Prevalence and Antibiotics Resistance of <i>Proteus mirabilis</i> in Raw Meat

Chenglu LAN; Yilin HU; Man WANG; Chuyi LI; Shuilian BI

doi:10.13386/j.issn1002-0306.2022100028

Volume 44 Issue 13

Jun. 2023

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Science and Technology of Food Industry > 2023 > 44(13): 257-263. > DOI: 10.13386/j.issn1002-0306.2022100028

LAN Chenglu, HU Yilin, WANG Man, et al. Prevalence and Antibiotics Resistance of Proteus mirabilis in Raw Meat[J]. Science and Technology of Food Industry, 2023, 44(13): 257−263. (in Chinese with English abstract). doi: 10.13386/j.issn1002-0306.2022100028.

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Prevalence and Antibiotics Resistance of Proteus mirabilis in Raw Meat

Chenglu LAN^{1, 2,},
Yilin HU¹,
Man WANG¹,
Chuyi LI¹,
Shuilian BI^1, ,

1.
School of Food Science, Guangdong Pharmaceutical University, Zhongshan 528405, China
2.
School of Public Health, Guangdong Pharmaceutical University, Guangzhou 510315, China

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Received Date: October 07, 2022
Available Online: April 21, 2023

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Abstract

Abstract

To understand the contamination and antibiotic resistance of Proteus mirabilis in raw meat, a total of 579 samples of pork, chicken, and duck meats were collected from 5 markets, and P. mirabilis in the samples was isolated and identified. The susceptibility to 21 antibiotics of the P. mirabilis isolated in this study was tested by the disk diffusion method. A total of 490 P. mirabilis in those 579 samples were isolated and identified. The contamination rates of P. mirabilis in pork, chicken, and duck meats were 65.61%, 78.95%, and 67.90%, respectively. Market 5 had the highest contamination rate (82.00%) among the chicken samples. The antibiotic resistance rates of all P. mirabilis isolates to erythromycin was the highest, which was higher than 97.85% in all markets, followed by trimethoprim (78.00%~93.68%), doxycycline (73.12%~79.82%), spectinomycin (65.26%~88.17%), tetracycline (64.52%~79.95%), streptomycin (60.55%~86.02%), trimethoprim-sulfameth (52.29%~87.10%), and gentamicin (51.61%~76.15%), all of which were more than 50.00%. The multiple-drug resistance of 490 strains of P. mirabilis was severe with a rate of 100.00%. P. mirabilis strains with pan drug-resistance to all 8 classes of antibiotics accounted for 14.90%. In conclusion, the fresh meats from 5 markets were seriously contaminated by P. mirabilis, and all the isolates had multiple-drug resistance. The contamination and antibiotic resistance of P. mirabilis in this area should be continuously monitored in order to provide more information for the prevention and control of food poisoning and the selection of clinical medication.
- Proteus mirabilis,
- fresh meat,
- markets,
- isolation and identification,
- antibiotic resistance

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References (39)

References

[1]	MOBLEY H L T. Proteus mirabilis overview[J]. Methods in Molecular Biology,2019,2021:1−4.
[2]	JACOBSEN S M, SHIRTLIFF M E. Proteus mirabilis biofilms and catheter-associated urinary tract infections[J]. Virulence,2011,2(5):460−465. doi: 10.4161/viru.2.5.17783
[3]	KWIECIŃSKA-PIRÓG J, SKOWRON K, GOSPODAREK-KOMKOWSKA E. Primary and secondary bacteremia caused by Proteus spp.: Epidemiology, strains susceptibility and biofilm formation[J]. Polish Journal of Microbiology,2018,67(4):471−478. doi: 10.21307/pjm-2018-055
[4]	NAGIAH S, BADBESS R. Unexpected source of Proteus mirabilis bacteraemia[J]. BMJ Case Reports,2018,11(1):2018226744. doi: 10.1136/bcr-2018-226744
[5]	GOMAA S, SERRY F, ABDELLATIF H, et al. Elimination of multidrug-resistant Proteus mirabilis biofilms using bacteriophages[J]. Archives of Virology,2019,164(9):2265−2275. doi: 10.1007/s00705-019-04305-x
[6]	CHEN C Y, CHEN Y H, LU P L, et al. Proteus mirabilis urinary tract infection and bacteremia: Risk factors, clinical presentation, and outcomes[J]. Journal of Microbiology Immunology and Infection,2012,45(3):228−236. doi: 10.1016/j.jmii.2011.11.007
[7]	SANCHES M S, RODRIGUES DA SILVA C, SILVA L C, et al. Proteus mirabilis from community-acquired urinary tract infections (UTI-CA) shares genetic similarity and virulence factors with isolates from chicken, beef and pork meat[J]. Microbial Pathogenesis,2021,158:105098. doi: 10.1016/j.micpath.2021.105098
[8]	KHATER D F, LELA R A, EL-DIASTY M, et al. Detection of harmful foodborne pathogens in food samples at the points of sale by MALDT-TOF MS in Egypt[J]. BMC Research Notes,2021,14(1):112. doi: 10.1186/s13104-021-05533-8
[9]	王霄晔, 任婧寰, 王哲, 等. 2017年全国食物中毒事件流行特征分析[J]. 疾病监测,2018,33(5):359−364. [WANG Xiaoye, REN Jinghuan, WANG Zhe, et al. Epidemiological characteristics of food poisoning events in China, 2017[J]. Disease Surveillance,2018,33(5):359−364. doi: 10.3784/j.issn.1003-9961.2018.05.004 WANG Xiaoye, REN Jinghuan, WANG Zhe, et al. Epidemiological characteristics of food poisoning events in China, 2017[J]. Disease Surveillance, 2018, 33(5): 359-364. doi: 10.3784/j.issn.1003-9961.2018.05.004
[10]	刘辉, 任婧寰, 伍雅婷, 等. 2018年全国食物中毒事件流行特征分析[J]. 中国食品卫生杂志,2022,34(1):147−153. [LIU Hui, REN Jinghuan, WU Yating, et al. Epidemic characteristics analysis for food poisoning events in China, 2018[J]. Chinese Journal of Food Hygiene,2022,34(1):147−153. LIU Hui, REN Jinghuan, WU Yating, et al. Epidemic characteristics analysis for food poisoning events in China, 2018[J]. Chinese Journal of Food Hygiene, 2022, 34(1): 147-153.
[11]	刘国恒, 黄琼. 广东省细菌性食物中毒流行特征及防控策略研究[J]. 食品安全导刊,2021(19):84−85. [LIU Guoheng, HUANG Qiong. Research on the epidemiological characteristics and prevention and control strategies of bacterial food poisoning in Guangdong Province[J]. China Food Safety Magazine,2021(19):84−85. LIU Guoheng, HUANG Qiong. Research on the epidemiological characteristics and prevention and control strategies of bacterial food poisoning in Guangdong Province[J]. China Food Safety Magazine, 2021(19): 84-85.
[12]	YU Z, JOOSSENS M, VAN DEN ABEELE A M, et al. Isolation, characterization and antibiotic resistance of Proteus mirabilis from Belgian broiler carcasses at retail and human stool[J]. Food Microbiology,2021,96:103724. doi: 10.1016/j.fm.2020.103724
[13]	陈善娇, 孙冷宁, 陈少婉, 等. 中山市生鲜畜禽肉中变形杆菌的污染分布及ERIC-PCR分型[J]. 肉类研究,2018,32(7):24−28. [CHEN Shanjiao, SUN Lengning, CHEN Shaowan, et al. Contamination and enterobacterial repetitive intergenic consensus-polymerase chain reaction typing of Proteus on fresh livestock and poultry meats in Zhongshan city[J]. Meat Research,2018,32(7):24−28. CHEN Shanjiao, SUN Lengning, CHEN Shaowan, et al. Contamination and enterobacterial repetitive intergenic consensus-polymerase chain reaction typing of Proteus on fresh livestock and poultry meats in Zhongshan city[J]. Meat Research, 2018, 32(7): 24-28.
[14]	孙冷宁, 陈善娇, 王观杏, 等. 市售鲜肉中奇异变形杆菌的ERIC-PCR分型与耐药性分析[J]. 食品工业科技,2019,40(2):137−141. [SUN Lengning, CHEN Shanjiao, WANG Guanxing, et al. Analysis of ERIC-PCR typing and drug resistance of Proteus mirabilis in commercially available fresh meat[J]. Science and Technology of Food Industry,2019,40(2):137−141. doi: 10.13386/j.issn1002-0306.2019.02.023 SUN Lengning, CHEN Shanjiao, WANG Guanxing, et al. Analysis of ERIC-PCR typing and drug resistance of Proteus mirabilis in commercially available fresh meat[J]. Science and Technology of Food Industry, 2019, 40(2): 137-141. doi: 10.13386/j.issn1002-0306.2019.02.023
[15]	KANG Q, WANG X, ZHAO J, et al. Multidrug-resistant Proteus mirabilis isolates carrying blaOXA-1 and blaNDM-1 from wildlife in China: Increasing public health risk[J]. Integrative Zoology,2021,16(6):798−809. doi: 10.1111/1749-4877.12510
[16]	LI Z, PENG C, ZHANG G, et al. Prevalence and characteristics of multidrug-resistant Proteus mirabilis from broiler farms in Shandong Province, China[J]. Poultry Science,2022,101(4):101710. doi: 10.1016/j.psj.2022.101710
[17]	ALGAMMAL A M, HASHEM H R, ALFIFI K J, et al. ATPD gene sequencing, multidrug resistance traits, virulence-determinants, and antimicrobial resistance genes of emerging XDR and MDR-Proteus mirabilis[J]. Scientific Reports,2021,11(1):9476. doi: 10.1038/s41598-021-88861-w
[18]	CHINNAM B K, NELAPATI S, TUMATI S R, et al. Detection of β-lactamase-producing Proteus mirabilis strains of animal origin in Andhra Pradesh, India and their genetic diversity[J]. Journal of Food Protection,2021,84(8):1374−1379. doi: 10.4315/JFP-20-399
[19]	SANCHES M S, SILVA L C, SILVA C R D, et al. Prevalence of antimicrobial resistance and clonal relationship in ESBL/AmpC-producing Proteus mirabilis isolated from meat products and community-acquired urinary tract infection (UTI-CA) in Southern Brazi[J]. Antibiotics-Basel,2023,12(2):370.
[20]	徐睿, 李颜桃. 鸡源致病性奇异变形杆菌的分离鉴定与遗传进化分析[J]. 中国畜牧兽医,2018,45(9):2550−2558. [XU Rui, LI Yantao. Isolation, identification and genetic evolution analysis of chicken pathogenic Proteus mirabilis[J]. China Animal Husbandry and Veterinary Medicine,2018,45(9):2550−2558. doi: 10.16431/j.cnki.1671-7236.2018.09.027 XU Rui, LI Yantao. Isolation, identification and genetic evolution analysis of chicken pathogenic Proteus mirabilis[J]. China Animal Husbandry and Veterinary Medicine, 2018, 45(9): 2550-2558. doi: 10.16431/j.cnki.1671-7236.2018.09.027
[21]	马婷婷, 韦显凯, 闭璟珊, 等. 猪源奇异变形杆菌的分离鉴定及其毒力的测定[J]. 中国兽医科学,2017,47(10):1234−1239. [MA Tingting, WEI Xiankai, BI Jingshan, et al. Isolation, identification and toxicity test of Proteus mirabilis from swine[J]. Veterinary Science in China,2017,47(10):1234−1239. MA Tingting, WEI Xiankai, BI Jingshan, et al. Isolation, identification and toxicity test of Proteus mirabilis from swine[J]. Veterinary Science in China, 2017, 47(10): 1234-1239.
[22]	GAZEL D, DEMIRBAKAN H, ERINMEZ M. In vitro activity of hyperthermia on swarming motility and antimicrobial susceptibility profiles of Proteus mirabilis isolates[J]. International Journal of Hyperthermia,2021,38(1):1002−1012. doi: 10.1080/02656736.2021.1943546
[23]	HUMPHRIES R, BOBENCHIK A M, HINDLER J A, et al. Overview of changes to the clinical and laboratory standards institute performance standards for antimicrobial susceptibility testing, M100, 31st edition[J]. Journal of Clinical Microbiology,2021,59(12):e0021321. doi: 10.1128/JCM.00213-21
[24]	PETCA R C, NEGOIȚĂ S, MAREȘ C, et al. Heterogeneity of antibiotics multidrug-resistance profile of uropathogens in Romanian population[J]. Antibiotics-Basel,2021,10(5):523. doi: 10.3390/antibiotics10050523
[25]	SUN Y, WEN S, ZHAO L, et al. Association among biofilm formation, virulence gene expression, and antibiotic resistance in Proteus mirabilis isolates from diarrhetic animals in Northeast China[J]. BMC Veterinary Research,2020,16(1):176. doi: 10.1186/s12917-020-02372-w
[26]	何欣怡, 徐睿, 任丽, 等. 鸡源致病性奇异变形杆菌分离鉴定及药敏试验[J]. 现代畜牧兽医,2018,356(7):10−15. [HE Xinyi, XU Rui, REN Li, et al. Isolation, identification and drug sensitivity test of chicken pathogenic Proteus mirabilis[J]. Modern Journal of Animal Husbandry and Veterinary Medicine,2018,356(7):10−15. HE Xinyi, XU Rui, REN Li, et al. Isolation, identification and drug sensitivity test of chicken pathogenic Proteus mirabilis[J]. Modern Journal of Animal Husbandry and Veterinary Medicine, 2018, 356(7): 10-15.
[27]	刘娜, 李慧芳, 姬晶晶, 等. 河北省鸡肉中四种主要致病菌的多重定量PCR检测方法的建立与应用[J]. 中国兽医科学,2019,49(12):1549−1554. [LIU Na, LI Huifang, JI Jingjing, et al. Establishment and application of multiplex qantitative PCR for the detection on four pathogenic bacteria from chicken meat in Hebei[J]. Chinese Veterinary Science,2019,49(12):1549−1554. LIU Na, LI Huifang, JI Jingjing, et al. Establishment and application of multiplex qantitative PCR for the detection on four pathogenic bacteria from chicken meat in Hebei[J]. Chinese Veterinary Science, 2019, 49(12): 1549-1554.
[28]	刘迎, 刘利强, 李慧芳, 等. 新鲜鸡肉中奇异变形杆菌定量PCR检测与耐药性分析[J]. 农产品加工,2022(17):63−67, 71. [LIU Ying, LIU Liqiang, LI Huifang, et al. Quantitative PCR detection and drug resistance analysis of Proteus mirabilis in fresh chicken[J]. Farm Products Processing,2022(17):63−67, 71. LIU Ying, LIU Liqiang, LI Huifang, et al. Quantitative PCR detection and drug resistance analysis of Proteus mirabilis in fresh chicken[J]. Farm Products Processing, 2022(17): 63-67, 71.
[29]	HUSSEIN E I, AL-BATAYNEH K, MASADEH M M, et al. Assessment of pathogenic potential, virulent genes profile, and antibiotic susceptibility of Proteus mirabilis from urinary tract infection[J]. International Journal of Microbiology,2020,2020:1231807.
[30]	贾沅铮, 胡剑刚, 王志豪, 等. 鸡源奇异变形杆菌分离鉴定及生物学特性[J]. 微生物学通报,2021,48(9):3013−3024. [JIA Yuanzheng, HU Jiangang, WANG Zhihao, et al. Isolation, identification and biological characteristics of a Proteus mirabilis from chicken[J]. Microbiology China,2021,48(9):3013−3024. JIA Yuanzheng, HU Jiangang, WANG Zhihao, et al. Isolation, identification and biological characteristics of a Proteus mirabilis from chicken[J]. Microbiology China, 2021, 48(9): 3013-3024.
[31]	QU X, ZHOU J, HUANG H, et al. Genomic Investigation of Proteus mirabilis isolates recovered from pig farms in Zhejiang province, China[J]. Frontiers in Microbiology,2022,13:952982. doi: 10.3389/fmicb.2022.952982
[32]	KIM S H, WEI C I, AN H. Molecular characterization of multidrug-resistant Proteus mirabilis isolates from retail meat products[J]. Journal of Food Protection,2005,68(7):1408−1413. doi: 10.4315/0362-028X-68.7.1408
[33]	BOUDJEMAA H, ALLEM R, FONKOU M D M, et al. Molecular drivers of emerging multidrug resistance in Proteus mirabilis clinical isolates from Algeria[J]. Journal of Global Antimicrobial Resistance,2019,18:249−256. doi: 10.1016/j.jgar.2019.01.030
[34]	LECURU M, NICOLAS-CHANOINE M H, TANAKA S, et al. Emergence of imipenem resistance in a CpxA-H208P-variant-producing Proteus mirabilis clinical isolate[J]. Microbial Drug Resistance,2021,27(6):747−751. doi: 10.1089/mdr.2020.0295
[35]	SILVA S, ARAÚJO L, NASCIMENTO J J A, et al. Effects of cefazolin and meropenem in eradication biofilms of clinical and environmental isolates of Proteus mirabilis[J]. Current Microbiology,2020,77(8):1681−1688. doi: 10.1007/s00284-020-01984-7
[36]	RUBIC Z, SOPREK S, JELIC M, et al. Molecular characterization of β-lactam resistance and antimicrobial susceptibility to possible therapeutic options of AmpC-producing multidrug-resistant Proteus mirabilis in a university hospital of Split, Croatia[J]. Microbial Drug Resistance,2021,27(2):162−169. doi: 10.1089/mdr.2020.0002
[37]	WONG M H, WAN H Y, CHEN S. Characterization of multidrug-resistant Proteus mirabilis isolated from chicken carcasses[J]. Foodborne Pathogens and Disease,2013,10(2):177−181. doi: 10.1089/fpd.2012.1303
[38]	GUO S, AUNG K T, TAY M Y F, et al. Extended-spectrum β-lactamase-producing Proteus mirabilis with multidrug resistance isolated from raw chicken in Singapore: genotypic and phenotypic analysis[J]. Journal of Global Antimicrobial Resistance,2019,19:252−254. doi: 10.1016/j.jgar.2019.10.013
[39]	申进玲, 杨保伟, 席美丽, 等. 陕西省部分地区零售肉中沙门氏菌和奇异变形杆菌Ⅰ类整合子检测与耐药分[J]. 食品科学,2011,32(9):130−134. [[SHEN Jinling, YANG Baowei, XI Meili, et al. Class Ⅰ integron and antibiotic resistance of salmonella and Proteus mirabilis in retail meat from Shanxi Province[J]. Food Science,2011,32(9):130−134. [SHEN Jinling, YANG Baowei, XI Meili, et al. Class Ⅰ integron and antibiotic resistance of salmonella and Proteus mirabilis in retail meat from Shanxi Province[J]. Food Science, 2011, 32(9): 130-134.

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