Parasites can cause a wide variety of serious economic and public health problems. The Ministry of Health of the People’s Republic of China conducted three nationwide surveys on the prevalence of human parasitic diseases in 1990, during 2001–2004, and 2014–2016, respectively, which showed that the positive rate of soil-transmitted nematodes, such as hookworm, Ascaris lumbricoides (A. lumbricoides), and Trichuris trichiura (T. trichiura), was significantly reduced, but the positive rate of foodborne parasites was significantly increased in some provinces (Yu et al., 1994; Xu et al., 1995; Coordinating Office of the National Survey on the Important Human Parasitic, 2005; Zhu et al., 2015). In 2006, soil-transmitted nematodiasis was included in the national infectious diseases and pathogenic media monitoring system by the Chinese Center for Disease Control and Prevention, and 22 monitoring spots were established nationwide, showing a declining trend of the human positive rate of intestinal nematodes from 2006 to 2013 (Chen and Zang, 2015). Over the years, the work of health education actively carried out by the Ministry of Health and periodic drug treatment for patients with parasitic infections prevent reinfection and reduce morbidity greatly (Zhao et al., 2012; McManus et al., 2014; Rivero et al., 2017; Guang-Han et al., 2018; Laoraksawong et al., 2018). Health education in primary schools showed a significant efficacy in preventing intestinal parasitic infections (Bieri et al., 2013a; Bieri et al., 2013b; Bieri et al., 2014; Cisse, 2019). The rapid economic growth over the past six decades witnessed the increased allocation of resources toward the control of parasitic diseases. Consequently, the status of parasitic diseases in China has improved significantly (De-Jian et al., 2013; Wang et al., 2016).

Foodborne parasites, most of which are zoonotic, can be transmitted by ingesting contaminated food and water. According to the life cycle and transmitted mode of parasites, foodborne parasites mainly include Trichinella, protozoa [e.g., Toxoplasma gondii (T. gondii), Giardia lamblia, and Cryptosporidium], tapeworms (e.g., Taenia solium and Spirometra mansoni), and trematodes [e.g., Paragonimus westermani (P. westermani), Clonorchis sinensis (C. sinensis), Schistosoma, and Fasciolopsis buski (F. buski)] (Robertson et al., 2014; Pozio, 2020). In 2006, the World Health Organization (WHO) established the Foodborne Disease Burden Epidemiology Reference Group (FERG), and in 2013, they summarized the burden of foodborne diseases (FBDs) and the important results available to date (Torgerson et al., 2014). The Global Burden of Disease Study published the global burden of foodborne trematodiasis and its sequelae in 2012 (Furst et al., 2012), showing that about 56.2 million people were infected with foodborne trematodes.

Great progress has been made in the prevention and treatment of human parasitic diseases in China over the past six decades. On June 30, 2021, the World Health Organization announced that malaria has been eliminated in China, but parasitic diseases are still one of the most serious public health problems in the world. China is still affected by parasitic infections, including leishmaniasis, schistosomiasis, toxoplasmosis, and other foodborne nematodiasis (Li et al., 2010; Wang et al., 2016). With increased income standards of living and consumption of exotic foods, foodborne parasitic infection has become one of the main factors that impact upon national food safety and public health (Li et al., 2010). The main foodborne parasitic diseases in China include paragonimiasis, clonorchiasis, toxoplasmosis, angiostrongyliasis, echinococcosis, trichinellosis, and cysticercosis (Torgerson et al., 2014). The overall prevalence of T. gondii infections in food animals was significantly higher than that in humans (Dong et al., 2018). In Hunan Province, because of the dietary habits of local residents, such as eating raw snake galls and undercooked fish and crabs, the status of some foodborne parasitic infections is serious. Due to the strengthening of international cooperation in globalization and the prosperity of tourism, imported cases are also increasing (Song et al., 2018).

In 2015, the investigation on the prevalence of major human parasitic diseases in Hunan Province showed that soilborne nematode infection accounted for 80.35% of the intestinal parasite infections (Zhuo et al., 2017), which suggested that we still need to strengthen the prevention and control of soilborne nematodes. In Hunan Province, the parasite epidemic situation in the recent 5 years is unclear. Through retrospective analysis of the examination of suspected cases of parasitic diseases in our laboratory from January 1, 2016, to December 31, 2020, our study aims to understand the current situation and prevalence of parasitic diseases and infection in Hunan Province and provide scientific data and basis for the prevention and treatment of parasitic diseases in the future.

In this survey, people suspected to have a parasitic infection by clinicians or themselves were recommended to the Parasitological Laboratory, Department of Parasitology, Xiangya School of Medicine, Central South University, Changsha, Hunan, China, for further testing; therefore, the positive rate of parasitic infection of the survey may be higher than that of the stratified cluster random sampling method. In 2015, the investigation on the prevalence of major human parasitic diseases in Hunan Province showed that soilborne nematode infection accounted for 80.35% of intestinal parasite infections (Zhuo et al., 2017). However, we found that foodborne parasites account for a major portion of parasite infections, and only eight cases of soilborne nematodes were detected in this study, which suggests that over these years the work of controlling soilborne nematode infections had achieved great success. On the other hand, nematode infection is relatively easy to identify and can be easily diagnosed by clinicians, so it does not require further examination in our laboratory. That is why the number of stool samples accepted by our laboratory is relatively small, resulting in a relatively small proportion of nematodes detected. In previous studies, both the positive rates of overall parasites and soilborne nematodes of female patients were higher than those of male patients (Yu et al., 1994; Xu et al., 1995; Coordinating Office of the National Survey on the Important Human Parasitic, 2005; Zhu et al., 2015), which was opposite of our results. Although the number of soilborne nematodes we detected was too small to be analyzed effectively, the positive rate of males for both overall parasites and foodborne parasites was significantly higher than that of females.

In this survey, the main parasites detected were foodborne parasites such as plerocercoid, P. westermani, T. gondii, cysticercus, and C. sinensis, which may be related to the dietary history of people. The Xiangjiang, Zishui, Yuanjiang, and Lishui rivers run through Hunan Province, so there are many small rivers and streams, which are conducive to the breeding of crabs, freshwater snails, freshwater fish, and shrimps. The local people have a habit of eating freshwater creatures and drinking raw water from streams, which greatly increases the risk of parasitic infection, such as P. westermani and C. sinensis (Peng et al., 2018; Li et al., 2019). A recent study found that the infection status of plerocercoid in snakes was severe in Hunan Province (Liu et al., 2020), while eating raw snake galls, using frog skin for injury and disease, and eating snakes and frogs were very common for local residents (Liu et al., 2010; Wang et al., 2011; Wang et al., 2014; Zhang et al., 2020). Hunan Province is one of the most important provinces in pork and mutton production, and wild snakes have been widely sold at food markets in some regions. Especially, foodborne parasites are usually zoonotic, so livestock usually can be infected with parasites, such as T. gondii, cysticercus, and Trichinella (Cui et al., 2013; Jiang et al., 2016; Li et al., 2016; Tan et al., 2018; Wang et al., 2019). Eating undercooked meat is popular in some areas of this province, which increases the risk of human parasitic infection with parasites.

With enhanced globalization as well as international and regional communication and cooperation, imported cases have become the main challenge to the elimination of several parasitosis, such as malaria and schistosomiasis, in mainland China (Song et al., 2018). A total of 31,740 cases of infectious diseases mainly from Africa and Asia were imported to mainland China during 2005–2016, and most of them were found in Yunnan Province (Wang et al., 2018). In this survey, we found three imported cases outside of Hunan Province, two of which were from Africa, and the imported S. mansoni myelopathy was the first case reported in China. The frequency of imported infection is increasing in China, and transmission of infection through international travel arises this health issue. Between January 1, 2014, and December 31, 2016, 22,797 cases were identified among 805,993,392 travelers arriving in China, with an incidence of 28.3 per million (Fang et al., 2018). In recent years, Kala-azar has been endemic and persistent in the mid-west regions of China. The reported cases were mainly from Xinjiang, Gansu, and Sichuan (Zheng et al., 2017). In general, we still need to step up efforts to prevent and control imported diseases.

In China, the relevant examinations in the parasitology diagnostic laboratory mainly include etiological and immunological assays. The examination of etiology is mainly used to observe whether there are worms, eggs, or trophozoite of protozoa in specimens through a microscope, but the detection rate of this method is very low (Lin et al., 2011). In recent decades, the immunological technology in the medical industry has been more and more mature, with a higher sensitivity and positive rate than that of etiological examination, and the detection of parasitosis is also more and more inseparable from immunological examination (Pacheco et al., 2020). That is why sometimes the positive result by immunological examination is negative by etiological examination. The diagnosis of parasitic diseases mainly depends on clinical manifestations and immunological examination, but immunological examination is only an auxiliary diagnosis method, which cannot be used as the basis for the diagnosis of parasitosis. The positive result of etiological examination is the direct evidence to confirm parasitic infection. There are still many limitations of current detection methods. On the one hand, both microscopy and immunological assays are labor-intensive and time-consuming, have low sensitivity and low specificity, and require professionals to clarify the results (McHardy et al., 2014). On the other hand, factors influencing the sensitivity of parasitic examinations include sporadic shedding (requiring the examination of multiple feces specimens), patient medications, sample collection interval, and the preservation of specimens prior to testing. Additionally, false positives in immunodetection may be related to the wrong time of reading results, improper dilution of specimen, use of out-of-date methods, and improper storage temperature of samples (Roellig et al., 2017). Considering the limitation of microscopic and immunological tests, molecular tests such as DNA-based and quantitative PCR (qPCR)-based detection methods have been gradually developed for parasite detection. Although molecular assays are more rapid and sensitive, the cost of many of them is much higher than traditional ones. Thus, a molecular test has not been extensively used in commercial laboratories (Verweij and Stensvold, 2014; van Lieshout and Roestenberg, 2015; Paulos et al., 2016; Ryan et al., 2017).

We observed an age distribution pattern among the patients, and the positive rate of people under the age of 15 was relatively high especially for foodborne parasites ( Figure 3 ). Some children and teenagers at this age live with their grandparents, and they spend lots of time playing outside without adult supervision such as playing in the river and eating undercooked freshwater fish, shrimps, and crabs, which would increase the risk of parasitic infections. The largest number of people tested for parasitic disease was between 50 and 69; most middle-aged people at this age are farmers, living in the village; and they usually work barefoot in the fields or in rivers. Some of them prefer drinking raw water and eating raw fish, shrimp, crab, and snake galls, and they work in areas where parasitic diseases are prevalent, which greatly increases the risk of parasitic infections.

Located in the middle reaches of the Yangtze River and the south of Dongting Lake, Hunan Province is surrounded by mountains and hills to the east, south, and west, while the central and northern parts are a U-shaped basin, open in the north. The Xiangjiang, Zishui, Yuanjiang, and Lishui rivers converge on the Yangtze River at the Dongting Lake. It has a complex terrain and a subtropical monsoon humid climate with a mild climate, four distinct seasons, and concentrated rainfall. Warm and humid climates are ideal for parasites to grow and reproduce, so parasitosis has long been a major public health problem in Hunan Province. The prevalence of overall parasitic infection in different regions of Hunan Province ranged from 6.49% to 22.10%, with the highest and lowest prevalence in Yongzhou and Xiangtan, respectively ( Figure 4 ). The difference of prevalence of several common parasites in different regions was also significant (P < 0.05), except for cysticercosis. The number of species was bigger, and the intensity of parasitic infection was greater in people who live in mountainous areas than those in hilly areas. People who lived in lake areas had the lowest parasitic infection, but S. japonicum infection was much more serious in lake areas and hilly areas. For example, Yueyang, Yiyang, and Changde are close to Dongting Lake, Wanzi Lake, and Dalian Lake, respectively, where Oncomelania hupensis, the intermediate host of S. japonicum, are abundant. That is why we found a relatively high positive rate of S. japonicum in these cities. This discovery was consistent with that found in goats in Hunan Province (Ma et al., 2014). There is a higher intensity and longer duration of precipitation in mountainous areas than that of hilly areas, which is suitable for parasites to multiply. In addition, more goats are raised in mountainous areas where people eat mutton more easily and frequently. Some people even prefer to eat undercooked lamb which increases the risk of parasitic infections. There are a lot of wild animals in mountainous areas, most of which are infected with parasites. An investigation in 2018 found that the prevalence rate of plerocercoid infection in wild snakes from Hunan Province was up to 91.7% (Liu et al., 2020). Eating raw snake galls and snakes was very common for the local people because many people believe snake galls possess therapeutic effects on many diseases and snake meat is a great health tonic. Such customs in this province may facilitate human infection with plerocercoid. Fortunately, China has now banned the sale of wild animals in the market, which may greatly reduce the risk of foodborne parasite infection in the future.

The prevalence of some parasites and their intermediate hosts is affected by season, climate, temperature, etcetera. For example, the snail is the intermediate host of S. japonicum, and there are more snails in spring and autumn, so the prevalence of S. japonicum is relatively high in the two seasons. In this study, there was a significant difference in the prevalence of parasitosis between months, which is consistent with a previous study (Wang et al., 2019). Additionally, a survey of helminths in goats in Hunan Province shows that the number and intensity of nematodes and cestodes peaked in summer and autumn, while the highest prevalence of trematodes was in winter (Ma et al., 2014).

In recent years, epidemic prevention and control departments have also carried out various prevention and control measures, such as changing the water supply, improving the flush system, taking medicine, and health education (De-Jian et al., 2013; Wang et al., 2016). The positive rate of soil-transmitted nematodes, such as hookworm, T. trichiura, and A. lumbricoides, was significantly reduced. Since the outbreak of COVID-19, the CPC Central Committee has attached great importance to the public health threat posed by overeating wild animals and introduced laws to strictly prohibit the predation of wild animals, which is conducive to reducing the infection of foodborne parasites. However, there is still much to do to prevent and control foodborne parasites.

The incidence of soilborne nematode infections has decreased significantly. However, foodborne parasites gradually become the main parasitic infections and multiple infections become more common. This study is of great significance evaluating the prevalence of parasitosis in Hunan Province in recent years, which suggests that we should not only continue the prevention and control of soilborne nematodes but also focus on the prevention and control of foodborne parasites.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The studies involving human participants were reviewed and approved by the Ethics Committee of the School of Basic Medical Science, Central South University, Changsha, China. Written informed consent to participate in this study was provided by the legal guardian/next of kin of the participants.

XL: conceptualization, provision of photographs, laboratory analyses, data analysis, writing—original draft preparation, writing—review and editing, and project administration. MW: laboratory analyses and raw data statistics. YL: laboratory analyses and review manuscript. JL: laboratory analyses. DY: laboratory analyses. LJ: conceptualization, data analysis, writing—review and editing, project administration, and funding acquisition. All authors contributed to the article and approved the submitted version.

This work was supported by the National Natural Science Foundation of China (grant number 32170510); Natural Science Foundation of Hunan Province, China (grant number 2020JJ4765); Open-End Fund for the Valuable and Precision Instruments of Central South University (grant number CSUZC2019046); Science and Technology Program of Hunan Province (grant number 2021ZK4154); and Graduate Case Base Construction Project of Central South University (grant number 2020ALK91).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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