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. 2024 Mar 23;13(2):tfae047. doi: 10.1093/toxres/tfae047

Impact of Saussurea lappa against foodborne parasite Trichinella spiralis experimental infections induced variation in DNA damage, oxidative stress and PCNA expression in rat skeletal muscles

Areej Jameel M Alghabban 1, Lamiaa Bakr 2, Aya A Elbatawy 3, Afaf El Atrash 4, Ehab Tousson 5,✉
PMCID: PMC10960925  PMID: 38529200

Abstract

Trichinellosis is a parasite zoonosis that is spread through ingesting raw or undercooked meat that contains the Trichinella spiralis (T. spiralis) infective larvae. It has three clinical phases: intestinal, migratory, and muscular. Kuth root, also known as Costus (Saussurea lappa) roots, is used in many traditional medical systems all over the world to treat a variety of illnesses, such as dyspepsia, diarrhoea, vomiting, and inflammation. Current study assessed the therapeutic Potential of costus roots extract (CRE) treatment on experimental trichinellosis induce changes in DNA damage, oxidative stress and Proliferating cell nuclear antigen (PCNA) expression in muscle fibers in male rats. A total of 60 male Sprague Dawley rats were divided into 6 groups (Gps) [Gp1, Negative control; Gp2, Costus (CRE); Gp3, Positive control or Infected rats with T. spiralis, Gp4; Pre-treated infection with CRE; Gp5 & Gp6, Post treated infection with CRE for one and two weeks respectively]. Current results revealed that; Trichinella spiralis experimentally infection induced significant elevation in tissue malondialdehyde (MDA), DNA damage, PCNA expression and significant depletion in tissue glutathione (GSH), superoxide dismutase (SOD) and catalase (Cat) activities. Pre or/and post CRE treated infected rats with T. spiralis (Gp4-Gp6) induced improvements and depletion in DNA damage, PCNA expression, MDA and elevation in GSH, SOD, catalase as compared to infected rats with T. spiralis (Gp3) with best results for the pretreatments (Gp4). Trichinella spiralis experimental infection induced DNA damage and oxidative stress in rat skeletal muscles and treatments with costus roots extract modulates these changes.

Keywords: Trichinella spiralis, Costus, Skeletal muscles, Oxidative stress, DNA damage

Introduction

Trichinella nematodes are among the most pervasive zoonotic infections in the globe.1 Trichinellosis is a risk to public health; according to Nada et al.,2 it affects up to 11 million individuals worldwide and results in 10,000 cases per year. Trichinosis can be lethal depending on the infection’s severity; death can happen 4–6 weeks after the infection and is typically brought on by myocarditis, encephalitis, or pneumonia.3 Mebendazole and albendazole are anthelmintic medications that are used to treat trichinellosis in the gut as well as encysted larvae in the skeletal and cardiac muscles.4,5T. spiralis infection has the power to control the human immune system by modulating.

A variety of chemical components that are produced by medicinal plants can be used to treat a wide range of ailments.6,7 In contrast to modern drug therapy, herbal medicines are composed of a vast variety of active compounds that are created by mixing fundamental medicinal elements, each of which has distinct pharmacological effects.8 Costus (Saussurea lappa) roots is one of these herbal plants, that belongs to the family Asteraceae which is commonly known as Sunflower family. Saussurea lappa is a crucial plant for medicine. Sesquiterpene lactones like costunolide, costunolide, Cynaropicrin, chlorogenic acid and dehydrocostus lactone are among the many active plant chemicals that have been identified and shown to have medical benefits.9–12 The bioactivities of Synapta lappa include those that are antifungal, antidiabetic, anthelmintic, anticancer, antiulcer, and antimicrobial. Immunostimulation, antihepatotoxic, and anti-histopathological.13,14 It was discovered that Costus roots was active against Trypanosoma cruzi, Clonorchis sinensis, and several nematodal diseases.

According to Preedy and Watson,15 oxidative stress results from an imbalance between a biological system’s ability to quickly detoxify reactive intermediates or repair the damage they have produced and the systemic manifestation of reactive oxygen species. Disruptions in the normal redox state of cells can be damaging because they generate peroxides and free radicals that destroy all components of the cell, including proteins, lipids, and DNA. Oxidative stress caused by oxidative metabolism leads to base damage and DNA strand breaks. Therefore this study evaluated the impact of costus roots extract (CRE) on experimental trichinellosis induce DNA damage, and oxidative stress in skeletal muscle fibers in male rats.

Materials and methods

We obtained Costus (Saussurea lappa) roots extracts from a local clinical plant market in Egypt. The dry roots were then crushed into a fine powder, and CRE were assayed by Abd Eldaim et al13.

Animals and ethical considerations

60 male albino rats (Rattus norvigicus) were used in this investigation; they were purchasable from NRC in Giza, Egypt, and appeared to be in good health and parasite-free. The Institutional Ethical Committee for Animal Care and Use (IACUC-SCI-TU-0222) approved the study’s design. Prior to the experiment, rats were kept at our Faculty’s animal house for a week. They were kept in regular settings with a standard mouse food, unlimited access to water, a temperature of 23 2 °C, a relative humidity of 40%, and a controlled lighting cycle of 12 h of light and 12 h of darkness.

Experimental design and animal groups (Gps)

Gp 1: Control (−ve), in which normal healthy non-infected animal.

Gp 2: Costus (CRE) in which rats received CRE (300 mg/Kg body weight/ day) for one week.

Gp 3: Control Infected group (+ve), in which rats were challenged with 1,000 larvae of trichinella spiralis.

Gp 4: Pre-treated group in which rats treated with CRE (300 mg/Kg body weight/ day) for two weeks then challenged with 1,000 larvae of trichinella spiralis muscle larvae (ML).

Gp 5: Post treated group in which rats were challenged with 1,000 larvae of trichinella spiralis muscle larvae (ML) then treated with CRE (300 mg/Kg body weight/ day) for 1-week post infection.

Gp 6: Post treated group in which rats were challenged with 1,000 larvae of trichinella spiralis muscle larvae (ML) then treated with CRE (300 mg/Kg body weight/ day) for another 2 weeks post infection.

Sample collection

At the conclusion of the trial, rats that have been fasting overnight will be anaesthetized with diethyl ether, have their skeletal muscles dissected for five weeks, and have their blood obtained by heart puncture and centrifuged at 3,000 g for 20 min. The plasma will be meticulously separated and maintained at - 20 0C.

Isolation and infection of Trichinella spiralis muscle larvae (ML)

T. spiralis muscle larvae were obtained from laboratory bred infected rats in parasitology unit, Zoology Department Faculty of Science, Tanta University. Larval preparation and extraction of inoculums were made after Dunn and Wright.16 Five weeks after infection,1% pepsin and 1% concentrated HCL are added to warm tap water to create an artificial gastric juice that is used to digest the muscles of infected rats. The mixture was incubated for 2 h at 37 °C while being continuously stirred by an electric stirrer. The digest was then filtered by sieve (50 mesh/cm2), then by sieve (200 mesh/cm2). After being collected, the larvae were rinsed in tap water two to three times before being suspended in a conical flask for 30 min to allow for sedimentation. Sediment larvae were counted microscopically while using a hemocytometer, and the supernatant fluid was discarded. Dead larvae were non-mobile and comma-shaped, whereas living larvae were coiled and motile. Each rat received the proper dose, which is 0.25 mL of fluid containing 1,000 living larvae, after the concentration of the counted larvae in the fluid was adjusted. Rats were given 0.25 mL of the infection orally after being deprived for 12 h prior to infection.

Tissue preparation

Ice-cold In a homogenizer of the Potter-Elvehjem type, skeletal muscle tissues were homogenised using 1.15% potassium chloride and 0.01 mol/L sodium potassium phosphate buffer with pH 7.4, resulting in 10% w/v homogenization. The homogenate was centrifuged for 20 min at 4 degrees Celsius and 10,000 g to obtain the supernatant, which was then used for enzyme tests.

Estimations of oxidative and antioxidants parameters in homogenate

According to Aldubayan et al.17 and Beutler18 malondialdehyde (MDA) and glutathione (GSH) activities in tissue homogenate were estimated respectively. Superoxide dismutase (SOD) and catalase (Cat) activities were estimated according to Misra and Fridovich19 and Saggu et al.20 methods respectively.

Estimations of DNA damage in skeletal muscles via comet assay

According to Abd Eldaim et al.,13 DNA damage in various Gps was evaluated using the comet assay (single-cell gel electrophoresis). Comet assay (also called, single cell gel electrophoresis, SCGE) was used to detect any prospective damage for DNA after various treatments. It detects DNA strand breaks and alkali labile sites by measuring the migration of DNA from immobilized nuclear DNA. 13 Advantages of the comet assay for assessing DNA damage includes: (1) damage to the DNA in individual cells is measured; (2) only small number of cells are needed to carry out the assay (<10,000); (3) the assay can be performed on virtually any eukaryotic cell type; (4) and it is faster and more sensitive than the alkaline elution method for detecting DNA damage.

Proliferating cell nuclear antigen (PCNA) expressions

According to the procedure outlined by Tousson et al.,21 The distribution of PCNA receptor subunits were examined in deparaffinized sections (5 μm) using an Avidin-Biotin-Peroxidase (ABC) immunohistochemical method (Elite–ABC, Vector Laboratories, CA, USA) with PCNA monoclonal antibody (dilution 1:100; DAKO Japan Co, Tokyo, Japan).

Statistical analysis

Results were analysed using an adapted SPSS programme. Data are presented as mean ± standard error of mean (SEM). A one-way ANOVA followed by Dunnett’s test was used to analyse the differences between groups. Unpaired T-test was used to assess the level of statistical significance between the groups, with the threshold set at P < 0.01.

Results

The activity of CRE on the number of larvae in the skeletal muscles of infected rats

According to Table 1 and Fig. 1 both treatment groups saw a substantial (p 0.001) decrease in the mean larvae count when compared to the control infected group (+ve). The pre-treated group showed the greatest drop in larval count. In comparison to the control infected group, the recovery of T. spiralis muscle larvae continued to occur during the third week after infection and continued through the completion of the experiment. In comparison to the control infected group, the CRE-treated group for 2 weeks exhibits a non-significant drop in T. spiralis ML in the skeletal muscles in week 2, but a substantial reduction starting from the third week until the completion of the trial. When compared to the control infected group, the CRE-treated group for 1 week following T. spiralis infection exhibits a non-significant reduction in T. spiralis ML in tongue up to week 3, but a substantial drop in the 4th and 5th weeks.

Table 1.

Number of larvae in the skeletal muscles in control and treated groups.

Group W1 W2 W3 W4 W5
G1 (+Ve Control) 0 14.7 ± 2.5 44.3 ± 2.5 76.0 ± 9.9 55.0 ± 4.6
G2 (pretreatments) 0 0 2.7 ± 1.2 6.7 ± 0.6 75.0 ± 2.0
G3 (Post treatments/1 week) 0 15.7 ± 2.1 41.0 ± 5.6 127.7 ± 5.1 129.7 ± 11.5
G4 (Post treatments/2 week) 0 14.3 ± 2.7 17.0 ± 3.4 6.7 ± 3.1 26.3 ± 7.5
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Fig. 1.

Fig. 1

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Diminished of larvae number in the skeletal muscles of infected rats elicited by CRE administration. *: Significant difference from the control group at P < 0.001, #: Significant difference from the positive control (Trichinella spiralis infection) group at P < 0.001.

Oxidative stress and antioxidant parameters

Figure 2 revealed that; in skeletal muscles presented a significant increase in TBARS levels and significantly decreased levels of catalase, GSH and SOD in the untreated T.spiralis group compared to the control, treated groups. In contrast, treatment of rats with costus in pretreated, post 1 week and post 2 weeks groups showed significant improvement in TBARS, GSH, CAT and SOD levels with best results for pre-treatment then post treatments for 2 weeks followed by post treatments for 1 week.

Fig. 2.

Fig. 2

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Changes in serum TBARS, GSH, CAT and SOD levels in different groups in skeletal muscles under study. *: Significant difference from the control group at P < 0.001, #: Significant difference from the positive control (Trichinella spiralis infection) group at P < 0.001.

DNA damage

Table 2 and Fig. 3 revealed the DNA damage in skeletal muscles in infected rats with 1,000 larvae of Trichinella spiralis (G3) and also after pre- and post-treatments by SLRE. Skeletal muscles in +ve control group exhibited a significant elevation in DNA damage (P < 0.01) that was indicated by an increase in tails (length, DNA% and moment) as compared to the control (G1) and CRE (G2) Gps. Pre-treated (G4) and post-treated for one or two weeks (G5 and G6) significantly reduced this elevated DNA damage, with best results in pre-treated (G4) group.

Table 2.

Parameters for the comet assay determined through image analysis in cells from all Gps.

Group Tailed % Untailed % Tails length (μm) Tail DNA% Tail moment
control 3 97 2.25# ± 0.17 1.85 3.80
treated 2.5 97.5 1.98# ± 0.14 1.69 3.12
+ve control 16 84 7.09* ± 0.38 3.79 18.47
Pre-treated 4.5 95.5 3.15# ± 0.26 2.21 8.04
Post 1 week 7 93 5.66* ± 0.33 2.88 13.10
Post 2 week 5.5 94.5 3.25# ± 0.24 2.50 8.54
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Significant deviations from the control group are indicated by the following symbols: *(p 0.01), #(p 0.01), and **(p 0.01).

Fig. 3.

Fig. 3

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Photomicrographs representation of DNA damage (arrows) in skeletal muscles using comet assay.

Deviations of PCNA expression in muscle fibres

Fig. 4 shows the expression of PCNA in the muscle sections of all groups. Muscle fibers in control and CRE showed negative reactions for PCNA expressions (Fig. 4A and B), while, muscle fibers of infected rats with T. spiralis showed strong positive reaction for PCNA in encysted larvae and intact muscles (Fig. 4C). On the other hand; moderate to strong positive reactions for PCNA were detected in muscle fibers of pre-treated infected rats with CRE (G4; Fig. 4 3D). In contrast; moderate positive reactions for PCNA were observed in muscle fibers in post treated infected rats with CRE for one and two weeks (G5&G6; Figs. 4E and F).

Fig. 4.

Fig. 4

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Photomicrographs of muscle section stained with PCNA in experimental Gps. A&B: Negative reaction in skeletal muscle fibers in control and CRE. C: Strong positive reaction in skeletal muscle fibers of infected rats with T. Spiralis in intact muscles. D&E: Moderate to moderate positive reactions for PCNA in skeletal muscle of pre-treated or post treated infected rats with CRE for one week. F: Moderate positive reactions for PCNA in skeletal muscle in post treated infected rats with CRE for two weeks.

Discussion

The spread of T. spiralis muscle larvae, DNA damage, and modifications in antioxidant systems were all positively linked in the current study. Experimental trichinellosis has been demonstrated to alter the activity of certain antioxidant enzymes, including SOD, CAT, and GST, in the host’s blood and muscle tissues.22,23 In the tissues from the T. spiralis group, significantly higher amounts of TBARS were found coupled with lower levels of catalase, SOD, and GSH. According to a prior study by Derda et al.,23 this is accurate. An increased rate of GSH oxidation and consumption during the elimination of hydrogen peroxide may be the cause of the lower GSH levels in the rats that had T. spiralis larvae. By increasing the levels of catalase, SOD, and GSH and depletion TBARS level, the current study showed that; CRE was effective in modulating antioxidant enzyme activities, suggesting that CRE had free-radical scavenging properties. The end result of the oxidation process between reactive ROS and lipids, malondialdehyde, can reflect the level of oxidative damage to cells from the side.24 Antioxidant enzymes including SOG, catalase, and GST are primarily responsible for scavenging ROS in living things. Consequently, a change in antioxidant enzyme activity is also linked to some oxidative damage.25,26 Our findings are consistent with those of Anyanwu et al.27 and Ezejiofor and Orisakwe,28 who demonstrated that CRE exhibits significant antioxidant activity, which has been linked to the presence of physiologically active substances like flavonoids.

It is well known that; DNA damage depends on time and that it can build up over time. DNA damage is also influenced by the amount of parasitic proteins present; this damage has been seen in vitro when donor blood cells and helminth protein somatic products are co-cultured.29 DNA damage in the nematode worm’s germline can cause the spatially distinct reactions of apoptosis and cell cycle halt. This latter process is closely regulated and genetically identical to developmental programmed cell death. ROS will harm organisms’ DNA and oxidative processes when they are under stress and accumulate in significant amounts.30

The potential for DNA-damaging chemicals was reflected in the variability of DNA distribution correlating to single-stranded breaks or double-stranded breaks.31 However, the use of the “Comet assay” technique in skeletal muscles was essentially beneficial to identify DNA division during mitotic division. Both Kumar et al.32 and Attia et al.33 have previously discussed the usefulness of the comet assay to determine the extent of DNA damage in exposed worms. The results of the current investigation showed that, in comparison to the normal control and costus groups, there was a substantial increase in DNA damage (P 0.05) as shown by an increase in tail length, tail DNA percentage, and tail moment. This outcome concurs with Taha et al.34 Our results agree with Kucukkurt et al.35 for reported that; Babesia ovis induced oxidative stress and DNA damage in Anatolian black goats. Infected rats treated with Costus, however, saw considerably less increased DNA damage. Current results agree with Tousson et al.10,36 who reported that; a significant decrease in liver and kidney DNA damage after intoxication of ethephon. These findings imply that the increased levels of free radicals produced as a result of T. spiralis infection not only support host-defense mechanisms used by organisms to kill the parasite but too induced oxidative damage in another cells.

Conclusion

Trichinella spiralis experimental infection induced DNA damage and oxidative stress in rat skeletal muscles were it elevate malondialdehyde (MDA), DNA damage, PCNA expression and deplete tissue glutathione (GSH), superoxide dismutase (SOD) and catalase (Cat) activities. Pre or/and post treatment of T. spiralis with costus roots extract induced depletion in DNA damage, PCNA expression, MDA and elevation in GSH, SOD, catalase with best results for the pretreatments. Costus roots extract may be a promising therapy for treating T. spiralis due to the synergistic effect of this antioxidant.

Contributor Information

Areej Jameel M Alghabban, Biology Department, Faculty of science, University of Tabuk, KSA.

Lamiaa Bakr, Zoology Department, Faculty of Science, Tanta University, Tanta, Egypt.

Aya A Elbatawy, Zoology Department, Faculty of Science, Tanta University, Tanta, Egypt.

Afaf El Atrash, Zoology Department, Faculty of Science, Tanta University, Tanta, Egypt.

Ehab Tousson, Zoology Department, Faculty of Science, Tanta University, Tanta, Egypt.

Author contributions

Ehab Tousson and Lamiaa Bakr proposed the idea and the experimental design, analyzed the data, authored or reviewed drafts of the paper, approved the final draft, and supervised the work. Aya A. Elbatawy performed the experiments, contributed reagents/materials/analysis tools, and wrote the original manuscript. Areej Jameel M. Alghabban and Afaf El Atrash analyzed the data, contributed reagents/materials/analysis tools, and collected data. Ehab Tousson performed the immunohistochemical investigations, reviewed drafts of the paper and, approved the final draft.

Funding

No fund.

 

Conflict of interest statement: The authors declare no competing interests.

Data availability

All the data and material were available. The data of this article are included within the article and its additional files.

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Data Availability Statement

All the data and material were available. The data of this article are included within the article and its additional files.

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