SARS-CoV-2 transmission via maritime cold chains: A statistical analysis of nucleic acid detection results of cold chain food imported from Fuzhou ports

doi:10.1016/j.heliyon.2023.e21954

. 2023 Nov 8;9(11):e21954.

doi: 10.1016/j.heliyon.2023.e21954. eCollection 2023 Nov.

SARS-CoV-2 transmission via maritime cold chains: A statistical analysis of nucleic acid detection results of cold chain food imported from Fuzhou ports

Yuxiang Chen¹, Shuai Zhao², Yiyuan Xu¹, Mingzhi Cai³, Guanbin Zhang^{1

4

5}

Affiliations

¹ Fujian CapitalBio Medical Laboratory, Fuzhou, 350108, China.
² Department of Breast Surgery, Fujian Provincial Maternity and Children's Hospital, Affiliated Hospital of Fujian Medical University, Fuzhou, 350001, China.
³ Zhangzhou Affiliated Hospital of Fujian Medical University, Zhangzhou, 363000, China.
⁴ National Engineering Research Center for Beijing Biochip Technology, Beijing, 102206, China.
⁵ Department of Laboratory Medicine, Fujian Medical University, Fuzhou, 350122, China.

PMID: 38034616
PMCID: PMC10685251
DOI: 10.1016/j.heliyon.2023.e21954

SARS-CoV-2 transmission via maritime cold chains: A statistical analysis of nucleic acid detection results of cold chain food imported from Fuzhou ports

Yuxiang Chen et al. Heliyon. 2023.

. 2023 Nov 8;9(11):e21954.

doi: 10.1016/j.heliyon.2023.e21954. eCollection 2023 Nov.

Authors

Yuxiang Chen¹, Shuai Zhao², Yiyuan Xu¹, Mingzhi Cai³, Guanbin Zhang^{1

4

5}

Affiliations

¹ Fujian CapitalBio Medical Laboratory, Fuzhou, 350108, China.
² Department of Breast Surgery, Fujian Provincial Maternity and Children's Hospital, Affiliated Hospital of Fujian Medical University, Fuzhou, 350001, China.
³ Zhangzhou Affiliated Hospital of Fujian Medical University, Zhangzhou, 363000, China.
⁴ National Engineering Research Center for Beijing Biochip Technology, Beijing, 102206, China.
⁵ Department of Laboratory Medicine, Fujian Medical University, Fuzhou, 350122, China.

PMID: 38034616
PMCID: PMC10685251
DOI: 10.1016/j.heliyon.2023.e21954

Abstract

Numerous epidemic outbreaks related to cold chains have occurred since the coronavirus disease 2019 (COVID-19) outbreak, suggesting the potential danger of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) transmission through cold chain foods (CCFs). By analyzing SARS-CoV-2 RNA contamination of CCFs imported from Fuzhou ports, this study evaluated the contamination and transmission of SARS-CoV-2 RNA via maritime cold chains, with the aim of provide suggestions for CCFs supervision and public health management. The statistical analysis included 131,385 samples. The majority of the CCFs imported into Fuzhou ports was aquatic raw food that originated in Southeast Asia (57.08 %), South America (19.87 %), and South Asia (11.22 %). South Asia had the highest positivity rate of 0.37 %, followed by Southeast Asia (0.21 %) and South America (0.08 %). The positivity rate showed that the outer packaging of CCFs was the most easily contaminated, accounting for 81.33 % of all positive samples. This suggested that CCFs storage and loading processes were the weak links vulnerable to SARS-CoV-2 contamination. The positivity rates in outer packaging, inner packaging, and content of raw food were 0.48 %, 0.08 %, and 0.05 %, respectively, which were obviously higher than those of processed and refined food. This indicated that increasing the mechanization of factories and implementing sensible worker management practices may decrease viral contamination. The monthly positivity rates varied widely from 0 % (March 2021) to 0.40 % (January 2021), with an average of 0.19 %. The positivity rates in outer packaging, inner packaging and content of crustaceans from Southeast Asia were 2.47 %, 0.41 %, and 0.69 %, which were approximately 5-14 times higher than those of fish and cephalopods. Meanwhile, the monthly detection number show that SARS-CoV-2 epidemic prevention strategies affected the trade of imported CCFs.

Keywords: Cold chain mediated transmission; Food safety supervision; Imported cold chain food; SARS-CoV-2; Surface contamination.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

**Fig. 1**
Sample collection methods for CCFs.

**Fig. 2**
Statistics on imported CCFs according to various classifications. (A) By country of origin. (B) By geographical region. (C) By food type. (D) By food processing degree.

**Fig. 3**
Monthly results of SARS-CoV-2 RNA detection of imported CCFs imported from various geographical regions. (A) Monthly total detection number and monthly positive detection number for each region. (B) Monthly positive rate of imported CCFs from each region.

**Fig. 4**
The heatmap based on a comprehensive analysis of origin, sample types, food processing degrees, food types, and the positivity rate.

**Fig. 5**
Monthly number of enterprises triggered circuit breakers measures and monthly detection number in (A) Southeast Asia, (B)South Asia, (C) South America. (D) The monthly number of positive confirmed cases was used to track changes in the three areas' COVID-19 epidemic condition.

See this image and copyright information in PMC

References

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[1] Han S., Liu X. Can imported cold food cause COVID-19 recurrent outbreaks? A review. Environ. Chem. Lett. 2022;20:119–129. doi: 10.1007/s10311-021-01312-w. - DOI - PMC - PubMed

[2] Han S., Liu X. Can imported cold food cause COVID-19 recurrent outbreaks? A review. Environ. Chem. Lett. 2022;20:119–129. doi: 10.1007/s10311-021-01312-w. - DOI - PMC - PubMed

[3] Liu P., Yang M., Zhao X., Guo Y., Wang L., Zhang J., Lei W., Han W., Jiang F., Liu W.J., Gao G.F., Wu G. Cold-chain transportation in the frozen food industry may have caused a recurrence of COVID-19 cases in destination: successful isolation of SARS-CoV-2 virus from the imported frozen cod package surface. Biosafety and Health. 2020;2:199–201. doi: 10.1016/j.bsheal.2020.11.003. - DOI - PMC - PubMed

[4] Liu P., Yang M., Zhao X., Guo Y., Wang L., Zhang J., Lei W., Han W., Jiang F., Liu W.J., Gao G.F., Wu G. Cold-chain transportation in the frozen food industry may have caused a recurrence of COVID-19 cases in destination: successful isolation of SARS-CoV-2 virus from the imported frozen cod package surface. Biosafety and Health. 2020;2:199–201. doi: 10.1016/j.bsheal.2020.11.003. - DOI - PMC - PubMed

[5] Ma H., Zhang J., Wang J., Qin Y., Chen C., Song Y., Wang L., Meng J., Mao L., Li F., Li N., Cai J., Zhang Y., Wang D., Xia Y., Wang H., Jiang S., Zhao X., Niu P., Tan W., Ma T., Yao Y., Mao N., Zhu Z., Ji T., Yang Q., Huang B., Zhao L., Yu J., Bai L., Zhu S., Wang D., Zhang Y., Sun Y., Luan M., Wang Y., Sun H., Yang S., Bo Z., Ren X., Li Z., Fu Gao G., Yao W., Yao W., Feng Z., Xu W. COVID-19 outbreak caused by contaminated packaging of imported cold-chain products — liaoning province, China. July 2020, China CDC Weekly. 2021;3:441–447. doi: 10.46234/ccdcw2021.114. - DOI - PMC - PubMed

[6] Ma H., Zhang J., Wang J., Qin Y., Chen C., Song Y., Wang L., Meng J., Mao L., Li F., Li N., Cai J., Zhang Y., Wang D., Xia Y., Wang H., Jiang S., Zhao X., Niu P., Tan W., Ma T., Yao Y., Mao N., Zhu Z., Ji T., Yang Q., Huang B., Zhao L., Yu J., Bai L., Zhu S., Wang D., Zhang Y., Sun Y., Luan M., Wang Y., Sun H., Yang S., Bo Z., Ren X., Li Z., Fu Gao G., Yao W., Yao W., Feng Z., Xu W. COVID-19 outbreak caused by contaminated packaging of imported cold-chain products — liaoning province, China. July 2020, China CDC Weekly. 2021;3:441–447. doi: 10.46234/ccdcw2021.114. - DOI - PMC - PubMed

[7] Pang X., Ren L., Wu S., Ma W., Yang J., Di L., Li J., Xiao Y., Kang L., Du S., Du J., Wang J., Li G., Zhai S., Chen L., Zhou W., Lai S., Gao L., Pan Y., Wang Q., Li M., Wang J., Huang Y., Wang J. COVID-19 field response group, COVID-19 laboratory testing group, cold-chain food contamination as the possible origin of COVID-19 resurgence in beijing. Natl. Sci. Rev. 2020;7:1861–1864. doi: 10.1093/nsr/nwaa264. - DOI - PMC - PubMed

[8] Pang X., Ren L., Wu S., Ma W., Yang J., Di L., Li J., Xiao Y., Kang L., Du S., Du J., Wang J., Li G., Zhai S., Chen L., Zhou W., Lai S., Gao L., Pan Y., Wang Q., Li M., Wang J., Huang Y., Wang J. COVID-19 field response group, COVID-19 laboratory testing group, cold-chain food contamination as the possible origin of COVID-19 resurgence in beijing. Natl. Sci. Rev. 2020;7:1861–1864. doi: 10.1093/nsr/nwaa264. - DOI - PMC - PubMed

[9] van Doremalen N., Bushmaker T., Morris D.H., Holbrook M.G., Gamble A., Williamson B.N., Tamin A., Harcourt J.L., Thornburg N.J., Gerber S.I., Lloyd-Smith J.O., de Wit E., Munster V.J. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. N. Engl. J. Med. 2020;382:1564–1567. doi: 10.1056/NEJMc2004973. - DOI - PMC - PubMed

[10] van Doremalen N., Bushmaker T., Morris D.H., Holbrook M.G., Gamble A., Williamson B.N., Tamin A., Harcourt J.L., Thornburg N.J., Gerber S.I., Lloyd-Smith J.O., de Wit E., Munster V.J. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. N. Engl. J. Med. 2020;382:1564–1567. doi: 10.1056/NEJMc2004973. - DOI - PMC - PubMed

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SARS-CoV-2 transmission via maritime cold chains: A statistical analysis of nucleic acid detection results of cold chain food imported from Fuzhou ports

Affiliations

SARS-CoV-2 transmission via maritime cold chains: A statistical analysis of nucleic acid detection results of cold chain food imported from Fuzhou ports

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Abstract

Conflict of interest statement

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