Analysis on Foodborne Pathogen Contamination of Food Samples in Longnan City from 2013 to 2022

Abstract

The objective was to determine the prevalence of foodborne pathogens in food in Longnan City, Gansu Province, China. In this research, we conducted tests on baked foods, catering foods, meat, and fruits and vegetables sold in supermarkets, farmers' markets, restaurants, retail stores, street stalls, and school canteens from 2013 to 2022. We analyzed the variety of foodborne pathogens (Salmonella, Staphylococcus aureus, Listeria monocytogenes, Bacillus cereus, and diarrheagenic Escherichia coli) in different sites and food types. Once foodborne pathogens were detected in the sample, it was deemed unqualified. The total detection rates of foodborne pathogens were 1.559%, 3.349%, 1.980%, 1.040%, 3.383%, and 1.303% in food from supermarkets, farmers' markets, restaurants, retail stores, street stalls, and school canteens, respectively. No pathogenic bacteria were detected in baked foods. Salmonella, S. aureus, L. monocytogenes, B. cereus, and diarrheagenic E. coli were detected in catering foods, among which B. cereus had the highest detection rate. Salmonella was the most common pathogenic bacteria detected in meat, while the detection rate of pathogenic bacteria in fruits and vegetables was low, with only one positive sample for diarrheagenic E. coli. Among the six sites, street stalls (3.382%) and farmers' markets (3.349%) had higher detection rates of pathogens. In general, the detection rate of pathogens from 2013 to 2022 was not high, but there were also some hidden dangers. Catering food is vulnerable to pathogen contamination, and street stalls and farmers' markets are the main sites of pollution. According to the above findings, the regulatory authorities should continue to strengthen supervision, guarantee food safety through early warning, and reduce the risk of food contamination.

Introduction

Food safety is a major public health issue worldwide, especially in densely populated countries like China (Zhang et al., 2022). The Chinese government has paid increasing attention to food safety, particularly in the wake of the 2008 melamine milk scandal and other recent food safety incidents (Sha et al., 2020). China established a comprehensive national foodborne disease surveillance platform in 2011 (Li et al., 2018), and the State Administration for Market Regulation has taken a series of risk control measures to improve food safety. In the food safety sampling assessment from 2016 to 2020, the overall qualification rate was higher than 96%, especially for meat products, edible oil/oil products, dairy products, and egg products (Wang et al., 2022). Food poisoning caused by microorganism contamination is the most food safety problems (Li et al., 2022).

The symptoms mostly include nausea, diarrhea, vomiting, and other gastrointestinal diseases, which can cause death in serious cases. While this disease is usually mild, a large number of people infect with the disease each year, causing a significant socioeconomic burden on the population and health care system (Wu et al., 2018). The World Health Organization (WHO) estimated that unsafe food caused 600 million cases of foodborne diseases and 420,000 deaths worldwide (Bass et al., 2022). According to Li et al. (2020), among the 13,307 outbreaks with known etiology, 25.3% were caused by foodborne pathogens in China from 2003 to 2017, second to poisonous mushrooms.

Li et al. (2022) conducted a survey of patients with acute gastroenteritis and diarrhea in Shenzhen, Guangdong Province, in 2010, showing that up to 70% of cases were caused by foodborne pathogens. Zhang et al. (2023) conducted pathogen monitoring on foodborne disease patients in Jinan from 2013 to 2021, and the results showed that the total detection rate of foodborne pathogens was 38.4%. Thus, foodborne pathogens are a major cause for many foodborne diseases (He and Shi, 2021).

Salmonella, Staphylococcus aureus (S. aureus), Listeria monocytogenes (L. monocytogenes), Bacillus cereus (B. cereus), and diarrheagenic Escherichia coli (Diarrheagenic E. coli) are common foodborne pathogens (Bintsis, 2017). Once people eat the food contaminated by these pathogens, they will often suffer from nausea, vomiting, diarrhea, and other gastrointestinal diseases, even life-threatening risks (Huang et al., 2021; Lima et al., 2019; Rodríguez-Melcón et al., 2019; Silva et al., 2022).

Baked foods, catering foods, meat, and fruits and vegetables are readily available in the market, but these foods that are easily contaminated with various foodborne pathogens are a major source of foodborne diseases. Baked foods, in addition to prepackaged products, are primarily sold in retail stores in the form of premade food. Because these foods are often prepared by hand, the direct exposure can lead to an increased contamination of potential foodborne pathogens (Kotzekidou, 2013). Catering foods, which are convenient and fast-serving, occupy a great market share (Arshad and Zahoor, 2018).

With a total revenue of RMB 4.7 trillion (about US$676.2 billion) in 2021, this is a key sector in China (China Hotel Association, 2022). Because of its ready-to-eat nature, consumers rarely reheat these foods before consuming them, so there are occasional outbreaks of food poisoning caused by catering foods (Wang et al., 2019). Meat is contaminated by foodborne pathogens at different stages, from preparation, processing, production, distribution, to wholesale (Rincón-Gamboa et al., 2021; Shiningeni et al., 2019). For fruits and vegetables, the contamination of foodborne pathogens can occur during the process of growing, harvesting, preparation/washing, distribution, and transportation, even in the consumer's kitchen (Machado Moreira et al., 2019).

Longnan City is an important transportation hub and logistics center in Gansu Province (Gao et al., 2022). Supermarkets, farmers' markets, restaurants, retail stores, street stalls, and school canteens are the last contact place between food and consumers. Salmonella, S. aureus, L. monocytogenes, B. cereus, and diarrheagenic E. coli are common foodborne pathogens. For these microorganisms, China has formulated corresponding detection standards, such as GB 4789.1-2010 (NHFPC, 2010). Through the detection of foodborne pathogens, the contamination situation and epidemic trend of foodborne pathogens can be summarized.

There has been no report of foodborne pathogen pollution in the food in Longnan City. Therefore, we conducted random sampling of food sold in these six sites (supermarkets, farmers' markets, restaurants, retail stores, street stalls, and school canteens) from 2013 to 2022 to assess foodborne pathogens as a public health concern in Longnan City, that is, the prevalence of Salmonella, S. aureus, L. monocytogenes, B. cereus, and diarrheagenic E. coli. The data collected can be used for microbial risk assessment and timely detection of food safety hazards, providing a basis for scientific interventions.

Materials and Methods

Sample collection

The food in various districts and counties in Longnan City, Gansu Province, was randomly sampled from 2013 to 2022. The sampling sites included supermarkets, farmers' markets, restaurants, retail stores, street stalls, and school canteens. A total of 3503 samples were collected from four categories of food (baked food, catering food, meat, and fruits and vegetables). Food samples were tested for Salmonella (n = 964), S. aureus (n = 827), L. monocytogenes (n = 873), B. cereus (n = 358), and diarrheagenic E. coli (n = 481). The collection method and transportation were strictly in accordance with Chinese food safety standard GB4789.1-2016 (NHFPC, 2016). All food samples were stored at 4°C within 24 h after being collected. The contamination caused by five kinds of foodborne pathogens was screened and monitored, and each process was repeated three times.

Microbiological testing

According to Chinese food safety standard GB29921-2013 (NHFPC, 2013), GB2726-2016 (NHFPC, 2016) and the interpretation of GB4789.30-2016 (NHFPC and CFDA, 2016a), Salmonella, S. aureus, L. monocytogenes, and B. cereus were detected in baked foods. Salmonella, S. aureus, L. monocytogenes, and B. cereus were detected in meat. Salmonella, S. aureus, L. monocytogenes, and diarrheagenic E. coli were detected in catering foods, and Salmonella, S. aureus, L. monocytogenes, B. cereus, and diarrheagenic E. coli were detected in fruits and vegetables.

The samples were enriched, isolated, and cultured, and biochemical identification, virulence gene detect ion, and pathogen preservation were conducted according to the Chinese food safety standard GB 4789-2016, for example, Salmonella: GB4789.4-2016 (NHFPC and CFDA, 2016b), S. aureus: GB4789.10-2016 (NHFPC and CFDA, 2016c), L. monocytogenes: GB4789.30-2016 (NHFPC and CFDA, 2016a), B. cereus: GB4789.14-2014 (NHFPC and CFDA, 2014), and diarrheagenic E. coli: GB4789.6-2016 (NHFPC and CFDA, 2016d). If foodborne pathogens were detected, the samples were considered positive. The detection methods for different pathogens described in GB 4789-2016 and by the International Organization for Standardization (ISO) are basically the same, except for culture time. All the quality control strains in this study were ATCC standard strains preserved in our laboratory.

Statistical analysis

GraphPad Prism 8.0 (GraphPad Software, San Diego, CA) was to generate figures in this study. SPSS 23.0 (IBM SPSS, Inc., Chicago, IL) statistical software was used for data processing and analysis. The counting data were expressed as cases or percentages (%), and the comparison of rates was conducted by χ ² test, with the test level α equal to 0.05.

Ethics statement

This study did not involve any animal experiments.

Results

Prevalence of foodborne pathogens at different times

From 2013 to 2022, a total of 3503 food samples were taken, and 75 of them were detected positive, a rate of 2.228%. As shown in Figure 1A, the detection rate from 2013 to 2022 was 2.107%, 1.102%, 1.429%, 1.361%, 0.552%, 1.961%, 5.085%, 2.970%, 2.537%, and 10.769% (p < 0.05). From 2013 to 2022, the detection rates of Salmonella were 0, 2.439%, 1.754%, 1.449%, 1.429%, 0, 2.941%, 10.000%, 0.909%, and 11.364%, respectively. Salmonella was not detected in 2013 and 2018. In addition, the detection rate was as low as 0.909% in 2021. However, the detection rate in 2022 reached 11.364%. S. aureus was only detected in food sampled from 2013 to 2016, with a detection rate of 0.816%, 2.174%, 0.870%, and 1.449%, respectively.

FIG. 1.

Detection rate of foodborne pathogens. (A) The positive detection rate (%) of different foodborne pathogens in food samples from 2013 to 2022. (B) The positive detection rate (%) of foodborne pathogens in different food samples from 2013 to 2022. (C) The positive detection rate (%) of foodborne pathogens at different sites. For total pathogen detection rates and detection rates at different sites, the comparison of rates was conducted by χ ² test, with the test level α equal to 0.05. For total pathogen detection rates, the statistical result was χ ² = 62.40, p = 0.001, the detection rate of different time had significant difference. The detection rates of different locations was χ ² = 13.246, p = 0.021, the detection rate of different time had significant difference, farmers' markets and street stalls had the highest rates of detection, while retail stores were the lowest.

For L. monocytogenes, the detection rate was only 0.980% and 2.105%, respectively, in 2013 and 2015. B. cereus was detected in 2013, 2015, 2018, 2019, and 2021, with a detection rate of 19.048%, 5.000%, 17.647%, 31.250%, and 15.385% respectively. Diarrheagenic E. coli was detected in 2013, 2016, 2021, and 2022, with a detection rate of 5.263%, 5.128%, 0.909%, and 3.571% respectively, excluding the years 2019 and 2020, when no food sample had been taken.

In this study, baked food (n = 316), catering food (n = 1985), meat (n = 982), and fruits and vegetables (n = 220) were sampled. For baked foods, Salmonella, S. aureus, L. monocytogenes, and diarrheagenic E. coli were tested. Noticeably, no positive sample was detected in baked foods (Fig. 1B). Salmonella, S. aureus, L. monocytogenes, and B. cereus were detected in catering food, and the detection rate in 2019 was the highest (7.936%), but no pathogen was detected in 2014 (Fig. 1B). Among the four foodborne pathogens, the detection rate of B. cereus was the highest (9.627%, Supplementary Table S1).

Meat tested for Salmonella, S. aureus, L. monocytogenes, and diarrheagenic E. coli. Overall, the highest detection rate was 13.265% in 2022 (Fig. 1B). Among the four foodborne pathogens, Salmonella had the highest detection rate of 6.137% (Supplementary Table S1), and raw meat, in particular, was more likely to be contaminated with Salmonella. Among the 17 Salmonella detected in meat, 14 were from raw meat and 3 were from cooked meat (Supplementary Table S2). Only in 2013, 2017, and 2021, fruits and vegetables were tested for Salmonella, L. monocytogenes, and diarrheagenic E. coli. The results showed that only the samples in 2017 were positive (Fig. 1B), and only one sample was positive for diarrheagenic E. coli (Supplementary Table S1).

Prevalence of foodborne pathogens in different sites

In this study, samples were collected from six sites, including supermarkets (n = 513), farmers' markets (n = 627), restaurants (n = 909), retail stores (674), street stalls (n = 473), and school canteens (n = 307). The detection rate of pathogens was 1.754%, 3.349%, 1.980%, 1.040%, 3.383%, and 1.303% respectively (Fig. 1C). There were significant differences in detection rates at different sites (p < 0.05). The samples from farmers' markets had the highest detection rate of Salmonella (6.395%), which mainly came from meat (Table 1). The highest detection rate of S. aureus was 2.655% in samples from the supermarket, including a catering food and two types of meat (Table 2).

Table 1.

Prevalence of Salmonella in Different Food Samples at Different Sites (Total Positive Samples/Total Samples)

Sites	Baked food	Catering food	Meat	Fruits and vegetables	Total positive samples	Total samples	% Positive
Supermarket	(0)/15	(0)/38	(2)/68	(0)/53	2	174	1.149
Farmers' market	—	(0)/52	(11)/91	(0)/29	11	172	6.395
Restaurant	—	(1)/184	(0)/35	—	1	219	0.457
Retail store	(0)/94	(1)/46	(2)/72	(0)/7	3	219	1.370
Street stall	—	(1)/101	(2)/11	(0)/5	3	117	2.564
School canteen	(0)/2	(0)/61	—	—	0	63	0
χ ² = 21.368, p = 0.01

Table 2.

Prevalence of Staphylococcus aureus in Different Food Samples at Different Sites (Total Positive Samples/Total Samples)

Site	Baked food	Catering food	Meat	Fruits and vegetables	Total positive samples	Total samples	% Positive
Supermarket	(0)/21	(1)/39	(2)/53	—	3	113	2.655
Farmers' market	—	(0)/56	(1)/73	—	1	129	0.775
Restaurant	—	(1)/184	(1)/35	—	2	219	0.913
Retail store	(0)/97	(0)/40	(0)/62	—	0	199	0
Street stall	(0)/1	(0)/92	(0)/11	—	0	104	0
School canteen	(0)/2	(0)/61	—	—	0	63	0
χ ² = 8.626, p = 0.125

However, there was no significant difference in the detection rates of L. monocytogenes in different sites (p > 0.05), and the detection rate was the highest in supermarkets, including one type of catering food and meat (Table 3). The main samples tested for B. cereus were baked food and catering food, and the detection rate of catering food in street stalls and restaurants was the highest, which were 15.00% and 9.420%, respectively (Table 4). Diarrheagenic E. coli had the highest detection rate of 5.000% in the samples from the farmers' markets, and the samples were mainly from five types of meats and one type of fruits and vegetables (Table 5).

Table 3.

Prevalence of Listeria monocytogenes in Different Food Samples at Different Sites (Total Positive Samples/Total Samples)

Site	Baked food	Catering food	Meat	Fruits and vegetables	Total positive samples	Total samples	% Positive
Supermarket	(0)/4	(1)/34	(1)/70	(0)/27	2	135	1.481
Farmers' market	(0)/2	(0)/48	(1)/105	(0)/25	1	180	0.556
Restaurant	(0)/5	(0)/180	(0)/36	—	0	221	0
Retail store	(0)/35	(1)/44	(0)/76	(0)/8	1	163	0.613
Street stall	—	(0)/101	(0)/7	(0)/3	0	111	0
School canteen	(0)/2	(0)/61	—	—	0	63	0
χ ² = 5.041, p = 0.411

Table 4.

Prevalence of Bacillus cereus in Different Food Samples at Different Sites (Total Positive Samples/Total Samples)

Site	Baked food	Catering food	Meat	Fruits and vegetables	Total positive samples	Total samples	% Positive
Supermarket	(0)/6	(0)/11	—	—	0	17	0
Farmers' market	(0)/2	(2)/24	—	—	2	26	7.692
Restaurant	(0)/5	(13)/133	—	—	13	138	9.420
Retail store	(0)/23	(1)/17	—	—	1	40	2.500
Street stall	—	(12)/80	—	—	12	80	15.000
School canteen	—	(3)/57	—	—	3	57	5.263
χ ² = 8.560, p = 0.128

Table 5.

Prevalence of Diarrheagenic Escherichia coli in Different Food Samples at Different Sites (Total Positive Samples/Total Samples)

Site	Baked food	Catering food	Meat	Fruits and vegetables	Total positive samples	Total samples	% Positive
Supermarket	—	—	(2)/47	(0)/27	2	74	2.702
Farmers' market	—	(0)/17	(5)/78	(1)/25	6	120	5.000
Restaurant	—	(2)/102	(0)/10	—	2	112	1.786
Retail store	—	(0)/12	(2)/33	(0)/8	2	53	3.773
Street stall	—	(1)/49	(0)/9	(0)/3	1	61	1.639
School canteen	—	(1)/61	—	—	1	61	1.639
χ ² = 3.204, p = 0.669

Discussion

The monitoring of important foodborne pathogens in regional food market can not only help us comprehensively understand the contamination situation of important foodborne pathogens but also facilitate the identification of key food types, key contamination sites, and related risk factors, providing a basis for food hygiene management and effective reduction of foodborne diseases (Li et al., 2020). In this study, different pathogens were detected in different food types at different sampling sites. The study showed that the total detection rate of important pathogens in food was 2.228% in Longnan City from 2013 to 2022, and the detection rate in different years was significantly different (p < 0.05).

Two thousand twenty-two saw the highest detection rate, a danger signal that cannot be ignored. Relevant authorities should strengthen the supervision of food safety. Meat is most easily contaminated, with five samples detected with Salmonella and eight samples with diarrheagenic E. coli. In addition, among the samples tested for Salmonella and diarrheagenic E. coli, meat has the highest detection rate. Meat can be contaminated by pathogens at various stages, from slaughter, processing, distribution, cooking, and so on (Dorotíková et al., 2022). In particularly, raw meat was more susceptible to contamination.

In addition, the use of antibiotics in animal breeding increases the antibiotic resistance of Salmonella that lives in the intestines of most livestock (Pulido-Landínez, 2019). Therefore, meat is likely to be contaminated with Salmonella during the slaughter process. The bacteria can survive a wide range of pH values and temperatures and become resistant to drugs, leading to serious food safety problems (Rincón-Gamboa et al., 2021; Silva et al., 2022). Salmonella has been the primary cause for food poisoning in China (Sun et al., 2020). According to Wu et al. (2021), the average contamination rate of Salmonella in food sold in mainland China from 2004 to 2018 was 5.91%, which fluctuated within 2.02–8.29%.

No pathogen was detected in baked foods. Studies have shown that contamination of baked foods can occur in raw materials, such as wheat, flour, eggs, and dairy products (Feng and Archila-Godinez, 2021). However, baked foods are cooked at high temperatures, so pathogens can be killed (Durmaz et al., 2008; Jung and Schaffner, 2022). Contamination of baked foods by pathogens can also occur during the packaging process, due to the exposure to pathogens in the environment, or unclean gloves or product packaging by the producer (Dorotíková et al., 2022; Tavelli et al., 2022). It should be noted that no pathogen was detected in baked foods, indicating that baked foods meet sanitation standards at all stages.

The detection rate of B. cereus was the highest in the catering food contaminated by pathogens. The ability of B. cereus to form spores through pili makes it difficult to remove during cleaning (Tewari and Abdullah, 2015). Improper storage temperature and long storage time of food will lead to the proliferation of B. cereus in contaminated food. Diarrheagenic E. coli, L. monocytogenes, S. aureus, and Salmonella were also detected. S. aureus is ubiquitous in nature and can produce one or more extracellular proteins called staphylococcal enterotoxin, which is believed to be an important cause of food poisoning (Bintsis, 2017; Huang et al., 2021; Samad et al., 2020). Diarrheagenic E. Coli is a kind of E. coli that can cause diarrheal diseases (Lima et al., 2019).

L. monocytogenes can grow at refrigerated temperatures and tolerate freezing temperatures, high concentration of salt, and low pH (Rodríguez-Melcón et al., 2019). Catering food includes starch products, such as flour, rice flour and rice, food rich in lipid and protein content, such as meat products and fried food, and mixed vegetable food. The diversity of food types increased the probability of cross contamination, and more types of pathogens were detected. The contamination types of pathogens detected in catering food were more than that in other foods. Only one sample from fruits and vegetables was tested positive for diarrheagenic E. coli. Salmonella and L. monocytogenes were not detected, which may be due to the low probability of cross contamination of fruits and vegetables in sampling locations of supermarkets, farmers' markets, retail stores, and street stalls.

In this study, six sampling sites were selected to analyze the prevalence of pathogens. Specifically, the detection rate of pathogens was the highest in farmers' markets and street stalls, followed by restaurants, supermarkets, school canteens, and retail stores. Farmers' markets have a wide range of food, high turnover, and relatively poor sanitation. Street stalls are usually located in crowded public areas, such as open-air markets, leisure parks, and busy footpaths (Asiegbu et al., 2016; Compaore et al., 2022), resulting in the lack of basic infrastructure and services. As a result, the food from street stalls is at a high risk of pathogen contamination (Manguiat and Fang, 2013). The types of food sold in restaurants and retail stores are relatively simple, but they cannot prevent the contamination of pathogenic bacteria in the process of processing and selling. Similar to farmers' markets and street stalls, supermarkets have a wide variety of food.

The difference is that their good sanitary conditions and hygiene-conscious workers can effectively reduce cross contamination of pathogens. In addition, cold chain facilities provided in supermarkets can be used to store perishable food, and can effectively inhibit the growth of pathogens in contaminated food (Wang et al., 2019), so as to ensure food safety. As for food samples from supermarkets, pathogens were mainly detected in meat. Therefore, supermarkets still need to avoid man-made pollution and provide disinfection facilities. School canteens mainly serve food for students who mostly eat in the public area, and they have a huge impact on teenagers' dietary intake and nutritional status (Delaney et al., 2019). Although the detection rate of pathogens was very low (1.302%), the supervision of food safety should not be ignored.

The important foodborne pathogens in food were detected in Longnan City, Gansu Province, with the detection rate of 11.52% in Tai’ an City, Shandong Province, and 4.64% in Qingpu District, Shanghai, during 2018–2021. The overall detection rate of foodborne pathogens was not high, but there are still hidden dangers that cannot be ignored. Catering food is prone to pathogen contamination (especially B. cereus), and the detection rate of foodborne pathogens was high in street stalls and farmers' markets.

Most samples could be contaminated during preparation due to improper refrigeration, cooking, and heating, or poor personal hygiene (Thwala et al., 2021). Therefore, we suggest that the supervision department should strengthen food safety and health management in the production and transportation of food. In particular, the supervision of catering food, coupled with early warming, can improve the food safety awareness in street stalls and farmers' markets, thus reducing the risk of food contamination. In addition, it is suggested that consumers should avoid eating raw food when eating out, and choose clean and suitable restaurants to prevent foodborne diseases.

Footnotes

Authors' Contributions

Y.C.: Investigation, formal analysis, and methodology. L.-X.L.: Investigation and formal analysis. X.L.: Investigation and software. W.Y.: Project administration and validation. X.M.: Methodology and software. Z.-W.L.: Validation, formal analysis, and supervision. W.M.: Supervision, conceptualization, and writing review. L.-L.M.: Writing original draft, visualization, and supervision. Y.-G.L.: Conceptualization, resources, supervision, and writing review.

Disclosure Statement

No competing financial interests exist.

Funding Information

This work was supported by the Central Funds for Guiding the Local Scientific and Technological Development (YDZX2023036), the Key Research and Development Program in Shandong Province (2019YYSP026), and the Innovation team of the introduction and education plan for young and innovative talents in Shandong Provincial University (2021QCYY007).

Supplementary Material

Supplementary Table S1

Supplementary Table S2

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