Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is an enveloped, positive-sense, single-stranded ribonucleic acid (RNA) virus with approximately a 30-kb genome. It is classified within the genus Betacoronavirus (subgenus Sarbecovirus) of the family Coronaviridae (1). COVID-19 is a zoonotic respiratory epidemic that has been declared by the World Health Organization (WHO) as a global public health emergency. SARS-CoV-2 is transmitted from person to person, mainly via respiratory droplets generated during normal activities such as coughing, sneezing, heavy breathing, singing, and talking (2). These droplets fall quickly on any surface, and people can become infected by breathing or by touching a contaminated surface followed by touching their eyes, nose, or mouth without washing their contaminated hands (fomite transmission) (3). Additionally, airborne transmission has been reported depending on the situational context (4). The risk of resurgence caused by other routes of virus introduction and transmission remains unclear.
Fomite transmission has aroused extensive attention with the detection of SARS-CoV-2 on imported frozen foods and their packaging materials, which was linked to re-emergent outbreaks of COVID-19 in Beijing, China (5). In particular, it has been hypothesized that contaminated cold-chain food sources may act as a virus carrier and present a risk of SARS-CoV-2 transmission between countries and regions (6). Thereafter, SARS-CoV-2 RNA contamination of the outer packaging of frozen food imported from countries or regions that suffered COVID-19 outbreaks has been much more frequently reported prior to goods clearance at customs in China. However, no direct links were established between SARS-CoV-2 infection and environment-to-human transmission until the infectious virus from the cold-chain products linked to two dock workers who were asymptomatic COVID-19 cases in Qingdao City, Shandong Province, in September 2020 was isolated by cell culture, and typical SARS-CoV-2 particles were observed under an electron microscope (7). Since then, the COVID-19 pandemic has had a dramatic impact on the global food system with direct and indirect consequences, causing widespread concern and economic hardship for consumers, businesses, and communities across the globe, although it is neither a food safety issue nor a foodborne disease. For these reasons, China has launched a nationwide program for the systematic screening of SARS-CoV-2 contamination on packaged frozen food produced, either domestic or imported, since July 2020.
This study aimed to carry out the surveillance and monitoring of SARS-CoV-2 RNA contamination on samples linked to frozen foods/food packaging at storage and retail levels in China. The findings might help formulate recommendations and strategies for both ensuring a safer food supply chain and facilitating livestock farmers, slaughterhouse workers, food processors and traders, and policymakers to combat COVID-19 effectively along the food chain.
SARS-CoV-2 contamination results in cold-chain food, packaging materials, and cold food storage environment at the storage and retail level, as well as the test results of nasopharyngeal swabs of people whose work was related to cold-chain food, between July 2020 and July 2021, are shown in Table 1.
Category No. of samples No. of positive samples
(%, packaging material)
Percentage of total positive samples (%) Food and food packaging materials 20,517,959 260 (18.6, cold-chain foods) 96.41 37 (2.6, inner packaging material) 1,101 (78.8, outer packaging material) Environment 15,656,958 52 3.59 Total 55,832,289 1,450 100 Abbreviation: SARS-CoV-2=severe acute respiratory syndrome coronavirus 2.
Table 1. SARS-CoV-2 contamination in cold-chain food-related samples collected between July 2020 and July 2021 in China.
Among more than 55.83 million swabs surveyed and monitored, more than 20.51 million were cold-chain food and packaging materials, and the rest were environmental and nasopharyngeal swabs. A total of 1,455 samples (0.26 per 10,000) were positive for SARS-CoV-2 nucleic acid. In terms of the virus-positive samples, 96.41% (1,398/1,450) and 3.59% (52/1,450) samples were swabs of food and food packaging materials, and environment, respectively. As for 1,398 SARS-CoV-2-positive samples of food and food packaging material, 99.50% (1,391/1,398) were imported, and 0.50% (7/1,398) were domestic. Regarding the SARS-CoV-2 positive food and packaging samples, 18.60% (260/1,398), 2.65% (37/1,398), and 78.75% (1,101/1,398) were food, inner packaging, and outer packaging, respectively. Additionally, 53.86% (753/1,398), 37.91% (530/1,398), and 8.23% (115/1,398) SARS-CoV-2-positive swabs were from seafood, poultry meat, and other foods, respectively (Table 2). Hence, aquatic foods were at the highest risk of SARS-CoV-2 contamination, followed by poultry meat. However, the outer packaging contamination by SARS-CoV-2 nucleic acid was much more frequent and serious than that of the inner packaging and food itself. The top-ranked PLADs with SARS-CoV-2 detection frequency higher than 2 per 10,000 were Tianjin (7.03 per 10,000), Yunnan (6.38 per 10,000), Zhejiang (3.41 per 10,000), and Fujian (2.85 per 10,000) (Table 3), which were either located on the border (Yunnan), or the most important ports of entry for foods in the regions of Bohai Rim (Tianjin), the Yangtze River Delta (Zhejiang), and the Southeast coast (Fujian) of China, respectively.
Food categories No. of positive samples Percentage of total positive samples (%) Seafood 753 53.86 Poultry meat 530 37.91 Other foods 115 8.23 Total 1,398 100 Abbreviation: SARS-CoV-2=severe acute respiratory syndrome coronavirus 2.
Table 2. Contamination of SARS-CoV-2 in different cold-chain food-related samples between July 2020 and July 2021 in China.
PLADs No. of samples No. of positive samples Positive rate (‱) Tianjin 112,314 79 7.03 Yunnan 89,288 57 6.38 Zhejiang 5,860 2 3.41 Fujian 231,933 66 2.84 Henan 385,672 73 1.89 Jilin 265,465 48 1.81 Guizhou 75,624 13 1.72 Qinghai 41,607 6 1.44 Shandong 4,441,257 630 1.42 Jiangsu 536,112 66 1.23 Guangdong 1,648,965 184 1.11 Shaanxi 784,633 64 0.81 Liaoning 81,505 6 0.73 Shanxi 383,436 15 0.39 Jiangxi 230,370 7 0.30 Anhui 1,648,214 36 0.21 Gansu 182,087 3 0.21 Hubei 2,030,209 14 0.16 Hebei 893,506 7 0.08 Sichuan 552,323 6 0.07 Heilongjiang 152,943 1 0.07 Hunan 205,012 1 0.05 Beijing 1,304,293 5 0.04 Inner Mongolia 664,049 9 0.14 Abbreviations: SARS-CoV-2=severe acute respiratory syndrome coronavirus 2; PLADs=provincial-level administrative divisions.
Table 3. SARS-CoV-2 contamination in cold-chain food-related samples detected from some PLADs of China between July 2020 and July 2021.
Regarding the 1,391 SARS-CoV-2-positive imported cold-chain foods and food packaging samples, the exporter of 99.07% (1,378/1,391) samples was confirmed. Of these, 46.66% (643/1,378) were from 11 European countries, 27.50% (379/1,378) from 6 South American countries, 16.04% (221/1,378) from 9 Asian countries, 5.81% (80/1,378) from 2 North American countries, and 3.99% (55/1,378) from 2 African countries (Table 4). These results suggested that SARS-CoV-2-contaminated cold/food chain products and their containers might be a potential source of SARS-CoV-2 infection by workers who contact with them followed by acting as a trigger of COVID-19 outbreak.
Regions No. of positive samples Percentage of total positive samples (%) Europe 643 46.66 South America 379 27.50 Asia 221 16.04 North America 80 5.81 Africa 55 3.99 Total 1,378 100 Abbreviation: SARS-CoV-2=severe acute respiratory syndrome coronavirus 2.
Table 4. SARS-CoV-2 contamination in the imported cold-chain food-related samples from some representative regions between July 2020 and July 2021 in China.