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. 2023 Dec 12;123(1):28. doi: 10.1007/s00436-023-08021-z

One-health approach on the future application of snails: a focus on snail-transmitted parasitic diseases

Chet Raj Pathak 1,2,✉, Himal Luitel 3, Kjersti Selstad Utaaker 2, Prabhat Khanal 2,✉
PMCID: PMC10713800  PMID: 38082123

Abstract

Snails are fascinating molluscs with unique morphological and physiological adaptive features to cope with various environments. They have traditionally been utilized as food and feed sources in many regions of the world. The future exploitation of alternative nutrient sources, like snails, is likely to increase further. Snails, however, also serve as an intermediate host for several zoonotic parasites. A category of parasitic infections, known as snail-transmitted parasitic diseases (STPDs), is harmful to humans and animals and is mainly driven by various trematodes, cestodes, and nematodes. The environment plays a crucial role in transmitting these parasites, as suitable habitats and conditions can facilitate their growth and proliferation in snails. In light of diverse environmental settings and biologically categorized snail species, this review evaluates the dynamics of significant STPDs of zoological importance. Additionally, possible diagnostic approaches for the prevention of STPDs are highlighted. One-health measures must be considered when employing snails as an alternative food or feed source to ensure the safety of snail-based products and prevent any adverse effects on humans, animals, and the environment.

Keywords: Intermediate host, One-health, Snails, Safety, Zoonotic parasitic diseases

Introduction

Molluscs, such as snails, slugs, and mussels, are a distinct group of spineless animals and play vital roles in the ecosystem (Fortunato 2015; Rosenberg 2014; Vaughn and Hakenkamp 2001). The snail species have been used as a food source in different regions worldwide (Hill et al. 2015; Ngenwi et al. 2010). Many production animals, such as poultry and fish, naturally feed on snails (Amobi et al. 2019; Pertiwi and Saputri 2020). In light of finding novel animal feed ingredients to ensure future food security, snails have been recognized as a potential alternative feed source for production animals that can undergo commercial-scale production (Adeyeye et al. 2020; Munonye and Moses 2019). Snails are considered a valuable supplement to conventional feedstuffs because they contain high levels of protein, calcium, and other essential nutrients (Wright et al. 2018) (Table 1). In addition, snail farming can be operated under relatively low-cost animal husbandry practices that can be profitable in areas where snails are abundant (Mvodo Meyo et al. 2021). Snails have several applications in multiple sectors, such as agriculture, medicine, the food industry, cosmetics, biotechnology, and environmental monitoring, due to their unique biological characteristics and their ability to adapt to changing environments (Akan et al. 2020; Cilia and Fratini 2018; Wang et al. 2020; Yuan et al. 2019) (Table 2). While having a valuable component for various applications, it is noteworthy that they act as agents for serious parasitic disease transmission.

Table 1.

Primary nutrient contents of different snail species (dry matter, DM)

Snail species Items CHO (%DM) TP (%DM) CF (%DM) Ash (%DM) Fat % Ca Fe References
Achatina achatina Fresh snail meat 24.38 63.46 2.88 1.97 2.85 201.36 0.64 Uboh et al. (2014)
Archachatina marginata Fresh snail meat 22.53 63.46 3.01 2.08 2.40 199.26 0.64 Uboh et al. (2014)
Achatina fulica - - 83.13 - 8.90 8.70 - - Ghosh et al. (2016)
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CHO, carbohydrates; TP, total protein; CF, crude fiber; Ca, calcium (mg/100g); Fe, iron (mg/100g)

Table 2.

Various applications of different snail species

Snail species Items Uses/properties References
Archachatina marginata Snail meat Food industry Djikeng et al. (2022)
Lymnaea stagnalis Crude extract, mucus, glycans, polypeptides Cosmetic, pharmaceutical (treatment of wart, cancer, dementia, and Alzheimer’s) Dhiman and Pant (2021)
Lissachatina fulica The mucus of the mantle collar, foot Antioxidant, antibacterial, and anti-tyrosinase activities Noothuan et al. (2021)
Helix aspersa muller Snail mucus Against gastric or peptic ulcers, antibacterial Di Filippo et al. (2022), Gugliandolo et al. (2021)
Achatina fulica Snail mucus Anti-cancer Edison et al. (2021)
Snails Secretions Biotechnology: dual properties on cancer Chang et al. (2020)
Pomacea canaliculata Snail body Environmental monitoring: bioaccumulation of heavy metal analysis Dummee et al. (2012)
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Snail-transmitted parasitic diseases (STPDs) are a significant public health concern in many parts of the world, particularly in tropical and sub-tropical regions (Lu et al. 2018). Snails serve as intermediate hosts in the transmission of various parasites, primarily three classes of helminths: trematodes, nematodes, and cestodes (Chakraborty and Joy 2020; Lopatek et al. 2022). Snails act as single intermediate hosts for certain parasites, such as Angiostrongylus and Schistosoma mansoni, whereas in others, e.g., Clonorchis sinensis, Paragonimus westermani, Fasciolopsis buski, and Fasciola hepatica, snails can be only first intermediate hosts and then the parasitic larva invade other second intermediate hosts like fish, crab, or encysted in the aquatic vegetations for more asexual reproductions (Ansari et al. 2021; Mehmood et al. 2017). After invading snails, the parasites go through some developmental stages. For example, in the case of most trematodes, miracidium penetrates the snails, develops further into sporocyst and redia, and then releases cercaria from the snails (Galaktionov and Dobrovolskij 2013). Then, the cercaria encysts and develops into metacercaria that can enter into livestock and human bodies through the consumption of feed, fodder, food, and water, or cercaria in the case of schistosomes can directly penetrate skins through contaminated water bodies (Lv et al. 2018). It is important to note that not all snail species are suitable for use as animal feed, and it is necessary to choose snail species that are safe, nutritious, and affordable for the intended animal food or feed applications. In this context, understanding the biology of snails and their interactions with parasites and pathogens is crucial for ensuring their safe and sustainable use within the food and feed sector (Colgan 2020; Imathiu 2020; Pissia et al. 2021; Ponder et al. 2019a).

The biology of snails in relation to parasitic disease transmission

Snails are essential hosts for many parasites, including those that cause significant morbidity and mortality in humans and animals. Understanding the physiological processes of snails is crucial to getting insights into the complex interactions between parasites and snail hosts and in developing effective prevention and control measures and management of snail-transmitted parasitic diseases (Lu et al. 2018; Malek 2018; Ponder et al. 2019b).

Characteristics of snail species

Snails are invertebrates belonging to the phylum, Mollusca, which is the second-largest animal group and is quite diverse (Ponder et al. 2019b). Under this phylum, gastropods are the largest, highly diversified class of molluscs consisting of snails and slugs present in saltwater, freshwater, and land. They are characterized by a single spiral shell and a foot for movement (Fig. 1) (Bouchet et al. 2017). Snails are further categorized into multiple orders based on certain morphological features and habitats, each containing several families (Table 3). The families including Achatinidae, Bradybaenidae, Camaenidae, Cyclophoridae, Helicarionidae, Subulinidae, and Succineidae belong to land snails, whereas the freshwater snails include Ampullariidae, Ancyclidae, Acroloxidae, Bithyniidae, Physidae, Planorbidae, Lymnaeidae, Viviparidae, Thiaridae, and Pomatiopsidae (Bouchet et al. 2017; Saadi et al. 2020; Soldatenko and Petrov 2019). Both land and water snail species are susceptible to being infected with at least one parasite during the life cycle from their surrounding environments, and the parasite can surpass the snails’ structural and biochemical barriers. However, the nature or species of the parasite infecting them depends on the body of snails and their physiological status, along with feeding and habitat diversity.

Fig. 1.

Fig. 1

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Three different snail species were collected from Rampur, Chitwan, Nepal (latitude: 27.658734, longitude: 84.35105; 4th September 2022; 28.7 °C). The morphological identification and comparison of published databases (Glöer and Bössneck 2013; Raheem et al. 2010) may suggest the following species: a Lissachatina spp. (Achatinidae), b Gyraulus spp. (Planorbidae), and c Radix spp. (Lymnaeidae)

Table 3.

Classification of important parasite-transmitting snail species

Subclass/order Family Snail species Infecting parasites species References

Pulmonata/Stylommatophora

(Land snails)

 Achatinidae Achatina sp. AC

Brozzo et al. (2020), Ding et al. (2016), Horsáková et al. (2020)

Federspiel et al. (2020), Segeritz et al. (2021), Turck et al. (2022)
Bradybaenidae Bradybaena sp., Euhadra sp., Plectotropis sp.
Camaenidae Satsuma sp., Camaena sp.
Cyclophoridae Pupin sp.
Helicarionidae Parnarion sp.
Subulinidae Allopeas sp., Opeas sp., Subulina sp.
Succineidae Succinea sp.

Pulmonata/Hygrophila

(Freshwater snails)

 Ampullariidae Pila sp., Pomacea sp.
Ancyclidae Ferrissia sp.
Bithyniidae Alocinma sp., Bithynia sp., Parafossarulus sp. CS, OF, OV Naveen and Singh (2019), Ovando and Marchi (2021), Palasio et al. (2018), Saadi et al. (2020), Saito (2022), Schultz et al. (2018); Adema et al. (2017), Anderson and Enabulele (2021), Hailegebriel et al. (2020), Llanwarne and Helmby (2021), Rey et al. (2021), Siles-Lucas et al. (2021)
Physidae Physa sp. AC
Planorbidae Biomphalaria sp. SM, AC
Bulinus sp. SH, SI
Gyraulus sp., Hippeutis sp. AC, FB
Indoplanorbis sp. AC
Lanistes sp. AC, SH
Planorbarius sp. SH
Segmentina sp. AC, CS

Heterobrachia/Basomatophora

(Freshwater snail)

 Lymnaeidae Fossaria sp. FH Ansari et al. (2021), Caldeira et al. (2016), Jackiewicz (2020), Swart et al. (2020); Hu et al. (2021); Lalor et al. (2021)
Galba sp., Lymnaea sp. FH, AC
Omphiscola sp., Pseudosuccinea sp. FH
Radix sp. FH, AC
Stagnicola sp. FH

Prosobrachia/Architaenioglossa

(Freshwater snails)

 Viviparidae Bellamya sp., Cipangopaludina sp., Filopaludina sp., Sinotaia sp. AC Dewi et al. (2017), Jin et al. (2022), Lydeard and Cummings (2019), Uehara et al. (2021)

Prosobrachia/Caenogastropoda

(Freshwater snails)

 Pomatiopsidae Neotricula sp. SMe Haase et al. (2021), Lee et al. (2019), Li et al. (2021), Limpanont et al. (2020)
Oncomelania sp. AC, SJ
Robertsiella sp. SMa

Prosobrachia/Neotaenioglossa

(Sea water snails)

 Buccinidae Clea sp. AC Squires (2022), Yamazaki et al. (2018), Zhang and Zhang (2018)
Thiaridae Melanoides sp. CS, PW, SH Lopes et al. (2021);, Wiggering et al. (2019); Blair (2022), Paller et al. (2021)
Tarebia sp. PW
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AC, Angiostrongylus cantonensis; CS, Clonorchis sinensis; FB, Fasciolopsis buski; FH, Fasciola hepatica; OF, Opisthorchis felineus; OV, Opisthorchis viverrini; PW, Paragonimus westermani; SM, Schistosoma mansoni; SMa, Schistosoma malayensis; SH, Schistosoma haematobium; SMe, Schistosoma mekongi; SJ, Schistosoma japonicum

Anatomical and physiological features of snails

The visceral mass is the main body cavity of the snail that contains digestive, respiratory, and reproductive organs (Fig. 2). The viscera are protected and supported by a species-specific shell containing calcium carbonate (Larsson et al. 2020; Parveen et al. 2020). The one pair of snail’s tentacles helps in sensory perception during the retraction of the head region (Brenzinger et al. 2021). The penetration of the first larval stage (miracidium) of Schistosoma species occurs from the outer surface of the head, foot, and tentacles, near the buccal mass esophagus, whereas the Fasciola species penetrates the mantle collar and anterior wall of the pulmonary sac (Malek 2018). The anatomical features and physiological activities of snails are crucial for the development, proliferation, and spread of pathogens in the body, as discussed below.

Fig. 2.

Fig. 2

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The major physiological systems of the snail. Nervous system in blue, circulatory and respiratory systems in pink, excretory system in green, reproductive system in yellow, digestive system in black, and digestive glands in red color. Adapted and modified from published literature (Ponder et al. 2019b)

The digestive system of snails

Parasites can induce physiological changes and pathology in their hosts, affecting metabolism, immune response, growth, development, and (Marcogliese). In natural environments and also in experimental investigations, fecundity

Parasites can induce systemic physiological changes and pathological lesions in the different organs of snails. Snails with different natures or feeding habits and life stages are prone to infection with a wide range of pathogens via the oral route through contaminated feeding materials (Marcogliese and Pietrock 2011). Land snails possess an esophagus, and the crop for temporary storage and digestion of ingesta, but freshwater snails have a gizzard, which is a strong muscular stomach that helps in the final digestion of ingesta (Fig. 3) (Ponder et al. 2019a; Pouil et al. 2020). Herbivores possess an oral cavity that employs amylase to process food material and eliminate harmful pathogens, allowing both to pass along with ingesta (Escobar-Correas et al. 2019; GHOSE 1961). Conversely, carnivores lack any amylase activity in their oral cavity. Nutrients derived from the digestion of food, such as amino acids, glucose, and fatty acids, can be utilized by the larval stage of parasites like redia and sporocysts (Malek 2018). Any interferences in the digestion of food, absorption, and metabolism of nutrients lead to the loss of tolerance by snails against environmental stress (Ponder et al. 2019b). Once nutrients are absorbed from the gastrointestinal tract of snails, they enter the circulatory system of snails.

Fig. 3.

Fig. 3

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The digestive system contains organs and digestive glands (in red). Adapted and modified from published literature (Ponder et al. 2019b)

The circulatory and respiratory systems of snails

Snails have an open circulatory system with a heart bag serving as the central organ for the pumping of haemolymph (blood) into the body cavity of snails (Fig. 4). Within the cavity, haemolymph bathes various organs and tissues (Ponder et al. 2019a). However, the majority of the larval stages of trematodes, like daughter sporocysts and cercariae, migrate posteriorly or to the distal end opposite to the flow of direction of the haemolymph infecting ovotestis and albumen glands (Malek 2018). Such trematode infections in the respiratory organs of snails lead to inflammatory reactions, congestion, and spread to various organs (Blair 2022; Malek 2018). Hence, the visceral organs of snails are prone to parasitic lodgement, infestation, and inflammatory responses. Thus, snails have adapted their lifestyle to efficiently fulfill their growth and reproductive functions in response to parasitic infections.

Fig. 4.

Fig. 4

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Representing different parts of the excretory in green, circulatory in pink, and respiratory systems in pink of the snail. Adapted and modified from published literature (Ponder et al. 2019b)

The reproductive system of snails

Most snail species are hermaphrodites, as they contain both male and female reproductive organs (Fig. 5). However, cross-fertilization occurs in snails to fertilize their eggs. After fertilization, snails lay eggs under soil or leaves, and the eggs hatch into the small juvenile stage (Fig. 6) (Ponder et al. 2019b). The reproductive system of snails does not appear to have a direct role in the growth and proliferation of infecting parasites, unlike digestive or circulatory systems. The duration of life stages and the development of body structures of snails can vary depending on environmental factors and their nutrient supply (Erkano 2021). As discussed below, the overall reproductive performance and weight gain of snails are affected by the interplay of biotic and abiotic factors surrounding them.

Fig. 5.

Fig. 5

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Representing the reproductive system of a snail: male in yellow and female in orange. Adapted and modified from published literature (Ponder et al. 2019b)

Fig. 6.

Fig. 6

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Representing the general life cycle of a snail. a Fertilized adult snail. b Snails eggs in clusters. c Juveniles. d Adult. e Mating

Environmental factors affecting snails’ growth and parasitic disease transmission

Environmental conditions lead to changes in both the physiology and morphology of snails. External abiotic factors, such as temperature, salinity, oxygen, and pH, influence the physiological processes of snails (Bula et al. 2017; Donham et al. 2022; Saallah et al. 2020).

Temperature

Temperature plays a vital role in the physiochemical activities of snails. For example, in Pila globosa, higher lipid peroxidation (51.8%) and antioxidative activity (26.4%) were reported in the summer than in other seasons (Pati et al. 2023). During environmental stressful situations, heat shock proteins interact with chaperone-assisted proteins to maintain cellular homeostasis and the survival of land snails, Helix pomatia Linnaeus (Idczak-Figiel et al. 2023). During summer, higher physical activities of snails lead to their migration, breeding, and growth. In the freshwater snails (Bulinus glolosus), at the temperatures of 15.5 °C and 36.0 °C, snails were unable to produce eggs, but egg mass output was found to be the highest at 25.8 °C (Kalinda et al. 2017). The optimum temperature for snail hosts and their infecting parasites is around 27 °C. The relative abundance of snail parasites can decrease by 8 to 17%, with the rise in temperature above the optimum level by 1 to 2 °C, respectively (Kalinda et al. 2018). These studies indicate that both snails and infecting parasites require a unique temperature range for their interaction, proliferation, and survival (Nguyen et al. 2020).

Oxygen, salinity, and pH

The abundance of snail species in certain habitats is also determined by their capacity to utilize oxygen either from the air or dissolved in surrounding environments, and this factor is more critical for aquatic snail species. For example, a higher abundance of Bulinus globosus (31.7%) followed by Lymnaea natalensis (21.6%), Lymnaea truncatula (15.1%), and Biomphalaria pfeifferi (14.6%) in the Ethiopian Rift Valley region was associated with variations in the oxygen concentrations of water bodies and the oxygen utilizing abilities of snails (Olkeba et al. 2020). Embryonic survival and development of snails were negatively affected by increased environmental salinity even though embryos reside inside their protective egg mass (Barrios-Figueroa and Urbina 2023). The optimum pH for snails is 7.8 to 8.5. Thus, a rise in acidity can lead to disturbances in the enzymatic activity of snails, and their shells may become more transparent and thinner and crack (O'Sullivan et al. 2011).

There is a lack of comprehensive research on the cellular signaling pathways of snails in response to variations in environmental factors. Understanding the impacts and interactions of various environmental parameters on the growth and physiology of snails and infecting parasites is critical while aiming to exploit snails for various commercial applications.

Snail-transmitted parasitic diseases in animals and humans

STPDs are a significant problem in veterinary and public health, causing heavy economic losses. Based on the class of parasites of snails, STPDs can be divided into three groups: trematode diseases (by infection of flukes such as liver flukes, intestinal flukes, blood flukes, and lung flukes), nematode diseases (rat lungworm infection), and cestode diseases (Davainea infection). The majority of STPDs are responsible for clinical manifestations and lesions in livestock and humans and belong to digenetic trematodes, metastrongyle nematodes, and a few tapeworms (Table 4) (Lu et al. 2018). As discussed in the following, the dietary habits of humans, animals, and birds can influence the prevalence of snail-associated parasitic diseases.

Table 4.

Snail transmitted parasitic diseases: parasite species, intermediate and definitive host, parasitic life stages, transmission, and pathological lesions

DISEASE
Parasite species		 DH Parasitic stage Transmission Pathological lesions References
Snail 2nd IH

FASCIOLOSIS

Fasciola hepatica,

F. gigantica

Human

Sheep

Goat

Cattle

 Mi-Sc-R-C -

Food, water vegetation

Mc via ingestion

 Hepatomegaly, cirrhosis, bile obstruction Lalor et al. (2021), Mehmood et al. (2017), Sabourin et al. (2018)

SCHISTOSOMIASIS

Schistosoma nasalis,

S. mansonia,

S. japonicum,

S. haematobium

Cattle

Human

 Mi-Sc- C - Skin penetration by Cercaria Dermatitis, granuloma of the nasal cavity, intestinal and urogenital carcinoma Anderson and Enabulele (2021)

ECHINOSTOMIASIS

Echinostoma spp.

Birds

Human

 Mi-Sc-R-C Mc in frogs, turtles Ingestion of raw, undercooked meat (molluscan, crustacean) vegetation Periportal lymphocytic infiltration and focal hepatic necrosis Pham et al. (2022), Toledo et al. (2022), Toledo et al. (2019)

PARAGONIMIASIS

Paragonimus westermani

Cattle

Human

 Mi-Sp-R-C

Mc in crabs’,

crustaceans

 Raw and infected undercooked meat of paratenic hosts. Pulmonary, neurological, and abdominal lesions Ahn et al. (2021), Blair (2022)

FASCIOLOPSIS

Fasciolopsis buski

Pigs

Human

 Mi-Sc-R-C -

Foodborne.

Mc via ingestion

 Intestinal mucosal destruction Toledo et al. (2019)

CLONOCHIASIS AND OPISTHORCHIASIS

Clonorchis sinensis,

Opisthorchis felineus,

O. viverrine

Dog

Cat

Human

Pigs

 Mi-Sc-C Mc in fish

Foodborne.

Mc infected fish

 Cholangitis, cirrhosis, hepatic fibrosis/cancer Charoensuk et al. (2022), Fedorova et al. (2020)
EURTYTREMIASIS

Ruminants

Herbivores

 Mi-Sc-C Mc in grasshopper Ingestion of contaminated vegetation Interstitial pancreatitis Schwertz et al. (2015)

ANGIOSTRONGYLIASIS

Angiostrongyliasis cantonensis

Rat

Human

 L1-L2-L3 - Ingestion of IH or paratenic host containing L3 Human neuro-angiostrongyliasis, Eosinophilic meningitis Turck et al. (2022)
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DH, definitive host; IH, intermediate host; Mi, miracidium; Sc, sporocyst; R, redia; C, cercaria; Mc, metacercaria; L1, 1st larval stage; L2, 2nd larval stage; L3, 3rd larval stage

Fasciolosis

The two species of parasites that cause fasciolosis in humans and animals are Fasciola hepatica and Fasciola gigantica, commonly known as liver flukes. Fasciolosis due to F. hepatica is widely distributed worldwide, whereas F. gigantica is found more in Africa, the Middle East, and Asia, with limited distribution of suitable intermediate lymnaeid snail hosts (Mehmood et al. 2017). In the global scenario, fasciolosis has susceptibility to more than 180 million people, whereas more than 35–72 million individuals are considered to be infected with liver fluke (Sabourin et al. 2018). Fasciolosis causes significant economic losses estimated annually at over US$3 billion worldwide (Sabourin et al. 2018).

Liver flukes have a complex life cycle. They involve humans or animals as the definitive host and snails as the intermediate host belonging to the Lymnaeidae family and are responsible for harboring the intermediate stages of liver fluke (miracidium, sporocyst, redia, and cercaria). The ingestion of encysted infective metacercaria stage found on aquatic vegetation is the means of transmission to the final host (Ansari et al. 2021; Caldeira et al. 2016; Hu et al. 2021; Lalor et al. 2021). Preventive measures may include grazing restriction in the areas where snails are abundant or sunlight treatment of grasses from such areas. To prevent human infections, freshwater vegetables should not be consumed raw, because water sources such as artificial irrigation channels are known to harbor snails (Stein 2018). The use of molluscicides or biological means (duck or poultry, plants) can prevent the snail population. One-health approach with multidisciplinary collaborative activities like vaccination of livestock, proper management of freshwater bodies, and improved diagnosis and treatment approaches are crucial steps in mitigating the zoonotic fascioliasis risk (Ali et al. 2017; Mas-Coma et al. 2023). Using triclabendazole to treat human fascioliasis highlights the need to focus on a one-health approach to animal reservoirs for better control (Bargues et al. 2020). Moreover, collaborative efforts from various international organizations, such as the World Health Organization (WHO), the Food and Agriculture Organization (FAO), the World Organization for Animal Health (OIE), and the United Nations Environment Programme (UNEP), could play a pivotal role in controlling and preventing fascioliasis in endemic areas of the world through awareness and education, animal health management, and meat inspection (Corning 2014; Mas-Coma et al. 2023).

Fasciolopsiasis

Fasciolopsiasis is a foodborne zoonotic parasitic disease caused by the infection of Fasciolopsis buski (intestinal fluke) and is transmitted by snails of the Planorbidae family (Lu et al. 2018). Fasciolopsiasis is categorized as a neglected disease by the WHO, and it is considered endemic in specific regions of the Far East and Southeast Asia, especially where pig farming, freshwater habitats, and open-air defecation are common (Siles-Lucas et al. 2021; Toledo et al. 2019). The life cycle of Fasciolopsis buski closely resembles that of Fasciola hepatica and begins with the hatching of eggs into miracidia, and then the miracidia invade snails of the Planorbidae family (Guerrant et al. 2011; Siles-Lucas et al. 2021). The infected snails, e.g., Planorbis spp. and Segmentina spp., with miracidia, often feed on plants fertilized with human night soil. The cercariae of Fasciolopsis buski then emerge and encyst on the tubers or nuts of these plants, and when humans or animals consume these infected plants and their raw derivatives, it can lead to infection (Siles-Lucas et al. 2021). Infections with Fasciolopsis buski are often asymptomatic but can lead to ulcers or abscesses in the duodenum and jejunum, causing epigastric pain resembling peptic ulcer disease (Mas-Coma et al. 2019). Severe cases of fasciolopsiasis may result in eosinophilia, anemia, and systemic allergic symptoms in children (Kimberlin et al. 2022; Long et al. 2012). Preventive measures for both fasciolosis and fasciolopsiasis should include proper sewage disposal, environmental sanitation, education, and personal hygiene (Mas-Coma et al. 2021; Zhou 2022).

Paragonimiasis

Paragonimiasis occurs in humans and animals by eating raw or inadequately cooked crabs or crayfish infected with metacercaria of Paragonimus spp. (Ahn et al. 2021). Several Paragonimus spp. have been reported to cause human infections globally. However, these infections are more common in Asian enclaves, including Korea, Japan, China, Taiwan, the Philippines, Thailand, Vietnam, and India (Blair 2019). Species of snail-like Melanoides and Tarebia act as the first intermediate host (Paller et al. 2021). This disease mainly infects livestock and humans, leading to pathological lesions, most commonly of the pulmonary system, although extra-pulmonary infections in the central nervous system also occur (Ahn et al. 2021). Effective anthelmintic drugs that can be used against paragonimiasis are praziquantel and triclabendazole (Richter 2022). In addition, the application of a one-health approach, such as raising awareness, implementing diagnostics, and emphasizing the importance of preventive measures for parasitic infections, is essential. Moreover, dietary recommendations include avoiding consuming raw or undercooked aquatic meat like freshwater crabs and crayfish and ensuring proper cooking to prevent Paragonimiasis effectively (Farag et al. 2023; Sadhukhan 2022).

Schistosomiasis

The infection of blood fluke of various species of Schistosoma causes schistosomiasis. The WHO has reported that approximately 770 million people are at risk of schistosomiasis, and it is spread over more than 78 countries in Africa, Asia, and Latin America, especially in poor communities (WHO 2022). Biomphalaria, Lanistes, Planorbarius, Neotricula, Oncomelania, Robertsiella, and Melanoides species of snails are responsible for acting as intermediate hosts for these blood flukes (Ovando and Marchi 2021; Saito 2022). The infective stage is either schistosomula or cercarial penetration on the skin (Anderson and Enabulele 2021; Li et al. 2021; Limpanont et al. 2020). The use of night soil (human waste) as fertilizers has been applied since ancient times (Kawa et al. 2019), and it has acted as a potential facilitator for parasites excreted by feces. In China, in 2007, half of the farmers in 36 selected villages applied night soil to crops, and its usage was highly associated with S. japonicum infections (Carlton et al. 2015). A preventive measure for schistosomiasis could be the breaking of the life cycle of the parasite in the endemic areas. The WHO employs several strategies to combat schistosomiasis. One key method is preventive treatment using the drug praziquantel, given as mass drug administration (MDA) (King et al. 2020). This approach targets high-risk populations, like school-age children and adults living in endemic areas (like Sub-Saharan Africa and Yemen), to reduce schistosomiasis infection and related health problems (Deol et al. 2019). The WHO also conducts health education campaigns to inform communities about the disease’s risks, transmission, and prevention, such as creating awareness toward clean and safe water sources in endemic regions. In non-endemic areas (like Europe and North America), strategies have focused on targeting the risks and safety measures for imported cases (Gabrielli and Garba Djirmay 2023). Surveillance systems help monitor disease prevalence and program impact while research improves diagnostics and treatment methods. Such integrated one-health approaches ultimately play a significant role in reducing the burden of schistosomiasis worldwide.

Echinostomiasis

Echinostomiasis is one of the most neglected trematode infections in humans (Toledo et al. 2019). Humans become infected after ingesting raw or insufficiently cooked molluscs, fish, crustaceans, amphibians, or aquatic vegetables (Toledo et al. 2022). Echinostomiasis is endemic in Southeast Asia, the Middle East, and East Africa (Siles-Lucas et al. 2021). Adult Echinostoma spp. of parasites commonly inhabit the intestines of a wide range of birds and mammals, including humans (also recorded in reptiles and fishes) (Pham et al. 2022; Seo et al. 2020; Toledo et al. 2019). The prevalence of echinostomiasis in endemic areas, especially in Sub-Saharan African and Asian countries, remained unchanged despite environmental measures and education (Yigezu et al. 2018). Cercarial infection rates of Echinostome spp. in snail species decreased from 58 to 3.6% between 2007 and 2016 in South-West Ethiopia, which could be due to increased resistance development by snails against the parasitic load (Mengistu et al. 2011; Mereta et al. 2019; Toledo and Esteban 2016). Protecting fishponds from night soil fertilization or fecal contamination, proper waste management, and education campaigns are important measures to protect potential hosts from this parasitic infection (Toledo and Esteban 2016).

Clonorchiasis and opisthorchiasis

Clonorchiasis and opisthorchiasis are parasitic diseases caused by the infections of Clonorchis sinensis, Opisthorchis viverrini, and Opisthorchis felineus flukes (Pozio and Morales 2022). These parasitic diseases are major public health problems affecting over 15 million in the trans-national region of the Mekong River basin in Asian countries: Cambodia, Yunnan Province and Guangxi Zhuang of China, Lao, Myanmar, Thailand, and Vietnam (Sripa et al. 2021). Snails of the Bithyniidae family have a major role in the transmission cycle as the first intermediate host, while fish act as the secondary/paratenic host (Charoensuk et al. 2022; Ovando and Marchi 2021). There should be proper selection, handling, and treatment of food of aquatic origin before consumption, as consumption of undercooked fish is the main route of infection in humans. Education, improving sanitary conditions, and treatment can be effective in preventing infections, especially in areas where human night soil and pig feces have been applied as nourishment for the fish.

Angiostrongyliasis

Angiostrongyliasis has been reported increasingly in parts of Asia, the Pacific islands, Australia, the USA, the Caribbean (initially Cuba), the Caribbean islands, Mallorca, and the Canary Islands. It is now widely distributed across many tropical/sub-tropical and a few more temperate localities, with the parasite found in numerous host species (Turck et al. 2022). It is estimated that more than 7000 cases of neuro-angiostrongyliasis have been reported in humans (Niebuhr et al. 2019). Angiostrongylus cantonensis (rat lungworm), the causative agent for angiostrongyliasis, is a nematode parasite having a complex life cycle where rats are the final hosts, gastropods (snails) act as intermediate hosts, and with several paratenic hosts (freshwater prawns/shrimp, crabs, flatworms, fish, frogs, toads, lizards, and centipedes) (Turck et al. 2022). The wide range of snail species (more than 60) belonging to gastropods is responsible for harboring the intermediate larval stage of this nematode (Brozzo et al. 2020; Segeritz et al. 2021; Turck et al. 2022). Since the wide range of infections occurs in different snail species and humans and other animals, it is crucial to raise awareness of the associated dangers of consuming snails as food and feeding materials. These food preferences are regarded as customs in, for example, China and Thailand, where undercooked snails have been consumed for generations (Wang et al. 2012). Changing such preferences may be challenging regardless of educational efforts. In Thailand, studies have shown that Angiostrongylus parasites, responsible for human angiostrongyliasis, were present in up to 33.3% of snail species, including Pila virescens and Pomacea canaliculata (Watthanakulpanich et al. 2021). For better prevention and control of angiostrongyliasis, regular screening and monitoring of its associated parasite in food, meat, and environment are needed, potentially applying one-health principles for the presence of the infective parasite (Sears et al. 2021; Turck et al. 2022).

Application of diagnostic techniques to detect the STPDs

The successful application of diagnostic techniques or tools for detecting the presence of parasites in snails, environment/habitats (water, soil), paratenic hosts, and the definitive hosts requires accurate knowledge of species of parasites and their snail vectors. Such techniques should be rapid, sensitive, and robust for detecting and identifying different stages of parasites (Hammoud et al. 2022). These diagnostic tools are crucial for adequately managing STPDs, limiting their spread from the environment to snails, humans, and animals (Table 5).

Table 5.

An overview of multiple diagnostic techniques to detect snail-transmitted parasites

Diagnostic technique types Diagnostic principle Advantages Disadvantages References
Direct shedding Microscopy and culture-based

• Examination of snail tissues, body fluid, and shedding material

• Relatively cheaper

 • Need expert in malacology and parasitology Joof et al. (2020)
ELISA and ICA Serology-based Ag-Ab reactions

• Sensitive and more specific than conventional approaches

• Best for disease screening in endemic areas

 • Sometimes, cross-reactivity can occur Yuan et al. (2023)
Conventional PCR Genetic material amplification and detection

• Possible to detect DNA or RNA from both parasites and snail hosts

• Confirmatory test

• Needs an equipped laboratory

• More expensive compared to microscopy and serology

 Rathinasamy et al. (2021)
qPCR coupled with eDNA PCR and genomics

• Highly sensitive to the detection of tiny amounts of organism genes from soil and water

• More precise and can cover a broader habitat than conventional PCR

• Needs an equipped lab

• Can be more expensive compared to conventional PCR, serology

 Rathinasamy et al. (2021)
LAMP Amplification of genetic material

• Simple and rapid

• Assist to improve current surveillance techniques (like eDNA)

 • False-positive result due to primer-primer reaction and contamination Tran et al. (2022)
Open in a new tab

ELISA, enzyme-linked immunosorbent assay; ICA, immunochromatographic assays: PCR, polymerase chain reaction: qPCR, quantitative polymerase chain reaction; eDNA, environmental DNA; LAMP, loop-mediated isothermal amplification; Ag, antigen; Ab, antibody

Direct shedding and microscopy are the traditional techniques used for the detection/identification of parasites in snails, where the snail tissues and their shedding materials are examined under a microscope to visualize the parasites (Joof et al. 2020). Serology-based techniques, for example, enzyme-linked immunosorbent assay (ELISA) and immunochromatographic assays (ICA), can be sensitive and specific for detecting parasitic antigens in snail tissues or body fluids (Yuan et al. 2023). The polymerase chain reaction (PCR) techniques were found to be more sensitive than the conventional shedding techniques for the detection of infection of S. mansoni in the Biomphalaria species of snails (Joof et al. 2020).

Multiplex PCR (simultaneous detection of multiple species of parasites and snails) and qPCR (amenable to high-throughput and multiplexing, sensitive, faster, cheaper) are methods of choice coupled with environmental DNA (eDNA). The eDNA detection technique can be a potential tool for monitoring of parasitic agents in water/soil samples (Jones et al. 2018). The limit of detection of the eDNA assays for the detection of Fasciola hepatica and snails (Austropeplea tomentosa) was observed to be 14 fg and 50 fg genomic DNA, respectively, in water samples (Rathinasamy et al. 2021). Thus, such eDNA-based techniques can be useful in detecting snail-borne parasites in various environmental samples (Rathinasamy et al. 2021).

Loop-mediated isothermal amplification (LAMP) is another molecular technique that is simple and rapid and can be used for the detection of parasites in snails (Tran et al. 2022). Recently, it has been suggested that LAMP results for certain STPDs, such as schistosomiasis, appear to be comparable to or better than commonly used diagnostic techniques (García-Bernalt Diego et al. 2021). PCR is a widely used molecular technique used for the detection of DNA or RNA either from parasites or from snails.

Future perspectives

It is noteworthy that STPDs are not only a concern of public health, but they also have the potential to be cross-transmitted between animals and birds. STPDs, like schistosomiasis, fascioliasis, and angiostrongyliasis, pose a significant threat to human and animal health globally (Hammoud et al. 2022). In the future, proper prevention and control of STPDs appears to be a significant challenge for public health systems and veterinary medicine. The one-health approach to most STPDs requires broader collaborative efforts between human and animal health professionals, environmental experts, and public health authorities. Promoting surveillance, health education, veterinary care, and environmental management can mitigate the risks and minimize the transmission of these STPDs. With advancements in diagnostic and treatment methods, there is hope for better management of these diseases, especially with the application of one-health approaches (Fig. 7).

Fig. 7.

Fig. 7

Open in a new tab

Demonstrating the multiple aspects of a one-health approach for STPDs. IH, intermediate host; PH, paratenic host

The dynamics of STPDs are likely to be affected by several factors, climate change, modified temperature, and rainfall patterns, which can affect the distribution and abundance of snail species and, consequently, the transmission of the diseases (Bula et al. 2017; Donham et al. 2022; Saallah et al. 2020). Likewise, urbanization and globalization can facilitate the spread of snails and parasites across borders and increase human exposure through travel and trade (Celis-Ramírez et al. 2022). While snails can serve as hosts for disease-causing parasites, it is important to note that they also play important roles in ecosystems as food sources for other animals and as decomposers. Therefore, any efforts to control snail populations and STPDs should be implemented in a naturally responsible manner and considered in conjunction with the current epidemiological situation in the endemic areas.

Snails are high in protein content, making them a nutritious food source for livestock and other animals (Uboh et al. 2014). Moreover, they efficiently convert feed into biomass, requiring fewer resources than traditional livestock (Mvodo Meyo et al. 2021). However, it is noted that snails can serve as hosts for disease-causing parasites, and there is a risk that these parasites could be transmitted to animals consuming snail-based feed. In addition, if snails are not raised under proper conditions, they may accumulate harmful substances in their tissues that could be toxic to animals (Bula et al. 2017; Donham et al. 2022; Saallah et al. 2020). Therefore, the establishment of appropriate protocols and methods for snail farming is essential to producing safe and nutritious snails that lead to minimal risks associated with the spread of STPDs. Moreover, strict regulations and monitoring should be put in place to ensure that snails used for animal feed are free from harmful substances and parasites.

Looking forward, the potential of snails as an alternative feed source should be explored further while ensuring that any hazards associated with their use are minimized. With careful planning and management, snails have the potential to be commercially utilized as food or feed sources that are sustainable, safe, and nutritious for humans and animals.

Conclusions

Snails are natural scavengers and play a vital role in the ecosystem. Both land and water snail species are prone to be infected with parasites from their surrounding environments. The physiological systems and visceral organs of snails are prone to parasitic lodgement, infestation, and inflammatory responses, and such parasitic infections in snails can compromise the growth and development of snails. As snails appear to be increasingly exploited for food or feed applications in the future, parasites invading snails can transmit to humans and animals. Such transmission can increase the risks of various parasitic diseases in humans and animals, including but not limited to fasciolosis, fasciolopsiasis, schistosomiasis, and angiostrongyliasis. These STPDs pose significant threats to human and animal health globally. Understanding the impacts and interactions of various abiotic factors on the growth and physiology of snails and infecting parasites is critical while aiming to exploit snails for various commercial applications. In this context, the application of a one-health concept is necessary to maximize the commercial utilization of snails as food and feed while minimizing the risks of snail-associated parasitic diseases. Various diagnostic tools can assist in detecting snail-infecting parasites in food, feed, animals, and the environment. The integrated use of more sensitive, specific, and cheaper diagnostic tools allows simultaneous monitoring of disease prevalence for better control and prevention of STPDs. Moreover, appropriate farming methods and protocols for snails must be developed, and regulations should be put in place to minimize the associated hazards of using snails as an alternative nutrient source. As the potential of snails as an alternative source of feed for animals is promising, future research efforts are necessary to ensure the safe and responsible use of snails for the benefit of human, animal, and environmental health.

Acknowledgements

The authors would like to thank the members of the Khanal Laboratory (KLab) for their scientific input and discussion.

Abbreviations

AC

Angiostrongylus cantonensis

C

Cercaria

Ca

Calcium

CF

Crude fiber

CHO

Carbohydrates

CS

Clonorchis sinensis

DH

Definitive host

IH

Intermediate host

FB

Fasciolopsis buski

Fe

Iron

DM

Dry matter

FG

Fasciola gigantica

FH

Fasciola hepatica

L1

1st larval stage

L2

2nd larval stage

L3

3rd larval stage

Mc

Metacercaria

Mi

Miracidium

OF

Opisthorchis felineus

OV

Opisthorchis viverrini

PW

Paragonimus westermani

R

Redia

Sc

Sporocyst

SH

Schistosoma haematobium

SJ

Schistosoma japonicum

SM

Schistosoma mansoni

SMa

Schistosoma malayensis

SMe

Schistosoma mekongi

STPDs

Snail transmitted parasitic diseases

TP

Total protein

Author contributions

CRP: Conceptualization, Visualization, Validation, Writing – Original Draft; Review and Editing; HL: Project administration, Validation, Supervision, Review & Editing; KSU: Validation, Review and Editing; PK: Conceptualization, Visualization, Validation, Supervision, Funding, Project administration, Resources, Validation, Review and Editing. All authors have read and approved the final manuscript.

Funding

Open access funding provided by Nord University. This study was supported by the CEER project (Project number: 2021/10345) funded by the Norwegian Agency for International Cooperation and Quality Enhancement in Higher Education (HK-dir) under the Norwegian Partnership Program for Global Academic Cooperation (NORPART) with support from the Norwegian Ministry of Education and Research (MER).

Data availability

Not applicable.

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Chet Raj Pathak, Email: crpathak@afu.edu.np.

Prabhat Khanal, Email: prabhat.khanal@nord.no.

References

  1. Adema CM, et al. Whole genome analysis of a schistosomiasis-transmitting freshwater snail. Nat Commun. 2017;8(1):15451. doi: 10.1038/ncomms15451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adeyeye SAO, Bolaji OT, Abegunde TA, Adesina TO. Processing and utilization of snail meat in alleviating protein malnutrition in Africa: a review. Nutr Food Sci. 2020;50(6):1085–1097. doi: 10.1108/NFS-08-2019-0261. [DOI] [Google Scholar]
  3. Ahn CS, et al. Spectrum of pleuropulmonary paragonimiasis: an analysis of 685 cases diagnosed over 22 years. J Inf Secur. 2021;82(1):150–158. doi: 10.1016/j.jinf.2020.09.037. [DOI] [PubMed] [Google Scholar]
  4. Akan M, Michling F, Matti K, Krause S, Muno-Bender J, Wendland J. Snails as taxis for a large yeast biodiversity. Fermentation. 2020;6(3):90. doi: 10.3390/fermentation6030090. [DOI] [Google Scholar]
  5. Ali SM, et al. Field use of molluscicides in schistosomiasis control programmes: an operational manual for programme managers. World Health Organization; 2017. [Google Scholar]
  6. Amobi M, Ebenebe C, Nwobodo J, Ezenwaeya G, Okereke N, Okpoko V. Effects of snail offal meal on performance of broiler chickens. Int J Livest Prod. 2019;10(2):43–48. doi: 10.5897/IJLP2018.0552. [DOI] [Google Scholar]
  7. Anderson TJ, Enabulele EE. Schistosoma mansoni. Trends Parasitol. 2021;37(2):176–177. doi: 10.1016/j.pt.2020.06.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ansari B et al (2021) Molecular phylogenetics of Physa acuta (Pulmonata: Basommatophora): an invasive species in Central Punjab Pakistan. Braz J Biol 83. 10.1590/1519-6984.246984 [DOI] [PubMed]
  9. Bargues MD, et al. Genetic uniformity, geographical spread and anthropogenic habitat modifications of lymnaeid vectors found in a One Health initiative in the highest human fascioliasis hyperendemic of the Bolivian Altiplano. Parasit Vectors. 2020;13:1–19. doi: 10.1186/s13071-020-04045-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Barrios-Figueroa R, Urbina M. Behavioural and physiological responses to salinization and air exposure during the ontogeny of a freshwater South American snail. Conserv Physiol. 2023;11(1):coac089. doi: 10.1093/conphys/coac089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Blair D. Digenetic Trematodes. 2019. Paragonimiasis; pp. 105–138. [Google Scholar]
  12. Blair D. Lung flukes of the genus Paragonimus: ancient and re-emerging pathogens. Parasitology. 2022;149(10):1286–1295. doi: 10.1017/S0031182022000300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Bouchet P, et al. Revised classification, nomenclator and typification of gastropod and monoplacophoran families. Malacologia. 2017;61(1-2):1–526. doi: 10.4002/040.061.0201. [DOI] [Google Scholar]
  14. Brenzinger B, Schrödl M, Kano Y. Origin and significance of two pairs of head tentacles in the radiation of euthyneuran sea slugs and land snails. Sci Rep. 2021;11(1):21016. doi: 10.1038/s41598-021-99172-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Brozzo A, et al. Molecular phylogeny and trait evolution of Madeiran land snails: radiation of the Geomitrini (Stylommatophora: Helicoidea: Geomitridae) Cladistics. 2020;36(6):594–616. doi: 10.1111/cla.12440. [DOI] [PubMed] [Google Scholar]
  16. Bula W, Leiwakabessy F, Rumahlatu D. The influence of environmental factors on the diversity of gastropods in Marsegu Island, Maluku. Biosaintifika. 2017;9(3):483–491. [Google Scholar]
  17. Caldeira RL, Teodoro TM, Jannotti-Passos LK, Lira-Moreira PM, Goveia CDO, Carvalho ODS (2016) Characterization of South American snails of the genus Biomphalaria (Basommatophora: Planorbidae) and Schistosoma mansoni (Platyhelminthes: Trematoda) in molluscs by PCR-RFLP. Biomed Res Int 2016. 10.1155/2016/1045391 [DOI] [PMC free article] [PubMed]
  18. Carlton EJ, Liu Y, Zhong B, Hubbard A, Spear RC. Associations between schistosomiasis and the use of human waste as an agricultural fertilizer in China. PLoS Negl Trop Dis. 2015;9(1):e0003444. doi: 10.1371/journal.pntd.0003444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Celis-Ramírez M, Quintero-Angel M, Varela-M RE. Control of invasive alien species: The Giant African snail (Lissachatina fulica) a difficult urban public management challenge. J Environ Manag. 2022;322:116159. doi: 10.1016/j.jenvman.2022.116159. [DOI] [Google Scholar]
  20. Chakraborty K, Joy M. High-value compounds from the molluscs of marine and estuarine ecosystems as prospective functional food ingredients: an overview. Food Res Int. 2020;137:109637. doi: 10.1016/j.foodres.2020.109637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Chang Z, et al. Snail promotes the generation of vascular endothelium by breast cancer cells. Cell Death Dis. 2020;11(6):457. doi: 10.1038/s41419-020-2651-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Charoensuk L, Ribas A, Chedtabud K, Prakobwong S. Infection rate of Opisthorchis viverrini metacercariae in cyprinoid fish from the markets and its association to human opisthorchiasis in the local community in the Northeast Thailand. Acta Trop. 2022;225:106216. doi: 10.1016/j.actatropica.2021.106216. [DOI] [PubMed] [Google Scholar]
  23. Cilia G, Fratini F (2018) Antimicrobial properties of terrestrial snail and slug mucus. J Complement Integr Med 15(3). 10.1515/jcim-2017-0168 [DOI] [PubMed]
  24. Colgan D. Molluscan Research and the sustainable development goals. Taylor & Francis; 2020. pp. 283–285. [Google Scholar]
  25. Corning S. World Organisation for Animal Health: strengthening Veterinary Services for effective One Health collaboration. Rev Sci Tech. 2014;33(2):639–650. doi: 10.20506/rst.33.2.2305. [DOI] [PubMed] [Google Scholar]
  26. Deol AK, et al. Schistosomiasis-assessing progress toward the 2020 and 2025 global goals. N Engl J Med. 2019;381(26):2519–2528. doi: 10.1056/NEJMoa1812165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Dewi V, Sato S, Yasuda H. Effects of a mud snail Cipangopaludina chinensis laeta (Architaenioglossa: Viviparidae) on the abundance of terrestrial arthropods through rice plant development in a paddy field. Appl Entomol Zool. 2017;52:97–106. doi: 10.1007/s13355-016-0458-8. [DOI] [Google Scholar]
  28. Dhiman V, Pant D. Human health and snails. J Immunoass Immunochem. 2021;42(3):211–235. doi: 10.1080/15321819.2020.1844751. [DOI] [PubMed] [Google Scholar]
  29. Di Filippo MF, et al. Effectiveness of snail slime in the green synthesis of silver nanoparticles. Nanomaterials. 2022;12(19):3447. doi: 10.3390/nano12193447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ding HL, et al. Revision of sinistral land snails of the genus Camaena (Stylommatophora, Camaenidae) from China based on morphological and molecular data, with description of a new species from Guangxi, China. Zookeys. 2016;584:25. doi: 10.3897/zookeys.584.7173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Djikeng FT, et al. Effect of different processing methods on the proximate composition, mineral content, and functional properties of snail (Archachatina marginata) meat. J Agric Food Res. 2022;8:100298. doi: 10.1016/j.jafr.2022.100298. [DOI] [Google Scholar]
  32. Donham EM, Strope LT, Hamilton SL, Kroeker KJ. Coupled changes in pH, temperature, and dissolved oxygen impact the physiology and ecology of herbivorous kelp forest grazers. Glob Chang Biol. 2022;28(9):3023–3039. doi: 10.1111/gcb.16125. [DOI] [PubMed] [Google Scholar]
  33. Dummee V, Kruatrachue M, Trinachartvanit W, Tanhan P, Pokethitiyook P, Damrongphol P. Bioaccumulation of heavy metals in water, sediments, aquatic plant and histopathological effects on the golden apple snail in Beung Boraphet reservoir, Thailand. Ecotoxicol Environ Saf. 2012;86:204–212. doi: 10.1016/j.ecoenv.2012.09.018. [DOI] [PubMed] [Google Scholar]
  34. Edison A, Hendra P, Sidharta BBR, Herwiyanti S, Jacub C. Inhibitory activity of snail (Achatina Fulica (Lam.) Bowdich) mucus on growth of mammary cancer in rat induced with DMBA (7, 12-Dimethylbenz (Α) Anthracene) J Pharm Sci Commun. 2021;18(2):102–111. doi: 10.24071/jpsc.002525. [DOI] [Google Scholar]
  35. Erkano WK. Impacts of environmental parameters on the infectivity of freshwater Snail. Intech Open; 2021. [Google Scholar]
  36. Escobar-Correas S, Mendoza-Porras O, Dellagnola FA, Colgrave ML, Vega IA. Integrative proteomic analysis of digestive tract glycosidases from the invasive golden apple snail, Pomacea canaliculata. J Proteome Res. 2019;18(9):3342–3352. doi: 10.1021/acs.jproteome.9b00282. [DOI] [PubMed] [Google Scholar]
  37. Farag MA, Mansour ST, Nouh RA, Khattab AR. Crustaceans (shrimp, crab, and lobster): a comprehensive review of their potential health hazards and detection methods to assure their biosafety. J Food Saf. 2023;43(1):e13026. doi: 10.1111/jfs.13026. [DOI] [Google Scholar]
  38. Federspiel F, Skovmand S, Skarphedinsson S. Eosinophilic meningitis due to Angiostrongylus cantonensis in Europe. Int J Infect Dis. 2020;93:28–39. doi: 10.1016/j.ijid.2020.01.012. [DOI] [PubMed] [Google Scholar]
  39. Fedorova OS, et al. Opisthorchis felineus infection, risks, and morbidity in rural Western Siberia, Russian Federation. PLoS Negl Trop Dis. 2020;14(6):e0008421. doi: 10.1371/journal.pntd.0008421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Fortunato H. Mollusks: tools in environmental and climate research. Am Malacol Bull. 2015;33(2):310–324. doi: 10.4003/006.033.0208. [DOI] [Google Scholar]
  41. Gabrielli AF, Garba Djirmay A (2023) Schistosomiasis in Europe. Curr Trop Med Rep:1–9. 10.1007/s40475-023-00286-9
  42. Galaktionov KV, Dobrovolskij A. The biology and evolution of trematodes: an essay on the biology, morphology, life cycles, transmissions, and evolution of digenetic trematodes. Springer Science & Business Media; 2013. [Google Scholar]
  43. García-Bernalt Diego J, Fernández-Soto P, Febrer-Sendra B, Crego-Vicente B, Muro A. Loop-mediated isothermal amplification in schistosomiasis. J Clin Med. 2021;10(3):511. doi: 10.3390/jcm10030511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Ghose KC. Observations on the digestive enzymes and cellulolytic bacteria of the giant land snail Achatina fulica and their occurrence in the Gastropoda. Proc Zool Soc Lond. 1961;137(1):127–133. doi: 10.1111/j.1469-7998.1961.tb06165.x. [DOI] [Google Scholar]
  45. Ghosh S, Jung C, Meyer-Rochow VB. Snail farming: an Indian perspective of a potential tool for food security. Ann Aquac Res. 2016;3(3):1–6. doi: 10.47739/2379-0881/1024. [DOI] [Google Scholar]
  46. Glöer P, Bössneck U. Freshwater molluscs from Nepal and North India with the description of seven new species. Arch Molluskenkd. 2013;142(1):137–156. doi: 10.1127/arch.moll/1869-0963/142/137-156. [DOI] [Google Scholar]
  47. Guerrant RL, Walker DH, Weller PF. Tropical infectious diseases: principles, pathogens and practice e-book. Elsevier Health Science; 2011. [Google Scholar]
  48. Gugliandolo E, et al. Protective effect of snail secretion filtrate against ethanol-induced gastric ulcer in mice. Sci Rep. 2021;11(1):3638. doi: 10.1038/s41598-021-83170-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Haase M, Grego J, Erőss ZP, Farkas R, Fehér Z (2021) On the origin and diversification of the stygobiotic freshwater snail genus Hauffenia (Caenogastropoda: Hydrobiidae) with special focus on the northern species and the description of two new species. Eur J Tax 775:143-184-143-184. 10.5852/ejt.2021.775.1555
  50. Hailegebriel T, Nibret E, Munshea A (2020) Prevalence of Schistosoma mansoni and S. haematobium in snail intermediate hosts in Africa: a systematic review and meta-analysis. J Trop Med. 10.1155/2020/8850840 [DOI] [PMC free article] [PubMed]
  51. Hammoud C, et al. Simultaneous genotyping of snails and infecting trematode parasites using high-throughput amplicon sequencing. Mol Ecol Resour. 2022;22(2):567–586. doi: 10.1111/1755-0998.13492. [DOI] [PubMed] [Google Scholar]
  52. Hill EA, Hunt CO, Lucarini G, Mutri G, Farr L, Barker G. Land gastropod piercing during the Late Pleistocene and early Holocene in the Haua Fteah, Libya. J Archaeol Sci Rep. 2015;4:320–325. doi: 10.1016/j.jasrep.2015.09.003. [DOI] [Google Scholar]
  53. Horsáková V, Nekola JC, Horsák M. Integrative taxonomic consideration of the Holarctic Euconulus fulvus group of land snails (Gastropoda, Stylommatophora) Syst Biodivers. 2020;18(2):142–160. doi: 10.1080/14772000.2020.1725172. [DOI] [Google Scholar]
  54. Hu R-S, et al. Differential expression of microRNAs and tRNA fragments mediate the adaptation of the liver fluke Fasciola gigantica to its intermediate snail and definitive mammalian hosts. Int J Parasitol. 2021;51(5):405–414. doi: 10.1016/j.ijpara.2020.10.009. [DOI] [PubMed] [Google Scholar]
  55. Idczak-Figiel PA, Ostrowski M, Nowakowska A (2023) The influence of environmental stressful conditions on the interaction between heat shock proteins and chaperone-assisted proteins in land snails, Helix pomatia L. Can J Zool. 10.1139/cjz-2023-0118
  56. Imathiu S. Benefits and food safety concerns associated with consumption of edible insects. Nutri Food Sci J. 2020;18:1–11. doi: 10.1016/j.nfs.2019.11.002. [DOI] [Google Scholar]
  57. Jackiewicz M. Phylogeny and relationships within European species of the family Lymnaeidae (Gastropoda: Pulmonata: Basommatophora) Folia Malacol. 2020;5(1):61–95. doi: 10.12657/folmal.005.003. [DOI] [Google Scholar]
  58. Jin W, et al. Chromosome-level genome assembly of the freshwater snail Bellamya purificata (Caenogastropoda) Zool Res. 2022;43(4):683. doi: 10.24272/j.issn.2095-8137.2022.118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Jones RA, et al. Detection of Galba truncatula, Fasciola hepatica and Calicophoron daubneyi environmental DNA within water sources on pasture land, a future tool for fluke control? Parasit Vectors. 2018;11(1):1–9. doi: 10.1186/s13071-018-2928-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Joof E, Andrus PS, Sowunmi K, Onyango VM, Wade CM. Comparing PCR techniques against conventional cercarial shedding methods for detecting Schistosoma mansoni infection in Biomphalaria snails. Acta Trop. 2020;212:105716. doi: 10.1016/j.actatropica.2020.105716. [DOI] [PubMed] [Google Scholar]
  61. Kalinda C, Chimbari MJ, Grant WE, Wang H-H, Odhiambo JN, Mukaratirwa S. Simulation of population dynamics of Bulinus globosus: effects of environmental temperature on production of Schistosoma haematobium cercariae. PLoS Negl Trop Dis. 2018;2(8):e0006651. doi: 10.1371/journal.pntd.0006651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Kalinda C, Chimbari MJ, Mukaratirwa S. Effect of temperature on the Bulinus globosus — Schistosoma haematobium system. Infect Dis Poverty. 2017;6(1):57. doi: 10.1186/s40249-017-0260-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Kawa NC, et al. Night soil. Ethnobiol Lett. 2019;10(1):40–49. doi: 10.14237/ebl.10.1.2019.1351. [DOI] [Google Scholar]
  64. Kimberlin D, Fischer M, Long SS, Prober CG. Principles and practice of pediatric infectious diseases E-Book. Elsevier Health Sciences; 2022. [Google Scholar]
  65. King CH, et al. Impact of different mass drug administration strategies for gaining and sustaining control of Schistosoma mansoni and Schistosoma haematobium infection in Africa. Am J Trop Med Hyg. 2020;103(1 Suppl):14. doi: 10.4269/ajtmh.19-0829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Lalor R, et al. Pathogenicity and virulence of the liver flukes Fasciola hepatica and Fasciola gigantica that cause the zoonosis Fasciolosis. Virulence. 2021;12(1):2839–2867. doi: 10.1080/21505594.2021.1996520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Larsson J, Westram AM, Bengmark S, Lundh T, Butlin R. A developmentally descriptive method for quantifying shape in gastropod shells. J R Soc Interface. 2020;17(163):20190721. doi: 10.1098/rsif.2019.0721. [DOI] [Google Scholar]
  68. Lee SY, Lee HJ, Kim YK. Comparative analysis of complete mitochondrial genomes with Cerithioidea and molecular phylogeny of the freshwater snail, Semisulcospira gottschei (Caenogastropoda, Cerithioidea) Int J Biol Macromol. 2019;135:1193–1201. doi: 10.1016/j.ijbiomac.2019.06.036. [DOI] [PubMed] [Google Scholar]
  69. Li HM, et al. Nucleic acid amplification techniques for the detection of Schistosoma mansoni infection in humans and the intermediate snail host: a structured review and meta-analysis of diagnostic accuracy. Int J Infect Dis. 2021;112:152–164. doi: 10.1016/j.ijid.2021.08.061. [DOI] [PubMed] [Google Scholar]
  70. Limpanont Y, Phuphisut O, Reamtong O, Adisakwattana P. Recent advances in Schistosoma mekongi ecology, transcriptomics and proteomics of relevance to snail control. Acta Trop. 2020;202:105244. doi: 10.1016/j.actatropica.2019.105244. [DOI] [PubMed] [Google Scholar]
  71. Llanwarne F, Helmby H. Granuloma formation and tissue pathology in Schistosoma japonicum versus Schistosoma mansoni infections. Parasite Immunol. 2021;43(2):e12778. doi: 10.1111/pim.12778. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Long SS, Pickering LK, Prober CG. Principles and practice of pediatric infectious disease. Elsevier Health Sciences; 2012. [Google Scholar]
  73. Lopatek M, Wieczorek K, Osek J. Prevalence and antimicrobial resistance of bacterial foodborne pathogens isolated from raw bivalve molluscs subjected to consumption in Poland during a ten-year period. Foods. 2022;11(21):3521. doi: 10.3390/foods11213521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Lopes AS, Pulido-Murillo EA, López-Hernández D, de Melo AL, Pinto HA. First report of Melanoides tuberculata (Mollusca: Thiaridae) harboring a xiphidiocercaria in Brazil: a new parasite introduced in the Americas? Parasitol Int. 2021;82:102284. doi: 10.1016/j.parint.2021.102284. [DOI] [PubMed] [Google Scholar]
  75. Lu XT, et al. Snail-borne parasitic diseases: an update on global epidemiological distribution, transmission interruption and control methods. Infect Dis Poverty. 2018;7:1–16. doi: 10.1186/s40249-018-0414-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Lv S, et al. Invasive Pomacea snails as important intermediate hosts of Angiostrongylus cantonensis in Laos, Cambodia and Vietnam: Implications for outbreaks of eosinophilic meningitis. Acta Trop. 2018;183:32–35. doi: 10.1016/j.actatropica.2018.03.021. [DOI] [PubMed] [Google Scholar]
  77. Lydeard C, Cummings KS. Freshwater mollusks of the world: a distribution atlas. JHU Press; 2019. [Google Scholar]
  78. Malek EA. Snail transmitted parasitic diseases: volume I. CRC Press; 2018. [Google Scholar]
  79. Marcogliese DJ, Pietrock M. Combined effects of parasites and contaminants on animal health: parasites do matter. Trends Parasitol. 2011;27(3):123–130. doi: 10.1016/j.pt.2010.11.002. [DOI] [PubMed] [Google Scholar]
  80. Mas-Coma S, Valero MA, Bargues MD. Digenetic Trematodes. 2019. Fascioliasis; pp. 71–103. [DOI] [PubMed] [Google Scholar]
  81. Mas-Coma S, Valero MA, Bargues MD (2023) One Health for fascioliasis control in human endemic areas. Trends Parasitol. 10.1016/j.pt.2023.05.009 [DOI] [PubMed]
  82. Mas-Coma S, et al. Domestic pig prioritized in one health action against fascioliasis in human endemic areas: experimental assessment of transmission capacity and epidemiological evaluation of reservoir role. One Health. 2021;13:100249. doi: 10.1016/j.onehlt.2021.100249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Mehmood K, et al. A review on epidemiology, global prevalence and economical losses of fasciolosis in ruminants. Microb Pathog. 2017;109:253–262. doi: 10.1016/j.micpath.2017.06.006. [DOI] [PubMed] [Google Scholar]
  84. Mengistu M, Shimelis T, Torben W, Terefe A, Kassa T, Hailu A. Human intestinal schistosomiasis in communities living near three rivers of Jimma town, southwestern Ethiopia. Ethiop J Health Sci. 2011;21(2):111–118. doi: 10.4314/ejhs.v21i2.69051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Mereta ST, et al. Environmental determinants of distribution of freshwater snails and trematode infection in the Omo Gibe River Basin, southwest Ethiopia. Infect Dis Poverty. 2019;8(1):1–10. doi: 10.1186/s40249-019-0604-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Munonye J, Moses P. Profitability analysis of snail farming in Owerri agricultural zone Imo state. AES; 2019. [Google Scholar]
  87. Mvodo Meyo ES, Nkemasong ZA, Shu G, Ngono JPN, Ngosong C. Snail farming as an alternative profitable livestock system for sustainable development sustainable development in Africa: fostering sustainability in one of the world’s most promising continents. Springer; 2021. pp. 477–490. [Google Scholar]
  88. Naveen Y, Singh A. Shell morphometric traits showing normal distribution pattern and positive correlation in freshwater snail, Lymnaea luteola (Hygrophila: Lymnaeidae) J Exp Zoology India. 2019;22(1):273–278. [Google Scholar]
  89. Ngenwi A, Mafeni J, Etchu K, Oben F. Characteristics of snail farmers and constraints to increased production in West and Central Africa. Afr J Environ Sci Technol. 2010;4(5):274–278. [Google Scholar]
  90. Nguyen K, Gemmell B, Rohr J. Effects of temperature and viscosity on miracidial and cercarial movement of Schistosoma mansoni: ramifications for disease transmission. Int J Parasitol. 2020;50(2):153–159. doi: 10.1016/j.ijpara.2019.12.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Niebuhr C, Jarvi SI, Siers SR. A review of rat lungworm infection and recent data on its definitive hosts in Hawaii. Hum Wildl Interact. 2019;13(2):238–249. [Google Scholar]
  92. Noothuan N, Apitanyasai K, Panha S, Tassanakajon A. Snail mucus from the mantle and foot of two land snails, Lissachatina fulica and Hemiplecta distincta, exhibits different protein profile and biological activity. BMC Res Notes. 2021;14(1):1–7. doi: 10.1186/s13104-021-05557-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Olkeba BK, et al. Environmental and biotic factors affecting freshwater snail intermediate hosts in the Ethiopian Rift Valley region. Parasit Vectors. 2020;13(1):1–13. doi: 10.1186/s13071-020-04163-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. O'Sullivan C, Fried B, Sherma J. Studies on the pH tolerance of freshwater snails. Trends Comp Biochem Physiol. 2011;15:63–66. [Google Scholar]
  95. Ovando XM, Marchi GF. An annotated checklist of Planorbinae (Heterobranchia, Hygrophila, Planorbidae) from northwestern Argentina. Check List. 2021;17(6):1493–1507. doi: 10.15560/17.6.1493. [DOI] [Google Scholar]
  96. Palasio RGS, Zanotti-Magalhães EM, Tuan R (2018) Genetic diversity of the freshwater snail Biomphalaria tenagophila (d'Orbigny, 1835) (Gastropoda: Hygrophila: Planorbidae) across two coastal areas of southeast Brazil. Folia Malacol 26(4). 10.12657/folmal.026.019
  97. Paller VG et al (2021) Paragonimus westermani infection of freshwater crab Sundathelphusa philippina and melaniid snails in Cadacan River in Irosin, Sorsogon, Philippines. J Parasit Dis:1–9. 10.1007/s12639-020-01340-3 [DOI] [PMC free article] [PubMed]
  98. Parveen S, Chakraborty A, Chanda DK, Pramanik S, Barik A, Aditya G. Microstructure analysis and chemical and mechanical characterization of the shells of three freshwater snails. ACS Omega. 2020;5(40):25757–25771. doi: 10.1021/acsomega.0c03064. [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Pati SG, Panda F, Samanta L, Paital B. Spatio-temporal changes in oxidative stress physiology parameters in apple snail Pila globosa as a function of soil Mg, Ca, organic carbon and aquatic physico-chemical factors. Environ Geochem Health. 2023;45:2591–2610. doi: 10.1007/s10653-022-01376-9. [DOI] [PubMed] [Google Scholar]
  100. Pertiwi MP, Saputri DD (2020) Golden apple snail (Pomacea canaliculata) as an alternative protein source in Pasupati catfish (Pangasius sp.) fish feed. Nus Biosci 12(2). 10.13057/nusbiosci/n120212
  101. Pham LTK, Saijuntha W, Lawton SP, Le TH. Mitophylogenomics of the zoonotic fluke Echinostoma malayanum confirms it as a member of the genus Artyfechinostomum Lane, 1915 and illustrates the complexity of Echinostomatidae systematics. Parasitol Res. 2022;121(3):899–913. doi: 10.1007/s00436-022-07449-z. [DOI] [PubMed] [Google Scholar]
  102. Pissia MΑ, Matsakidou A, Kiosseoglou V. Raw materials from snails for food preparation. Future Foods. 2021;3:100034. doi: 10.1016/j.fufo.2021.100034. [DOI] [Google Scholar]
  103. Ponder WF, Lindberg DR, Ponder JM. Biology and evolution of the mollusca, volume 1. CRC Press; 2019. [Google Scholar]
  104. Ponder WF, Lindberg DR, Ponder JM. Biology and evolution of the mollusca, volume 2. CRC Press; 2019. [Google Scholar]
  105. Pouil S, Jones NJ, Smith JG, Mandal S, Griffiths NA, Mathews TJ. Comparing trace element bioaccumulation and depuration in snails and mayfly nymphs at a coal ash-contaminated site. Environ Toxicol Chem. 2020;39(12):2437–2449. doi: 10.1002/etc.4857. [DOI] [PubMed] [Google Scholar]
  106. Pozio E, Morales MAG. Clonorchiasis and Opisthorchiasis helminth infections and their impact on global public health. Springer; 2022. pp. 221–256. [Google Scholar]
  107. Raheem D, Budha P, Naggs F, Preece R. An illustrated guide to the land snails of Nepal. London: The Natural History Museum; 2010. [Google Scholar]
  108. Rathinasamy V, et al. Towards understanding the liver fluke transmission dynamics on farms: detection of liver fluke transmitting snail and liver fluke-specific environmental DNA in water samples from an irrigated dairy farm in Southeast Australia. Vet Parasitol. 2021;291:109373. doi: 10.1016/j.vetpar.2021.109373. [DOI] [PubMed] [Google Scholar]
  109. Rey O, et al. Population genetics of African Schistosoma species. Infect Genet Evol. 2021;89:104727. doi: 10.1016/j.meegid.2021.104727. [DOI] [PubMed] [Google Scholar]
  110. Richter J. Current status of the treatment of paragonimiasis. Lung Cancer. 2022;8:10. [Google Scholar]
  111. Rosenberg G. A new critical estimate of named species-level diversity of the recent Mollusca. Am Malacol Bull. 2014;32(2):308–322. doi: 10.4003/006.032.0204. [DOI] [Google Scholar]
  112. Saadi AJ, Davison A, Wade CM. Molecular phylogeny of freshwater snails and limpets (Panpulmonata: Hygrophila) Zool J Linnean Soc. 2020;190(2):518–531. doi: 10.1093/zoolinnean/zlz177. [DOI] [Google Scholar]
  113. Saallah S, Ishak N, Sarbon N. Effect of different molecular weight on the antioxidant activity and physicochemical properties of golden apple snail (Ampullariidae) protein hydrolysates. Food Res. 2020;4(4):1363–1370. doi: 10.26656/fr.2017.4(4).348. [DOI] [Google Scholar]
  114. Sabourin E, Alda P, Vázquez A, Hurtrez-Boussès S, Vittecoq M. Impact of human activities on fasciolosis transmission. Trends Parasitol. 2018;34(10):891–903. doi: 10.1016/j.pt.2018.08.004. [DOI] [PubMed] [Google Scholar]
  115. Sadhukhan SK. Prevention and control of parasitic zoonoses textbook of parasitic zoonoses. Springer; 2022. pp. 83–90. [Google Scholar]
  116. Saito T (2022) First record of the non-indigenous freshwater snail Galba humilis (Say, 1822) (Mollusca: Hygrophila: Lymnaeidae) in Japan. Bioinvasions Rec 11(2). 10.3391/bir.2022.11.2.16
  117. Schultz JH, Bu L, Adema CM. Comparative immunological study of the snail Physella acuta (Hygrophila, Pulmonata) reveals shared and unique aspects of gastropod immunobiology. Mol Immunol. 2018;101:108–119. doi: 10.1016/j.molimm.2018.05.029. [DOI] [PubMed] [Google Scholar]
  118. Schwertz CI, et al. Eurytrematosis: an emerging and neglected disease in South Brazil. World J Exp Med. 2015;5(3):160. doi: 10.5493/wjem.v5.i3.160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  119. Sears WJ, et al. AcanR3990 qPCR: a novel, highly sensitive, bioinformatically informed assay to detect Angiostrongylus cantonensis infections. Clin Infect Dis. 2021;73(7):e1594–e1600. doi: 10.1093/cid/ciaa1791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Segeritz L, Cardona A, Taubert A, Hermosilla C, Ruiz A. Autochthonous Angiostrongylus cantonensis, Angiostrongylus vasorum and Aelurostrongylus abstrusus infections in native terrestrial gastropods from the Macaronesian Archipelago of Spain. Parasitol Res. 2021;120:2671–2680. doi: 10.1007/s00436-021-07203-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Seo M, et al. Ancient echinostome eggs discovered in archaeological strata specimens from a Baekje Capital Ruins of South Korea. J Parasitol. 2020;106(1):184–187. doi: 10.1645/19-55. [DOI] [PubMed] [Google Scholar]
  122. 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. doi: 10.1016/j.rvsc.2020.10.011. [DOI] [PubMed] [Google Scholar]
  123. Soldatenko EV, Petrov AA. Musculature of the penial complex: a new criterion in unravelling the phylogeny of Hygrophila (Gastropoda: Pulmonata) J Morphol. 2019;280(4):508–525. doi: 10.1002/jmor.20960. [DOI] [PubMed] [Google Scholar]
  124. Squires RL (2022) The earliest Ancistrolepis (Gastropoda: Buccinidae) and its geologic implications. Paleo Bios 39(2). 10.5070/P939257077
  125. Sripa B, Suwannatrai AT, Sayasone S, Do DT, Khieu V, Yang Y. Current status of human liver fluke infections in the Greater Mekong Subregion. Acta Trop. 2021;224:106133. doi: 10.1016/j.actatropica.2021.106133. [DOI] [PubMed] [Google Scholar]
  126. Stein E. Microbiologically safe foods. Scientific e-Resources; 2018. [Google Scholar]
  127. Swart EM, Starkloff NC, Ypenburg S, Ellers J, van Straalen NM, Koene JM. The effect of mating on female reproduction across hermaphroditic freshwater snails. Invertebr Biol. 2020;139(1):e12275. doi: 10.1111/ivb.12275. [DOI] [Google Scholar]
  128. Toledo R, Álvarez-Izquierdo M, Esteban JG, Muñoz-Antoli C. Neglected food-borne trematodiases: echinostomiasis and gastrodiscoidiasis. Parasitol. 2022;149(10):1319–1326. doi: 10.1017/S0031182022000385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  129. Toledo R, Alvárez-Izquierdo M, Muñoz-Antoli C, Esteban JG. Digenetic Trematodes. 2019. Intestinal trematode infections; pp. 181–213. [DOI] [PubMed] [Google Scholar]
  130. Toledo R, Esteban J. An update on human echinostomiasis. Trans R Soc Trop Med Hyg. 2016;110(1):37–45. doi: 10.1093/trstmh/trv099. [DOI] [PubMed] [Google Scholar]
  131. Tran L, Toet H, Beddoe T. Environmental detection of Fasciola hepatica by loop-mediated isothermal amplification. PeerJ. 2022;10:e13778. doi: 10.7717/peerj.13778. [DOI] [PMC free article] [PubMed] [Google Scholar]
  132. Turck HC, Fox MT, Cowie RH (2022) Paratenic hosts of Angiostrongylus cantonensis and their relation to human neuroangiostrongyliasis globally. One Health:100426. 10.1016/j.onehlt.2022.100426 [DOI] [PMC free article] [PubMed]
  133. Uboh FE, Williams IO, Essien NC. Effect of processing on the proximate and mineral composition of Archachatina marginata and Achatina achatina. Food Public Health. 2014;4(1):10–14. [Google Scholar]
  134. Uehara H, Murakami H, Yusa Y. Predation by the carrion crow Corvus corone (Passeriformes: Corvidae) on the apple snail Pomacea canaliculata (Architaenioglossa: Ampullariidae) in different locations in Japan. Appl Entomol Zool. 2021;56(3):385–392. doi: 10.1007/s13355-021-00747-5. [DOI] [Google Scholar]
  135. Vaughn CC, Hakenkamp CC. The functional role of burrowing bivalves in freshwater ecosystems. Freshw Biol. 2001;46(11):1431–1446. doi: 10.1046/j.1365-2427.2001.00771.x. [DOI] [Google Scholar]
  136. Wang J, Lu X, Zhang J, Ouyang Y, Qin Z, Zhao B. Using golden apple snail to mitigate its invasion and improve soil quality: a biocontrol approach. Environ Sci Pollut Res. 2020;27:14903–14914. doi: 10.1007/s11356-020-07998-9. [DOI] [PubMed] [Google Scholar]
  137. Wang QP, Wu ZD, Wei J, Owen R, Lun ZR. Human Angiostrongylus cantonensis: an update. Eur J Clin Microbiol Infect Dis. 2012;31:389–395. doi: 10.1007/s10096-011-1328-5. [DOI] [PubMed] [Google Scholar]
  138. Watthanakulpanich D, et al. Co-occurrence of Angiostrongylus malaysiensis and Angiostrongylus cantonensis DNA in cerebrospinal fluid: Evidence from human eosinophilic meningitis after ingestion of raw snail dish in Thailand. Food Waterborne Parasitol. 2021;24:e00128. doi: 10.1016/j.fawpar.2021.e00128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  139. WHO . WHO guideline on control and elimination of human schistosomiasis. World Health Organization; 2022. [PubMed] [Google Scholar]
  140. Wiggering B, Neiber MT, Krailas D, Glaubrecht M. Biological diversity or nomenclatural multiplicity: the Thai freshwater snail Neoradina prasongi Brandt, 1974 (Gastropoda: Thiaridae) Syst Biodivers. 2019;17(3):260–276. doi: 10.1080/14772000.2019.1606862. [DOI] [Google Scholar]
  141. Wright AC, Fan Y, Baker GL. Nutritional value and food safety of bivalve molluscan shellfish. J Shellfish Res. 2018;37(4):695–708. doi: 10.2983/035.037.0403. [DOI] [Google Scholar]
  142. Yamazaki T, Sonoda T, Nobetsu T, Goshima S. Contribution to the knowledge of the taxonomy of the Japanese species of Volutharpa (Gastropoda: Buccinidae) Venus. 2018;76(1-4):1–18. [Google Scholar]
  143. Yigezu G, et al. Habitat suitability modelling for predicting potential habitats of freshwater snail intermediate hosts in Omo-Gibe river basin, Southwest Ethiopia. Ecol Inform. 2018;45:70–80. doi: 10.1016/j.ecoinf.2018.04.002. [DOI] [Google Scholar]
  144. Yuan L, et al. Resveratrol inhibits the invasion and metastasis of colon cancer through reversal of epithelial-mesenchymal transition via the AKT/GSK-3β/Snail signaling pathway Corrigendum in/10.3892/mmr. 2022.12870. Mol Med Rep. 2019;20(3):2783–2795. doi: 10.3892/mmr.2019.10528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  145. Yuan X, et al. The 22nd chromatography component of the Fasciola gigantica excretory-secretory products decreased the proliferation of peripheral blood mononuclear cells from buffalo. Animals. 2023;13(4):564. doi: 10.3390/ani13040564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  146. Zhang S, Zhang S. Three species of Siphonalia Adams, 1863 (Gastropoda, Buccinidae) from China seas, with descriptions of two new species. J Oceanol Limnol. 2018;36(6):2333–2336. doi: 10.1007/s00343-019-7218-x. [DOI] [Google Scholar]
  147. Zhou X-N. Infectious Diseases of Poverty: progress achieved during the decade gone and perspectives for the future. Infec Dis Poverty. 2022;11:1–4. doi: 10.1186/s40249-021-00931-3. [DOI] [PMC free article] [PubMed] [Google Scholar]

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