Asian Journal of Dairy and Food Research

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Dual Protective Effects of Taraxacum officinale Ethanolic Extract against Cephalosporin-induced Anemia and HCl/Ethanol-induced Gastric Ulcer in Wistar Rats

Mahjouba Lakehal1, Abdelmalek Chaalel1,*, Mokhtaria Yasmina Boufadi2, Nawal Boukezzoula1, Djilali Benabdelmoumene3, Choukri Tefiani4
  • https://orcid.org/ 0009-0002-0976-718X, https://orcid.org/0000-0002-9334-4288, https://orcid.org/0000-0003-2087-4058, https://orcid.org/0000-0002-9334-4288, https://orcid.org/0000-0002-4857-9467, https://orcid.org/0000-0002-5932-4654
1Laboratory of Beneficial Microorganisms, Functional Foods and Health, Faculty of Natural Sciences and Life, Abdelhamid Ibn Badis, University of Mostaganem, BP 188, Mostaganem-27000, Algeria.
2Laboratory of Bioeconomy, Food Safety and Health, Faculty of Natural Sciences and Life, University of Abdelhamid Ibn Badis-27000 Mostaganem, Algeria.
3Laboratory of Applied Animal Physiology, Abdelhamid Ibn Badis, University of Mostaganem, BP 188, Mostaganem-27000, Algeria.
4Laboratory of Functional Agrosystems and Technologies of Agronomic Sectors, Faculty of Natural and Life Sciences, Earth and Universe Sciences, University of Abou Bekr Belkaïd, Tlemcen-13000, Algeria.

ABSTRACT

Background: Taraxacum officinale, a traditional medicinal plant in Africa and notably Algeria, is widely used for its hematopoietic and gastrointestinal benefits. It is believed to stimulate red blood cell production and protect against gastric ulcers. This study aimed to evaluate the erythropoietic and antiulcer effects of its ethanolic extract in Wistar rats.

Methods: In the anemia model, 25 male rats were divided into four groups. Anemia was induced using cephalosporin (10 mg/kg) for 10 days, while treatment groups received ethanolic extract of T. officinale  (EETO) (200 mg/kg, twice daily). Blood samples were analyzed for hematological and biochemical parameters. For the ulcer model, gastric lesions were induced with HCl/ethanol (1.50 mMol/60%) and treated with EETO (200 mg/kg) for 7 days. Gastric tissue was examined microscopically and malondialdehyde levels were measured.

Result: In anemic rats, T. officinale significantly increased red blood cells RBCs (52.10%), hemoglobin (38.56%), iron (50.95%) and several vitamins and minerals while reducing erythropoietin. In the ulcer model, the EETOreduced ulceration by 68% and oxidative stress markers. Histology confirmed mucosal protection. These findings support the therapeutic potential of Taraxacum officinale against anemia and gastric ulcers.

INTRODUCTION

Nature is a rich source of remarkable plants with notable nutritional and medicinal benefits, such as Buniumbul- bocastanum (Bouhalla et al., 2024; Bouhalla et al., 2025) and dandelion (Urüşan, 2023), which are encountered in Algeria.
       
Dandelion (Taraxacum officinale) has been valued since antiquity as a nutrient-rich remedy, traditionally used as a medicine for its diuretic, anti-inflammatory and hepato-biliary properties (Kisiel and Barszcz, 2000; Ahmad et al., 2000).
       
Many medications, particularly antibiotics, can cause red blood cell lysis-a serious issue given RBCs’ vital role in oxygenation. This raises significant safety concerns about frequent/long-term use of hemolytic drugs, despite their therapeutic necessity (Ighodaro et al., 2020).
       
Anemia is an abnormality of the blood count. It is a health condition characterized by reductions in the number of red blood cells or hemoglobin, with the accompanying effect of a reduction in the ability of the blood to transport oxygen to the body’s tissues. Abnormal low hemoglobin and circulating levels may result from decreased production of red blood cells, or increased lysis of red blood cells. Anemia is arguably the most common blood disorder, posing a critical health risk to at least a third of the world’s population. It remains a major public health problem in many developing and underdeveloped countries. People of all ages, especially infants, young pregnant women and the elderly, are affected by this problem (Luka et al., 2014). It is diagnosed by the blood count, an examination carried out on a blood test. It can be caused by destruction of red blood cells (hemolysis) or blood loss (hemorrhage) (De Benoist et al., 2008).
       
Erythropoietin is the main hormone that regulates erythropoiesis (a complex, multi-step process of blood production). In addition to erythropoietin, the erythropoietic machinery requires a constant supply of certain minerals (iron, copper) and vitamins (A, B12, B6, C, E, folic acid, riboflavin and nicotinic acid). Insufficient supply of any of these propensity constituents can result in anemia (Owoyele et al., 2011). Gastritis or gastric ulcer results in the destruction of gastric mucosa due to several inducers such as excessive acid secretion, pro-inflammatory cytokines and free radicals and Helicobacter pylori invasion (Boeing et al., 2016). The presence of HCl with ethanol accelerates the process of gastric ulcerogenesis and impairs the protection of the mucous membranes against chemical agents like ethanol to exacerbate the lesions (Marotta et al., 1999).
       
This work aims to highlight the anti-anemic effect as well as the anti-ulcer activity of Taraxacum officinale on Wistar rats.

MATERIALS AND METHODS

Collecting the plant
 
The plant material consists of the aerial part of Taraxacum officinale ²Telfaf² at maturity. The harvest was carried out the Tazgait region of Mostaganem (Algeria) (Fig 1) in printer (March) 2020. The plant was washed with water to remove debris and soil particles.

Fig 1: Geographical area of Taraxacum officinale harvest.


 
Extraction of polyphenols
 
The extraction of the plant was done by maceration according to the protocol of (You et al., 2010) with a small modification. The plant material is crushed using a mortar, 200 g of the latter is added to 1000 ml of 70% ethanol. Allow the suspension to macerate at room temperature for 48 hours in the dark. After filtration using Whatman No. 4 paper, the filtrate was concentrated using a steam rotator at 45oC so that the ethanol was evaporated. The ethanolic  extract of Taraxacum officinale will be collected in a dark glass bottle then stored at 4oC.
 
Determination of total polyphenols of extract of Taraxacum officinale
 
We used the Folin-ciocalteu method to determine the content of phenolic compounds according to (Li et al., 2009). The concentration of total polyphenols is calculated from the calibration line established with gallic acid (0-200 mg/ml) and is expressed in mg of gallic acid equivalent per gram of extract.
 
Animals and accommodation conditions
 
40 male Wistar rats (150-180 g) from Pasteur Institute (Bouzareah, Algiers) were acclimatized for 2 weeks under standard conditions (12h light/dark cycle, ventilated housing, ad libitum access to food/water). Animal care followed National Institute of Health (NIH-USA) guidelines.
 
Induction of anemia with cephalosporin in experimental rats
 
Anemia was induced in test animals with Cefuroxime, (10 mg/kg BW, 1 ml distilled water) was administered orally (2 × daily, 10 days) to induce anemia (modified Ighodaro et al., 2020 protocol).
       
20 rats were randomly grouped into 4 groups (n=5/group):

· Group I: Untreated control.
· Group II: Cefuroxime only (10 mg/kg BW).
· Group III: EETO only (200 mg/kg BW).
· Group IV: Cefuroxime (10 mg/kg BW) + EETO.
       
Animals received oral doses of T. officinale ethanolic extract and Cephalosporin twice daily for 10 days with ad libitum access to food/water. After overnight fasting, blood was collected via retro-orbital eye puncture under light chloroform anesthesia prior to sacrifice. Samples were stored in dry and EDTA tubes for analysis. The experimental animals are as follows:
       
Group 1 (G1): Control group Group 2 (G2): Untreated anemic group (10 mg/kg cephalosporin) Group 3 (G3): Non-anemic group treated with 200 mg/kg of EETO Group 4 (G4): Anemic group pre-treated with 200 mg/kg of EETO.

Estimation of hematological parameters (cell blood count)
 
Blood was collected in EDTA tubes for the determination of hematological parameters. A differential blood count was performed using a Coulter machine (ERMA PCE-210, Ermainc, Japan).
 
Estimation of serum iron and ferritin
 
The determination of serum iron and ferritin is carried out using a Cobas Integra 400 Plus automatic device according to (Fretellier et al., 2014; Koivunen et al., 2006) respectively.
 
Estimation of blood magnesium
 
The dosage of magnesium (mg) in serum is carried out using a colorimetric method using Chronolab kit.
 
Estimation of copper (Cu) and zinc (Zn) copper
 
(Cu) and zinc (Zn) determination in serum was carried out by atomic absorption spectrophotometry (SpectrAA 220 FS, Varian, Springvale, Australia) (Southon et al., 1984).
 
Estimation of vitamins
 
- Estimation of vitamin C
 
The vitamin C content in blood serum was estimated according to the method of Omaye et al., (1979).
 
- Estimation of folate B9 and B12
 
The analytical performances of the in vitro quantitative determination techniques for folate B9 and vitamin B12 were evaluated on the Immulite 2000 analyzer by chemilum-inescence using the method of (Colombier et al., 2002).
 
Erythropoietin estimation
 
Erythropoietin was estimated using ELISA with Quantikine IVD ELISA kits (R and D Systems #DEP00).
 
Ulcer induction with HCl/ethanol in experimental rats
 
The study utilized 20 male rats divided into four groups (n=5 per group). Groups G1 and G2 received 1 ml physiological water orally, while G3 and G4 received 200 mg/kg EETO. Following a 24-hour fast on day 6, G2 and G4 were administered 1 ml HCl/ethanol solution (1.50 µMol/60%) on day 7 to induce gastric ulcers (Yang et al., 2017). One hour post-induction, animals were anesthetized with chloroform and sacrificed. Blood samples were collected via retro-orbital puncture into heparinized tubes. Stomachs were excised, rinsed with saline and divided for histological analysis (10% formalin fixation) and lesion assessment (PBS preservation). Gastric mucosal injury was quantified as percentage of total surface area using microscopic evaluation (Morsy et al., 2012). Experimental groups comprised: G1 (control), G2 (ulcer control), G3 (EETO-only) and G4 (EETO pretreatment + ulcer induction).

RESULTS AND DISCUSSION

Antibiotics are defined as substances in small quantities produced from microorganisms (Bertrand, 2005). These compounds which alter the normal functioning of bacteria can inhibit their growth (bacteriostatic antibiotic) or destroy them (bactericidal antibiotic) (Hefnawy et al., 1999). Cephalosporins form a large group of semi-synthetic antibiotics of lactam core derivatives; they are used in clinical medicine. They are linked to the fundamental structure and the mechanism of bactericidal action of penicillins. They are used for the treatment of infections caused by Gram-negative and Gram-positive bacteria. Cephalosporins are among the oldest and most frequently prescribed natural antimicrobial agents (AL-Ghannam, 2008).
       
Chronic cephalosporin use can induce hemolytic anemia (Garratty, 2012). This study evaluated Taraxacum officinale as a natural anti-anemic adjunct to cefuroxime therapy.
 
Content of total polyphenols of ethanolic extract of Taraxacum officinale (EETO)
 
The results of total polyphenol content of EETO in Fig 2, indicating that the extract has a proportion of total polyphenols, which is 88.33 mg EAG/g.

Fig 2: Calibration curve of gallic acid of total polyphenols from ethanolic extract of Taraxacum officinale.


       
Plants of the genus Taraxacum, known as dandelion, have long been used in traditional medicine due to the presence of chicoric acid (dicaffeyl tartaric acid), which belongs to phenylpropanoids and one of the main constituents of T. officinale (Ivanov, 2014).
       
When the volume percentage of ethanol was less than 50%, content of total phenols, chicoric and caffeic acid and derived acids increased with increases in ethanol concentrations (Tsai et al., 2012).
       
Phenolic acids, plant-derived secondary metabolites, are potent antioxidants with significant health benefits (Ivanova et al., 2005). Our study found 88.33 mg/100 g polyphenols, comparable to Yang et al., (2017) (99.9±0.7 mg/100g) but higher than Domitrovic et al., (2010) (3.11± 0.14 mg GAE/g), likely due to solvent polarity effects (Xi et al., 2009).
 
Effect of ethanolic  extract of Taraxacum officinale on Hb, RBC and PCV in anemic rats induced by cephalosporins
 
According to Table 1, compared to controls, the anemic group (G2) showed significant reductions (p<0.05) in RBCs (43.11%), Hb (17.19%) and hematocrit (29.79%). EETO pretreatment (200 mg/kg) effectively restored these parameters, increasing Hb (52.10%), RBCs (38.56%) and hematocrit (40.29%).

Table 1: Effect of ethanolic extract of Taraxacum officinale on Hb, RBC and hematocrit in anemic rats induced by cephalosporins.


       
According to the WHO, a hemoglobin threshold (Hb<11g/dL) was chosen for the determination of anemia (Fehr et al., 2009).
 
Effect of ethanolic  extract of Taraxacum officinale on minerals
 
Table 2 shows the effect of EETO on iron, ferritin, magnesium, zinc and copper in experimental rats. Iron shows the same variations as ferritin in all groups. Iron and ferritin values are expressed as the average of five rats. The results also indicate that administration of cephalosporin at 10 mg/kg (bw) to rats in the positive control group led to a significant decrease (P<0.05) in iron, ferritin, magnesium, copper and zinc with the levels of 49.67%, 48.12%, 43.03%, 47.17% and 45.20% respectively compared to the control group. On the other hand, pre-treatment of rats with the EETO significantly restored iron, ferritin and magnesium, copper and zinc (P<0.05) to 50.95%, 47.40%, 45.78%, 53.81% and 44.96% respectively.

Table 2: Effect of ethanolic extract of Taraxacum officinale on minerals.


       
Although the stored iron is deposited in these cells in the form of ferritin (Cattan, 2004). When there is a lack of iron, the iron stored in the form of ferritin can be released. evidence. In general, the macrophage (villus apex macrophage and others), through the process of erythro-phagocytosis, can continuously supply iron to the plasma. Indeed, during this process (Loréal et al., 2012).
       
Zinc has anti-inflammatory properties and a deficiency can cause immune disorders (Derai, 2014).Copper deficiency has recently emerged as a cause of anemia (Esposito et al., 2003).
       
Anemia could lead to abnormal blood–zinc status in the body (Jeng and Chen, 2022).
 
Effect of ethanolic  extract of Taraxacum officinale on vitamins
 
Table 3 shows the effects of the EETO on the vitamins contained in rats. Values are expressed as the average of five rats. According to our results, we note that the concentration of vitamins C, B9 and B12 in rats in the group pre-treated with the ethanolic  extract of the plant increases significantly (P<0.05) by 85.58%, 89.22% and 56% respectively compared to untreated anemic rats. The concentration of vitamins C, B9 and B12 were too low in the positive control group with 85.82%. 86.91% and 35.62% respectively compared to the control group. A moderate improvement was observed in rats in the group pre-treated with the EETO at 200 mg/kg (bw).

Table 3: Effect of ethanolic extract of Taraxacum officinaleon vitamins.


       
Vitamin C is capable of mobilizing iron stores in the reticuloendothelial system, it also potentiates the enzymatic reaction of iron incorporation for the synthesis of heme (Giancaspro et al., 2000).
       
A combined deficiency of cobalamin (B12) and iron can have opposing effects on red blood cell volume and give rise to anemia (Mahmood et al., 2014).
 
Effect of ethanolic  extract of Taraxacum officinale on erythropoietin (EPO) concentration)
 
Table 4 shows the effects of the EETO on the erythropoietin content of rats. Daily administration of cephalosporin significantly increased the erythropoietin concentration of the positive control group. This percentage is 30.4% higher than that of the control group. On the other hand, the pre-treatment of rats in the fourth group recorded an improvement in the concentration of erythropoietin to 36.98% compared to the positive control rats.
       
Ferrucci et al., (2005) suggest that inflammatory anemia evolves from a "pre-anemic" stage, characterized by a compensatory increase in erythropoietin that maintains a normal hemoglobin level.
       
So according to these results, Taraxacum officinale extract is able to improve blood constituents in most erythropoietic markers (Hb, GR, Hematocrit, Hb, Iron, Ft, Mg, Cu, Zn, vitamin C, B9, B12 and erythropoietin) in animals in the group treated with 200 mg/kg of the plant extract. Previous studies show that the plant had an inhibitory effect on vascular permeability (Jeon et al., 2008), that it has antioxidant activities because it stimulates catalase and glutathione reductase (You et al., 2010) and subsequently the red blood cells become more resistant to hemolysis. Rodriguez-Fragoso et al., (2008) show that Taraxacum officinale can be used to improve blood circulation.
 
Effect of ethanolic extract of Taraxacum officinale on malon-dialdehyde (MDA)
 
Fig 3 shows EETO’s effect on lipid peroxidation. HCl/ethanol significantly increased MDA (8.92 vs 1.7 nmol/ml in controls, p<0.05). EETO pretreatment reduced MDA by -6 nmol/ml (71.76% decrease vs control group).

Fig 3: Malondialdehyde (MDA) content (nmol/ml) in rats treated or/not with the EETO and/or HCl/ethanol The values represent the mean(m) of 5 determinations ±SEM( n =5).


       
Our study shows that Taraxacum officinale extract decreased MDA levels. This trend was also observed by (Yang et al., 2017). This trend was also observed by Yang et al., (2017). Turkistani, (2019) obtained similar results with the aqueous extract of Taraxacum officinale.
 
Macroscopic study of the stomach
 
Percentage inhibition of gastric mucosal injury (%INH)
 
Microscopic examination allowed us to note the effectiveness and gastro-protective action of the EETO. It should be noted that the administration of a dose of 200 mg/kg of EETO at a dose of 200 mg/kg of EETO, in gastric ulcerated rats (G4), significantly inhibited (P<0.05) the ulceration rate of 68%, against the group of ulcerated rats (0%) G2. On the other hand, daily administration of EETO has an inhibition value of 98.2% similar to that of the control (Fig 4).

Fig 4: Percentage inhibition of gastric mucosal lesion (%) in rats treated or not with EETO and/or HCl/ethanol. The values represent the mean(m) of 5 determinations ±SEM (n =5).


       
The same results are observed by (Turkistani, 2019), who showed that the aqueous extract of T. officinale containing these phytochemicals would be strongly linked to anti-ulcer benefits.

Microscopic analysis revealed :

• The control group (G1) presented a normal gastric structure (mucosa, muscularis, serosa) (Fig 5a) and which is similar with the group (G3) (Fig 5c).

Fig 5: Histological sections of stomach of group: (a): G1, control; (b): G2, 1ml physiological water (7 days) then 10 ml of HCl/Ethanol (1 day); (c): G3, 200 mg/kg of EETO (7 days); (d): G4; 200 mg/kg of EETO (7 days) then 10 ml of HCl/Ethanol (1 day).



• HCl/ethanol treatment caused increased gastric thickness with edema and polynuclear neutrophils (Fig 5b).
• EETO pretreatment (G4, 200 mg/kg) showed significant lesion reduction, prevented thickness increase and reduced dema/polynuclear neutrophils (Fig 5d).
       
Among the various factors that contribute to gastritis and gastric ulcer is the consumption of alcohol with high acid content in the stomach. HCl/ethanol is widely used to induce chronic gastritis in animal models of this disease since their similarity in symptoms to those of humans (Santin et al., 2013). Ethanol is one of the agents that promotes gastritis by increasing oxidative stress and inflammation, leading to necrosis and tissue depletion of gastric mucus and reducing gastric blood flow (Breviglieri et al., 2017; Zanatta et al., 2009). Ethanol reduces gastric blood flow, which is attributed to hemorrhage and necrosis of stomach tissues (Zanatta et al., 2009). Solubilizing ethanol also increases gastric mucosal loss (Marotta et al., 1999). It induces hemorrhage and necrosis with an associated increase in lipid peroxidation rates. The presence of HCl with ethanol accelerates the process of gastric ulcerogenesis (Marotta et al., 1999).
       
In the present study, the models were established by administering a dose of HCl/ethanol for one day to induce chronic gastritis, which was expressed by reddish discoloration of the inner layer, as well as hemorrhage and edema due to increased oxidative stress and inflammation. EETO reduce gastritis compared to the positive control, it has a positive and preventive effect to treat gastritis and ulcer, with better protection against ulcer, because the maintenance of the gastric mucosa plays an important role in gastric protection (Suo et al., 2016). Mahmood et al., (2010) claimed that phenols as well as flavonoids in Taraxacum officinale have anti-ulcerogenic activity.

CONCLUSION

According to the results of this study, it can be said that the consumption of Taraxacum officinale during a treatment causing anemia such as cephalosporin or another medication, can maintain healthy homeostasis, particularly regarding red blood cells, hematocrit and white blood cells. It is capable of reducing lipid peroxidation, which is one of the main manifestations of oxidative damage to organs and reducing gastric lesion surfaces. It is important to use this plant and introduce it into the diet as a preventative measure, or in case of erythropoietic or gastric problems and further work would be necessary to produce a phytomedicine based on Taraxacum officinale.

ACKNOWLEDGEMENT

The first author expresses sincere gratitude to the Ministry of Higher Education and Scientific Research (Algeria) through  the University of Mostaganem for financial support in Algeria.
       
This work was conducted at the Laboratory of Beneficial Microorganisms, Functional Foods and Health (LMBAFS), University Abdelhamin Ibn Badis, Mostaganem, Algeria.
 
Disclaimers
 
The views and conclusions expressed in this article are solely those of the authors and do not necessarily represent the views of their affiliated institutions. The authors are responsible for the accuracy and completeness of the information provided, but do not accept any liability for any direct or indirect losses resulting from the use of this content.
 
Informed consent
 
All animal procedures for experiments were approved by the Committee of Experimental Animal care and handling techniques were approved by the University of Animal Care Committee.

CONFLICT OF INTEREST

The authors declare that there are no conflicts of interest regarding the publication of this article. No funding or sponsorship influenced the design of the study, data collection, analysis, decision to publish or preparation of the manuscript.

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