Abstract
Schistosomiasis, a neglected tropical disease (NTD), is one of the most prevalent parasitoses in the World. Certain freshwater snail species are the intermediate host in the life cycle of schistosome species. Controlling snails employing molluscicides is an effective, quick, and convenient intervention strategy to prevent the spread of Schistosoma species in endemic regions. Advances have been made in develo** both synthetic molluscicides and molluscicides derived from plants. However, at present, the development of molluscicides is not adapted to the actual demand for snails and schistosoma controlling. We undertake a systematic review of exploitation and application of synthetic molluscicides and molluscicides derived from plants to combat intermediate host snails. The detailed molluscicidal activity, structure–activity relationship, structural feature, and possible mechanism of some molluscicides are also highlighted, which may afford an important reference for the design of new, more effective molluscicides with low environmental impact and realize the aim of controlling schistosome at transmission stages.
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Introduction
Schistosomiasis, a neglected tropical disease (NTD), is one of the most important infectious parasitoses of humans and animals in the tropical and subtropical regions (Njoroge et al. 2014; Thétiot-Laurent et al. 2013). It is estimated that schistosomiasis could affect more than 200 million people in approximately 70 countries (WHO (World Health Organization) 2021, 2020). About 700 million people live in endemic area (Colley et al. 2014). Six species of the genus Schistosoma including S. japonicum, S. mansoni, S. haematobium, S. mekongi, S. malayensis, and S. intercalatum can cause disease in people (Gryseels et al. 2006). The life cycle of the parasite is complex with an intermediate host (Oncomelania snails), definitive host (humans and mammals), and seven lifecycle stages involving the adult worm, egg, miracidium, mother sporocyst, daughter sporocyst, cercariae, and schistosomulum (Colley et al. 2014; Guo et al. 2008, 2015). It is a great challenge to control schistosomiasis in undeveloped regions because of financial burden and environmental pressures. The current strategies for schistosomiasis control mainly rely on snail control, drug treatment (such as Praziquantel), advanced sanitation, and health education (Limpanont et al. 2020). Although the present method for the control of schistosomiasis is largely based on drug treatment, snail control using molluscicides still plays a crucial role (de Souza 1995; Yuan et al. 2005; Wang et al. 2009).
There are three major species of snails acting as the intermediate hosts: Oncomelania hupensis (O. hupensis) for S. japonicum, Biomphalaria species for S. mansoni, and Bulinus species for S. haematobium (Sturrock 1995). At present, three main strategies including biological control, ecological control, and molluscicidal control have been carried out for the control of schistosome snails (Lardans and Dissous 1998; McCullough et al. 1980). For biological control, some natural predators of snails such as aquatic birds, turtles, fish, crayfish, and insects have been considered as well as competitor snails (Madsen 1990; Ohmae et al. 2003; Pointier and Jourdane 2000; Li et al. 2016). Furthermore, some small creatures such as trematodes, leeches, nematodes, rotifers, and ostracods can attack or devour the snails (Younes et al. 2017). However, the above biological control experiments were often investigated in the laboratory; further field studies are essential in evaluating the control of the snails. The ecological control is also a useful approach including advanced sanitation, agricultural and hydrological exploitation and management (Dong et al. 2018; Liang et al. 2018). However, the potential risk factors are negligible including the limited natural resources, extreme climate changes, and severe financial burden (Lo et al. 2018).
Up to now, the application of molluscicides is the most effective intervention strategy for the control of snails in endemic regions (King et al. 2015). For example, chemical treatment using molluscicides was performed in an area of 78,308.26 hectare in China, and environmental improvements were only carried out in an area of 4738.37 hectare in 2018 (Zhang et al. 2019). Great efforts have been made to explore all kinds of molluscicidal substances including chemical and plant molluscicides (Perrett and Whitfield 1996; de Paula-Andrade et al. 2019). Herein, we undertake a systematic review of molluscicides, and their detailed molluscicidal activity, structure–activity relationship, and possible mechanism of some molluscicides are also highlighted.
Development of chemical molluscicides
Inorganic salts
Copper sulfate (CuSO 4 )
Copper sulfate (compound 1, Table 1, Tab. S1, see Supplementary materials) was evaluated as molluscicides to combat B. alexandrina snails in Egypt (Hoffman and Zakhary 1953). The mortality of snails could reach 100% within 2 weeks at 0.25 ppm. Copper sulfate is an inexpensive inorganic salt. However, the toxicity of the molluscicides on non-target organisms and secondary environmental pollution issues are not ignorable.
Calcium cyanamide
Calcium cyanamide (2, Table 1) was previously reported as an efficient molluscicide for O. hupensis and has low toxicity for fish and other aquatic animals (Wei et al. 2008). The mortality of snails was up to 100% after 2 days at 80 ppm in immersion experiments, which is not good for a molluscicide. In pesticide spraying experiments in the laboratory, the mortality of snails was also 100% after 1 day with the concentration of 30 g/m2. While in natural field conditions, the mortality of snails was 97.18% at 50 ppm. In the field spraying experiments, the mortalities of snails were 81.11% and 96.03% in the concentrations of 30 and 50 g/m2 in 15 days, respectively (Wei et al. 2008). Calcium cyanamides exhibited low toxicity to other aquatic animals at the effective concentration. Further molluscicidal mechanism investigation showed that calcium cyanamide could damage epithelial cells, hepatocytes, and muscle cells of snails (**a et al. 2010). However, for calcium cyanamide, the toxicological explorations are worth of further investigation for practical applications.
Organic molluscicides
Sodium 2,3,4,5,6-pentachlorophenolate (NaPCP) and its derivatives
Sodium 2,3,4,5,6-pentachlorophenolate (3, Table 1) was found to have molluscicidal activity (LC50 = 0.54 ppm, LC100 = 2.0 ppm, 48 h) in immersion experiments (Moon et al. 1958; Zhang et al. 2006). In field experiments, NaPCP was effective at dosages of 10–20 ppm (immersion method) and 5–10 g/m2 (spraying method). Furthermore, NaPCP could kill snail eggs, young snails, and adult snails (Zhang et al. 2006). However, NaPCP has toxicity against fish, aquatic animals, and mammals, along with the risk of teratogenicity, carcinogenesis, and mutagenicity (** et al. 2016). In addition, the technical products of NaPCP often contain highly toxic tetrachloro dibenzodioxines and dibenzofuranes, and that these agents can also arise from light exposure or heat (fire) of pentachlorophenol-contaminated objects. Subsequently, the molluscicidal activity of sodium 2,5-dichloro-4-bromophenol (4, Table 1) was explored for the control of O. nasophora in immersion experiments (Kajihara et al. 1979). The LC50 and LC90 values of sodium 2,5-dichloro-4-bromophenol were 0.54 ppm and 1.59 ppm. Additionally, this compound showed lower toxicity than NaPCP for carp, rainbow trout, and killifish.
N-Bromoacetamide and its derivatives
N-Bromoacetamide (5, Table 1) exhibited molluscicidal activity against adult snails, young snails, and snail eggs, and low toxicity to fish (Zhu et al. 1984). The LC50 and LC90 values were 0.64 ppm and 1.0 ppm in immersion experiments in 24 h, respectively. The mortality of snails exceeded 80% after 7 days at a surface concentration of 1 g/m2 in spraying tests (Zhu et al. 1984). In particular, N-bromoacetamide has the advantages of low-dosage, good solubility in water, low toxicity and non-mutagenicity, which may be an ideal molluscicidal candidate. Nicotinanilide (6, Table 1) was also found to have the same molluscicidal activity as N-bromoacetamide (Sukumaran et al. 2004). The LC50 values of nicotinanilide against different stages of snails were 0.23 ppm (immature snails), 0.77 ppm (young mature snails), and 0.59 ppm (adult snails) in 24 h, respectively. In field immersion experiments, nicotinanilide could kill 95% of the snails at the concentration of 1–2 ppm in 3 days. Nicotinanilide was also harmless to humans, animals, fish, and plant (Sukumaran et al. 2004). Disadvantages include strong irritation to human skin, low toxicity to snail eggs, and high cost, which seriously restrict the large-scale application of the molluscicide.
Dipterex
Dipterex (7, Table 1) is an important organic phosphorous pesticide. Dipterex displayed promising molluscicidal activity, and the mortality of snails was 96% at 10 ppm in 3 days (Xu et al. 2016). Huang’s group explored the molluscicidal activity of 4% niclosamide ethanolamine salt powder-granula (PG) derived from niclosamide ethanolamine salt and additives (You et al. 2016). Compared with 4% NESDP, PG showed lower mortalities of the snails (O. hupensis) in laboratory test. However, in field experiments, for PG, the mortalities of snails were 91.71% (1 day) and 92.91% (3 days), which were higher than that of 4% NESDP with the mortalities of snails of 71.09% (1 day) and 90.11% (3 days). 4% PG has the advantages of good adsorption and penetrability, which may be more suitable for field applications.
To solve the solubility of niclosamide, emulsifiable concentrate of 25% niclosamide (ECN) was further prepared from niclosamide, organic solvents, and emulsifiers (Dai et al. 2007). In immersion experiments, the LC50 values of ECN were 0.041 ppm (24 h), 0.032 ppm (48 h), and 0.029 ppm (72 h), respectively, significantly lower than the control groups of SCN and WPN. ECN has more chance to contact snails, resulting in better molluscicidal activities. However, the addition of solvents and emulsifiers causes higher cost of molluscicide and environmental pollution.
Three new polymeric controlled release formulations of niclosamide (B1, B2, and B3) against B. alexandrina were developed by Kenawy et al. (Kenawy and Rizk 2004). These polymeric formulations were prepared either by the chemical modifications of poly(glycidyl methacrylate) or by physical entrapment of the niclosamide in calcium alginate beads. In the immersion experiments, LC50 values were 0.098 ppm (B1), 1.09 ppm (B2), and 0.073 ppm (B3), respectively. For B3, the mortality of snails was still up to 100% after 10 days. The polymeric molluscicide (B3) showed the highest molluscicidal activity than B1 and B2.
Recently, Harras et al. reported a new polymeric molluscicide-attractant from niclosamide and L-glutamate by a controlled-release technology to control B. alexandrina (Kenawy et al. 2020). The alginate niclosamide-L-glutamate formulation had good affinity ability to snails. The polymeric formulations B3-4b-L-glutamate (0.3 ppm niclosamide and 75% L-glutamate) caused the aggregation of snails and showed 100% mortality after 5 days. The novel polymer-niclosamide-L-glutamate not only prolonged the validity and efficiency of the niclosamide, but also still was effective at low concentrations with increasing concentrations of the applied attractants, which could reduce the toxicity to the ecosystem.
Though excellent advances on novel niclosamide formulations have been accomplished, there is still a huge challenge to reduce the toxicity through the structure modification strategy.
Yuan et al. reported the sodium of niclosamide sodium quinoid-2′, 5-dichloro-4′-nitrosalicylanilide (13, Table 1) (LDS) obtained through the reaction of NaOH with niclosamide (Yuan et al. 2011). LDS showed better solubility in water and ethanol, and lower toxicity than that of niclosamide. The molluscicidal activities of 10% LDS and 50% WPN were further investigated (Yuan et al. 2011). In immersion experiments, the mortalities of snails for LDS and WPN were 100% and 96.7% at 0.4 ppm in 72 h, respectively. In spraying experiments, the mortalities of snails for LDS and WPN were up to 100% and 97.3%, respectively. In field immersion and spraying experiments, LDS and WPN showed the similar molluscicidal activities (Xu et al. 2007; Zhang et al. 2013). In addition, LDS exhibited climbing-inhibition effect against snails (O. hupensis), and the cost of LDS was also less than that of WPN (** of novel formulations and rational structural modification may be an important research area.
Pyridylphenylureas
Wang et al. developed a series of pyridylphenylurea derivatives against B. straminea snails through the introduction of a urea functional group into the structure of nicotinanilide (Wang et al. 2018). For compounds 21 and 22 (Table 1), the mortalities against adult snails were all up to 100% at 1.0 ppm, and the LC50 values were 0.50 ppm and 0.51 ppm in immersion experiments, respectively (LC90 = 0.98 and 0.78 ppm). And the LC50 values against snail eggs were 0.05 ppm and 0.09 ppm, respectively (LC90 = 0.21 and 0.39 ppm). The acute lethal fish toxicity experimental results revealed that the safe dose of compound 22 was up to 5 ppm, which was higher than that of the effective molluscicidal dose (LC90, 0.78 ppm).
Furthermore, compound 21 (named PPU07) was made into the form of 25% PPU07 sulfate WP. The field molluscicidal activity and toxicity of 25% PPU07 sulfate WP were investigated against O. hupensis and local fish (Chen et al. 2019). In the spraying experiments, the mortality of snails was up to 95% at the concentration of 2.0 g/m2. When snails were exposed in the 2.0 g/m3 of the 25% PPU07 sulfate WP, the mortality reached 96%. In the spraying and immersion trials, the WHO-recommended molluscicidal concentrations of niclosamide were 1 g/m2 and 1 g/m3, respectively. Additionally, 25% PPU07 sulfate WP showed little toxicity to local fish and other aquatic organisms at the effective molluscicidal concentrations. PPU07 could be explored as promising molluscicide candidate for the control of snails.
Nitro-compounds
Abreu et al. explored the molluscicidal activity of nitroaromatic compounds against B. glabrata snails (de Abreu et al. 2001). Compounds 23–26 (Table 1) presented a significant bioactivity and the LC50 values of them (23, LC50 = 1.8 ppm; 24a, LC50 = 8.2 ppm; 24b, LC50 = 0.7 ppm; 25, LC50 = 7.6 ppm; 26, LC50 = 6.4 ppm) were lower than 10 ppm in 24 h. Further electrochemical tests revealed that the presence of the electro-active NO2 group in the molecular structures was crucial for the retention of molluscicidal activity. Bond et al. also discovered the molluscicidal activity of 4-(substituted phenoxy)-3,β-dinitrostyrenes against B. glabrata (Bond et al. 1969). The LC50 values of compounds 27a-d (Table 1) were 8.5, 12, 8.5, and 22 ppm, respectively. It is notable that β-nitrostyrene 28 (Table 1) displayed the best activity among the tested compounds (LC50 = 1.3 ppm).
Phenolic compounds
Lahlou et al. prepared some phenolic compounds for the control of Bulinus truncates snails (Lahlou 2004). Compounds 29–31 (Table 1) demonstrated good molluscicidal activity (29, LC50 = 8.89 ppm, LC90 = 16.82 ppm; 30, LC50 = 3.60 ppm, LC90 = 4.47 ppm; 31, LC50 = 7.71 ppm, LC90 = 14.14 ppm). The compound 30 was the most effective among the phenolic products.
Chalcones and its derivatives
Adewunmi et al. tested the molluscicidal activity of a serial of chalcones and chalcone epoxides (32, Table 1) against B. glabrata snails (Adewunmi et al. 1987). An appropriate hydrophile-lipophile balance in the structure of chalocones should facilitate the improvement of activity. For example, the mortality of compound 32c against snails was up to 100% at 10 ppm in 24 h; however, the activity of compound 32f declined dramatically (37.5% mortality) when the two OH groups were methylated. Furthermore, the epoxidation of the chalcones also resulted in the loss of molluscicidal activity. Nawwar et al. investigated the molluscicidal activity of several l-(hydroxy/substituted phenyl) propenones (33–35, Table 1) against B. alexandria snails (Nawwar et al. 1993). The activity of the prepared compounds was related to the conjugated system. Compounds 34a–c showed the best results among the synthetic products. Especially compound 34b afforded 100% mortality of the snails at 2 ppm in 24 h. When the furan moiety was removed, the molluscicidal activity exhibited negative results. Barsoum et al. evaluated the molluscicidal activity of bis[1-aryl-2-propen- 1-ones] (chalcones) (36a–h, Table 1) and bis[3-aryl-4,5-dihydro-1H-pyrazol-1-carboxaldehydes] (37a–h, Table 1) against B. alexandrina snails (Barsoum et al. 2006). Most of the synthesized products showed moderate bioactivity at 20 ppm in 24 h. Compounds 37 exhibited superior molluscicidal activity than those of 36a–h. The substitution of F and Cl groups on pyrazol rings of substrates should enhance the molluscicidal activity.
3-Hydroxy-arylpropanenitriles
Vasconcellos et al. evaluated the molluscicidal activity of 3-hydroxy-arylpropanenitriles (38–40, Table 1) against B. glabrata snails (Vasconcellos et al. 2006). Compound 38 showed the highest activity among the tested compounds in 24 h (38, LC50 = 6.64 ppm, LC90 = 9.23 ppm; 39, LC50 = 7.30 ppm, LC90 = 10.64 ppm; 40, LC50 = 17.71 ppm, LC90 = 22.7 ppm). Compound 40 displayed the lowest toxicity to snails, which could be attributed to the different hydrophilic-lipophilic ability of the naphthalene nucleus. The detailed structural-activity relationships of the 3-hydroxy-arylpropanenitriles should be further explored in future experiments.
Five-membered heterocylces
Kanawade et al. explored novel thiophenedicarboxamide and dicyanothiopheneacetamide derivatives for the control of Indoplanorbis exustus snails (Kanawade et al. 2011). The LC50 values of compounds 41a and 42a (Table 1) were 0.6043 and 0.6511 ppm in immersion experiments, respectively. Fadda et al. evaluated the molluscicidal activity of thiophene, thiadiazole, and pyrazole derivatives (43–45, Table 1) against B. alexandrina snails (Fadda et al. 2009). Thiadiazole derivatives (44a–c) possessed higher activity than that of thiophene derivatives (43a–d) apparently because of the strong electron-donating effect of the thiadiazole ring. For example, compounds 44b and 44c demonstrated the best activity with the LC50 value of 5.5 ppm and 6 ppm, respectively. The surface of snails demonstrated the effusion of the gelatinous materials, which could cause the toxic effect on the cell membranes and resulted in hemolysis and subsequent death (Fadda et al. 2009).
El Shehry et al. carried out the molluscicidal activity of 3-((2,4-dichlorophenoxy)methyl)-1,2,4-triazolo(thiadiazoles and thiadiazines) (46–50, Table 1) against B. alexandrina snails (El Shehry et al. 2010a, b). Compounds 46 and 47 displayed 100% mortality of snails at 10 ppm in 24 h. However, the other compounds (48–50) showed moderate to low activity against snails. Abdelrazek et al. developed a serial of pyrazole derivatives for the control of B. alexandrina snails. Products 51a–d (Table 1) exhibited good molluscicidal activity in immersion experiments (LC50 = 11–13 ppm; LC90 ≥ 14 ppm) (Abdelrazek et al. 2006a, b).
Six-membered N-heterocyles
Some novel functionally substituted pyridines and pyridazines (52–54, Table 1) were prepared and evaluated against B. alexandrina snails in 24 h (LC100 = 6–15 ppm) (Abdelrazek and Fathy 2005). The electron-withdrawing groups on the aromatic ring (Ar group) of the tested compounds (52b, 53b, 54b) showed higher molluscicidal activity in 24 h.
El-Bayouki et al. discovered the molluscicidal activity of some thiazolo[5,4-d]pyrimidines (55, Table 1) against B. alexandrina snails (El-Bayouki and Basyouni 1988). Compounds 55a and 55i showed more effective activity, and the mortalities of snails were up to 100% at 25 ppm in 24 h. Bakhotmah et al. evaluated the molluscicidal activity of the phosphorus compounds bearing an amino pyrimidine-substituted pyrazolo[3,4-d]pyrimidine moiety against B. alexandrina snails (Bakhotmah 2019). For compounds 56 and 57 (Table 1), the mortalities of snails were all only 30% at 50 ppm in immersion experiments in 24 h.
Abdelrazek et al. developed new cinnoline derivatives and evaluated the molluscicidal activity to B. alexandrina snails (Abdelrazek et al. 2006a). Compounds 58–59 (Table 1) possessed good effects on the snails (58a, LC50 = 8 ppm, LC90 = 11 ppm; 58b, LC50 = 7 ppm, LC90 = 15 ppm; 58c, LC50 = 7 ppm, LC90 = 9 ppm; 59a, LC50 = 8 ppm, LC90 = 13 ppm; 59b, LC50 = 9 ppm, LC90 > 15 ppm; 59c, LC50 = 7 ppm, LC90 = 9 ppm). Compounds 58c and 59c showed superior activities mainly attributed to the 4-chlorophenyl group. Ali et al. explored the molluscicidal activity of phosphorus-containing 3-hydrazino-1,2,4-triazines against B. alexandrina snails (Ali et al. 2008). However, the tested products (60–62, Table 1) showed low activity at 50 ppm in 24 h. Abdel-Rahman et al. investigated a serial of 6-methyl-5-styryl-1,2,4-triazin-3-thiol derivatives for the control of B. alexandrina snails (Abdel-Rahman et al. 2003). Compounds 63, 64, and 66 (Table 1) had the moderate molluscicidal activity at 50 ppm in immersion experiments in 24 h. The p-dimethylamino, 1, 2, 4-dichloro phenyl, and β-naphthol moieties should play an essential role against snails. The molluscicidal activity of phthalazin-one 67 (Table 1) was also investigated for the control of B. alexandrina snails, and the LC50 value was 9 ppm in 24 h (67, LC90 = 13 ppm) (Abdelrazek et al. 2006a, b).
Pyrane derivatives
Souza et al. evaluated the molluscicidal activity of the 5,6-dimethyl-dihydro-pyran-2,4-dione and 6-substituted analogous (de Souza et al. 2004). Compounds 68–70 (Table 1) showed moderate activity against B. glabrata egg masses. The substitution of the propenyl or phenyl group in C-6 position of dihydro-pyran-2,4-diones could improve the molluscicidal activity. Flavones 71 and 72 (Table 1) were developed for the control of Bulinus truncatus snails, and the LC50 values of them were 5.47 ppm and 8.91 ppm in 24 h, respectively (71, LC90 = 9 ppm; 72, LC90 = 17 ppm) (Lahlou 2004).
Abdelrazek et al. synthesized and evaluated the molluscicidal activity of new chromene and pyrano[2,3-c]pyrazole derivatives (73–77, Table 1) against B. alexandrina snails (Abdelrazek et al. 2007). Compounds 75 and 76b afforded the most effective activity. The decoration of dimethyl substituents in the cyclohexanone ring and the fused pyran ring might improve molluscicidal bioactivity. For 76b, the NH of the indolyl moiety afforded the chelation effect, resulted in the enhancement of molluscicidal activity. The pyrane derivatives 78–82 (Table 1) were prepared for the control of B. alexandrina snails. All synthesized products exhibited generally moderate molluscicidal activity in immersion experiments. The most effective of them are 79a, 80a, 82a, and 82b (LC50 < 10 ppm). It seemed that pyranopyrazole derivative 79a should be a promising leading compound after appropriate modifications in future (Abdelrazek et al. 2006a, b).
Abdelrazek et al. discovered the molluscicidal activity of 5-oxo-5,6,7,8-tetrahydro-4H-chromene derivatives against B. alexandrina snails (Abdelrazek et al. 2004). The LC50 values of compounds 83a and 84a (Table 1) were 5 ppm (17.61 nM) and 8 ppm (28.17 nM) in 24 h, respectively, which are still far inferior to niclosamide (LC100 = 1 ppm). New pyrano derivative 85a (Table 1) exhibited the highest activity against B. alexandrina snails within the pyrano[2,3-c]pyrazole series (Abdelrazek et al. 2006a), which should be modified and considered in future research.
Benzofuran derivatives
El Shehry et al. screened the molluscicidal activity of some pyrazole, isoxazole, pyridine, pyrimidine, 1,4-thiazine, and 1,3,4-thiadiazine derivatives incorporating benzofuran moiety (86–89, Table 1) against B. alexandrina snails (El Shehry et al. 2010a, b). Compound 86 showed the highest molluscicidal activity and the mortality of snails was up to 100% at 10 ppm in immersion experiments in 24 h. Compounds 87–89 displayed good to moderate activity among the tested products. Giri et al. found that 1-aryl-1-(substituted benzofur-2-yl)-2-benzylcarbinols (90, Table 1) and 1-aryl-1-(substituted benzofur-2-yl)-2-phenylethylenes (91, Table 1) exhibited moderate activity against Lymnea acuminata snails (Giri and Mishra 1984a, b). Hassan et al. developed furo-salicylanilides for the control of B. alexandrina snails (Hassan et al. 2006). Compounds 92b and 92d showed lower molar concentration than that of Bayluscicide. However, cyclization of compound 92b to afford compound 93b (Table 1) resulted in the decrease of molluscicidal activity.
Benzimidazole derivatives
Nofal et al. developed the molluscicidal activity of benzimidazole derivatives for the control of B. alexandrine snails (Nofal et al. 2002). Compounds 94 and 95 (Table 1) exhibited moderate molluscicidal activity at 24 h in immersion experiments. However, the polycyclic benzimidazole derivatives 96–97 showed worse molluscicidal activity.
Coumarin derivatives
Giri et al. developed the molluscicidal activity of 3-substituted 4-hydroxycoumarin derivatives for the control of Lymnaea acuminata snails (Giri and Mishra 1984a, b). The compounds 98 and 99 (Table 1) showed the good molluscicidal activity at 5 ppm, and the mortalities of snails were 58.33% and 68.33% in 24 h, respectively. Schönberg et al. explored the molluscicidal activity of furocoumarins against Biomphalaria alexandrina snails (Schönberg and Latif 1954). Compounds 100 and 101 (Table 1) killed 100% and 69% of the snails at 5 ppm in immersion experiments in 24 h, respectively.
Lapachol and its derivatives
Lapachol (102, Table 1) is a notable natural product from Tecoma heptaphylla (Vell Mart.) (Bignoniaceae). Lapachol showed poor molluscicidal activity against snails in earlier reports (Marston et al. 1984). Santos et al. re-investigated the activity of lapachol and its derivatives against the B. glabrata snails (dos Santos et al. 2000). In immersion experiments, the tested compounds 102–105 (Table 1) showed a significant molluscicidal activity against adult snails in 24 h (compound 102, LC50 = 2.57 ppm, LC90 = 6.18 ppm; compound 103, LC50 = 1.53 ppm, LC90 = 4.30 ppm; compound 104, LC50 = 4.02 ppm, LC90 = 7.15 ppm; and compound 105, LC50 = 5.19 ppm, LC90 = 18.46 ppm). Additionally, compound 104 exhibited the highest molluscicidal activity against snail eggs (LC50 = 0.014 ppm, LC90 = 0.070 ppm) in immersion experiments in 24 h. Furthermore, the activity of 2-hydroxy-3-substituted-aminomethyl derivatives was also investigated against snail eggs. However, the activity of them was lower than compounds 102–105. Santos et al. developed a soluble potassium salt of lapachol 106 (Table 1) from the reaction of lapachol with KOH (dos Santos et al. 2001). The LC50 values of 106 against B. glabrata adult snails and eggs reached 2.70 and 1.43 ppm after 24 h in the immersion experiments, respectively. Silva et al. developed a series of amino and hydrogenated lapachol derivatives (107–108, Table 1) for the control of B. glabrata snails (Silva et al. 2005). Compounds 107a, 107b, 108a, 108c, 108d, 108e, and 108 h showed medium toxicity against snails (23.8 < LC50 < 89.0 mmol/L) in immersion experiments. However, 107c, 108b, and 108f were less active (LC50 > 200 mmol/L). It is notable that compounds 108 g and 109 (Table 1) exhibited significant molluscicidal activity and the LC50 values were 13.8 and 7.6 mmol/L in 24 h, respectively.
The molluscicidal activity of the potassium salt of isolapachol (110, Table 1) was explored for the control of B. glabrata (Lima et al. 2002a, b). Compound 110 exhibited good activity against adult snails (24 h LC50 3.05 ppm, LC90 4.71 ppm) and snail eggs (24 h LC50 0.33 ppm, LC90 0.48 ppm) in immersion experiments. However, 110 showed high toxicity against fishes (T. nilotica) (24 h LC50 2.05 ppm, LC90 2.43 ppm) and planktonic crustaceae (A. salina) (24 h LC50 2.05 ppm, LC90 2.43 ppm). Lima et al. evaluated the molluscicidal activity of lapachol and its derivatives and analogues for the control of B. glabrata snails (Lima et al. 2002a). The LC50 values of compounds 111a and 111c (Table 1) against adult snails were 0.98 and 1.66 ppm in 24 h, respectively. Compounds 111b, 111d, 111e, and 112 (Table 1) also displayed the moderate molluscicidal activity, with LC50 values in the range of 3.82–7.72 ppm in 24 h.
Ribeiro et al. prepared some naphthoquinones and evaluated the molluscicidal activity of compounds 113–114 (Table 1) for the control of B. glabrata snails (Ribeiro et al. 2009). The LC50 values of the tested products ranged from 0.475 to 3.049 ppm in 24 h. Camara et al. evaluated the molluscicidal activity of naphthoquinone derivatives for the control of B. glabrata snails (Camara et al. 2008). The presence of a bromine group in compound 115c (Table 1) resulted in almost 15-fold molluscicidal activity compared to compound 115a. However, these synthesized products exhibited obvious toxicity to the brine shrimp A. salina (Camara et al. 2008). Barbosa et al. developed new 2-aminoalkyl substituted anthraquinones from norlapachol for the control of B. glabrata snails (Barbosa et al. 2005). Compounds 116a–h (Table 1) displayed moderate activity. The increase of polarity of molecules can lead to the decrease of bioactivity (for 116b and 116c), which exhibits a similar trend to that of amino lapachol derivatives reported by Silva’s group (Silva et al. 2005). Therefore, compound 116 g displays the best molluscicidal activity among the tested products. However, the molluscicidal activity was sharply diminished when the aminoalkyl substituted compounds were converted into the cyclic molecules 117 and 118 (Table 1).
The above findings confirm the importance of lapachol and its derivatives as promising molluscicides.
Quinoline derivatives
Serials of novel enaminones derived from 4-hydroxyquinolinones (119–122, Table 1) were prepared by Abass’ group (Abass and Mostafa 2005). Part of these products exhibited good molluscicidal activity of against B. alexandrina and Lymnaea natalensis snails (LC50 < 20 ppm). For compounds 122a–c, the structure–activity relationship showed that the molluscicidal activity increased with the improvement of the lipophilicity of the molecules. In addition, the acute toxicity of the tested molluscicides against D. magna was also explored, and the experimental results revealed that the candidate compounds showed 0% mortality at LC50 concentrations after 48 h. Kujime et al. evaluated the molluscicidal activity of acridone alkaloids against B. glabrata snails (Kujime et al. 1992). Compounds 123 and 124 (Table 1) showed moderate bioactivity in 24 h. El Bardicy et al. evaluated the molluscicidal activity of aminoalkylamino substituted neo- and norneocryptolepine derivatives (125–131, Table 1) against B. alexandrina snails (El Bardicy et al. 2012). The LC50 values of the tested products were 0.63–3.9 ppm in 24 h.
Our group discovered the molluscicidal activity of 3-substituted quinazolinone derivatives 132 (Table 1) through a scaffold hop** approach using a pseudo-ring based on the intramolecular hydrogen bond formation (Guo et al. 2016). Most of the tested compounds showed good molluscicidal activity against O. hupensis with the LC50 values ranged from 2.69 to 10 ppm. The preliminary structure–activity relationship exhibited that the aromatic rings are essential for C section and the electron-donating groups on the C ring can promote the molluscicidal activity.
Thiaxanthene derivatives
El-Sakka et al. evaluated thiaxanthene derivatives (133–137, Table 1) against B. alexandrina snails (El-Sakka et al. 1994). Compounds 136–137 showed considerable activity, and 135 possessed the highest mortality in 24 h at 25 ppm.
Development of plant molluscicides
Chemical molluscicides are still the most convenient option for the control of snails and have been used successfully in practical applications (Perrett and Whitfield 1996). However, the registered chemical molluscicides (such as niclosamide, copper sulfate, and sodium pentachlorophenate) are still rare due to high cost, toxicity to non-target organisms, high residual risk, and relatively complicated synthesis process (Brackenbury and Appleton 1998). Some plant molluscicides are considered inexpensive and environmental friendly to the health of aquatic organisms and mammals, and some pure compounds have also been isolated from plant and proven to have molluscicidal activity against snails. Development of natural plant molluscicides may be a suitable alternative for snail control (Zhu et al. 2010).
Sesquiterpene lactones
Borkosky et al. evaluated the molluscicidal activity of sesquiterpene lactones from the tribe Vernonieae, family Asteraceae (Borkosky et al. 2009). The tested products 138–147 (Table 1) demonstrated moderate molluscicidal activity against B. peregrina snails. The LC50 values ranged from 27.99 to 88.25 ppm in 24 h.
Monoterpenoids
Radwan et al. evaluated the molluscicidal activity of monoterpenoid derivatives (148–155, Table 1) for the control of B. alexandrina snails (Radwan et al. 2008). Most of the compounds showed molluscicidal activity; especially compound 155b was the most effective among the tested compounds (LC50 = 5.43 ppm). Furthermore, mixing compounds 154a and 155a with piperonyl butoxide (PBO) afforded the LC50 values of 2.69 and 2.72 ppm in 24 h, respectively.
Diterpenoids
Dos Santos et al. discovered the molluscicidal activity of diterpenoids (156–157, Table 1) isolated from Jatropha elliptica (Pohl) Muell. Arg (dos Santos and Sant’Ana 1999). Compared with product 157, products 156 showed molluscicidal with the LC50 values of 1.16 ppm (adult snails) and 1.14 ppm (snail eggs) in 24 h. However, product 157 was not active against B. glabrata snails at a concentration of 100 ppm. Abdelgaleil et al. extracted some diterpenes (158–161, Table 1) from Euphorbia paralias L and evaluated the molluscicidal activity against B. alexandrina snails (Abdelgaleil et al. 2002). Most of the obtained products showed moderate molluscicidal activity except product 160c. Notably, among the isolated products, product 158b showed the best activity with the 100% mortality at 15 ppm in 24 h. The preliminary structure–activity relationship of the tested products exhibited that paraliane diterpenes (158a–b) showed higher activity than segetane diterpenes (159, 160a–c) to snails. For paraliane diterpenes, the acetoxyl group at C1 in compound 158a was unfavorable for the improvement of activity. In the case of 160a–c, the present of acetoxy group (R2) facilitated the molluscicidal activities, which were similar to 161a–c.
Triterpenoid saponins
Molluscicidal activity of triterpenoid saponins from Maesa lanceolata was assessed by Apers et al. (2001). Among the tested products, compound 162c (Table 1) showed the best activity against B. glabrata snails and the LC50 value was 0.5 ppm in 24 h. Novel triterpene saponins (163a–d, Table 1) were isolated from African medicinal plant, Pachyelasma tessmannii for the control of B. glabrata snails (Nihei et al. 2005). The LC50 values of 163a–d were 2, 2, 2, and 8 ppm within 24 h, respectively. Triterpenoid saponins 164 and 165 (Table 1) were extracted from the roots of Pueraria peduncularis (Chen et al. 2020). The two products 164 and 165 displayed moderate molluscicidal activity with the mortalities of 15% and 21.25% at 30 ppm in 24 h, respectively. A pentacyclic triterpenoid saponin 166 (Table 1) was exacted from the seed pomace of Camellia oleifere, which was widely cultivated in South China (Jia et al. 2019). Product 166 has been named as tea-seed distilled saponin (TDS) and been registered as Luo-Wei by the Ministry of Agriculture (MoA) of China. Compound 166 showed significant molluscicidal activity against O. hupensis, B. alexandrina, and Bulinus truncates, and the LC50 values were 0.701 ppm, 1.975 ppm, and 1.396 ppm in 24 h, respectively. In addition, TDS showed moderate toxicity to Japanese quail and shrimp, and high toxicity to zebrafish (96 h LC50 = 0.15 ppm). For all that, TDS may be a promising candidate molluscicide of plant origin to eliminate snails in high-risk areas. Ekabo et al. tested the novel saponins (167–168, Table 1) extracted from Serjania salzmanniana for the control of B. alexandrina snails (Ekabo and Farnsworth 1996). For products (167a–b, 168), the mortalities of snails were 70–100% at 10 ppm in 24 h. However, product 167c exhibited no activity at 10 ppm.
Cardiac glycosides
The two molluscicidal active cardiac glycosides, cerberin 169 and neriifolin 170 (Table 1), were isolated from the stems of Adenium obesum (Alzabib et al. 2019). Products 169 and 170 had significant molluscicidal activity against Monacha obstructa snails with LC50 values of 5.39 and 4.30 ppm in 24 h, respectively.
Ginkgolic acids
Yang et al. evaluated the molluscicidal activity of ginkgolic acids (171a–c, Table 1), isolated from Ginko sarcotesta against O. hupensis (Yang et al. 2005). However, the stability of these new formulations should be screened, and simultaneously require more field experiments in future works.
Plant molluscicides attract more and more attention. However, some unfavorable factors should not be overlooked (Li et al. 2002): (1) low content of the active ingredients resulted in low molluscicidal activity; (2) regional limitations for some specific molluscicidal plants; (3) relative complicated extraction process resulting in high cost; (4) environmental pollution because of the application of fresh molluscicidal plants. In addition, for plant molluscicides, the characterization of the structures of active ingredients is also very important, which could provide the reference for the development of novel chemical molluscicides and later modifications (Whitfield 1996). However, develo** novel, low-toxicity, and highly effective plant molluscicides and elucidating the possible mechanism in detail are still great challenges.
For laboratory and field testing of molluscicides for schistosomiasis (WHO (World Health Organization) 2019), we have: (1) for the new candidate molluscicide compound and for new end-use formulations of existing molluscicide compounds, an optimum effective dose should be determined based on the dose–response curve. The manufacturer’s label claim may also be considered to decide the optimum dose to be tested; (2) the efficacy of exposure in immersion bioassay and residual activity at this effective dose is then determined according to the immersion bioassay. The efficacy cut-off is the 80% mortality and the effective residual action is the duration until when the mortality in treatments remains ≥ 80%; (3) a dose–response curve is needed to determine LC50 and LC95 values. The results are recorded in a standard data recording form. The relationship between dose and mortality is analyzed using log-probit (Finney 1971) or logit regression; (4) from the dosages tested against a target species in the small-scale or simulated field trials, the minimum efficacious dosage (mortality and residual effect) should be selected as the optimum field application dosage for each type of habitat; (5) the WHO cut-off for the efficacy of a molluscicide formulation against adult snails is ≥ 80% mortality in 24 h post-exposure. The residual efficacy of the molluscicide is calculated as the duration (days) when mortality in snails remains ≥ 80%.
The present mechanism investigations for chemical and natural molluscicides focus on the simple interactions between molluscicides and some enzymes, and lack visual evidence in structural biology. Therefore, investigating the structure biology of target enzymes/proteins and studying the corresponding the action sites could help in designing novel molluscicides to combat snails (Wu et al. 2006). We believe that the original and innovative molluscicides will soon emerge after the above issues are resolved by more scientists, followed by a prompt growth in advancements.
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Acknowledgements
The work is supported by the National Natural Science Foundation of China (21867001, 22167002, 21662002 and 21602031), the Academic &Technical Leadership Development Program of Jiangxi Province (20194BCJ22014), the Double-Thousand Talents Plan of Jiangxi Province (2019) and the Jiangxi Natural Science Foundation (20202ACBL206022, 20171BAB203010), the Science Foundation of Jiangxi Provincial Department of Education (GJJ201429), and the Graduate Innovation Research Project of Jiangxi Province (YCX20A009).
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Zheng, L., Deng, L., Zhong, Y. et al. Molluscicides against the snail-intermediate host of Schistosoma: a review. Parasitol Res 120, 3355–3393 (2021). https://doi.org/10.1007/s00436-021-07288-4
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DOI: https://doi.org/10.1007/s00436-021-07288-4