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Frontiers of Medicine

ISSN 2095-0217

ISSN 2095-0225(Online)

CN 11-5983/R

Postal Subscription Code 80-967

2018 Impact Factor: 1.847

Front. Med.    2018, Vol. 12 Issue (1) : 104-112    https://doi.org/10.1007/s11684-017-0593-9
RESEARCH ARTICLE
Prevalence and molecular characteristics of Listeria monocytogenes in cooked products and its comparison with isolates from listeriosis cases
Hong Wang1, Lijuan Luo2, Zhengdong Zhang1, Jianping Deng1, Yan Wang2, Yimao Miao1, Ling Zhang1, Xi Chen1, Xiang Liu1, Songsong Sun1, Bo Xiao1, Qun Li1(), Changyun Ye2()
1. Zigong Center for Disease Control and Prevention, Zigong 643000, China
2. State Key Laboratory of Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, Chinese Center for Disease Control and Prevention, Beijing 102206, China
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Abstract

This study aimed to investigate the prevalence and molecular characteristics of Listeria monocytogenes in cooked products in Zigong City, China. The overall occurrence of the L. monocytogenes in the ready-to-eat (RTE) shops and mutton restaurants surveyed was 16.2% (141/873). An occurrence of 13.5% was observed in RTE pork, 6.5% in RTE vegetables, and more than 24.0% in either cooked mutton or cooked haggis. Serotype 1/2b (45.4%), 1/2a (33.3%), and 1/2c (14.2%) were the predominant types. By comparing the clonal complexes (CCs) based on multilocus sequence typing (MLST) of the L. monocytogenes from cooked foods in Zigong City and 33 listeriosis cases from different districts of China, CC87, CC9, CC8, and CC3 were showed to be prevalent in cooked products and CC87 and CC3 were the first two frequent types in the 33 clinic-source strains. All CC87 stains harbored the newly reported Listeria pathogenicity island 4 (LIPI-4) gene fragment ptsA, and all CC3 strains possessed the Listeria pathogenicity island 3 (LIPI-3) gene fragment llsX. These may increase the occurrence of the strains belonging to CC87 and CC3 in listeriosis cases in China and also underline the risk of infection owing to the consumption of the cooked products from Zigong. ST619 (serotype 1/2b) harbored both llsX and ptsA, indicating a potential hypervirulent sequence type in Zigong.

Keywords Listeria monocytogenes      MLST      LIPI-3      LIPI-4      RTE      listeriosis     
Corresponding Author(s): Qun Li,Changyun Ye   
Just Accepted Date: 03 November 2017   Online First Date: 25 January 2018    Issue Date: 06 February 2018
 Cite this article:   
Hong Wang,Lijuan Luo,Zhengdong Zhang, et al. Prevalence and molecular characteristics of Listeria monocytogenes in cooked products and its comparison with isolates from listeriosis cases[J]. Front. Med., 2018, 12(1): 104-112.
 URL:  
https://academic.hep.com.cn/fmd/EN/10.1007/s11684-017-0593-9
https://academic.hep.com.cn/fmd/EN/Y2018/V12/I1/104
Sample types No. of total samples No. of LM positive samples LM rate (%)
RTE food shops 560 66b 11.8
Cooked muttona 37 9 24.3
Sum of RTE foods 523 57 10.9
RTE beef 11 2 18.2
RTE chicken 25 0 0.0
RTE pork 334 45 13.5
RTE vegetables 153 10 6.5
Mutton restaurants 313 75c 24.0
Cooked haggis 125 34 27.2
Cooked mutton 102 32 31.4
Refrigerator swab 31 3 9.7
Meat containers swab 20 2 10.0
Table and knife swab 35 4 11.4
Total 873 141 16.2
Tab.1  Occurrence of L. monocytogenes (LM) in different sample types
RTE food shops Mutton restaurants
Total LMa LM rate (%) Total LMa LM rate (%)
Winter 124 15 12.1 53 12 22.6
Spring 136 26 19.1 86 29 33.7
Summer 149 11 7.4 82 17 20.7
Autumn 151 14 9.3 92 17 18.5
Total 560 66 11.8 313 75 24.0
Tab.2  Seasonal variation of isolation rate of L. monocytogenes (LM) from different sources
CCs Source Patients llsX ptsA Serotype ST
MRa,c RSb,c Totalc
CC87 6 (5) 20 (10) 26 (15) 8 + 1/2b 87, 1166
CC3 18 (1) 15 (6) 33 (7) 6 + 1/2b 3, 778
CC5 2 (2) 0 2 (2) 2 1/2b 5
ST619 1 (1) 2 (1) 3 (2) 0 + + 1/2b 619
CC7 2 (1) 1 (1) 3 (2) 5 1/2a 7
CC8 11 (3) 7 (5) 18 (8) 3 1/2a 8
CC121 1 (1) 2 (2) 3 (3) 1 1/2a 121
CC19 4 (3) 0 4 (3) 1 1/2a 19, 1036
CC412 15 (4) 0 15 (4) 0 1/2a 412
CC101 0 1 (1) 1 (1) 0 1/2a 101
CC14 0 2 (2) 2 (2) 0 1/2a 14, 91
CC475 0 1 (1) 1 (1) 0 1/2a 504
CC9 12 (7) 8 (6) 20 (13) 1 1/2c 9
CC155 2 (2) 2 (2) 4 (4) 3 3a 155, 381
CC2 0 2 (2) 2 (2) 2 4b 2
CC1 0 4 (3) 4 (3) 1 + 4b 1, 308
Total 74 (14) 67 (21) 141 (35) 33
Tab.3  CCs and virulence factors distribution of L. monocytogenes from different sources
Fig.1  Minimum spanning tree based on multilocus sequence typing of L. monocytogenes from different sources. This tree was constructed with BioNumerics 4.0 based on the 33 clinical strains from different districts of China and the 141 cooked food strains from Zigong City in 2015. The number in the circle referred to the sequence type (ST). The size of circles represents the number of isolates, which were indicated in Table S2. The length and the numbers of the strings between circles represent the number of housekeeping genes that differed between the two STs. STs differed with one allele were defined as the same CC, being surrounded with one color.
Fig.2  Infection types of the 33 clinic-source L. monocytogenes strains in different CCs. This column chart was constructed using Microsoft Excel 2010. Different colors represent different infection types: purple refers to bacteremia, green refers to CNS infections, and red refers to MN infections (maternal-neonatal infections).
Fig.3  Maximum likelihood-based phylogenetic tree of L. monocytogenes by concatenating the seven sequenced housekeeping genes of each isolate and the presence of llsX and ptsA. This tree was constructed using Mega 5.04 software, based on the seven concatenated housekeeping genes (which were aligned with EditSeq software [DNASTAR/Lasergene]) of 40 STs, including the 22 STs in this study and the dominant STs of the top 30 CCs among the 6633 food and clinical isolates in Maury et al.’s study and ST382 in Chen et al.’s report [15,23]. All of the bootstrap values (1000 replicates) were shown on the branch nodes of the tree.
1 Cartwright EJ, Jackson  KA, Johnson SD,  Graves LM,  Silk BJ,  Mahon BE. Listeriosis outbreaks and associated food vehicles, United States, 1998–2008. Emerg Infect Dis 2013; 19(1): 1–9, quiz 184
https://doi.org/10.3201/eid1901.120393 pmid: 23260661
2 Kvistholm Jensen A,  Nielsen EM,  Björkman JT,  Jensen T,  Müller L,  Persson S,  Bjerager G,  Perge A,  Krause TG,  Kiil K, Sørensen  G, Andersen JK,  Mølbak K,  Ethelberg S. Whole-genome sequencing used to investigate a nationwide outbreak of listeriosis caused by ready-to-eat delicatessen meat, Denmark, 2014. Clin Infect Dis 2016; 63(1): 64–70
https://doi.org/10.1093/cid/ciw192 pmid: 27025820
3 Swaminathan B, Gerner-Smidt  P. The epidemiology of human listeriosis. Microbes Infect 2007; 9(10): 1236–1243
https://doi.org/10.1016/j.micinf.2007.05.011 pmid: 17720602
4 Adrião A, Vieira  M, Fernandes I,  Barbosa M,  Sol M, Tenreiro  RP, Chambel L,  Barata B,  Zilhao I,  Shama G,  Perni S,  Jordan SJ,  Andrew PW,  Faleiro ML. Marked intra-strain variation in response of Listeria monocytogenes dairy isolates to acid or salt stress and the effect of acid or salt adaptation on adherence to abiotic surfaces. Int J Food Microbiol 2008; 123(1-2): 142–150
https://doi.org/10.1016/j.ijfoodmicro.2007.12.016 pmid: 18258322
5 NicAogáin K,  O’Byrne CP. The role of stress and stress adaptations in determining the fate of the bacterial pathogen Listeria monocytogenes in the food chain. Front Microbiol 2016; 7: 1865
https://doi.org/10.3389/fmicb.2016.01865 pmid: 27933042
6 Jayaraj K, Di Bisceglie  AM, Gibson S. Spontaneous bacterial peritonitis caused by infection with Listeria monocytogenes: a case report and review of the literature. Am J Gastroenterol 1998; 93(9): 1556–1558
https://doi.org/10.1111/j.1572-0241.1998.00482.x pmid: 9732945
7 Schett G, Herak  P, Graninger W,  Smolen JS,  Aringer M. Listeria-associated arthritis in a patient undergoing etanercept therapy: case report and review of the literature. J Clin Microbiol 2005; 43(5): 2537–2541
https://doi.org/10.1128/JCM.43.5.2537-2541.2005 pmid: 15872306
8 Bourgeois N, Jacobs  F, Tavares ML,  Rickaert F,  Deprez C,  Liesnard C,  Moonens F,  Van de Stadt J,  Gelin M,  Adler M. Listeria monocytogenes hepatitis in a liver transplant recipient: a case report and review of the literature. J Hepatol 1993; 18(3): 284–289
https://doi.org/10.1016/S0168-8278(05)80271-5 pmid: 8228121
9 Mylonakis E, Hohmann  EL, Calderwood SB. Central nervous system infection with Listeria monocytogenes. 33 years’ experience at a general hospital and review of 776 episodes from the literature. Medicine (Baltimore) 1998; 77(5): 313–336
https://doi.org/10.1097/00005792-199809000-00002 pmid: 9772921
10 McLauchlin J. Human listeriosis in Britain, 1967–85, a summary of 722 cases. 1. Listeriosis during pregnancy and in the newborn. Epidemiol Infect 1990; 104(2): 181–189
https://doi.org/10.1017/S0950268800059343 pmid: 2108869
11 Commission of European Communities. Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Luxembourg: Publications Office of the European Union 2005. 22.12.2005:L 338/1. 
12 Garrido V, Vitas  AI, García-Jalón  I. Survey of Listeria monocytogenes in ready-to-eat products: prevalence by brands and retail establishments for exposure assessment of listeriosis in Northern Spain. Food Control 2009; 20(11): 986–991
https://doi.org/10.1016/j.foodcont.2008.11.013
13 Scallan E, Hoekstra  RM, Angulo FJ,  Tauxe RV,  Widdowson MA,  Roy SL, Jones  JL, Griffin PM. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis 2011; 17(1): 7–15
https://doi.org/10.3201/eid1701.P11101 pmid: 21192848
14 Scallan E, Hoekstra  RM, Mahon BE,  Jones TF,  Griffin PM. An assessment of the human health impact of seven leading foodborne pathogens in the United States using disability adjusted life years. Epidemiol Infect 2015; 143(13): 2795–2804
https://doi.org/10.1017/S0950268814003185 pmid: 25633631
15 Maury MM, Tsai  YH, Charlier C,  Touchon M,  Chenal-Francisque V,  Leclercq A,  Criscuolo A,  Gaultier C,  Roussel S,  Brisabois A,  Disson O,  Rocha EPC,  Brisse S,  Lecuit M. Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity. Nat Genet 2016; 48(3): 308–313
https://doi.org/10.1038/ng.3501 pmid: 26829754
16 Cotter PD, Draper  LA, Lawton EM,  Daly KM,  Groeger DS,  Casey PG,  Ross RP,  Hill C. Listeriolysin S, a novel peptide haemolysin associated with a subset of lineage I Listeria monocytogenes. PLoS Pathog 2008; 4(9): e1000144
https://doi.org/10.1371/journal.ppat.1000144 pmid: 18787690
17 Quereda JJ, Meza-Torres  J, Cossart P,  Pizarro-Cerdá J. Listeriolysin S: a bacteriocin from epidemic Listeria monocytogenes strains that targets the gut microbiota. Gut Microbes 2017; 8(4): 384–391
https://doi.org/10.1080/19490976.2017.1290759 pmid: 28156183
18 Luo L, Zhang  Z, Wang H,  Wang P, Lan  R, Deng J,  Miao Y, Wang  Y, Wang Y,  Xu J, Zhang  L, Sun S,  Liu X, Zhou  Y, Chen X,  Li Q, Ye  C. A 12-month longitudinal study of Listeria monocytogenes contamination and persistence in pork retail markets in China. Food Control 2017; 76: 66–73
https://doi.org/10.1016/j.foodcont.2016.12.037
19 Wang Y, Jiao  Y, Lan R,  Xu X, Liu  G, Wang X,  Zhang L,  Pang H, Jin  D, Dai H,  Yuan X, Zhang  W, Xu J,  Ye C. Characterization of Listeria monocytogenes isolated from human listeriosis cases in China. Emerg Microbes Infect 2015; 4(8): e50
https://doi.org/10.1038/emi.2015.50 pmid: 26421272
20 Doumith M, Buchrieser  C, Glaser P,  Jacquet C,  Martin P. Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J Clin Microbiol 2004; 42(8): 3819–3822
https://doi.org/10.1128/JCM.42.8.3819-3822.2004 pmid: 15297538
21 Ragon M, Wirth  T, Hollandt F,  Lavenir R,  Lecuit M,  Le Monnier A,  Brisse S. A new perspective on Listeria monocytogenes evolution. PLoS Pathog 2008; 4(9): e1000146
https://doi.org/10.1371/journal.ppat.1000146 pmid: 18773117
22 Clayton EM, Hill  C, Cotter PD,  Ross RP. Real-time PCR assay to differentiate Listeriolysin S-positive and-negative strains of Listeria monocytogenes. Appl Environ Microbiol 2011; 77(1): 163–171
https://doi.org/10.1128/AEM.01673-10 pmid: 21075895
23 Chen Y, Luo  Y, Pettengill J,  Timme R,  Melka D,  Doyle M,  Jackson A,  Parish M,  Hammack TS,  Allard MW,  Brown EW,  Strain EA. Singleton sequence type 382, an emerging clonal group of Listeria monocytogenes associated with three multistate outbreaks linked to contaminated stone fruit, caramel apples, and leafy green salad. J Clin Microbiol 2017; 55(3): 931–941
https://doi.org/10.1128/JCM.02140-16 pmid: 28053218
24 Chen M, Wu  Q, Zhang J,  Wang J. Prevalence and characterization of Listeria monocytogenes isolated from retail-level ready-to-eat foods in South China. Food Control 2014; 38: 1–7
https://doi.org/10.1016/j.foodcont.2013.09.061
25 Hassani M, Álvarez  I, Raso J,  Condón S,  Pagán R. Comparing predicting models for heat inactivation of Listeria monocytogenes and Pseudomonas aeruginosa at different pH. Int J Food Microbiol 2005; 100(1-3): 213–222
https://doi.org/10.1016/j.ijfoodmicro.2004.10.017 pmid: 15854706
26 Chau ML, Aung  KT, Hapuarachchi HC,  Lee PSV,  Lim PY, Kang  JSL, Ng Y,  Yap HM, Yuk  HG, Gutiérrez RA,  Ng LC. Microbial survey of ready-to-eat salad ingredients sold at retail reveals the occurrence and the persistence of Listeria monocytogenes sequence types 2 and 87 in pre-packed smoked salmon. BMC Microbiol 2017; 17(1): 46
https://doi.org/10.1186/s12866-017-0956-z pmid: 28245788
27 Stephan R, Althaus  D, Kiefer S,  Lehner A,  Hatz C, Schmutz  C, Jost M,  Gerber N,  Baumgartner A,  Hächler H,  Mäusezahl-Feuz M. Foodborne transmission of Listeria monocytogenes via ready-to-eat salad: a nationwide outbreak in Switzerland, 2013–2014. Food Control 2015; 57: 14–17
https://doi.org/10.1016/j.foodcont.2015.03.034
28 Heisick JE, Wagner  DE, Nierman ML,  Peeler JT. Listeria spp. found on fresh market produce. Appl Environ Microbiol 1989; 55(8): 1925–1927
pmid: 2506809
29 Jensen AK, Björkman  JT, Ethelberg S,  Kiil K, Kemp  M, Nielsen EM. Molecular typing and epidemiology of human listeriosis cases, Denmark, 2002–2012. Emerg Infect Dis 2016; 22(4): 625–633
https://doi.org/10.3201/eid2204.150998 pmid: 26982714
30 Wang Y, Zhao  A, Zhu R,  Lan R, Jin  D, Cui Z,  Wang Y, Li  Z, Wang Y,  Xu J, Ye  C. Genetic diversity and molecular typing of Listeria monocytogenes in China. BMC Microbiol 2012; 12(1): 119
https://doi.org/10.1186/1471-2180-12-119 pmid: 22727037
31 Wu S, Wu  Q, Zhang J,  Chen M, Guo  W. Analysis of multilocus sequence typing and virulence characterization of Listeria monocytogenes isolates from Chinese retail ready-to-eat food. Front Microbiol 2016; 7: 168
https://doi.org/10.3389/fmicb.2016.00168 pmid: 26909076
32 Ebner R, Stephan  R, Althaus D,  Brisse S,  Maury M,  Tasara T. Phenotypic and genotypic characteristics of Listeria monocytogenes strains isolated during 2011–2014 from different food matrices in Switzerland. Food Control 2015; 57: 321–326
https://doi.org/10.1016/j.foodcont.2015.04.030
33 Wang K, Ye  K, Zhu Y,  Huang Y,  Wang G, Wang  H, Zhou G. Prevalence, antimicrobial resistance and genetic diversity of Listeria monocytogenes isolated from chilled pork in Nanjing, China. Lebensm Wiss Technol 2015; 64(2): 905–910
https://doi.org/10.1016/j.lwt.2015.06.015
34 Althaus D, Lehner  A, Brisse S,  Maury M,  Tasara T,  Stephan R. Characterization of Listeria monocytogenes strains isolated during 2011–2013 from human infections in Switzerland. Foodborne Pathog Dis 2014; 11(10): 753–758
https://doi.org/10.1089/fpd.2014.1747 pmid: 25007293
35 Wang G, Qian  W, Zhang X,  Wang H, Ye  K, Bai Y,  Zhou G. Prevalence, genetic diversity and antimicrobial resistance of Listeria monocytogenes isolated from ready-to-eat meat products in Nanjing, China. Food Control 2015; 50: 202–208
https://doi.org/10.1016/j.foodcont.2014.07.057
36 Huang YT, Ko  WC, Chan YJ,  Lu JJ, Tsai  HY, Liao CH,  Sheng WH,  Teng LJ,  Hsueh PR. Disease burden of invasive listeriosis and molecular characterization of clinical isolates in Taiwan, 2000–2013. PLoS One 2015; 10(11): e0141241
https://doi.org/10.1371/journal.pone.0141241 pmid: 26555445
37 Pérez-Trallero E,  Zigorraga C,  Artieda J,  Alkorta M,  Marimón JM. Two outbreaks of Listeria monocytogenes infection, Northern Spain. Emerg Infect Dis 2014; 20(12): 2155–2157
https://doi.org/10.3201/eid2012.140993 pmid: 25418800
38 Yan H, Neogi  SB, Mo Z,  Guan W, Shen  Z, Zhang S,  Li L, Yamasaki  S, Shi L,  Zhong N. Prevalence and characterization of antimicrobial resistance of foodborne Listeria monocytogenes isolates in Hebei Province of Northern China, 2005–2007. Int J Food Microbiol 2010; 144(2): 310–316
https://doi.org/10.1016/j.ijfoodmicro.2010.10.015 pmid: 21074885
39 Korsak D, Borek  A, Daniluk S,  Grabowska A,  Pappelbaum K. Antimicrobial susceptibilities of Listeria monocytogenes strains isolated from food and food processing environment in Poland. Int J Food Microbiol 2012; 158(3): 203–208
https://doi.org/10.1016/j.ijfoodmicro.2012.07.016 pmid: 22874767
40 Martín B, Perich  A, Gómez D,  Yangüela J,  Rodríguez A,  Garriga M,  Aymerich T. Diversity and distribution of Listeria monocytogenes in meat processing plants. Food Microbiol 2014; 44: 119–127
https://doi.org/10.1016/j.fm.2014.05.014 pmid: 25084653
41 Chen J, Chen  Q, Jiang J,  Hu H, Ye  J, Fang W. Serovar 4b complex predominates among Listeria monocytogenes isolates from imported aquatic products in China. Foodborne Pathog Dis 2010; 7(1): 31–41
https://doi.org/10.1089/fpd.2009.0353 pmid: 19735205
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[7] Jichun Yang, Kaiyue Jin, Jiajun Xiao, Jing Ma, Duan Ma. Endogenous tissue factor pathway inhibitor in vascular smooth muscle cells inhibits arterial thrombosis[J]. Front. Med., 2017, 11(3): 403-409.
[8] Yanlin Zhao,Xiao Zhong,Xiaohong Ou,Huawei Cai,Xiaoai Wu,Rui Huang. Cotransfecting norepinephrine transporter and vesicular monoamine transporter 2 genes for increased retention of metaiodobenzylguanidine labeled with iodine 131 in malignant hepatocarcinoma cells[J]. Front. Med., 2017, 11(1): 120-128.
[9] Liangyun Zhou,Guang Yang,Haifeng Sun,Jinfu Tang,Jian Yang,Yizhan Wang,Thomas Avery Garran,Lanping Guo. Effects of different doses of cadmium on secondary metabolites and gene expression in Artemisia annua L.[J]. Front. Med., 2017, 11(1): 137-146.
[10] Zhiwei Hu,Meiping Chen,Jimin Wu,Qing Song,Chao Yan,Xing Du,Zhonggao Wang. Improved control of hypertension following laparoscopic fundoplication for gastroesophageal reflux disease[J]. Front. Med., 2017, 11(1): 68-73.
[11] Lan Wang,Sen Jiang,Jingyun Shi,Sugang Gong,Qinhua Zhao,Rong Jiang,Ping Yuan,Bigyan Pudasaini,Jing He,Zhicheng Jing,Jinming Liu. Clinical characteristics of pulmonary hypertension in bronchiectasis[J]. Front. Med., 2016, 10(3): 336-344.
[12] Marijke A. de Vries,Arash Alipour,Erwin Birnie,Andrew Westzaan,Selvetta van Santen,Ellen van der Zwan,Anho H. Liem,Noëlle van der Meulen,Manuel Castro Cabezas. Coronary leukocyte activation in relation to progression of coronary artery disease[J]. Front. Med., 2016, 10(1): 85-90.
[13] Dan Wu,Qingxun Hu,Yizhun Zhu. Therapeutic application of hydrogen sulfide donors: the potential and challenges[J]. Front. Med., 2016, 10(1): 18-27.
[14] David P. Taggart. Contemporary coronary artery bypass grafting[J]. Front. Med., 2014, 8(4): 395-398.
[15] Zhe Zheng, Lu Zhang, Xi Li, Shengshou Hu, on behalf of the Chinese CABG Registry Study. SinoSCORE: a logistically derived additive prediction model for post-coronary artery bypass grafting in-hospital mortality in a Chinese population[J]. Front Med, 2013, 7(4): 477-485.
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