Estimation the Effect of Ficus carica Active components’ Nanoparticles on Mice Infected by Schistosomal cercariae and treated with praziquantel

doi:10.21203/rs.3.rs-4339172/v1

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Estimation the Effect of Ficus carica Active components’ Nanoparticles on Mice Infected by Schistosomal cercariae and treated with praziquantel

https://doi.org/10.21203/rs.3.rs-4339172/v1

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published 15 Aug, 2024

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Bilharzia is parasitic flatworm that causes schistosomiasis, a neglected tropical illness of worldwide. Praziquantel (PZQ) is a commercial single treatment of schistosomiasis so the alternative drugs are needed to get rid of its side effects on liver. The current study aimed to estimate the effective role of Ficus carica nanoparticles (Fc-NPCs), silver nanoparticles (Ag-NPCs) and Ficus carica nanoparticles loaded on silver nanoparticles (Fc-Ag NPCs) on C57BL/6 black female mice infected by Schistosoma mansoni and treated with PZQ treatment. It was proved that the schistosomiasis causes liver damage in addition to the PZQ is ineffective as anti-schistosomiasis; it is recorded in infected mice group and PZQ treated group as in liver function tests, oxidative stress markers & anti-oxidants, pro-inflammatory markers, pro-apoptotic and anti-apoptotic markers also in liver cells’ DNA damage. The amelioration in all tested parameters has been clarified in nanoparticles’ protected mice groups. Obviously, The Fc-Ag NPCs + PZQ group recorded the best preemptive effects as anti-schistosomiasis. Fc-NPCs, Ag-NPCs and Fc-Ag NPCs could antagonize PZQ effects that were observed in amelioration of all tested parameters. The study showed the phytochemicals’ nanoparticles groups have ameliorated effect on the health of infected-administered mice.

Health sciences/Diseases/Gastrointestinal diseases

Health sciences/Diseases/Infectious diseases

Biological sciences/Biological techniques/Nanobiotechnology

Health sciences/Biomarkers

C57BL/6 Mice

Protection

Fig

Nanoparticles

Schistosomiasis

Praziquantel

Schistosomiasis is a parasitic disease caused by blood flukes of the genus Schistosoma. The disease has an acute phase that is followed by a chronic phase based on repeated exposure to the parasite if untreated. The main species causing human infections are Schistosoma mansoni Schistosoma haematobium, Schistosoma japonicum and Schistosoma mekongi. Approximately 779 million people are at risk of infection per year ^{1, 2}.

Praziquantel (PZQ) is the only treatment against all Schistosoma species. The lack of its cure highly encourages efforts to identify an alternative treatment of schistosomiasis, in anticipation of PZQ resistance and tolerance ^{3, 4}. It is necessary to find natural alternatives to be efficient tool as new drugs against helminthiases, reducing time and costs of drug research and development ⁵. Its advantage in killing 100% of only adult worms’ stage not recorded now that reaches 60–90%.

Ficus carica L., is known as one of the oldest trees, belongs to the Moraceae family, which mostly cultivated in the Mediterranean territory. Its fruits are rich source of sugar, vitamins, minerals, amino acids and organic acids ⁶. Previous studies have shown that Ficus carica active compounds extracted from common fig fruit exhibits antioxidant and immune-enhancing properties. Nevertheless, it remains uncertain whether it can modulate the metabolism of gut microbiota that ameliorates the overall health ⁷.

Nanoparticles play a pivotal role since they exhibit unique properties; these properties depend on morphological aspects (e.g., shape, size, structure, crystallinity) and thus have led to a large range of applications in various areas such as electronics, molecular diagnostics, drug release and catalysis ⁸. The biosynthesis strategy of nanoparticles has drawn much consideration instead of physical or chemical, since they are green, proficient manufactured forms, and cost-effective strategy. It will play a crucial role in diagnostics, drug delivery, bandages, related cosmetics, etc. ⁹.

Ethical approval

The current study is reported in accordance with ARRIVE guidelines. The experimental protocol was agreed from the local experimental animal ethics committee of Faculty of Medicine, Mansoura University accordance to the guide of the National Institute of Health for the care and use of Laboratory animals (NIH publication No. 8523, revised 1996) with approval number Sc. Ms. 22.12.12. The date of approval: 16/12/2022.

Chemicals

Praziquantel (PZQ) tablets were purchased from the Egyptian International Pharmaceutical Industries Company (EPICIO), Mansoura, Egypt.

Mice groups and mode of administration

Thirty female mice C57BL/6 aged 11 weeks with average weight of 30-35 g were cared in wood-chip bedding plastic cages, refreshed day by day for acclimation with standard food as pellets of commercial rodents’ food and water ad libitum at experimental period, at 22 ± 3 °C for 12 h cycle dark/ 12 h light in animal house of Faculty of Science, Mansoura University, Mansoura, Egypt. Mice were randomly divided into six groups (n=5) during the experimental period= 8 weeks as following:

G1-Uninfected control group: Uninfected and non-treated. G2-Infected control group: Infected- non-treated. G3- PZQ group: 200 mg/Kg for two consecutive days was given orally during 7^th week after infection ¹⁰. G4- Fc-NPCs + PZQ: Mice were pre-treated by Fc-NPCs (400 mg/Kg) in 1^st, 3^rd and 5^th during 1^st week before infection, PZQ was administrated for two consecutive days (200 mg/day/ kg bw) during 7^th week after infection ¹⁰. G5- Ag-NPCs + PZQ: Mice were Pre-treated by Ag-NPCs (400 mg/Kg) in 1^st, 3^rd and 5^th during 1^st week before infection, PZQ was administrated for two consecutive days (200 mg/day/ kg bw) during 7^th week after infection ¹⁰. G6- Fc-Ag NPCs + PZQ: Mice were Pre-treated by Fc-Ag NPCs (400 mg/Kg) in 1^st, 3^rd and 5^th during 1^st week before infection, PZQ was administrated for two consecutive days (200 mg/day/ kg bw) during 7^th week after infection ¹⁰.

All infected mice were injected subcutaneously by freshly shedding cercariae from stock solution containing about 70 cercariae/ 0.5 ml distilled water.

Preparation of praziquantel stock solution (Fresh)

Two hundred mg of PZQ was mixed with only one drop of highly purified olive oil until reaching paste texture, and then 5.2 ml of sterile water was added drop by drop with continuous stirring.

Ficus carica extract nanoparticles

Hydrothermal squeeze methods were confirmed for the preparation process; 20g of washed and dried powdered leave plant were soaked into 100 ml ethanol for 12 hrs. in absence of light. In a Teflon-lined autoclave, samples were been introduced and placed in an incubator at 50 ± 2 °C for 6 hrs. After incubator, the solutions were kept cool to room temperature for another 6 hrs. Then filtered, centrifuged, and freeze-dried. The process is repeated until the required amount of extract was obtained ¹¹.

Preparation of silver nanoparticles

About 10 ml of prepared F. carica extract was added to 100 ml of 2 mM of a pre-prepared aqueous solution of silver nitrate according to Green synthesis technique. The solution was stirred at 60 °C for 6 hrs. The formation of the Ag-NPCs was detected by the appearance of deep brown ¹².

Preparation of Fig extract nanoparticles loaded on silver nanoparticles

By adding 1:1 of ethanoic F. carica extract: Silver nitrate, with continuous stirring for 1 hr. at pH=7, after 24 hrs. in the dark, with stirring and then left until yellowish green color appears.

Scarification, blood sampling and hepatic samples preparation

At the end of experiment, mice were drugged by Ketamine (43.5 mg/ kg) and Xylazine (6.5 mg/ kg) for half hr. to be fully euthanized ¹³. Mice were sacrificed by decapitation using sharp, cleaned and sterilized blades (The decapitation was used for collecting blood samples to be followed by dissection to obtain liver and intestine for other investigations) and blood samples were obtained in centrifuge glass tubes, after clotting, samples were centrifuged at 3000 r.p.m. for quarter of hr., the clear supernatant was collected. The sera were kept in labeled Eppendorf’s tubes, frozen at -20 °C until usage. Hepatic samples were washed, dried and homogenized (10% w/v) by distilled water; homogenates were stored in labeled Eppendorf tubes at -20 °C for biochemical analysis.

Physiological markers

Liver function tests

Serum Alanine aminotransferase (ALT), aspartate aminotransferase (AST) and alkaline phosphatase (ALP) activity have been evaluated according to the colorimetric kit methods of ^{14, 15}, respectively using Biodiagnostic and research reagents kit. Serum gamma glutamyl transferase (GGT) activity has been evaluated according to the colorimetric kit method of ¹⁶, using kit from Clinical chemistry. Serum albumin and albumin content was investigated according to the methods described by ^{17, 18}, respectively using of kit from Spinreact.

Oxidative stress and antioxidant markers

Hepatic malondialdehyde (MDA), reduced glutathione (GSH), superoxide dismutase (SOD) and catalase (CAT) were investigated according to the methods described by ^{19, 20, 21, 22}, respectively by the use of kit from Biodiagnostic and research reagents.

Pro-inflammatory markers

Serum C reactive protein (CRP) was estimated using ELISA kit from BD™ ELISA, Franklin Lakes, New Jersey, USA. Hepatic interleukin-6 (IL-6) and vascular adhesion molecule-1 (VCAM-1) were estimated by ELISA kit from CUSABIO, Houston, TX, USA. Intercellular adhesion molecule-1 (ICAM-1) was investigated using ELISA kit from Quantikine®ELISA, Riham Tower El-Etehad Squre, Maadi, Cairo, Egypt.

Pro-apoptotic and anti-apoptotic markers

Hepatic p53, Bax, cytochrome c and caspase 9 were estimated by ELISA kit from Rat P53/Tumor Protein (P53/TP53) ELISA Kit, ELISA kit from Rat apoptosis regulator BAX (BAX) ELISA Kit, ELISA kit and ELISA kit from Rat CASP9 (Caspase 9) ELISA Kit, respectively CUBIO Innovation Center, Houston, TX, USA. Hepatic Bcl-2 was estimated by ELISA kit from Rat B-cell CLL/lymphoma 2 (BCL2) ELISA Kit, Creative Bio labs, Ramsey Road, Shirley, USA. Hepatic caspase-3 was estimated by using ELISA kit from Biovision, Grove Street, Waltham, Massachusetts.

DNA damage by single cell electrophoresis assay

The DNA damage was investigated by using hepatic cells according to ^{23, 24}.

Statistical analyses

The Graphpad prism 8.0software was used for preparing all statistics. The results are shown as the mean ± standard error of the mean (SEM) (n=5). A one-way analysis of variance (ANOVA) was used to make the different statistical comparisons, followed by the Neuman-Keuls post-hoc test. The data was considered significant when P ≤ 0.05 ²⁵.

Liver function tests

Figure 1 (a, b, c, d, e & f) observed activity of each ALT, AST, ALP, GGT, content of each albumin and bilirubin in control and tested animal groups. Serum activity of ALT, AST, ALP, GGT and content of bilirubin recorded significant reduction unlike in albumin content recorded a significant increase in Ag-NPCs, Fc-NPCs and Fc-Ag NPCs, respectively pre-treated groups compared to infected mice. PZQ showed a significant effect on the above serum markers compared with +ve control group that had an agreement with ²⁶ who explained the increment of such enzymes in serum is probably due to the destruction of hepatocytes by the action of parasite eggs-releasing toxins with low effectiveness of PZQ drug in fully recovery. These results had an agreement with ²⁷ who stated that it was approved that using PZQ (sub-curative dose) in combination with other anti-schistosomicides such as F. carica leaves ethanolic extract is an important step to reduce the PZQ dose and avoid side effects. ²⁸ noted that Ag-NPCs could reduce changes in liver AST, ALT, and ALP. From the obtained findings, it may be due to the green synthesis method which reduced the toxicity of silver, which indicated a potential protective role of Ag-NPCs. The group that showed the best recovered liver after cercarial infection is Fc-Ag NPCs + PZQ; it may be come from Fc-NPCs and Ag-NPCs synergize each other and reduced the side effect of sub-curative dose of PZQ treatment.

Oxidative stress marker & Anti-oxidants

Figure 2 (a, b, c & d) observed content of each MDA and GSH activity of each SOD and CAT in control and tested animal groups. Hepatic level of MDA showed a significant decrease contrary GSH level and activity of SOD and CAT recorded significant elevation in Ag-NPCs, Fc-NPCs and Fc-Ag NPCs, respectively pre-treated groups compared to infected group. Natural antioxidant compounds of Ficus carica leaves such as phenolic compounds, organic acids, vitamin E, and carotenoids are healthy compounds; these compounds can inhibit free radical formation by reducing or donating hydrogen to other compounds. Among them, phenolic compounds are the most popular due to their well-known antioxidant capacities. Two major categories of phenolic compounds are phenolic acids and flavonoids ²⁹. ³⁰ had the same conclusion who explained that it may restore the GSH was found in liver in Ag-NPs treated animals. Alleviated activities of adenosine triphosphatase (ATPase), glucose-6- phosphatase (G6Pase) and antioxidant enzymes viz. SOD and CAT due to acetaminophen (APAP) induced toxicity in liver were recovered by the treatment of Ag-NPs.^{29, 31}who stated the ameliorative effect of fig nanoparticles and silver nanoparticles in addition their effect on PZQ treatment to antagonize it so, this combined group marked the best effect on anti-oxidation process.

Pro-inflammatory markers

Figure 3 (a, b, c & d) observed content of each CRP, IL-6, VCAM-1 and ICAM-1 in control and tested animal groups. Serum CRP, hepatic IL-6, VCAM-1 and ICAM-1 showed significant decrease in Ag-NPCs, Fc-NPCs and Fc-Ag NPCs, respectively pre-treated mice groups compared with infected group. Oxidative stress is closely related to inflammatory response since unbalance of redox homeostasis can cause cellular damage, thus activating the innate immune response or causing apoptosis ³². Formononetin (one of phytochemicals of F. carica) indicated that it has a positive effect, as it increases the activity of antioxidant enzymes, and reduce the levels of pro-inflammatory markers (TNF-α, IL-1β, and IL-6) via HMGB1/TLR4/NF-κB signaling and NLRP3 inflammasome pathways ³³. ³⁴ explained their results by using Ag-NPCs ameliorated liver inflammation and damage by reduced macrophage and neutrophil infiltrates. A reduction in count and size was evaluated in the granulomas, as well as a change to an exudative-proliferative phase, with a local increased of IFN-γ (anti-tumor). From the previous explanations about the ameliorative effects of Fc-NPCs, Ag-NPCs and PZQ as antioxidants, anti-inflammatory agents, and the recorded data observed the best anti-inflammatory treatment in this group that may be caused by the three chemicals can synergize each other.

Pro-apoptotic and anti-apoptotic markers

Figure 4 (a, b, c, d, e & f) observed content of each P53, Bax, Bcl-2, cytochrome C, caspase 9 and caspase 3 in control and tested animal groups. Hepatic P53, Bax, cytochrome C, caspase 9 and caspase 3 showed significant decrease otherwise Bcl-2 recorded a significant increase in Ag-NPCs, Fc-NPCs and Fc-Ag NPCs, respectively pre-treated mice groups compared with infected group. ³⁵ who used Ziziphus spina-christi leaf extract (ZLE) that had polyphenols as Fc-NPCs; the results indicated that ZLE had anti-fibrotic activity by reversing S. mansoni-induced liver fibrosis through reducing hepatic expression of TGF-β1, MMP-9, and TIMP-1 and increasing anti-oxidative status while limiting apoptosis. ZLE had anti-schistosomal activity, in addition to the antioxidant, anti-inflammatory, anti-apoptotic and anti-fibrotic effects. ³⁶ who explained that Ag-NPCs had antioxidant, anti-inflammatory, and anti-apoptotic effect as mentioned above. Presence of Ag-NPCs might improve the effect of PZQ so the obtained result showed better effect than PZQ singly. From the previous data about the ameliorative effects of Fc-NPCs and Ag-NPCs as antioxidants, anti-inflammatory and anti-apoptotic agents, and the recorded data observed the best anti-apoptotic treatment in this group (Fc-Ag NPCs + PZQ) that may be caused by the chemicals can synergize each other with reducing the side effects of PZQ.

DNA damage by single cell electrophoresis assay

Figure 5 (a, b, c, d, e & f) and Figure 6 (a, b & c) showed DNA damage of single cell of hepatic tissue to record Tail length (TL), Tail DNA (DNA %) & Tail moment (TM) in infected mice and other tested groups. The data showed normal spots in uninfected group and abnormal spots in infected group. The presented data showed amelioration in Ag-NPCs, Fc-NPCs and Fc-Ag NPCs, respectively in reducing DNA damage spots (Tail length, Tail moment and DNA %) compared with infected group. The current study observed that the active phytochemicals of Ficus carica leaves had protective role against reactive oxygen species (ROS) and reduced DNA. ³⁷ supported their opinion by proving that Ag-NPCs had a protective effect on DNA against Triclosan-induced DNA damage, the combined combination of phytochemical nanoparticles F. carica and silver nanoparticles showed better results than each of them separately, and this showed decay destruction in DNA so, it might be able to antagonize PZQ side effects that appeared the best protected-treated mice group.

The current study proved the protective effect of phytochemicals nanoparticles of fig leaves and silver nanoparticles against bilharzia infection in presence of praziquantel treatment that can improve the health to fight the disease and reduce the side effects of the drug. The Ag-NPCs may synergize the Fc-NPCs which may be able to increase the antagonistic effect for PZQ which appeared in the combined group (Fc-Ag NPCs + PZQ); the current experiment was summarized in Figure 7.

Availability of data statement:

The datasets generated and analyzed during the current study are available in the file; its name is supplementary file.

Acknowledgements:

The resources that Mansoura University offers are greatly appreciated. The graphical abstract and histograms were designed by Naira A. El-Attar (Corresponding author).

Author contributions:

By contributing to the research, data analysis, and presentation of results, as well as the drafting and editing of the manuscript by Naira A. El-Attar who worked to create the methodology, prepare figures and run the experiments. Mamdouh R. El-Sawi and Eman A. El-Shabasy performed data analysis and interpretation. Naira A. El-Attar were involved in the study consultation, the conceptualization of the manuscript, and the overall writing and editing. The content was reviewed, discussed and revised by all authors.

Competing Interests Statement:

Naira A. El-Attar, Mamdouh R. El-Sawi and Eman A. El-Shabasy declare that they have no conflict of interest.

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No competing interests reported.

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Estimation the Effect of Ficus carica Active components’ Nanoparticles on Mice Infected by Schistosomal cercariae and treated with praziquantel

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