Review on pathogenicity of Staphylococcus aureus in food
WANG Xuan1, 2, WANG Ping1, GE Yi-qiang2, 3, CHEN Ying1
1. Agro-product Safety Research Center, Chinese Academy of Inspection and Quarantine, Beijing 100176, China; 2. College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, China; 3. China Rural Technology Development Center, Ministry of Science and Technology, Beijing 100045, China
Abstract：Staphylococcus aureus, an important foodborne pathogen, can contaminate foods through variety of ways and produce enterotoxin that may cause Staphylococcal food poisoning. In addition to food safety problems, Staphylococcus aureus could also cause clinical infection. The study of its pathogenicity is not only beneficial to prevent and control foodborne diseases, but also provide a new point for clinical treatment. This paper analyzes the types and characteristics of common strains of Staphylococcus aureus in food, and summaries the effect of food processing on pathogenicity and the methods for pathogenicity research in order to provide reference for the related study on pathogenicity of Staphylococcus aureus.
王璇, 王娉, 葛毅强, 陈颖. 食品中金黄色葡萄球菌致病性研究进展[J]. 中国人兽共患病学报, 2017, 33(6): 553-558.
WANG Xuan, WANG Ping, GE Yi-qiang, CHEN Ying. Review on pathogenicity of Staphylococcus aureus in food. Chinese Journal of Zoonoses, 2017, 33(6): 553-558.
[1] Ingraham JL, Ingraham C A.Introduction to microbiology II [M].Barcelona:Editorial Reverte, 1998. [2] National Health and Family Planning Commission of the People’s Republic of China.The report of the food poisoning events occurred in 2015 of China [EB/OL].(2016-04-01)[2016-05-15].http://www.nhfpc.gov.cn/yjb/s7859/2016-04/8d34e4c442c54 d33909319954 c43311c.shtml.(in Chinese). 中华人民共和国国家卫生和计划生育委员会.国家卫生计生委办公厅关于2015年全国食物中毒事件情况的通报[EB/OL].http://www.nhfpc.gov.cn/yjb/s7859/201604/8d34e4c442c54 d33909319954c43311c.shtml.2016-04-01. [3] Authority EFS.The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2013 [J].EFSa Journal, 2015, 13(1): 3391. [4] Scallan E, Hoekstra RM, Angulo FJ, et al.Foodborne illness acquired in the United States-major pathogens [J].Emerg Infect Dis, 2011, 17: 7-15.doi:10.3201/eid1701.P11101 [5] Li QQ, Fan YL, Song MH, et al.Research advances on foodborne staphylococcal enterotoxins and its detection methods [J].J Food Safety Quality, 2016, 7(2): 555-560.(in Chinese) 李琼琼, 范一灵, 宋明辉, 等.食源性金葡菌肠毒素及其检测方法[J].食品安全质量检测学报, 2016, 7(2): 555-560. [6] Xu ZB, Liu XC, Li L, et al.Development of Staphylococcus aureus enterotoxin in food-borne bacteria [J].Mod Food Sci Technol, 2013, 29(9): 2317-2324.(in Chinese) 徐振波, 刘晓晨, 李琳,等.金葡菌肠毒素在食源性微生物中的研究进展[J].现代食品科技, 2013, 29(9): 2317-2324.doi:10.13982/j.mfst.1673-9078.2013.09.020 [7] Suzuki Y, Omoe K, Hu DL, et al.Molecular epidemiological characterization of Staphylococcus aureus isolates originating from food poisoning outbreaks that occurred in Tokyo, Japan [J].Microbiol Immunol, 2014, 58(10): 570-580.doi:10.1111/1348-0421.12188 [8] Armand-Lefevre L, Ruimy R, Andremont A.Clonal comparison of Staphylococcus aureus isolates from healthy pig farmers, human controls, and pigs [J].Emerg Infect Dis, 2005, 11(5): 711-714. [9] Uhlemann AC, Dumortier C, Hafer C, et al.Molecular characterization of Staphylococcus aureus from outpatients in the Caribbean reveals the presence of pandemic clones [J].Euro J Clin Microl Infec Dis, 2012, 31(4): 505-511.doi:10.1007/s10096-011-1339-2 [10] Paterson GK, Larsen J, Harrison EM, et al.First detection of livestock-associated meticillin-resistant Staphylococcus aureus CC398 in bulk tank milk in the United Kingdom, January to July 2012 [J].Euro Surveillance, 2012, 17(50). [11] Chairat S, Gharsa H, Lozano C, et al.Characterization of Staphylococcus aureus from raw meat samples in tunisia: Detection of clonal lineage ST398 from the African Continent [J].Foodborne Pathog Dis, 2015, 12(8): 686-692.doi:10.1089/fpd.2015.1958 [12] Song M, Bai Y, Xu J, et al.Genetic diversity and virulence potential of Staphylococcus aureus isolates from raw and processed food commodities in Shanghai [J].Int J Food Microbiol, 2015, 195(16): 1-8.doi:10.1016/j.ijfoodmicro.2014.11.020 [13] Wendlandt S, Schwarz S, Silley P.Methicillin-resistant Staphylococcus aureus : a food-borne pathogen [J].Annual Rev Food Sci Technol, 2013, 4: 117-139.doi:10.1146/annurev-food-030212-182653 [14] de Bentzmann S, Tristan A, Etienne J, et al.Staphylococcus aureus isolates associated with necrotizing pneumonia bind to basement membrane type I and IV collagens and laminin [J].J Infect Dis, 2004, 190(8): 1506-1515.doi:10.1086/424521 [15] Kraushaar B, Ballhausen B, Leeser D, et al.Antimicrobial resistances and virulence markers in Methicillin-resistant Staphylococcus aureus from broiler and turkey: A molecular view from farm to fork [J].Vet Microbiol, 2016.doi:10.1016/j.micpath.2016.01.008 [16] Otto M.MRSA virulence and spread [J].Cell Microbiol, 2012, 14(10): 1513-1521.doi:10.1111/j.1462-5822.2012.01832.x [17] Merz A, Stephan R, Johler S.Genotyping and DNA microarray based characterization of Staphylococcus aureus isolates from rabbit carcasses [J].Meat Sci, 2016, 112: 86-89.doi:10.1016/j.meatsci.2015.11.002 [18] Omoe K, Hu DL, Ono HK, et al.Emetic potentials of newly identified staphylococcal enterotoxin-like toxins [J].Infec Immun, 2013, 81(10): 3627-3631.doi:10.1128/IAI.00550-13. [19] Chang Y, Gao H, Zhu Z, et al.High prevalence and Properties of enterotoxin-producing Staphylococcus aureus ST5 Strains of food sources in China [J].Foodborne Pathog Dis, 2016.doi:10.1089/fpd.2015.2085 [20] Souza EL, Oliveira CEV, Stamford TLM, et al.Influence of carvacrol and thymol on the physiological attributes, enterotoxin production and surface characteristics of Staphylococcus aureus strains isolated from foods [J].Brazilian J Microbiol, 2013, 44(1): 29-36. [21] Wang Q, Tang JN, Tang C, et al.The inhibitory effect of six food antiseptics on the growth and SEs genes expression of S.aureus [J].Food Sci, 2016, 37(21): 151-156.(in Chinese) 王琼, 唐俊妮, 汤承, 等.六种食品防腐剂对金黄色葡萄球菌抑菌效果及肠毒素基因表达的影响[J].食品科学, 2016, 37(21): 151-156.doi:10.7506/spkx1002-6630-201621026 [22] Zeaki N, Radstrom P, Schelin J.Evaluation of potential effects of NaCl and sorbic acid on Staphylococcal enterotoxin A formation [J].Microorganisms, 2015, 3(3): 551-566.doi:10.3390/microorganisms3030551 [23] Wang XJ, Wang N, Song JL, et al.Sublethal injury and inactivation of Staphylococcus aureus under freezing stress [J].Food Sci, 2013, 34(19): 5-9.(in Chinese) 王晓杰, 王娜, 宋金丽, 等.冷冻胁迫下金黄色葡萄球菌的亚致死及失活规律[J].食品科学, 2013, 34(19): 5-9.doi:10.7506/spkx1002-6630-201319002 [24] Suo B, Ju R, Wang N, et al.Effect of frozen stress on sublethal rule and clfA and msrR gene transcriptions of Staphylococcus aureus [J].J Chin Food Sci Technol, 2015 (11): 154-159.(in Chinese) 索标, 居冉, 王娜, 等.冷冻胁迫对金黄色葡萄球菌亚致死及 clfA , msrR 毒力基因转录的影响[J].中国食品学报, 2015 (11): 154-159.doi:10.16429/j.1009-7848.2015.11.023 [25] Portocarrero SM, Newman M, Mikel B.Staphylococcus aureus survival, staphylococcal enterotoxin production and shelf stability of country-cured hams manufactured under different processing procedures [J].Meat Sci, 2002, 62(2): 267-273.doi:10.1016/S0309-1740(02)00026-8 [26] Chen XW, Ding J, Wang W, et al.Inhibiting effects of different lactobacilli on growth and toxin production of Staphylococcus aureus [J].Chin J Health Lab Technol, 2004, 14(3): 306-307.(in Chinese) 陈晓蔚, 丁洁, 王炜, 等.不同乳酸菌对金黄色葡萄球菌生长和产毒的抑制作用研究[J].中国卫生检验杂志, 2004, 14(3): 306-307. [27] Ma J.Study on the growth regulation of Staphylococcus aureus and inhibitive factor in fermented-dry beef producting [D].Inner Mongolia Agricultural University, 2006.(in Chinese) 马菊.干腌牛肉中金黄色葡萄球菌生长规律及其抑菌因素研究[D].内蒙古农业大学, 2006. [28] Bennett RW.Staphylococcal enterotoxin and its rapid identification in foods by enzyme-linked immunosorbent assay-based methodology[J].J Food Protection, 2005, 68(6):1264-1270. [29] Min KJ, Jung YJ, Kwon KY, et al.Effect of temperature on the production of Staphylococcal enterotoxin and thermal inactivation kinetics of Staphylococcus aureus in selected ready-to-eat (RTE) foods in Korea [J].J Food Safety, 2013, 33(1): 17-24.doi:10.1111/jfs.12018 [30] Rajkovic A.Incidence, growth and enterotoxin production of Staphylococcus aureus in insufficiently dried traditional beef ham “govedja prsuta” under different storage conditions [J].Food Control, 2012, 27(2): 369-373.doi:10.1016/j.foodcont.2012.03.028 [31] Spaulding AR, Satterwhite EA, Lin YC, et al.Comparison of Staphylococcus aureus strains for ability to cause infective endocarditis and lethal sepsis in rabbits [J].The Staphylococci and Staphylococcal pathogenesis, 2012: 71.doi:10.3389/fcimb.2012.00018 [32] Pastar I, Nusbaum AG, Gil J, et al.Interactions of methicillin resistant Staphylococcus aureus USA300 and Pseudomonas aeruginosa in polymicrobial wound infection [J].PLoS One, 2013, 8(2): e56846.doi:10.1371/journal.pone.0056846 [33] Kim HK, Missiakas D, Schneewind O.Mouse models for infectious diseases caused by Staphylococcus aureus [J].J Immunological Methods, 2014, 410: 88-99.doi:10.1016/j.jim.2014.04.007 [34] Wacker M, Wang L, Kowarik M, et al.Prevention of Staphylococcus aureus infections by glycoprotein vaccines synthesized in Escherichia coli [J].J Infect Dis, 2014, 209(10): 1551-1561.doi:10.1093/infdis/jit800 [35] Wang ZC, Wang DF,Li JJ, et al.Development and immune efficacy of polyvalent Staphylococcus aureus vaccine against bovine mastitis [J].Chin Vet Drug, 2012, 46(10): 1-4.(in Chinese) 王治才, 王登峰, 李建军, 等.金黄色葡萄球菌性奶牛乳房炎多价疫苗研制和免疫效果评价[J].中国兽药杂志, 2012, 46(10): 1-4. [36] Horsmon JR, Cao CJ, Khan AS, et al.Real-time fluorogenic PCR assays for the detection of entA, the gene encoding staphylococcal enterotoxin A [J].Biotechnol Letters, 2006, 28(11): 823-829.doi:10.1007/s10529-006-9011-0 [37] Zeinhom M, Abdel-Latef GK, Jordan K.The use of multiplex PCR to determine the prevalence of enterotoxigenic Staphylococcus aureus isolated from raw milk, feta cheese, and hand swabs [J].J Food Sci, 2015, 80(12): 2932-2936.doi:10.1111/1750-3841.13147 [38] Sowmya N, Thakur MS, Manonmani HK.Rapid and simple DNA extraction method for the detection of enterotoxigenic Staphylococcus aureus directly from food samples: comparison of PCR and LAMP methods [J].J Applied Microbiol, 2012, 113(1): 106-113.doi:10.1111/j.1365-2672.2012.05315.x [39] Lin WH, Zou BJ, Song QX, et al.Progress in multiplex loop-mediated isothermal amplification technology[J].Hereditas, 2015, 37(9): 899-910.(in Chinese) 林文慧, 邹秉杰, 宋沁馨, 等.多重环介导等温扩增技术研究进展[J].遗传, 2015, 37(9): 899-910.doi:10.16288/j.yczz.15-141 [40] Jin T, Zhu YL, Li J, et al.Staphylococcal protein A, Panton-Valentine leukocidin and coagulase aggravate the bone loss and bone destruction in osteomyelitis [J].Cellular Physiol Biochem, 2013, 32(2): 322-333.doi:10.1159/000354440 [41] Li TM.Control of virulence by the AraC family transcriptional regulator Rsp in Staphylococcus aureus [D].Fudan University, 2014.(in Chinese) 李天铭.AraC家族转录调节蛋白RSP对金黄色葡萄球菌毒力的调节及机制[D].复旦大学, 2014. [42] Kuroda M, Ohta T, Uchiyama I, et al.Whole genome sequencing of meticillin-resistant Staphylococcus aureus [J].Lancet, 2001, 357(9264): 1225-1240.doi:10.1016/S0140-6736(00)04403-2 [43] Baba T, Bae T, Schneewind O, et al.Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes: polymorphism and evolution of two major pathogenicity islands [J].J Bacteriol, 2008, 190(1): 300-310.doi:10.1128/JB.01000-07
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