Home The abrogative effect of propolis on acrylamide-induced toxicity in male albino rats: Histological study
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The abrogative effect of propolis on acrylamide-induced toxicity in male albino rats: Histological study

  • Khalid M. Al Syaad , Amin A. Al-Doaiss , Ahmed Ezzat Ahmed , Haitham El-Mekkawy , Mohamed Abdelrahman , Ahmed A. El-Mansi , Muhammad Fakhar-e-Alam Kulyar and Montaser Elsayed Ali EMAIL logo
Published/Copyright: May 5, 2023
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Open Chemistry
From the journal Open Chemistry Volume 21 Issue 1

Abstract

The present study investigated the toxic action of acrylamide (ACR) and the abrogative effect of aqueous propolis extract on ACR-induced toxicity in male albino rats. Forty adult male albino rats were randomly divided into four groups and administered the treatment doses orally by gavage. Control, treated with a physiological solution (5.0 ml/rat). ACR-treated group, treated with ACR 25 mg/kg. ACR + propolis, treated with 25 mg/kg ACR + 100 mg/kg propolis. Propolis-treated group, treated with 100 mg/kg. The treatment period was 28 days, the treatment doses were administered orally using a gavage stomach tube. The results showed that the presence of ACR increased (P < 0.001) the level of liver enzymes alanine aminotransferase (167.2 vs 90.15) and aspartate aminotransferase (120.66 vs 41.52) in the liver tissue serum and lipid peroxidation products (80.11 vs 39.3); also, it decreased (P < 0.001) the total capacity of antioxidants (113.4 vs 189.41) compared to the control group. The histological analysis of the kidney revealed alterations induced by ACR, including atrophy, necrosis, renal glomeruli atrophy, tubular necrosis, enlargement of the glomeruli, hemorrhage, and edema surrounding the blood vessels. Also, the results showed that the rats treated with propolis improved liver and kidney functions because of propolis’s efficiency against the harmful effects of ACR. Moreover, the histological examination of the liver tissue revealed negative changes, with focal necrosis in hepatocytes. Microscopic examination showed tubular necrosis within the seminiferous tubules, sloughing, and desquamation of sperm cells into the lumen. Also, an infiltration of protein substances between the tubules and degenerative vacuolar changes between sperm cells was observed. The renal, hepatic, and testicular tissues appeared almost similar to the control group, except for some minor changes. This study proved that feeding the rats with propolis reduced these pathological effects and restored the tissues to a normal state. It is concluded that using propolis with ACR significantly reduced the biochemical and histological damage caused by ACR, and recommends using propolis as a cytoprotective agent against pathological toxicity of ACR.

Keywords: acrylamide; propolis; antioxidant; toxicity; rat

1 Introduction

There has been widespread use of acrylamide (ACR) in many industries, such as cosmetics, paper, textile, wastewater treatment, printing materials, polymers, and copolymer production worldwide [1]; even in medicine, it has been used to create high molecular polymers like poly-ACR [2]. Acrylamide (C3H5NO) is a highly reactive, white, odorless crystalline toxic carbonyl compound with high-water solubility and chemical activities. Furthermore, there are numerous inadvertent ACR sources in daily life, such as processed foods, where ACR is created by the Maillard reaction between monosaccharaides and proteins while cooking these foods at high temperatures (>120°C). ACR is formed during the cooking of carbohydrate-rich foods such as potato chip fries, bread, biscuits, cereals, toasted bread, roasted coffee beans, crisps, malt beverages, fish, and chicken nuggets [3,4]. The International Agency for Research on Cancer classified ACR as a class 2A drug in 1994 because it was most likely carcinogenic to humans [2]. Many studies have indicated that ACR has a toxic effect that disturbs different body organs and systems (hepato-nephrotoxicity, neurotoxic, genotoxic, and carcinogenic effects and has a reproductive toxic action) [5,6,7]. In comparison, other studies showed that ACR has neurotoxic and hepatotoxic effects, as well as pathological embryogenesis [6,8,9]. ACR is absorbed in the alimentary tract and metabolized in the liver [10].

Globally, natural medicinal products have been increasingly used more than synthetic ones. In this regard, antioxidant-rich substances have been identified as potential therapeutic agents. Furthermore, because of their antioxidant activities, natural herbal products protect against toxic side effects and are used as chemotherapeutic agents [1,7]. Propolis is the natural resinous material of different plants and is collected by honeybees; it consists of many natural compounds [11]. Honeybees synthesize propolis, a sticky, resinous substance used in constructing and maintaining their hives, combining the waxes produced by them with resins gathered from various plants. Polyphenols (flavonoid aglycones, phenolic acids and their esters, phenolic aldehydes), alcohols and ketones, sesquiterpenes, quinones, coumarins, steroids, amino acids, and inorganic chemicals are all found in propolis [12,13]. It contains around 150 polyphenol components, including flavonoids, phenolic acid, and their esters [14]. Previously, different countries have used propolis for a long time to compact many diseases due to its antioxidant content [15]; therefore, it is commonly used in traditional medicines. Also, many previous recommendations exist for supplementing propolis in fighting diseases and cancer prevention [16,17]. In addition, investigators are interested in propolis potential to minimize the adverse effects of cancer therapy [18,19]. Caffeic acid phenethyl ester (CAPE), an active ingredient of propolis, could depress tumor growth by signaling networks that control the growth of the cancer cells in breast, bladder, and prostate cancers [20].

Moreover, propolis flavonoids showed cytotoxic activity against fibrosarcoma and lung adenocarcinoma [16]. In addition, some studies reported that propolis has anticarcinogenic properties through immunomodulation action [21]. The extracts of propolis have been attributed to biological and pharmacological activities, such as free radical scavenging, antitumor, local, immunomodulatory effects, anesthetic, anti-inflammatory, antibiotic, antioxidative, antiviral, antimicrobial, antifungal [13,14]. Free radical scavenging is one of the propolis therapeutical actions; according to many in vivo and in vitro studies, it is used as a stimulant agent of the immune system [22]. Moreover, this natural product was reported to support tissue regeneration and blood capillary strengthening [23]. However, the studies evaluating propolis’s efficiency against ACR toxicity are still limited.

The current study aims to evaluate the histological and histochemical changes in the hepatic, renal, and testicular tissues induced by oral administration of ACR and the potential protective role of the propolis extract against ACR-induced toxicity in rats.

2 Materials and methods

All experiments were carried out in the Physiology Lab., Department of Biology, College of Science, King Khalid University, Saudi Arabia.

2.1 Chemicals

Acrylamide (catalog No: A9099; Sigma-Aldrich, St. Louis, MO, USA) and propolis (catalog Sigma-Aldrich, St. Louis, MO, USA) were used in this study.

2.2 Experimental animals

Forty adult male Wistar albino rats (10–12 weeks old) weighing 200–230  g were used in this study. Animals were randomly divided into four groups (n = 10 per group). Control, treated with a physiological solution (5.0 ml/rat). ACR-treated group, treated with ACK 25 mg/kg. ACR + propolis, treated with 25 mg/kg ACR + 100 mg/kg propolis. Propolis-treated group, treated with 100 mg/kg. Animals were housed under standard temperature conditions (23 ± 2°C) and lighting (12 h; light/dark cycles), with free access to food and drinking water ad libitum. The experiment lasted for 28 days, and the treatment doses were administered orally by gavage.

2.3 Collection of serum and estimation of aspartate aminotransferase (AST), alanine aminotransferase (ALT), total antioxidant capacity (TAC), thiobarbituric acid reactive substance (TBARS)

At the end of the experimental period, blood samples were taken from the retro-orbital plexus under light ether anesthesia without anticoagulant and allowed to clot for 10 min at room temperature. The blood was centrifuged at 3,500 rpm for 10 min at 0°C to obtain the serum. The serum collected was kept at ‒80°C until used. The enzymes for liver functions included AST, estimated according to Belfield and Goldberg [24], and ALT, estimated according to Kind and King [25]. Also, the TAC (Biodiagnostic) was measured according to Koracevic et al. [26]. In contrast, lipid peroxidation and TBARS were measured according to Svingen et al. [27], and determined in the homogenized liver samples of all groups. Biochemical analysis was performed using Spectrophotometer Model 25 Lambda (manufactured by Elmer Perkin, Germany).

2.4 Histology

Fresh samples of each rat’s liver, kidney, and testes were rapidly dissected and fixed in neutral buffered formalin (10%). The fixed specimens were processed according to El-Refaiy and Eissa [28] for dehydration with different grades of ethanol (70, 80, 90, 95, and 100%), clearing in two changes of xylene and impregnation with two changes of molten paraffin wax, using an automatic tissue processor (Sakura, Japan). The specimens were embedded and blocked using an embedding station (Sakura, Japan). Serial sections of 4–5 µm thickness were cut using a microtome (ModelRM2245; Leica, Germany), while an autostainer (Model 5020; Leica, Germany) was used for hematoxylin/eosin staining of the sections. Histochemical staining was performed using standard hematoxylin eosin and periodic acid schiff techniques [29]. The mounted specimens were examined for alterations in the hepatic tissues of each rat under study using an optical microscope (Olympus Microscope with Digital Camera DP73, Japan). An experienced pathologist performed all subsequent histopathological examinations without knowledge of the previous treatments. Stained sections of control and treated rats were examined for alterations in the architecture.

2.5 Statistical analysis

The biochemical parameters were represented as mean ± standard deviation (SD). Differences between mean values in different groups were tested for significance using a one-way analysis of variance followed by Duncan’s test, and P < 0.05 was considered significant using the statistical analysis system (SPSS, 1996).

3 Results

3.1 Biochemical parameters

The animals treated with ACR exhibited a significant increase in the liver profile enzymes (P < 0.05) in ALT, AST, TAC levels, as well as lipid peroxidation (TBARS) compared to the control group and treated groups (Table 1). Meanwhile, propolis enhanced liver and kidney functions in rats treated with ACR and propolis. In contrast, a significant decrease was observed in ALT and AST enzymes compared to samples treated with ACR only (Table 1).

Table 1

AST, ALT levels, and TAC in the serum and the level of lipid peroxidation (TBARS) in the liver tissue

Parameters mean ± SD Control Acrylamide Acrylamide + propolis Propolis
TBARS (nmol/g tissue) 39.3 ± 3.51 80.11 ± 4.43*** 48.7 ± 4.23 38.66 ± 4.22
TAC (µm/l) 189.41 ± 8.1 113.4 ± 7.2** 170.23 ± 6.9 194.2 ± 7.11
ALT (mg/dl) 90.15 ± 7.61 167.2 ± 8.17*** 122.04 ± 7.47* 87.07 ± 6.1
AST (mg/dl) 41.52 ± 4.51 120.66 ± 7.4*** 77.4 ± 6.41* 48.13 ± 5.01

Mean ± SD, ***P < 0.001, **P < 0.01, *P < 0.05, significant compared with the control group.

There was a significant increase (P < 0.001) in the level of lipid peroxidation products (TBARS) in the liver tissues of the ACR-treated group compared with the control group. In contrast, a non-significant increase (P > 0.05) was observed in the ACR + propolis-treated group and a non-significant decrease in the propolis-treated group compared to the control group (Table 1).

The study showed a significant decrease (P < 0.01) in the TAC level in the serum of the ACR-treated group. Moreover, there was a decrease (P > 0.05) in the ACR + propolis-treated group. Also, there was a non-significant increase in the propolis-treated group compared with the control group.

Meanwhile, the serum ALT and AST levels were higher (P < 0.001) in the ACR-treated group, and there was a significant decrease (P < 0.05) in the ACR + propolis-treated group compared with the control group. However, when treated with propolis, the liver functions improved and helped liver enzymes to return to normal levels (Table 1).

3.2 Histopathological studies

3.2.1 Renal alterations

The kidneys showed normal glomeruli and renal tubular microanatomy in the control group, as shown in Figure 1.

Figure 1 Cross section of the kidney cortex of the control group, showing Bowman’s capsule (BC), proximal convoluted tubules (PCT), distal convoluted tubules (DCT), and normal blood vessels (arrows) between renal tubules.
Figure 1

Cross section of the kidney cortex of the control group, showing Bowman’s capsule (BC), proximal convoluted tubules (PCT), distal convoluted tubules (DCT), and normal blood vessels (arrows) between renal tubules.

Histopathological examinations of the kidneys of rats exposed to the ACR indicated the appearance of many histopathological changes, such as dilatation and congestion of glomerular capillaries, dilatation, and congestion of blood vessels between the renal tubules compared with the control rats.

In addition to the infiltration of protein materials inside and outside the renal tubules, hydropic degeneration in the cells of the renal tubules, atrophy in some renal glomeruli, necrosis, and edema or inflammatory edema, with some bleeding around renal blood vessels, infiltration of inflammatory cells and focal fibrosis in between the renal tubules were also seen (Figure 2a–h).

Figure 2 (a–h) Photomicrographs of the cross sections of the kidney cortices in the ACR -treated group indicating dilated and congested glomerular capillaries (✺) and dilated and congested blood vessels between the renal tubules (✸). In addition to the infiltration of protein materials inside and outside the renal tubules (☼), hydropic degeneration in the cells of the renal tubules (H), atrophy in some renal glomeruli (△), necrosis (N), and edema or inflammatory edema (E), with some bleeding around renal blood vessels, infiltration of inflammatory cells (IF) and focal fibrosis (F) in between the renal tubules are also seen.
Figure 2

(a–h) Photomicrographs of the cross sections of the kidney cortices in the ACR -treated group indicating dilated and congested glomerular capillaries (✺) and dilated and congested blood vessels between the renal tubules (✸). In addition to the infiltration of protein materials inside and outside the renal tubules (☼), hydropic degeneration in the cells of the renal tubules (H), atrophy in some renal glomeruli (△), necrosis (N), and edema or inflammatory edema (E), with some bleeding around renal blood vessels, infiltration of inflammatory cells (IF) and focal fibrosis (F) in between the renal tubules are also seen.

The cortex of the kidney of the (ACR + propolis)-treated group and the propolis-treated group showed normal renal architecture with normal PCT, normal DCT, and normal peritubular blood vessels, and the absence of any pathological changes (Figure 3a and b).

Figure 3 (a) A cross section of the cortex of the kidney of the (ACR + propolis)-treated group, (b) a cross section of the renal cortex of the propolis-treated group. The two sections show a normal renal architecture with normal glomeruli (G) surrounded by BC, normal PCT, DCT, and normal peritubular blood vessels (arrows) associated with the absence of any pathological changes.
Figure 3

(a) A cross section of the cortex of the kidney of the (ACR + propolis)-treated group, (b) a cross section of the renal cortex of the propolis-treated group. The two sections show a normal renal architecture with normal glomeruli (G) surrounded by BC, normal PCT, DCT, and normal peritubular blood vessels (arrows) associated with the absence of any pathological changes.

3.2.2 Hepatic alterations

Microscopic examination of the liver of control rats demonstrated a normal well-preserved architecture, with normal histological components of the hepatic lobules and portal areas, a normal central vein (CV) bounded by an intact endothelium. Parallel cords of hepatocytes radiate from the CV toward the periphery of the hepatic lobule and are separated by normal sinusoidal spaces in the liver of all control rats (Figure 4a and b).

Figure 4 (a and b) Photomicrographs of a hepatic tissue cross section of the control group showing the CV, polygonal hepatocytes (H) with rounded nuclei (N); the hepatocytes are arranged in the form of hepatic cords radiating from the CV to the border hepatic lobule, separating the hepatic cords by small blood sinusoids (S).
Figure 4

(a and b) Photomicrographs of a hepatic tissue cross section of the control group showing the CV, polygonal hepatocytes (H) with rounded nuclei (N); the hepatocytes are arranged in the form of hepatic cords radiating from the CV to the border hepatic lobule, separating the hepatic cords by small blood sinusoids (S).

Histopathological examinations of the hepatic tissues of rats exposed to ACR indicated the presence of histopathological changes such as necrotic and hemorrhagic foci associated with pyknosis of the nuclei of hepatocytes compared to the control groups (Figure 5a and b).

Figure 5 (a and b) A cross-section of hepatic tissue from the ACR-treated group showing necrotic (✺) and hemorrhagic (⇒) foci associated with pyknosis of the nuclei of hepatocytes.
Figure 5

(a and b) A cross-section of hepatic tissue from the ACR-treated group showing necrotic (✺) and hemorrhagic (⇒) foci associated with pyknosis of the nuclei of hepatocytes.

Hepatic tissue of rats of the ACR-propolis group and the propolis group showed normal hepatic architecture with normal CV, hepatocytes, and absence of any pathological changes (Figure 6a and b).

Figure 6 Photomicrograph of (a) a cross-section of hepatic tissue from the (ACR + propolis)-treated group, (b) a cross-section of hepatic tissue from the propolis-treated group. The two sections show normal hepatic architecture with the normal CV, hepatocytes (H), and the absence of any pathological changes.
Figure 6

Photomicrograph of (a) a cross-section of hepatic tissue from the (ACR + propolis)-treated group, (b) a cross-section of hepatic tissue from the propolis-treated group. The two sections show normal hepatic architecture with the normal CV, hepatocytes (H), and the absence of any pathological changes.

3.2.3 Testicular alterations

Microscopic analysis of the testicular tissue from the control group revealed a normal testicular architecture with intact seminiferous tubules (ST) and normal interstitial tissue. The ST is lined with a stratified epithelium (SE) composed of spermatogenic cells, including spermatogonia, primary and secondary spermatocytes, spermatocytes, spermatids, and spermatozoa. The spermatogenic cells are associated with columnar supporting cells (Sertoli cells) and rest on a basement membrane (Figure 7a and b).

Figure 7 (a and b) A cross section of testicular tissue from the control group showing the ST and interstitial tissue and interstitial cells (IC), the ST lined with an SE composed of spermatogenic cells: spermatogonia, primary and secondary spermatocytes, spermatids, and spermatozoa in addition to columnar supporting cells (Sertoli cells). Note that the spermatogenic cells rest on a basement membrane (arrows).
Figure 7

(a and b) A cross section of testicular tissue from the control group showing the ST and interstitial tissue and interstitial cells (IC), the ST lined with an SE composed of spermatogenic cells: spermatogonia, primary and secondary spermatocytes, spermatids, and spermatozoa in addition to columnar supporting cells (Sertoli cells). Note that the spermatogenic cells rest on a basement membrane (arrows).

The histological results showed several histopathological alterations in the ACR group compared to the control group. Edema, protein material infiltration between tubules, and degenerative vacuolar alterations were among the observed abnormalities. The seminal tubule tissue had degenerative alterations, sperm cell variations, sloughing off, and desquamation of spermatogenic cells, in addition to deformation and tortuosity of the basement membrane (Figure 8a and b).

Figure 8 (a–d) A cross-section of the testicular tissue in the ACR-treated group showing edema and protein infiltration between the ST (☼) and sloughing off and desquamation of spermatogenic cells into the lumen of the ST (✺) with degenerative changes in the seminal tubule tissue (✸). Deformation and tortuosity of the basement membrane (arrows).
Figure 8

(a–d) A cross-section of the testicular tissue in the ACR-treated group showing edema and protein infiltration between the ST (☼) and sloughing off and desquamation of spermatogenic cells into the lumen of the ST (✺) with degenerative changes in the seminal tubule tissue (✸). Deformation and tortuosity of the basement membrane (arrows).

However, the propolis-treated group and the (ACR + propolis)-treated group exhibited healthy testicles. It showed healthy ST, interstitial tissue and cells, stratified epithelial tissue lining the ST made up of spermatogonia, primary and secondary spermatocytes, spermatids, and spermatozoa, and some hydropic degenerations as well as normal basement membrane (Figure 9a and b).

Figure 9 Photomicrographs of a testicular tissue cross section of male albino rat from (a and c) (ACR + propolis)-treated group, (b and d) the propolis-treated group. The two sections show normal testicular architecture with normal ST, normal interstitial tissue and IC, SE tissue lining the ST consisting of spermatogonia, primary and secondary spermatocytes, spermatids, and spermatozoa with some hydropic degenerations (*) and good basement membrane (arrows).
Figure 9

Photomicrographs of a testicular tissue cross section of male albino rat from (a and c) (ACR + propolis)-treated group, (b and d) the propolis-treated group. The two sections show normal testicular architecture with normal ST, normal interstitial tissue and IC, SE tissue lining the ST consisting of spermatogonia, primary and secondary spermatocytes, spermatids, and spermatozoa with some hydropic degenerations (*) and good basement membrane (arrows).

Although some minor changes remained in the (ACR + propolis)-treated group, the hepatic, renal, and testicular tissues were almost similar to the control group. The results of this study proved that supplementing propolis reduced the occurrence of these pathological effects and restored the tissues almost to a normal state.

4 Discussion

This experiment evaluated the effect of propolis orally by gavage, and the potential protective role in the rats’ hepatic, renal, and testicular tissues induced by propolis extract against ACR-induced toxicity.

The above results on the kidney section revealed that rats treated with ACR + propolis had a normal renal structure with PCT, and distal and blood vessels. This indicates that propolis positively reduced the harmful effects of ACR in kidney tissues. In contrast, there is an observed decrease in ALT and AST enzymes compared to samples treated with ACR only. Meanwhile, propolis prevented harmful effects on the main organ responsible for the biotransformation of various components and many toxic chemical substances [14,30]. The enzymes superoxide dismutase, catalase (CAT), and glutathione peroxidase (GSH-Px) activity convert superoxide radicals into hydrogen peroxide, and then water and molecular oxygen are the first lines of defense against oxidative stress. The redox state of the cells is altered when the activity of these enzymes is reduced. As a result, increasing the activity of these enzymes probably aids in the removal of ROS produced by pesticide exposure [13,31].

The current study revealed that ACR-treated affected hepatic alteration in rats; hydropic vacuolated degenerations in the cytoplasm and pycnotic nuclei were observed. Also, the CV and blood sinusoids were dilated and congested, and infiltration of inflammatory cells was also seen as a result of exposure to ACR. These ACR-induced alterations are consistent with the Rady and Osman’s [32] findings of hepatotoxicity following ingestion of an excess ACR-containing diet. In addition, the current research revealed congested CV and blood sinusoids could indicate metabolic abnormalities in the hepatic tissue, implying that ACR may have a toxic effect on the liver [33]. ACR may interact with cytochrome P450 to create glycidamide, resulting in glutathione depletion, an important antioxidant enzyme. As a result, oxidative damage interferes with cell function and may lead to cell death [33,34].

ACR-induced toxicity is driven by oxidative stress, oxygen generation, and apoptosis (Mehri et al., [35]). However, the cytoplasmic degeneration, necrosis, and metabolic enzyme activity defects are major ACR-hepatotoxic effects [36], in addition to the enlarged and congested CV and blood sinusoids, which were noticed by Hu et al. [37], Amin [33], and Hussein et al. [38].

In the present study, the testicular tissue of the rats treated with propolis showed healthy ST, interstitial tissue and cells, and SE tissue lining the ST made up of spermatogonia and primary and secondary spermatocytes. Most of the therapeutic properties of propolis are due to anti-inflammatory and antioxidant effects, which mitigate oxidative damage by scavenger-free radicals and are attributed to protecting normal histological structure in ACR + propolis-treated rats [13]. The beneficial properties of propolis have been linked to its high amount of flavonoids, phenolic acids, and terpenoids [14].

In the present study, the hepatic renal and testicular tissues of the (ACR + propolis)-treated group were almost similar to the control group, except that some minor changes remained. Propolis’ benefits may be due to its inhibitory effects on lipid peroxidation mechanisms, prevention of free radical formation, scavenging action on free radicals, and decreased levels of MDA [39]. CAPE is another active component of propolis, which is a practical component in reducing oxidative stress in the liver through reduced lipid peroxidation, as reported in several studies [14,16,30,40].

The biochemical parameters such as the total oxidative status and oxidative stress index were measured in hepatic tissue to examine if propolis might help reduce ACR-induced reno-hepatic and testicular damage. The results indicated an improvement in hepatic architecture in the (ACR + propolis)-treated group. Furthermore, the CVs and blood sinusoids are either normal or slightly dilated. Polygonal hepatocytes have vesicular nuclei and acidophilic cytoplasm in most cells. Some cytoplasmic degenerations are still present in some sections. In the present study, the increase in the presence of free radicals during oxidative stress caused damage to the membrane structure of hepatocytes, as indicated by the levels of AST, ALT, and TAC in serum and TBARS in tissues. These findings are consistent with ACR altering metabolic parameters in rats and causing DNA damage, inflammation, and oxidative stress in rat testes [38,41,42], besides the ACR’s negative effect on enzyme activity and lipid peroxidation [8,43].

5 Conclusions

Acrylamide has negative effects on animal and human health; however, propolis supplementation may reduce ACR’s adverse consequences and helps the liver, kidney, and testes return to their normal state. The effectiveness of propolis in reducing pathological changes caused by ACR may be due to the anti-inflammatory and antioxidant effects of propolis. Moreover, the blood biochemical findings in the present study confirmed the efficacy of propolis on ACR toxicity. Propolis can be used as a cytoprotective agent against ACR-induced toxicity. Further research is needed to determine the precise mechanism by which propolis protects against ACR toxicity.

Acknowledgments

The authors extend their appreciation to the Deanship of Scientific Research at King Khalid University, Abha, KSA, for funding this work through the research group project (G.R.P/23/43).

  1. Funding information: The deanship of scientific research, King Khalid University, Saudi Arabia, for the fund through the research group project (G.R.P/23/43).

  2. Author contributions: KMAS, AAA, and AEA: conceptualization, methodology, data curation, and writing the original draft. HEM, MA, and AAE: methodology, writing-review and editing, and critical reading. MEA and MFK: editing, critical reading, data curation, and formal analysis. All authors listed in this paper have contributed to the preparation and execution of this research. All authors have read and agreed to the published version of the manuscript.

  3. Conflict of interest: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

  4. Ethics statement: All experiments were reviewed and approved following the rules and regulations of the Research Ethics Committee, King Khalid University (Approval NO. ECM#2023-1206). All experiments were carried out in the Physiology Lab., Department of Biology, College of Science, and King Khalid University, Saudi Arabia. The authors confirm that the ethical policies of the journal, as noted on the journal's author guidelines page, have been adhered to.

  5. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2023-03-10
Revised: 2023-04-04
Accepted: 2023-04-05
Published Online: 2023-05-05

© 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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https://doi.org/10.1515/chem-2022-0321
Keywords for this article
acrylamide; propolis; antioxidant; toxicity; rat
Creative Commons
BY 4.0

Articles in the same Issue

  1. Characteristics, source, and health risk assessment of aerosol polyaromatic hydrocarbons in the rural and urban regions of western Saudi Arabia
  2. Regular Articles
  3. A network-based correlation research between element electronegativity and node importance
  4. Pomegranate attenuates kidney injury in cyclosporine-induced nephrotoxicity in rats by suppressing oxidative stress
  5. Ab initio study of fundamental properties of XInO3 (X = K, Rb, Cs) perovskites
  6. Responses of feldspathic sandstone and sand-reconstituted soil C and N to freeze–thaw cycles
  7. Robust fractional control based on high gain observers design (RNFC) for a Spirulina maxima culture interfaced with an advanced oxidation process
  8. Study on arsenic speciation and redistribution mechanism in Lonicera japonica plants via synchrotron techniques
  9. Optimization of machining Nilo 36 superalloy parameters in turning operation
  10. Vacuum impregnation pre-treatment: A novel method for incorporating mono- and divalent cations into potato strips to reduce the acrylamide formation in French fries
  11. Characterization of effective constituents in Acanthopanax senticosus fruit for blood deficiency syndrome based on the chinmedomics strategy
  12. Comparative analysis of the metabolites in Pinellia ternata from two producing regions using ultra-high-performance liquid chromatography–electrospray ionization–tandem mass spectrometry
  13. The assessment of environmental parameter along the desalination plants in the Kingdom of Saudi Arabia
  14. Effects of harpin and carbendazim on antioxidant accumulation in young jujube leaves
  15. The effects of in ovo injected with sodium borate on hatching performance and small intestine morphology in broiler chicks
  16. Optimization of cutting forces and surface roughness via ANOVA and grey relational analysis in machining of In718
  17. Essential oils of Origanum compactum Benth: Chemical characterization, in vitro, in silico, antioxidant, and antibacterial activities
  18. Translocation of tungsten(vi) oxide/gadolinium(iii) fluoride in tellurite glasses towards improvement of gamma-ray attenuation features in high-density glass shields
  19. Mechanical properties, elastic moduli, and gamma ray attenuation competencies of some TeO2–WO3–GdF3 glasses: Tailoring WO3–GdF3 substitution toward optimum behavioral state range
  20. Comparison between the CIDR or sponge with hormone injection to induce estrus synchronization for twining and sex preselection in Naimi sheep
  21. Exergetic performance analyses of three different cogeneration plants
  22. Psoralea corylifolia (babchi) seeds enhance proliferation of normal human cultured melanocytes: GC–MS profiling and biological investigation
  23. A novel electrochemical micro-titration method for quantitative evaluation of the DPPH free radical scavenging capacity of caffeic acid
  24. Comparative study between supported bimetallic catalysts for nitrate remediation in water
  25. Persicaline, an alkaloid from Salvadora persica, inhibits proliferation and induces apoptosis and cell-cycle arrest in MCF-7 cells
  26. Determination of nicotine content in locally produced smokeless tobacco (Shammah) samples from Jazan region of Saudi Arabia using a convenient HPLC-MS/MS method
  27. Changes in oxidative stress markers in pediatric burn injury over a 1-week period
  28. Integrated geophysical techniques applied for petroleum basins structural characterization in the central part of the Western Desert, Egypt
  29. The impact of chemical modifications on gamma-ray attenuation properties of some WO3-reinforced tellurite glasses
  30. Microwave and Cs+-assisted chemo selective reaction protocol for synthesizing 2-styryl quinoline biorelevant molecules
  31. Structural, physical, and radiation absorption properties of a significant nuclear power plant component: A comparison between REX-734 and 316L SS austenitic stainless steels
  32. Effect of Moringa oleifera on serum YKL-40 level: In vivo rat periodontitis model
  33. Investigating the impact of CO2 emissions on the COVID-19 pandemic by generalized linear mixed model approach with inverse Gaussian and gamma distributions
  34. Influence of WO3 content on gamma rays attenuation characteristics of phosphate glasses at low energy range
  35. Study on CO2 absorption performance of ternary DES formed based on DEA as promoting factor
  36. Performance analyses of detonation engine cogeneration cycles
  37. Sterols from Centaurea pumilio L. with cell proliferative activity: In vitro and in silico studies
  38. Untargeted metabolomics revealing changes in aroma substances in flue-cured tobacco
  39. Effect of pumpkin enriched with calcium lactate on iron status in an animal model of postmenopausal osteoporosis
  40. Energy consumption, mechanical and metallographic properties of cryogenically treated tool steels
  41. Optimization of ultra-high pressure-assisted extraction of total phenols from Eucommia ulmoides leaves by response surface methodology
  42. Harpin enhances antioxidant nutrient accumulation and decreases enzymatic browning in stored soybean sprouts
  43. Physicochemical and biological properties of carvacrol
  44. Radix puerariae in the treatment of diabetic nephropathy: A network pharmacology analysis and experimental validation
  45. Anti-Alzheimer, antioxidants, glucose-6-phosphate dehydrogenase effects of Taverniera glabra mediated ZnO and Fe2O3 nanoparticles in alloxan-induced diabetic rats
  46. Experimental study on photocatalytic CO2 reduction performance of ZnS/CdS-TiO2 nanotube array thin films
  47. Epoxy-reinforced heavy metal oxides for gamma ray shielding purposes
  48. Black mulberry (Morus nigra L.) fruits: As a medicinal plant rich in human health-promoting compounds
  49. Promising antioxidant and antimicrobial effects of essential oils extracted from fruits of Juniperus thurifera: In vitro and in silico investigations
  50. Chloramine-T-induced oxidation of Rizatriptan Benzoate: An integral chemical and spectroscopic study of products, mechanisms and kinetics
  51. Study on antioxidant and antimicrobial potential of chemically profiled essential oils extracted from Juniperus phoenicea (L.) by use of in vitro and in silico approaches
  52. Screening and characterization of fungal taxol-producing endophytic fungi for evaluation of antimicrobial and anticancer activities
  53. Mineral composition, principal polyphenolic components, and evaluation of the anti-inflammatory, analgesic, and antioxidant properties of Cytisus villosus Pourr leaf extracts
  54. In vitro antiproliferative efficacy of Annona muricata seed and fruit extracts on several cancer cell lines
  55. An experimental study for chemical characterization of artificial anterior cruciate ligament with coated chitosan as biomaterial
  56. Prevalence of residual risks of the transfusion-transmitted infections in Riyadh hospitals: A two-year retrospective study
  57. Computational and experimental investigation of antibacterial and antifungal properties of Nicotiana tabacum extracts
  58. Reinforcement of cementitious mortars with hemp fibers and shives
  59. X-ray shielding properties of bismuth-borate glass doped with rare earth ions
  60. Green supported silver nanoparticles over modified reduced graphene oxide: Investigation of its antioxidant and anti-ovarian cancer effects
  61. Orthogonal synthesis of a versatile building block for dual functionalization of targeting vectors
  62. Thymbra spicata leaf extract driven biogenic synthesis of Au/Fe3O4 nanocomposite and its bio-application in the treatment of different types of leukemia
  63. The role of Ag2O incorporation in nuclear radiation shielding behaviors of the Li2O–Pb3O4–SiO2 glass system: A multi-step characterization study
  64. A stimuli-responsive in situ spray hydrogel co-loaded with naringenin and gentamicin for chronic wounds
  65. Assessment of the impact of γ-irradiation on the piperine content and microbial quality of black pepper
  66. Antioxidant, sensory, and functional properties of low-alcoholic IPA beer with Pinus sylvestris L. shoots addition fermented using unconventional yeast
  67. Screening and optimization of extracellular pectinase produced by Bacillus thuringiensis SH7
  68. Determination of polyphenols in Chinese jujube using ultra-performance liquid chromatography–mass spectrometry
  69. Synergistic effects of harpin and NaCl in determining soybean sprout quality under non-sterile conditions
  70. Field evaluation of different eco-friendly alternative control methods against Panonychus citri [Acari: Tetranychidae] spider mite and its predators in citrus orchards
  71. Exploring the antimicrobial potential of biologically synthesized zero valent iron nanoparticles
  72. NaCl regulates goldfish growth and survival at three food supply levels under hypoxia
  73. An exploration of the physical, optical, mechanical, and radiation shielding properties of PbO–MgO–ZnO–B2O3 glasses
  74. A novel statistical modeling of air pollution and the COVID-19 pandemic mortality data by Poisson, geometric, and negative binomial regression models with fixed and random effects
  75. Treatment activity of the injectable hydrogels loaded with dexamethasone In(iii) complex on glioma by inhibiting the VEGF signaling pathway
  76. An alternative approach for the excess lifetime cancer risk and prediction of radiological parameters
  77. Panax ginseng leaf aqueous extract mediated green synthesis of AgNPs under ultrasound condition and investigation of its anti-lung adenocarcinoma effects
  78. Study of hydrolysis and production of instant ginger (Zingiber officinale) tea
  79. Novel green synthesis of zinc oxide nanoparticles using Salvia rosmarinus extract for treatment of human lung cancer
  80. Evaluation of second trimester plasma lipoxin A4, VEGFR-1, IL-6, and TNF-α levels in pregnant women with gestational diabetes mellitus
  81. Antidiabetic, antioxidant and cytotoxicity activities of ortho- and para-substituted Schiff bases derived from metformin hydrochloride: Validation by molecular docking and in silico ADME studies
  82. Antioxidant, antidiabetic, antiglaucoma, and anticholinergic effects of Tayfi grape (Vitis vinifera): A phytochemical screening by LC-MS/MS analysis
  83. Identification of genetic polymorphisms in the stearoyl CoA desaturase gene and its association with milk quality traits in Najdi sheep
  84. Cold-acclimation effect on cadmium absorption and biosynthesis of polyphenolics, and free proline and photosynthetic pigments in Spirogyra aequinoctialis
  85. Analysis of secondary metabolites in Xinjiang Morus nigra leaves using different extraction methods with UPLC-Q/TOF-MS/MS technology
  86. Nanoarchitectonics and performance evaluation of a Fe3O4-stabilized Pickering emulsion-type differential pressure plugging agent
  87. Investigating pyrolysis characteristics of Shengdong coal through Py-GC/MS
  88. Extraction, phytochemical characterization, and antifungal activity of Salvia rosmarinus extract
  89. Introducing a novel and natural antibiotic for the treatment of oral pathogens: Abelmoschus esculentus green-formulated silver nanoparticles
  90. Optimization of gallic acid-enriched ultrasonic-assisted extraction from mango peels
  91. Effect of gamma rays irradiation in the structure, optical, and electrical properties of samarium doped bismuth titanate ceramics
  92. Combinatory in silico investigation for potential inhibitors from Curcuma sahuynhensis Škorničk. & N.S. Lý volatile phytoconstituents against influenza A hemagglutinin, SARS-CoV-2 main protease, and Omicron-variant spike protein
  93. Physical, mechanical, and gamma ray shielding properties of the Bi2O3–BaO–B2O3–ZnO–As2O3–MgO–Na2O glass system
  94. Twofold interpenetrated 3D Cd(ii) complex: Crystal structure and luminescent property
  95. Study on the microstructure and soil quality variation of composite soil with soft rock and sand
  96. Ancient spring waters still emerging and accessible in the Roman Forum area: Chemical–physical and microbiological characterization
  97. Extraction and characterization of type I collagen from scales of Mexican Biajaiba fish
  98. Finding small molecular compounds to decrease trimethylamine oxide levels in atherosclerosis by virtual screening
  99. Prefatory in silico studies and in vitro insecticidal effect of Nigella sativa (L.) essential oil and its active compound (carvacrol) against the Callosobruchus maculatus adults (Fab), a major pest of chickpea
  100. Polymerized methyl imidazole silver bromide (CH3C6H5AgBr)6: Synthesis, crystal structures, and catalytic activity
  101. Using calcined waste fish bones as a green solid catalyst for biodiesel production from date seed oil
  102. Influence of the addition of WO3 on TeO2–Na2O glass systems in view of the feature of mechanical, optical, and photon attenuation
  103. Naringin ameliorates 5-fluorouracil elicited neurotoxicity by curtailing oxidative stress and iNOS/NF-ĸB/caspase-3 pathway
  104. GC-MS profile of extracts of an endophytic fungus Alternaria and evaluation of its anticancer and antibacterial potentialities
  105. Green synthesis, chemical characterization, and antioxidant and anti-colorectal cancer effects of vanadium nanoparticles
  106. Determination of caffeine content in coffee drinks prepared in some coffee shops in the local market in Jeddah City, Saudi Arabia
  107. A new 3D supramolecular Cu(ii) framework: Crystal structure and photocatalytic characteristics
  108. Bordeaux mixture accelerates ripening, delays senescence, and promotes metabolite accumulation in jujube fruit
  109. Important application value of injectable hydrogels loaded with omeprazole Schiff base complex in the treatment of pancreatitis
  110. Color tunable benzothiadiazole-based small molecules for lightening applications
  111. Investigation of structural, dielectric, impedance, and mechanical properties of hydroxyapatite-modified barium titanate composites for biomedical applications
  112. Metal gel particles loaded with epidermal cell growth factor promote skin wound repair mechanism by regulating miRNA
  113. In vitro exploration of Hypsizygus ulmarius (Bull.) mushroom fruiting bodies: Potential antidiabetic and anti-inflammatory agent
  114. Alteration in the molecular structure of the adenine base exposed to gamma irradiation: An ESR study
  115. Comprehensive study of optical, thermal, and gamma-ray shielding properties of Bi2O3–ZnO–PbO–B2O3 glasses
  116. Lewis acids as co-catalysts in Pd-based catalyzed systems of the octene-1 hydroethoxycarbonylation reaction
  117. Synthesis, Hirshfeld surface analysis, thermal, and selective α-glucosidase inhibitory studies of Schiff base transition metal complexes
  118. Protective properties of AgNPs green-synthesized by Abelmoschus esculentus on retinal damage on the virtue of its anti-inflammatory and antioxidant effects in diabetic rat
  119. Effects of green decorated AgNPs on lignin-modified magnetic nanoparticles mediated by Cydonia on cecal ligation and puncture-induced sepsis
  120. Treatment of gastric cancer by green mediated silver nanoparticles using Pistacia atlantica bark aqueous extract
  121. Preparation of newly developed porcelain ceramics containing WO3 nanoparticles for radiation shielding applications
  122. Utilization of computational methods for the identification of new natural inhibitors of human neutrophil elastase in inflammation therapy
  123. Some anticancer agents as effective glutathione S-transferase (GST) inhibitors
  124. Clay-based bricks’ rich illite mineral for gamma-ray shielding applications: An experimental evaluation of the effect of pressure rates on gamma-ray attenuation parameters
  125. Stability kinetics of orevactaene pigments produced by Epicoccum nigrum in solid-state fermentation
  126. Treatment of denture stomatitis using iron nanoparticles green-synthesized by Silybum marianum extract
  127. Characterization and antioxidant potential of white mustard (Brassica hirta) leaf extract and stabilization of sunflower oil
  128. Characteristics of Langmuir monomolecular monolayers formed by the novel oil blends
  129. Strategies for optimizing the single GdSrFeO4 phase synthesis
  130. Oleic acid and linoleic acid nanosomes boost immunity and provoke cell death via the upregulation of beta-defensin-4 at genetic and epigenetic levels
  131. Unraveling the therapeutic potential of Bombax ceiba roots: A comprehensive study of chemical composition, heavy metal content, antibacterial activity, and in silico analysis
  132. Green synthesis of AgNPs using plant extract and investigation of its anti-human colorectal cancer application
  133. The adsorption of naproxen on adsorbents obtained from pepper stalk extract by green synthesis
  134. Treatment of gastric cancer by silver nanoparticles encapsulated by chitosan polymers mediated by Pistacia atlantica extract under ultrasound condition
  135. In vitro protective and anti-inflammatory effects of Capparis spinosa and its flavonoids profile
  136. Wear and corrosion behavior of TiC and WC coatings deposited on high-speed steels by electro-spark deposition
  137. Therapeutic effects of green-formulated gold nanoparticles by Origanum majorana on spinal cord injury in rats
  138. Melanin antibacterial activity of two new strains, SN1 and SN2, of Exophiala phaeomuriformis against five human pathogens
  139. Evaluation of the analgesic and anesthetic properties of silver nanoparticles supported over biodegradable acacia gum-modified magnetic nanoparticles
  140. Review Articles
  141. Role and mechanism of fruit waste polyphenols in diabetes management
  142. A comprehensive review of non-alkaloidal metabolites from the subfamily Amaryllidoideae (Amaryllidaceae)
  143. Discovery of the chemical constituents, structural characteristics, and pharmacological functions of Chinese caterpillar fungus
  144. Eco-friendly green approach of nickel oxide nanoparticles for biomedical applications
  145. Advances in the pharmaceutical research of curcumin for oral administration
  146. Rapid Communication
  147. Determination of the contents of bioactive compounds in St. John’s wort (Hypericum perforatum): Comparison of commercial and wild samples
  148. Retraction
  149. Retraction of “Two mixed-ligand coordination polymers based on 2,5-thiophenedicarboxylic acid and flexible N-donor ligands: The protective effect on periodontitis via reducing the release of IL-1β and TNF-α”
  150. Topical Issue on Phytochemicals, biological and toxicological analysis of aromatic medicinal plants
  151. Anti-plasmodial potential of selected medicinal plants and a compound Atropine isolated from Eucalyptus obliqua
  152. Anthocyanin extract from black rice attenuates chronic inflammation in DSS-induced colitis mouse model by modulating the gut microbiota
  153. Evaluation of antibiofilm and cytotoxicity effect of Rumex vesicarius methanol extract
  154. Chemical compositions of Litsea umbellata and inhibition activities
  155. Green synthesis, characterization of silver nanoparticles using Rhynchosia capitata leaf extract and their biological activities
  156. GC-MS analysis and antibacterial activities of some plants belonging to the genus Euphorbia on selected bacterial isolates
  157. The abrogative effect of propolis on acrylamide-induced toxicity in male albino rats: Histological study
  158. A phytoconstituent 6-aminoflavone ameliorates lipopolysaccharide-induced oxidative stress mediated synapse and memory dysfunction via p-Akt/NF-kB pathway in albino mice
  159. Anti-diabetic potentials of Sorbaria tomentosa Lindl. Rehder: Phytochemistry (GC-MS analysis), α-amylase, α-glucosidase inhibitory, in vivo hypoglycemic, and biochemical analysis
  160. Assessment of cytotoxic and apoptotic activities of the Cassia angustifolia aqueous extract against SW480 colon cancer
  161. Biochemical analysis, antioxidant, and antibacterial efficacy of the bee propolis extract (Hymenoptera: Apis mellifera) against Staphylococcus aureus-induced infection in BALB/c mice: In vitro and in vivo study
  162. Assessment of essential elements and heavy metals in Saudi Arabian rice samples underwent various processing methods
  163. Two new compounds from leaves of Capparis dongvanensis (Sy, B. H. Quang & D. V. Hai) and inhibition activities
  164. Hydroxyquinoline sulfanilamide ameliorates STZ-induced hyperglycemia-mediated amyleoid beta burden and memory impairment in adult mice
  165. An automated reading of semi-quantitative hemagglutination results in microplates: Micro-assay for plant lectins
  166. Inductively coupled plasma mass spectrometry assessment of essential and toxic trace elements in traditional spices consumed by the population of the Middle Eastern region in their recipes
  167. Phytochemical analysis and anticancer activity of the Pithecellobium dulce seed extract in colorectal cancer cells
  168. Impact of climatic disturbances on the chemical compositions and metabolites of Salvia officinalis
  169. Physicochemical characterization, antioxidant and antifungal activities of essential oils of Urginea maritima and Allium sativum
  170. Phytochemical analysis and antifungal efficiency of Origanum majorana extracts against some phytopathogenic fungi causing tomato damping-off diseases
  171. Special Issue on 4th IC3PE
  172. Graphene quantum dots: A comprehensive overview
  173. Studies on the intercalation of calcium–aluminium layered double hydroxide-MCPA and its controlled release mechanism as a potential green herbicide
  174. Synergetic effect of adsorption and photocatalysis by zinc ferrite-anchored graphitic carbon nitride nanosheet for the removal of ciprofloxacin under visible light irradiation
  175. Exploring anticancer activity of the Indonesian guava leaf (Psidium guajava L.) fraction on various human cancer cell lines in an in vitro cell-based approach
  176. The comparison of gold extraction methods from the rock using thiourea and thiosulfate
  177. Special Issue on Marine environmental sciences and significance of the multidisciplinary approaches
  178. Sorption of alkylphenols and estrogens on microplastics in marine conditions
  179. Cytotoxic ketosteroids from the Red Sea soft coral Dendronephthya sp.
  180. Antibacterial and biofilm prevention metabolites from Acanthophora spicifera
  181. Characteristics, source, and health risk assessment of aerosol polyaromatic hydrocarbons in the rural and urban regions of western Saudi Arabia
  182. Special Issue on Advanced Nanomaterials for Energy, Environmental and Biological Applications - Part II
  183. Green synthesis, characterization, and evaluation of antibacterial activities of cobalt nanoparticles produced by marine fungal species Periconia prolifica
  184. Combustion-mediated sol–gel preparation of cobalt-doped ZnO nanohybrids for the degradation of acid red and antibacterial performance
  185. Perinatal supplementation with selenium nanoparticles modified with ascorbic acid improves hepatotoxicity in rat gestational diabetes
  186. Evaluation and chemical characterization of bioactive secondary metabolites from endophytic fungi associated with the ethnomedicinal plant Bergenia ciliata
  187. Enhancing photovoltaic efficiency with SQI-Br and SQI-I sensitizers: A comparative analysis
  188. Nanostructured p-PbS/p-CuO sulfide/oxide bilayer heterojunction as a promising photoelectrode for hydrogen gas generation
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