Research Article

Prevalence of Natural Gastrointestinal Helminth Infection of Thai Indigenous Chickens Aged 12–18 Weeks in Small–Scale Chicken Farms on River Plains in Central Thailand

Kunlayaphat Wuthijaree1, Pattaraporn Tatsapong1, Sukanya Yung-Rahang2, Prayad Thirawong2, Koonphol Pongmanee2*

1Faculty of Agriculture, Natural Resources and Environment, Naresuan University, Phitsanulok 65000, Thailand; 2Department of Animal Science, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Kamphaeng Saen Campus, Nakhon Pathom 73140, Thailand.

Received | November 25, 2023; Accepted | January 21, 2024; Published | February 23, 2024

*Correspondence | Koonphol Pongmanee, Department of Animal Science, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Kamphaeng Saen Campus, Nakhon Pathom, Thailand; Email: koonphol.p@ku.th

Citation | Wuthijaree K, Tatsapong P, Yung-Rahang S, Thirawong P, Pongmanee K (2024). Prevalence of natural gastrointestinal helminth infection of thai indigenous chickens aged 12–18 weeks in small–scale chicken farms on river plains in Central Thailand. Adv. Anim. Vet. Sci. 12(4): 693-702.

DOI | https://dx.doi.org/10.17582/journal.aavs/2024/12.4.693.702

ISSN (Online) | 2307-8316

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

Indigenous chickens can easily be infested with both gastrointestinal and blood parasitic pathogens (Opara et al., 2014; Takang et al., 2017). Gastrointestinal helminth parasites are a significant impediment to the productive performance of free–range and backyard chicken farming around the world (Jeni et al., 2021). Gastrointestinal helminths have the potential to serve as vectors for transmitting pathogens (such as Histomonas meleagridis) that cause avian blackhead disease (McDougald, 2005; Marchiondo et al., 2019). However, these helminths can serve as vectors and cause secondary infections, such as by Escherichia coli (McDougald, 2005; Permin et al., 2006) and Salmonella enterica (Shohana et al., 2023). Helminthiasis stands out as one of the prevalent diseases frequently encountered, affecting scavenging chickens (Soulsby, 1976). Environmental factors (for example, rainfall, humidity, and ambient temperature) can have a major impact on the occurrence of helminth infective stages (Chilinda et al., 2020; Van et al., 2020; Shifaw et al., 2021, Kerroucha et al., 2022). The parasites are ingested directly by the scavenging chickens through contaminated feed, water, or soil, or indirectly through the consumption of invertebrates (intermediate hosts) such as snails, earthworms, or others that may transport the eggs (Soulsby, 1976; Shifaw et al., 2021). Parasitic infections interfere with the digestive system and nutrient metabolism in chickens. The presence of worms has a negative effect on feed efficiency and overall chicken performance (Yazwinski et al., 2013; Van et al., 2020). Helminth infections can cause seriously affect chicken health and behavior (Gauly et al., 2007), resulting in the manifestation of both clinical and subclinical diseases, overall decreased productivity and economic loses (Gauly et al., 2005; Daş et al., 2010; Singh et al., 2021).

Sam Leuang, Tapaotong, and Sam Leuang × Tapaotong crossbred chickens are slow–growing indigenous breeds, commonly reared by Thai smallholder farmers using family labor under free-range, non-intensive or backyard conditions in the central Thailand. Generally, male and female indigenous chickens are collectively reared until they reach to market weight of 1.5–1.7 kg (Choprakarn and Wongpichet, 2007; Yung-rahang et al., 2017) at a slaughter age of 12–16 weeks (Jaturasitha et al., 2008; Yung-rahang et al., 2017). Indigenous chicken meat has a better flavor and taste than commercial broiler meat; consequently, it can fetch a higher price. Therefore, people in central Thailand continue to raise and maintain the breeding stock of indigenous chickens for local market consumption. However, the present research on gastrointestinal helminth infections in indigenous chickens in Thailand exhibits deficiencies, particularly in comprehensive data regarding prevalence and geographic distribution. Although there have been investigations into the presence of gastrointestinal helminths in indigenous chickens in the northern, northeastern, and southern of Thailand, (Kunjara Na Ayudthaya and Sangvaranond, 1993, 1997; Butboonchoo and Wongsawad, 2017), there is no published information in central Thailand. The objective of this study was to determine the infection rate of gastrointestinal helminths, identify helminth parasite species in male and female indigenous chickens of different ages, and estimate the correlation between age at slaughter and helminth infection in Thai native chickens reared in free-range backyard production systems in central Thailand. These results may provide useful epidemiological data on specific helminths in indigenous chickens in central Thailand.

MATERIALS AND METHODS

Ethical Statement

All chickens included in this study were naturally infected and all procedures performed adhered to the applicable guidance of the World Association for the Advancement of Veterinary Parasitology for Poultry. This study was carried out following the approved protocol by the Animal Care and Use Research Ethics Committee of Kasetsart University, Bangkok, Thailand (Approval No. ACKU63–AGK–002).

Study Area

The study was conducted in three selected districts in central Thailand: Kamphaeng Saen (13°59′ N; 99°59′ E) and Don Tum (13°57′ N; 100°4′E) districts, Nakhon Pathom province; and Song Phi Nong district (14°13′ N; 100°1′ E), Suphan Buri province. Both provinces are dominated by floodplains and their main agricultural products consist of rice and livestock, including chickens and pigs. The climate is tropical and characterized by hot summers (mid-February to mid-May) and cold, wet winters (mid-October to mid-February). Typically, the total annual rainfall is 127–942 mm, with the rainy season occurring take place mid-May until mid-October. The annual precipitation is 200–350 mm, reaching its highest point in August to September. The average temperature is 28.7°C, with little seasonal variation (Thai Meteorological Department, 2019). All three selected districts were in the low river plains zone at an altitude of 4.74–7.25 m above sea level. This study was conducted between June and December 2019.

Experimental Animals And Diets

In total, 229 Sam Leuang × Tapaotong one-day-old mixed-sex chicks were obtained from the Department of Animal Science, Kasetsart University, Kamphaeng Saen Campus, Thailand. All of the chick received a vaccination for Marek’s disease on the first day. The chicks were randomly allocated to three groups and delivered to one small-scale chicken farm in each of the three selected study areas. At each farm, chicks were kept according to routine management practices in an optimum hygienic environment until the age of 2 weeks; subsequently, they were raised under free-range conditions. The birds were fed corn–soy-based diets providing 21% protein and 3,100 kcal/kg of metabolizable energy during the first 4 weeks and 18% protein and 2,900 kcal/kg metabolizable energy after 4 weeks. No veterinary treatments were administered during the study. The feed intake was not measured. Live body weights were recorded on the day of slaughter.

Chicken Population And Sample Size

The sample size was determined using the methodology outlined by Thrusfield (2005). Given the parasites’ unknown prevalence, an approximate value of 50% was used to determine the maximum sample size. Considering a desired absolute precision of 10% with a confidence level of 95%, it was determined that a minimum sample size of 96 chickens was necessary. In total, 229 chickens were obtained after considering natural mortality and escape.

Sampling Methods And Parasitological Measurements

At 12, 14, 16, and 18 weeks of age, 15–20 birds of the same age from each farm were randomly chosen and examined for the prevalence of worms and average amount of worms per chicken (worm burden). Feed was withdrawn 10 h before slaughter but drinking water was available. On the day of slaughter, the body weight of the selected chickens was measured, the trachea and gastrointestinal tract were removed, and helminths were investigated. The gastrointestinal tract of each chicken was dissected into distinct sections, including the proventriculus, gizzard, small intestine (consisting of the duodenum, jejunum, and ileum), and cecum. Each section was longitudinally dissected and rinsed with tap water, adhering to the protocols outlined by the World Association for the Advancement of Veterinary Parasitology (Yazwinski et al., 2003). The intestinal mucosa and contents of the digestive tract were carefully removed to extract the adherent parasites present in the mucosa. The residue from each sample was rinsed with distilled water using a 100-μm mesh screen and then moved to a Petri dish. The remaining worms were isolated using a stereomicroscope (Leica model M26, Germany) after all visible parasites were collected. The identification of all helminth species was conducted using characteristics of morphology, as outlined by Soulsby (1976), McDougald (2008), and Yazwinski and Tucker (2008). The sex of all mature A. galli and H. gallinarum worms was identified using the approach described by Yazwinski and Tucker (2008). Additionally, the presence of helminths was examined in the proventriculus and gizzard. This study used a light microscope with magnifications ranging from 10x to 100x for cestode species identification. The identification is based on their morphological characteristics, as outlined by McDougald (2008), Yazwinski and Tucker (2008) and Soulsby (1976). The Mello-Campos approach was adapted for the cestode identification process, as described by Silva et al. (2016).

Statistical Analysis

The statistical analysis was performed using R software (R Core Team, 2019). The prevalence of each parasite species was determined by calculating the ratio of chickens infected with a particular parasite to the total number of chickens (Thrusfield, 2005). The prevalence of mixed helminth infections and individual helminth species was ascertained using the frequencies. Infection intensity was determined by calculating the mean number of worms harbored by a particular parasite species. To determine the sex ratio of each helminth species, the total number of female worms was divided by the number of male worms. The Kolmogorov-Smirnov test was employed to assess the normality of the distribution of quantitative variables before analysis. The correlations between different parasitological parameters within the nematode species were determined using Spearman’s correlation coefficients. The data regarding the number of worms present has been analyzed using a general linear model, with the fixed effects of host sex (male versus female) and age at slaughter (12, 14, 16, and 18 weeks) and the random effects of the farm. The results are presented as mean value and standard deviation (SD). Differences in the prevalence of worm species depending on host sex and age at slaughter were analyzed using the chi-square test, and differences in worm burden were analyzed using the t-test. The confidence level was set at 95% for all analyses, and differences were considered significant at P≤0.05.

RESULTS

Body Weight, Infection Rate, And Parasite Diversity Of Indigenous Chickens

The body weights of the indigenous chickens increased with age. The mean body weight at the age of 12 weeks was 1,324 g. Body weight increased gradually at 14 weeks (1,407 g), peaked at 16 weeks (1,768 g), and remained constant until 18 weeks (1,755 g) (Figure 1). Of the 229 chickens, 183 (79.9%) were subjected to infection by at least one species of helminth. (Table 1). Nematodes were found in 72.1% of chickens, with a mean ± SD burden of 7.41 ± 12.81 (ranging from 0 to 78) worms per chicken. H. gallinarum emerged as the predominant nematode species, accounting for 70.3%, succeeded by A. galli at 14.8% and Capillaria spp. at 6.6%. Cestodes were detected in 34.5% of the chickens. In terms of cestodes, the prevalence of Raillietina cesticillus, Raillietina echinobothrida, Raillietina tetragona, Amoebotaenia cuneata, Choanotaenia infundibulum, Hymenolepis carioca, and Hymenolepis cantaniana was 29.7, 18.8, 12.2, 9.6, 9.2, 8.7, and 8.3%, respectively (Table 1). All helminths were retrieved from the gastrointestinal tract, with none identified in the trachea. Among the chickens, 45.4% exhibited infection with a single helminth species, whereas 34.5% were demonstrated infection with two or more helminth species (Table 2). The indigenous chickens exhibited no discernible clinical signs of disease throughout the study.

Prevalence Of Gastrointestinal Parasites By Sex

Table 1 displays the overall prevalence of the identified species categorized by host sex. The examination of helminth distribution within host sexes revealed that the prevalence

 

Table 1: Overall and host sex-dependent prevalence of helminth species (N = 229) and the odd ratios (Ψ) to show the probability of a female being infected compared with a male.

Species	Prevalence of helminth infection (%)			Gender effect (Pr > ChiSq)	Ψ
	Overall (N = 229)	Female (N = 116)	Male (N = 113)
Nematodes	72.1	69.8	74.3	0.447	1.25
A. galli	14.8	14.7	15.0	0.934	1.03
H. gallinarum	70.3	68.1	72.6	0.460	1.24
Capillaria spp.	6.6	6.9	6.2	0.830	0.89
Cestodes	34.5	39.7	29.2	0.096	0.63
A. cuneata	9.6	10.3	8.8	0.701	0.84
H. carioca	8.7	9.5	7.0	0.684	0.83
H. cantaniana	8.3	9.5	7.1	0.510	0.73
R. cesticillus	29.7	34.5	24.8	0.108	0.63
C. infundibulum	9.2	10.3	8.0	0.533	0.75
R. echinobothrida	18.8	19.8	17.7	0.680	0.87
R. tetragona	12.2	11.2	13.3	0.633	1.21
Trematodes	4.4	5.2	3.5	0.546	0.67
Echinostoma revolutum	4.4	5.2	3.5	0.546	0.67
Total	79.9	77.6	82.3	0.373	1.34

 

Table 2: Prevalence of different parasites in indigenous chickens on river plains in central Thailand by genera

Parameters		Parasitic infection (%)		Nematodes	Cestodes	Trematodes
		Single infection	Multiple infection
Age	12 weeks (N)	46.0 (23)	10.0 (5)	40.0 (20)	22.0 (11)	2.0 (1)
	14 weeks (N)	46.9 (30)	37.5 (24)	78.1 (50)	35.9 (23)	6.3 (4)
	16 weeks (N)	44.8 (26)	39.7 (23)	77.6 (45)	41.4 (24)	5.2 (3)
	18 weeks (N)	43.9 (25)	47.4 (27)	87.7 (50)	36.8 (21)	3.5 (2)
Sex	Male (N)	52.2 (59)	30.1 (34)	74.3 (84)	29.2 (33)	3.5 (4)
	Female (N)	38.8 (45)	38.8 (45)	69.8 (88)	39.7 (46)	5.2 (6)
Total (N)		45.4 (104)	34.5 (79)	72.1 (165)	34.5 (79)	4.4 (10)

 

Table 3: Parasitological parameters of indigenous chickens infected with gastrointestinal parasites at the age of 12, 14, 16, or 18 weeks (Mean ± SD)

		Age				p value
		12 weeks N=50	14 weeks N=64	16 weeks N=58	18 weeks N=57
A. galli	Infected, % (N)	2.0b (1)	20.3a (13)	17.2a (10)	17.5a (10)	0.035
	Total worm burden	0.02±0.14	1.61±5.96	1.03±4.36	1.79±6.40	0.258
	Number of female worms	0.02±0.14	0.50±2.15	0.45±2.18	0.81±4.91	0.581
	Number of male worms	0	0.30±1.14	0.29±1.74	0.23±0.78	0.490
	Number of larvae	0	0.81±3.31	0.29±0.96	0.75±3.61	0.286
	Sex ratio (F:M)	-	0.98±1.01	0.74±0.65	6.82±14.83	0.523
H. gallinarum	Infected, % (N)	40.0b (20)	73.4a (47)	75.9a (44)	87.7a (50)	<0.001
	Total worm burden	1.30±2.25c	6.86±10.58b	2.81±3.15c	11.95±16.54a	<0.001
	Number of female worms	0.07±1.57c	3.94±7.92b	1.41±1.74c	6.23±8.42a	<0.001
	Number of male worms	0.52±1.23b	2.16±3.40b	0.93±1.45b	4.61±7.83a	<0.001
	Number of larvae	0.08±0.44b	0.77±1.64a	0.47±1.11ab	1.11±2.54a	0.011
	Sex ratio (F:M)	1.17±1.28	1.71±2.11	1.11±1.21	1.98±2.01	0.239
Capillaria spp.	Infected, % (N)	0 (0)	9.4 (6)	10.3 (6)	5.3 (3)	0.119
	worm burden	0	0.80±3.34	0.21±0.64	0.33±1.43	0.150
Nematodes	Incidence, % (N)	40.0b (20)	78.1a (50)	77.6a (45)	87.7a (50)	<0.001
	worm burden	1.32±2.27c	9.27±13.53b	4.05±6.08c	14.07±18.07a	<0.001
Tapeworms	Infected, % (N)	22.0 (11)	35.9 (23)	41.4 (24)	36.8 (21)	0.182
	worm burden	0.40±1.12	2.00±5.20	3.37±8.35	2.32±5.24	0.076
Trematodes	Infected, % (N)	2.0 (1)	6.3 (4)	5.2 (3)	3.5 (2)	0.704
	worm burden	0	0.13±0.68	2.74±18.63	0.02±0.13	0.325
total	Infected, % (N)	56.0b (28)	84.4a (54)	84.5a (49)	91.2a (52)	<0.001
	worm burden	1.77±2.55b	11.19±16.08a	10.05±21.86a	16.40±18.82a	<0.001

 

a–c means with different superscripts are significantly different (P≤0.05)

 

Table 4: Correlation between the different parameters in indigenous chickens infected with gastrointestinal parasites

	Age	A. galli	H gallinarum	Capillaria spp.	Nematodes	Cestodes	Trematodes	Worm burden
Age	-	0.12	0.36**	0.06	0.36**	0.18**	0.02	0.38**
A. galli	0.12	-	0.20**	0.52**	0.39**	0.19**	0.09	0.37**
H. gallinarum	0.36**	0.20**	-	0.19**	0.97**	0.14*	0.02	0.86**
Capillaria spp.	0.06	0.52**	0.19**	-	0.34**	0.19**	0.07	0.33**
Nematodes	0.36**	0.39**	0.97**	0.34**	-	0.19**	0.06	0.90**
Cestodes	0.18**	0.19**	0.14*	0.19**	0.19**	-	0.09	0.49**
Trematodes	0.02	0.09	0.02	0.07	0.06	0.09	-	0.18**
Worm burden	0.38**	0.37**	0.86**	0.33**	0.90**	0.49**	0.18**	-

 

*P≤0.05.

**P≤0.01.

 

of infections with diverse helminth species exhibited variations between males and females; however, there was no statistically significant distinction observed in the gender of the chickens. Of the male chickens, 52.2% had helminth infections with only one species, in contrast to 38.8% in female chickens (Table 2).

Prevalence Of Gastrointestinal Parasites By Age

The species-specific nematode prevalence was 56.0–91.2% at 12–18 weeks of age. The average worm burden was 10.2 ± 17.5. The prevalence of H. gallinarum was higher in chickens at 18 weeks of age than in the other age groups (P<0.001; Table 3). The same pattern was observed for nematode infections. The total nematode worm burden was higher in chickens at 18 weeks of age than in chickens of other ages (P<0.001). There was a higher prevalence of total gastrointestinal parasites in chickens at 14–18 weeks (84.0–91.2%) than in chickens at 12 weeks (56%) of age P<0.001; Table 3). Resembling trends were observed at the species level for both A. galli and H. gallinarum.

Post-mortem parasitological examinations revealed that 45.4% of chickens harboured single helminth species, while 34.5% manifested mixed infections involving at least two helminth species (Table 2). However, the prevalence of multiple infections at 12 weeks of age was lower than that at 14, 16, and 18 weeks of age. The prevalence of different worm species in chickens was lowest at 12, whereas it was highest at 18, weeks of age.

 

Figure 2 illustrates the incidence of multiple infections at 12, 14, 16, and 18 weeks of age. The quantity of helminth species harboured per chicken differed according to chicken age. At 12, 14, 16, and 18 weeks of age, most chickens exhibited infection with a singular helminth species. The chickens were infected with fewer helminth species at 12 and 14 weeks of age than at other ages. At 12 and 14 weeks, 25.0% and 28.2% of chickens, respectively, demonstrated mixed infections involving at least two species. Conversely, at 16 and 18 weeks, 37.9% and 40.4% of chickens, respectively, displayed mixed infections with at least two species.

 

Correlations

Table 4 presents the estimated correlations among various worm species, the total worm burden, and the age of the chickens. The number of H. gallinarum exhibited a strong correlation (0.86) with total worm burden. The nematode count was highly correlated (0.90) with the total worm burden. Moreover, there were moderate positive correlations observed between the age of chickens and the overall worm burden. (0.38), chicken age and the number of H. gallinarum (0.36), and chicken age and nematode count (0.36).

DISCUSSION

There is no published information regarding the species identity, prevalence, and infection intensity of gastrointestinal helminth parasites in indigenous chickens produced on small-scale farms in the Nakhon Pathom and Suphan Buri provinces. Gastrointestinal helminths pose minimal concerns in short period of production cycle (such as broilers) reared in contemporary intensive livestock production systems; however, they continue to be a significant issue in long-cycle birds, specifically in the case of layers, particularly when reared under conditions of low biosecurity measures and inadequate sanitation (Ybañez et al., 2018; Ola-Fadunsin et al., 2019; Van et al., 2020). The overall prevalence of parasitic helminth infection (79.9%) reported in this study was comparatively lower than that reported in previous studies conducted in southern (83.7%; Kunjara Na Ayudthaya and Sangvaranond, 1997), northeastern (87.6%; Kunjara Na Ayudthaya and Sangvaranond, 1993), and northern (73.9%; Wuthijaree et al., 2019) Thailand. However, the total prevalence of helminth infection is 99.2% in the Phayao Province in northern Thailand (Butboonchoo and Wongsawad, 2017). The prevalence of natural helminth infection of the gastrointestinal tract varies regionally; it is between 97.6 and 99.2% in Germany (Kaufmann et al., 2011; Wongrak et al., 2014), 99.3% in Italy (Wuthijaree et al., 2017), 77.3% in Colombia (Montes-Vergara et al., 2021), 73.1% in Jordan (Abdelqader et al., 2008), 72% in Iran (Ebrahimi et al., 2014), and 56.43% in Indonesia (Zalizar et al., 2021). The probable reason for such differences in the prevalence of helminth infection might be climatic and environmental conditions, bird age, and intermediate host availability, which are the main determinants of variability in parasite prevalence. The occurrence and level of helminth infections can be impacted by temperature and humidity, affecting larvae or eggs within the environment (Ola-Fadunsin et al., 2019; Shifaw et al., 2021). In addition to environmental factors, the study season, individual host resistance, and housing management influence the prevalence rate. The indigenous chickens used in this study were housed in a free-range system. They were afforded unrestricted freedom to roam and scavenge diverse agricultural by-products, pastures, and soil. This environment exposed chickens to infective stages of parasites, including earthworms, insects, and snails, which functioned as intermediate hosts. (Yousfi et al., 2013).

In this study, nematodes were the most frequently reported, followed by cestodes, and trematodes. It has been suggested that the increase in the diversity and richness of helminths in indigenous chickens is linked to location, region, and climatic conditions. Temperature, humidity, and rainfall represent critical determinants impacting both the occurrence and severity of natural helminth infections (Chilinda et al., 2020; Van et al., 2020; Shifaw et al., 2021). Lowlands with warm temperatures, high humidity, and adequate rainfall on river plains in the Nakhon Pathom and Suphan Buri provinces may facilitate the survival of helminths in the environment, promoting the developmental success of the infective stage. Magnitude and geographical area may also affect the number of helminth species, resulting in increased helminth infections in indigenous chickens.

The most common nematode species found in the river plains was H. gallinarum (70.3%). According to current knowledge, no study has investigated the prevalence of natural helminth infections in indigenous Thai chickens in central Thailand. However, the prevalence of infection by H. gallinarum is between 70.6 (Wuthijaree et al., 2019) and 86.7% (Butboonchoo and Wongsawad, 2017) in northern Thailand. In contrast, the prevalence of H. gallinarum in southern Thailand is only 33.7% (Kunjara Na Ayudthaya and Sangvaranond, 1997). The dominance of H. gallinarum (60%) has been reported in the Mediterranean climates of Oran and Algeria (Kerroucha et al., 2022). Van et al. (2020) documented that the predominant helminth infection in small-scale commercial chickens in the Mekong Delta of Vietnam is H. gallinarum, with a prevalence of 43.3%. A study by Ybañez et al. (2018) of backyard chicken flocks in the Philippines revealed that the prevalence of H. gallinarum is 59.3%. This variation may depend on the breed and age of the chickens, housing systems, management, and environmental factors. H. gallinarum exhibited higher prevalence and infection intensity compared to other parasites. This could be because H. gallinarum is capable of infecting multiple species of galliform birds. The higher infection rates of H. gallinarum compared to other helminth species may be attributed to interactions with wild birds within particular environmental settings. Additionally, H. gallinarum exhibits both direct and indirect life cycles and can serve as a paratenic host (Soulsby, 1976; Yazwinski and Tucker, 2008), a crucial role in transmitting infective eggs in backyard farming environments. Moreover, Permin and Hansen (1998), Papini and Cacciuttolo (2008), and Yazwinski and Tucker (2008) have all noted that eggs of the cecal worm, H. gallinarum, are exceptionally resistant to environmental factors and can persist in the soil for years in the infectious. Although Heterakis spp. have a low level of pathogenicity in chickens, their significance is related to the dissemination of the protozoa Histomonas meleagridis, which leads to a severe re-emerging disease (histomonosis or avian blackhead disease; Daş et al., 2021). Previous studies by McDougald (2005) and Daş et al. (2021) demonstrated that the majority of H. gallinarum eggs obtained from hens exhibit H. meleagridis positivity under natural conditions.

We observed a cestode prevalence of 34.5%; the most prevalent cestode was R. cesticillus. In general, increased infection intensity and abundance were correlated with values of cestode prevalence. The surrounding environment is a critical determinant in natural helminth infections (Skallerup et al., 2005; Rufai and Jato, 2017). Poultry cestodes and trematodes have indirect life cycles. The ova typically undergo hatching in aquatic environments and undergo life cycles that involve freshwater snails or dragonflies. While the majority of species necessitate two to three intermediate hosts, a subset demands four intermediate hosts (Permin and Hansen, 1998; McDougald, 2008). The reasons for this could include geographical variations in parasite distribution or intermediate worm hosts. These results point to increased susceptibility to these parasites among the chickens kept in the wet system owing to more favorable environmental conditions, which would be associated with a greater presence of intermediate hosts. Cestodes are parasitic helminths that require intermediate hosts and optimum humidity to disseminate their susceptible components (gravid proglottids and eggs). Our findings indicate that humidity and parasite prevalence in low river plains are related, which aligns with the earlier research conducted by García Cuadrado et al. (2021). Their study revealed a connection between parasite prevalence and soil moisture. Moreover, the presence of swamps and, thus, a sufficient amount of intermediate hosts in the current study location might be the reason for the existence of trematodes. The findings of this study align with those of another study conducted in a location characterized by high humidity levels (Mukaratirwa et al., 2009).

This study did not find any correlation between parasitic infectious diseases (both the number of species and the prevalence of each species) and the sex of the host. This finding is consistent with the results of previous studies (Hussen et al., 2012; Ebrahimi et al., 2014; Butboonchoo and Wongsawad, 2017; Wuthijaree et al., 2019), indicating that helminth species have no natural affinity for either sex of host chicken.

The findings of this investigation demonstrated that chicken age had a variable influence on gastrointestinal parasitic infections, as chickens at 14–18 weeks of age were more likely to carry parasites than those at 12 of age. The risk of gastrointestinal helminth infections and the variety of helminth species escalated in correlation with age and access to outdoor activities. In general, the occurrence of helminth infections was significantly elevated in all husbandry systems during the period of the highest production. The increase was substantial until the time of slaughter, which aligns with the belief that the age of the host has minimal impact on resistance (Idi et al., 2004; Zloch et al., 2021). A possible reason for this could be continuous reinfection from a very contaminated surrounding environment (Höglund and Jansson, 2011; Tarbiat et al., 2016). The duration of host exposure to parasites influences the prevalence of natural helminth infections. As a result, backyard chickens that are raised for more extended periods and have more freedom to scavenge are likely to have a greater occurrence of gastrointestinal helminths. This is because they are more frequently exposed to these parasites’ infectious stages or infected intermediate hosts (Kumar et al., 2015). Furthermore, more contact with contaminated environments outdoors may increase the likelihood of being reinfected. Additionally, it is crucial to consider that certain types of nematodes and cestodes rely on intermediary hosts like earthworms, houseflies, or beetles for transmission (Permin et al., 1999; Shifaw et al., 2021).

CONCLUSIONS

Gastrointestinal parasites are frequently discovered in domestic chickens raised in the backyard systems of river plains in central Thailand. Most chickens under common, extensive backyard production conditions are subclinically infected with single or multiple helminth species, the most frequent being H. gallinarum, Tapeworms, and A. galli. Increasing age correlates with a higher incidence of natural helminthic infections. The gathered gastrointestinal parasitic infection data will be useful for providing information on prevalence status and disease control and predicting future disease trends for effective farm management. Comprehending the conditions of a farm is necessary for the development of optimal practices and preventive programs, facilitating the identification of factors that impact disease incidence.

ACKNOWLEDGMENTS

The authors would like to express sincere thanks to the Department of Agricultural Science, Faculty of Agriculture, Natural Resources and Environment, Naresuan University for support the research laboratory facilities. The authors acknowledge the Department of Animal Science, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Kamphaeng Saen Campus for partial funding this study.

CONFLICTS OF INTEREST

The authors declare that there is no conflict of interest regarding the publication of this article.

novelty statement

This paper publishes the prevalence of gastrointestinal helminth infection in free-range indigenous chickens on river plains in central Thailand for the first time. This comprehension is crucial for developing region-specific knowledge and prevention protocols regarding helminth infections in chickens with outdoor access.

AUTHORS CONTRIBUTIONS

All the authors contributed to designing research, data collection, data acquisition, data analysis and reporting, and manuscript preparation.

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