Diversity of gastrointestinal parasites of turkeys (Meleagris gallopavo) under different housing systems in Bessarabia, Ukraine

Turkey farming is one of the most intensive and dynamic branches of poultry farming, producing dietary and high-calorie meat and eggs. At the same time, the development of turkey farming is significantly restrained by parasitic diseases, which have become widespread and cause significant economic losses to specialized and homestead farms (Bogach et al., 2016).

The number of breeding and commercial turkey farms in Ukraine has recently decreased somewhat, while the population in backyard farms has increased significantly (Khariv, 2013).

Backyard or rural “family poultry farming” is a form of traditional domestic animal husbandry that requires few resources and includes various types of birds, such as chickens, turkeys, ducks, geese and quails, and is the most traditional and widespread activity in rural communities, as this benefits rural families by providing high-nutrient foods such as meat and eggs, as well as surplus income (Centeno-Bautista et al., 2007; Avilés et al., 2019).

Gastrointestinal (GI) parasites are considered a major problem in poultry production, leading to economic losses due to reduced productivity, feed digestibility and poor weight gain, reduced egg production, anorexia, diarrhea, intestinal obstruction, emaciation, anemia, paralysis, poor plumage and even deaths (Jegede et al., 2015; Divyamery et al., 2016; Balarabe et al., 2017).

Parasites commonly infect various bird species’ gastrointestinal tracts, such as helminths and protozoa (Bayzid et al., 2023).

Helminth parasites of poultry are usually cestodes, nematodes, and trematodes, among which nematodes are considered the most important group in terms of the number of species and the damage they cause. Only a small number of cestodes and trematodes are known to parasitize domestic and wild birds (McJunkin et al., 2003; Udoh et al., 2014; Goria et al., 2018).

Eimeria is a major gastrointestinal protozoan affecting all poultry species (Lawal et al., 2016; El-Shall et al., 2022). Young birds affected by gastrointestinal parasites show severe clinical disease. In contrast, adult birds can sustain the parasitic infection and act as a reservoir to maintain continuous environmental contamination and circulation of the infestation among all bird species (Singh et al., 2017).

Histomonas meleagridis is a flagellate protozoan parasite that inhabits the caecum of poultry and causes high mortality in turkeys, sometimes approaching 100 % of the flock (McDougald et al., 2005). Although PCR confirmed the presence of the parasite in most tissues of infected birds, the caecum and liver appeared to be the most favorable sites (Huber et al., 2006).

Cryptosporidium baileyi is a zoonotic pathogen that causes respiratory symptoms in chickens for which no effective control measures currently exist (Wu et al., 2021). C. baileyi and C. meleagridis usually cause cryptosporidiosis in chickens and/or turkeys. C. baileyi is generally the most common species in poultry, causing respiratory and intestinal infections (including histopathological changes in the bursa of Fabricius) (Ramirez et al., 2004).

Tetratrichomonas gallinarum is known as one of the protozoan organisms that parasitizes the caecum of chickens (Amin et al., 2014) and turkeys (Hauck et al., 2010).

There are many reasons for disease occurrence. The timely identification of the disease pathogen is essential. The time spent on making a laboratory diagnosis of the disease and delivering the research results to poultry owners often exceeds the time required to develop the invasive process in poultry flocks. It does not allow the necessary measures to be taken in time (Bogach et al., 2021). Therefore, the study of the variety of pathogens and the prevalence of gastrointestinal invasions in relation to turkeys’ age and housing system is relevant.

The aim of the research is to study the distribution patterns and diversity of gastrointestinal parasites in turkeys of different age groups were kept in poultry houses and under a cage-pasture management systems.

The research program was reviewed and approved by the bioethics commission of the National Research Center “Institute of Experimental and Clinical Veterinary Medicine.”

The entire experimental part was carried out in compliance with the international principles of the European Convention “On the Protection of Vertebrate Animals Used for Experiments and Other Scientific Purposes” (Strasbourg, 1985; Simmonds, 2018; Kabene & Baadel, 2019; Festing & Wilkinson, 2007).

In turkeys of different age groups, which were kept in a poultry house, the total infestation with endoparasites was 59.8 %. The extensiveness of endoparasitoses in turkeys 30 – 60 days old was 67.7 %, turkeys 90 – 120 days old – 67.9 %, turkeys 150 – 180 days old – 57.7 %, and adult birds older than one year - 23.0 %. Turkeys 30 – 60 days old were most affected by protozoa - 51.8 %, while nematode infection was 14.8 % and only 1.1 % by cestodes (Table 1).

Nematodes were detected in 31.7 % 90 – 120 days old turkeys, protozoa in 28.0 % of turkeys, and cestode infestation increased to 8.1 %, compared to 30 – 60 days old turkeys. The damage caused by nematodes 150 – 180 days old in turkeys was the greatest and amounted to 32.2 %. Protozoans were 14.0 %, and cestodes 11.3 %. Adult 360-day-old turkeys and older were most affected by nematodes (16.1 %), and only 9.3 % of the birds were infested with protozoans and 5.5 % with cestodes.

When turkeys of different age groups were kept on pasture, the total infestation by endoparasites was 63.3 %. Infestation 30 – 60 days old of turkeys by endoparasites was 56.4 %, 90 – 120 days old 71.3 %, 150 – 180 days old 68.7 %, and 360 days old 45.4 %. It was established that 35.2 % of turkeys aged 30–60 days were infested with protozoans, 16.8 % with nematodes and 4.4 % with cestodes (Table 2).

Turkeys 90 – 120 days old were affected by nematodes (30.1 %,) protozoans (22.3 %), and cestodes (17.9 %). The extent of damage to turkeys 150 – 180 days old was high, with cestodes 27.9 %, nematodes 27.5 %, and protozoans only 13.3 %. Adult 360-day-old turkeys and older were also mostly infested with cestodes (18.5 %) and nematodes (17.6 %). Infestation with protozoans was 9.3 %.

In 30–60 days old of turkeys that were kept in poultry houses, the lesions of Histomonas meleagridis were registered on 5.9 % more, Cryptosporidium baileyi and Eimeria spp. on 4.7 % and 4.3 %, respectively, than in free-range turkeys. The prevalence of cestodes Davainea meleagridis and Raillietina echinobothrida, a potentially pathogenic parasite in turkeys, was very low (less than 2.4 %) (Graph 1).

Graph 1.

Prevalence of endoparasites in turkeys 30 – 60 days old in the Bessarabia in 2023.

When keeping 90 – 120 days-old turkeys in the poultry house, H. meleagridis was 7.5 % higher than in free-ranging turkeys. H. gallinarum eggs were recorded at almost the same level, while R. echinobothrida was higher at 5.6 %, D. meleagridis at 4.2 % and A. dissimilis at 3.3 % (Graph 2).

Graph 2.

Prevalence of endoparasites in turkeys 90 – 120 days old in the Bessarabia in 2023.

It was visually established that in the intestinal form of histomonosis, the wall of the caecum was unevenly thickened due to edema hyperemic with individual dotted and striped hemorrhages (Fig. 2). In the fundal part of the cecum, mushroom-like and nodular formations of various shapes and sizes were found, clearly distinguished above the surface of the mucous membrane. In some cases, these formations merged with each other and formed a so-called solid “cheesy” mass. Damage to its integrity, as well as minor dotted and streaked hemorrhages, were observed in places where the cheesy mass was tightly attached to the intestinal mucosa.

Fig. 2.

Inflammation of the caecum with perforation of the wall during the acute course of histomonosis in turkeys 90 – 120 days old.

Penetration of histomonads into blood vessels led to a violation of hemodynamics in the intestinal wall due to the formation of blood clots and a violation of the permeability of the vascular wall, which led to hyperemia and hemorrhages in the mucous membrane, as well as to severe swelling of the submucosal layer.

In the hepatic form of histomonosis, pronounced patho-anatomical changes were recorded, characterized by noticeable grayish-white nodules, the size of which is from a millet grain to a pea (Fig. 3).

Fig. 3.

Miliary necrosis of the liver during the chronic course of histomonosis in turkeys 90 – 120 days old.

Such nodules had clear boundaries between healthy liver tissue and slightly protruded on the surface of the capsule, which penetrated deeply into the liver parenchyma. The edges of the liver are slightly rounded, have a flabby consistency, and the capsule is tense.

At the pathological autopsy of turkeys affected by A. dissimilis, from 9 to 35 nematodes were recorded, as well as thickening and swelling of the small intestines (Fig. 4).

Fig. 4.

The small intestine of 90 – 120 days old turkey infected with Ascaridia dissimilis.

The course of the disease was characterized by catarrhal-dystrophic and destructive processes, accompanied by a pronounced vascular reaction, hemorrhages and desquamation of the covering epithelium. A significant accumulation of lymphoid tissues was recorded at the base of the mucous membrane.

In turkeys 150 – 180 days old, infestation by protozoa significantly decreased, regardless of the housing system (Graph 3).

Graph 3.

Prevalence of endoparasites in turkeys 150 – 180 days old in the Bessarabia in 2023.

The extensiveness of H. gallinarum differed by only 1 %, while the infestation in free-ranging turkeys on D. meleagridis cestodes increased by 8.7 % and R. echinobothrida by 7.9 %.

Cryptosporidium baileyi oocysts were not recorded in adult turkeys 360 days old and older (Graph 4).

Graph 4.

Prevalence of endoparasites in turkeys 360 days old and older in the Bessarabia in 2023.

The extensiveness of Eimeria spp. and T. gallinarum was very low (less than 2.7 %). H. gallinarum nematode infestation of turkeys in the poultry house was only 1.9 % higher than by free-ranging, while A. dissimilis infestation of poultry was, on the contrary, 2.1 % higher. Also, in free-ranging turkeys, infestation to D. meleagridis increased by 6.8 % and R. echinobothrida by 5.8 %, compared to birds kept in a poultry house.

When dissecting the turkey’s small intestine, 18 cestodes of R. echinobothrida were recorded (Fig. 5).

Fig. 5.

The small intestine of a 360-day-old turkey infected with Raillietina echinobothrida.

The main pathomorphological changes in raietinosis were characterized by a violation of the integrity of villi and crypts in the small intestine of turkeys, as well as the formation of parasitic nodules in the places of fixation of cestodes. In the place of fixation of R. echinobothrida, the tissues of the intestinal wall were compacted and necrotic.

In the case of Davainea meleagridis, turkeys’ damage, inflammation and mucous membrane thickening were recorded in the small intestines (Fig. 6).

Fig. 6.

The small intestine of a 360-day-old turkey infected with Davainea meleagridis.

The small intestine’s mucous membrane was bright red, and spot hemorrhages were recorded in some of its areas. Fibrinous layering was recorded on the mucous membrane, sometimes with blood impurities on the wall and a large amount of mucus in the intestines’ lumen.

Statistical data show that more than 90.0 % of the turkey population in Ukraine use walking areas and pastures where birds of different ages and species categories are kept together. Contact with other domestic and wild birds significantly spreads invasive diseases (Bogach, 2010).

Poultry kept in cages is always highly susceptible to intestinal parasitic infections, especially protozoa and nematodes, which are the most common (Peng et al., 2021).

Indoor poultry support is widely used, as it is believed that a higher infection rate is recorded in an extensive system of housing (21.46 %) compared to a semi-intensive system (6.82 %) (Agmas et al., 2022).

Parasite prevalence in captive birds is directly proportional to cage sanitation and affects endoparasite populations at high densities (Hasan et al., 2018). According to our results, the total infestation of turkeys with endoparasites in cages was 59.8 %, while Mohammed et al. (2017) reported 40 % of gastrointestinal infections in turkeys in Abuja, Nigeria.

The total percentage of turkeys infected with gastrointestinal parasites in Erbil city was 35.21 %. Five species of nematodes were registered: Heterakis gallinarum 28 %, Capillaria spp. 24 %, Trichostrongylus spp. 16 %, Strongyloides avium 12 % and Ascaridia galli 4 %. In addition, Eimeria spp. was diagnosed with an infection rate of 48 % (Khalaf et al., 2022).

In northern Iran, in the city of Amola, 75 % of slaughtered turkeys were infected with nematodes, cestodes and trematodes, namely 20 % Capillaria, 51 % A. gali, 8 % R. tetragona, 8 % R. echinobothrida and 11 % Echinostoma (Banadory et al., 2014).

Our data shows no Cryptosporidium baileyi oocysts were recorded in adult turkeys 360 days old and older. Instead, 10.3 % of turkeys were infected with Heterakis gallinarum and 10.2 % of birds were infected with Davainea meleagridis.

The level of infection in poultry is related to differences in environmental conditions, climatic, seasonal and meteorological variations, the number of birds examined, the types of breeding and rearing, and the diagnostic methods used (El-Sayed et al., 2020).

Endoparasites strongly influence birds’ behavior and ecological interactions (Abdu et al., 2022). In poultry, A. galli, C. annulata and H. gallinarum are considered the main parasites that spread invasive diseases such as ascariasis and cestodosis (Al-Badrani et al., 2023). A. galli is a highly pathogenic and widespread parasite worldwide (Faraj et al., 2020) in poultry species such as pigeons, turkeys, and chickens, which leads to reduced growth and egg-laying rates of birds, ultimately causing significant economic losses in poultry farming (Ara et al., 2021).

Parasitic nematode species commonly cause severe infections of birds’ gastrointestinal tracts (Al-Quraishi et al. 2020). Hasan et al. (2018) also reported A. galli in turkeys with an extent of 12.5 %, almost similar to the prevalence recorded in our study at 11.8 %. They recorded 25 % of E. maxima cases in turkeys, while we recorded a maximum rate of 11.5 % in turkeys 30–60 days old when kept in a poultry house.

A. galli is a widespread nematode that is a common problem for poultry health (Yousaf et al., 2019). The nematode Ascaridia causes an increase in feed conversion ratio and suppression of the immune system, leading to increased co-morbidities in poultry (Wongrak et al., 2014).

Raillietina echinobothrida is one of the most common pathogenic tapeworms worldwide, which causes distinct intestinal nodules in their hosts (Al-Marsomy et al., 2016; Bogach et al., 2020).

In Punjab, Pakistan, turkeys were infested with R. echinobothrida (78 %), A. galli (69 %), Capillaria annulata (59 %), C. anatis (53 %), E. maxima (43 %), H. gallinarum (36 %), H. meleagridis (28 %) (Saim et al., 2023).

The pathogenesis of histomonosis begins with colonization of the cecum by the parasite, which leads to severe inflammation and necrosis. After destroying the intestinal tissue, the parasite can enter the blood vessels and reach the liver through the portal veins. As a result, inflammation and destruction may occur in the liver. In the final stage, the disease can become systemic when the parasite spreads to different organs of the bird (Grabensteiner et al., 2023).

Because the parasite multiplies efficiently in infected birds, intra-flock transmission can occur rapidly, as demonstrated experimentally (Landman et al., 2015). Recent research demonstrated that histomonosis could spread rapidly through a flock of turkeys by direct contact, probably involving the phenomenon of cloacal drinking (McDougald, 2005). In any case, the bioprotection effect against introducing histomonads depends on the housing system. It is very limited in free-range flocks or poultry houses that cannot be completely closed (Liebhart et al., 2017).

Turkeys infected with H. meleagridis had significantly enlarged cecum with thickened walls and their lumens filled with fibrinous material, as well as swollen livers with numerous rounded areas of necrosis, with the entire liver affected in most cases (Hess et al., 2006). In broiler turkeys infected with H. meleagridis, sudden death was observed at the end of the 5th week without specific clinical signs. An autopsy of 15 affected turkeys revealed severe caecal lesions characterized by thickening of the caecal walls filled with necrotic and caseous material. In addition, multiple cecal tears and necrosis were observed, along with localized peritonitis (Grafl et al., 2011).

A large number of outbreaks of histomonosis on standard turkey farms in France have been reported in birds between four and eight weeks of age, but there have been cases in three-week-old birds and some in birds under 17 weeks of age (Callait-Cardinal et al., 2010). Some species of Eimeria that can infect turkeys include Eimeria meleagridis, E. meleagrimitis, E. dispersa, E. gallopavonis, E. adenoids, and E. innocua. Infection with E. adenoids and E. meleagrimitis can cause malabsorption, reduced feed intake, reduced growth, dehydration, poor feed conversion and high mortality (Chapman, 2008).

According to our data, 11.5 % of turkeys 30 – 60 days old in poultry houses and 7.2 % in free-ranging conditions were infested with Eimeria spp.

Samples of the genus Eimeria spp. were present in 100 % of the gastrointestinal tract of turkeys; the more significant number of oocysts was in the large intestine (88 %) and in the small intestine - only 12 % (Martinez-Guerrero et al., 2010).

In a commercial herd, turkeys were infected with moderate levels of A. dissimilis but not H. gallinarum. Compression smears from liver tissues showed the typical histotrophic phase of H. meleagridis, while smears from the caecum showed abundant Trichomonas gallinarum (Norton et al., 1999).

Endogenous stages of development of Cryptosporidium meleagridis were detected in 42.6 % of turkeys in the Central Czech Republic. Asexual stages (meronts at various stages of development) were first sporadically observed in 23-day-old birds. The maximum number of infected turkeys (63.3 %), in which all stages of development of C. meleagridis were localized, primarily in the ileum and caecum, were aged 30 – 39 days (Pavlásek, 1994).

According to our research, when turkeys 30–60 days old were kept in poultry houses, C. baileyi was recorded in 11.5 % of birds, while on farms in Algeria, 13 % of broiler turkeys were infected with C. meleagridis (Laatamna et al., 2017).

A large gathering of poultry in limited areas, violations of feeding and keeping of poultry, and changes in temperature, humidity and other parameters of the external environment lead to a decrease in the protective barrier of poultry, the development of many infections and invasions due to the activation of opportunistically pathogenic microflora and potential conditions for the development of bacterial, viral and endoparasitic diseases (Cadmus et al., 2019).

Therefore, knowledge about the distribution, extensiveness and intensity of gastrointestinal parasites in turkeys is a fairly well-argued indicator when planning and carrying out treatment and preventive measures.

The distribution and intensity of endoparasitoses in turkeys is affected by the bird’s age and type of keeping. It has been proven that in Bessarabia (Ukraine), endoparasites of turkeys are pretty common invasive diseases, the causative agents of which are Histomonas meleagridis, Eimeria spp., Cryptosporidium baileyi, Tetratrichomonas gallinarum, Ascaridia dissimilis, Heterakis gallinarum, Capillaria spp., Davainea meleagridis and Raillietina echinobothrida.

When turkeys were kept in poultry houses, 51.8 % of poults aged 30 – 60 days were affected by protozoans, while 31.7 % of turkeys aged 90 – 120 days, 32.2 % of turkeys aged 150 – 180 days, and 16.1 % of turkeys aged 360 days and older were infested with nematodes.

Under a cage-pasture management system, 35.2 % of poults aged 30 – 60 days were affected by protozoans, 30.1 % of turkeys aged 90 – 120 days, and 27.5 % of turkeys aged 150 – 180 days were infested with nematodes, and 18.5 % of turkeys aged 360 days and older were affected by cestodes.

In acute histomonosis in turkeys, lesions of the cecum with perforation of the intestinal wall are observed, while in chronic cases, liver lesions with necrotic foci develop.