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Efficacy of myrrh extract against Eimeria labbeana-like experimental infection in Columba livia domestica: in vivo study

BMC Veterinary Research volume 20, Article number: 586 (2024) Cite this article

Abstract

Background

The Protozoan pathogen Eimeria is a significant issue in poultry production. Scientists are concerned with finding alternative strategies due to the spread of resistance against the commonly employed coccidiostats. This study examined how well myrrh extract (MyE) protected domesticated pigeons from an experimental Eimeria labbeana-like infection.

Methods

Female pigeons were divided into six groups (5 pigeons/group): Group1: control pigeon group, Group2: Non-infected and treated pigeon group with MyE (500 mg/kg). Group3: Infected and non-treated pigeon group, Group4: Infected and treated pigeon group with MyE (250 mg/kg), Group5: Infected and treated pigeon group with MyE (500 mg/kg), Group6: Infected and treated pigeon group with amprolium (1 g/L of H2O). Oral infection with 3 × 104 sporulated E. labbeana-like oocysts was used to inoculate groups (3–6). Three days after infection, groups (4–6) received daily treatment with MyE and amprolium for five days. Oocyst output was assessed on day 8 post-infection. After sacrificing the pigeons, the small intestine and blood were collected from each pigeon and processed for histological, biochemical, and oxidative damage examinations.

Results

This study looked into the overall phenolic and flavonoid contents and MyE’s antioxidant activity. According to the data, the best dose of MyE was 500 mg/kg, which significantly decreased the output of oocysts produced (2.090 × 105 ± 1.04 × 104 oocysts/g.feces). This result has been linked to a -2.51% decrease in the pigeon’s body weight gain. The morphometric characteristics of freshly unsporulated and sporulated oocysts were obtained, and pigeons treated with MyE significantly decreased size. Furthermore, there was a significant decrease in both the number and size of the developmental stages of E. labbeana-like (i.e. meronts, gamonts, and developing oocysts) in the intestinal tissue among the MyE-treated group. MyE facilitates the disruption of intestinal homeostasis caused by E. labbeana-like infection, specifically concerning carbohydrates and proteins. Concurrent with the state of total antioxidant capacity (TAC), the antioxidant activity of MyE reduced the blood plasma levels of trace elements (Fe, Cu, Cr, Zn, and Ni).

Conclusion

Our findings suggest that MyE could be a useful antioxidant source and a replacement for coccidiostats in preventing and treating avian coccidiosis.

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Introduction

A highly distributed intestinal disease, avian coccidiosis has major economic implications in the global poultry industry [61]. With a high degree of host specificity, Eimeria species are the most common cause of avian coccidiosis [70]. Oral ingestion of the invasive Eimeria parasite forms, i.e., sporulated oocysts, causes infection [50]. Sporozoites enter the host’s tissue by the action of the stomach’s hydrochloric acid action and the intestine’s digestive juice. Once inside, they pierce the intestinal villi’s epithelial cells [54].

In pigeons, it is caused by twenty-one species of intracellular apicomplexan protozoan parasite of the genus Eimeria, including E. chalcoptereae, E. choudari, E. columbae, E. columbapalumbi, E. columbarum, E. columbinae, E. curvata, E. duculai, E. gourai, E. janovyi, E. kapotei, E. labbeana, E. labbeana-like, E. livialis, E. mauritiensis, E. palumbi, E. sphenocerae, E. tropicalis, E. turturi, E. waiganiensis, and E. zenaidae [11]. Of these species, E. labbaena, E. columbae, and E. columbarum are regarded as economically important pathogenic species, causing impaired digestion and food absorption, anorexia, dehydration, and even mortality [3, 76]. The body’s distribution of minerals is changed during enteric infections, which has an impact on changes in mineral metabolism and absorption [30].

Strong management strategies, both prophylactic and therapeutic, are crucial for the control of Eimeria because of the disease’s widespread prevalence due to the high survival rate of oocysts in the environment [59]. Anticoccidial drugs are among these programs that are commonly used to treat and prevent coccidiosis [42]. One anticoccidial drug that prevents coccidia from growing, metabolizing, and reproducing normally is amprolium [7]. Alternative therapies are urgently needed to avoid negative health effects because drug-resistant strains of Eimeria are emerging in avian populations and drug residues in meat are becoming a growing public health concern [24]. Plants and their byproducts are seen to be promising anticoccidial prospects because of their various benefits, which include low prices, less drug resistance, and minimal drug residues and adverse effects [2].

Myrrh is an aromatic gum resin, present in the stem bark of Commiphora myrrha [19]. With a wide variety of pharmacological activities, it is frequently utilized in traditional Saudi Medicine [26]. It exhibits strong antimicrobial activity [20, 48, 63, 66]. Additional physiological effects of myrrh include its antioxidant [22, 34], immunoenhancer [44], anti-hyperlipidemic [51, 69], and anti-inflammatory [9, 62] properties, all of which control the body’s immune functions. Additionally, myrrh possesses antiparasitic properties against Trichinella spiralis [4,5,6, 23, 28], Fasciola gigantica [52], and Schistosoma mansoni [57]. Myrrh can reduce Eimeria stiedae oocyst shedding and the ensuing liver injury [25].

Pathological alterations related to the infection of E. labbeana-like in domestic pigeons (Columba livia domestica) were noted in an early study by Abdel-Gaber et al. [3]. Furthermore, in vitro efficacy of myrrh against coccidiosis has been demonstrated against E. labbeana-like in pigeons [12]. However, there is little evidence of myrrh’s oocysticidal effect in pigeons infected with Eimeria. Therefore, the goal of the current study is to evaluate the antioxidant activity and in vivo efficacy of myrrh extract in treating coccidiosis caused by E. labbeana-like experimental infection in pigeons.

Materials and methods

Plant collection and extract preparation

Myrrh was purchased from a local market in Riyadh, Saudi Arabia. Following the suggested methodology of Akande et al. [8], 100 g of myrrh resin was crushed into powder using a pestle and mortar. The resin was then extracted using maceration with 1000 ml of 70% methanol (MeOH). For 24 h, the mixture was constantly agitated at 4 °C in the dark. After that, it was centrifuged for 15 min at 5000 rpm. The supernatant was collected, filtrated using Whatman No. 1 filter paper, and concentrated at 50ºC in a rotary evaporator (Thermo Fisher Scientific Inc., Waltham, MA, USA) to obtain the crude extract. Before being analyzed, the myrrh extract (MyE) was frozen and allowed to dry at room temperature.

Phenolics and flavonoid content estimation

The Folin–Ciocalteu technique was utilized to ascertain the phenolic content of MyE, following the uniform method of Singleton et al. [71]. Gallic acid (GAE) concentrations ranging from 25 to 400 g/ml were used to produce a calibration curve from which data was collected. The data was expressed as mg GAE/g dry extract. Furthermore, the flavonoid content of MyE was determined at 415 nm using the aluminum chloride colorimetric method of Ordoñez et al. [56]. A standard curve with different quercetin (QUE) values of 50–400 g/ml produced the flavonoid content, which was then expressed in mg QUE/g dry extract.

DPPH radical scavenging activity

The extract’s ability to scavenge the 2,2-diphenyl-1-picrylhydrazyl (DPPH) radicals was assessed using the Akillioglu and Karakaya [10] technique of antioxidant activity. Using a microplate reader (Thermo Fisher Scientific Inc., Waltham, MA, USA), absorbance was measured at 515 nm against the blank (methanol), and the results were represented as the percentage of DPPH radical suppression.

Experimental animals

A total of 35 females of the white domestic pigeons, Columba livia domestica (weighing 300–380 gm), were used as experimental animals. The pigeons were purchased from the local animal market in Riyadh, Saudi Arabia. The fecal samples of the pigeons were checked to ensure that they were free of infection. The pigeons were housed in specific pathogen-free conditions at a controlled temperature (23 ± 5℃) with a 12/12 hrs light-dark cycle. Pigeons were given ad libitum access to tap water and balanced seed mixtures. All pigeon-handling procedure was carried out following the ethical guidelines of the Research Ethics Committee (REC) at King Saud University.

Preparation of Eimeria infection

A model coccidian parasite, a lab strain of Eimeria labbeana-like was taken from our collection in the Parasitology Laboratory (Zoology Department, College of Science, King Saud University) and used in the experiment. Five pigeons were utilized in the propagation of Eimeria oocysts. Each pigeon received 3 × 104 sporulated oocysts orally, according to Qudoos et al. [60]. Oocysts were found in the infected pigeon’s feces eight days post-infection (p.i.). The Eimeria oocysts were recovered and allowed to sporulate in 2.5% (w/v) potassium dichromate (K2Cr2O7) at 24 °C [3]. After centrifuging the sporulated oocysts in a buffered phosphate solution for 5 min at 2500 rpm, they were washed three times with distilled water [67].

Grouping of experimental birds

Pigeons were divided equally and randomly into six groups (five pigeons in each), as follows:

Group 1

(control group); received a basal diet and tap water.

Group 2

(non-infected treated group); received MyE (500 mg/kg) without infection [21].

Group 3

(infected group); received E. labbeana-like oocysts without treatment.

Group 4

(infected treated group); received a low dose of MyE (250 mg/kg) after infection with E. labbeana-like oocysts [21].

Group 5

(infected treated group): received a high dose of MyE (500 mg/kg) after infection with E. labbeana-like oocysts [21].

Group 6

(infected treated group): received the anticoccidial drug amprolium (1 gm soluble powder dissolved in 1 L of H2O) after infection with E. labbeana-like oocysts [21].

All groups except 1 and 2 were orally inoculated with 3 × 104 sporulated E. labbeana-like oocysts, according to Qudoos et al. [60]. The treatments with MyE and amprolium were started from day 3 p.i. and carried out daily for five days, according to Anwar et al. [21]. Each pigeon was weighed separately, and the difference between the pre-treatment (at day 0 p.i.) and post-treatment (at day 8 p.i.) weights was used to compute the body weight gain (BWG). Samples of feces (n = 3) were taken from each pigeon and kept separately to monitor the oocyst count. At the peak of oocyst count, which was at day eight p.i., treatment terminated. The McMaster counting technique was used to count the oocysts of feces, which were then expressed as oocysts/gram.feces [68].

Oocysts morphometry

In both the treated and untreated groups with infection, some of the oocysts could sporulate in K2Cr2O7. Using an Olympus compound microscope supplied with a CP72 digital camera (Olympus Corporation, Tokyo, Japan), both sporulated and unsporulated oocysts were photographed. An ocular micrometer that has been calibrated was used for oocyst measurements.

Sample collection

The pigeons were all euthanized with sodium pentobarbital on the 8th day p.i. Heparinized tubes were used to collect blood via cardiac puncture for hematological examination. Furthermore, the small intestine was isolated from each pigeon and then divided into two parts: (1) the first portion was preserved at -80 °C for biochemical studies, and (2) the second portion was suspended in neutral buffered formalin (NBF) (10%) for histological studies.

Plasma preparation

Heparinized tubes containing blood samples (about 3 ml) were centrifuged for 20 min at 3000 rpm. Before being used, blood plasma was isolated and stored at -20 °C [58].

Intestinal homogenate preparation

Standard protocol was followed in the preparation and homogenization of the small intestinal tissues [73]. In a cold centrifuge, the homogenate was spun for 15 min at 3000 rpm. After that, the supernatant was divided and stored at -20 °C until use.

Histopathological evaluation

The preserved small intestinal tissues in 10% NBF were removed and then dehydrated, embedded in paraffin wax, sectioned into 5 μm, and stained with hematoxylin-eosin (H&E) for the histological studies [3]. Using an Olympus B×61 microscope (Tokyo, Japan), sections were examined and photographed. Within 10 intestinal crypt villi, the number of merozoites, gamonts, and developing oocysts was counted [33]. Data was expressed as the mean number of each stage/ten well-oriented crypt villi. Using a calibrated ocular micrometer, the developmental stages of parasites were measured and expressed as a range (mean in parentheses).

Intestinal glucose and protein detection

Other intestinal sections were stained with periodic acid-Schiff’s method for qualitative demonstration of total carbohydrates [17], and with mercuric bromophenol blue method for qualitative detection of total proteins [17]. Using an Olympus B×61 microscope (Tokyo, Japan), sections were examined and photographed.

Biochemical analysis

Using commercial kits (Bio-Diagnostic kits, Bio-Diagnostic Co., Egypt), the level of glucose and total proteins were determined in the intestinal homogenate of pigeons following the protocol of Trinder [41, 72], respectively, using Ultrospec 2000 UV spectrophotometer (Amersham Pharmacia Biotech, Cambridge, UK). The data were expressed in g/dL for both biochemical parameters.

Antioxidant capacity estimation

Using commercial kits (Bio-Diagnostic kits, Bio-Diagnostic Co., Egypt), the total antioxidant capacity (TAC) was determined in the intestinal homogenate of pigeons following the protocol of Koracevic et al. [47] using Ultrospec 2000 UV spectrophotometer (Amersham Pharmacia Biotech, Cambridge, UK). The data was expressed in mM/L for the detectable parameter.

Trace element concentrations

Plasma samples were diluted as required with deionized water, according to Bravo et al. [31]. Samples were run through the atomic emission spectrometer with inductivity coupled plasma iCAP-6500 Duo (Thermo Scientific, UK) to analyze five trace elements i.e. iron (Fe), copper (Cu), chromium (Cr), zinc (Zn), and nickel (Ni). For each element, the same is calibrated using standard solutions. To ensure quality control, each analysis was carried out three times, and five samples were tested with a single blank. Heavy metals suppression (%) was calculated as follows: Trace element suppression (%) = 100 – [(Element in treated group/Element in the infected group)×100)].

Statistical analysis

Data was presented as mean and standard deviation (i.e., mean ± SD). Version 18 of SPSS was used for statistical analysis. To assess differences between the groups, a one-way analysis of variance (ANOVA) with Duncan’s comparison test (p < 0.05) was used.

Results

Phenolics and flavonoid content estimation

The total phenolic content in MyE determined using the Folin–Ciocalteu technique was found to be 57.63 ± 0.59 mg GAE/g dry extract (Fig. 1). Moreover, the total flavonoid in MyE determined using the aluminum chloride colorimetric method was found to be 9.57 ± 0.14 mg QUE/g dry extract (Fig. 1).

Fig. 1
figure 1

The concentration of phenolics and flavonoids content that determined in myrrh extract (MyE)

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Oocyst output

On day 8 p.i., oocyst shedding in feces peaked at around 5.249 × 105 ± 3.13 × 104 oocysts/g feces in the infected group (Fig. 2). Of the groups treated with MyE, the group treated with 500 mg/kg showed a significant (p < 0.05) reduction of the oocyst output by 2.090 × 105 ± 1.04 × 104 oocysts/g feces, followed in ascending order by the group treated with 250 mg/kg. This dose was the most effective for reducing the fecal oocysts output in comparison to 4.232 × 104 ± 1.22 × 104 oocysts/g feces with the reference drug (Fig. 2).

Fig. 2
figure 2

Oocyst output in pigeons infected with Eimeria labbeana-like parasite and for infected treated groups with MyE (250 mg/kg and 500 mg/kg) and 1 g/L.H2O AMP (reference drug) on day 8 p.i. All values are presented in means ± SD. * represents the significance change between infected and treated groups at p < 0.05

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Body weight gain (BWG)

The BWG showed no significant difference on the day of infection in all groups. On the 8th day, the control group had a significant (p < 0.05) increase in BW by an average percent of 1.69%, while the E. labbeana-like infection caused a significant (p < 0.05) diminish in BW of the infected group by an average percent of -3.91% (Fig. 3). The infected-treated groups showed a significant (p < 0.05) increase in BW by -3.04 and − 2.01% for those treated with 250 mg/kg and 500 mg/kg, respectively. Both MyE doses showed less BW than the reference drug − 1.72% (Fig. 3).

Fig. 3
figure 3

The weight change among the experimental pigeon groups. Values are presented in means ± SD. * represents the significance change against the non-infected control group at p < 0.05, and # represents the significance change against the infected group at p < 0.05

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Morphometry of Eimeria oocysts

Before starting the experiment, the unsporulated E. labbeana-like oocysts were observed with a spherical shape and surrounded by a thick bi-layered wall and measured to be 17.80 ± 1.11 (16.18–20.34) × 15.98 ± 0.72 (14.17–17.64) in size (Fig. 4). In the infected group, oocysts were measured 17.77 ± 1.08 (16.29–20.28) × 15.90 ± 0.83 (14.04–17.51) in size (Table 1). Oocysts in the infected-treated groups showed a significant (p < 0.05) lower size as compared to the infected group and measured 16.37 ± 0.41 (15.22–16.86) × 14.71 ± 0.43 (14.38–15.98) for oocysts size in the group treated with 250 mg/kg MyE, 15.96 ± 0.83 (14.10-15.77) × 13.98 ± 0.52 (13.27–14.75) for those oocysts in the group treated with 500 mg/kg MyE, and 14.40 ± 1.01 (13.23–15.02) × 12.02 ± 1.58 (10.35–13.37) for oocysts get out from pigeons treated with the reference drug (Table 1).

Fig. 4
figure 4

Oocysts of Eimeria labbeana-like parasite among the infected, infected-MyE, and infected-drug pigeon groups before sporulation (A-D) and after sporulation (E-H) with K2Cr2O7 showed changes in the oocyst size after treatment. (OL, outer layer; IL, inner layer; RF, refractile body; SB, stieda body; PG, polar granule; SPC, sporocyst; RBS, residuum of sporocyst; SPZ, sporozoite; S, sporont). Scale bar = 10 μm

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Table 1 Morphometric changes of oocysts for Eimeria labbeana-like parasite in the infected and treated pigeon groups
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After complete sporulation in K2Cr2O7, the sporulated E. labbeana-like oocysts were observed with four sporocysts and measured, before giving infection, to be 19.80-20.29 (19.40) × 17.39–18.57 (17.94) (Fig. 4). In the infected group, sporulated oocysts were measured 19.73 ± 0.49 (19.27–20.22) × 17.83 ± 0.59 (17.23–18.45) in size (Table 1). All treated groups showed a significant (p < 0.05) lower oocyst size as compared to the infected group and measured as 18.67 ± 0.42 (18.21–19.32) × 17.43 ± 0.31 (16.35–17.99) for sporulated oocysts in 250 mg/kg MyE, 17.67 ± 0.39 (17.11–18.42) × 16.35 ± 0.48 (15.84–16.97) in 500 mg/kg MyE, and 16.26 ± 0.38 (15.79–16.26) × 15.15 ± 0.35 (14.76–15.48) for those in the reference drug (Table 1).

Histopathological analysis

Experimental infection of pigeons with E. labbeana-like oocysts led to the development of different parasite stages (meronts, gamonts, and developing oocysts) in the intestinal epithelial cells that were observed in the hematoxylin and eosin-stained sections (Fig. 5). These stages were counted per 10 VCUs. They were 11.56 ± 0.69 meronts, 32.91 ± 2.18 gamonts, and 28.43 ± 1.52 developing oocysts in the intestinal villi of the infected pigeons (Fig. 6). Remarkably, the number of meronts, male and female gamonts, and developing oocysts were significantly (p < 0.05) decreased after treatment with 250 mg/kg MyE (3.21 ± 0.52, 19.87 ± 0.63, and 9.45 ± 0.97, respectively), 500 mg/kg MyE (1.80 ± 0.50, 11.09 ± 0.70, and 4.09 ± 1.01, respectively), compared to the amprolium’s values (0.33 ± 0.57, 3.00 ± 0.57, and 2.33 ± 0.57, respectively) (Fig. 6).

Fig. 5
figure 5

Sections stained with hematoxylin and eosin (H&E) for the infected intestinal tissue with Eimeria labbeana-like on day 8 p.i. showing different developmental parasitic stages. Note: ME, meronts; MA, macrogamont; MI, macrogamont; DO, developing oocyst. Scale bar = 5 μm

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Fig. 6
figure 6

The number of developmental parasitic stages of Eimeria labbeana-like in the intestinal tissue among the infected and treated pigeon groups. All values are presented in means ± SD. * represents the significance between the infected group and the treated group at p < 0.05

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Morphometry of the developmental Eimeria stages

Morphometric changes of E. labbeana-like stages (oocysts, micro-, and macrogamonts) were observed in the intestinal epithelial cells for the infected and treated groups (Fig. 7; Table 2). They were measured 11.75 ± 1.53 (10.02–14.84) × 9.52 ± 0.48 (9.01–10.11) in size of macrogamont, 12.70 ± 0.69 (12.07–14.17) × 8.60 ± 0.42 (8.04–9.23) in size of microgamont, and 14.06 ± 0.64 (13.30-14.94) × 11.49 ± 0.53 (10.70-11.87) in size of developing oocysts in the intestinal villi of the infected pigeons (Table 2). In the 250 mg/kg MyE, stages were measured 10.35 ± 0.40 (9.91–10.94) × 8.82 ± 0.34 (8.03–9.78) in size of macrogamont, 11.85 ± 0.30 (11.14–12.75) × 7.87 ± 0.32 (7.15–8.49) in size of microgamont, and 12.32 ± 0.23 (12.11–13.32) × 10.45 ± 0.27 (10.21–10.95) in size of developing oocysts (Table 2). Our findings showed that the developmental parasite stages in the infected group treated with 500 mg/kg were measured 9.26 ± 0.30 (8.68–9.67) × 7.74 ± 0.54 (7.02–8.61) in size of macrogamont, 10.85 ± 0.50 (10.03–11.86) × 6.73 ± 0.46 (6.10–7.47) in size of microgamont, and 11.50 ± 0.41 (11.06–12.25) × 9.80 ± 0.34 (9.71–10.44) in size of developing oocysts (Table 2). Moreover, parasite stages were measured in the intestinal villi of the infected-treated pigeon with amprolium to be 7.19 ± 0.43 (6.66–7.61) × 6.34 ± 0.45 (5.33–6.83) in size of macrogamont, 9.24 ± 0.47 (8.21–9.74) × 5.40 ± 0.33 (4.81–5.65) in size of microgamont, and 9.98 ± 0.97 (8.98–10.94) × 8.39 ± 0.45 (7.70–8.98) in size of developing oocysts (Table 2).

Fig. 7
figure 7

Sections stained with hematoxylin and eosin (H&E) for different developmental Eimeria stages in the infected, infected-MyE (250 mg/kg and 500 mg/kg), and infected-drug groups on day 8 p.i. showing changes in the stage size after treatment. Scale bar = 5 μm

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Table 2 Morphometric changes of developmental changes of Eimeria labbeana-like in the infected and treated pigeon groups
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Intestinal glucose and protein detection

Qualitative and quantitative analyses of glucose content revealed depletion in the intestinal tissue of the infected group with E. labbeana-like (0.92 ± 0.05 g/dL) in comparison to the control one (2.53 ± 0.17 g/dL) (Figs. 8 and 9). After MyE treatment, the glucose status showed a significant (p < 0.05) change (1.20 ± 0.12 g/dL for 250 mg/kg and 1.99 ± 0.19 g/dL for 500 mg/kg) compared to the infected group (Figs. 8 and 9).

Fig. 8
figure 8

Carbohydrate content in the intestinal sections stained with periodic acid Schiff’s (PAS) method. (A) control non-infected intestinal tissue with normal content. (B) non-infected-treated group with 500 mg/kg MyE. (C) E. labbeana-like infected intestinal tissue with depletion in their carbohydrate content. (D and E) infected treated pigeons (250 mg/kg and 500 mg/kg MyE, respectively) with improvement in their level. (F) infected treated pigeons with AMP (1 g/L.H2O) with improvement in their level. Scale bar = 100 μm

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Fig. 9
figure 9

Glucose concentration among the experimental pigeon groups on day 8 p.i. All values are presented in means ± SD. * represents the significant change concerning the control group at p < 0.05, # represents the significance change concerning the infected group at p < 0.05

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Moreover, E. labbeana-like infection caused depletion in the soluble protein content (38.07 ± 1.54 g/dL) in the intestinal tissue in comparison to the control group (75.96 ± 1.75 g/dL) (Figs. 10 and 11). Treatment with MyE restored the intestinal soluble proteins (46.43 ± 1.01 g/dL for 250 mg/kg and 58.68 ± 1.39 g/dL for 500 mg/kg) compared to the infected group (Figs. 10 and 11).

Fig. 10
figure 10

Protein content in the intestinal sections stained with mercuric bromophenol blue method. (A) control non-infected intestinal tissue with normal content. (B) non-infected-treated group with 500 mg/kg MyE. (C) E. labbeana-like infected intestinal tissue with depletion in their protein content. (D and E) infected treated pigeons (250 mg/kg and 500 mg/kg MyE) with improvement in their level. (F) infected treated pigeons with AMP (1 g/L.H2O) with improvement in their level. Scale bar = 100 μm

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Fig. 11
figure 11

Protein content in the experimental pigeon groups on day 8 p.i. All values are presented in means ± SD. * represents the significant change concerning the control group at p < 0.05, # represents the significance change concerning the infected group at p < 0.05

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Antioxidant activity

The infection of pigeons with E. labbeana-like significant decrease in the total antioxidant capacity (TAC) level from 2.41 ± 0.19 mM/L in the control group to 1.33 ± 0.17 mM/L in the infected group. When compared to the infected group, MyE treatment resulted in a significant (p < 0.05) increase in TAC (Fig. 12). While the level of TAC of pigeons treated with 250 mg/kg and 500 mg/kg of MyE and amprolium was upregulated to 1.53 ± 0.18, 1.89 ± 0.15, and 1.85 ± 0.17 mM/L, respectively (Fig. 12). Also, the percentage of 2,2-diphenyl-1-picrylhydrazyl (DPPH) assay was 94.41%.

Fig. 12
figure 12

Total antioxidant capacity among the experimental pigeon groups on day 8 p.i. All values are presented in means ± SD. * represents the significant change concerning the control group at p < 0.05, # represents the significance change concerning the infected group at p < 0.05

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Trace element concentrations

The Eimeria infection caused a marked disturbance in the trace elements level (Table 3). The trend of element concentration in blood plasms was Fe > Zn > Cr > Cu > Ni as given in Table (3). The concentration of Fe has dramatically increased from 1.325 ± 0.35 µg/mL in the control to 4.708 ± 0.16 µg/mL in the infected pigeon group (Table 3). Cu and Ni levels were significantly (p < 0.05) increased more than 2-fold in the infected pigeon (0.691 ± 0.03 µg/mL and 0.053 ± 0.001 µg/mL, respectively) than that of the control group (Table 3). Moreover, the infection with E. labbeana-like was able to significantly (p < 0.05) increase the Cr and Zn levels to approximately 60% in the pigeon of the infected group (0.600 ± 0.06 µg/mL and 0.702 ± 0.03 µg/mL, respectively) from those in the control group (0.362 ± 0.03 µg/mL and 0.452 ± 0.05 µg/mL, respectively) (Table 3). Treatment with 250 mg/kg MyE suppressed the level of measured trace elements by 17.77% (Fe), 40.52% (Cu), 29.50% (Cr), 3.41% (Zn), and 18.86% (Ni) from those in the infected group, as shown in Table (3). Our findings showed a high suppression level of trace elements with 500 mg/kg MyE by 36.55% (Fe), 48.19% (Cu), 39.66% (Cr), 18.09% (Zn), and 32.07% (Ni) in comparison to the reference drug group (Table 3).

Table 3 Trace element levels (µg/mL) in the blood plasma of pigeons among experimental groups
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Discussion

According to Aleksandra and Pilarczyk [13], coccidiosis in pigeons is regarded as an important parasitic disease that causes significant economic losses for the pigeon industry. Grandi et al. [43] suggest that using natural remedies and their extracts could serve as a substitute for coccidiostats in coccidiosis management. In Saudi Arabia, myrrh is one of the common herbs used with various pharmacological effects [14, 26]. In this study, the potential role of myrrh against E. labbeana-like infection was investigated. Two MyE doses (250 and 500 mg/kg) have been tested. In terms of anticoccidial activity, MyE might impede E. labbeana-like development in the host and finally oocysts shedding in pigeon’ feces, with the highest (500 mg/kg) being the most potent. According to the previously discussed issues, MyE has a strong oocysticidal activity because of its phytoconstituents (i.e., phenols and flavonoids), which can destroy parasites including oocysts and sporozoites, associated with decreasing the severity of Eimeria infection [12]. However, taking large doses of myrrh is possibly unsafe which leads to kidney problems and heart rate changes [35], skin rash [78], miscarriage [16], unbalanced blood sugar levels [18].

On day 8 p.i., the infected pigeon group’s body weight significantly decreased along with changes in the intestinal tissues’ protein and carbohydrate composition. This result was in line with Chapman [32] findings, which indicated the presence of several factors (i.e., Eimeria species and strain, pathogen load, and site of parasitic infection) that affect the disease severity of coccidial infection and have a varying range of diverse impacts on overall bird health. Furthermore, according to Williams [75], the endogenous portion of the Eimeria life cycle damages the host’s intestinal wall, which lowers growth performance parameters, the viscosity of the digesta, and nutrient malabsorption. A significant improvement in body weight was observed following treatment of the pigeons infected with the Eimeria parasite with MyE for five days because of the presence of bioactive compounds in MyE (i.e., triterpenoids), which aided in improving the intestinal histological architecture and restoring nutrient absorption across the intestinal wall. Similar findings on the use of phytochemicals as plant extracts with antioxidant functions, such as Zingibar officinale [15], Azadirachta indica and Psidium guajava [60], to alleviate avian coccidiosis in pigeons, have been published.

The histopathological outcomes, in this study, indicated the presence of a high parasitic load of E. labbeana-like, at the 8th -day p.i., at the site of infection leads to intestinal cell damage, which agreed with the findings of Abdel-Gaber et al. [3]. MyE disrupted the life cycle of E. labbeana-like, maximizing nutrient absorption and promoting the growth performance of pigeons, by significantly reducing the number of developmental Eimeria stages. This is also associated with a significant reduction in the micrometry of Eimeria stages (gamonts and oocysts) following MyE treatment. MyE’s high concentration of polyphenolic compounds, as previously reported by Fatani et al. [1, 39, 64, 65], may be the cause of the reduction in the micrometry of Eimeria stages. This outcome is consistent with Mohammed et al. [53] who reported that the therapeutic active components (i.e., phenols and flavonoids) in the plants have a potent antimicrobial activity via interaction with the microbial membranes and disrupting them, which affects the fluidity and permeability of the membranes, impairs their functions, allows cellular components to leak out, and ultimately causes cell death. Albasyouni et al. [12] have reported that MyE exhibits antiparasitic activity against E. labbeana-like. Its mode of action is related to the sporozoite membrane, which causes the Eimeria parasite to lose calcium ions which are necessary for invasion, replication, and development.

Estevez [38, 55] concur that the oxidative stress resulting from intestinal coccidiosis is linked to an imbalance between reactive oxygen species (ROS) and endogenous antioxidants. This result is related to pathological (oocyst count) and/or physiological (body weight gain) conditions that were noted following Eimeria infection. Our finding demonstrated that MyE can indirectly disrupt the metabolism of parasites by increasing the antioxidant defense system, which prevents parasite invasion and hinders the development of Eimeria stages. This result is consistent with that reported by Tsiouris et al. [74], who found that the addition of herbal extracts with high polyphenolic contents increased antioxidant parameters and reduced the infection caused by Eimeria. Corresponding with our findings, Elmoslemany et al. [36] discovered that myrrh possesses polyphenolic compounds with strong antioxidant activity, which significantly lower free radical levels and provide protective effects on intestinal cells.

According to earlier research, a bird’s intracellular essential elements were regulated in a homeostatic regulation [27, 40, 77]. The findings of this study demonstrated that the pigeon group infected with E. labbeana-like parasite had a high mean content of trace elements (Fe, Cu, Cr, Zn, and Ni). This is in line with the findings of Bauerová et al. [29], who found that most pathogenic diseases can alter the levels of many trace elements in an animal’s blood through the disruption of the intestinal cells and liberating the elements into the blood. Since metals are significant metalloproteins that facilitate pathogen adhesion to host cells, trace elements are essential to the pathogenic infection process. When antioxidant levels are insufficient to protect against the increasing amounts of free radicals, these antioxidants might produce oxidative stress by boosting the formation of ROS [46]. MyE reduced the concentration of these elements in the blood plasma, and when this impact was coupled with the elimination of free radicals, the antioxidant status was balanced since phytochemicals influence this homeostasis. Comparable findings of the oxidative stress and metabolic alterations brought on by heavy metals in pigeons have been documented [37, 45, 49].

Conclusion

Our study highlights the encouraging discovery that myrrh extract (MyE) is more effective than amprolium, the reference drug, in treating parasitic Eimeria infection in pigeons. As a result, MyE might serve as a natural alternative to the coccidiostats that are presently available. Further investigation is advised to identify the active myrrh components and examine how they influence the tissues of the pigeons that are afflicted as well as the limitations such as interactions of these compounds with all biomolecules, cells, and tissues need to be adjusted.

Data availability

All the datasets generated or analyzed during this study are included in this published article.

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Acknowledgements

This study was supported by the Researchers Supporting Project (RSP2025R25), King Saud University, Riyadh, Saudi Arabia.

Funding

This study was funded by the Researchers Supporting Project (RSP2025R25), King Saud University, Riyadh, Saudi Arabia.

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Authors and Affiliations

  1. Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia

    Shurug Albasyouni, Afra Alharbi, Esam Al-Shaebi, Saleh Al Quraishy & Rewaida Abdel-Gaber

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  1. Shurug Albasyouni
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Contributions

Conceptualization, R.A.-G. and S.A.Q.; methodology, R.A.-G., S.A. and A.A.; software, R.A.-G., E.M.A.-S. and S.A.; validation, R.A.G., S.A., A.A. and S.A.Q.; formal analysis, R.A.-G., E.M.A.-S. and S.A.; investigation, R.A.-G. and S.A.; resources, R.A.-G. and S.A.; data curation, R.A.-G. and S.A.; writing—original draft preparation, R.A.-G. and S.A.; writing—review and editing, S.A. and R.A.-G.; funding acquisition, R.A.-G. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Rewaida Abdel-Gaber.

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The animal study was approved by the Research Ethics Committee (REC) at King Saud University (approval number KSU-SU-23-45). The study was conducted following the local legislation and institutional requirements. All authors agreed to participate in this study.

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Albasyouni, S., Alharbi, A., Al-Shaebi, E. et al. Efficacy of myrrh extract against Eimeria labbeana-like experimental infection in Columba livia domestica: in vivo study. BMC Vet Res 20, 586 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12917-024-04450-9

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BMC Veterinary Research

ISSN: 1746-6148

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