Molluscicidal activity and physiological toxicity of quaternary benzo[c]phenanthridine alkaloids (QBAs) from Macleaya cordata fruits on Oncomelania hupensis.

Wenshan Ke,Chang Tu,Qiqiang Sun,Xiong Lin,Dezhi Cao,Qian Zhang,Matty Knight

doi:10.1371/journal.pntd.0007740

Abstract

Schistosomiasis is a serious worldwide parasitic disease. One of the best ways to control schistosomiasis is to control the population of Oncomelania hupensis snails. We sought to identify a high-efficiency biogenic molluscicide against Oncomelania with low toxicity, to avoid chemical molluscicide contamination and toxicity in aquatic organisms. We extracted quaternary benzo[c]phenanthridine alkaloids (QBAs) from Macleaya cordata fruits. Molluscicidal activity of the QBAs against Oncomelania was determined using bioassay. Our results showed that the extracted QBAs had a strong molluscicidal effect. In treatment of O. hupensis with QBAs for 48 h and 72 h, the lethal concentration (LC50) was 2.89 mg/L and 1.29 mg/L, respectively. The molluscicidal activity of QBAs was close to that of niclosamide (ethanolamine salt), indicating that QBAs have potential development value as novel biogenic molluscicides. We also analyzed physiological toxicity mechanisms by examining the activity of several important detoxification enzymes. We measured the effect of the extracted QBAs on the activities of glutathione S-transferase (GST), carboxylesterase (CarE), acid phosphatase (ACP), and alkaline phosphatase (AKP) in the liver of O. hupensis. We found that the effects of QBAs on detoxification metabolism in O. hupensis were time and concentration dependent. The activities of GST, CarE, AKP, and ACP in the liver of snails increased significantly in the early stage of treatment (24 h), but decreased sharply in later stages (120 h), compared with these activities in controls. GST, CarE, AKP, and ACP activity in the liver of snails treated with LC50 QBAs for 120 h decreased by 62.3%, 78.1%, 59.2%, and 68.6%, respectively. Our results indicate that these enzymes were seriously inhibited by the extracted QBAs and the detoxification and metabolic functions of the liver gradually weakened, leading to poisoning, which could be the main cause of death in O. hupensis snails.

Highlights

Schistosomiasis is an acute and chronic parasitic disease that is caused by blood flukes of the genus Schistosoma
The number of deaths among O. hupensis snails treated with quaternary benzo[c]phenanthridine alkaloids (QBAs) increased with increased treatment concentration and prolongation of the treatment time, revealing a concentration-dependent and time-dependent effect (Table 1)
Compared with niclosamide at the same concentration (1 mg/L), we found that molluscicidal activity of QBAs against the snails was close to that of niclosamide (Table 1)

Summary

Introduction

According to statistics in 2017, the area with a presence of O. hupensis snails in China was 172,501.56 hm, of which 208.54 hm were areas with newly discovered populations of O. hupensis; snails have been found distributed over areas covering entire villages [2]. Such a wide and complex distribution of snails along the Yangtze River Basin is one of the important factors hampering the elimination of schistosomiasis in China and one of the main causes for a reemergent epidemic situation [7]

Methods

Results

Discussion

Conclusion