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The prevalence of Listeria monocytogenes in meat products in

China: A systematic literature review and novel meta-analysis
approach

Yangtai Liu, Wanxia Sun, Tianmei Sun, Leon G.M. Gorris, Xiang
Wang, Baolin Liu, Qingli Dong

PII: S0168-1605(19)30288-0
DOI: https://doi.org/10.1016/j.ijfoodmicro.2019.108358
Reference: FOOD 108358

To appear in: International Journal of Food Microbiology

Received date: 1 January 2019

Revised date: 11 June 2019
Accepted date: 8 September 2019

Please cite this article as: Y. Liu, W. Sun, T. Sun, et al., The prevalence of Listeria
monocytogenes in meat products in China: A systematic literature review and novel meta-
analysis approach, International Journal of Food Microbiology (2019), https://doi.org/
10.1016/j.ijfoodmicro.2019.108358

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© 2019 Published by Elsevier.

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The prevalence of Listeria monocytogenes in meat products in China: A systematic

literature review and novel meta-analysis approach

Yangtai Liua#, Wanxia Suna#, Tianmei Suna#, Leon G.M. Gorrisb, Xiang Wanga, Baolin Liua *,

Qingli Donga*

a
School of Medical Instrument and Food Engineering, University of Shanghai for Science and

Technology, Shanghai, China

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b
Unilever R&D, Olivier van Noortlaan 120, 3133 AT, Vlaardingen, Netherlands

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#
These authors contributed equally to this work.
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* Corresponding authors:
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Baolin Liu
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Mailing address: School of Medical Instrument and Food Engineering, University of Shanghai
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for Science and Technology, 516 Jun Gong Rd., Shanghai 200093, China.

Tel.: +86-21-5527-0702
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Email: blliuk@163.com
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Qingli Dong

Mailing address: School of Medical Instrument and Food Engineering, University of Shanghai

for Science and Technology, 516 Jun Gong Rd., Shanghai 200093, China.

Tel.: +86-21-5527-1117

Email: dongqingli@126.com

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Abstract

Meat products are commonly regarded as one of the main sources of human listeriosis caused

by Listeria monocytogenes. The objective of this study was to estimate the prevalence of L.

monocytogenes in a range of meat products from 24 different Chinese regions by using meta-

analysis of literature data and a novel sensitivity analysis approach. A total of 112 publications

from five databases, published between 1 January 2007 and 31 December 2017, were

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systematically selected for relevance and covered meat products sampled between 2000 and

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2016. Estimated by the random-effects model, the pooled prevalence of L. monocytogenes was

8.5% (95% CI: 7.1%-10.3%) in raw meats and 3.2% (95% CI: 2.7%-3.9%) in ready-to-eat (RTE)
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meats. The prevalence differed from high to low among raw meats including prefabricated raw
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meats 12.6% (95% CI: 6.9% - 21.7%), fresh pork 11.4% (95% CI: 8.6% - 14.9%), fresh beef
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9.1% (95% CI: 6.3% - 13.0%), fresh poultry 7.2% (95% CI:4.9% - 10.4%), frozen raw meats
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7.2% (95% CI: 5.7% - 9.0%), and fresh mutton 5.4% (95% CI: 2.5% - 11.0%). A higher L.

monocytogenes prevalence level was shown in the meat products from central and northeastern
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China provincial regions. The entropy-based sensitivity analysis utilized in the meta-analysis
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indicated that the sampling period and location were two critical factors influencing the

prevalence level of L. monocytogenes in meat products. A better understanding of differences

in prevalence levels per geographic region and between meat product sources may allow the

competent authorities, industry, and other relevant stakeholders to tailor their interventions to

control the occurrence of L. monocytogenes in meat products effectively.

Keywords: microbiological safety; listeriosis; entropy-based uncertainty analysis; monitoring;

food sampling

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1. Introduction

Listeria monocytogenes is ubiquitous along supply chains of many food commodities and able

to transmit via food and food contact surfaces, including processing equipment, packaging

materials, and humans (Buchanan et al., 2017; Possas et al., 2017). It is a food-borne pathogen

that causes human listeriosis, particularly in young, old, pregnant and immune-compromised

individuals (Radoshevich et al., 2017; Scallan et al., 2011). On the basis of incidence data from

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45 countries, listeriosis led to 5,463 deaths globally in 2010 (de Noordhout et al. 2014). L.

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monocytogenes is a significant contributor to disease burdens globally and a problem for public

health protection for many governments. In China, a total of 147 food-related listeriosis
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incidents have been reported during the period of 1964 to 2010 by the China National Center
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for Food Safety Risk Assessment (CFSA) (Zhou et al., 2017).
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Among the food commodities, contaminated meat products are considered as the main
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source for L. monocytogenes infections (Li et al., 2018a; USDA/ FSIS, 2003). Especially of

concern are contaminated ready-to-eat (RTE) meat products since they can be eaten without
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further decontaminating treatment (EFSA, 2018; FAO/ WHO, 2004). Several countries
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consider the identification and tracking of L. monocytogenes in meats and the establishment of

efficient surveillance systems as the foundation for effective public health protection and food

safety management. For instance, in the USA, a monitoring and verification program has been

set-up under the United States Department of Agriculture Food Safety Inspection Service that

reports on the prevalence of L. monocytogenes in RTE meat and poultry products (USDA/FSIS,

2018). An EU-wide baseline survey was conducted by the European Food Safety Authority to

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estimate the prevalence and contamination levels of L. monocytogenes in RTE foods (including

meat products) at retail between 2010 and 2011 (EFSA, 2013).

In China, the first nation-wide surveillance on L. monocytogenes in meat products was

conducted in 2000, supported by some provincial Chinese Centers for Disease Control and

Prevention (CCDC). Starting from 2010, the Chinese national monitoring network for microbial

hazards in foods was set-up to survey all major food-borne pathogens in 31 provincial regions,

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i.e. provinces, autonomous regions, and municipalities (Pei et al., 2015; Wu and Chen, 2018).

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Although official reports or open-source datasets covering the national-wide findings on L.

monocytogenes prevalence in different Chinese meat products are not available, some
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provincial CCDC branches have published partial findings in the accessible literature that has
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been used for periodic reviews. Chen et al. (2009), using data from 13 Chinese provincial
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regions from between 2000 and 2007, found that the prevalence level of Listeria species in raw
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meats and RTE meats were around 7.7% and 3.5%, respectively. According to the Chinese

literature between 2011 and 2016, Li et al. (2018b) estimated that the overall L. monocytogenes
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prevalence of meat and poultry products (including raw and RTE products) was the highest
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(8.91%) among different food commodities.

Currently, China is the world’s largest meat-producing as well as meat-consuming country

(Shimokawa, 2015; Wang et al., 2018). Also, Chinese dietary patterns have changed

significantly from plant food to animal food (Happer and Wellesley, 2019; He et al., 2016).

According to predictions by the OECD-FAO (2018), the China’s per capita meat consumption

will reach 55.01 kg in 2027, which is almost double that of the average level in developing

countries. In this context, the occurrence of L. monocytogenes in meat products in China may

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well be of significant concern to the relevant authorities. Evidently, a scientific and effective

management system should be in place and constantly improved to prevent potential risks in a

timely fashion (Shimokawa, 2015). It is thus critical to regularly review the published literature

and to obtain up-to-date insights into the prevalence of L. monocytogenes in different types of

meat products and in different geographic regions across China to guide risk-based and

effective risk management by the state and provincial authorities.

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In the past few years, meta-analysis has increasingly been applied in the area of food safety

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(den Besten and Zwietering, 2012; Gonçalves-Tenório et al., 2018; Gonzales-Barron and Butler,

2011; Gonzales-Barron et al., 2013, 2017; Xavier et al., 2014). In food safety research, meta-
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analysis may be conducted to address a broad range of research questions such as disease
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incidence, prevalence and concentrations of microorganisms in foods, effect of interventions
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pre- and post- harvest, risk ranking of pathogens and consumer practices, among others
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(Gonzales-Barron et al., 2013). Thus, meta-analysis maybe a powerful tool in the field of food

safety for the identification, appraisal and summarization of results from large quantities of
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research.
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The objective of the present study was to obtain an overview of the prevalence of L.

monocytogenes in different types of Chinese meat products based on the latest scientific data

that was systematically extracted from authoritative publication databases. Meta-analysis was

used to quantify L. monocytogenes prevalence reported for different meat categories and

provincial regions. A novel entropy-based sensitivity analysis was used to compare the

influence of different sampling factors on the prevalence level of L. monocytogenes in meat

products. The insights obtained in this study may further assist competent authorities and other

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stakeholders such as industry to design effective mitigation strategies targeting the meat types

and provincial regions in China that are at most risk for meat-borne listeriosis.

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2. Methods

2.1. Literature collection

In this study, we followed the convention of PRISMA (Preferred Reporting Items for

Systematic Reviews and Meta-Analyses, http://www.prisma-statement.org/) to search for and

collect the relevant research for meta-analysis. Two English-language databases (i.e. PubMed

and Web of Science) and three Chinese-language databases (i.e CNKI (www.cnki.net),

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Wanfang (www.wanfangdata.com.cn), and CQVIP (http://qikan.cqvip.com/)) were searched

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for relevant scientific reports published between 01/01/2007 and 30/12/2017. The following

search strategy was applied for collecting potentially relevant publications from two English-
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language databases: [(China) OR (Chinese)] AND [(meat) OR (pork) OR (beef) OR (mutton)
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OR (poultry)] AND (Listeria) AND (2007:2017). The general format of the searches for three
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Chinese-language databases was: [(meat) OR (pork) OR (beef) OR (mutton) OR (poultry)]

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AND (Listeria) AND (2007:2017); all the terms were used in Chinese. The full version of each

identified publication was obtained from the web portal of the University of Shanghai for
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Science and Technology Library.

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After removing duplicate records retrieved in the searches, all publications were checked

against a set of exclusion criteria. Publications were excluded when they were review articles

or research articles with overlapping information that could lead to double accounting of data.

Unrelated studies were not included, such as researches focusing on detection methods,

predictive modeling, hurdle technology, or non-Chinese meat products. Researches on sampling

matters without clearly specifying the meat category and/or without qualitative/quantitative

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analysis of L. monocytogenes was considered not appropriate to be included. Finally, small-

scale sampling research efforts (<100 samples) were excluded from the final data collection.

2.2. Data extraction

The following data were extracted from the final selection of records: meat category,

sampling method, sampling period (start and end year), sampling stage, sampling location (i.e.

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provincial region), sampling size, positive sample number as well as the serotype and serovar

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of L. monocytogenes. Data were extracted and compiled independently by three of the authors

(Y-T. Liu, W-X. Sun, and T-M. Sun) and formatted in MS Excel for further analysis.
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The meat products were categorized into ‘Raw meats’ and ‘RTE meats’. The ‘Raw meats’
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category was further subdivided into ‘Fresh pork’, ‘Fresh beef’, ‘Fresh mutton’, ‘Fresh poultry’,
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‘Prefabricated raw meats’, and ‘Frozen raw meats’ sub-categories, which covered the
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corresponding uncooked fresh or frozen muscle tissue and uncooked minced, flavored or

reformed meat. The collected investigations did not mention sufficient details to allow
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establishing consistent sub-categories of ‘RTE meats’. Thus, this overall category was adhered
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to in our study, which consisted of for instance prepackaged and unpackaged Chinese or

Western cooking style meat products consumed without further listericidal treatment. In

accordance with the administrative division of China, the sampling location of ‘Raw meats’ and

‘RTE meats’ was subdivided into sub-categories of different provincial regions. Before meta-

analysis, all authors cross-checked the overall data collection in full detail to delete any

incorrect double-accounted data records from the final selection of relevant publications.

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2.3. Meta-analysis and statistical analyses

Description of the heterogeneity (or variability) among primary studies is critical in meta-

analysis. Heterogeneity exists when the true effects being evaluated differ between studies. It

is detectable when the variation between the results of the studies are above what is expected

(Higgins et al. 2003). Most meta-analysis approaches reported on in literature were based on

sets of collected studies that were not exactly identical in sampling methods, experimental

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manipulations or methodologies, which may introduce variability among the true effects

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estimated by the primary studies (Gonzales-Barron et al., 2013; Xavier et al., 2014). As

Gonzales-Barron and Butler (2011) proposed, a fixed-effect model may thus not be suitable for
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application in the meta-analysis of variability of biological systems. Thus, a random- effects
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model (Eq.1, Martinez-Rios and Dalgaard, 2018) was applied in our study by using the 𝑄
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statistic,
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𝑝𝑖
∑ 𝑤𝑖 [ln( )+𝜀𝑖 ]
1−𝑝𝑖
𝜇= ∑ 𝑤𝑖
1
𝑤𝑖 = Eq. 1
𝜎𝑖2 +𝜏𝑖2
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𝑝 2
𝑖
{𝑄 = ∑ 𝑤𝑖 [ln (1−𝑝𝑖) − 𝜇 + 𝜀𝑖 ]
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where 𝑝𝑖 is the prevalence result of each specific research (𝑖 = 1,2, …); 𝜇 is the mean true

effect size; 𝑤𝑖 is the weight assigned to each primary study; 𝜀𝑖 is the sampling error; and the

DerSimonian-Laird method (DerSimonian and Laird, 1986; Gonzales-Barron and Butler, 2011;

Martinez-Rios and Dalgaard, 2018) was introduced to estimate the between-studies variance

𝜏𝑖2 (Eq. 2),

𝑄−(𝑛−1)
∑ 𝑤𝑖 2
, 𝑄 > (𝑛 − 1)
2
𝜏̂ = { ∑ 𝑤𝑖 −
∑ ̅̅̅̅
𝑤𝑖 Eq. 2
0, 𝑄 ≤ (𝑛 − 1)

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where 𝑛 is the number of primary studies. Furthermore, the inverse variance index (𝐼 2 , Eq. 3)

derived by Higgins and Thompson (2002) was recommended to illustrate the level of

heterogeneity.

𝑄−(𝑛−1)
𝐼2 = 𝑄
× 100% Eq3

The values of 𝐼 2 with percentages of 25%, 50% and 75% represent low, medium and high

heterogeneity, respectively (Martinez-Rios and Dalgaard, 2018).

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The meta-analysis was performed by using R language (Version 3.4.3, http://www.R-

project.org) with the ‘meta’ package. Forest plots of each category were prepared for the

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different meat (sub-)categories or sampling locations. Geographical maps showing the
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provincial distribution in China of L. monocytogenes prevalence levels were generated by
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Tableau Desktop (Academic version 2018.1) based on the sub-grouping analysis results.
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2.4. Entropy-based sensitivity analysis

In this study, we chose to apply a sensitivity analysis approach to explore the impact of different
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sampling factors collected from the included primary studies, i.e., sampling stage, sampling
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size, sampling location, sampling period, sampling method, and meat sub-category (note: the

latter two factors were not available for RTE meats), on the prevalence level of L.

monocytogenes in meat products. These factors were considered to potentially influence the

prevalence of L. monocytogenes on Chinese meat products. Furthermore, the choice of factors

to investigate was also pragmatically based on the actually available information in the selected

literature reports, accepting that other factors with possible influence on prevalence levels could

not be investigated as they were not reported on systematically in the collected datasets. Notably,

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the sampling factors were expressed in different types, such as characters, numbers, or dates in

the original reports. While it was uncertain whether these factors had linear associations with

the prevalence level of L. monocytogenes, which was the warrant for applying Galton’s method

(Galton, 1886). Thus, we choose to use the concept of mutual information (Speed, 2011) for

correlation and sensitivity analyses.

The chosen sensitivity analysis approach was an entropy-based sensitivity analysis

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methodology which was applied previously in other research areas than food safety (Hassani et

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al., 2019; Li et al., 2014; Sakar and Kursun, 2012). In this study, we applied this methodology

in food safety by using the meta data information collected from various literature and open
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data sources. The prevalence of L. monocytogenes and other input sampling variables, were
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considered as pieces of information of variable type, but consistently represented by entropy.
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The correlation between the prevalence level (𝑋) and different sampling factors (𝑌) could be
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compared by the concept of mutual information (Speed, 2011), or 𝐼(𝑋; 𝑌). According to Cover

and Thomas (1991), 𝐼(𝑋; 𝑌) could be calculated by Eqs.5–7. The entropy-related values were
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expressed in Shannon’s entropy in the unit of bits (Shannon and Weaver, 1949).
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𝐻(𝑋) = ∑𝑥𝜖𝑋 −𝑝(𝑥) log 2 𝑝(𝑥) Eq.5

𝐻(𝑋|𝑌) = ∑𝑦𝜖𝑌 𝑝(𝑦)𝐻(𝑋|𝑌 = 𝑦) = − ∑𝑦𝜖𝑌 𝑝(𝑦) ∑𝑥𝜖𝑋 𝑝(𝑥|𝑦) log 2 𝑝(𝑥|𝑦) Eq.6

𝐼(𝑋; 𝑌) = 𝐻(𝑋) − 𝐻(𝑋|𝑌) Eq.7

where 𝑝(𝑥) and 𝑝(𝑦) refer to the probability mass function of 𝑋 and 𝑌; 𝑝(𝑥|𝑦) is the

probability mass function of 𝑋 conditioned on 𝑌; 𝐻(𝑋) is the entropy of 𝑋; and 𝐻(𝑋|𝑌)

is the entropy of 𝑋 conditioned on 𝑌. The mutual information was a measure of the amount

of information (certainty) that one discrete random variable contains about another discrete

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random variable (Cover and Thomas, 1991). A stronger correlation between 𝑋 and 𝑌 would

cause a higher value of 𝐼(𝑋; 𝑌) in the unit of bits, which also inferred that 𝑌 provided more

impact on 𝑋 (Frey and Patil, 2002).

In order to improve the comparability, an entropy-based uncertainty coefficient or

sensitivity indicator 𝜂 could be described in Eq.8 with the range from 0 to 1 (Auder and Ioss,

2009; Press et al., 2007). If 𝑋 and 𝑌 are completely independent, then 𝜂 equals 0, which

means the uncertainty of 𝑋 is the biggest with a known 𝑌. In contrast, if 𝑋 and 𝑌 are

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completely dependent, then 𝜂 equals 1, and 𝑋 can be completely determined by a known 𝑌.

𝜂=
𝐼(𝑋;𝑌)
=1−
𝐻(𝑋│𝑌)

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𝐻(𝑋) 𝐻(𝑋)
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Note that the prevalence values of L. monocytogenes in meats were discretized into the
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low (<5%), medium (≥5% and <10%) and high level (≥10%) for simplifying the calculation.
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To explore the relationship between serotypes and contaminated meats, serogroup

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information and the pooled were gathered in Supplementary data 1-Table 1. The individual

estimated effect size within the collected studies was illustrated by the forest plot
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(Supplementary data 2 and 3), especially for the sub-category of provincial sampling location
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(Supplementary data 4, Supplementary data 5 and Supplementary data 1-Table 2). The

calculation for entropy was all listed in Supplementary data 1 from Table.3 to Table 14. The

organized data and R code were provided in Supplementary data 6, 7 and 8.

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3. Results

3.1. Characteristics of literatures and datasets

The detailed flowchart of the literature search is provided in Fig.1. A total of 1,382 publications

were initially identified from the selected five electronic databases. After removing duplicates

and manual screening based on the specified criteria, 112 public reports of independent

investigations from 24 Chinese provincial regions were finally included. While of these all

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publication dates were between 2007 and 2017, sampling periods were between 2000 and 2016.

A total of 63 and 89 sets of prevalence data were respectively categorized into either the ‘Raw

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meats’ or the ‘RTE meats’ for the meta-analysis. Among the ‘Raw meats’ category, most
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frequent were ‘Fresh poultry’ (n = 25), followed by ‘Fresh pork’ (n = 18), ‘Fresh beef’ (n = 7),
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‘Fresh mutton’ (n = 5), ‘Prefabricated raw meats’ (n = 4) and ‘Frozen raw meats’ (n = 4). The
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data involved a total of 50,153 samples (2,617 positive) at the stage of retail (22,546), catering
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(138), or both (27,469). Among them, 13,940 (1,072 positive) samples belonged to the ‘Raw

meats’ category, and 36,213 (1,545 positive) to the ‘RTE meats’ category.
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The overall prevalence levels of L. monocytogenes found before and after 2010 in the two
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meat categories are shown in Fig.2. For qualitative or quantitative analysis of L. monocytogenes,

the Chinese national standard GB 4789.30 (versions 2003, 2008 or 2010) was the major

reference (n=110). The two deviating investigations deployed the NMKL method No.136 or

ISO 11290 for raw meats testing, but the results were considered relevant and thus included in

this study.

Most of the included literature in Chinese (100 out of 101) only provided information on

the L. monocytogenes prevalence in the investigated meat products. In contrast, most of the

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English-language papers (10 out of 12) also reported on molecular features of isolated L.

monocytogenes strains by using the polymerase chain reaction (PCR), random amplified

polymorphic DNA (RAPD), pulsed-field gel electrophoresis (PFGE), or multilocus sequence

typing (MLST) methods. Serotyping of the isolated L. monocytogenes strain was undertaken in

634 cases (429 from raw meats, 205 from RTE meats) reported in 12 investigations. According

to Doumith et al. (2004), serotypes of L. monocytogenes strains may be categorized into 5

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distinct phylogenetic groups, namely, I.1 (1/2a and 3a), I.2 (1/2c and 3c), II.1 (4b, 4d and 4e),

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II.2 (1/2b, 3b and 7), and III (4a and 4c). Fig.3 illustrates that I.2 (35.4%), II.2 (34.5%), and I.1

(28.5%) were the major serogroup identified in raw meats, and nearly half of isolated strains
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belong to the serogroup of I.1 (44.9%) in RTE meats. Isolates of serogroup of III were rarely
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found in meat products.
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3.2. Pooled prevalence of L. monocytogenes in different meat products

Among the included publications, the highest prevalence reported for a raw meat product was
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up to 41.7% (in a fresh poultry product) and for an RTE meat product was 14.8%. As shown in
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Table 4, the mean pooled prevalence levels and heterogeneity of L. monocytogenes in RTE

meats were lower than those of the raw meats. Overall, the pooled prevalence of L.

monocytogenes in raw meats was 8.7%, with a heterogeneity (as indicated by the inverse

variance index) as high as 91.6%. The pooled prevalence of L. monocytogenes in RTE meats

was 3.2%, with again a high heterogeneity (86.7%). Among different raw meat subcategories,

prefabricated raw meats had the highest mean pooled prevalence (12.6%), followed by fresh

pork (11.3%), fresh beef (9.1%), fresh poultry (7.2%), frozen raw meats (7.2%), and fresh

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mutton (5.4%). Heterogeneity values were relatively low for prevalence levels reported for

frozen raw meats (0.0%) and fresh beef (72.4%).

3.3. Pooled prevalence of L. monocytogenes in different geographical regions

Reports on L. monocytogenes prevalence in meat products included only 24 out of 34 Chinese

provincial regions (provinces, municipalities and autonomous regions). For those regions, the

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ranges in L. monocytogenes prevalence level found (indicated a low (<5%), medium (≥5% and

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<10%) and high level (≥10%)) in either raw meat products or RTE meat products is illustrated

in Fig.4. The highest prevalence level was reported for products from the north-central province
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Shaanxi for both raw meats, 17.2% (95% CI: 8.4% - 31.8%), and RTE meats, 7.2% (95% CI:
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4.6% - 11.3%). Somewhat lower levels were reported for two north-east provinces, Jilin and
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Heilongjiang. In contrast, Guangdong, a southern province, had a relatively low value of L.

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monocytogenes prevalence in meat products.

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3.4. Entropy-based sensitivity analysis on the sampling factors

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The reported prevalence levels were further investigated using a new approach and basing

sensitivity analysis of the results on the concept of mutual information expressed by the

measure of entropy. As shown in Fig. 5, the estimated entropy value for the overall prevalence

levels reported for raw meat products and RTE meat products was 1.5567 bits and 1.1267 bits,

respectively. Since both values are larger than zero, it is likely that the included sampling

information influences the reported prevalence levels, in other words, that there is a dependence

of prevalence level on sampling. Also, the entropy values estimated per sampling factor

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indicated such an influence or dependence (see Supplement 1). The dependence between

different sampling factors and the prevalence level as compared by the 𝜂 value is shown in

Fig.5. Sampling period had the highest value of 𝜂 in both meat categories, followed by the

sampling location, whereas size and stage showed little dependence. The influence of method

was only relevant for raw meats, but its value was relatively low.

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Discussion

Food safety is a topic of significant concern for the Chinese government as well as of the general

public in China (Dong et al., 2015; Wu et al., 2018). The Chinese Food Safety Law implemented

on 1 June 2009 has promoted the provincial government to intensify the regulation and control

on food-borne pathogens in different foods and food-contact environments (Pei et al., 2015; Wu

and Chen, 2018). The total food compliance rate against relevant food safety standards has

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increased about 20% between 2006 to 2017, but the proportion of microbiological hazards

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underlying the cause of food safety incidents has increased during the last three years. (Wu and

Chen, 2018). Specific to the occurrence of L. monocytogenes in foods in China, a downward

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trend is apparent from the publicly available reports on the prevalence of L. monocytogenes in
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meat products after 2010 in China (Fig.2). This decrease may be a positive indication for the
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impact of the gradual upgrading of Chinese institutional infrastructures and technical

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capabilities for monitoring and controlling food‐ borne pathogens along the food supply chain

(Chen and Zhang, 2017).

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Based on pooled analysis data obtained in this study, the mean prevalence of L.
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monocytogenes reported for raw meat products was often higher than that for RTE meat

products. Notably, there is little epidemiological linkage of listeriosis to raw meat and eating

raw meat is not common in China, except for some minority groups, such as people of Bai

nationality, Dai nationality, and Hani nationality, especially on festival days (Bai et al., 2017).

Raw meats generally receive some form of treatments (i.e. heating and microwaving) that

adequately kills L. monocytogenes, so a high prevalence observed for raw meats would not be

a significant consumer risk concern in itself. Rather, somewhat speculatively, cross-

17
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contamination may pose a more significant risk. At retail and consumer stages, raw meat

products are often stored or handled at close proximity to other food commodities, including

RTE food products, which may lead to cross-contamination of L. monocytogenes onto other

foods, directly or indirectly through food contact surfaces, and potential pathogen proliferation

(Shimokawa, 2015; Possas et al., 2017; EFSA, 2018). Cross-contamination may also be

prominent in consumer homes. A cooking practice survey in households of China (Zhu et al.,

of
2017) indicated that only one-third of 251 interviewees separated the cutting board for raw

ro
chicken meat and RTE foods and among those not separated, only about 50% of them intended

to use the soap and other reagents to remove bacteria. The observations pointed out that the
-p
cross-contamination of RTE meat from raw meats could very likely occur in Chinese kitchens,
re
which may increase the risk of listeriosis. Possibly not surprisingly, prefabricated raw meats
lP

showed the highest pooled prevalence value among different raw meat sub-categories,
na

considering the rather intensive handling and treatment associated with these products.

Moreover, most Chinese prefabricated raw meat products are traditional or ethnic meat products,
ur

which typically originate from unregulated small workshops or family businesses (Zeng et al.,
Jo

2016; Zhou et al., 2017). Inadequate sanitation and unhygienic practices common to such small

food operations may increase contacts with contaminated surfaces (Paudyal et al., 2017).

Since RTE meats may be the main consumer concern, it may be relevant to compare the

results of this study to some data from developed countries. According to the annual testing

program in the USA (USDA, 2018) mentioned before, the overall prevalence of L.

monocytogenes in RTE meat products was about 0.5% (830/184,606) between 2001 and 2016.

The Base-line survey undertaken across European Union Member States for samples between

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2001 and 2016 showed that the prevalence of L. monocytogenes in certain RTE meat products

was about 2.1% (72/3,470) (EFSA, 2013). A survey of Japanese RTE meat products

investigated between 2000 and 2012 reported that the prevalence level of L. monocytogenes in

Tokyo was around 1.7% (Shimojima et al., 2016). Compared to these, the mean L.

monocytogenes prevalence level estimated for Chinese RTE meats in this study was higher

(3.2%). It is of note that China effectively has a zero-tolerance policy for L. monocytogenes in

of
RTE meats (GB 29921‐ 2013), while positive rates of pathogen presence occur in practice. The

ro
same is true, however, for the USA, while Japan and the EU have a specific tolerance for

pathogen levels but only for certain foods that do not support the growth of L. monocytogenes.
-p
Notably, in our study we considered RTE meats as one single group, despite recognizing the
re
heterogeneity of this group. However, we could not sub-divide the RTE meats in meaningful
lP

sub-categories based on the limited details provided in the investigations included in our
na

analysis. Such a sub-division would allow for a more pertinent assessment of consumer

exposure and thus of consumer risk relative to particular RTE food categories. In China, most
ur

of RTE meat products belong to one of nine classes of processed meat products (officially
Jo

categized by the processing method), which are known to have very different physicochemical

characteristics (pH, water activity, additives etc.). These intrinsic environments could strongly

impact the behavior of L. monocytogenes cells (Uyttendaele et al., 1999). Thus, for future

sampling investigations on RTE meat products, it is advisable to report relevant details of the

meat to determine the specific sub-category and better inform exposure and risk assessments.

Although not every isolated strain had complete detailed serotype information, serogroups

I.1 and II.1, which are associated with the majority of human listeriosis cases (Buchanan et al.,

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2017; Yao et al., 2018), made up a very high percentage of cases (22.4%+44.9%=67.3%) of all

serotypes isolated from RTE meats as compared to a rather low percentage

(1.4%+28.4%=29.8%) for isolates from raw meats. This confirms the general observation that

the prevalence of L. monocytogenes in RTE foods is more closely related to the occurrence of

listeriosis. Therefore, it is necessary to strengthen the supervision and epidemiological analysis

of RTE meats.

of
In terms of the geographical prevalence levels, the occurrence of L. monocytogenes is more

ro
prevalent in meat samples from north-central China, northeastern China, and eastern coasts of

China, whereas its occurrence is relatively less prevalent in the south regions (Fig.4). There is
-p
no known scientific rationale for the observed geographical differences in L. monocytogenes
re
prevalence levels. Some underlying reasons may relate to differences in retail environments
lP

(Lianou and Sofos, 2007), economic status (Wilcock et al., 2004), and market supervision (Liu,
na

2010) between those regions. Hypothetically, the psychrotolerant nature of L. monocytogenes

may provide some competitive advantage (Bayles et al., 1996). As speculated by Wu et al.
ur

(2015), the climate in north China is usually colder than that in south China, which may possibly
Jo

give L. monocytogenes more opportunities to multiply than other food-borne pathogens.

Consumer preference may contribute somewhat to the observed differences given that there is

a preference for non-chilled fresh meat (60% of market share) over chilled meat (25% of market

share) or frozen meat (15% of market share) in China (Liu et al., 2017). Finally, supply chain

factors could play a role, since the coverage ratio of the cold-chain for agricultural products in

China is still much lower (about 20%, Ren, 2017) than that in developed countries (about 90%,

Ren, 2017). Compared to developed regions with advanced retail operations, underdeveloped

20
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regions with their farmer markets rather have worse refrigeration conditions in warehouses and

display cabinets, which more likely provide an unacceptable storage condition for meat

products (Han et al., 2012).

The current status of information as well as the limited sampling/testing and public

reporting of the occurrence and prevalence of L. monocytogenes in meat products across China,

nevertheless may warrant the local authorities responsible for food safety in high prevalence

of
regions to further investigate this pathogen more closely at retail and consumer phases.

ro
Notably, microbiological contamination of food is a dynamic process and the

concentration and/or prevalence measured for a microorganism in food is a rather complex

-p
undertaking that is influenced by multiple factors, such as microorganism characteristics, food
re
properties, enumeration or detection methods, sampling conditions, general hygiene of foods
lP

and environments, etc. Different from the randomized controlled trial in clinical medicine
na

studies, a meta-analysis of microbial prevalence in a food or an environment often shows high

heterogeneity (Martinez-Rios and Dalgaard, 2018; Paudyal et al., 2017, 2018). Also, in our
ur

results such a phenomenon is obvious.

Jo

In the typical meta-analysis, sensitivity analysis was commonly used to remove source

studies of such heterogeneity, and the meta-regression is applied to build the linear correlation

between different factors and the output (Borenstein et al., 2009). However, these approaches

may be not suitable for microbial prevalence studies given the plethora of potentially

influencing factors (Paudyal et al., 2018). Instead, it is necessary to determine and compare the

possible factors that may affect the prevalence level without omitting particular investigations.

For this purpose, the EFSA implemented a generalized estimating equations (GEE) model to

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analyze the factors related to L. monocytogenes prevalence in foods, but the estimates of

influencing factors that they observed were unstable during sensitivity analysis (EFSA, 2014).

As introduced before, the entropy-based uncertainty coefficient chosen in our study could be

used for sensitivity analysis, because it is not sensitive to the types or units that data or

information is represented by nor to possible linear correlation of the input random variables

(Speed, 2011, Tang et al., 2013).

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From the sensitivity analysis, it is apparent that sampling period and location may

ro
significantly influence the prevalence level of L. monocytogenes in meat products. Thus, when

developing the sampling plan and reporting data, it is necessary to identify the information of
-p
the sampling period and location to reduce the uncertainty of the prevalence level. On the basis
re
of our results, it may also be suggested to enhance the consistency and synchronization of
lP

sampling plans for different provincial regions, such that a clearer comparison between regions
na

can be made for the same period. This is especially important given that the food supply system

of Chinese food commodities such as meat products generally consists of complex networks
ur

across different geographical regions, for which improved quantitative insight in pathogen
Jo

levels and product traceability may help in further consumer health protection.

One of the limitations in the current study was the given limited specificity and detail of

sampling information in the data that by itself were expressed in very different units. However,

applying the concept of entropy in the food safety area did make it possible for us to such

diverse types of information.

Our study expresses geographical differences in the association of L. monocytogenes with

meat products in a relative metric, namely pathogen prevalence, as this may give important

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information to industry and government on pathogen control and occurrence, respectively. To

assess the magnitude of importance of L. monocytogenes contamination in meats between

various provinces/regions, it would have been better to be able to relate such prevalence data

to either meat production or meat consumption data for these provinces/regions. However, such

data were not available from the investigations analyzed in our study. It would be advisable that,

where possible, in addition to geographical prevalence data, future investigations consider

of
generating data on geographical productions and/or consumption of the meats investigated in

ro
order to be able to compile a more informed exposure assessment and, ultimately, a risk

assessment.
-p
Although the differentiator ‘meat sub-category’ applied in this study was probably not the
re
most sensitive factor to compare L. monocytogenes prevalence levels in raw meats, it is practical
lP

to keep it as a basic classifying strategy for meat samples. This simple classification is likely
na

an informative approach when investigating the wide range of uncoordinated reports that we

analyzed in our study or when planning future investigations that need to be easy to understand
ur

and organize. However, as discussed before, different meat products may have quite different
Jo

physicochemical properties and relate to different abilities to sustain L. monocytogenes growth,

consumption patterns, production methods, etc. Alternative categorizations may be investigated

in the future based on better and/or on more narrowly defined characteristics, such as those

mentioned above, as these may provide additional insights that can be used to predict L.

monocytogenes behavior in foods and ultimately exposure and risk of consumers. While sub-

categories of meat products were established on a rather informal and pragmatic basis for the

investigation reported here, a more formal and unified classification of meat products would be

23
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beneficial in a country of the size and complexity as China.

In the future, it would be advisable to establish a sub-divide RTE meats into pertinent sub-

categories according to their physicochemical property and to then generate data on both L.

monocytogenes concentration, rather than prevalence, as well as on geographic population

consumption against the RTE sub-categories. The results of such studies may allow for much

better estimations of the differences in geographic consumer risk concerning listeriosis

of
associated to consumption of meat products, and as such better inform risk management by

ro
competent authorities and industries. Considering data generation by competent authorities,

food safety surveillance in rural areas may need to be strengthened to well assess the presence
-p
and level of L. monocytogenes in meat products across all regions in China.
re
lP
na
ur
Jo

24
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Conclusions

The food safety situation has improved over recent years and the ambition is to improve it

further in China continuously. By analyzing published reports on meat products across

mainland China, this study determined a decline in the overall prevalence of L. monocytogenes

for sampling data obtained after 2010 as compared to those before 2010. However, the pooled

prevalence level of L. monocytogenes in raw meats, especially prefabricated raw meats and

fresh pork, was still relatively high. While the pooled prevalence level for RTE meats was

of
markedly lower than that for raw meats, there is a greater potential consumer risk associated

ro
with RTE meats.
-p
A high heterogeneity and a quite poor comparability were found for mean L.
re
monocytogenes prevalence data for most meat (sub-)categories, which according to the novel
lP

entropy-based sensitivity analysis deployed, were mainly caused by dependencies of prevalence

levels on sampling period and/or sampling location. It is concluded that up-to-date and detailed
na

assessments of L. monocytogenes prevalence levels on various meat products for all provincial
ur

regions may assist Chinese government authorities, industry and other relevant stakeholders to
Jo

target their food safety management interventions on those meats and regions that mostly

contribute to the risk for listeriosis through meat consumption in China. Future assessment

efforts would greatly benefit from synchronization of the national-wide monitoring and a more

systematic classification of meat (sub-)categories.

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Acknowledgment

This work was supported by the National Key Research and Development Program of China

(Grant NO. 2018YFC1602502 & 2018YFC1602900), and National Natural Science

Foundation of China (Grant No. 31801455).

Appendix A. Supplementary data

of
Supplementary data to this article can be found online at [ ].

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Zeng, W., Wen, W., Deng, Y., Tian, Y., Sun, H., Sun, Q., 2016. Chinese ethnic meat products:
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salmonellosis linked to chicken meals prepared in households of china. Food Control 79,

279-287.

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Tables

Table 1. Meta-analysis results for mean prevalence of L. monocytogenes for specific meat sub-categories based on the included report.

Category Total Positive Pooled prevalence (95% CI) * τ2** I2***

Raw meats overall (random-effects) 13940 1545 8.7% (7.2% - 10.4%)

o f
0.5469 91.6%

Fresh pork 4446 540

r o
11.4% (8.6% - 14.9%) 0.3816 90.2%

Fresh beef 1154 109

- p
9.1% (6.3% - 13.0%) 0.1994 72.4%

Fresh mutton 833 56

r e
5.4% (2.5% - 11.0%) 0.5780 81.7%

Fresh poultry 5428 584

l P 7.2% (4.9% - 10.4%) 0.9224 94.2%

a
Prefabricated raw meats 1152 191 12.6% (6.9% - 21.7%) 0.3886 91.0%

Frozen raw meats 927

r n 65 7.2% (5.7% - 9.0%) 0.0000 0.0%

RTE**** meats overall (random-effects)

o u
36213 1072 3.2% (2.6% - 3.8%) 0.5812 86.7%

*95% CI: 95% confidence interval;

**τ2: between-study variance;

J
***I2: inverse variance index;

****RTE: Ready-To-Eat.

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Table 2. Sensitivity analysis results of Listeria monocytogenes prevalence regarding entropy for different meat categories and regarding conditional entropy

and mutual information for different sampling factors.

Prevalence level Entropy (bits) Sampling factor Conditional entropy (bits) Mutual information (bits)

Raw meats
H(X)

1.5567 Stage
Y H(X|Y)

1.5463
I(X; Y)

0.0104
o f
Method 1.4920
r o0.0647

Size 1.3787
- p 0.1779

Category 1.3644c
r e 0.1922

Location

l
0.9165
P 0.6401

Period
a0.6035 0.9532

RTE meats* 1.1267 Stage

u rn 1.0891 0.0376

o
Size 1.0609 0.0659

Location

Period
J 0.6025

0.3061
0.5242

0.8206

*RTE: Ready-To-Eat.

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Figure legends

Fig.1 The flowchart of the literature searching and collecting.

o f
o
Fig.2 Overall prevalence of L. monocytogenes in raw meats and RTE meats sampled before 2010 and after 2010 in China.

p r
e -
r
Fig.3 Serovar percentages of L. monocytogenes isolated from Chinese raw meats and RTE meats between 2007 and 2017.

P
a l
n
Fig.4 The pooled prevalence of L. monocytogenes in (A) raw meats from 15 Chinese provincial regions and (B) RTE meats from 23 Chinese provincial regions

r
u
according to literature reports published between 2007 and 2017. Note: low (<5%), medium (≥5% and <10%) and high level (≥10%).

o
J
Fig.5 Sensitivity analysis for sampling factors influencing the prevalence level of L. monocytogenes in (A) raw meats and (B) RTE meats.

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Fig.1

o f
r o
- p
r e
l P
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u r
J o

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Fig.2

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r o
- p
r e
l P
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u r
J o

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Fig.3

o f
r o
- p
r e
l P
na
u r
J o

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Fig.4

o f
r o
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r e
l P
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J o

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Fig.5

o f
r o
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r e
l P
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Highlights

 A meta-analysis of L. monocytogenes prevalence in Chinese meats was conducted.

 Categorized meat products sampled from different provincial regions were compared.

o f
 An entropy-based approach was implemented for sensitivity analysis.

r o


- p
Central and northeastern China showed a higher L. monocytogenes prevalence level.

r e
The prevalence level had the highest dependency relationship with sampling period.

P


a l
r n
o u
J

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