Internet-Sold Snail Pomacea canaliculata and Achatina fulica Might Transmit Angiostrongylus cantonensis in Mainland China

Yu Liang Cao1, Yue Guo2,3*, Hui Zhang2 and Chun Sheng Wang2

1Emergency Department, South Taihu Hospital and Affiliated Hospital of Huzhou College, 1566 Gangnan Road, Huzhou, Zhejiang, China

2School of Medicine, Huzhou University, 759 Erhuan Rd, Huzhou, China

3Key Laboratory of Vector Biology and Pathogen Control of Zhejiang Province, Huzhou University, Huzhou, China

Yuliang Cao and Yue Guo contributed equally to this paper.

ABSTRACT

In China, snails Pomacea canaliculata and its new breed the gold snail, Achatina fulica and its new breeds the white jade snail, have been sold on the Internet in recent years. We concluded that 24,853 sales of P. canaliculata and A. fulica had been made through the Internet selling platform before 2019. Further surveys indicated that 51% sellers were located in endemic areas of Angiostrongylus cantonensis. However, no A. cantonensis-positive snails were found among Internet-sold snails. Laboratory animal infection experiments proved that all 4 breeds of snails could transmit A. cantonensis. Internet sales of the 4 snails are of bio-safty temporarily but still present a high risk to spread angiostrongyliasis in China; moreover. Internet sales of P. canaliculata and A. fulica should be brought to the attention of concerned administrations in China.

Article Information

Received 29 March 2022

Revised 10 April 2022

Accepted 17 April 2022

Available online 09 August 2022

(early access)

Published 21 July 2023

Authors’ Contribution

YLC provided the idea and collected the data.YG designed the study. HZ contributed in manuscript writing.CSW analyzed the data.

Key words

Pomacea canaliculata, Gold snail, Achatina fulica, White jade snail, Angiostrongylus cantonensis

DOI: https://dx.doi.org/10.17582/journal.pjz/20220329070315

* Corresponding author: guoyue66@126.com

0030-9923/2023/0004-1993 $ 9.00/0

Copyright 2023 by the authors. Licensee Zoological Society of Pakistan.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Angiostrongyliasis is an important worldwide parasitic disease caused by the nematode Angiostrongylus cantonensis. In humans, A. angiostrongylus is the most common cause of meningoencephalitis or eosinophilic meningitis (Lv et al., 2008; Wang et al., 2008). The global geographic distribution of A. cantonensis includes China, South Asia, the Americas, etc. The life cycle of A. cantonensis is typically complex. To complete its life cycle, the parasite needs two hosts, rat as the terminal host and snail as the middle host. In China, the two main snail vectors are Pomacea canaliculata (Karraker et al., 2014; Yang et al., 2013) and Achatina fulica (Lv et al., 2009; Song et al., 2016).

The freshwater snail P. canaliculata is also known as the golden apple snail or the channeled apple snail. This snail is among the top 100 of the “World’s Worst Invasive Alien Species” and it invaded China in the 1980s (Yang et al., 2010). In nature, apple snails exhibit a diversity of shell colors, from gold to black (Estebenet et al., 2006; Yusa, 2004). In China, gold-shelled P. canaliculata has been called the gold snail for its shell color.

The land snail A. fulica, also known as the African snail and the giant African snail, is the most prevalent invasive snail too (Lv et al., 2009). At present, the giant African snail is widely distributed in southern China. In some places, the albino breed of A. fulica (white jade snail) has been cultured as a food source, forming the snail-farming industry (Qin et al., 2007).

In recent years, online shopping and purchasing have become a popular, quick and fashionable way of consumption in China. Live snails can be sold and bought online, including P. canaliculata and A. fulica, as well as gold snails and white jade snails.

In this study, internet selling of P. canaliculata, the gold snail, A. fulica and the white jade snail is being reported for the first time, and their infection status has been examined. In addition, A. cantonensis transmission mediated by P. canaliculata and A. fulica has been determined by animal infection experiments.

Materials and methods

Relevant information of online sales was collected from the Taobao sales platform, the earliest and largest Internet shopping platform in China (website: https://www.taobao.com/) using the keywords of snail, apple snail, white jade snail and gold snail. The natural endemic area of A. cantonensis, especially the geographical distribution of P. canaliculata and A. fulica, was obtained from published articles (Wang et al., 2008; Lv et al., 2009; Song et al., 2016).

Forty wild type P. canaliculata, gold snails, wild type A. fulica and white jade snails were bought from the Internet. Their infection status was detected both directly under a microscope and indirectly by enzyme digestion. Ten-gram snail meat was grinded and digested at 37 °C, 1.5 h. Then the digest was filtered by 260 mesh filter and the sediment on the filter was taken for microscopic examination. The digest composition was 1000 ml distilled water, 7 ml hydrochloric acid, pepsin 5 g (He et al., 1983).

Microscopic detection was conducted after the snail was cracked and the lung sac of the snail was cut from the body. Worm nodules found in the lung sac were used for morphological examination of worms inside the nodules to determine A. cantonensis infection status. Enzyme lysis of snails was undertaken as previously described.

To determine the 4 breeds of snails’ ability to transmit A. cantonensis, artificial animal infection examinations were conducted. In short, 4 groups of snails were formed, and each group had 20 snails that were 20 g in weight. Each snail was infected with 1000 larvae of A. cantonensis individual, and larvae that developed in the snail were collected 10 dpi (days post infection). Collected larvae were used to infect Sprague-Dawley rats (SD rats), with 200 larvae for each rat. Rat stool examination was conducted under a microscope 40 dpi to determine the infection status of A. cantonensis.

Results and discussion

According to the data obtained from the internet selling platform, a total number of 24,853 snail sales had been made by 2019. Most of the sales, that is, 19,662, were of the apple snail (Table I). The remaining 5191 sales were of the giant African snail. Some sellers did not provide information in detail, and the snails they sold were divided into unspecified groups. Besides, 51% of all selling (12,668) took place in endemic regions.

The geographical information of 2 species and 4 breeds are shown in Figure 2.

Neither worm nodules in the lung sac nor larvae 3 stage of A. cantonensis were found by snail dissection or enzymolysis. No A. cantonensis was detected among none of 4 snail group, indicating that all 4 breeds of snail bought on the Internet were A. cantonensis negative.

Table I. Snails sold on the internet in China.

Animal experiments proved that all 4 snail breeds could be infected by the 1st satge larvae of A. cantonensis, and the 3rd stage larvae obtained from the snail host could infect SD rats without a difference in ability, suggesting that all 4 snail breeds could be transmitters of A. cantonensis.

In China, angiostrongyliasis has become an important parasitic disease in many southern provinces, including Yunnan, Hainan, Guangxi, Guangdong, Fujian, Zhejiang, Jiangsu and Hunan (Lv et al., 2008; Wang et al., 2012). Historical angiostrongyliasis outbreaks have occurred in Zhejiang, Fujian, Yunnan, Heilongjiang, Liaoning, and Beijing many times. At present, two species of invasive snails, P. canaliculata and A. fulica, are becoming the most important transmitters of A. cantonensis in China. In most provinces, wild type P. canaliculata is strictly monitored to avoid human infection and spread of the disease by the local CDC (Center for Disease Control and Prevention). However, Internet sales of snails lack monitoring.

Recent analysis has shown that the natural distribution of P. canaliculata includes Sichuan, Yunnan, Guangxi, Guangdong, Fujian, Zhejiang, Jiangxi, Hunan, and Hainan. A. fulica is mainly distributed in Yunnan, Guangxi, Guangdong, and Fujian.

Although all 4 breeds of snail bought on the Internet were A. cantonensis negative, animal experiments showed that all 4 breeds could transmit A. cantonensis. We believe that the 4 breeds of internet-sold A. fulica and P. canaliculata present a risk of transmission of A. cantonensis for the following reasons: (1) the sources of internet-sold snails lack supervision; some internet-sold snails might be collected from the wild in endemic regions, and some snails might even be A. cantonensis positive. Internet selling might cause new infections. Taking P. canaliculata as an example, the A. cantonensis endemic region, natural habitat, and internet sellers are commonly distributed in Guangdong, Fujian and Zhejiang. There is no report indicating that A. fulica has invaded Zhejiang, but many snail farms have been established in the cities of Jinhua and Jiaxing, Zhejiang. This will be discussed in another paper. Local snail internet sellers might collect wild snails for sale with a high risk of transmitting A. cantonensis. (2) Although most of the snails were bought as pets and aquarium cleaners, some snails might escape or be dumped into the wild, leading to new spreading of these invasive snails. Internet selling might carry the risk of new introductions of snails, even damaging ecological systems and leading to new endemic regions of angiostrongyliasis.

Conclusion

Overall, this is the first report on the internet-sold A. cantonensis intermediate hosts, namely wild type of P. canaliculata, A. fulica, the gold snail and the white jade snail. Raw data indicated that 24,853 sales had been made by 2019. Besides, current surveys found no A. cantonensis-positive snails among internet-sold snails, suggesting that all internet-sold snails were biosafe temporarily. However, laboratory animal infection experiments exhibited that all 4 breeds of snails could transmit A. cantonensis. It is our strong recommendation that internet sales of all 4 snail breeds be strictly monitored.

Acknowledgements

This research was supported by Open project of Key Laboratory of Vector Biology and Pathogen Control of Zhejiang Province (HUZUL202101).

Statement of conflict of interest

The authors have declared no conflict of interest.

References

Estebenet, A.L., Martín P.R., and Burela S., 2006. Biocell, 30: 329-335.

He, J.Z., Ding, B.L., and Luo, Y.Z., 1983. Acad. J. Guangzhou. Med. Coll., 2: 1-11. (in Chinese).

Karraker, N.E. and Dudgeon, D., 2014. Invasions, 16: 1785-1789. https://doi.org/10.1007/s10530-014-0640-2

Lv, S., Zhang, Y., Liu, H.X., Hu, L., Yang, K., Steinmann, P., Chen, Z., Wang, L.Y., Utzinge, R.J., Zhou, X.N., 2009. PLoS. Neglect. Trop. D., 3: e368. https://doi.org/10.1371/journal.pntd.0000368

Lv, S., Zhang, Y., Steinmann, P., and Zhou, X.N., 2008. Emerg. Infect. Dis., 14: 161. https://doi.org/10.3201/eid1401.061529

Qin, Y., Zhou, W., Li, X.W., Feng, M.Q., and Zhou, P., 2007. Enzyme Microb. Tech., 40: 1358-1366.

Song, L.G., Wang, X.W., Yang, Z., Lv, Z.Y., and Wu, Z.D., 2016. Parasitol. Res., 115: 913-923. https://doi.org/10.1007/s00436-015-4849-5

Wang, Q.P., Lai, D.H, Zhu, X.Q., Chen, X.G., and Lun, Z.R., 2008. Lancet Infect. Dis., 8: 621-630. https://doi.org/10.1016/S1473-3099(08)70229-9

Wang, Q.P., Wu, Z.D., Wei, J., Owen, R.L., and Lun, Z.R., 2012. Eur. J. clin. Microbiol., 31: 389-395. https://doi.org/10.1007/s10096-011-1328-5

Yang, T.B., Wu, Z.D., and Lun, Z.R., 2013. Hawaii. J. Med. Publ. Hlth., 72(6 Suppl 2): 23.

Yang, Y.X., Hu, Y.C., Li, X.H., Wang, X.J., Mou, X.D., Song, H.M., Wang, P.X., Liu, C., and Luo, J.R., 2010. Chinese Agric. Sci. Bull., 5.

Yusa, Y., 2004. J. Mollus. Stud., 70: 43-48. https://doi.org/10.1093/mollus/70.1.43