Research Article

Pathological and Hematological Study for Intestinal Infections with Cestoda and Nematoda in the Domestic Chickens of Thi-Qar Province

Rand K. Abbas1, Zahraa S. Hadi1*, Zainab A. Hussein2, Sajad K. Matooq3

1Department of Biology, College of Education for women, University of AL-Shatrah, Iraq; 2Department of Biology, College of Education for Pure Sciences, University of Thi-Qar, Iraq; 3Department of Animal Production, College of Agriculture and Marshes, University of Thi-Qar Iraq.

Received | May 14, 2024; Accepted | June 19, 2024; Published | September 20, 2024

*Correspondence | Zahraa S. Hadi, Department of Biology, College of Education for women, University of AL-Shatrah, Iraq; Email: Zahra@shu.edu.iq

Citation | Abbas RK, Hadi ZS, Hussein ZA, Matooq SK (2024). Pathological and hematological study for intestinal infections with cestoda and nematoda in the domestic chickens of thi-qar province. Adv. Anim. Vet. Sci. 12(11): 2085-2092.

DOI | https://dx.doi.org/10.17582/journal.aavs/2024/12.11.2085.2092

ISSN (Online) | 2307-8316; ISSN (Print) | 2309-3331

Copyright: 2024 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

INTRODUCTION

Birds are an important source of animal protein in the world; their meat contains many indispensable compounds, such as essential amino acids and vitamins, which are an important source of the B-complex, in addition containing iron and lower cholesterol levels (Al-Aredhi and Al-Mayali, 2020). The common internal parasitic infections occur in poultry include gastrointestinal helminthes (cestodes and nematodes), Raillietina echinobothrida, R. tetragona, R. cesticillus, Davainea proglotina, Choanotaenia infundibulum, Amoebotaenia cuneata, Hymenolepis cantaniana, and H. carioca. These helminthes are among the most significant cestodes of poultry (Shifaw et al., 2021). Raillietina species can cause reduced growth, emaciation, weakness, dullness, emaciation, and convulsions. Additionally some birds showed paralysis and obstruction of the digestive tract. Their larval stage, known as a cysticercoid, is found in a variety of invertebrate intermediate hosts, including small mini-wasps, termites, ants, beetles, and houseflies (Jha, 2019). In poultry, the illness is known as “nodular tapeworm disease,” and the infected birds’ hemoglobin and sugar levels are below average (Jilo et al., 2022).

The most important nematoda found in chicken are Ascaridia galli, Heterakis gallinarum, Capillaria caudinflata, Strongyloides avium, Trichostrongylus tenuis, and Subulura brumpti (Ohaeri and Okwum, 2013). The information on prevalence status, illness control, and future disease trends, which can be predicted using the gastrointestinal parasite infection data, will be helpful for efficient farm management. Understanding a farm’s conditions is essential to creating best practices and preventive initiatives, which in turn makes it easier to pinpoint the variables that influence the prevalence of disease (Wuthijaree et al., 2024). Other significant microscopic changes linked to tapeworm infection include capillary congestion, fibrosis, and proliferation in the gut as well as lymphocytic and eosinophilic infiltrations (Demis et al., 2015). Some common characteristics of village chickens that infected with helminthes include a significant reduction in hemoglobin, villous atrophy, catarrhal enteritis, granuloma formation in the duodenum, desquamation of villi, congestion of sub- mucosal glands, inflammatory response, and vacuolation of epithelial cells (Belete et al., 2016). Helminthes infections are known to cause interference with host metabolism, which results in poor feed utilization and reduced growth rate as well as size and age at maturity (Thyagarajan, 2011; Nnadi and George, 2010; Van et al., 2020). The great danger posed by these worms is caused by the movement of the parasite within the tissues of the body leading to many pathological changes such as diarrhea, infections and weight loss in severe cases (Singh et al., 2021). The severity of symptoms caused by worms depends on the type, number and location of the parasite in the host body (Elmajdoub et al., 2023). Because there haven’t been much research on the subject in Thi-Qar province, the current study aims to identify and diagnose helminthes (cestoda, nematode), as well as determine their impact on certain blood parameters and examine the histological changes in the intestinal tract of domestic chickens.

MATERIALS AND METHODS

Sample of Study

From March 2023 to October 2023, 60 domestic chickens were chosen randomly and bought from the local markets in Thi-Qar Province, which is located in the south of Iraq. Every chicken was brought alive and housed in cages at the biology department/ College of Education for Women/ University of Al-Shatrah.

Blood samples collection and Sample Processing

To study the hematological parameters, blood samples were collected from jugular vein of each chicken, 1 ml of blood was place into a test tube that contain Ethylene Diamine Tetra Acetic acid), tubes then shacked gently. The hematological parameters then were analyzed following (Dacie and Lewis, 1991) description.

Isolation of helminthes

Cervical dislocation was used to sacrifice the chickens. The jugular vein and carotid arteries were then cut. Then the chickens’ intestines were divided into several sections and placed in a sterile petri dish containing 0.9% normal saline physiological solution. The intestines then divided into four parts: esophagus, gizzard, intestine, and cloaca. The four parts were then cut longitudinally, and their content were examined under a stereoscope. The process of searching for intestinal worms begins with the naked eye and using a magnifying glass and dissecting microscope. The micro-needle was also used to isolate the small worms.

After isolating the worms and washing them with distilled water. The cestoda and nematode which removed from the intestine were preserved into vials containing AFA (Alcohol Formalin Acetic acid). The methods outlined by (Gibbons et al., 1996) were used to process the helminths. Regarding cestodes following the process outlined by (Permin and Hansen ,1998), identification was completed once the whole mounts had been dyed. For the overall staining necessary to conduct morphological investigations, aceto alum carbine solution was utilized. For morphological identification, nematodes were positioned on glass slides and submerged in glycerine for a minimum of half an hour. A light microscope with x10 and x40 objective lenses was used to examine the slides (Khalil et al., 2006). These helminths were identified using helminthological keys (Yamaguti, 1959; Yamaguti, 1961; Schmidt, 1986; Calnek et al., 1991).

Hematological analysis

Hemoglobin level determination (HB), Packed cell volume (PCV), red blood cell (RBC) and total count of leukocytes (WBC) were measured using the Cell- Dyn Ruby device, which is an automated multi- scale device designed for diagnostic test in clinical laboratories (Abbott Diagnostic Division, 2008).

Tissue samples collection and histological examination

Following sampling, the checkins were put to death, and the intestinal sections were removed in order to examine the pathological changes. Tissue samples were kept in a 10% formalin solution, subjected to standard histopathological procedures, stained with hematoxylin and eosin, and histologically examined. The histological preparation of the intestine was according to (Bancroft and Steven, 2012).

Statistical analysis

In the current study, chi-square test, t-test, and the mean ± standard deviation (Mean ± SD) were used to investigate the significant differences in the effect of worm infections in chickens All statistical analyses were performed using the statistical software package SPSS V.17.

RESULTS AND DISCUSSION

Isolation of Helminthes

The different helminthes were isolated and identified from the gastrointestinal tracts of the infected chickens obtained in the study area. The parasites recovered consist of four (4) Cestodes and three (3) Nematodes. The cestodes are Raillietina tetragona, Raillietina echinobothridia, Raillietina cesticillus, and Choanotaenia infundibulum. While the nematodes are Ascaridia galli, Heterakis gallinarum, and Capillaria spp. The overall prevalence of gastrointestinal helminthes in the study area as shown in (Table 1) was (86.67 %). The prevalence rates of chicken with cestodes infections were (84.62 %) and (36.54 %) nematodes. There was a statistically significant difference (P<0.05) in the prevalence rates of Cestodes and Nematodes infection.

 

Table 1: Number and percentage of local chickens infected with helminthes.

Tapeworm	Chickens	No. infected	%*
Cestode	60	44	84.62
Nematoda		19	36.54
Total		52	86.67

 

Cal.X2: 0.674, df:1, Tab.X2: 6.53, P. value ≤0.05

 

*Many cases with mixed infection.

The highest infection prevalence was due to Raillietina echinobothrida (71.15%); followed by Hymenolopis cantainana (53.85%) and R.tetragona (38.46%), while R. cesticillus (13.46%) and Choanotenia infundibulum (17.31%) were found to be the least frequently recorded cestode species (Table 2).

Ascaridia galli (28.85%) was the most prevalent Nematode species followed by Heterakis gallinarum (21.15%), Epomidiostomum (7.69%) was the least frequently recorded (Table 3).

Hematological Parameters

Results showed that there is some effect of helimethes on the blood parameters, by decreasing the Hemoglobin level determination (HB) (12.83 ± 1.65), Packed cell volume (PCV) (20.0 2 ± 3.07), red blood cell (RBC) (2.59 ± 0.45) and total count of leukocytes (WBC) (8.96±7.72) (P ≤ 0.05) of chickens infected with tapeworms compared to the control group. While the WBC (8.96±7.72) noticed to be significantly increased in the infected chickens compared to the control group (8.40 ± 3.18). The results of the current study showed significant differences (P value= 0.048) for the percentage of granulocytes (3.65 ± 0.81) when compared with the control group (3.15 ± 0.25). The current study showed a non-significant decrease in lymphocytes (88.38 ± 5.68) compared with the control group (3.15 ± 0.25) as shown in (Table 4).

 

Table 2: Isolated Custody and their incidence in local chickens.

Custody	Infected	%
Raillietina echinobothrida	37	71.15
Raillietina tetragona	20	38.46
Raillietina cesticillus	7	13.46
Choanotaenia infundibulum	9	17.31
Hymenolepis cantainana	28	53.85
Total	44	84.62

 

Cal.X2: 0.572, df:1, Tab.X2: 5.54, P. value ≤0.05.

 

Table 3: Isolated Nematoda and their incidence in local chickens.

Nematoda	Infected	%
Ascardia galli	15	28.85
Heterakis gallinarum	11	21.15
Epomidiostomum	4	7.69
Total	19	36.54

 

Cal.X2: 0.723, df:1, Tab.X2: 6.82, P. value ≤0.05.

 

Gross Pathology

Each bird was between mildly and severely malnourished, with ruffled feathers and signs of diarrhea on the bird’s rear feathers. During the anatomical examination, tapeworms were found in the intestine’s duodenum and jejunum. The white worms, which ranged in length from 15 to 25 cm, produced intestinal blockage in the intestinal mucosa where their anterior ends were firmly attached. There was evidence of mucosal tissue in the colon as well as dark red exudates, or digested blood. The tapeworm produced necrotic foci where their heads adhered to the intestinal wall. Raillietina echinobothrida has an oval-shaped sucker and a retractable, hook-armed rostellum that can reach a maximum length of 25 cm. The scolex of worm is spherical in shape, with short and broad neck, as shown in (Figure 1).

By measuring 10-15 cm long and having rostella hooks, the tapeworms were microscopically identified as Choanotaenia infundibulum. The sucker has an almost circular form. The scolex was found to be triangular in form and pointed anteriorly. The mature segments have a bell-shaped shape, and the neck is thin. Consisting of several ribbon-like body

 

Table 4: The effect of the helimenthes on some blood parameters of infected chickens and controls.

Groups	HB g/dL Mean ±SD	PCV% Mean ±SD	RBC 106/μL Mean ±SD	WBC 103/μl Mean ±SD	LYMPH % Mean ±SD	GRAN % Mean ±SD
Infected chickens	12.83 ± 1.65	20.0 2 ± 3.07	2.59 ± 0.45	8.96±7.72	88.38 ± 5.68	3.65 ± 0.81
Controls	14.9 ± 0.69	32.77 ± 1.26	2.71 ± 0.10	8.40 ± 3.18	88.65 ± 3.39	3.15 ± 0.25
P-value	0.021	0.009	0.034	0.045	0.078	0.048

 

segments that progressively get wider from the front to the back. It has a pale color, completely covered in tegument, elongated, and flat dorso-ventrally. The head section, known as the scolex, the unsegmented neck or growth region, and the body proper, known as the strobila, make up the complete body.

 

Raillietina Cesticillus: This species is easily identified from other birds by its large scolex with a broad rostellum, bright white color, and absence of neck. This massive, powerful tapeworm, which can reach a length of 15 cm, deeply embeds its scolex in the mucosa of the duodenum or jejunum. The unique, broad, flat rostellum has a double row of 300–500 hammer-shaped hooks that operate as a retractable piston, pushing in to the scolex’s outer sleeve and providing the mucosa with a firm grip. It has four feeble, unarmed suckers (Figure 2).

 

Heterakis gallinarum: This small white caecal worm has three tiny, equal-sized lips on its mouth in addition to two lateral membranes that almost completely round its body. The vulvar apparatus is housed in a fully developed bulb at the end of the worm’s distinctive oesophagus. The male, which has long alae with 12 pairs of papillae and a fully formed preanal sucker, is 7–13 mm in length. The left spicule is big and is 0.37-1.9 mm in length, whereas the right spicule is thin and measures 2 mm. The spicules are not equal. About 10 to 15 mm is her length. Its visible vulva is located around midway down the body (Figure 3).

Female Epomidiostomum sp.: Excretory hole, Pharynx, and Vulva region (located from the anterior end of the body). There is a nerve ring, however it is distant from the anterior end. The smooth vulva is situated behind the midsection of the body, a distance from the posterior end. The body visibly narrows behind the anus.

 

 

Histology

Histological examination of many intestinal sections showed heterophilic infiltration together with villi and mucosal gland loss and degradation. Edematous villi associated with cell necrosis. the wall of the small intestine showing fibrosis in lamina muscularis mucosae, with the presence of blood bleeding and inflammatory cells (Figure 5). Erosion and degeneration of the mucosa layer, with the appearance of ulcer and irregularity of the muscular layer (Figure 5), and transformation of the muscle layer into fatty tissue and the complete destruction of all layers of the intestine (Figure 6). Necrosis of the epithelial cells of the mucosa layer, necrosis of the muscle layer, and shedding of the epithelial cells towards the intestinal lumen (Figure 6).

 

Isolation of helimenthes

The general morphological characterizations of Railleitina echinobothrida and Railleitina tetragonain in the current study correspond with previous descriptions (Elmajdoub et al., 2023), recorded this study prevalence rate of infected with tapeworms in local chickens (11%).

The high overall prevalence of infection with gastrointestinal helminthes that were observed in this study (86.6%) confirmed the report of (Afia et al., 2019) that gastrointestinal helminthes in local chicken countries may be close to 100% and, the same percentage was recorded in Kenya (Wamboia et al., 2020). (Mathews et al., 2024), found that the overall prevalence of infection was 87%.

One of factors that may be responsible for the high prevalence rate of gastrointestinal helminthes recorded in this study include a favorable climatic condition which encourages the development of the helminthes, another factor that might be responsible for the high prevalence free feeding, this method allows chickens to roam freely in search of food thereby feeding on insects and other soil dwelling invertebrates (Adekola and Promise, 2023).

 

In this study, Cestode is found to be the most prevalent followed by Nematoda. This data is similar to the reports of (Abah et al., 2019) who recorded a higher prevalence in Cestodes especially Raillietina spp. than Nematodes in their studies. However, these results disagree with (Adekola and Promise, 2023) in Nigeria which found that Nematodes are found to be most prevalent followed by Cestodes. We think that the reason for the high infection rate is consistent with what was mentioned in (Ayeh-Kumi et al., 2016). The reason for this could be attributed to the scavenging habit of local chickens, which involves searching for food in places like soil, drains, dumpsite etc. This behavior could expose them to parasitic organisms thus allowing individual birds to contact one or more forms of gastrointestinal parasites.

The most common Cestode in this study was Railleitina echinobothrida 71.15% higher than other Cestode. This result agrees with (Elmajdoub et al., 2023) in Libya where they found that the infection rate of R. echinobothrida was 54.5%, and (Wamboia et al., 2020) in Kenya reported that the infection rate of R. echinobothrida was 33.3 %. Additionally, (Mathews et al., 2024) mentioned that R. echinobothrida was the most dominant with a prevalence of 72.67%. R. echinobothrida is one of the most common types in domestic chickens (Islam et al., 2020).

A nematode, Ascaridia galli had the highest prevalent rate among other helminthes that was recovered in this study. The result of this study is similar to reports of (Adekola and Promise, 2023) in Nigeria as the commonest and important helminthes of poultry. A. galli infection which causes mild/acute enteritis, hinders vital nutrients absorption and lowers erythropoiesis (Wamboia et al., 2020). Heterakis gallinarum was detected in the small intestine and caecum of 21.15% of chickens, this result was accepted with (Taweya et al., 2020). Epidimiostumum sp. was recorded in experimentally infections of chickens (Al-Mayali, 2009).

Hematological Parameters

The concentrations of Hb, PCV, and RBC were decreased as a result of parasitic’ influence on the hematological parameters. The tapeworms’ cased iron and copper deficiency. Some types of Cestoda penetrate the villi deeply, resulting in hemorrhagic enteritis and necrosis in cases of severe infection. Birds are impacted by intestinal worms because they cause nutritional depletion by removing necessary nutrients from the digestive system (Demis et al., 2015; Berhanu and Dessie, 2014).

Blood loss is caused by a certain kind of Nematoda. Heavy infections are associated with bloody diarrhea and hemorrhagic enteritis. This is most likely the result of multiple factors, particularly a vitamin B12 deficiency, which can cause large but few red blood cells to form, malabsorption, and gastrointestinal blood loss from an infection with intestinal parasites (Belete et al., 2016; Aade and Wankhede, 2022).

This result agreed with (Taweya et al., 2020) in Ethiopia, (Bhure et al., 2011) in India and (Anah et al., 2017) in Al-Diwaniyah city who study the cestode in domestic chickens and their effect on some hematological parameters.

While, the WBCs were elevated in this study it may be an immune reaction against the parasite and the infectious process, and this response in turn may also contribute to reducing the effect of the parasite on the bird and the possibility of bird continuing to live and survive death (Ibrahim, 2013), this result agree with (Bhure et al., 2010) in India and (Anah et al., 2017) in Al-Diwaniyah city. The average rise in lymphocytes between positive and negative chickens (Al-Obaidi, 2011; Al-Abady et al., 2016; Naza et al., 2023) observed a similar finding, The influence of the intestinal and caecal inflammation may be responsible for the increase in the lymphocyte count. Because humeral antibody production, cell-mediated immunity, and immunological response are the main functions of lymphocytes, chronic antigenic stimulation may lead to a significantly increased circulating lymphocyte pool (Taweya et al., 2020).

The proportion of granular blood cells is an indicator of the immune and inflammatory response of chickens infected with tapeworms. According to some studies, tapeworm infection can lead to a decrease in the proportion of total granulose blood cells, which are the cells responsible for fighting parasites and allergies. It is believed that these changes are reflected in the effect of tapeworms on blood and immune functions in chickens, this result agree with (Anah et al., 2017) in Al-Qadisiya.

The study concluded that tapeworms negatively affect blood standards in domestic chickens and reduce their disease resistance and productivity.

Histology

Pathological lesions in the intestines were accompanied by the release of bloody mucus with glaucoma. This may be due to the erosion and migration of these parasites in the intestinal wall and their attachment to the intestinal layers, which makes them easy to move and travel to the deeper layers. This was confirmed by the researcher (Aldiri, 2020).

The worms caused catarrhal enteritis at the site of their attachment inside the intestine, which was accompanied by hyperplasia and the formation of granulomas, which is considered to be of pathological importance because it causes a decrease in the efficiency of intestinal flora in absorbing nutrients, and this was confirmed by researchers (Mushattat et al., 2022).

During histological examination, it was revealed that there was necrosis in the intestinal villi and destruction of epithelial cells where the worm’s head attached. This led to the infiltration of white blood cells in response to the inflammatory reaction, and this is consistent with that reported previously (Yagoob et al., 2017).

Worm toxins can occasionally be secreted together with the secretory and excretory (E/S) products of the worms. These toxins disrupt the intestine’s enzymatic function and make it harder for nutrients to pass through the intestinal membrane. (Shohana et al., 2023).

CONCLUSIONS AND RECOMMENDATIONS

According to the findings of this study, local chicken in Thi-Qar province have a high prevalence rate of gastrointestinal helminthes (cestode and nematode). The infection influenced blood parameters and caused histological changes in the intestinal tract. The frequency and biological variables that have a major impact on the helminth population require more investigation. Consequently, the local chicken’s infection rate will decline. Raising the level of education for breeders of chickens by extending testing and administering the necessary vaccinations to safeguard the birds. Therefore, in order for farmed hens to provide as wholesome food for humans, they must be kept free from parasitic infections.

ACKNOWLEDGEMENTS

The authors sincerely thank the Research Laboratories/Department of Biology, College of Education for Women, University of AL- Shatrah, Iraq, for their infrastructure and technical support.

NOVELTY STATEMENT

The novelty of our research is that it includes studying the effect of parasitic infection in domestic chickens, which are considered an important source of human food, with few studies in Dhi Qar Governorate that include the effect of this infection on blood parameters and tissue changes in infected chickens.

AUTHOR’S CONTRIBUTION

A. RK. Conceptualization. Sample collection, methodology (worms’ isolation and diagnosis, staining), first draft writing.

H. ZS. Sample collection, methodology (worms’ isolation and diagnosis, staining), methodology supervised, first draft writing- editing- and corresponding.

H. ZA. Material preparation and supplies, blood parameters analysis, formal analysis.

M. SK. Sample collection. blood parameters analysis, Histology work.

conflict of Interest

The authors have declared no conflict of interest.

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