Prevalence and Serotypes of Listeria monocytogenes Contamination in Chinese Beef Processing Plants

Abstract

The aim of this work was to study the epidemiology of Listeria spp., particularly Listeria monocytogenes, and to identify the serotypes present in contaminated samples from beef processing plants in China. A total of 439 samples were obtained from bovine feces, hides, and carcasses at three commercial processing plants. A standard protocol (ISO 11290-1) was followed to detect Listeria spp. and L. monocytogenes, and multiplex polymerase chain reaction was used to identify the various L. monocytogenes serotypes. The overall prevalences of Listeria spp. and L. monocytogenes were 65.6% and 26.4%, respectively, and the contamination was highest in the hide samples. The identified L. monocytogenes serotypes were 1/2c and 1/2a. The results of the current study indicate that Listeria spp. contamination is common in Chinese beef processing plants; specific measures should be taken to prevent and/or treat L. monocytogenes contamination of feces and hides in beef slaughter plants. Furthermore, because Listeria spp. contamination was found to be prevalent, it should, therefore, be studied further. The prevention of cases of sporadic listeriosis in China should also be addressed.

Introduction

L isteria monocytogenes is a foodborne pathogen (Schlech et al., 1983) that can cause serious life-threatening diseases, such as listeriosis (Ryser and Marth, 2007). The invasive forms of L. monocytogenes may cause septicemia, encephalitis, and meningitis, and listeriosis has been considered an important foodborne disease due to its potential effect on pregnant women, newborns, elderly individuals, and immunosuppressed individuals (Barros et al., 2007), with mortality rates approaching 30% (Chen et al., 2009). Feng et al. (2010) conducted a retrospective analysis of the reported cases of human nonperinatal listeriosis between 1964 and 2009, and concluded that the clinical features and the average case mortality of the nonperinatal cases of listeriosis in China were in accordance with the internationally published data.

L. monocytogenes is often present in meat production environments, including beef production plants (Gray et al., 2004). Previous studies have shown that cattle are a reservoir for L. monocytogenes (Madden et al., 2007), and this bacterium has been isolated from the feces and beef hides at slaughter plants (Guerini et al., 2007). The prevalence of L. monocytogenes ranged from 0.8% to 18.7% on beef carcass hides and from 0.0% to 1.1% on post-intervention (after the full complement of antimicrobial intervention) carcasses from two large beef processing plants in the United States (Rivera-Betancourt et al., 2004). A major survey of 2,089 steer and heifer carcasses in the United States showed that 4.1% were positive for L. monocytogenes (McNamara, 1995). A UK survey of cattle carcasses (n=29) found that 15.4% of the carcasses were positive for L. monocytogenes (Fenlon et al., 1996). In Australia, Vanderlinde et al. (1998) found contrasting results for the presence of Listeria spp. in domestic and export meat plants: 15% of the carcasses in the domestic plants were positive (n=20), but only 0.77% of the carcasses in the export plants were positive (n=130). A previous study in China reported that L. monocytogenes was present in retail raw meat, fish, vegetables, and ready-to-eat foods (Zhou and Jiao, 2006; Zhang et al., 2007; Shao et al., 2009); however, there is no information regarding the L. monocytogenes contamination of cattle at the time of slaughter, that is, from the time of arrival of the cattle to the processing plant to the production of final beef carcasses.

Pre-slaughter and processing interventions that prevent pathogenic bacterial contamination may improve the health of the cattle, may reduce the presence and/or concentrations of the bacteria in the feces and hides of the cattle, and may consequently reduce the prevalence of beef contamination (Dodd et al., 2011). Previous studies have indicated that contamination of meat products with L. monocytogenes can occur in the processing environment (Gandhi and Chikindas, 2007). Thus, environmental contamination may be a source of Listeria spp. contamination in beef plants (Autio et al., 2000). However, good hygienic practice during skinning and evisceration may significantly reduce the prevalence of L. monocytogenes contamination of carcasses (Madden et al., 2001).

The objectives of this study were to identify the factors associated with the prevalence of Listeria spp. and L. monocytogenes at different times during processing and to determine the primary serotypes of L. monocytogenes present at commercial beef processing plants in China.

Methods

Experimental design and sample isolation

Three beef processing plants (designated as plants A, B, and C) participated in the study over a period of 7 months (from October 2009 to April 2010). The three plants were located in different cities that were geographically distributed in the northeast, northwest, and southwest of a Chinese province. Fecal, hide, and carcass swabs and beef meat samples were collected at various times during processing, for a total of 439 samples. The commercial plants involved in the study were equipped with a product line that can slaughter 30–50 animals per hour. Following dressing, the carcasses were washed with cold water before chilling.

Sample collection

Feces

The fecal samples were collected after de-legging. A sterile plastic bag was inverted over the sampler's hand to prevent contamination of the exposed inner surface of the bag. The bag was inserted inside the rectum to remove the fecal material. Approximately 100 g of fecal content was extracted, and the bag was placed on ice and transported to the laboratory. Each sample was collected with a new plastic bag, and the samples were analyzed within 12 h.

Beef meat

One hundred grams of meat sample was obtained from beef cuts and placed in an ice storage box. All of the beef meat samples were transported to the laboratory, and 10 g of each sample was used for further analysis.

Hide, carcass, and environmental samples

The samples were collected according to a previously described method (Lasta et al., 1992). Briefly, swab samples were collected from the hides, pre-evisceration carcasses, post-evisceration carcasses, post-final washed carcasses (before chilling), and chilled carcasses from the hindquarter to the forequarter. Environmental samples were taken by swabbing the conveyor belt, working table, box, hook, chilling room floor, and cutting room floor. The swabs were pre-wetted with 10 mL of buffered peptone water. The samples were placed in a sterile stomacher bag on ice and were transported to the laboratory for further analysis.

Listeria spp. and L. monocytogenes detection

A standard protocol, which was modified from previously described methods, was followed to detect Listeria spp. and L. monocytogenes (ISO, 1996; Guerini et al., 2007). Briefly, the fecal, meat (10 g), and swab samples were pre-enriched in 90 mL of half Fraser broth and incubated at 30°C for 24 h. An aliquot (0.1 mL) was removed and subjected to secondary enrichment in 10 mL of full Fraser broth at 35°C for 24–48 h. The samples were then plated onto Listeria CHROMagar (CHROMagar Co., Ltd., Paris, France), and the plates were incubated at 37°C for 24 h. Colonies with a blue phenotype indicated the presence of L. innocua, L. seeligeri, L. welshimeri, or L. grayi, whereas blue colonies with halos indicated the presence of L. ivanovii or L. monocytogenes. The blue colonies with halos were purified, and the L. monocytogenes samples were identified using a Gram stain, a catalase test, hemolysis (trypticase soy agar with 5% ovine blood), carbohydrate fermentation (mannitol, rhamnose, xylose and dextrose), and motility at 25°C in SIM medium.

Serotyping of isolates

The L. monocytogenes isolates were serotyped at the laboratory using a multiplex polymerase chain reaction (PCR) method, according to Doumith et al. (2004, 2005). The primers for the lmo0737, lmo1118, ORF2819, ORF2110, and prs genes, previously published by Doumith et al. (2004), were commercially synthesized.

Statistical analysis

All of the results were statistically analyzed with SAS 9.1 (SAS Institute, Cary, NC) software. A value of p<0.05 was considered significant. The chi-squared test or Fisher's exact test was used to determine significant differences between proportions.

Results

Overall, 65.6% (288/439) of the samples were positive for Listeria spp. (Table 1). Bacteria were isolated from almost all of the samples from plant B (99.3%, 140/141), and there was a significantly higher percentage of positive samples from plant B (p<0.05) than from plant A (60.3%, 94/156) and plant C (38.0%, 54/142). Listeria spp. were also more prevalent in the hide samples from both plant A (83.3%, 35/42) and plant C (70%, 14/20) than in the other sample types (Table 1).

Table 1.

Frequency of Listeria spp. in Fecal, Hide, Carcass, Meat, and Environmental Samples from Three Beef Processing Plants in China

Sample points	Plant A (%)	Plant B (%)	Plant C (%)
Feces	17/26 (65.4)	15/16 (93.8)	4/20 (20.0)
Hides	35/42 (83.3)	21/21 (100.0)	14/20 (70.0)
Pre-evisceration carcasses	3/10 (30.0)	20/20 (100.0)	6/17 (35.3)
Post-evisceration carcasses	2/10 (20.0)	17/17 (100.0)	0/16 (0.0)
Post-washing carcasses	10/16 (62.5)	22/22 (100.0)	9/20 (45.0)
Chilled carcasses	10/22 (45. 5)	20/20 (100.0)	6/25 (24.0)
Meat	17/30 (56.7)	19/19 (100.0)	15/24 (62.5)
Environmental samples	—	6/6 (100.0)	—
Total	94/156 (60.3)	140/141 (99.3)	54/142 (38.0)

Overall, 26.4% (116 of 439) of the samples were positive for L. monocytogenes (Table 2). The percentage of samples that were positive for L. monocytogenes was the highest in plant B (Fig. 1), and 78.0% (110/141) of the positive samples from plant B were contaminated with L. monocytogenes. In contrast, L. monocytogenes was only detected in the fecal samples (7.7%, 2/26) from plant A and in the post-washed carcasses (5%, 1/20), chilled carcasses (8%, 2/25), and meat (4.2%, 1/24) from plant C (Table 2). All environmental samples from plant B were positive for L. monocytogenes (Table 2).

FIG. 1.

The overall prevalence of Listeria spp. and L. monocytogenes in fecal, hide, carcass, meat, and environmental samples from three beef processing plants in China. ^a,b,cThe percentages of Listeria spp.–positive samples in the different plants are all significantly different from each other, p<0.05. ^x,yThe percentage of Listeria monocytogenes–positive samples from plant B is significantly higher than the percentages for plants A and C, p<0.05.

Table 2.

Frequency of Listeria monocytogenes in Fecal, Hide, Carcass, Meat, and Environmental Samples from Three Beef Processing Plants in China

Sample points	Plant A (%)	Plant B (%)	Plant C (%)
Feces	2/26 (7.7)	4/16 (25.0)	0/20 (0.0)
Hides	0/42 (0.0)	16/21 (76.2)	0/20 (0.0)
Pre-evisceration carcasses	0/10 (0.0)	16/20 (80.0)	0/17 (0.0)
Post-evisceration carcasses	0/10 (0.0)	12/17 (70.6)	0/16 (0.0)
Post-washed carcasses	0/16 (0.0)	18/22 (81.8)	1/20 (5.0)
Chilled carcasses	0/22 (0.0)	19/20 (95.0)	2/25 (8.0)
Meat	0/30 (0.0)	19/19 (100.0)	1/24 (4.2)
Environmental samples	—	6/6 (100.0)	—
Total	2/156 (1.3)	110/141 (78.0)	4/142 (2.8)

Of the L. monocytogenes isolates that were serotyped, 112 of the isolates from plants A and B are serotype 1/2c, and four of the isolates from plant C are serotype 1/2a (Table 3).

Table 3.

Listeria monocytogenes Serotypes Isolated from Three Beef Processing Plants in China

Source	Number of serotyped isolates	Serotypes
Plant A	2	1/2c
Plant B	110	1/2c
Plant C	4	1/2a

Discussion

To our knowledge, this is the first study describing the prevalence of Listeria spp. in Chinese beef processing plants. In these plants, cattle are purchased from small-scale farms and are centrally processed. Our results indicate that Listeria spp. is present in several types of samples from several different plants.

The prevalence of Listeria spp. may be influenced by several factors, including management practices (feeding and transportation) and geography (Fenlon et al., 1996; Mohammed et al., 2010; Rivera-Betancourt et al., 2004). Our data showed that the prevalence of Listeria spp. and L. monocytogenes was higher in plant B than in plants A and C (Fig. 1). Plant B had a high percentage of fecal samples that were positive for Listeria spp. and a higher percentage that were positive for L. monocytogenes relative to the other plants (Table 2). This finding suggests that the cross-contamination of carcasses may be serious and that animal feces may be an important source of L. monocytogenes contamination in plant B. The detection of L. monocytogenes in all of the environmental samples from plant B indicated that the cattle might enter this plant with intestinal L. monocytogenes and spread them to the environment during slaughter and processing.

Cattle hide has also been identified as a source of general microbial contamination of carcasses (McEvoy et al., 2000). The relatively high prevalence of Listeria spp. on the hide indicates that the hide may be a main source of the organism in all three of the plants that we studied. The transfer of microorganisms from contaminated hides to carcasses during de-hiding poses an enormous threat during cattle slaughtering (Antic et al., 2010). Guerini et al. (2007) found that an average of 75.9% (61–92%) and 20.3% (8.4–47.9%) of hide samples were positive for Listeria spp. and L. monocytogenes, respectively, in U.S. beef factories, which is similar to our findings in the present study. In contrast, Rivera-Betancourt et al. (2004) reported much lower prevalence of Listeria spp. (56.8%) and L. monocytogenes (9.9%) in two other U.S. beef processing plants. Our findings that Listeria spp. was more prevalent in the hide samples than in the feces (Table 1) suggest that the hides are a more significant source of carcass contamination.

The overall prevalence of Listeria spp. and L. monocytogenes in the fecal samples in our study is similar to the data from a Scandinavian study (Husu, 1990). Compared with the data of the present research, higher prevalence has been observed in Denmark (Skovgaard and Morgen, 1988), the United States (Nightingale et al., 2004), Canada (Fedio and Jackson, 1992), and Yugoslavia (Bunčić, 1991). However, relative to the results of our study, lower frequencies have been reported in Japan (Iida et al., 1991), Germany (Anonymous, 2006), Sweden (Unnerstad et al., 2000), and Northern Ireland (Madden et al., 2007). Moreover, Bailey et al. (2003) did not detect L. monocytogenes in the fecal samples from Australian slaughter-age cattle. Several factors may contribute to this variation in prevalence, including management practices, animal age, transportation stress, differences in the number of samples collected, and differences in the isolation method. For example, L. monocytogenes fecal contamination has been associated with such practices as silage feeding (Mohammed et al., 2010). These results indicate that animal feces may be an important source of L. monocytogenes contamination.

The frequency of contamination of beef carcases with Listeria spp. and L. monocytogenes beef carcass varies widely among different countries. In the United States, Guerini et al. (2007) reported that 4.8% and 2.8% of the samples were positive for L. monocytogenes in pre-evisceration and post-intervention carcasses, respectively. In Iran, 3.0% of the cattle carcasses were positive for L. monocytogenes (Rahimi et al., 2008), whereas in Northern Ireland, L. monocytogenes could not be isolated from chilled beef carcasses (Madden et al., 2001). The overall prevalence of Listeria spp. and L. monocytogenes in beef carcasses and meat samples in this study is higher than the prevalence found in these previous studies (Table 2); we speculate that differences in the sampling methods and techniques, together with the hygiene management and pathogen control strategies in the various facilities, may also contribute to these differences. In the present study, no antimicrobial strategy was employed by the plants during carcass processing, which may be one reason for the high prevalence of isolatable Listeria spp.

L. monocytogenes isolates can be classified into at least 13 serotypes, and several of these serotypes have been associated with sporadic (1/2a, 1/2b, 1/2c, and 4b) and epidemic (4b) listeriosis in humans (Gianfranceschi et al., 2003). Serotypes 1/2c and 1/2a were detected in the current study (Table 3), and the present results are inconsistent with the previous findings of Guerini et al. (2007) and Barros et al. (2007), which identified L. monocytogenes serotypes 1/2a and 4b in beef processing plants. In fact, the majority of outbreaks and sporadic cases of listeriosis are associated with serotype 4b, which is less frequently isolated from contaminated foods (Gianfranceschi et al., 2003). However, our data indicate that L. monocytogenes is present in Chinese beef plants, thus highlighting the importance of preventing food contamination.

Overall, Listeria spp. and L. monocytogenes are common contaminants of bovine feces and hides in Chinese slaughterhouses. Thus, there is a risk of contracting sporadic foodborne listeriosis from Chinese beef, and this risk should be addressed. The poor hygiene found in the abattoirs may increase the prevalence of contamination. The prevention/treatment of L. monocytogenes contamination in beef plants should therefore be addressed.

Footnotes

Acknowledgments

This research was supported by an earmarked fund for the Modern Agro-Industry Technology Research System of China, by the Non-Profit Project of Quality Control for Meat Production and Processing (200903012) and by the National 863 Projects of “Key Technologies to Reduce and Control Biohazard from Low Temperature Cold Fresh Animal Derived Food” (2012AA10160503) in the 12th 5-Year Plan.

Disclosure Statement

None of the authors of this article has a financial or personal relationship with other people or organizations that could inappropriately influence or bias the content of the article.

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