Epidemiology of Taeniosis/Cysticercosis in Humans and Animals

Abstract

Taenia saginata, Taenia solium, and Taenia asiatica popularly known as beef, pork, and Asian tapeworm, are important food-borne parasites. Human taeniosis occurs as a zoonotic consequence of consumption of raw or under-cooked meat contaminated by viable larvae of T. saginata (Cysticercus bovis), T. solium (Cysticercus cellulosae) and T. asiatica (Cysticercus viscerotropica) and further development of their adult forms in human intestines. T. solium is highly endemic in pork-consuming poor communities of Asia, Africa, and Latin America, T. asiatica is restricted to Asia and is mainly confirmed in South Korea, China, Taiwan, Indonesia, and Thailand, while T. saginata is distributed worldwide. Tapeworms cause cysticercosis in pigs and cattle (intermediate hosts) and taeniosis in humans (definitive host). Cysticercosis can also affect people who unintentionally swallow T. solium eggs—contaminated soil, water, or food (mainly vegetables) or through self-infection or person-to-person transmission when hygiene practices are insufficient. In humans, human cysticercosis or neurocysticercosis is frequently caused by cysticerci that establish in the central nervous system. Given the effect of T. solium on public health and the potential negative effects of T. saginata and T. asiatica on the economy and trade, defining risk factors, reporting of taeniosis and human cysticercosis is crucial, and surveillance and notification methods in animals should be strengthened.

1. Introduction

Tapeworms and cysticerci are mentioned during the time of ancient Egypt and Greece. However, their life cycle, including intermediate and definite hosts, are explained in the nineteenth century. Cysticercosis and taeniosis represent food-borne zoonotic infections by the larvae and adult forms of Taenia saginata (beef tapeworm), Taenia solium (pork tapeworm), and Taenia asiatica (Asian tapeworm). These parasites are unique since their life cycle includes humans as definite hosts.

Adult forms of T. saginata, T. solium, and T. asiatica cause human taeniosis. Transmission occurs via consumption of larvae found in animal tissues (beef or pork) and the consequent development of parasites to adult forms in human intestines. Symptoms of intestinal infection are stomachache, intermittent diarrhea, and weight loss, while anal pruritus manifests due to the active migration of proglottids.

Cysticercosis represents infection of tissues by larval stage of Cysticercus (metacestode) found in pigs, cattle, and humans, who in this case can be both intermediate and definite hosts. Larvae of the T. saginata are found in the muscles of cattle, larvae of the T. asiatica prefer inner organs of pigs (gut and liver), while larvae of the T. solium are usually localized in muscles, inner organs, and brain of pigs and humans. After consumption of T. solium egg, parasite evolves by larvae (oncospheres) exiting the eggs, which then penetrate the intestine wall and migrate to the eye, striated muscles, and subcutaneous tissue. This is diagnosed as human cysticercosis (HCC). Neurocysticercosis (NCC), occurs when cysticerci migrate to central nervous system tissues and currently it is the most common helminth infection of the nervous system and the leading cause of acquired epilepsy in the world [1]. Hence, T. solium is considered as the sole causative agent of NCC in humans with great public health importance, while T. saginata and T. asiatica are less clinically important. Their main impact is economic losses in animal production. However, the possibility that T. asiatica can cause cysticercosis in humans similar as T. solium is under investigation due to indications that T. asiatica caused several cases of human cysticercosis in Asia [2].

World Health Organization (WHO) considers human cysticercosis and taeniosis as neglected diseases, especially in undeveloped countries where many people live in poor hygiene conditions. Even though taenia-causing infections in humans have a worldwide distribution, cases are mostly reported in regions where cattle and pigs are reared extensively. Therefore, the distribution of each of the three taenia species depends on the culture and nutritional habits (i.e., consummation of raw or undercooked contaminated meat or organs of pigs and cattle) [3, 4, 5]. Occurrence of T. asiatica is limited to Asia. It is still not reported in Europe, where T. solium occurs but not as often, while infections by T. saginata are still common. Even though the life cycle of Cestoda is less likely to maintain with appropriate sanitary conditions and good farming practices, infections in such areas still can occur due to migrations. Imported infections increase global distribution into free areas such as the United States of America and Europe. Here infected people contaminate the environment leading to new infections.

Considering the global public health significance of taenia infections, maintaining vigilant surveillance is still needed as a tool to reduce disease incidence as much as possible, as the first step to the eradication of cysticercosis and taeniosis. This chapter summarizes etiology, pathology, and epidemiology of taeniosis/cysticercosis along with science-based approaches to its surveillance as food-borne parasites.

2. Characteristics of the parasites

The genus Taenia belongs to the Phylum—Platyhelminthes; Class—Cestoda; Order—Cyclophyllidea; Family—Taeniidae; Genus—Taenia. The genus Taenia is a highly diverse, paraphyletic group with 45 species identified to date, among which T. solium, T. saginata, and T. asiatica are infectious to humans.

T. asiatica differs from T. solium and T. saginata by morphological characteristics such as the scolex, mature and gravid proglottids of adults, and the scolex and bladder surface in the larval stage [6]. Today, the characterization of T. saginata, T. solium, and T. asiatica is based on molecular identification and determinations of the mitochondrial genome sequence. The complete mitochondrial genome sequence is available. The difference in the genome between T. asiatica and T. saginata is 4.6%, while T. solium differs by 11% [7]. T. asiatica is a relatively recently described species and received much attention in past decades. Discovery came from the paradoxical observation of a high prevalence of taeniosis caused by a T. saginata-like tapeworm in humans who did not consume beef, and the consequent description of the complete mitochondrial genome of “new” species. Experimental studies conducted in the 1980s and 1990s clearly demonstrated that the life cycle of T. asiatica is comparable to that of T. saginata, except that pigs are the preferred intermediate hosts and the liver is the preferred larval site.

Mitochondrial DNA data suggest that T. saginata and T. asiatica are very closely related [8, 9, 10]. T. saginata shows high genetic polymorphism (0.2–0.8%), while the genetic diversity of T. asiatica appears to be minimal, indicating that this parasite may be on the verge of extinction. However, research has shown the existence of hybrids between T. asiatica and T. saginata, reviving the issue of T. asiatica’s genetic diversity and its position as a distinct species. The identification of T. saginata and T. asiatica is by morphological and molecular characteristics and observed differences in the life cycle [6]. Genetic variation within the species T. solium was until recently almost unknown, even though investigations are ongoing. DNA analysis of T. solium isolates from around the world indicate variations between two geographic regions, Asia and Africa/South America, where T. solium appears as two genotypes and second is the Asian and the American/African genotype [11]. Analysis of the mitochondrial DNA of T. saginata shows great variation indicating greater complexity of this parasite species compared to T. solium [12].

2.1 Morphology of the parasites

The three morphological forms of the parasites are adults, eggs, and larvae. Tapeworms of the genus Taenia are flat, white or yellowish, and very long-segmented parasites. T. solium has a length of 2–8 m, while T. saginata and T. asiatica are thicker and wider and can be longer. The head or scolex (attachment organ) has four shoots and a rostellum that may contain hooks (T. solium), be unhooked and depressed (T. saginata), or with rudimentary hooks (T. asiatica). Hooks of T. solium make a crown with two rows of 22–32 hooks, whose size is 159–173 μm. The scolex is the size of a pinhead, followed by a short and undivided region, the neck. In T. saginata the neck is longer and thinner, and in T. solium thicker and shorter. The neck continues with a long chain of proglottids or segments (called strobilas). The strobila resembles a ribbon and may consist of several thousand proglottids. Proglottids have different developmental stages: proximal are immature, followed by mature proglottids and distal proglottids containing eggs and gradually increasing in size. The posterior end of the tapeworm has the widest, longest, and oldest proglottids [13, 14, 15]. Mature proglottids have both male and female reproductive organs. The female reproductive apparatus includes an ovary, a closed uterus with branches—an ootype, a single mass of bile glands, and a lateral genital pore. Male organs consist of testes (follicles), vas deferens, and cirrus. The uterus in the gravid proglottid of T. saginata has 15–30 lateral branches compared to T. solium with 7–13 branches. On average, adult T. solium has about 1000 proglottids, each containing 50,000 eggs; adult T. saginata has about 1000–2000 proglottids, each with 100,000 eggs; while adult T. asiatica has 700–900 proglottids, with 80,000 eggs each.

The eggs are spherical, 20–50 μm in size, and morphologically indistinguishable between species of the Taeniidae family. Each egg contains a multicellular embryo with six hooks, hence called a hexanth embryo or oncosphere. Manny eggs released from the definitive host are fully embryonated and infectious. T. saginata eggs are infectious to cattle, T. solium to both pigs and humans, and T. asiatica eggs are infectious to pigs. Because of their resistance to desiccation, eggs can survive for days or months in the environment, in soil, or in water.

Cysticercus T. solium (Cysticercus cellulosae) is found in the liver, brain, and skeletal muscles of pigs 6 days after infection, while in humans they can be located in the nervous system, eye, heart, muscles, and subcutaneous tissue. A mature cysticercus is usually spherical or oval, white or yellow, 0.5 and 1.5 cm in size, and has a transparent wall, through which the scolex is visible. Cysticerci have two chambers: an inner one containing the scolex and a spiral canal surrounding an outer fluid-containing chamber. The racemous form of cysticercus appears as a large, round, lobulated bladder, limited by a delicate wall or resembles a cluster 10–20 cm in size containing 60 ml of fluid. The most important characteristic of the racemous form is that the scolex cannot be clearly seen. Young cysticerci cause mild inflammation in the surrounding tissue, while mature lead to a stronger immune reaction [16, 17]. Following ingestion by the final host, the pores of the bladder wall expand, resulting in the release of the scolex [18].

Cysticercus T. saginata (Cysticercus bovis), is a 1 cm wide oval bladder, filled with fluid and containing an invaginated scolex without hooks. Cysticercus are localized in the skeletal muscles of cattle, however, there are sporadic reports of cysticercosis in llamas, pronghorn, oryx, topi and other antelopes, gazelles, wildebeests, and giraffes [19]. These intermediate hosts are infected by grazing.

Cysticercus of T. asiatica (Cysticercus viscerotropica) is smaller than T. saginata with a diameter of approximately 2–3 mm. Both have a scolex with a round rostellum surrounded by four symmetrically placed suckers, while T. asiatica has two rows of rudimentary hooks that usually do not develop into morphologically recognizable hooks. Cysticerci of T. asiatica are found in domestic and wild pigs and develop in the liver and extrahepatic organs, but not in the muscles [20, 21].

Animals carrying cysticerci are usually asymptomatic while muscle stiffness occurs in extremely severe infections. C. bovis and C. cellulosae do not develop severe pathology in cattle and pigs unless vital organs, such as the heart, are massively infested.

2.2 The life cycle of the parasites

Parasites of the family Taeniidae uniquely require two obligate hosts (mammalians): a carnivorous/omnivorous definitive host for the adult tapeworm stage and an herbivorous/omnivorous intermediate host for the larval (cysticercus) stage. The life cycle begins when herbivores/omnivores as intermediate hosts ingest plants, food, or water contaminated with taeniid eggs (or gravid proglottids). In the intestines, oncospheres hatch, activate, invade the intestinal wall, and migrate to tissues and organs, where they develop into cysticerci.

When the definitive host carnivore/omnivore eats raw or undercooked pork (T. solium, T. asiatica) and beef (T. saginata) containing fluid-filled cysticerci, the cyst (bladder) gets dissolved and the inverted scolex evacuates under the stimulus of the host’s digestive enzymes. The scolex embeds in the intestinal wall, and the neck buds and the strobila is formed. As the adult parasite grows, the release of gravid proglottids begins, and the first shedding occurs between 8 and 12 days after infection. New eggs may appear in the feces of the definitive host within 6–9 weeks, initiating the next cycle of infection [12].

People are infected in three ways:

• by swallowing undercooked/raw beef containing the encysted larval stage (T. saginata),

• by swallowing undercooked/raw pork containing the encysted larval stage (T. solium, T. asiatica), and

• by ingestion of food (mainly vegetables) or water contaminated with taenia eggs.

3. Epidemiology and public health importance of the parasites

The taeniosis/cysticercosis complex represents a group of zoonoses that are extremely important for public health, and are still endemic in countries of Africa, Asia, and South America (Table 1) [22, 23]. In addition to recognition as neglected food-borne zoonotic diseases in many underdeveloped regions, they are also recognized as a significant cause of economic losses in livestock production and pose a danger of spreading in developed countries.

Parasite species	Definitive (intermediate) host	Stages in humans	Stage that infects humans	Human taeniosis/HCC/NCC	Cysticercosis in animals
T. saginata	Human (Cattle)	Adult tapeworms in intestine	Larvae in undercooked beef	Prevalent in Africa, Southeast Asia, South Asia, and Latin America	Central and East Africa, East, Southeast and South Asia (absent in Japan), and Latin America; low prevalence in Europe
T. solium	Human (pigs, humans)	Adult tapeworms in intestine; Cysticercus	Larvae in undercooked pork; Eggs in food or water contaminated with human feces	Cosmopolitan, and highly prevalent in Central and South America, Western and Central Africa, Russia, India, Pakistan, China, and Southeast Asia	South America, Asia, Western and Central Africa
T. asiatica	Human (pigs, cattle, goats)	Adult tapeworms in intestine	Larvae in undercooked pork	Prevalent in Taiwan, South Korea, Indonesia, the Philippines, Thailand, China, Vietnam, Japan, and Nepal	East and Southeast Asian countries

Table 1.

Characteristics and distribution of T. saginata, T. solium and T. asiatica.

3.1 Epidemiology of T. solium

Estimates are that millions of people worldwide are infected with T. solium, a tapeworm with more important clinical significance than the other two taenia species. In addition, infections with T. solium have greater importance in economically undeveloped countries with poor sanitary conditions, practices of inappropriate cooking and meat processing, extensive pig farming, and low awareness about taeniosis and cysticercosis.

Taeniosis and cysticercosis are endemic in the Andean region of South America, Brazil, Central America, and Mexico; China, the Indian subcontinent, Southeast Asia; and sub-Saharan Africa (Figure 1) [25]. In non-endemic countries, that is, many European countries, the USA, Canada, and Australia, reporting of HCC is due to increased consumption of pork, travel, and an increased flow of immigrants [26, 27].

Figure 1.

Worldwide distribution of T. solium infection in 2022 [24].

Epidemiological studies estimate 2.56 million human taeniosis cases worldwide and 8.3 cases of cysticercosis [28, 29, 30, 31], including at least 400,000 symptomatic cases in South America [32], 1.5–3 million cases in sub-Saharan Africa [29], and 3–7 million cases of HCC in China [32]. Prevalence figures vary in these countries but are usually less than 1:1000 for taeniosis, 1–10% for HCC (undifferentiated cysticercosis and neurocysticercosis), and up to 20–40% for porcine cysticercosis. Estimated seroprevalences are; for T. solium in Africa 17.3%, South America 13%, and Asia 15.6% [26]. Children get NCC less often than adults, probably due to a shorter exposure time and/or a different immune response. Likewise, there is no significant differences in the prevalence of HCC between genders or different genetic predispositions in humans.

In most African countries where pigs are raised extensively, cysticercosis caused by T. solium is extremely widespread. In the previous decades, this zoonosis in Africa receives more attention due to the recognition of the importance of NCC in the etiology of epilepsy. Likewise, data from West and Central Africa suggest that human cysticercosis often does not reflect a true picture of the situation, in contrast to reported prevalences of porcine cysticercosis. Regions of hyperendemicity are in Africa [33] where a high prevalence of cysticercosis in pigs is accompanied by frequent infections with T. solium in humans (HCC/NCC). In West Africa, cysticercosis caused by T. solium in pigs and humans is reported in Benin, Zambia, Cameroon, Burkina-Faso, Ghana, Côte d’Ivoire, Senegal, and Togo. Although official data are lacking, T. solium is probably present in a number of other West African countries [34]. In Central African countries, pig and human cysticercosis are (hyper) endemic in Rwanda, Burundi, the Democratic Republic of Congo, Cameroon, and Chad [34]. Epidemiological studies carried out in Togo and Benin revealed that the prevalence of HCC in Togo was 2.4% and 1.3% in Benin. In some regions of Nigeria, the prevalence of porcine cysticercosis was 20.5%, while the prevalence of taeniosis 8.6%. However, it is surprising that not a single case of HCC/NCC is reported, although epilepsy is very common. Epidemiological data on HCC clearly indicate that, with the exception of predominantly Muslim countries in North Africa, cysticercosis caused by T. solium is endemic in all regions of Africa [35]. Thus, cysticercosis is probably one of the main causes of epilepsy in Cameroon with an incidence rate of as much as 44.6% [36, 37]. Although there is a significant association between cysticercosis and acquired epilepsy in Africa, research on this topic is lacking [35].

In Eastern and Southern African countries, T. solium is a serious public health and agricultural problem [38, 39]. Based on available information, annual losses due to cysticercosis in pigs in 10 West and Central African countries amount to around 25 million euros. The financial losses caused by HCC are very difficult to estimate, but they certainly exceeded burden of diseases on the animal side. Because NCC is an important cause of epilepsy, complex treatment dramatically increases the burden of the disease due to the social stigma and discrimination that accompanies the condition. The actual prevalence of cysticercosis caused by T. solium in pigs and humans in Central and West Africa is still underestimated due to unreliable data and lack of awareness and diagnostic capacity.

Available data from South America indicate a very significant risk of infection with T. solium in humans, although prevalence rates vary from country to country. For example, studies in Honduras, Peru, Mexico, and Guatemala reveal neurological symptoms of NCC in rural populations in 9–18% of residents [40]. Mexico is one of the countries with the highest prevalence of the disease, ranging from 0.2 to 3.4%. NCC in humans in Mexico has often been confirmed post-mortem as the cause of 4–13% of deaths. The reported prevalence of cysticercosis in pigs in Mexico, determined in slaughterhouses, is 0.2%, which is extremely low and does not represent a realistic estimate, as there are a large number of unconfirmed cases [40]. Data on the epidemiology of cysticercosis in most South American countries are unreliable due to a lack of official disease reporting and databases.

Fewer hospitalizations due to cysticercosis were reported in Brazil, Ecuador, and Mexico, as well as reductions in mortality rates in Brazil and in ambulatory cases care in Mexico. Data available in Ecuador compile all forms of cysticercosis, while data on HCC and NCC from Brazil and Mexico allow us to determine that NCC accounts for approximately 90% of all recorded cases of cysticercosis. Thus, the trend of confirmation of cysticercosis in pigs results in higher confirmation of NCC in humans. The trend of NCC burden in Colombia increased significantly between 2009 and 2019 [41]. Serological surveys of HCC and NCC conducted in Colombia from 2008 to 2010 showed high human exposure to T. solium [41].

The trend of increasing seropositivity with age is not surprising given that T. solium antibodies probably persist for several years. Seropositivity may be an indicator of lifetime prior exposure. In Colombia, T. solium antibodies were confirmed more in women than men. This data is consistent with the results of numerous other studies conducted in South America [42, 43, 44, 45]. In contrast, in other endemic areas, such as sub-Saharan Africa, males are associated with an increased risk of exposure and higher antibody positivity [46].

Due to human migration, HCC and NCC are also reported in developed countries, such as the USA, where HCC is predominantly an imported disease with a high prevalence in immigrants [47, 48]. In Western Europe, cysticercosis was under control during the last century, but with a significant increase in connection with immigration. Imported human cases are reported from 1990 to the present in all countries except Iceland [49]. Most of the cases are confirmed in Portugal and Spain, but suspected indigenous cases are rare. Simultaneously, cases of cysticercosis in pigs are sporadically reported [50, 51]. In Eastern European countries, the prevalence of cysticercosis exceeds the occurrence in Western Europe. Cases of infection are confirmed in 15 out of 22 countries with the largest number of diagnoses in Romania and Serbia, considered as autochthonous cases [49]. In cases of taeniosis, species identification was not performed [49].

In Asia, taeniosis/cysticercosis has been occurring for several hundred years, but until recently has not received much attention. Consequently, epidemiological data for some areas of the continent do not exist. Data on taeniosis are more available than on cysticercosis [52]. Taeniosis and cysticercosis caused by T. solium are common in Bali and Indonesia [53]. In the serological survey in Bali, 21% of people were positive for cysticercosis [54]. Taeniosis is widespread especially among the non-Muslim population, although it is not always certain which species of Taenia is a cause. Cysticercosis is confirmed in India, especially in the north [55]. NCC is confirmed in 50% of patients with epileptic seizures in India. Infections with T. solium are reported in Thailand [56], South Korea [57], Taiwan [58], and Nepal [59]. In Nepal, a surprisingly high rate of taeniosis of 50% is found in areas with extensive pig farming. In China, the average prevalence of T. solium taeniosis in the investigated regions ranged from 0.05 to 15% [59]. In endemic areas, pig cysticercosis prevalence varied from 0.4 to 15%, and occasionally up to 40%.

3.2 Epidemiology of T. saginata

T. saginata has a global distribution; however, the taeniosis it causes is of particular importance in Africa, South America, and Asia [60, 61]. In contrast to T. solium, it is considered that T. saginata represents a less serious public health problem because this taeniosis rarely leads to serious clinical signs and symptoms in humans. T. saginataalso leads to significant economic losses, especially in livestock production, and represents a serious problem when it comes to food safety.

Ingestion of T. saginata eggs cannot cause cysticercosis in humans, and the public health impact of this parasite is limited to intestinal infection (taeniosis). A risk factor for taeniosis caused by T. saginata in humans is the consumption of raw or undercooked beef. According to the prevalence of T. saginata an area can fall into one of three categories: (i) highly endemic areas with a prevalence exceeding 10%; (ii) areas with moderate prevalence; and (iii) regions with a prevalence below 0.1% or free of infection. Highly endemic areas include the Central and East African countries (Ethiopia, Kenya, and the Democratic Republic of the Congo) [62]. Endemic areas appear in the Caucasus, Turkey, Iran, Central Asian regions (Figure 2), and in the Mediterranean (Syria, Lebanon, and the countries of the former Yugoslavia). The prevalence of taeniosis in humans and cysticercosis in cattle is particularly high in Africa, South America, and some parts of Asia [64].

Figure 2.

Prevalence of human taeniosis in central and western Asia and the Caucasus [63].

Research on the prevalence of T. saginata in Asia indicates the highest occurrence in the Philippines (33.7%), Pakistan (7%), Vietnam (5.8%), Indonesia (4.6%), Nepal (4.3%), and India (3.8%). In highly endemic regions, for example, Ethiopia, Bali, and Tibet, the prevalence of taeniosis is 22–27%. Cases of taeniosis are reported in Angola, Ethiopia, Kenya, Madagascar, Malawi, South Africa, Tanzania, Uganda, Zambia, and Zimbabwe. In Sichuan and Yunnan provinces of southwestern China, Bali, and Indonesia, raw beef is a delicacy. Consequently, in these rural areas, the prevalence of taeniosis in humans is higher than 20% [65].

T. saginata infections in North America are rare, except in cases where livestock and humans live in close proximity and where poor sanitation prevails. The prevalence of T. saginata (under 0.5%) is low in the USA, Canada, Australia, South America, and some countries of the western Pacific, but is slightly higher in Central America [66]. In Europe, infection with T. saginata is still endemic in some regions, although the prevalence is low (usually <0.05%) [61].

Taeniosis/cysticercosis caused by T. saginata is largely considered a neglected disease in southern and eastern Africa. The reason is low confirmation of infection in cattle, lack of data on the impact of the infection on livestock production and economy, and viewing the disease in humans as a minor health problem. Nevertheless, the presence of cysticercosis in cattle is a clear indicator of inadequate sanitary conditions, inadequate meat inspection and human habits that may favor transmission.

The prevalence of cysticercosis in cattle relates to the prevalence of taeniosis in humans. Prevalence in cattle varies from very low (0.03%) in North America and Europe, to very high in Africa and South America (10%–80%) [61, 66]. Cattle cysticercosis in Eastern Europe is generally more frequent than in Western Europe [67]. Information on the prevalence of cysticercosis in cattle in African countries is quite limited, but a very high prevalence of up to 80% is reported (Ethiopia, Botswana, and Nigeria). In Asia, information is also scarce, in general, Japan is considered free of autochthonous bovine cysticercosis based on meat inspection results [68], very high prevalences are reported in various parts of Korea and 2.2% in Indonesia [69]. In contrast, the prevalence is very low in India [70] and the Philippines [71].

3.3 Epidemiology of T. asiatica

T. asiatica is overlooked in the context of its impact on the global distribution of taeniosis/cysticercosis in humans. We assume that there are two reasons for the above; the first is the supposedly non-cosmopolitan character of the tapeworm and the second is the close molecular similarity to T. saginata, suggesting that T. asiatica probably does not cause HCC since T. saginata eggs are not infectious to humans. However, T. saginata does not cause cysticercosis in pigs, while T. asiatica does.

T. asiatica was described in 1993 as a new species of tapeworm that infects humans [6]. Previously, its occurrence in rural communities in Southeast Asia was attributed to T. saginata which is morphologically very similar but described in patients who ate raw pork liver but not beef [72]. Currently, there is no specific immunodiagnostic method to confirm T. asiatica, and molecular techniques (the only tool for distinguishing between the 3 Taenia species) are not used in routine diagnostics. Hence, the geographic distribution of T. asiatica and its ability to cause HCC remain open questions. T. asiatica is confirmed in Asia (Korea, China, Japan, Taiwan, Indonesia, Thailand, Nepal, Vietnam, the Philippines, Cambodia, and Myanmar) [72]. In a study conducted in Thailand, all three species of Taenia appeared in communities where undercooked pork and beef were consumed, and at least one dual infection with adult tapeworms T. solium and T. asiatica was confirmed by DNA analysis. In many countries of East, Southeast, and South Asia, which are rich in cultural, ethnic, and religious diversity, all three types of Taenia coexist.

4. Meat inspection changes in monitoring of cysticercosis

Bovine cysticercosis and porcine cysticercosis are common parasitic infections of mainly skeletal muscles of bovines and swine by larval stages (cysticerci) of the two large tapeworms T. saginata (beef tapeworm) and T. solium (pork tapeworm). Human taeniosis occurs as a zoonotic consequence of consumption of raw or under-cooked meat contaminated by viable larvae of T. saginata (C. bovis) and T. solium (C. cellulosae) and further development of their adult forms in human intestines. T. asiatica was also described as the new taenia species that parasitize in humans as definitive hosts [6], which geographical distribution is limited to Asia [72]. In addition, unlike T. saginata and T. solium, this tapeworm infects pigs, cattle, goats, and certain monkey species as intermediate hosts, in which cysticerci are predominantly located in liver [73]. T. asiatica is not considered to cause human cysticercosis [74]. Other Taenia spp., such as T. multiceps, that parasitize in domestic and wild animals, do not normally invade humans, although cases of coenurosis (infection of the brain, spinal cord, and eyes with Coenurus cerebralis as the larval stage of T. multiceps) have been reported in humans [75, 76]. Human cysticercosis or neurocysticercosis is another zoonotic form of food-borne infection by T. solium, which occurs as a life-threatening illness subsequently to invasion of the central nervous system by C. cellulosae. Human cysticercosis is considered as the most dominant helminthic infection of the nervous system and a major global cause of acquired epilepsy [77, 78]. The diseases caused by T. saginata and T. solium are worldwide reported, with estimates on their occurrence ranging regionally, as well from country to country. As for Bosnia and Herzegovina, the available data are scarce and limited, but cases of human and bovine cysticercosis were reported [79].

Due to the zoonotic potential, bovine, porcine and other forms of animal cysticercosis are notifiable to the World Organization for Animal Health [80]. As for the European Union (EU), monitoring of cysticercosis in the EU Member States (MS) becomes compulsory depending on the epidemiological situation, as regulated by List B of Annex I of the Directive 2003/99/EC [81]. Based on the monitoring data, each MS must evaluate the trends and sources of zoonoses, zoonotic agents, and antimicrobial resistance in their territory and send annual national reports to the European Commission. Each year the national reports from all MS are evaluated and published by European Food Safety Authority (EFSA) as the EU Summary Report on the trends and sources of zoonoses, zoonotic agents, and antimicrobial resistance in the EU. Since 2019, the annual EU Summary Reports on zoonoses, zoonotic agents and foodborne outbreaks have been renamed the “EU One Health Zoonoses Summary Report” (EUOHZ), which is co-authored by EFSA and European Centre for Disease Prevention and Control. The latest published EUOHZ report for 2021 [82] included very scarce data on Cysticercus spp. in several animal host species from only eight MS. Frequency of cysticerci detected in bovine carcasses at slaughterhouses was 0.271% (74 positive out of the 27,326 inspected) in Luxembourg, 0.111% in Belgium (857 positive out of the 770,235 inspected), 0.009% in Slovakia (3 positive out of 34,771) and Slovenia (11 positive out of 123,961), 0.005% in Spain (125 out of 2,332,666), while Sweden reported only one positive out of 411,650 inspected cattle carcasses. As for inspected pork, cysticerci were found in 0.001% (7 positive out of 675,234 checked) and in 0.007% (2902 positive out of 41,059,466 inspected) pig carcasses in Slovakia and Spain, respectively. Spain also detected cysticerci in 33 of 111,100 wild boars (0.03%), 17,332 out of 799,767 goats (2.18%), 200,810 out of 7,077,050 sheep (2.84%), and in 110 out of 4544 inspected solipeds (2.42%). Moreover, cysticerci were not detected in 2,200,672 cattle, pig and wild boar carcasses inspected in Finland, in 65,334 cattle, pig, sheep or goat carcasses collected in Malta, or in 7415 mouflons and 118,899 deer inspected in Spain [82].

The existing problem of low reporting data on cysticercosis in EU has been previously recognized and evaluated by the EFSA Panel on Biological Hazard [83] and other scientific report submitted to EFSA [84], where it has been generally assumed that cysticercosis is more frequent in animal and human populations in the EU, with very low sensitivity of slaughterhouse inspection recognized as the main reason for underreporting of cysticercosis.

The major constraint with regard to monitoring of cysticercosis is the lack of a “gold-standard” reference diagnostic test that would solely ensure a high level of confidence in detecting the disease, particularly in animals with low parasite burdens [85]. Monitoring of cysticercosis is performed by post-mortem meat inspection at the slaughterhouse. Meat inspection by visual inspection, palpation and incision of appropriate organs was originally introduced at the end of nineteenth century by Robert Ostertag [86, 87]. In Bosnia and Herzegovina, post-mortem meat inspection is currently imposed by specific national regulation [88], which is completely harmonized with Regulation (EC) No 854/2004 [89], imposing mandatory visual inspection of all surfaces of each carcass of slaughtered animals by the official veterinarian. In addition, the official veterinarian may require carcasses of bovine animals over 6 months old, and domestic swine over 4 weeks old to be submitted for post-mortem inspection split lengthways into half carcasses down the spinal column. Furthermore, if the inspection so necessitates, the official veterinarian may also require any head or any carcass to be split lengthwise. Also, specific examinations such as palpation and incision of parts of the carcasses (such as predilection locations for cysticerci; tongue, esophagus, diaphragm, internal and external masseters, pericardium and heart), offal and laboratory tests, must be carried out to, among other reasons, detect the presence of a zoonotic disease such as cysticercosis. Also, requirements for systematic visual inspection, palpation, and incisions of carcasses from bovines under and above 6 weeks old, and for domestic swine carcasses are specified as well. In addition to the specified post-mortem meat inspection procedures as the minimum requirements for the examination for cysticercosis in bovine animals over 6 weeks old and swine, the use of specific serological tests is also allowed. In the case of bovines over 6 weeks old, incision of the masseters at post-mortem inspection is not compulsory when a specific serological test is used, as well as when bovine animals over 6 weeks old have been raised on a holding officially certified to be free of cysticercosis. Finally, it is stated that carcasses infected with cysticerci must be declared as unfit for human consumption and condemned. However, when the animal is not generally infected with cysticerci, the uninfected parts may be declared as fit for human consumption after having undergone a cold treatment [90], such as kept at temperatures below −10°C minimally for 2 weeks or at −7°C for at least 3 weeks [91].

Diagnostic sensitivity of the post-mortem visual inspection lower than 30% (or reduced to 1% for very low parasite burden and localized infections) and its questionable specificity triggered by possible misdiagnosis are known, which results in low official reporting and underestimated prevalence of cysticercosis [92]. Also, the effectiveness of visual inspection, incision and palpation in detecting cysticercosis-positive carcasses greatly rely on the level of training, experience, and skills of official veterinarians, which makes the post-mortem meat inspection very subjective, time-demanding, and laborious and results in absence of proficiency scheme, ring trials and standardization of the method [86, 92], and in the lack of a proficiency scheme or ring trials. In addition to evident financial costs and losses due to cysticercosis and taeniosis [92], these are the main reasons that alternative diagnostic techniques have been studied to be introduced in meat inspection procedures and improve diagnostics of cysticercosis.

Mostly deficient and unspecific clinical manifestation of the disease in bovines and swine reflects in overall ineffectiveness to screen cysticercosis in animals during the ante-mortem inspection. Bovine cysticercosis does not cause clinically apparent symptoms in infected animals, except for ones with observed multi-organ infestation with C. bovis. Gholami et al. [93] described obvious symptoms, such as different degrees of lethargy, dullness, unthriftiness, and reluctance to move in feedlot cattle in Iran, in which post-mortem inspection showed multi-organ infection with the cysticerci, such as heart, tongue muscle, masticatory muscle, lungs, and liver. The authors reported that the most and least invaded organs were heart (100%) and liver (14.28%), respectively. On the other hand, clinical manifestation of porcine cysticercosis largely depends on localization of C. cellulosae in infected pigs, which is primarily in muscle tissue and the brain [94]. Predilection of the cysticerci for the brain of infected pigs may trigger disorders of the central nervous system as dominant clinical manifestations of porcine neurocysticercosis. Trevisan et al. [95] reported that clinical signs of porcine neurocysticercosis included severe seizures with stereotyping walking in circles, chewing motions, foamy salivation, and ear stiffening, accompanied with tonic muscle contractions followed by a generalized rapid loss of muscular function and collapse of the animal. Even though the authors reported a significant positive association between seizures and age of the animals (p < 0.001), they observed the seizures in only two of 16 infected animals, while significant relations between seizures and total number, distribution and localization of cysticerci in the brain were not reported. In addition to seizures, less severe signs of porcine cysticercosis may include excessive salivation, excessive blinking and tearing, and presence of subconjunctival nodule [96], as well as dullness, sluggishness, somnolence, apathy, and loss of consciousness [97, 98].

Unlike irregular and non-pathognomonic neurological manifestations of porcine cysticercosis, localization of C. cellulosae in tongue muscular tissue was the rationale for antemortem lingual palpation (tongue inspection) as a rapid and inexpensive tool for pig producers, buyers, and veterinarians to screen cysticercosis in pigs [98]. Dorny et al. [99] reported that lingual palpation was 100% specific in detecting cysticercotic pigs if performed correctly by experienced persons and combined by the visual inspection of the tongue base. However, the authors estimated the overall sensitivity of tongue inspection at only 21%, which confirmed previous observations that the sensitivity of detecting cysticercosis-positive pigs solely by lingual inspection is greatly limited if the tongue is not heavily invaded with the cysts [100]. The sensitivity of tongue inspection fluctuates depending on the infection intensity and the test is suitable only in the areas where porcine cysticercosis is highly endemic [101].

Serological techniques, such as ELISA, have been widely employed to screen cysticercosis in pigs [101, 102, 103] and in bovines [104, 105, 106], where the estimated values for sensitivity and specificity of the applied tests varied greatly. Chembensofu et al. [103] evaluated the performance of circulating antigen detection (Ag-ELISA) against full carcass dissection as the gold standard method in detecting naturally T. solium-infected pigs in Zambia. The authors reported the Ag-ELISA specificity and sensitivity in detecting infected carcasses to be 67% and 68%, respectively, and increasing to 90 and 100% for the detection of carcasses with one or more viable cysticerci, and more than 10 viable cysts, respectively. Using a similar approach, Kabulu et al. [101] estimated Ag-ELISA sensitivity and specificity in detecting T. solium cysticerci in naturally infected pigs in Tanzania to be 82.7% and 86.3%, respectively, and concluded that the Ag-ELISA test used in the study is more reliable in ruling out T. solium cysticercosis in pigs, than in confirming it, since the positive and negative predictive values of the test were 35.2% and 98.2%, respectively. Using an Ag-ELISA test to estimate the prevalence of bovine cysticercosis, Dorny et al. [104] examined 1164 serum samples of cattle slaughtered in Belgium and detected 3.09% cysticercosis-positive serum samples, while the routine post-mortem meat inspection of the same cattle detected the disease only in 0.26% carcasses, which underlines very low sensitivity as the most important disadvantage of the routine meat inspection in detecting cysticercosis. Eichenberger et al. [106] assessed diagnostic values of various ELISA tests and the EU mandatory antemortem visual meat inspection for detecting T. saginata cysticercosis in 793 dairy cows slaughtered in three EU-approved slaughterhouses in Switzerland. In the absence of the “gold-standard” reference diagnostic test, the results of the mandatory meat inspection test and four ELISA tests were further analyzed by use of Bayesian inference. The reported Bayesian estimates of the ELISA tests sensitivity ranged from 14.3% (95% CI: 8.7–21.5) for monoclonal Ab-ELISA to 81.6% (95% CI: 70.1–92.0) for T. saginata metacestode excretory/secretory antigen ELISA, while the reported specificity values were between 84.7% (95% CI: 81.6–87.6) for commercial synthesized purified peptide ELISA and 96.3% (95% CI: 93.5–99.0) for T. saginata metacestode excretory/secretory antigen ELISA. Sensitivity of the EU routine visual meat inspection was very low, estimated at 15.6% (95% CI: 10.0–23.3), with assumed specificity of 100 [106].

Obviously, the low sensitivity and specificity of the EU mandatory routine visual meat inspection in detecting cysticercosis at slaughterhouses by can be enhanced by combining it with ELISA testing. However, some properties of the ELISA techniques, such as lack of officially registered and commercially available tests for bovine cysticercosis [84] and requirement to be performed by a specialized laboratory [92], make serological techniques unsuitable for routine use to detect cysticercosis in cattle and pigs. In addition, introduction of serological tests for monitoring cysticercosis in animals would greatly increase overall costs related to the disease monitoring. As projected by Jansen et al. [92], employment of an Ag-ELISA test (with estimated sensitivity of 36.37% and specificity of 99.36%) at cattle slaughter would greatly reduce the estimated prevalence of bovine cysticercosis in Belgium from 42.5 to 0.6%. However, such an improvement would generate economic losses for the cattle owners up to 21 million EUR and 10 million EUR for the slaughterhouses just in the first year after implementing the Ag-ELISA, which are enormous increases in financial damages if compared to estimated annual loss of 3.5 million EUR and 200,000 EUR without the test, respectively. Other analytical methods used to for the monitoring and reporting Cysticercus in animals and foodstuffs in the EU, such as the parasite taxonomic identification, histopathology, and molecular (DNA) methods were found to be deficient in estimates of their sensitivity and/or specificity, and characterized with lower diagnostic throughput and higher estimated costs when compared to the routine meat inspection and ELISA methods and require specialized diagnostic facilities [84], which has not resulted in routine use of serological methods as an alternative to visual meat inspection [91].

Evidently, meat inspection based on the post-mortem visual inspection, palpation, and incision of carcasses with proven low sensitivity and substantial financial burden need to be advanced toward the risk-based meat safety assurance system in order to provide a better public health protection from meat-borne diseases, as suggested by EFSA [107, 108, 109]. To enable MS to perform risk analysis essential for risk categorization of animals and an effective implementation of risk-based meat inspection, EFSA proposed Harmonized Epidemiological Indicators (HEIs) for all meat-producing animal species, including pigs [110] and bovines [111]. The proposed HEIs include, among others, prevalence of hazards in animals or meat at different stages of the food production chain, and other criteria, such as animal hygiene indicators or visible carcass contamination. To be measurable against objective criteria and to achieve an acceptable level, each HEI is defined in terms of respective food production stage, analytical/diagnostic method, and required specimens, if applicable. Such an effort and contribution of EFSA resulted in adoption of the current EU meat inspection legislation [112, 113, 114, 115]. The main drive for the change in EU legislation has been to boost quality improvement and better use of data collected along the integrated food production chain (Food Chain Information—FCI), which are of pivotal importance for establishing reliable HEIs and consequent risk analysis and risk categorization of animal herds. This should enable the shift from the traditional meat inspection approach to the current risk-based meat safety assurance system in which meat of low risk-animals is visual-only inspected (VOI), while meat of high-risk animals is subject to palpation and/or incision [116]. The VOI approach was initiated by the Regulation (EC) No 854/2004 [89] for indoor-raised finisher pigs, while the current Regulation (EU) No 218/2014 [112] allows VOI for all low-risk pigs. As for bovine carcasses, VOI is legalized by the EU Regulation No 2019/627 [115], since the regulation recognizes the actual risks of cysticerci in various cattle categories, which should enable reduction of manual inspection of the carcasses. However, as recognized by Blagojevic et al. [117], a full benefit from legal introduction of VOI approach has not yet been fully achieved, since reduced incisions cause a further decrease in already low sensitivity of traditional meat inspection in detecting bovine cysticercosis, and the additional costs of alternative serological testing hinder its utilization. Challenges and opportunities in the implementation of the new risk-based meat inspection system were recently studied by Antunovic et al. [116]. The authors identified existing trade agreements with third countries, costs of implementation, and inadequate FCI and resistance from meat inspectors as the most frequent obstacles to implementing the new meat inspection systems. In addition, the stakeholders are more confident in the new systems than in the traditional system, while reduced or equal inspection workload compared to the traditional system was observed.

Therefore, further research and expand of means of employing FCI and HEIs are crucial to reach better risk categorization of and enhanced implementation of risk-based meat safety assurance system which should consequently reduce the workload of veterinary inspection, decrease the related costs for the whole meat industry, improve sensitivity of detecting meat-borne hazards and enhance overall public health protection.

5. Conclusion

The high prevalence of taeniosis and cysticercosis is a reflection of poor sanitary conditions, which are below standards and poor food safety measures. Therefore, in endemic areas there is a need to improve local surveillance, sanitary conditions, diagnostics and the regulatory system.