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Trichinellosis is a meat-borne zoonotic disease caused by nematode worms of the genus Trichinella in humans. Sylvatic animals are the main reservoir hosts of this helminth but domesticated animals, mainly swine, can also acquire the infection when they are fed with scraps of game meat. The genus used to have only one species; however, it has subsequently evolved into a multispecies genus. Due to its broad host range, it has been able to establish itself in both domestic and sylvatic cycles, allowing it to maintain a vast host reservoir. Infection has been documented in a variety of experimental species, showing that it could potentially happen in natural settings as well. Due to the considerable genetic differences among the isolates, researchers predict that the number of species and genotypes discovered within Trichinella will increase. Outbreaks caused by various species in different parts of the world have also been reported therefore prevention and control are critical in order to limit the parasite’s transmission to humans. Although molecular methods are used to identify the Trichinella species but these methods are not appropriate for the diagnosis of the infection in animals.
Department of Medical Parasitology, Postgraduate Institute of Medical Research and Research, Chandigarh, India
Upninder Kaur
Department of Medical Parasitology, Postgraduate Institute of Medical Research and Research, Chandigarh, India
Rakesh Sehgal*
Department of Medical Parasitology, Postgraduate Institute of Medical Research and Research, Chandigarh, India
*Address all correspondence to: sehgalpgi@gmail.com
1. Introduction
Trichinellosis, often referred to as Trichinosis, is a meat-borne zoonotic disease, which is spread by helminths belonging to the genus Trichinella. It is caused by the consumption of raw or undercooked meat of domestic or sylvatic animals infected with the larvae of the parasite [1]. The effective establishment of this parasite in nature was due to the availability of a diverse variety of animal reservoirs. With the exception of Antarctica, they are found all over the world [2, 3]. The discovery of T. spiralis was by serendipity when James Paget in 1835 discovered the cysts in the muscles of a patient who had succumbed to tuberculosis. They were then further described by Richard Owen in the same year [4]. The establishment of a multispecies genus concept within the Trichinella genus can be attributed to the scientific findings on the biological variety of T. spiralis isolates gathered from various geographical regions and wildlife [5]. Till date ten species and three genotypes have been identified. These are further classified according to whether a collagen capsule surrounds the larvae in the host muscle, later forming a nurse cell complex [6]. The encapsulated clade consists of six Trichinella species and three genotypes, which include T. spiralis, T. nativa, T. britovi, T. murrelli, T. nelsoni, T. patagoniensis, T. chanchalensis, T6, T8 and T9, respectively. Another peculiar feature is that only mammals have been infected by them [7]. Till now only three species have been defined in the non-encapsulated clade infecting mammals along with birds or reptiles [8]. The study results of SSCP demonstrate that nonencapsulated species form a complex group that is distinguishable from encapsulated species, and support the current hypothesis that the encapsulated Trichinella group is present external to non-encapsulated forms, based on the independent biological and biochemical data sets [9]. The three non-encapsulated species revealed significant variation in four gene loci (cytochrome oxidase, P450, cyanate lyase and SB147D), indicating that they are distinct species [1]. A lot of experiments are still being carried out to determine the possible hosts of non-encapsulated species as well as their infectivity to humans, which will further widen our knowledge about them.
The life cycle of Trichinella plays an important role in its establishment in domestic as well as wildlife settings. Figure 1 represents the diagrammatic life cycle of the parasite. In many aspects, the life cycle is peculiar. To begin with, only one host serves as both the definitive and intermediate host. There are two types of cycles: domestic and sylvatic. The infection is transferred to humans in the domestic cycle by eating undercooked meat infected with the encysted larvae. The only ones who develop clinical symptoms are humans, also forming the dead end in the parasite’s life cycle. The larva is released in the intestine after the digestion of the cyst, where they disrupt the columnar epithelium and moult four times before growing into male and female worms within 30 hours. After fertilising the female, the male dies, but the viviparous female continues to produce thousands of larvae. The larvae will only encyst in striated muscles, where they will modify muscle cells to ensure their own survival, establishing a nurse cell complex. A collagen capsule is produced around the nurse cell as a result of the host immune cell reaction, with a capillary network around it for nutrition. The larva experiences a developmental halt at this point, before this it becomes infective within five weeks and calcifying after months or years according to the Trichinella species and host species. The parasite is passed on to domestic pigs, rats and boars through cannibalism and the ingestion of meat scraps. Predation and scavenging habits among wildlife species, such as those of carnivores and omnivores, are pronounced in the sylvatic cycle. Humans become infected after consuming raw undercooked meat (Table 1) [1, 9, 10].
Figure 1.
Life cycle of Trichinella species [10, 11, 12, 13]. Image from the Centers for Disease Control and Prevention Image Library.
The first species to be discovered in the non-encapsulated clade was T. pseudo spiralis andsubsequently the fourth one in the genus Trichinella. Figure 2 represents the timeline of discovery of the three non-encapsulated species. T. pseudospiralis was isolated from Procyon lotor, a raccoon caught in Krasnodar region. Significant differences were observed from the other species, which has been recorded earlier. Firstly, it can infect both mammals as well as birds, secondly, it was devoid of any collagen capsule and lastly, the adult worms and larvae had a smaller size from other species [8, 13]. It exhibits a cosmopolitan distribution in America, Asia, Australia and 20 different European countries, highlighting the importance of birds in carrying and spreading the parasite to new areas [14, 18]. The larvae of T. pseudospiralis is shown in Figure 3. In this case, the striated muscle fibres that surround the nurse cells are dense and branching longitudinally, but there is no netting pattern as seen in T. spiralis [20].
Figure 2.
Timeline of discovery of Trichinella species.
Figure 3.
T. pseudospiralis larvae in the muscle of domestic pig [19].
Since its discovery in 1972, this species has been detected in 249 animals, 237 of which were single infections and 11 of which were mixed infections with other Trichinella species. It has been discovered in 18 mammalian and eight avian species [14]. The parasite has also been detected in raccoon dogs in Germany [21, 22, 23], American mink in Poland [24], cougars from Colorado, United States [25], red foxes in Poland [26], raccoon dogs in Central Europe [27], wolverines from the Canadian north [28], Eurasian blackbird from Armenia [29], wild boars in Estonia [30], red kite from Italy [31], wolf from Central Italy [32], bobcats from Oklahoma [33]. T. pseudospiralis infection in red-eared sliders was found to be influenced by environmental temperature, as the infection was successful in turtles maintained at 38°C compared to those reared at 32°C and 28°C [32]. In order to identify the larvae, artificial digestion tests are preferred over trichinoscopy [1, 18].
Various studies have been carried out to elucidate the immune response of T. pseudospiralis. Matrix mettaloproteinases 9 and 2 have been identified as the markers for inflammatory response of both T. spiralis and T. pseudospiralis infection [33]. Infection with T. pseudospiralis also resulted in a reduction of follicular T helper cell differentiation [34]. A serpin gene, on the other hand, was discovered to play a key role in infection by activating the M2-polarised signaling pathway [35]. The parasite’s excretory-secretory proteins can be used for early detection and the development of a vaccine candidate [36].
3.2 Trichinella papuae
An examination of domestic and wild swine from Papuae New Guinea, along with eighty-three wild animals, was conducted after the detection of non-encapsulated Trichinella larvae in five domestic female swine in the settlement of Balamuk in 1988. Six wild pigs were then tested positive in the Bula Plain in the years 1988 to 1998. The larvae detected in the diaphragm muscles of pigs can be seen in Figure 4. However, none of the 83 wild animals tested, including domestic pigs, had any larvae. The larvae from one of the wild pigs were then characterised and classified by Edoardo Pozio [12]. In Western Province, near Indonesia, 8.8% of the wild pig population was shown to be infected. Intake of infected wild pig meat was the source of infection [37].
Figure 4.
In the village of Balamuk, larvae of Trichinella papuae were discovered in the diaphragm of an infected female pig (PNG), 1988 [12].
It was also found in PNG’s saltwater crocodiles and the source of infection was improper feeding of wild pigs to them [38, 39]. Varans, caimans, pythons and turtles have also been infected with T. papuae and T. zimbawensis in an experimental setting where varans were found to have the highest reproductive capacity rating of all the species. Despite receiving a high infection dose, just a small number of larvae were found in pythons and turtles. Furthermore, no clinical indications of the infection have been reported indicating that they do not play a substantial role in epidemiology. Only these two Trichinella species can complete their life cycle in both cold- and warm-blooded animals. As a result, they could trigger distinct physiological processes depending on the host they are infecting [40]. Further infection was investigated in the equatorial freshwater fishes Serrasalmus nattereri and Serrasalmus rhombeus, but no larvae or adult worms were found in any organ, implying that, despite being a food source for reptiles like crocodiles, they have no role to play in the epidemiology due to the entozoic habitat of these fishes, which is not suitable for these two Trichinella species [41]. Table 2 lists the natural and experimental hosts of T. papuae.
Natural host
Crocodylus porosus Papua New Guinea Wild pig Australian island in the Torres Strait region
List of natural and experimental hosts of T. papuae.
Despite the absence of a collagen capsule, the larvae can thrive in a tropical climate, making them more likely to be e transmitted to a new host [45]. Infection with T. papuae was reported to reduce the severity of dextran sulphate sodium-induced colitis in mice. The absence of 57% of T. papuae lipids in humans indicates variations in lipid metabolism, which could aid in the development of innovative treatments [46].
3.3 Trichinella zimbawensis
Trichinella larvae were identified in crocodile muscles in Zimbabwe in 1995. This was the first time Trichinella was found to naturally infect a reptile [47]. In an epidemiological survey, a farm near Victoria Falls was revealed to be the source of infection. The larvae isolated from crocodiles were able to infect domestic pigs and laboratory rats [48]. In the year 2002, Edoardo Pozio was the first to characterise and describe the larvae. This species has been found to infect both mammals and reptiles [11, 40]. Morphology of adults and larvae was determined to be comparable to that of T. papuae. T. Zimbabwensis males and females can procreate in both ways with T. papuae adults. As a result, the F1 offspring produces less viable F2 larvae [11]. Figure 5 shows the T.zimbawensislarvae in the muscles of mice after four months of infection.
Figure 5.
T. Zimbawensis larvae in muscles of mice after four months of infection [11].
The parasite was then discovered in monitor lizards and Nile crocodiles in Zimbabwe and Mozambique, marking the first time to be found in wild reptiles [49]. Later, 38.5% prevalence rate was also been detected in wild Nile crocodiles in South Africa [15]. Natural infection has also been seen in mammals. In another experimental set-up baboons and vervet monkeys were also infected with the larvae. The most prevalent symptoms were fever, diarrhoea and muscular soreness. The infection was treated with ivermectin, but two baboons and two monkeys died as a result of the trial [50]. Table 3 lists the experimental and natural hosts of T. zimbawensis.
Hosts
Species
Region
References
Natural hosts
Reptiles Nile crocodiles; Monitor lizards
KNP of South Africa (Zimbabwe, Mozambique and Ethiopia) and Limpopo and Mpumalanga provinces of South Africa
List of natural and experimental hosts of T. zimbawensis.
Host age was found to have no effect on the distribution of parasites in various segments of intestine in case of golden hamsters and Balb C mice [51]. Also, increased progesterone levels in pregnant mice had a parasiticidal effect on the newly born larvae [53]. Co-infection of Plasmodium berghei with T. zimbawensis resulted in increased parasitemia in mice, which could further lead to severe malaria infection [54]. Various experiments have been carried out to study the immune response of T. zimbawensis infection. Non-encapsulated species have shown reduced inflammation and nitrosylation levels [55]. In an ELISA devised to detect the humoral response, T. zimbawensis was shown not to elicit a substantial immunological response in Nile crocodiles in terms of antibody titres and antibody persistence [56]. Another study revealed the same results, with the infection intensity not correlating with the amplitude of the humoral immune response [57]. The Th1, Th2 and T regulatory responses that are induced during the different stages of infection were also shown to have significant variations [58]. This species has also been observed to affect metabolic parameters by inducing compensatory feeding in the host. During chronic infection, it was found to influence the host’s Th1/Th17 immunological response [59]. The larvae were observed to invade the predilection muscles nearest to their release point in the small intestine first. The parasite load was found to be the highest in the fore and hind limb muscles. The use of biopsy samples from the dorso-lateral areas of the tail has also been recommended for surveillance purposes [60].
A hypothetical transmission cycle for T. zimbawensis has been presented by Louis J. La Grange and Samson Mukaratirwa as shown in Figure 6. Recently, leopard and hyaena have been added as the apex predators along with few mesopredators [61].
Figure 6.
Hypothetical transmission cycle of T. zimbawensis in Kruger National Park [61].
The green arrows indicate the original hypothesised mode of transmission, while the blue arrows represent the modified way of transmission [61].
4. Human outbreaks due to non-encapsulated Trichinella species
Only T. pseudospiralis and T. papuae have been related to human outbreaks to date, while T. zimbawensis has not been associated to any such outbreaks. Figure 7 represents the different outbreaks. Before the first outbreak in Kamchatka, only one case of T. pseudospiralis had been discovered in New Zealand [46, 63]. According to Edoardo Pozio, there were no species-specific primers available at the time of the outbreaks, therefore the species could have been T. papuae in the case of the Thai outbreak [47] but it had not been discovered yet [11]. The larvae were first isolated in a laboratory and then identified using cross-breeding procedures in the context of the Kamchatka epidemic [63]. Species-specific primers were utilised in the case of the French outbreak [11, 48]. The majority of outbreaks caused by Trichinella Papuae have occurred in Thailand, usually caused by the consumption of wild raw pig flesh [49, 50, 52]. In Taiwan, one outbreak was caused by the ingestion of soft-shelled turtles [51]. The most common clinical signs in these epidemics were myalgia, facial oedema and fever. The levels of creatine phosphokinase and aspartate aminotransferase were likewise higher. A few muscle biopsy specimens also included larvae [53]. These outbreaks suggest that there is a strong link between parasites and human behaviour, particularly the eating habits and certain rituals, such as the ‘mumu’ cooking method in Morehead District, PNG, which could have been a source of T. papuae infection [46, 64]. Albendazole, glucocorticosteroids and various supportive medications such as painkillers are generally used in the treatment [65]. A study found that the maslinic acid’s efficiency in rats was comparable to that of fenbendazole, with no side effects, indicating that it could be a promising anthelminthic drug against Trichinella larvae (Table 4) [76].
Figure 7.
Map representing the outbreaks caused by non-encapsulated Trichinella species [62].
Outbreaks caused due to different non-encapsulated Trichinella species.
4.1 Species identification methods
A polymerase chain reaction-based on the mitochondrial large subunit ribosomal RNA gene was paired with a pyrosequencing technique to distinguish the four Trichinella species, this was successfully found to be sensitive enough to identify the individual larvae [77]. PCR based on the ITS1, ITS2 and ESV regions has also been utilised for the molecular identification of the species among wildlife in South Africa [78]. FRET-PCR and a melting curve analysis have also been utilised for the differential detection of the species [79]. Using Western blot, T. pseudospiralis infection can be differentiated from T. spiralis or T. britovi infection. When the source is unknown, this technique may be beneficial in epidemiological investigations [80].
The genus Trichinella used to have only one species; however, it has subsequently evolved into a multispecies genus. Due to its broad host range, it has been able to establish itself in both domestic and sylvatic cycles, allowing it to maintain a vast host reservoir. The infection has been documented in a variety of experimental species, showing that it could potentially happen in natural settings as well. Due to the considerable genetic differences among the isolates, researchers predict that the number of species and genotypes discovered within Trichinella will increase. Although molecular methods are used to identify the Trichinella species but these methods are not appropriate for the diagnosis of the infection in animals. Outbreaks caused by various species in different parts of the world have also been reported, therefore prevention and control are critical in order to limit the parasite’s transmission to humans.
Professor Samson Mukaratirwara, Professor Edoardo Pozio and Professor Violeta Santrac graciously allowed us to use their valuable images of Trichinella species larvae. Special thanks to Professor Edoardo Pozio for revising the manuscript and providing valuable insights. Financial support was provided by Department of Science and Technology, New Delhi, India.
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Written By
Devyani Sharma, Upninder Kaur and Rakesh Sehgal
Submitted: 09 May 2022Reviewed: 02 June 2022Published: 01 November 2022
Open access peer-reviewed chapter
