Infection and biogeographical characteristics of Paragonimus westermani and P. skrjabini in humans and animal hosts in China: A systematic review and meta-analysis

Kai Liu, Yuan-Chao Sun, Rui-Tai Pan, Ao-Long Xu, Han Xue, Na Tian, Jin-Xin Zheng, Fu-Yan Shi, Yan Lu and Lan-Hua Li

PLOS Neglected Tropical Diseases, 2024, vol. 18, issue 8, 1-24

Abstract: Background: Paragonimiasis, primarily caused by Paragonimus westermani and P. skrjabini in China, is a common food-borne parasitic zoonosis. However, the national distribution of Paragonimus spp. infection and its associated environmental determinants remain poorly understood. In this paper, we summarize the infection of P. westermani and P. skrjabini and describe key biogeographical characteristics of the endemic areas in China. Methods: Data on Paragonimus infection in humans and animal hosts were extracted from eight electronic databases, including CNKI, CWFD, Chongqing VIP, SinoMed, Medline, Embase, PubMed, and Web of Science. A random-effects meta-analysis model was used to estimate the pooled prevalence. All survey locations were georeferenced and plotted on China map, and scatter plots were used to illustrate the biogeographical characteristics of regions reporting Paragonimus infection. Results: A total of 28,948 cases of human paragonimiasis have been documented, with 2,401 cases reported after 2010. Among the 11,443 cases with reported ages, 88.05% were children or adolescents. The pooled prevalence of P. skrjabini is 0.45% (95% CI: 0.27–0.66%) in snails, 31.10% (95% CI: 24.77–37.80%) in the second intermediate host, and 20.31% (95% CI: 9.69–33.38%) in animal reservoirs. For P. westermani, the pooled prevalence is 0.06% (95% CI: 0.01–0.13%) in snails, 52.07% (95% CI: 43.56–60.52%) in the second intermediate host, and 21.40% (95% CI: 7.82–38.99%) in animal reservoirs. Paragonimus are primarily distributed in regions with low altitude, high temperature, and high precipitation. In northeastern China, only P. westermani infections have been documented, while in more southern areas, infections of both P. westermani and P. skrjabini have been reported. Conclusions: Paragonimiasis remains prevalent in China, particularly among children and adolescents. Variations exist in the intermediate hosts and geographical distribution of P. westermani and P. skrjabini. Additionally, altitude, temperature, and precipitation may influence the distribution of Paragonimus. Author summary: Paragonimiasis, a foodborne zoonotic parasitic disease caused by lung flukes (Paragonimus spp.), remains a significant neglected public health threat in many Asian countries, including China. Human infection occurs through the ingestion of raw or undercooked freshwater crab or crayfish containing the metacercariae stage. Given the popularity of consuming raw or undercooked freshwater products in many areas of China, understanding the infection status and spatial distribution of Paragonimus spp. in humans and animal hosts is crucial for controlling paragonimiasis. Our study provides a comprehensive summary of the infection levels of the two most important zoonotic Paragonimus species, P. westermani and P. skrjabini, in humans and animal hosts in China, along with a description of the spatial distribution and environmental characteristics of their endemic areas. We observe a wide distribution of Paragonimus infection in China, with a significant prevalence found in freshwater crabs and crayfish. Our findings underscore the importance of avoiding the consumption of raw or undercooked freshwater products to prevent foodborne diseases, including paragonimiasis.

Date: 2024
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DOI: 10.1371/journal.pntd.0012366

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