] Fallah AA, Siavash Saei-Dehkordi S, Rahnama M, et al. (2012) Prevalence and antimicrobial resistance patterns of Listeria species isolated from poultry products marketed in Iran. Food Control 28: 327-332. doi: 10.1016/j.foodcont.2012.05.014
    [31] Escolar C, Gómez D, del Carmen Rota García M, et al. (2017) Antimicrobial resistance profiles of Listeria monocytogenes and Listeria innocua isolated from ready-to-eat products of animal origin in Spain. Foodborne Pathog Dis 14: 357-363. doi: 10.1089/fpd.2016.2248
    [32] Rahimi E, Ameri M, Momtaz H (2010) Prevalence and antimicrobial resistance of Listeria species isolated from milk and dairy products in Iran. Food Control 21: 1448-1452. doi: 10.1016/j.foodcont.2010.03.014
    [33] Vitas ANAI, Aguado V, Mari R (2007) Antimicrobial susceptibility of Listeria monocytogenes isolated from food and clinical cases in Navarra , Spain. J Food Prot 70: 2402-2406. doi: 10.4315/0362-028X-70.10.2402
    [34] Cerf O, Carpentier B, Sanders P (2010) Tests for determining in-use concentrations of antibiotics and disinfectants are based on entirely different concepts: ‘Resistance’ has different meanings. Int J Food Microbiol 136: 247-254. doi: 10.1016/j.ijfoodmicro.2009.10.002
    [35] Davies J, Davies D (2010) Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74: 417-433. doi: 10.1128/MMBR.00016-10
    [36] Christensen EG, Gram L, Kastbjerg VG (2011) Sublethal triclosan exposure decreases susceptibility to gentamicin and other aminoglycosides in Listeria monocytogenesAntimicrob Agents Chemother 55: 4064-4071. doi: 10.1128/AAC.00460-11
    [37] Karmi M (2014) Detection and presumptive identification of antibiotic residues in poultry meat by using FPT. Glob J Pharmacol 8: 160-165.
    [38] Allen KJ, Wałecka-Zacharska E, Chen JC, et al. (2016) Listeria monocytogenes-An examination of food chain factors potentially contributing to antimicrobial resistance. Food Microbiol 54: 178-189. doi: 10.1016/j.fm.2014.08.006
    [39] Aureli P, Fiorucci GC, Caroli D, et al. (2000) An outbreak of febrile gastroenteritis associated wth corn contaminated by Listeria monocytogenesN Engl J Med 342: 1236-1241. doi: 10.1056/NEJM200004273421702
    [40] NICD Situation report prepared by National Listeria Incident Management Team, 2018 (2018) .Available from: http://www.nicd.ac.za/wp-content/uploads/2018/07/Listeriosis-outbreak-situation-report-_26July2018_fordistribution.pdf.
    [41] Bamford C, Bosman N, Boyles T, et al. Division of Public Health Surveillance and Response, Listeriosis: Clinical recommendations for diagnosis and treatment, 2017 (2017) .Available from: https://www.nicd.ac.za/wp-content/uploads/2017/12/Listeriosis_Clinical_Guidelines.pdf.
    [42] Schutte CM, Van Der Meyden CH, Kakaza M, et al. (2019) Life-threatening Listeria meningitis: Need for revision of South African acute bacterial meningitis treatment guidelines. South African Med J 109: 296-298. doi: 10.7196/SAMJ.2019.v109i5.13866
    [43] NICD Management of persons following exposure to Listeria -contaminated Foods (2018) .Available from: https://www.nicd.ac.za/wp-content/uploads/2019/03/FAQ_Exposure-to-Listeriosis_20180308.pdf.
    [44] WHO Listeriosis outbreak in South Africa, 2018 (2018) .Available from: https://www.afro.who.int/news/listeriosis-outbreak-south-africa.
    [45] Blais BW, Phillippe LM, Burzynski M, et al. (1995) Applicability of the PCR technique in the food testing laboratory: Identification of Listeria monocytogenesBiotechnol Tech 9: 629-632. doi: 10.1007/BF00156346
    [46] Bester IM (2011) Detection and molecular subtyping of Listeria monocytogenes isolated from a South African avocado processing facility, MSc Thesis. Stellenbosch University, Stellenbosch .
    [47] Cossart P, Fransisca Vicente M, Mengaud J, et al. (1989) Listeriolysin O is essential for virulence of Listeria monocytogenes: direct evidence obtained by gene complementation. Infect Immun 57: 3629-3636. doi: 10.1128/IAI.57.11.3629-3636.1989
    [48] Rasmussen OF, Beck T, Olsen JE, et al. (1991) Listeria monocytogenes isolates can be classified into two major types according to the sequence of the listeriolysin gene. Infect Immun 59: 3945-3951. doi: 10.1128/IAI.59.11.3945-3951.1991
    [49] Epstein FH, Southwick FS, Purich DL (1996) Intracellular pathogenesis of listeriosis. N Engl J Med 334: 770-776. doi: 10.1056/NEJM199605163342008
    [50] Doyle ME FRI Briefings, Virulence characteristics of Listeria monocytogenes, 2001 (2001) .Available from: https://fri.wisc.edu/files/Briefs_File/virulencelmono.pdf.
    [51] Rip D, Gouws PA (2020) PCR–restriction fragment length polymorphism and pulsed-field gel electrophoresis characterization of listeria monocytogenes isolates from ready-to-eat foods, the food processing environment, and clinical samples in South Africa. J Food Prot 83: 518-533. doi: 10.4315/0362-028X.JFP-19-301
    [52] EUCAST Antimicrobial susceptibility testing EUCAST disk diffusion method, 2012 (2012) .Available from: http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Disk_test_documents/Manual_v_2.1_EUCAST_Disk_Test.pdf.
    [53] Maćkiw E, Modzelewska M, Mąka Ł, et al. (2016) Antimicrobial resistance profiles of Listeria monocytogenes isolated from ready-to-eat products in Poland in 2007–2011. Food Control 59: 7-11. doi: 10.1016/j.foodcont.2015.05.011
    [54] Wang J, Ray AJ, Hammons SR, et al. (2015) Persistent and transient Listeria monocytogenes strains from retail deli environments vary in their ability to adhere and form biofilms and rarely have inlA premature stop codons. Foodborne Pathog Dis 12: 151-158. doi: 10.1089/fpd.2014.1837
    [55] Wiggins GL, Albritton WL, Feeley JC (1978) Antibiotic susceptibility of clinical isolates of Listeria monocytogenesAntimicrob Agents Chemother 13: 854-860. doi: 10.1128/AAC.13.5.854
    [56] Magiorakos A., Srinivasan A, Carey RB, et al. (2012) Multidrugresistant, extensively drugresistant and pandrugresistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18: 268-281. doi: 10.1111/j.1469-0691.2011.03570.x
    [57] Noll M, Kleta S, Dahouk S Al, et al. (2017) Antibiotic susceptibility of 259 Listeria monocytogenes strains isolated from food, food-processing plants and human samples in Germany. J Infect Public Health 11: 572-577. doi: 10.1016/j.jiph.2017.12.007
    [58] Chen B, Pyla R, Kim T, et al. (2010) Antibiotic resistance in Listeria species isolated from catfish fillets and processing environment. Lett Appl Microbiol 50: 626-632. doi: 10.1111/j.1472-765X.2010.02843.x
    [59] R Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria (2018) .Available from: https://www.R-project.org/.
    [60] Jamali H, Paydar M, Ismail S, et al. (2015) Prevalence, antimicrobial susceptibility and virulotyping of Listeria species and Listeria monocytogenes isolated from open-air fish markets. BMC Microbiol 15: 1-7. doi: 10.1186/s12866-015-0476-7
    [61] Alonso-Hernando A, Capita R, Prieto M, et al. (2009) Comparison of antibiotic resistance patterns in Listeria monocytogenes and Salmonella enterica strains pre-exposed and exposed to poultry decontaminants. Food Control 20: 1108-1111. doi: 10.1016/j.foodcont.2009.02.011
    [62] Davis JA, Jackson CR (2009) Comparative antimicrobial susceptibility of Listeria monocytogenes, L. innocua, and L. welshimeriMicrob Drug Resist 15: 27-32. doi: 10.1089/mdr.2009.0863
    [63] Haubert L, Mendonça M, Lopes GV, et al. (2016) Listeria monocytogenes isolates from food and food environment harbouring tetM and ermB resistance genes. Lett Appl Microbiol 62: 23-29. doi: 10.1111/lam.12516
    [64] Abdollahzadeh E, Ojagh M, Hosseini H, et al. (2016) Antimicrobial resistance of Listeria monocytogenes isolated from seafood and humans in Iran. Microb Pathog 100: 70-74. doi: 10.1016/j.micpath.2016.09.012
    [65] Pesavento G, Ducci B, Nieri D, et al. (2010) Prevalence and antibiotic susceptibility of Listeria spp. isolated from raw meat and retail foods. Food Control 21: 708-713. doi: 10.1016/j.foodcont.2009.10.012
    [66] Yücel N, Citak S, Önder M (2005) Prevalence and antibiotic resistance of Listeria species in meat products in Ankara, Turkey. Food Microbiol 22: 241-245. doi: 10.1016/j.fm.2004.03.007
    [67] Safdar A, Armstrong D (2003) Antimicrobial activities against 84 Listeria monocytogenes isolates from patients with systemic listeriosis at a Comprehensive Cancer Center (1955–1997). J Clin Microbiol 41: 483-485. doi: 10.1128/JCM.41.1.483-485.2003
    [68] Nyasulu P, Murray J, Perovic O, et al. (2012) Antimicrobial resistance surveillance among nosocomial pathogens in South Africa: Systematic review of published literature. J Exp Clin Med 4: 8-13. doi: 10.1016/j.jecm.2011.11.002
    [69] Charpentier E, Courvalin P (1999) Antibiotic resistance in Listeria spp. Antimicrob Agents Chemother 43: 2103-2108. doi: 10.1128/AAC.43.9.2103
    [70] Duffy G, Walsh D, Sheridan JJ, et al. (2001) Comparison of selective and non-selective enrichment media in the detection of Listeria monocytogenes from meat containing Listeria innocua. J Appl Microbiol 90: 994-999. doi: 10.1046/j.1365-2672.2001.01336.x
    [71] Li Q, Sherwood JS, Logue CM (2007) Antimicrobial resistance of Listeria spp. recovered from processed bison. Lett Appl Microbiol 44: 86-91. doi: 10.1111/j.1472-765X.2006.02027.x
    [72] Morvan A, Moubareck C, Leclercq A, et al. (2010) Antimicrobial resistance of Listeria monocytogenes strains isolated from humans in France. Antimicrob Agents Chemother 54: 2728-2731. doi: 10.1128/AAC.01557-09
    [73] Olaimat AN, Al-Holy MA, Shahbaz HM, et al. (2018) Emergence of antibiotic resistance in Listeria monocytogenes isolated from food products: A comprehensive review. Compr Rev Food Sci Food Saf 17: 1277-1292. doi: 10.1111/1541-4337.12387
    [74] Meyer E, Gastmeier P, Deja M, et al. (2013) Antibiotic consumption and resistance: Data from Europe and Germany. Int J Med Microbiol 303: 388-395. doi: 10.1016/j.ijmm.2013.04.004
    [75] Tanwar J, Das S, Fatima Z, et al. (2014) Multidrug resistance: An emerging crisis. Interdiscip Perspect Infect Dis 2014: 541340. doi: 10.1155/2014/541340
    [76] Medina E, Pieper DH (2016) Tackling threats and future problems of multidrug-resistant bacteria. How to Overcome the Antibiotic Crisis Springer, 3-33. doi: 10.1007/82_2016_492
    [77] Munita JM, Arias CA (2016) Mechanisms of antibiotic resistance. Microbiol Spectr 4: 1-37. doi: 10.1128/microbiolspec.VMBF-0016-2015
    [78] Wright GD (2019) Environmental and clinical antibiotic resistomes, same only different. Curr Opin Microbiol 51: 57-63. doi: 10.1016/j.mib.2019.06.005
    [79] Wang K, Ye K, Zhu Y, et al. (2015) Prevalence, antimicrobial resistance and genetic diversity of Listeria monocytogenes isolated from chilled pork in Nanjing, China. LWT-Food Sci Technol 64: 905-910. doi: 10.1016/j.lwt.2015.06.015
    [80] Chen B, Pyla R, Kim T, et al. (2010) Prevalence and contamination patterns of Listeria monocytogenes in catfish processing environment and fresh fillets. Food Microbiolo 27: 645-652. doi: 10.1016/j.fm.2010.02.007
    [81] Warriss P (2010)  Meat Science-An Introductory Text United Kingdom: Cabi Publishing.
    [82] Moyane J, Jideani AI, Aiyegoro O (2013) Antibiotics usage in food-producing animals in South Africa and impact on human: Antibiotic resistance. African J Microbiol Res 7: 2990-2997. doi: 10.5897/AJMR2013.5631
    [83] Agyare C, Boamah VE, Zumbi CN, et al. (2018) Antibiotic use in poultry production and its effects on bacterial resistance. Antimicrob Resist-A Global Threat 33–50.
    [84] Mund MD, Khan UH, Tahir U, et al. (2017) Antimicrobial drug residues in poultry products and implications on public health: A review. Int J Food Prop 20: 1433-1446. doi: 10.1080/10942912.2016.1212874
    [85] Gómez D, Azón E, Marco N, et al. (2014) Antimicrobial resistance of Listeria monocytogenes and Listeria innocua from meat products and meat-processing environment. Food Microbiol 42: 61-65. doi: 10.1016/j.fm.2014.02.017
    [86] Ferri M, Ranucci E, Romagnoli P, et al. (2017) Antimicrobial resistance: A global emerging threat to public health systems. Crit Rev Food Sci Nutr 57: 2857-2876. doi: 10.1080/10408398.2015.1077192
    [87] DoH Surveillance for antimicrobial resistance and comsumption of antibiotcs in South Africa, 2019 (2019) .Available from: http://www.health.gov.za/index.php/antimicrobial-resistance?download=3374:surveillance-for-antimicrobial-resistance-and-consumption-of-antibiotics-in-south-africa.
    [88] Sattar S, Hassan MM, Islam SKMA, et al. (2014) Antibiotic residues in broiler and layer meat in Chittagong district of Bangladesh. Vet World 7: 738-743. doi: 10.14202/vetworld.2014.738-743
    [89] Hakem A, Titouche Y, Houali K, et al. (2013) Screening of antibiotics residues in poultry meat by microbiological methods. Bull Univ Agric Sci Vet Med Cluj-Napoca Vet Med 70: 77-82.
    [90] Amjad H, Iqbal J, Naeem M (2005) Analysis of some residual antibiotics in muscle, kidney and liver samples of broiler chicken by various methods. The 4th Session of 2005 Workshop of Pakistan Academy of Sciences 2–10.
    [91] Henton MM, Eagar HA, Swan GE, et al. (2011) Antibiotic management and resistance in livestock production. South African Med J 101: 1-7.
    [92] Vasconcelos V De, Hofer E, Christina D, et al. (2016) Occurrence and antimicrobial resistance patterns of Listeria monocytogenes isolated from vegetables. Brazilian J Microbiol 47: 438-443. doi: 10.1016/j.bjm.2015.11.033
    [93] David OM, Odeyemi AT (2007) Antibiotic resistant pattern of environmental isolates of Listeria monocytogenes from Ado-Ekiti, Nigeria. African J Biotechnol 6: 2135-2139. doi: 10.5897/AJB2007.000-2332
    [94] Gullberg E (2014) Selection of resistance at very low antibiotic concentrations. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine Uppsala: Acta Universitatis Upsaliensi.
    [95] Javadi A (2011) Effect of roasting, boiling and microwaving cooking method on doxycline residues in edible tissues of poultry by microbial method. African J Pharm Pharmacol 5: 1034-1037.
    [96] Walsh SE, Maillard JY, Russell AD, et al. (2003) Development of bacterial resistance to several biocides and effects on antibiotic susceptibility. J Hosp Infect 55: 98-107. doi: 10.1016/S0195-6701(03)00240-8
    [97] Eagar H, Swan G, Van Vuuren M (2012) A survey of antimicrobial usage in animals in South Africa with specific reference to food animals. J S Afr Vet Assoc 83: 1-8. doi: 10.4102/jsava.v83i1.16
    [98] Bester LA, Essack SY (2012) Observational study of the prevalence and antibiotic resistance of campylobacter spp. from different poultry production systems in KwaZulu-Natal, South Africa. J Food Prot 75: 154-159. doi: 10.4315/0362-028X.JFP-11-237
    [99] Ayaz ND, Erol I (2010) Relation between serotype distribution and antibiotic resistance profiles of Listeria monocytogenes isolated from ground turkey. J Food Prot 73: 967-972. doi: 10.4315/0362-028X-73.5.967
    [100] Wang G, Qian W, Zhang X, et al. (2015) Prevalence, genetic diversity and antimicrobial resistance of Listeria monocytogenes isolated from ready-to-eat meat products in Nanjing, China. Food Control 50: 202-208. doi: 10.1016/j.foodcont.2014.07.057
    [101] Skowron K, Kwiecińska-Piróg J, Grudlewska K, et al. (2018) The occurrence, transmission, virulence and antibiotic resistance of Listeria monocytogenes in fish processing plant. Int J Food Microbiol 282: 71-83. doi: 10.1016/j.ijfoodmicro.2018.06.011
    [102] Kovacevic J, Sagert J, Wozniak A, et al. (2013) Antimicrobial resistance and co-selection phenomenon in Listeria spp. recovered from food and food production environments. Food Microbiol 34: 319-327. doi: 10.1016/j.fm.2013.01.002
  • microbiol-07-01-004-s001.pdf
  • Reader Comments
  • © 2021 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(1272) PDF downloads(118) Cited by(0)

Article outline

Figures and Tables

Figures(4)  /  Tables(2)

Other Articles By Authors

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog