Abstract
Purpose of Review
This review focuses on key foodborne helminths: providing an overview of their lifecycles and major transmission routes to humans, their geographical distribution, clinical manifestations, human health burden and control aspects.
Recent Findings
Many foodborne helminths appear to be increasing in geographical distribution, driven by climatic and demographic changes; predominately increases in global humidity and temperature, favouring environmental survival and changes in human consumption practices, exposing many more people to high-risk foodstuffs. Although current estimates of human health burden indicate the need for us to focus on these diseases it is acknowledged that poor diagnostic performance and inefficient surveillance leads to an underestimate of burden and for some highly neglected helminths no burden estimates have been performed. It is acknowledged that intervention strategies should consider the full value chain and involve multiple stakeholders following a ‘One Health’ approach.
Summary
As well as improving burden estimates, key research needs for foodborne helminths include the need for improved diagnostic tools and better integration of the social sciences to ensure the development of contextually relevant and socially acceptable control strategies.
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Introduction
Helminths, incorporating Nematoda (roundworms), Cestoda (tapeworms), Trematoda (flukes) and Acanthocephala (thorny headed worms) are an important global public health threat and a significant route of helminth infections for humans is through the consumption of larvae or eggs in food products, foodborne helminthiasis. Foodborne helminth infections cause a substantial health burden with a particularly high impact in low- and middle-income countries, particularly affecting people living in rural deprived areas [1]. Some foodborne helminthiasis have been traditionally underappreciated and represent a substantial fraction of the neglected tropical diseases [2]. It is important, however, to appreciate that these helminths are a global concern due to their worldwide distribution, globalisation of the food supply, the increase of international travel and highly susceptible populations, changes in eating patterns and improvements in diagnostic techniques and communication [3]. In this article, we provide an overview of the most relevant helminths transmitted to humans by consumption of food-products. We focus on those where the food-product forms an integral aspect of the parasite lifecycle rather than when food products are inadvertently contaminated by parasite eggs. These products predominately include those of animal origin where the animal represents the intermediate host of the parasite, though we also include aquatic vegetation which represents a key vehicle of transmission for metacercariae of Fasciola spp. from the intermediate host to a human definitive host. We focused on parasite life cycle, pathogenesis, health burden, clinical symptoms, and diagnosis, control aspects and throughout have identified areas of consideration for research. A summary of key helminth species, their geographical distribution, transmission routes, clinical manifestations and human health burden is provided in Table 1.
Trematoda (Flukes)
Foodborne trematodes are considered to infect 75 million people, with 750 million people living at risk of infection [5, 6]. Parasites from this class are also known as flukes and are classified in three groups: liver flukes (Fasciolidae & Opistorchiidae), lung flukes (Paragonimidae) and intestinal flukes (of multiple families) [6]. Figure 1 provides an overview of the lifecycles of these different flukes.
(A) Fasciolidae: (1) Humans and ruminants are the definitive host with the adult fluke developing within the hepatic ducts. Eggs are released into the biliary tree and excreted in faeces. (2) Eggs embryonate in the water and miracidia emerge from the egg. (3) Miracidia penetrate an aquatic snail intermediate host of the family Lymnaeidae where they develop into cercariae (4) Free swimming cercariae emerge from the intermediate host. (5) Cercariae encyst on aquatic vegetation such as watercress as metacercariae (6) Upon ingestion by of vegetation with metacercariae by the definitive host, the newly excysted juveniles penetrate the intestinal wall and burrow into the hepatic ducts before developing into adult worms. (B) Opistorchiidae: (1) Humans, carnivores and many birds are the definitive host. Embryonated eggs are excreted in faeces. (2) Eggs are ingested by the aquatic snail first intermediate host of the families Bithyniidae, Hydrobiidae, or Thiaridae where the miracidia hatch, migrate to the intestine where they develop into cercariae (3) Free swimming cercariae emerge from the intermediate host. (4) Cercariae seek the second intermediate host, being fish or crustacean where they develop into metacercariae. (5) Upon ingestion of the second intermediate host containing metacercariae by the definitive host, juvenile flukes migrate to the liver where they mature. (C) Paragonimidae: (1) Humans and many domestic and wild animals including pigs, dogs and cats are the definitive host with the adult fluke developing within the respiratory tract. Unembryonated eggs are released into the tracheobronchial tree and coughed out or coughed up and swallowed after which they are excreted in faeces. (2) Eggs embryonate within water and miracidia emerge from the eggs. (3) Miracidia penetrate an aquatic snail first intermediate host of the families Assimineidae, Hydrobiidae, Pomatiopsidae, Pleuroceridae and Thiaridae where they develop into cercariae. (4) Free swimming cercariae emerge from the snail host. (5) Cercariae invade a crab or crayfish second intermediate host and develop into metacercariae. (6) Upon ingestion of raw, undercooked, or picked crabs and crayfish containing metacercariae by the definitive host, juvenile flukes migrate from the intestine, through the diaphragm into the lungs where they develop into adults. (D) Intestinal Flukes: (1) Humans and multiple wild and domestic mammals and birds are definitive hosts of intestinal flukes and pass unembryonated eggs in their faeces. (2) Eggs embryonate and miracidia emerge from the eggs in water. (3) Miracidia penetrate the body pf an aquatic snail as first intermediate host in which they develop into cercariae. (4) Free swimming cercariae. (5) Cercariae either encyst on aquatic vegetation or invade a second intermediate host (fish) and encyst into metacercariae. (6) Definitive hosts ingest fish or aquatic vegetation with metacercariae.
Fasciolidae
Fascioliasis is a re-emerging disease which is clustered in tropical & subtropical regions [7]. Fasciola hepatica and Fasciola gigantica are the two most important foodborne trematodes of the family Fasciolidae [8]. Ruminants are definitive hosts of F. hepatica and F. gigantica and fascioliasis often correlates with the presence of livestock, although once established in humans, animal reservoirs become dispensable with infection more likely to be correlated with poor sanitation [8]. Infection with F. hepatica is most widely reported, with wild aquatic vegetation such as wild watercress with the encysted metacercariae (see Fig. 1a) most often implicated as the source of infection [8].
Clinical severity, from asymptomatic to severe hepatic and intestinal manifestations, depends on worm burden and host immune response. The acute phase, driven by juvenile fluke migration, manifests as fever, abdominal discomfort, and gastrointestinal disturbances, and is sometimes accompanied by anorexia, flatulence, nausea, diarrhoea, urticaria, and coughing. The chronic phase, appearing months to years after infection, can present with biliary colic, epigastric pain, nausea, and jaundice [8]. Infections are generally diagnosed by coproscopy, and treatment primarily relies on triclabendazole and remains effective [9], although there are resistance concerns in livestock which stem from Its excessive use in animals [8].
Opistorchiidae
The Opistorchiidae is a family of liver flukes of which the three most important species are Clonorchis sinensis, Opistorchis felineus, and Opistorchis viverrini. Their intricate life cycles involve a freshwater snail as the first intermediate host, followed by a second intermediate host, frequently a freshwater cyprinid fish [10] as summarised in Fig. 1b. Humans are infected upon the consumption of raw, partially cooked or fermented fish or crustaceans containing the metacercariae and can be the definitive host of all species [11].
Global infection estimates underscore the widespread impact of these flukes, with C. sinensis affecting around 35 million people, O. viverrini 10 million in Southeast Asia, and O. felineus afflicting 1.2 million in Eastern Europe and Russia [11]. Infection sources differ regionally and is often facilitated through traditional cuisine. Local dishes like goi ca. mai, raw fish salad in Vietnam, yusheng in China, and sushi in Korea and Japan, contribute to C. sinensis transmission, while dried or salted fish constitutes the main source of O. felineus infection in Eastern Europe and Russia. Considering the consumption of undercooked freshwater cyprinid fish, over 680 million individuals are at risk of infection [11].
Clinical symptoms, like that of fascioliasis are usually non-specific and dependent on the parasite load and host susceptibility [11]. One of the most severe potential consequences of infection is the development of cholangiocarcinoma, with the carcinogenic potential of O. felineus being lower than that of C. sinensis and O. viverrine [12]. Coproscopy remains the key diagnostic method, yet its effectiveness is hindered by the potential resemblance of eggs to those of other trematodes, often necessitating specialized expertise [10]. A suite of serological tests for clonorchiasis and opisthorchiasis are available which exhibit increased sensitivity and specificity compared to faecal examination techniques. Praziquantel is the drug of choice having high efficacy and no indication of resistance to date, although reinfection rates following treatment are high [11].
Paragonimidae
The genus Paragonimus of the family Paragonimidae, has a very broad geographical distribution which includes tropical and subtropical Asia, Africa, and the Americas. An estimated 20.7 to 22 million individuals are infested by Paragonimus species, while 195 to 292.8 million live in areas of risk [13]. At least 15 species of the lung fluke have been reported in humans, with P. westermani responsible for most human cases [14]. This trematode usually resides in the respiratory tract of its wide array of mammalian definitive hosts, including humans, dogs, pigs, and domestic and wild cats [14]. Extrapulmonary infections do occur, particularly in the brain and spinal cord, but also in the subcutaneous tissues, hepatobiliary system, and colon [13, 15].
Paragonimiasis is contracted through the ingestion of raw, undercooked or pickled crustaceans, and as such, cultures with a strong tradition of consuming raw fish dishes exhibit a higher prevalence of paragonimiasis [14]. Metacercaria can also enter a non-definitive paratenic host, such as wild boar, and encyst as a juvenile parasite, leading to the infection of definitive hosts with no history of crustacean ingestion [15].
Clinical signs of paragonimiasis vary depending on the stage and location of the parasite. Migration of worms from the intestine into the abdomen may result in symptoms such as diarrhoea and abdominal pain. Migration into the lungs often elicits an allergic response, characterized by fever, chills, coughing, chest pain, urticaria, and eosinophilia and can often be misdiagnosed as tuberculosis or pulmonary neoplasia. Spinal involvement can lead to paraplegia, monoplegia, limb weakness, and sensory deficiencies, whilst cerebral paragonimiasis can lead to headache, fever, vomiting, seizures, and visual disturbances. An estimated one out of ten cases of cerebral paragonimiasis results in death [14].
The gold standard for diagnosing the disease is the microscopic examination and identification of eggs in either the sputum or stool. However, the intermittent discharge of eggs in the sputum and its similarity to other trematode eggs can decrease its sensitivity [15]. The drug of choice for treatment of paragonimiasis is praziquantel, although bithionol and triclabendazole has also successfully treated the disease [14].
Intestinal Flukes
The intestinal flukes are a group of approximately 74 species of trematode worldwide distributed which can colonise the human intestinal tracts including those from the families: Echinostomatidae, Gymnophalidae, Heterophyidae, Nanophytetidae, Neodiplostomidae, and Plagiorchiidae [16]. Humans become infected by Fasciolopsis buski’s on consumption of aquatic vegetation with encysted metarcercariae whilst other intestinal flukes such as Metagonimus yokogawai or Metagonimus miyatai from the family Heterophyidae, have a freshwater fish (sweetfish, dace, chub, or minnow) as second intermediate host, infecting humans after the consumption of raw or undercooked fish [10].
Infected patient clinical symptoms are strongly associated with the parasite load. In mild infections, symptoms such as headache, abdominal pain constipation or mild diarrhoea are observed. Whilst moderate to heavy infections can cause colic, vomiting, fever, nausea, oedema in patients, being sometimes fatal if the parasites cause intestinal ulceration, haemorrhage, erosions, or abscesses [6]. Intestinal flukes in humans are generally diagnosed by coprological examinations to recover eggs and posterior microscopic observation. For human echinostomiasis, the identification of adult flukes is also highly recommended [17] although sometimes can be difficult due to the lack of molecular data and understanding of the taxonomy of this parasite [18]. For Fasciolopsis buski diagnosis, serological tests are available to detect antibodies that might help for the diagnosis [19]. Praziquantel and Niclosamide have both proven effective in treating intestinal flukes [10].
Cestoda (Tapeworms)
Family Taeniidae
The Taeniidae is a family of tapeworms of the order Cyclophyllidea with four genera, Echinococcus, Hydategera, Taenia and Versteria [20]. Taenia solium and Taenia saginata are classical foodborne parasites, with humans being the definitive host after ingestion of raw or undercooked meat from infected livestock species, being pigs and cattle respectively. The Asian tapeworm T. asiatica which utilises swine as the intermediate host was originally assumed to be a separate species, is now considered most likely a local variant of T. saginata, due to only minor genetic differences [20]. The adult Taenia spp. worm reside in the small intestine, taeniasis, and eggs or whole proglottids containing eggs, are excreted with faeces of the definitive host which are then ingested by the intermediate host as illustrated in Fig. 2a&b. Humans can also act an aberrant intermediate host of T. solium due to faecal-oral contamination (see Fig. 2a) developing encysted metacestode larvae in the brain, known as neurocysticercosis (NCC), but also in skeletal muscle, eye, heart, skin, and subcutaneous tissue.
Taeniasis is generally asymptomatic thought episodes of diarrhoea, nausea, epigastric pain, weight loss or increased hunger might be caused by the tapeworm and some rare severe sequalae such as gall bladder perforation have been reported. The diagnosis of taeniasis is difficult due to poor sensitivity of microscopy due to intermittent shedding of gravid proglottids and free eggs. Microscopy is poor at speciation of Taeniid eggs, molecular or immunological methods are available for speciation, but rarely used in a clinical capacity. Taeniasis of all species can be effectively treated with Nicolsamide, Praziquantel and triple dose of Albendazole [21]. T. solium has the highest health burden of all foodborne parasites [22], making it the most important of the Taeniidae family due to the severe consequences of NCC, including the development of seizures and epilepsy [23]. Neurocysticercosis is believed to be one of the most common causes of acquired epilepsy in endemic countries, responsible for approximated 1/3 of cases [24]. No reports of humans as aberrant intermediate hosts have been made for either T. saginata or T. saginata asiatica. They are therefore of relatively low public health importance, though bovine cysticercosis has a high economic burden due to the processing, downgrading, or condemnation of infected beef [25].
While T. saginata has a worldwide distribution [26,27,28,29,30,31], T. solium is distributed predominately in rural areas of India, Africa, South America, and Southeast Asia where risk factors, such as the presence of free-ranging pigs, low sanitation provision and poor access to health care are prevalent [32]. Reports of T. solium are however, reported in high income countries due to human mobility [25, 33, 34].
Cases of NCC are likely highly under-reported due to the paucity of diagnostic capacity in endemic countries with advanced neuroimaging (CT & MRI) being the gold standard. Serological tests are also available, including a highly sensitive and specific enzyme-linked immunoelectrotransfer blot assay, but these are also rarely applied in a clinical setting in endemic areas. The treatment of neurocysticercosis requires an individual case by case approach depending on viability, cyst location and host clinical signs, which vary from the symptomatic treatment of seizures with antiepileptic drugs to surgical intervention [35].
(A) T. saginata: (1) Humans eat raw or undercooked cysticerci infected meat. (2) Parasites grow to its adult form in the small intestine (taeniasis). (3) Eggs are deposited in the large intestine and released to the environment. (4) Cattle (or pigs in the case of T. saginata asiatica) become infected by ingesting infective eggs in the environment. (5) Oncospheres penetrate the intestine wall and travel to the musculature. (6) Oncospheres develop into cysticerci in muscle of the intermediate host (cysticercosis). (B) T. solium: (1) Humans eat raw or undercooked cysticerci infected meat. (2) Parasites grow to its adult form in the small intestine (taeniasis). (3) Eggs are deposited in the large intestine and released to the environment. (4) Pigs become infected by ingesting infective eggs in the environment. (5) Oncospheres penetrate the intestine wall and travel to the musculature. (6) Oncospheres develop into cysticerci in muscle (porcine cysticercosis). (7) Faecal-oral contamination or auto-infection leads to ingestion of eggs by humans. (8) Oncospheres penetrate the intestinal wall and travel to the musculature, ocular and nervous tissues, humans become an aberrant intermediate host.
Nematoda
Nematodes, also known as roundworms, account a range of 100,000–1 million species, of which several are transmitted to humans through consumption of raw or undercooked meat, fish or slugs [36]. Key foodborne nematode species include: Trichenella spiralis, Anisakis spp., Gnathostoma spp., Angiostrongylus spp., (cantonensis & costaricensis) and their lifecycles are summarised in Fig. 3.
(A)Trichinella spiralis: Has a single host lifecycle with one animal functioning as both the definitive and intermediate hosts (1) A Human (dead-end host) or non-human animal host consumes raw or undercooked meat from an animal with encysted larva (e.g., pig, horse, rodent, or wildlife). (2) Larvae encysted in the meat are released in the digestive tract and migrate to the small intestinal mucosa (3) Larvae mature to adult worms and undergo sexual reproduction (4) The larvae released by the female parasite migrate through the lymphatic vessels to the striated muscle (5) Within 2 weeks larvae encyst in started muscle, where they can survive and remain infective for many years until ingestion of the infected meat by a new host. (6) The life cycle can be propagated within domestic or sylvatic cycles. (B) Anisakis spp. (1) The definitive host acquires infection through the ingestion of raw or undercooked paratenic hosts (fish or cephalopods) and larvae develop into adults in gastric mucosa (2) Unembryonated eggs are excreted in faeces, eggs embryonate in water and free-living larvae hatch from eggs (3) Crustaceans ingest free-living larvae (4) Fish or cephalopod paratenic hosts ingest infected crustaceans and larvae migrate to musculature (5) Marine mammals or humans ingest infected fish or cephalopods. (C) Gnathostoma spp. (1) The definitive host (suids, canids, felids) excrete unembryonated eggs from the adult worms which live within in tumour-like masses within the gastric wall. (2) Eggs embryonate in the water and hatch releasing the first stage larvae. (3) The first intermediate host, Cyclops crustaceans, ingest the larvae which develop into the second stage larvae. (4) The second intermediate host, fish or amphibians, ingest the first intermediate host with stage-two larvae which develop into third-stage larvae. (5) Definitive or dead-end (human) hosts acquire infection through the consumption of the second intermediate host or paratenic host (birds or snakes) infected with third-stage larvae. (D) Angiostrongylus spp. (1) The adult worm lives in the right ventricle and pulmonary artery of the rat definitive host. The eggs travel through the blood stream to the lungs where they hatch into first-stage larvae which penetrate the alveoli and move up to the trachea. Here they are coughed up, swallowed and excreted with the faeces. (2) Faeces with first-stage larvae are eaten by a slug or snail intermediate host where they develop through to third-stage larvae. (3) Freshwater shrimps, crayfish, land crabs, frogs, toads or monitor lizards may ingest the intermediate hosts becoming paratenic hosts (4) The rat definitive host, or human dead-end host becomes infected through ingestion of the infected intermediate or paratenic hosts. The larvae penetrate the intestinal wall and migrate to the CNS where they develop to the sub-adult stage which in the rat then move to the bloodstream to continue the life cycle.
Trichinella spiralis is a widely distributed parasite for which a wide number of different domestic and wild animal species including reptiles, birds and mammals and be both definitive and intermediate host [37, 38]. Trichinella spiralis cause trichinellosis in humans, historically transmitted through the consumption of undercooked meat from pigs, wild game or horses containing encysted Trichinella spiralis larvae [39]. Clinical signs of trichinellosis are dependent of the life cycle phase. During the enteral phase vomiting, mild transient diarrhoea, nausea, and low-grade fever caused by the invasion of the parasite of the intestinal mucosa might be observed. Larval migration and encystment (parenteral phase) can result in periorbital and/or facial oedema, paralysis, conjunctivitis, headache, fever, and myocarditis. Serological tests including ELISA and Western Blot are available for the diagnosis of trichinellosis in humans. Muscle biopsy can be also collected for confirmation of inspection and identification of the species [40] though is not usually used in practice because it as an invasive, painful, and expensive method [36]. Mebendazole, albendazole and pyrantel are the principal drugs to treat trichinellosis. These drugs applied at the enteral phase eliminate the worms from the intestinal tract as well as prevent the skeletal muscle tissue invasion. Together with anthelmintics, glucocorticoids, such as prednisolone, and immunomodulating drugs support the therapy in the acute and severe stages of the disease [41].
Anisakiasis is an emerging nematode infection caused by the aquatic-derived third-stage larvae of the genus Anisakis [42]. This worldwide distributed nematode [43], particularly affects populations from countries where raw or undercooked fish is consumed. While Japan, Spain and South Korea have the highest number of published cases ‘hot-spots’ of allergic anisakiasis appear to be Portugal & Norway [44, 45]. Anisakiasis can cause gastro-intestinal symptoms as well as symptoms related to parasite migration to other organs [44, 45]. A high public health issue is allergic anisakiasis, characterised by allergic reactions within 1-2hrs of ingestion of the fish from mild urticaria to severe anaphylaxis [42]. This disease is both underdiagnosed and underreported due to the lack of diagnostic tests and specific clinical symptoms in affected patients [46]. The assessment of clinical signs, serological anti-Anisakis IgG/A antibody test and the use of endoscopy for gastric anisakiasis and Computed Tomography scan for intestinal anisakiasis are useful for the diagnosis of the parasite [47]. Endoscopic extraction of the Anisakis larvae is the elected treatment for gastric anisakiasis whilst conservative treatment is the chosen for intestinal anisakiasis evolving into surgical intervention in severe scenarios [48].
Gnathostomiasis is another emerging foodborne nematode of worldwide distribution, clustering in southeast Asia, caused by the third-stage larvae of Gnathostoma spp. due to the consumption of raw, marinated or undercooked freshwater fish as well as fish, frogs, snake or poultry [49]. Humans are an aberrant host of Gnathostoma spp., and the third-stage larvae migrate through the body causing damage, inflammation and allergy and, without proper treatment, death. Clinical signs depend upon the parasitic load and the organs involved in the infection, with cutaneous gnathostomiasis being the most common presentation causing nodular migratory panniculitis with pain and swelling intermittently over time [49]. Morphological identification is required to diagnose the parasite as serological tests might cross react between Gnathostoma spp. and the Echinocephalus genus [50,51,52]. Albendazole for 21 days appears to be an effective treatment for human gnathostomiasis and cutaneous gnathostomiasis may be treated by surgical removal of larvae [53].
Foodborne infection with Angiostrongylus spp., (A. costaricensis and A. cantonensis), previously distributed predominately across Asia and Australia, have more recently been recorded throughout the Americas and Caribbean as well Europe [54]. Larval infections of the central nervous system are associated with eosinophilic meningitis or encephalitis due to the strong inflammatory response to the migrating third-stage larvae and result in neurological deficits, paralysis, seizures and sometimes death [55]. Humans acquire infection through ingestion of raw or undercooked gastropod intermediate hosts (slugs or snails) or paratenic hosts including freshwater shrimps, land crabs, frogs, toads or monitor lizards [55]. Diagnoses relies on the detection of eosinophilia in the cerebrospinal fluid, alongside a relevant exposure history and confirmatory serological testing (ELISA or immunoblot) and treatment options are predominately a combination of anthelmintic and corticosteroid therapy, with success dependent upon the location and degree of infection [56].
Acanthocephala
Acanthocephala, commonly known as thorny- or spiny-headed worms, include multiple parasite families spanning approximately 1300 species which can parasitise multiple arthropod and vertebrate hosts [57]. Many species are aquatic and although rarely considered as an important foodborne helminth, the ingestion of undercooked fish or shellfish can lead to gastro-intestinal complications as reported in Japan and Alaska due to infection with Corynosoma spp. [58, 59]. Corynosoma spp. utilise marine amphipods as an intermediate host, fish as paratenic hosts and marine mammals, including walrus and seals, and birds as definitive hosts [58]. Yet Acanthocephala is considered a minor zoonoses, though species of this phylum have been identified in many edible fish species, indicating the need to ensure appropriate freezing or cooking of seafood products and to consider infection with these parasites in patients presenting with compatible histories [60].
Global Trends in Foodborne Helminth Transmission
Various factors have a strong influence on the trends in global foodborne helminthiasis infections [61]. Climate change has an impact not only in the ability of the foodborne parasite stages to survive in the environment, but also in the biology of the host [61]. An increase in humidity and temperature triggers respectively a longer survival and a faster development of parasite stages in the environment and in the host, favouring the settlement of parasites from tropical regions in temperate ones. Additionally, intense rainfalls favour the spread of eggs and cysts whilst droughts, despite of reducing egg and cyst survival, favour parasite concentration in water [61]. An increase in travel, tourism and migration due to socio-economic circumstances contribute to the globalisation of foodborne helminth transmission and extension of endemic areas [62,63,64]. New behavioural and cooking habits of eating raw, undercooked, pickled, or smoked foods increase the likelihood of foodborne parasite infection. Popular examples are sushi and marinated anchovies which contain raw fish being responsible of anisakiasis [65, 66]. Rapid expansion of the aquaculture industry and shifts towards outdoor and organic farming practices may also increase the risk of foodborne parasite infection. This can be observed in free-range pig production which increases the risk of Trichinella spiralis exposure [65, 66]. Monitoring the prevalence and distribution of foodborne parasites is an important step towards quantifying health burden and stimulating investment in control, additional surveillance activities and data sharing is urgently required.
Controlling Food Borne Helminths
While anthelmintic treatments are available for individuals infected by the foodborne helminths covered in this review, sustainable control of foodborne parasites must focus on breaking the cycle of transmission between humans and the relevant intermediate hosts [67]. Control of food borne helminths, as per other food safety challenges require a farm (sea or pond) to fork approach, with interventions targeting both human and animal hosts likely to improve sustainability of control strategies [67]. Control of these parasites therefore will require a focus on appropriate animal husbandry, effective inspection and processing of food products, improved water, sanitation and hygiene provision and supporting human behaviour change to reduce exposure.
Preventing the transmission of helminths to the intermediate or paratenic hosts which may then be consumed by humans requires strong biosecurity measures, which may include raising animals under highly controlled systems [68], ensuring pasture land cannot be contaminated by sewerage effluent from contaminated stream or surface water [69] and improving human sanitation provision, from building of basic latrines to installation of tertiary treatment plants to prevent contamination of the environment with faeces containing infective eggs [70]. The prudent use of anthelmintics in livestock production is advised in high-risk areas though the risk of resistance must always be considered. The development of effective anthelminthic vaccines, such as that against Taenia solium is an exciting development, though the production and distribution of such vaccines requires scaling up for maximal effectiveness [8, 71, 72].
Official veterinary inspectors play an important role in controlling food borne helminths in food processing facilities [73] and therefore, it is crucial that they are adequately trained in recognising life cycles and morphological features of relevant veterinary and human parasites [74]. Currently visual inspection, palpation and incision practices are utilised to detect, and then process or condemn, food products infected with macroscopic parasites such as Taenia spp., Fasciola hepatica and Anisakis spp. Whilst specificity of such techniques may be good, the sensitivity is often poor, particularly in light infections. Classical meat inspection is estimated to have only a 27% sensitivity for light infections of Taenia spp., increasing to 78% when more than 20 cysts are present on the carcase [73], the palpation and incision of the gastric surface and the base of the caudate lobe of the liver for Fasciola hepatica is estimated to have only 68% sensitivity while visual inspection of fish for Anisakis is limited in its ability to identify the parasite when embedded in the muscle of the fish [75].
Handling and incising food products can also introduce microbial cross-contamination to the meat from authorised officer’s hands and equipment and hence a European Union (EU) move towards visual-only meat inspection within risk-based meat assurance systems [76]. These risk-based systems have four components: harmonised epidemiological indicators, food chain information, risk-based meat inspection and reactive interventions and can support a move towards visual-only inspection [77].
Risk-based inspection for Trichinella spiralis is already in place in the EU [78]. Additional research is required to support the continued scale-up of risk-based assurance systems in relation to other foodborne helminths, including additional modelling studies to refine risk indicators and determine the most cost-effective inspection processes [79] and the continued improvement in rapid, cost-effective, and sensitive diagnostic procedures. For example, progress has been made in other real-time, non-destructive inspection technologies such as hyperspectral imagining which can be used as a parasite detector to assess the quality and safety of foods [80]. This technique has been applied to accurately detect Anisakis on sashimi [81] and in cod fillets [82].
The application of heat, cold or chemical preservation plays an important role in controlling many foodborne helminths. Cooking temperatures (core) 60 –70 °C for 15–30 min or freezing at -5 °C (for 2 weeks) to -18 °C (for 1–3 days) inactivates parasite larvae in most food of animal origin [83]. The application of some other food processing techniques can be also used to inactivate these hazards in meat and fish and may be most applicable when cultural norms relating to cooking restrict the ability to encourage cooking as a control measure [84]. These techniques include marination, fermentation, drying, addition of organic acids and salt, which lower the pH of the product being effective NaCl contents of 2–5% to inactivate food borne parasites, as proved marinating fish in 2.6% acetic acid and 5–6% salt for 12 weeks which inactivates Anisakis larvae [83].
To implement sustainable control of foodborne helminths along the whole value chain it is important that the interventions proposed are acceptable to the community and appropriate to the context in which they are being undertaken [85, 86], considering society, culture and gender norms [87, 88]. The social science disciplines play an important role in understanding the contextual aspects of foodborne helminth control and in creating optimal strategies to encourage human behaviour change for the adoption of risk-mitigation strategies and is an area where much research is still needed [89].
Conclusion
Foodborne helminthiasis are a substantial cause of human health burden globally and their distribution is likely to increase due to climate change, global travel and alterations in eating patterns without substantial investment in appropriate integrated control strategies along the food supply chains. Robust surveillance is required to monitor the epidemiological situation and to improve the burden estimates for these pathogens to stimulate investment in control. Further research is required on low-cost, non-invasive, and sensitive diagnostic tools, vaccines for use in food-producing livestock and on the development of contextually appropriate, sustainable control strategies with a particular focus on the social sciences.
Data Availability
No datasets were generated or analysed during the current study.
References
Anisuzzaman, Hossain MS, Hatta T, Labony SS, Kwofie KD, Kawada H, Tsuji N, Alim MA. Food- and vector-borne parasitic zoonoses: global burden and impacts. Adv Parasitol. 2023;120:87–136.
King CH. Helminthiasis Epidemiology and Control: Scoring successes and meeting the remaining challenges. Adv Parasitol. 2019;103:11–30.
Dorny P, Praet N, Deckers N, Gabriel S. Emerging food-borne parasites. Vet Parasitol. 2009;163:196–206.
Torgerson PR, Devleesschauwer B, Praet N, et al. World Health Organization Estimates of the Global and Regional Disease Burden of 11 foodborne parasitic diseases, 2010: A Data Synthesis. PLoS Med. 2015. https://doi.org/10.1371/journal.pmed.1001920.
Robinson MW, Sotillo J. Foodborne trematodes: old foes, new kids on the block and research perspectives for control and understanding host-parasite interactions. Parasitology. 2022;149:1257–61.
Keiser J, Utzinger J. Food-Borne Trematodiases. Clin Microbiol Rev. 2009;22:466–83.
Rosas-Hostos Infantes LR, Paredes Yataco GA, Ortiz-Martínez Y, et al. The global prevalence of human fascioliasis: a systematic review and meta-analysis. Ther Adv Infect Dis. 2023;10:1–18.
Siles-Lucas M, Becerro-Recio D, Serrat J, González-Miguel J. Fascioliasis and fasciolopsiasis: current knowledge and future trends. Res Vet Sci. 2021;134:27–35.
Gandhi P, Schmitt EK, Chen C-W, Samantray S, Kumar Venishetty V, Hughes D. Triclabendazole in the treatment of human fascioliasis: a review. Trans R Soc Trop Med Hyg. 2019;113:797–804.
Chai JY, Jung BK. General overview of the current status of human foodborne trematodiasis. Parasitology. 2022;149:1262–85.
Saijuntha W, Sithithaworn P, Petney TN, Andrews RH. Foodborne zoonotic parasites of the family Opisthorchiidae. Res Vet Sci. 2021;135:404–11.
Mordvinov VA, Pakharukova MY. Similarities and differences among the Opisthorchiidae liver flukes: insights from Opisthorchis Felineus. Parasitology. 2022;149:1306–18.
Berger S. Paragonimiasis: global status. INC: GIDEON INFORMATICS; 2023.
Adams A. Foodborne trematodes: Paragonimus and Fasciola. In: Ortega YR, Sterling CR, editors. Foodborne parasites, Second. Springer International Publishing; 2018. pp. 293–324.
Blair D. Parasitology lung flukes of the genus Paragonimus: ancient and re-emerging pathogens. Parasitology. 2022;149:1286–95.
Chai JY, Jung BK. Foodborne intestinal flukes: a brief review of epidemiology and geographical distribution. Acta Trop. 2020;201:105210.
Chai JY, Shin EH, Lee SH, Rim HJ. Foodborne intestinal flukes in Southeast Asia. Korean J Parasitol. 2009;47:69–102.
Ray M, Trinidad M, Francis N, Shamsi S. (2024) Characterization of Echinostoma spp. (Trematoda: Echinostomatidae Looss, 1899) infecting ducks in south-eastern Australia. Int J Food Microbiol 110754.
Quang TD, Duong TH, Richard-Lenoble D, Odermatt P, Khammanivong K. Émergence Chez L’homme De fasciolose à Fasciola gigantica et de distomatose intestinale à Fasciolopsis buski Au Laos. Cahiers d’études et de recherches Francophones / Santé. 2008;18:119–24.
Ito A, Budke CM. Genetic diversity of Taenia solium and its relation to clinical presentation of Cysticercosis. YALE J BIOLOGY Med. 2021;94:343–9.
Okello AL, Thomas LF. Human taeniasis: current insights into prevention and management strategies in endemic countries. Risk Manag Healthc Policy. 2017;10:107–16.
Li M, Havelaarid AH, Hoffmannid S, Hald T, Kirk MD, Torgerson PR, Devleesschauwer B. Global disease burden of pathogens in animal source foods, 2010. PLoS ONE. 2019;14:1–18.
Lè Ne Carabin H, Ndimubanzi PC, Budke CM, Nguyen H, Qian Y, Cowan LD, Stoner JA, Rainwater E, Dickey M. Clinical manifestations Associated with neurocysticercosis: a systematic review. PLoS Neglected Trop Disease. 2011;5:1–13.
Ndimubanzi PC, Lè Ne Carabin H, Budke CM, Nguyen H, Qian Y-J, Rainwater E, Dickey M, Reynolds S, Stoner JA. A systematic review of the frequency of Neurocyticercosis with a focus on people with Epilepsy. PLoS Neglected Trop Disease. 2010;4:e870.
Laranjo-González M, Devleesschauwer B, Trevisan C, et al. Epidemiology of taeniosis/cysticercosis in Europe, a systematic review: Western Europe. Parasit Vectors. 2017;10:349.
Eichenberger RM, Thomas LF, Gabriël S, et al. Epidemiology of Taenia Saginata taeniosis/cysticercosis: a systematic review of the distribution in East, Southeast and South Asia. Parasit Vectors. 2020;13:234.
Braae UC, Thomas LF, Robertson LJ, Dermauw V, Dorny P, Willingham AL, Saratsis A, Devleesschauwer B. Epidemiology of Taenia Saginata taeniosis/cysticercosis: a systematic review of the distribution in the Americas. Parasit Vectors. 2018;11:518.
Hendrickx E, Thomas LF, Dorny P, et al. Epidemiology of Taenia Saginata taeniosis/cysticercosis: a systematic review of the distribution in West and Central Africa. Parasit Vectors. 2019;12:324.
Torgerson PR, Abdybekova AM, Minbaeva G, et al. Epidemiology of Taenia Saginata taeniosis/cysticercosis: a systematic review of the distribution in central and western Asia and the Caucasus. Parasit Vectors. 2019;12:175.
Saratsis A, Sotiraki S, Braae UC, et al. Epidemiology of Taenia Saginata taeniosis/cysticercosis: a systematic review of the distribution in the Middle East and North Africa. Parasit Vectors. 2019;12:113.
Dermauw V, Dorny P, Braae UC, Devleesschauwer B, Robertson LJ, Saratsis A, Thomas LF. Epidemiology of Taenia Saginata taeniosis/cysticercosis: a systematic review of the distribution in southern and eastern Africa. Parasit Vectors. 2018;11:578.
Donadeu M, Bote K, Gasimov E et al. (2022) WHO Taenia solium endemicity map- 2022 update. Geneva. https://www.who.int/publications/i/item/who-wer9717-169-172
Gabriël S, Johansen MV, Pozio E, Smit GSA, Devleesschauwer B, Allepuz A, Papadopoulos E, Van Der Giessen J, Dorny P. Human migration and pig/pork import in the European Union: what are the implications for Taenia solium infections? Vet Parasitol. 2015;213:38–45.
Stelzle D, Abraham A, Kaminski M, et al. Clinical characteristics and management of neurocysticercosis patients: a retrospective assessment of case reports from Europe. J Travel Med. 2023;30:1–13.
World Health Organization. WHO guidelines on management of Taenia solium neurocysticercosis. Geneva: World Health Organization; 2021.
Pozio E. (2018) Trichinella and Other Foodborne Nematodes. In: Ortega YR, Sterling CR, editors Food Borne Parasites, Second. pp 175–215.
Feidas H, Kouam MK, Kantzoura V, Theodoropoulos G. Global geographic distribution of Trichinella species and genotypes. Infect Genet Evol. 2014;26:255–66.
Pozio E. World distribution of Trichinella spp. infections in animals and humans. Vet Parasitol. 2007;149:3–21.
Gottstein B, Pozio E, Nöckler K. Epidemiology, diagnosis, treatment, and control of trichinellosis. Clin Microbiol Rev. 2009;22:127–45.
Bruschi F, Angeles Gómez-Morales M, Hill DE. International Commission on trichinellosis: recommendations on the use of serological tests for the detection of Trichinella infection in animals and humans. Food Waterborne Parasitol. 2019;12:e00032.
Koci˛ W. Trichinellosis: human disease, diagnosis and treatment. Vet Parasitol. 2000;93:365–83.
Adroher-Auroux FJ, Benítez-Rodríguez R. Anisakiasis and Anisakis: an underdiagnosed emerging disease and its main etiological agents. Res Vet Sci. 2020;132:535–45.
Morozińska-Gogol J. Anisakis spp. as etiological agent of zoonotic disease and allergy in European region-an overview. Pol Parasitological Soc. 2019;2019:303–14.
Shamsi S, Barton DP. A critical review of anisakidosis cases occurring globally. Parasitol Res. 2023;122:1733–45.
Raouf Rahmati A, Kiani B, Afshari A, Moghaddas E, Williams M, Shamsi S. World-wide prevalence of Anisakis larvae in fish and its relationship to human allergic anisakiasis: a systematic review. Parasitol Res. 2020;119:3585–94.
Ziarati M, Zorriehzahra MJ, Hassantabar F, Mehrabi Z, Dhawan M, Sharun K, Emran T, Bin, Dhama K, Chaicumpa W, Shamsi S. Zoonotic diseases of fish and their prevention and control. Veterinary Q. 2022;42:95–118.
Shimamura Y, Muwanwella N, Chandran S, Kandel G, Marcon N. Common symptoms from an uncommon infection: gastrointestinal anisakiasis. Canadial J Gastroenterol Hepatol. 2016;2016:1–7.
Shrestha S, Kisino A, Watanabe M, Itsukaichi H, Hamasuna K, Ohno G, Tsugu A, Itsukaichi H-S, Tsugu A-S. Intestinal anisakiasis treated successfully with conservative therapy: importance of clinical diagnosis. World J Gastroenterol. 2014;20:598–602.
Liu G-H, Sun M-M, Elsheikha HM, Fu Y-T, Sugiyama H, Ando K, Sohn W-M, Zhu X-Q, Yao C. Human gnathostomiasis: a neglected food-borne zoonosis. Parasit Vectors. 2020;13:616.
Shamsi S, Sheorey H. Seafood-borne parasitic diseases in Australia: are they rare or underdiagnosed? Intern Med J. 2018;48:591–6.
Shamsi S, Suthar J, Zhu X, Barton DP. Infection levels of Gnathostomatidae (Nematoda) larvae in commercial fishes in north-eastern Australian waters and related food safety concerns. Int J Food Microbiol. 2023;403:110340.
Shamsi S, Steller E, Zhu X. The occurrence and clinical importance of infectious stage of Echinocephalus (Nematoda: Gnathostomidae) larvae in selected Australian edible fish. Parasitol Int. 2021;83:102333.
Herman JS, Chiodini PL. Gnathostomiasis, another emerging imported disease. Clin Microbiol Rev. 2009;22:484–92.
Federspiel F, Skovmand S, Skarphedinsson S. Eosinophilic meningitis due to Angiostrongylus cantonensis in Europe. Int J Infect Dis. 2020;93:28–39.
da Silva AJ, Morassutti AL. Angiostrongylus spp. (Nematoda; Metastrongyloidea) of global public health importance. Res Vet Sci. 2021;135:397–403.
Sawanyawisuth K, Sawanyawisuth K. Treatment of angiostrongyliasis. Trans R Soc Trop Med Hyg. 2008;102:990–6.
Perrot-Minnot M-J, Cozzarolo C-S, Amin O, et al. Hooking the scientific community on thorny-headed worms: interesting and exciting facts, knowledge gaps and perspectives for research directions on Acanthocephala. Parasite. 2023;30:1–18.
Fujita T, Waga E, Kitaoka K, et al. Human infection by acanthocephalan parasites belonging to the genus Corynosoma found from small bowel endoscopy. Parasitol Int. 2016;65:491–3.
de FONSECA MENEZESPQF, MCG, Gomes DC, de SÃO CLEMENTE SC, Knoff M. Nematodes and acanthocephalans of hygienic-sanitary importance parasitizing Hyporthodus Niveatus (Valenciennes, 1828) (Actinopterygii) collected from fish markets of the municipality of Niterói, RJ, Brazil. Food Sci Technol. 2023;43:e1119022.
Williams M, Hernandez-Jover M, Shamsi S. Fish substitutions which may increase human health risks from zoonotic seafood borne parasites: a review. Food Control. 2020;118:107429.
Pozio E. How globalization and climate change could affect foodborne parasites. Exp Parasitol. 2020;208:107807.
Semenza JC, Ebi KL. Climate change impact on migration, travel, travel destinations and the tourism industry. J Travel Med. 2019;26:1–13.
Macpherson CNL. Human behaviour and the epidemiology of parasitic zoonoses. Int J Parasitol. 2005;35:1319–31.
Robertson LJ, Sprong H, Ortega YR, van der Giessen JWB, Fayer R. Impacts of globalisation on foodborne parasites. Trends Parasitol. 2014;30:37–52.
Trevisan C, Torgerson PR, Robertson LJ. Foodborne parasites in Europe: Present Status and Future trends trends in Parasitology. Trends Parasitol. 2019;35:695–703.
Murrell KD. The dynamics of Trichinella Spiralis epidemiology: out to pasture? Vet Parasitol. 2016;231:92–6.
Gabriël S, Dorny P, Saelens G, Dermauw V. Foodborne parasites and their Complex Life cycles challenging Food Safety in different food chains. Foods. 2023;12:142.
Gamble HR. Trichinella spp. control in modern pork production systems. Food Waterborne Parasitol. 2022;28:e00172.
Dorny P, Praet N. Taenia saginata in Europe. Vet Parasitol. 2007;149:22–4.
Petterson S, Medema G. How to use the GWPP knowledge? A risk management approach for safe sanitation. Water Sanitation 21st Century: Health Microbiol Aspects Excreta Wastewater Manage (Global Water Pathogen Project). 2019. https://doi.org/10.14321/WATERPATHOGENS.67.
Lightowlers MW. Eradication of Taenia solium cysticercosis: a role for vaccination of pigs. Int J Parasitol. 2010;40:1183–92.
Sander VA, Sánchez López EF, Mendoza Morales L, Ramos Duarte VA, Corigliano MG, Clemente M. Use of Veterinary vaccines for Livestock as a strategy to Control Foodborne Parasitic diseases. Front Cell Infect Microbiol. 2020;10:288.
Hill AA, Horigan V, Clarke KA, Dewé TCM, Stärk KDC, O’brien S, Buncic S. A qualitative risk assessment for visual-only post-mortem meat inspection of cattle, sheep, goats and farmed/wild deer. Food Control. 2014;38:96–103.
Bradbury RS, Sapp SGH, Potters I, et al. Where have all the diagnostic morphological parasitologists gone? J Clin Microbiol. 2022;60:e0098622.
● Gómez-Morales MA, Martínez Castro C, Lalle M, Fernández R, Pezzotti P, Abollo E, Pozio E, Ring Trial T, Participants -testing. UV-press method versus artificial digestion method to detect Anisakidae L3 in fish fillets: comparative study and suitability for the industry. Fish Res. 2018;202:22–8. Exciting advances in non-invasive methods of parasite detection.
Buncic S, Alban L, Blagojevic B. From traditional meat inspection to development of meat safety assurance programs in pig abattoirs-the European situation. Food Control. 2019;106:106705.
Ferri M, Blagojevic B, Maurer P, et al. Risk based meat safety assurance system-An introduction to key concepts for future training of official veterinarians. Food Control. 2023;146:109552.
Alban L, Häsler B, van Schaik G, Ruegg S. Risk-based surveillance for meat-borne parasites. Exp Parasitol. 2020;208:107808.
● Chengat Prakashbabu B, Marshall LR, Crotta M, Gilbert W, Johnson JC, Alban L, Guitian J. (2018) Risk-based inspection as a cost-effective strategy to reduce human exposure to cysticerci of Taenia saginata in low-prevalence settings. Parasit vectors 11:257. There are few studies investigating the economic efficiency of food safety interventions for foodborne helmiths, more studies like this are needed.
● Huang H, Liu L, Ngadi MO. (2014) Recent Developments in Hyperspectral Imaging for Assessment of Food Quality and Safety. Sensors 14:7248–7276. An overview of non-invasive methods for parasite detection.
Xu S, Lu H, Fan C, Qiu G, Ference C, Liang X, Peng J. Visible and near-infrared hyperspectral imaging as an intelligent tool for parasite detection in sashimi. LWT-Food Sci Technol. 2023;181:114747.
Sivertsen AH, Heia K, Stormo SK, Elvevoll E, Nilsen H. Automatic nematode detection in cod fillets (Gadus morhua) by transillumination hyperspectral imaging. J Food Sci. 2011;76:77–83.
Franssen F, Gerard C, Cozma-Petruţ A, et al. Inactivation of parasite transmission stages: efficacy of treatments on food of animal origin. Trends Food Sci Technol. 2019;83:114–28.
Na BK, Pak JH, Hong SJ. Clonorchis sinensis and clonorchiasis. Acta Trop. 2020;203:105309.
Craig P, Ruggiero E, Di, Frohlich KL, Mykhalovskiy E, White M. Taking account of context in the population health intervention research process. Southampton: NIHR Journals Library; 2018.
● Ngwili N, Johnson N, Wahome R, Githigia S, Roesel K, Thomas L. (2021) A qualitative assessment of the context and enabling environment for the control of taenia solium infections in endemic settings. PLoS Negl Trop Dis 15:e0009470. Of relevance to all foodborne helminth controls, lays out the domains of context researchers should consider when designing interventions.
● Galiè A, McLeod A, Campbell ZA, Ngwili N, Terfa ZG, Thomas LF. (2024) Gender considerations in One Health: a framework for researchers. Front Public Health 12:1345273. Again, of relevance to all foodborne helminths, this framework guides researchers in how they can engage with integrated and strategic gender questions in their research.
Macpherson CNL, Bidaisee S. Role of society and culture in the epidemiology and control of foodborne parasites. Foodborne parasites in the Food Supply web: occurrence and control. Woodhead Publishing; 2015. pp. 49–73.
Vandemark LM, Jia TW, Zhou XN. Social Science Implications for Control of Helminth Infections in Southeast Asia. Adv Parasitol. 2010;73:137–70.
Acknowledgements
The Authors would like to dedicate this review to the memory of our friend and colleague Dr Camille Glazer who passed away in February 2023 from acute myeloid leukemia before she had a chance to write this review. Having graduated from the R(D)SVS in 2021, Camille was passionate about the epidemiology of zoonotic infections and improving both human and animal health. Shortly before her tragic death she had been selected to undertake a PhD focussed on T. solium in Malawi as a Wellcome Trust Clinical Research Fellow at the University of Liverpool. She is much missed.
Funding
LFT is supported by the German Federal Ministry for Economic Cooperation and Development through the One Health Research, Education and Outreach Centre in Africa (OHRECA). No additional support was received for the submitted work.
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JBO, MU and LFT wrote the main manuscript and LFT prepared Figs. 1, 2 and 3. All authors reviewed and approved the final manuscript.
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Ortiz, J.B., Uys, M., Seguino, A. et al. Foodborne Helminthiasis. Curr Clin Micro Rpt 11, 153–165 (2024). https://doi.org/10.1007/s40588-024-00231-y
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DOI: https://doi.org/10.1007/s40588-024-00231-y