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BY 4.0 license Open Access Published by De Gruyter Open Access November 22, 2023

Effects of green decorated AgNPs on lignin-modified magnetic nanoparticles mediated by Cydonia on cecal ligation and puncture-induced sepsis

  • Lei Zhou , Yanfen Yao , Quanzhen Wang , Peng Wang , Shan Hong and Li Kong EMAIL logo
From the journal Open Chemistry

Abstract

Sepsis is a common and deadly syndrome that despite all the progress in its control, the death rate caused by it is high. Sepsis is a serious problem that needs immediate attention and treatment. This infection, especially if it is caused by bacteria resistant to several drugs, causes high mortality. About two-thirds of sepsis cases occur in hospitalized patients. Several factors such as increasing the age of the population, increasing the duration of chronic diseases, high consumption of antibiotics and corticosteroids, use of mechanical devices and intravascular devices play a role in increasing its incidence. We herein demonstrate the biogenic procedure for the in situ immobilizing gold nanoparticles over lignin (Lig)-modified Fe3O4 magnetic nanoparticles mediated by Cydonia leaf extract (Fe3O4@Lig-Ag NPs) and its catalytic activity on the acetylation of alcohols using acetic anhydride and subsequent biological performances. The successful synthesis of Fe3O4@Lig-Ag NPs was assessed using an array of advanced techniques like field emission scanning electron microscopy, fourier transformed infrared spectroscopy, transmission electron microscopy EDX, elemental mapping, vibrating-sample magnetometer, and X-ray diffraction. Cecal ligation and puncture was used for inducing the sepsis model in rats. Several doses of Fe3O4@Lig-Ag NPs (45, 15, and 5 µg/kg) on oxidant–antioxidant, inflammatory mediators mRNA such as IL-1 and TNF-α, and its effects on the levels of expression were assessed in the kidney, liver, duodenum, lung, and stomach. When septic rats kidney, liver, duodenum, lung, and stomach were compared with those of the control group, it was found that Fe3O4@Lig-Ag NPs dose-dependent administration raised glutathione levels and superoxide dismutase activity and significantly reduced the levels of malondialdehyde. The Fe3O4@Lig-Ag NPs (45 µg/kg) indicated greater anti-oxidative effects than the 5 and 15 µg/kg doses for all the assessed parameters. In addition, the expression of TNF-α mRNA in the CLP + 45 µg/kg group was decreased in comparison with the control group. Fe3O4@Lig-Ag NPs reduced oxidative stress by enhancing the free radicals scavenging effects and supporting endogenous antioxidants. The Fe3O4@Lig-Ag NPs potent antioxidant property may be related to the cytokine cascade suppression during sepsis. The above findings offer that Fe3O4@Lig-Ag NPs administration may indicate a modern treatment for the inhibition of liver, kidney, lung, duodenum, and stomach tissues damage caused by septic conditions.

1 Introduction

Sepsis is a disease that occurs due to toxic substances produced by infectious agents such as bacteria, viruses, or fungi, or due to a weak defense system. People with a weak immune system are more prone to this disease [14]. The weakness of the body’s immune system can be caused by diseases such as diabetes, AIDS, the use of certain drugs such as steroids or chemotherapy drugs, and the use of strong drugs in cancer and transplant patients. Babies and old people (adults) are among the groups that are at risk of contracting this disease due to their weak immune system [46]. Hospitalized patients are another group who are at risk of contracting this disease due to intravenous injection, surgical wounds, or bed sores. Diseases such as lung infection, bladder infection, abdominal infection (such as appendicitis), skin infection, urinary tract infection (kidney infection), bone infection, and brain infection (such as meningitis) can also cause this disease by spreading in the body [710]. Symptoms of sepsis include an increase and decrease in body temperature, chills, increased heart rate and breathing, decreased level of consciousness, delirium and confusion, small subcutaneous bleeding (which can be in the form of a change in skin color or in the form of small red dots). Pain in the joints such as the spine, pain in the wrists, thighs, elbows, and knees are other symptoms [1012]. In the worst case, it can cause a rapid drop in blood pressure, which is called septic shock. Some of the above symptoms can be caused by flu or other diseases. Prompt treatment of a blood infection is essential because the infection can quickly spread to the tissues and valves of the heart. If this disease occurs, the patient may need to be admitted to the hospital. If symptoms such as shock develop in a person, he should be transferred to the intensive care unit. Recently, nanotechnology and nanoparticles have been applied for the treatment of infectious and microbial diseases [1114].

The science of nanotechnology has contributed greatly to the development and discovery of modern infection treatment options. For example, we can mention the use of modified nanoparticles for the selective and targeted delivery of drugs to infectious tissue [1517]. The use of nanotechnology in the production of drugs is one of the promising fields for the diagnosis and treatment of microbial diseases. Because of their excellent physical characteristics, nanoparticles have been applied as an effective candidate for drug treatment, the most important of which is silver nanoparticles [15,16]. Although there are different methods for nanoparticle synthesis, biocompatible methods such as synthesis using bacteria, fungi, and plants are very simple and cost-effective alternatives to chemical and physical methods [16]. Meanwhile, plants have received more attention. Various studies have also shown the anticancer potential of plant nanoparticles, so that these plants have been applied for the AgNPs green synthesis [15]. If the anti-microbial and therapeutic effects of these nanoparticles are approved, this issue can be a step forward in the advancement of infections treatment methods [15,16].

Acetylated alcohols, as a valuable class of organic compounds have significant importance as intermediates during the synthesis of biologically active compounds [17,18]. Usually, the alcohol acetylation has been carried out by acetyl chloride or acetic anhydride using acid or base catalysts [1929]. Many of the methods for acetylation of alcohols in the literature have disadvantages such as low yields, relatively long time, harsh conditions, toxic organic solvents, and the use of expensive catalysts [3034]. Therefore, this study’s aim is to provide a new nanocatalyst with high efficiency for the synthesis of acetylated alcohol derivatives under solvent-free conditions as an eco-friendly method. So, we are interested in designing and introducing a mild method for in situ decorated silver nanoparticles over lignin (Lig) functionalized Fe3O4 NPs using Cydonia leaf extract to obtain the Fe3O4@Lig-Ag NPs (Scheme 1), and analyzing it using various analytical techniques, and evaluated its catalytic performance for acetylation of alcohols and study its anti-septic activities.

Scheme 1 
               Schematic fabrication of Fe3O4@Lig-Ag NPs nanocomposite mediated by Cydonia leaves and its catalytic activity for acetylation of alcohols.
Scheme 1

Schematic fabrication of Fe3O4@Lig-Ag NPs nanocomposite mediated by Cydonia leaves and its catalytic activity for acetylation of alcohols.

2 Experimental

2.1 Synthesis of the Fe3O4@Lig

The Fe3O4 NPs were prepared according to known procedures [30]. About 0.1 g of lignin (Lig) was added in H2O (50 mL) in a flask and sonicated for 10 min and then 0.5 g of the as-synthesized Fe3O4 NPs were mixed to Lig mixture. Then it was sonicated for 15 min and subsequently stirred for 12 h at 25°C. The prepared Fe3O4@Lig was isolated by a magnet, washed with water, and dried in air.

2.2 Preparation of Cydonia leaf extract

The aqueous extract of Cydonia leaves was obtained by boiling of 1 g of dried leaves in 30 mL DI H2O for 30 min. Then, to obtain a clear solution, the mixture was filtered by a Whatman No. 1 filter paper and used for the next step

2.3 Fabrication of Fe3O4@Lig-Ag NPs

About 0.5 g of Fe3O4@Lig was added to H2O (50 mL) and sonicated for 10 min. Next, an aqueous solution of AgNO3 (25 mg in 50 mL H2O) was added dropwise and stirred for 5 min. Next, the prepared extract of Cydonia leaves (20 mL) is added to the reaction mixture, which causes it to turn dark brown. The prepared Fe3O4@Lig-Ag NPs were collected from the medium by a magnet. The amount of Ag content was determined to be 0.063 mmol/g analyzed by inductively coupled plasma optical emission spectroscopy technique.

2.4 Acetylation of alcohols catalyzed by Fe3O4@Lig-Ag NPs

Generally, alcohols (1 mmol), acetic anhydride (3 mmol), and Fe3O4@Lig-Ag NPs (2 mol%) were added in a balloon flask and stirred under solvent-free condition at 25°C. After completion of the reaction that was monitored by TLC, the nanocatalyst was isolated by a magnet, and the products as well-known compounds were extracted with EtOAc.

2.5 In vivo design

In the recent study, 100 rats with weights of 220–230 g were used. Cecal ligation and puncture (CLP) were used for inducing the sepsis model in rats except control group. After anesthetizing the rats with Ketamine and Xylazine, 1 cm midline laparotomy was done under aseptic conditions. The cecum was tied tightly between the cecum floor and the ileocecal cap with a 4/0 silk suture. With the help of a 16-gauge needle, four holes in total were drilled from the cecum to the opposite side of mesentery. Sepsis was induced by CLP under anesthesia. Then, the cecum was placed and closed with 4/0 silk sutures.

The rats were divided into the following groups:

  1. Control group.

  2. Untreated group: CLP.

  3. Fe3O4@Lig-Ag NPs (5 µg/kg) group: CLP + Fe3O4@Lig-Ag NPs (5 µg/kg).

  4. Fe3O4@Lig-Ag NPs (15 µg/kg) group: CLP + Fe3O4@Lig-Ag NPs (15 µg/kg).

  5. Fe3O4@Lig-Ag NPs (45 µg/kg) group: CLP + Fe3O4@Lig-Ag NPs (45 µg/kg).

At the end of study, the rats were sacrificed by Ketamine and Xylazine and duodenum, stomach, liver, lung, and kidney were separated and washed with saline.

The levels of superoxide dismutase (SOD) (U/mg protein), glutathione (GSH) (mM/mg protein), and malondialdehyde (MDA) (µM/mg protein) in duodenum, stomach, liver, lung, and kidney tissues were measured by the methods of Sun et al. [35], Sedlak and Lindsay [36], and Ohkawa et al. [37], respectively.

The TNF-α mRNA and IL-1β expression levels in duodenum, stomach, liver, lung, and kidney tissues were measured by Livak and Schmittgen’s [38] method.

In this research, the results are displayed as an average of three repetitions of the standard error. T-test and one-way ANOVA were used for data statistical analysis, and p < 0.01 was considered significant.

3 Results and discussion

3.1 Characterization of the prepared Fe3O4@Lig-Ag NPs nanocomposite

The Fe3O4@Lig-Ag NPs was prepared by in situ decorating Ag NPs over Lig-coated Fe3O4 magnetic nanoparticles mediated by Cydonia leaf extract as shown in Scheme 1. The characterization of synthesized Fe3O4@Lig-Ag was performed over several analytical methods.

To investigate the surface shape and morphology of the Fe3O4@Lig-Ag and Fe3O4 nanoparticles, an FE-SEM electron microscope was used and is presented in Figure 1. The SEM images of Fe3O4@Lig-Ag reveal the defined globular to quasi-spherical morphology. In addition to compare with Fe3O4 nanoparticles, the successful functionalization with lignin and silver nanoparticles is detectable.

Figure 1 
                  Field emission scanning electron microscopy (FE-SEM) images of (a) Fe3O4 and (b) Fe3O4@Lig-Ag.
Figure 1

Field emission scanning electron microscopy (FE-SEM) images of (a) Fe3O4 and (b) Fe3O4@Lig-Ag.

Next, the electron dispersive X-ray spectrometer (EDX) data for establishing the preparation of Fe3O4@Lig-Ag nanocomposite, and the stepwise images during the synthesis from the substrate and intermediate are presented in Figure 2. The results depict the addition of carbon components of lignin to Fe (Figure 2a and b), and then the appearance of the Ag signal in Figure 2c confirmed the successful preparation of the Fe3O4@Lig-Ag. The EDX output was further studied by elemental mapping analysis for Fe3O4@Lig-Ag that illustrated the silver particles uniform distribution on the nanocomposite surface (Figure 3).

Figure 2 
                  EDX data of (a) Fe3O4, (b) Fe3O4@Lig, and (c) Fe3O4@Lig-Ag.
Figure 2

EDX data of (a) Fe3O4, (b) Fe3O4@Lig, and (c) Fe3O4@Lig-Ag.

Figure 3 
                  Elemental mapping of the Fe3O4@Lig-Ag.
Figure 3

Elemental mapping of the Fe3O4@Lig-Ag.

Transmission electron microscopy (TEM) analysis was provided to determine a more detailed structure of synthesized Fe3O4@Lig-Ag nanocomposite. Figure 4 presents the TEM images of Fe3O4 NPs, Fe3O4@Lig, and Fe3O4@Lig-Ag, respectively. From Figure 4b, the Fe3O4@Lig intermediate seems to be globular shaped, like Fe3O4 NPs (Figure 4a) with a shell over the particles corresponding to lignin coated on the surface of Fe3O4. The size of the magnetic nanoparticles was around 10–20 nm and the Ag spots as black-colored and bigger with a dimension of 20–30 nm over the Fe3O4@Lig NPs are detectable.

Figure 4 
                  TEM images of (a) Fe3O4, (b) Fe3O4@Lig, and (c) Fe3O4@Lig-Ag.
Figure 4

TEM images of (a) Fe3O4, (b) Fe3O4@Lig, and (c) Fe3O4@Lig-Ag.

The magnetic properties of the prepared Fe3O4, Fe3O4@Lig, and Fe3O4@Lig-Ag NPs were recorded by vibrating-sample magnetometer (VSM) analysis (Figure 5). The magnetic saturation value for Fe3O4, Fe3O4@NaLS, and Fe3O4@NaLS/Ag NPs were 56.8, 42.9, and 13.7 emu g−1, respectively. The magnetic saturation decrease is because of adding the diamagnetic lignin layers and the supported Ag NPs on the magnetic surface.

Figure 5 
                  VSM data of (a) Fe3O4, (b) Fe3O4@Lig, and (c) Fe3O4@Lig-Ag.
Figure 5

VSM data of (a) Fe3O4, (b) Fe3O4@Lig, and (c) Fe3O4@Lig-Ag.

Figure 6 depicts the comparative fourier transformed infrared spectroscopy (FT-IR) spectrum of the precursor of Fe3O4@Lig and Fe3O4@Lig-Ag nanocomposite in a common frame to justify the successful support of Ag NPs. The existence peaks at 455 and 630 cm−1 belong to Fe–O–Fe bond and a broad band at 3,000–3,500 cm−1 (O–H stretching vibration), confirmed the presence of magnetite nanoparticles (Figure 6a). The successful synthesis of Fe3O4@Lig was shown by the appearance of the vibrations at 3,421 cm−1 (O–H), 2,922 cm−1 (C–H), 1,645 cm−1 (C═O), and 1,433 cm−1 (C–H) belonging to lignin attachment. Next, from the FT-IR spectrum of Fe3O4@Lig-Ag (Figure 6b), the Ag NPs decoration on the Fe3O4@Lig surface could be detected by minor changes in peak positions as compared to Figure 6a.

Figure 6 
                  FT-IR spectra of (a) Fe3O4@Lig and (b) Fe3O4@Lig-Ag.
Figure 6

FT-IR spectra of (a) Fe3O4@Lig and (b) Fe3O4@Lig-Ag.

The X-ray diffraction (XRD) result of the Fe3O4@Lig-Ag indicated the crystalline nature of Fe3O4 nanoparticles by appearance of the related reflections as (220), (311), (400), (422), (511), and (440) that is given in Figure 7. Comparing the XRD pattern of Fe3O4 (Figure 7a), it is established that the support of Ag NPs over Fe3O4@Lig nanoparticles does not affect the magnetite structure. The significant diffraction peaks at 2θ = 39.1°, 44.5°, 64.3°, and 77.1° are assigned to the Ag fcc planes (111), (200), (220), and (311) (JCPDS No. 04-0783).

Figure 7 
                  XRD profile of (a) Fe3O4 and (b) Fe3O4@Lig-Ag.
Figure 7

XRD profile of (a) Fe3O4 and (b) Fe3O4@Lig-Ag.

3.2 Catalytic performance of Fe3O4@Lig-Ag nanocomposite

Next, the catalytic activity of the prepared Fe3O4@Lig-Ag composite in the acetylation of alcohols in the presence of acetic anhydride (acetylating agent) was evaluated. The benzyl alcohol reaction with Ac2O is selected as the probe reaction for the optimization of the amount of catalyst, solvent, and the reaction time at room temperature. The obtained findings revealed in Table 1 are shown in entry 7 as the best conditions for the model reaction that involve catalyst loading (2 mol%) and solvent-less conditions.

Table 1

Optimizing acetylation of benzyl alcohol in the presence of Fe3O4@Lig-Ag catalysta

Entry Solvent Catalyst (mol%) Time (h) Yield (%)
1 EtOH 2 5 75
2 MeOH 2 2 70
3 CH2Cl2 2 2 75
4 Toluene 2 3 70
5 CH3CN 2 3 65
6 H2O 2 4 15
7 2 1 98
8 3 1 98
9 1 2 85
10 12 10

aReaction conditions: benzyl alcohol (1 mmol), Ac2O (3 mmol), 25°C, and solvent (3 mL).

After finding the conditions, the acetylation reaction was carried out using different alcohol derivatives. Benzylic alcohols with electron‐withdrawing and electron‐donating substitutions were found to be carried out with good yields (Table 2, entries 21-4). Table 2 documents that the corresponding acetylated products for phenols, cinnamyl alcohol, phenylethyl alcohol, benzhydrol, and cyclohexanol were obtained with good yields (Table 2, entries 4–10). Also, the tertiary alcohol (1‐adamantanol and 2‐adamantanol) was efficiently affording good yields (Table 2, entries 11, 12).

Table 2

Acetylation of alcohols catalyzed by Fe3O4@Lig-Ag under solvent‐free conditiona

Entry Substrate Time (h) Yield (%)b
1 Benzyl alcohol 1 98
2 4-Bromo-benzyl alcohol 0.75 98
3 4-Chloro-benzyl alcohol 0.75 98
4 2,4-Dichloro-benzyl alcohol 0.5 96
5 Phenol 3 95
6 4-Chloro-phenol 4 95
7 Cinnamyl alcohol 3 80
8 Phenylethyl alcohol 3 90
9 Benzhydrol 2 96
10 Cyclohexanol 4 80
11 2-adamantanol 2 90
12 1-adamantanol 3 90
  1. aReaction conditions: substrate (1 mmol), catalyst (2 mol%), Ac2O (3 mmol) at 25°C under solvent free conditions.

  2. bIsolated yields.

Recycling of the catalyst is one of the important factors in the field of catalyst synthesis. To investigate this item, the isolated Fe3O4@Lig-Ag catalyst after the first run was applied again with the model reaction for ten runs without significant loss in its activity (Figure 8). Furthermore, the TEM and SEM images of the recovered catalyst (Figure 9) indicated that the morphology of the reused catalyst did not affect any change, which confirmed the stability and efficiency of the catalyst.

Figure 8 
                  Reusability of the Fe3O4@Lig-Ag in the acetylation of benzyl alcohol.
Figure 8

Reusability of the Fe3O4@Lig-Ag in the acetylation of benzyl alcohol.

Figure 9 
                  (a) TEM and (b) FE-SEM images of reused catalyst after 10th cycles.
Figure 9

(a) TEM and (b) FE-SEM images of reused catalyst after 10th cycles.

Scheme 2 presents the catalytic mechanism of Fe3O4@Lig-Ag for the acetylation of alcohols. The Ag NPs can attach to the carbonyl of acetic anhydride and activate the nucleophilic attack of the oxygen group of alcohol. Then the related product was obtained with the silver release to regenerate the catalyst for the next use [34].

Scheme 2 
                  Plausible reaction mechanism of Fe3O4@Lig-Ag-catalyzed acetylation.
Scheme 2

Plausible reaction mechanism of Fe3O4@Lig-Ag-catalyzed acetylation.

When the metallic nanoparticles enter the body, the immune system recognizes and responds to them. This answer can be different according to the nanoparticles physicochemical properties, such as hydrophobicity degree, shape, charge, and size. The nanoparticles interaction with several immune system components such as antigen-processing cells and neutrophils depends on the nanoparticles characteristics [39]. Allergic reactions of nanoparticles also are other immune system stimulation. Several studies have linked nanoparticle exposure to allergic reactions in humans and animals. Also, many reactions of the body’s immune system are caused by the inflammatory cytokines production. Different research studies have presented cytokine induction with several types of NPs (lipid nanoparticles, polymers, dendrimers, gold colloids, etc.). Information about the immunological effects of nanoparticles on innate immune system cells (natural killer cells, mast cells, dendritic cells, neutrophils, and macrophages) and acquired immune system cells helps to develop immunological products based on nanoparticles [40]. Innate immune system cells express inflammatory cytokines, activate T lymphocytes, and activate inflammasomes. By affecting mast cells, nanoparticles cause the release of histamine and the increase of cytosolic calcium ions. Also, metallic nanoparticles can increase the stimulation of natural killer cells in the antigen presentation process. Nanoparticles strengthen the acquired immunity during vaccination by affecting B cells and help to target B cell lymphoma without any chemotherapy. Nanoparticles interaction with T lymphocytes can cause Thi and The response and increase cytokine production [40]. Based on the body’s immune responses to NPs, these substances can be applied in the treatment of cancers and autoimmune diseases, as well as being used as vaccines [41,42].

Nanoparticles have an extremely small size and their size can be controlled to perform antimicrobial operations and fight against intracellular microbes. Infection treatment caused by drug-resistant strains and intracellular pathogens using antibiotics becomes more complicated due to the poor transport of antibiotics [4345]. Therefore, medium-sized drugs have low activity on intracellular microbes. A treatment way by nanoparticle-carried drugs has been suggested to solve this problem. Host phagocytes easily phagocyte the nanoparticles due to their small size. In addition, the structure of several kinds of nanoparticles is suitable for carrying liposomal nanoparticles, whose walls are covered by one or more lipid layer around the nanoparticles [46], Therefore, nanoparticles can enter the host cells through endocytosis and release the drug.

Drug carriers made of nanoparticles can raise the antibiotic serum level and protect the drug against mechanisms that cause resistance in microbes. These carriers protect drugs from harmful chemical reactions, thus maintaining the drugs potency to exert antimicrobial activity. In addition, protection against mechanisms that cause resistance in microbes is a very important mechanism [46,47]. Increasing the efflux flow of pumps and reducing the antibiotic absorption in bacterial cells (such as Escherichia coli and Pseudomonas aeruginosa) are the two main reasons for antibiotic resistance. But, scientists have indicated that several nanoparticles can overcome these mechanisms and inhibit the resistance of drug. In the digestive tract, dendrimers can prevent the flow created by P-glycoprotein pumps [47].

Drug carriers made of nanoparticles can help in targeting the infection site by antibiotics and thereby reduce systemic side effects. Absorption of high-dose drugs and their concentration in the desired place (the site of infection) while inhibiting side effects, including drug toxicity, is a difficult task when by conventional antibiotics without a carrier. Antimicrobial drug systems use nanoparticles to transfer the drug to the infection place, thus reducing unwanted side effects due to high doses in this area [47,48]. Drug delivery using nanoparticles is based on active or passive targeting. Passive targeting is achieved by increasing penetration and retention at the site of infection, and active targeting is achieved by modifying the nanoparticles surface, and the drug delivery system based on nanoparticles is allowed to recognize selectively specific ligands on the infection site cells. Active targeting includes temperature, receiver, and magnetic targeting. Vancomycin prevents Gram-positive bacteria, but has strong toxicity to the kidney and ear. One of the ways to ameliorate the treatment is to raise the amount of drug transfer to the desired site, i.e., the site of infection [4648]. Therefore, the amount of organs affected by the drug is limited in the parts that are unnecessary. With the help of nanoparticles, the modified vancomycin carrier was designed with mesoporous silica nanoparticles, and these nanoparticles have made it possible to selectively destroy Gram-positive disease bacteria such as macrophages on the cells. An important and effective strategy that is often used to achieve targeted therapy is to first target macrophages with nanoparticles. Since many active bacteria in infected places are swallowed and targeted by macrophages, and the drugs in the nanoparticles are released inside the macrophages in which there are bacteria [48].

By using nanoparticles as a carrier, the release of antibiotics can be controlled. By using old methods for drug delivery, the level of the drug in the blood for a short time is in a large range, which is more than the maximum dose tolerated by the body, or it may not be able to reach the lowest effective dose [4850]. Totally, we need frequent doses of the drug, which is associated with more side effects for the patient. As a result, proper stability reduces the dosage of the drug, improves the patient’s performance, and reduces the patient’s pain [49,50]. Comparing the use of a drug that is delivered through a nanoparticle carrier with the same drug in a similar concentration when it is used freely and without a carrier, shows that nanoparticle carriers have a much more prominent inhibitory activity on cell growth, and in addition, long-term release of the drug also occurs. Also, nanoparticles may be activated by several types of controllable excitable agents such as chemicals, heat, pH, light, and magnetic field [49]. The use of a suitable carrier with the type of nanoparticle in ophthalmic drugs can increase the retention time in the pre-cornea region. The drugs released such as levofloxacin is controlled and compared to the usual eye solutions, and the therapeutic effect is better [50].

Carrier nanoparticles have the ability to combine and transport several antibacterial drugs. This feature is available on two levels. On the one hand, when the bacterial cell encounters a type of nanoparticle that contains several types of antibacterial drugs, it becomes very difficult to create resistance in the bacteria [49,50] because probability of creating multiple mutations at the same time is very small. Combination of several drugs simultaneously leads to higher efficiency because of the use of multiple mechanisms. Also, several types of nanoparticles can be applied in combination to increase antibacterial properties and prevent resistance. Each type of nanoparticles has disadvantages that can be adjusted if two or more nanoparticles are used at the same time [49,50]. For example, liposomal nanoparticles have disadvantages, such as their poor stability, short shelf life, rapid uptake, less cellular interaction, or slower absorption and transmembrane transfer. Also, solid lipid nanoparticles inherently have little ability to bind and also tend to bind to gelatin in an unpredictable manner, while hybrid nanoparticles can compensate for all the above-mentioned weaknesses. In addition, by using the combined method, a long-term effective time can be obtained, which significantly and effectively reduces the possibility of developing resistance in bacteria [49].

In the current research, CLP was used for inducing the sepsis model in rats. Several doses of Fe3O4@Lig-Ag NPs (45, 15, and 5 µg/kg) on oxidant-antioxidant, inflammatory mediators mRNA such as IL-1 and TNF-α and its effects on the levels of expression were assessed in kidney, liver, duodenum, lung, and stomach. The TNF-α mRNA expression in the CLP+ 5, 15, and 45 µg/kg group was decreased in comparison with the control group (Figures 10 and 11). Fe3O4@Lig-Ag NPs reduce oxidative stress by enhancing the free radicals scavenging effects and supporting endogenous antioxidants. The Fe3O4@Lig-Ag NPs high antioxidant property may be related to the cytokine cascade suppression during sepsis.

Figure 10 
                  Effects of Fe3O4@Lig-Ag NPs on the IL-1β mRNA expression levels.
Figure 10

Effects of Fe3O4@Lig-Ag NPs on the IL-1β mRNA expression levels.

Figure 11 
                  Effects of Fe3O4@Lig-Ag NPs on the TNF-α mRNA expression levels.
Figure 11

Effects of Fe3O4@Lig-Ag NPs on the TNF-α mRNA expression levels.

When septic rats kidney, liver, duodenum, lung, and stomach were compared with those of the control group, it was found that Fe3O4@Lig-Ag NPs administration dose-dependent raised glutathione levels and superoxide dismutase activity and reduced significantly the levels of malondialdehyde (p < 0.01). The Fe3O4@Lig-Ag NPs (45 µg/kg) indicated greater anti-oxidative effects than the 5 and 15 µg/kg doses for all the assessed parameters (Figures 1216).

Figure 12 
                  Effects of Fe3O4@Lig-Ag NPs on the oxidant–antioxidant levels (SOD [U/mg protein], GSH [mM/mg protein], and MDA [µM/mg protein]) in the liver tissues.
Figure 12

Effects of Fe3O4@Lig-Ag NPs on the oxidant–antioxidant levels (SOD [U/mg protein], GSH [mM/mg protein], and MDA [µM/mg protein]) in the liver tissues.

Figure 13 
                  Effects of Fe3O4@Lig-Ag NPs on the oxidant–antioxidant levels (SOD [U/mg protein], GSH [mM/mg protein], and MDA [µM/mg protein]) in the kidney tissues.
Figure 13

Effects of Fe3O4@Lig-Ag NPs on the oxidant–antioxidant levels (SOD [U/mg protein], GSH [mM/mg protein], and MDA [µM/mg protein]) in the kidney tissues.

Figure 14 
                  Effects of Fe3O4@Lig-Ag NPs on the oxidant–antioxidant levels (SOD [U/mg protein], GSH [mM/mg protein], and MDA [µM/mg protein]) in the lung tissues.
Figure 14

Effects of Fe3O4@Lig-Ag NPs on the oxidant–antioxidant levels (SOD [U/mg protein], GSH [mM/mg protein], and MDA [µM/mg protein]) in the lung tissues.

Figure 15 
                  Effects of Fe3O4@Lig-Ag NPs on the oxidant–antioxidant levels (SOD [U/mg protein], GSH [mM/mg protein], and MDA [µM/mg protein]) in the duodenum tissues.
Figure 15

Effects of Fe3O4@Lig-Ag NPs on the oxidant–antioxidant levels (SOD [U/mg protein], GSH [mM/mg protein], and MDA [µM/mg protein]) in the duodenum tissues.

Figure 16 
                  Effects of Fe3O4@Lig-Ag NPs on the oxidant–antioxidant levels (SOD [U/mg protein], GSH [mM/mg protein], and MDA [µM/mg protein]) in the stomach tissues.
Figure 16

Effects of Fe3O4@Lig-Ag NPs on the oxidant–antioxidant levels (SOD [U/mg protein], GSH [mM/mg protein], and MDA [µM/mg protein]) in the stomach tissues.

One of the ways to remove the bacteria is reactive oxygen species (ROS) produced by nanoparticles. ROS production is the main antibacterial mechanism for NPs. ROS is a general term for mediators and molecules in the reaction that several types of nanoparticles yield several types of ROS by decreasing the oxygen molecules. Four types of ROS are O2, H2O2, OH, and superoxide radical [51], which indicate several levels of activity and dynamics. For example, MgO and CaO NPs can produce O2, while ZnO NPs can produce OH and H2O2, but they do not have the ability to produce O2. Meanwhile, CuO NPs can yield all four types of ROS. Research has shown that H2O2 and O are neutralized by internal antioxidants such as catalase and superoxide enzymes and cause less stress reactions. While O2 and OH can cause acute microbial death [51].

Normally, the ROS production in bacterial cell is balanced, on the other hand, with the excessive production of ROS, the cell redox balance moves toward oxidation. The unbalanced state damages the bacterial cell components by creating oxidative stress [52]. In a research approved that Al2O3 nanoparticles pass by the cell membrane and enter the cell. Then the nanoparticles interact with the cell membrane and probably because of intracellular oxidative stress causes the loss of membrane integrity. In the same method, nano-silver ions are applied as the catalytic activity center to activate oxygen in water or air. It results in the reactive oxygen ions and hydroxyl radical’s production that inhibit the bacteria proliferation or destroy them [53]. Many studies have also shown that ROS are effective in raising the gene expression level producing oxidative proteins, which is the main mechanism of bacterial cell apoptosis. In addition, oxygen-active species can attack proteins and decrease some periplasmic enzyme activity, which is necessary to maintain normal physiological and morphological processes [54,55]. As another example, nanoparticles are activated under the effect of ultraviolet rays and visible light, and as a result, they create very reactive oxygen-active species. Hydroxyl superoxide radicals with a negative charge can be kept on the surface of cell, while H2O2 can pass by the cell membrane and enter the bacterial cell. SEM presents that oxide nanoparticles affected the Campylobacter jejuni cells spiral shape and turned them into spherical shape and caused some cell damage degree as well as cell leakage [56]. In addition, the RT-PCR method showed that ROS increase the oxidative stress genes expression level, Ahp C, Kat A, and Dna K [57]. The thiorude and casein (Trx) system, which consists of nicotinamide adenine dinucleotide, thiorude phosphate, and casein reductase (TrxR), is a main disulfide reductase system that bacteria use in the condition of oxidative stress. It was determined based on the studies of Qing et al. that silver binds to the Trx and TrxR active sites and causes oligomerization and dysfunction of TrxR and TrxR [58].

4 Conclusion

This article represents an environmental-friendly green procedure for the bio-synthesis of Fe3O4@Lig-Ag, where Ag NPs were in situ supported over the surface of lignin (Lig)-coated Fe3O4 nanocomposite mediated by Cydonia leaf extract. Several advanced instrumental techniques were employed in assessing the physicochemical properties. The Fe3O4@Lig-Ag showed good catalytic performance for the acetylation of alcohols with good efficiency. In the in vivo condition, the TNF-α mRNA expression in CLP + 5, 15, and 45 µg/kg group was decreased in comparison with the control group. When septic rats kidney, liver, duodenum, lung, and stomach were compared with those of the control group, it was found that Fe3O4@Lig-Ag NPs dose-dependent administration raised antioxidant enzyme activity and reduced significantly the levels of malondialdehyde. The Fe3O4@Lig-Ag NPs high antioxidant potential may be related to the cytokine cascade suppression during sepsis. Fe3O4@Lig-Ag NPs reduced oxidative stress by enhancing the free radicals scavenging effects and supporting endogenous antioxidants. The above findings offer that Fe3O4@Lig-Ag NPs administration may indicate a modern treatment for the inhibition of liver, kidney, lung, duodenum, and stomach tissues damage caused by septic conditions.

  1. Funding information: This study was supported by Development Plan of Traditional Chinese Medicine Science and Technology of Shandong Province (2019-0390), Shandong Provincial Natural Science Foundation (No. ZR2020MH347), and National Natural Science Foundation of China (81974545).

  2. Author contributions: Lei Zhou, Yanfen Yao, Quanzhen Wang: Visualization, Writing original draft, Formal analysis. Peng Wang, Shan Hong, Li Kong: Writing original draft, Formal analysis, Writing – review and editing, Funding acquisition, Methodology, Supervision. All authors reviewed the manuscript.

  3. Conflict of interest: The authors state no conflict of interest.

  4. Ethical approval: The conducted research is not related to either human or animal use.

  5. Data availability statement: Derived data supporting the findings of this study are available from the corresponding author on request.

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Received: 2023-06-20
Revised: 2023-08-26
Accepted: 2023-09-08
Published Online: 2023-11-22

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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