Introductory Chapter: Taeniasis and Cysticercosis/Neurocysticercosis – Differences, Risk Factors, and Vaccines

1. Introduction

Humans are known hosts for two well-known Taenia species: Taenia saginata (the cattle tapeworm) and Taenia solium (the pig tapeworm). Taenia asiatica, a third species that shares traits with the other two because its adult morphology resembles that of T. saginata, and its life cycle corresponds to that of T. solium, was identified in the 1990s. Cysticercosis is caused by the T. solium and T. saginata larva (cysticercus) and manifests itself in the host’s internal organs, pigs and cattle, respectively; neurocysticercosis (NCC) results from T. solium cysticercus infection of the host’s central nervous system, namely humans with larval accidental infection [1].

2. Taenia life cycles

Figure 1 depicts the human Taenia spp. life cycle. T. asiatica and T. solium use the pig as an intermediate host (IH), while Taenia saginata uses cattle as an IH. In the small intestine of intermediate hosts, the enveloping structures of taeniid eggs undergo digestion. Subsequently, the oncospheres enter the host’s circulation, eventually navigating to their intended target organs via the intestinal membrane. When humans accidentally consume these eggs, namely those of T. solium, they can encyst in various tissues (cysticercosis), with a particular affinity for the brain, resulting in NCC. The clinical features of NCC vary depending on the parasites’ location, quantity, maturation, regression phases, and the host’s immunological response.

Figure 1.

T. saginata, T. asiatica, and T. solium life cycles.

The scolex of the parasite will evaginate and attach to the mucosa of the duodenum-jejunum if an individual eats uncooked or semi-cooked pork or beef with live cysticerci. Gravid proglottids are passed naturally or via bowel movements 8–12 weeks after infection. Eggs consumed by pigs or cattle are broken down into their embryophoric structures, and the oncospheral membrane is digested by bile and enzymes. It takes around 12 weeks for cysticerci to develop in a pig’s skeletal muscle, heart muscle, and brain. These cysticerci will continue reproducing until the pigs are slaughtered for at least a year. T. saginata cysticercus has a limited life history, as shown by the calcification of its cysticerci in mature cattle. The cysticerci of T. saginata and T. asiatica vary primarily because the former are musculotropic in cattle (especially in the liver), while the latter are viscerotropic in pigs. About 8–10 weeks after infection, metacestodes from cattle and swine become infectious to humans. Eggs from infected T. solium adults may spread the disease to humans when ingested via the fecal-oral pathway (Table 1).

Morphological features	T. solium	T. saginata	T. asiatica
Mature proglottid
Testis (number)	375–575	800–1200	324–1216
Ovary (number of lobes)	3	2	2
Vaginal sphincter	—	+	+
Gravid proglottid
Uterine branches (each side number)	7–16	14–32	11–31
Pattern of uterine branching	Dendritic	Dichotomous	Dichotomous
Posterior protuberance	—	+	+
Size (length × width; mm)	3.1–10 × 3.8–8.7	10–20 × 6.5–9.5, longer than wide	4–22 × 3–12
Scolex
Shape	Globular	Quadrilateral	Quadrilateral
Rostellum	+	—	+
Number of hooks	22–32	—	—
Diameter (mm)	0.6–1.0	1.5–2.0	0.8
Adult tapeworm
Length (m)	1–5	4–12	1–8
Number of proglottids	700–1000	1000–1500	200–1200
Oncosphere
Tissue tropism	Musculotropism and neurotropism	Musculotropism	Viscerotropism
Cysticercosis/neurocysticercosis	Cysticercus cellulosae in pork	Metacestode, Cysticercus bovis in cattle	Metacestode, Cysticercus viscerotropica in pig
Cysticercus
Size (mm)	5–8 × 3–6	6–10 × 4–6	2 × 2
Hooks in scolex	+	—	Rudimentary
Genomic features
Assembly size (Mb)	131	169	168
GC content (%)	43.5	43.5	43.2
Coding gene number	11,902	13,161	13,323
Average gene length (Kb)	4.6	6.0	5.9
Protein length (aa)	444	464	466
Gene density (genes per Mb)	90.9	77.9	79.3
No. of exons/gene	6.6	6.2	6.2
Exon mean length (bp)	237	237	244
Intron no./gene	5.6	5.2	5.2
Intron mean length (bp)	775	864	831
Exon GC content (%)	50.2	49.7	49.6
Intron GC content (%)	40.8	41.5	41.2
Repeat content (%)	18.1	10.4	10.9
tRNA number	162	339	353

Table 1.

T. saginata, T. asiatica, and T. solium morphological and genetic differences [2, 3, 4].

+ Present; − absent.

3. Taenia egg survival and dispersal

Taeniid eggs can survive for up to a year in moderate temperatures and are commonly found on vegetables, soil, and water samples, posing a risk to consumers. Invertebrates may serve as transport hosts for taeniid eggs, and wastewater treatment systems are not completely effective in removing them, making access to surface water and using sewage sludge as pasture fertilizer significant risk factors for bovine cysticercosis [5, 6]. However, flies and dung beetles play no significant role in transmitting T. solium to pigs, and corralling reduces but does not eliminate the infection risk with cysticercosis (Figure 2). Other mechanisms of egg dispersal should be evaluated for a better understanding of transmission dynamics [8].

Figure 2.

Taeniid eggs in a variety of environmental matrices [7].

4. Risk factors for bovine cysticercosis (BCC)

Bovine cysticercosis is a disease that affects cattle and is caused by a parasite called T. saginata. Identified risk factors include herd/farm-related, feed-related, and animal-related factors. Age and gender of animals are correlated with the occurrence of bovine cysticercosis. Environmental contamination is the main cause of BCC cases (Figure 3).

Figure 3.

Risk factors for bovine cysticercosis [9, 10, 11, 12, 13].

5. Risk factors for porcine cysticercosis

Pigs may get infected with T. solium or T. asiatica if they consume eggs shed by human tapeworm carriers. Although both parasites harm humans, only T. solium causes neurocysticercosis, a serious public health problem worldwide. Furthermore, both parasites have an economic influence on the livestock sector. T. solium and T. asiatica have the same transmission paths from humans to pigs and back. Site transmission may therefore be addressed using comparable intervention strategies. Cysticercosis can be caused by T. solium in both humans and pigs. The major cysticercosis risk factor is the presence of adult T. solium in human carriers. The main risk factor for humans getting adult T. solium is the inclusion of contaminated pork in the food chain. Free-range pig rearing and the absence or incorrect use of latrines are other T. solium cysticercosis risk factors in pigs. These risk factors are prevalent in many low-income Latin American, Asian, and sub-Saharan African countries. Increased age, feedstuff, and dirt floors have also been identified as T. solium cysticercosis risk factors in pigs [14, 15, 16, 17, 18]. In endemic areas with improper use or a lack of latrines, causing public defecation, roaming pigs are more likely to contract T. solium cysticercosis. Low-income endemic regions with free-roaming pigs, indiscriminate feces contamination, and poor personal and meat hygiene, inadequate or nonexistent meat inspection, are particularly susceptible to T. solium infection. These risk factors are strongly associated with illiteracy, choices in life, and poverty. In addition, milder infections are typically brought on by indirect transmission, while heavier infections are typically brought on by infective egg direct ingestion produced by Taenia carriers. Although we emphasize the seriousness of severe infections, we propose that moderate infections pose a hidden risk and a distinct public health concern because it is more possible that both pre- and postmortem examinations will miss them, allowing them to enter the food chain and pose a public health risk [19].

6. Risk factors for human taeniasis and cysticercosis

One of the risk factors is eating undercooked pork, which can contain the larvae of the tapeworms. Another risk factor is living in a household with infected pigs. Pigs can act as intermediate hosts for the tapeworms, and their meat can be contaminated with the larvae. In addition, humans can shed tapeworm eggs in their feces, which can contaminate the environment and infect both pigs and humans. The risk of infection is higher in females aged 10–39 years, although the reasons for this are not clear. It could be due to differences in dietary habits, hygiene practices, or hormonal factors. The presence of Taenia carriers in the household is also a risk factor. These are individuals who are infected with tapeworms and can shed their eggs in their feces, contaminating the environment and infecting others. Seropositivity for anti-cysticercus antibodies is a risk factor. This means that the person has been exposed to the tapeworm larvae and has developed an immune response against them. Seropositivity can be detected through blood tests and indicates past or current infection [20, 21, 22, 23, 24]. Risk factors for porcine cysticercosis include a human Taenia carrier existence, the absence of a latrine, a free-range backyard or roaming pigs, and a seropositive pig with a Taenia carrier nearby. However, human cysticercosis outbreaks have also been reported in urban areas of endemic nations. T. solium transmission occurs primarily in rural areas of underdeveloped nations with significant pig ownership, but human cysticercosis outbreaks have also been reported in urban areas of endemic nations [25, 26].

7. Livestock cysticercosis vaccinations

Researchers have developed subunit vaccines against echinococcosis and cysticercosis based on ovine and bovine protective immune responses after egg challenge or immunization with taeniid oncosphere antigen extracts. In 1989, the first recombinant subunit anti-parasite vaccine (To45W) was generated to fight Taenia ovis infections, a nonzoonotic metacestode disease of economic relevance in sheep. Bovine cysticercosis-causing T. saginata was found to contain homologous genes, and when the produced peptides (TSA-9/TSA-18) were administered intramuscularly to calves with adjuvant, 99% protection was seen against oral challenge with T. saginata eggs. This means that the vaccination effectively protected the calves from the disease caused by T. saginata. Further efforts have been focused on scaling up the manufacturing of ovine and bovine cysticercosis vaccines so that sufficient quantities and quality-controlled vaccinations are accessible for practical usage. Pigs were also protected against experimental egg challenge infection by a T. solium recombinant subunit oncosphere vaccine (TSOL18) for cysticercosis, the most efficient protective vaccination in pigs against T. solium cysticercosis [27]. The researchers have focused on scaling up the manufacturing of both vaccines to make them more accessible for practical usage. The study found that pigs were protected against experimental egg challenge infection by a T. solium recombinant subunit oncosphere vaccine (TSOL18) for cysticercosis. TSOL18 is the most efficient protective vaccination in pigs against T. solium cysticercosis, which makes it a promising candidate for further studies and inclusion in T. solium control programs [28, 29, 30]. In mice, the expression and immunogenicity of the codon-optimized TSOL18 gene were much higher than those of the un-optimized gene. These findings provide the groundwork for developing an improved TSOL18 gene vaccination against cysticercosis [31]. The TSOL16 antigen (for ovine psoroptic mange control) might be a beneficial addition to existing swine vaccination approaches, allowing for the development of novel T. solium cysticercosis vaccine tactics [32]. With oral vaccination, the recombinant pMG36e-SP-TSOL18/Lactococcus lactis and pMG36e-TSOL18/L. lactis vaccines can trigger specific mucosal, cellular, and humoral immunity in mice. More notably, the recombinant pMG36e-SP-TSOL18/L. lactis vaccination produces a stronger immunological response, which reveals the feasibility of employing the L. lactis strain as a vehicle to carry T. solium protective antigens [33]. Although there have been discussions about the therapeutic immunization of intermediate hosts against Taenia larval cysts, it remains in its nascent phases, and more research is needed to develop effective therapies.

8. Conclusion

A standardized detection instrument is needed to understand the epidemiology of Taenia species and develop strategies for enhancing veterinary public health. Vaccinating swine with recombinant T. solium antigens and anthelmintics may reduce the risk of infection in human populations in endemic areas. Moreover, a comprehensive One Health approach, including interventions for people, pigs, and the environment, is expected to result in a stronger and longer-lasting benefit in eliminating cysticercosis.

Acknowledgments

The authors extend their appreciation to the Deanship of Scientific Research, Kind Saud University for funding Through Vice Deanship of Scientific Research Chairs, Research Chair of Vaccine against infectious Diseases.