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Taenia solium taeniasis/cysticercosis is an important global food-borne zoonosis transmitted between humans and pigs. In China, the prevalence of Theridion solium taeniasis/cysticercosis has been marked decline in recent decades based on the data revealed by both national surveys and field prevalence investigations. Health education and promotion, meat inspection, and chemotherapy are unquestionably the main control measures for diseases. It is worth noting that a variety of socio-ecological variables have been identified in the process of controlling T. solium taeniasis/cysticercosis. It has become difficult for pigs to come into direct or indirect contact with or consume human excreta as pig farming practices have been shifted from traditional backyard farms to large-scale commercial pig raising systems that are still in progress. The human toilet revolution in rural areas of China has ensured hygienic separation of human excreta from contact, and thereby preventing human excreta from polluting the soil, feeds, and water. These two important fundamental preventive measures are crucial to establishing an environmental restriction between humans and pigs cannot be overlooked for interrupting or limiting T. solium transmission. In this chapter, we reviewed the epidemiology, traditional measures, and ecological determinants that significantly contributed to the dramatic decline of taeniasis/cysticercosis in China.
College of Veterinary Medicine, Henan Agricultural University, Zhengzhou, China
International Joint Research Laboratory for Zoonotic Diseases of Henan, Zhengzhou, China
Longxian Zhang*
College of Veterinary Medicine, Henan Agricultural University, Zhengzhou, China
International Joint Research Laboratory for Zoonotic Diseases of Henan, Zhengzhou, China
*Address all correspondence to: zhanglx8999@henau.edu.cn
1. Introduction
Taenia solium taeniasis/cysticercosis is an important food-borne zoonosis which is transmitted between humans and pigs all over the world [1, 2]. Taeniasis typically causes several digestive problems in humans, whereas cysticercosis is a very serious disease in both humans and pigs [3]. Porcine cysticercosis primarily parasitizes muscle tissues and visceral organs throughout the body of pig resulting in poor quality of pork. However, human cysticercosis may take several pathological forms such as neurocysticercosis (NCC), ocular cysticercosis (OCC), subcutaneous muscle cysticercosis, oral cavity cysticercosis, visceral cysticercosis, and others [3, 4, 5]. Human NCC is mainly responsible for seizures, high intracranial pressure, and psychiatric disorders, and it is considered to be one of the major disease burdens in people in many parts of the world [6].
Theridion solium taeniasis/cysticercosis is a severe helminth infection common in humans and domestic pigs raised in close proximity to human settlements, particularly those in warm and mild climates in Latin America, Sub-Saharan Africa, Southeast Asia, the Indian subcontinent, and China [7, 8, 9]. In some endemic areas of T. solium, cysticercosis is a leading cause of epileptic seizures in humans [10, 11], while NCC has been noticed as a health burden even in non-endemic regions such as America and Europe owing to frequent traveling and immigration [2, 12]. Approximately 50 million people worldwide suffer from NCC caused by T. solium with more than 50,000 deaths per year [13], and studies have indicated a higher prevalence of cysticercosis and its burden than has been recognized by the public health service systems [14, 15].
As the life cycle of T. solium involves humans and pigs (Figure 1), humans acquire tapeworm infection by consuming raw or under-cooked pork containing cysticerci [16]. Following ingestion, the larval tapeworm grows into an adult worm within approximately 2 months in the human small intestine [16]. Humans are the only natural definitive hosts who harbor the adult form of T. solium in their small intestines [8]. Eggs or the most distal worm segments (proglottids) containing mature eggs are released as they frequently detach from the worm and then are passed out into the environment with human feces [8, 17]. These eggs can infect the same (auto-infection) or other humans through fecal-oral transmission from direct contact with tapeworm carriers or consumption of water or food contaminated with human feces [6, 16, 18]. Pigs acquire infection through consumption of human feces containing infectious eggs (gravid proglottids) as well as contaminated food, water, and soil [8]. Humans and pigs could both serve as intermediate hosts, and the embryo (oncosphere) is released after ingestion and migrates through the intestinal mucosa. Later, the larval stages (cysticerci) lead to systemic infection in brain, eyes, subcutaneous tissues, and viscera of the host via blood circulatory system [8].
Figure 1.
The life cycle and mode of transmission of Taenia solium in humans and pigs. The blue cycle indicates the traditional life cycle of Taenia solium. Humans become infected and the tapeworms colonize in the gut after consuming raw or undercooked pork containing larval tapeworm, the cysticerci that matures into an adult worm in the human small intestine in about 2 months. The worm’s eggs or the most distal segments (proglottids) carrying mature eggs are periodically released/detached and subsequently discharged into the environment with human stool. Pigs get infected when they consume infectious eggs (gravid proglottids) in human excrement, food, water, and soil. Both humans and pigs could serve as intermediate hosts, and the embryo (oncosphere) is released after ingestion and migrates through the intestinal mucosa. Later, the larval stages (cysticercus) commonly infest host body organs such as the brain, eyes, subcutaneous tissues, and viscera via the blood circulatory system. Similarly, humans become infected by consuming raw or undercooked pork containing cysticerci that mature into an adult worm in the small intestine in about 2 months. The red dashed cycle represents the rebuilding Theridion solium life cycle. As a result of a structural shift in pig farming from backyard to large-scale intensive pig farming, as well as a toilet revolution aimed at improving sanitary conditions, the transmission of T. solium between humans and pigs has been significantly interrupted, and spread of the disease is being gradually lessened.
Domestication of wild boars (Sus scrofa) began 9000 years ago, and pig rearing has been a common practice in Asian countries for more than 2500 years [19]. Cysticercosis has long been a worldwide zoonosis transmitted between pigs and humans [3]. In China, the prevalence of T. solium taeniasis/cysticercosis has been significantly reduced in the recent decades as a result of ongoing health education and promotion as well as sanitary improvements [3, 20, 21]. There have been noticeably dramatic changes in pig-rearing methods and socio-ecological factors as well in China [22, 23]. In this chapter, we reviewed the epidemiology, traditional measures, and ecological determinants that outstandingly contributed to the decline of T. solium taeniasis/cysticercosis in China.
2.1 National surveys on human taeniasis/cysticercosis
Three national surveys on parasitic diseases in humans have been conducted in China until now (Table 1). In the first national survey (1988–1992), a total of 1,477,742 individuals from 30 out of 34 provinces in China were investigated, and 2449 individuals from 28 provinces were found to have Taenia spp. infections [24]. These data led to an estimation of about 1.3 million cases of Taenia spp. infection in the country [25]. The second nationwide survey (2001–2004) conducted in 31 provinces (out of 34 provinces in China) with a total sample size of 356,629 people revealed that 983 people from 12 provinces (38.7%, 12/31) were diagnosed to have Taenia spp. infestation [26]. According to these findings, 0.55 million people were infected in total estimation [26]. Likewise, in the third nationwide survey (2014–2015), Taenia spp. was found in 1752 people from 12 provinces (38.7%, 12/31) out of 617,441 people under investigation from 31 provinces (out of 34 provinces in China) [27]. Considering the demographic structure in the whole population, a weighted prevalence of 0.06 percent was calculated, implying that 0.37 million people were infected [27].
Surveys
Sampling periods
Number of provinces surveyed/total number of participants
National surveys on human taeniasis/cysticercosis in China.
It was a weighted prevalence, and it was estimated after adjustment by the population structure in total population.
Three national surveys on human parasitic disease in China revealed a significant decline in human T. solium taeniasis/cysticercosis, while recorded cases indicated that T. solium cysticercosis was traditionally endemic in northeastern, central, and southwestern China (Figure 2). However, infection rates have been high in areas in the southwest of China with poor socioeconomic conditions, particularly in Tibet, Sichuan, and Yunnan [3, 28, 29, 30].
Figure 2.
Three national surveys on human taeniasis/cysticercosis in China (adapted from [3]). Different colors represent different prevalence of taeniasis during three national surveys. The darker color (red) indicates the higher prevalence rate, and the lighter color (green) indicates the lower prevalence rate. Theridion solium cysticercosis was historically prevalent in northeastern, southwestern, and central China, and three national surveys claimed that the frequency of taeniasis has decreased considerably in most areas of China. However, infections have been high in areas of Southwest China with poor socioeconomic conditions, particularly in Chinese Tibet, Sichuan, and Yunnan.
2.2 Case summary of human taeniasis/cysticercosis
There are a variety of human taeniasis/cysticercosis case reports in China. Among them, brain neurocysticercosis (NCC) was the most prevalent (75.87%), followed by subcutaneous infections (11.17%). Several reports have documented mixed infections related to multiple organs, with the brain and subcutaneous cysticercosis being the most common (4.74%) (Figure 3).
Figure 3.
Case records from hospitalized patients with taeniasis/cysticercosis in China.
2.3 Prevalence of human taeniasis/cysticercosis
The epidemiology of human taeniasis/cysticercosis has been well documented and recorded in the same area for many years (Figure 4A). It is observed that the prevalence rates have generally been declining when the prevalence rates for various years in the same location are compared [3, 28, 29]. Analysis of risk factors revealed that the prevalence of human cysticercosis is the highest in areas where sanitation is poor, toilets are lacking, and people traditionally consume raw or under-cooked pork (or viscera) and/or where pig husbandry is substandard [3, 28, 29, 31, 32, 33].
Figure 4.
Field prevalence investigations of human taeniasis/cysticercosis (a) and porcine cysticercosis (b) in the past decades by regional distributions. The prevalence of porcine cysticercosis has been noticeably declining, according to a comparison of the documented cases during the slaughter quarantine for various years in the same region.
2.4 Field prevalence of porcine cysticercosis
As with human cysticercosis, there were numerous studies on the epidemiology of porcine cysticercosis, which were mostly carried out during the slaughter quarantine. For a comparative analysis of the prevalence rates of the human cysticercosis for different years in the same area, it is found that the prevalence has been significantly declining (Figure 4B). Humans are the only natural definitive host for cysticercosis [8], and pigs become infected through consumption of human feces in areas where open human defecation is common, and also through contaminated food, water, and soil [8].
As with other infectious diseases, the transmission of T. solium taeniasis/cysticercosis requires three key links, such as infectious source, route of transmission, and susceptible population which are correlated [21]. Health education and promotion primarily target the susceptible population and infected individuals (Table 2). In view of the serious harm to human health and animal husbandry for taeniasis and cysticercosis of swine, the “Qu Tao Mie Nang” movement had been extensively carried out in the endemic areas from 1970s to 1990s in Chinese mainland. The main objective of the movement was the treatment of the human taeniasis and elimination of pig cysticercosis. The strategy of the same movement was the early treatment of taeniasis in patients once diagnosed, carry out extensive pork quarantine in urban and rural areas to ensure the quality of meat products, speed up the transformation of rural toilets, and improve the environmental sanitation to obstacle the disease transmission routes, and treatment of human patients and pigs with cysticercosis with the application of effective drugs. It refers to a comprehensive social and political process that includes not only improving individual knowledge, lifestyle, and life skills, but also changing societal, environmental, and economic conditions to reduce the negative effects of parasitism on individuals and communities [20, 21].
Serial number
Main content
1st
Keep the human toilet and pigsty separate, and keep the pigpen clean
2nd
Avoid pigs eating human stool or contaminated feeds and water
3rd
Strengthen slaughter quarantine of pigs, prohibit the sale of pork with cysticercosis, and use harmless treatment
4th
Do not eat raw pork or pig skins
5th
Treatment in time if got sick
Table 2.
Health education and promotion for Theridion solium taeniasis/cysticercosis in China (adapted from [34]).
3.2 Meat inspection
Pork contaminated with cysticercus is a major source of human T. solium taeniasis and cysticercosis transmission. Inspection of pork at slaughter is an important public health measure to prevent the transmission of T. solium to humans [16]. However, meat inspection is usually only effective in detecting heavily infected carcasses and is not much reliable in detecting lightly infected carcasses because it depends on the expertise of the meat inspector [35]. Cysticerci can be confused with sarcocystis, milk spots, hydatid cysts, and even unstructured fat and muscle fasciae [35, 36].
Unfortunately, in some parts of China, national pork inspection guidelines are insufficient for detecting cysticercosis. In particular, illegal slaughters occur frequently when pigs are suspected of having cysticercosis in order to avoid economic loss due to the fear of infected pigs likely to be confiscated [16]. Another example is the consumption of raw or under-cooked pork as a traditional way of life in some areas, particularly in/from Sichuan, Yunnan, and Guangxi, China, where pigs are raised in substandard conditions [28, 30, 31, 33, 37, 38]. These days, great strides have been made in health education and promotion.
3.3 Chemotherapy
For the current chemotherapy, it is now possible to actively identify and treat parasite-infected patients, and even to perform mass chemotherapy due to the availability of effective anthelmintic drugs, such as praziquantel (PZQ), niclosamide, albendazole, and others [8, 20, 39, 40]. Therefore, the possible sources of infections could be minimized to the greatest extent possible, and the transmission of T. solium taeniasis/cysticercosis could be controlled.
The treatment of cysticercosis must be tailored to the location of the lesions, the stage of disease progression, and the host’s immune response [41]. In most cases, antiparasitic drugs should be used to destroy live or degenerating cysticerci [9]. It has been reported that the therapeutic effects of albendazole and praziquantel treatments for cerebral cysticercosis are well understood, and the combination treatment using albendazole and praziquantel treatments can increase the therapeutic efficacy for cerebral cysticercosis [20]. However, due to their high toxicity, these drugs are used at concentrations that inhibit parasite growth and reproduction rather than killing them [42]. Thus, novel targets and compound classes with low toxicity and high efficacy at low doses are urgently needed for disease prevention, control, and intervention. Recently, a combination of pumpkin seeds and areca nut has been investigated against taeniasis, while praziquantel and albendazole are administrated concurrently against cysticercosis with promising efficacy and low side effects [3].
While adult worm infestations are largely asymptomatic, living in the intestine without causing harm, the larval stages, particularly cysts, can cause symptomatic pathologic symptoms, often leading to serious life-threatening conditions as they spread to other body parts such as the brain, muscles, or other organs including the liver. Depending on the patient’s condition and cyst location, NCC is traditionally treated with chemotherapy or surgery. In severe cases, such as for NCC, surgery is required to lower intracranial pressure and resolve hydrocephalus [43, 44]. It is performed when cysts lodge in such areas of the brain that may cause CSF obstruction, resulting in hydrocephalus. Given the advances in minimally invasive techniques, minimally invasive neurosurgery can be successfully applied in cases of mild NCC (i.e., only a few cysts), especially in the case of a single cyst [45]. Surgery is the only option for ocular cysticercosis due to the risk of blindness from antiparasitic reactions, and asymptomatic subcutaneous or intramuscular cysticerci do not require treatment [3].
Surgical treatments are needed in some patients afflicted with cerebral cysticercosis with very high intracranial tension, but not all the cysticercus can be removed completely. Antiparasitic therapy cannot be substituted. Therefore, antiparasitic drugs are still required after surgery [20].
In general, the pig industry in China has three breeding modes: backyard farm, specialized household farm, and large-scale commercial farm [23]. For thousands of years, small-scale farmers raised all sorts of pork in China. Prior to 1978, these so-called backyard farms, which raised fewer than five pigs per year along with crops and other livestock, produced at least 95 percent of the country’s pork [46].
In 2007, backyard farmers accounted for approximately 27% of the national pork production though the smallholder share was much higher in some regions of China. For example, in Sichuan, the historic and current national leader in pork production was backyard farms, which contributed 70% of the entire pork in the province, compared to roughly 20% in Guangdong Province [23]. Feeding troughs, the human toilet, and the pigsty used to be always next to each other in those backyard farms, and pigs could easily consume human stool or contaminated food and water. Following China’s Reform and Opening (which began in 1978), the structure of pig farming in China has changed extensively kicking off the trend toward large-scale commercial pig raising, which still continues today [46]. Production on these farms ranges from 500 to 50,000 pigs per year and is rapidly expanding. It is not unusual for a single company to produce 100,000 hogs in a single year [23]. In 1985, these farms accounted for only 2.5% of total pork production in the country, but by 2007, their share had increased to 22% [23]. In that situation, the human toilet and the pigsty were completely separated, and the pigs were not allowed to have direct access to consume human excreta or contaminated feeds and water. The specialized household farm (5–500 pigs per year) falls somewhere between the backyard farm and the large-scale commercial farm. In Sichuan, specialized households accounted for 25% of the total, while large-scale commercial farms contributed only 5% [23]. As farming practices have changed, it has become increasingly difficult for pigs to come into contact with human stool or contaminated feeds and water, and the transmission of T. solium would be cut off (Figure 1). As a result, if environmental reconstruction can create unfavorable conditions for these intermediate hosts, the T. solium transmission route could be disrupted, and the disease transmission could be minimized to a greater extent [21].
4.2 Human toilet revolution
Many pathogens can be found in human feces, including T. solium eggs, which can cause serious intestinal infections. The discharge of large amount of untreated feces sludge into the open environment endangers public health [47]. The human toilet revolution in extensively rural areas in China is a step-by-step campaign aimed at ensuring hygienic separation of human excreta from human contact, providing sanitary and comfortable space for users, preventing human excreta from polluting the environment, and realizing resource recycling [47].
The toilet revolution aims to increase the use of sanitary toilets, which definitely aids in disease prevention. During the ongoing toilet retrofitting campaign in rural areas, China has made significant progress. In China, the number of sanitary and innocuous-sanitary toilets has increased in the last decade, while significant regional diversification requires to be completed [48]. Sanitary toilet coverage in the rural areas has increased from 7.5% in 1993 to 78.5% in 2015, while harmless sanitary toilet coverage reached 57.5% by the end of 2015 [47]. The numbers have been increasing in most regions. Overall, the toilet revolution has made significant progress in improving sanitation infrastructure in rural China.
Currently, the concept of a toilet revolution is being enlarged and extended. Furthermore, it is not confined to the toilet, but to the entire sanitary system [47]. Consequently, pigs are getting very little opportunity to feed on human stool, and the transmission of T. solium between humans and pigs is being controlled.
Comprehensive prevention and control encompasses chemotherapy for taeniid tapeworm carriers, cysticercosis patients and pigs in the community, as well as government initiatives for food safety laws, and meat inspections and regulations [16, 21]. Since 1970s, there have been surveillance and intervention measures for cysticercosis/taeniasis in endemic areas across the country through government health education and promotion programs [16]. Government and international funds have consistently supported the community-based investigations of cysticercosis and taeniasis in order to advance disease control efforts. In China, health education and promotion have proven to be effective in the control of T. solium taeniasis/cysticercosis [20, 21, 49].
Great efforts have been made in the last few decades to develop effective vaccines and novel chemotherapeutic agents for the purpose of immunizing pigs and preventing T. solium transmission between humans and pigs, and continue in progress [50]. In recent field trials, a vaccine for porcine cysticercosis (TSOL18) has been shown to be highly effective against naturally acquired infection with T. solium in pigs [6]. In the recent years, evidence of active elimination of T. solium transmission with the use of the porcine cysticercosis vaccine TSOL18 in combination with a single dose of oxfendazole treatment of pigs has been obtained from endemic areas of Cameroon [51]. Indeed, it has the potential to be an excellent tool in the fight against cysticercosis.
Mass treatment of taeniasis is a cost-effective control strategy in the endemic areas [52]. Oxfendazole has been shown to be an effective drug for curing pigs by eliminating the cysts and providing resistance to further infection. Educating farmers about the importance of resource management strategy to minimize such kind of infections will encourage them to invest more money on pig farms [53, 54].
Interventions focused on pigs will not only control the sources of taeniasis transmission but may also potentially ameliorate the economic value of the pigs. Preventing T. solium infection and treating cysticercosis in pigs obviously benefit the farmers financially and may lead to increased compliance with other control activities such as community-based screening, therapy, and health education [55].
5.2 From the human aspect
Poor hygiene, inadequate sanitation, the use of untreated or partially treated human waste in agriculture, improper food handling, lack of knowledge about the risk of infection while visiting endemic countries, and the consumption of raw or undercooked pork, particularly in/from regions where pigs are raised in poor conditions, all contribute to the spread of human taeniasis/cysticercosis [31, 33, 37, 38]. Moreover, person-to-person transmission should not be ignored [56, 57].
Enhancing sanitation and health education to improve sanitary and food hygiene practices, interventions consisting of human chemotherapy with better diagnostic tools for taeniasis, and porcine chemotherapy and immunization should all be included in the prevention and control of Taenia pp. infections and cysticercosis [58]. Co-infection of multiple helminthes and other parasites is very common in cysticercosis-endemic regions and countries. In order to develop effective integrated parasite control programs, health systems and services must consider the presence of various parasites [3]. According to the available data, implementation of a single approach to T. solium control is insufficient. Thus, an integrated approach is required to ensure long-term prevention and control.
5.3 From the ecological aspect
In the past few decades, significant efforts have been made and are still being realized to eliminate human cysticercosis. Among these efforts are health promotions, meat inspection, chemotherapy, and combined comprehensive measures, which no doubt are the primary control measures for the diseases [21]. However, some additional factors such as modification in pig farming practices and the development of modern toilets that could affect human and pig T. solium taeniasis/cysticercosis have also been identified. These preventive measures could significantly hinder the T. solium transmission route. Although these two factors were often mentioned in the previous articles [59, 60, 61], the fundamental significance for reducing human cysticercosis by minimizing disease transmission was not adequately addressed. The spread of T. solium taeniasis and cysticercosis is noticeably being gradually reduced along with the shift in pig farming practices from small-scale to large-scale intensive farms as well as the revolution made in the use of sanitary toilets by humans.
However, T. solium taeniasis and cysticercosis are still prevalent in some low-socioeconomic areas of China, particularly in rural communities in Sichuan, Yunnan, and Guangxi provinces, where pigs are reared in substandard management conditions, and the consumption of raw or undercooked pork is a traditional feeding habit [28, 31, 37, 58]. Therefore, in order to completely eliminate cysticercosis, promotion of health and education, meat inspection, and chemotherapy are warranted and must be continued in the days to come.
T. solium taeniasis/cysticercosis is an important food-borne zoonotic parasitic disease frequently transmitted worldwide between pigs and humans. Poor hygiene, inadequate sanitation, the use of untreated or partially treated human excreta in agriculture, improper food handling, lack of proper knowledge regarding the risk of infection while visiting the endemic countries, and the consumption of raw or under cooked pork (or viscera) particularly in/from regions where pigs are raised under poor conditions facilitate its spread.
Based on the epidemiological studies on taeniasis/cysticercosis in both humans and pigs, a number of factors have been identified to have contributed to decreasing trend of this disease in China over the last few decades. The promotion of health and education, meat inspection at slaughterhouses, and chemotherapies have significantly contributed to a marked decline in the prevalence of T. solium taeniasis/cysticercosis in China. Furthermore, the two most crucial measures, that is, the structural shift in pig farming from backyard to large-scale intensive farms, and the revolution made in the practice of using toilets to improve sanitary conditions created unfavorable conditions for the pigs (i.e. intermediate hosts) to acquire cysticercosis.
If any of the essential links to the source of infections are missing, infectious disease transmission can be disrupted, and no new infections could occur. The disease transmission nexus and its intensity are affected by natural and social factors. Therefore, to control and probably to eliminate cysticercosis, a One Health approach is required, which includes the provision of awareness and education, construction and proper usage of latrines, better farm management, treatment and/or vaccination of pigs, and timely treatment of infected human cases.
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Written By
Junqiang Li and Longxian Zhang
Submitted: 08 January 2023Reviewed: 20 February 2023Published: 20 March 2023
Open access peer-reviewed chapter
