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Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology logoLink to Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology
. 2024 Feb 9;48(1):95–107. doi: 10.1007/s12639-023-01644-0

Prevalence of gastrointestinal helminth parasite infections in country chicken from Visakhapatnam district Andhra Pradesh India

Anisha Mathews 1, Janakiram Pasupuleti 2, Ummey Shameem 1,✉
PMCID: PMC10909052  PMID: 38440751

Abstract

Birds in a free environment carry huge risk of helminth parasite infections affecting the health of poultry and thereby indirectly leading to great economic loss. The present study aimed to evaluate the prevalence, intensity and species diversity of gastrointestinal helminth parasites (GIH) of country chicken (Gallus gallus domesticus) from local chicken markets of Visakhapatnam district, Andhra Pradesh. A total of 300 gastrointestinal tract (GIT) samples were examined from January to December 2021 and the collected parasites were separated, counted, identified and statistically analysed. The overall prevalence of infection was found to be 87% with an intensity of 139.29. The study showed high prevalence with mixed infections (66%), whereas the prevalence with individual groups i.e. cestodes, nematodes and trematodes was found to be 83.00%, 70.33%, and 0.67% respectively. Altogether 10 parasite species were identified viz. Raillietina echinobothrida being the most dominant with a prevalence of 72.67%, followed by Raillietina tetragona (62.00%), Heterakis gallinarum (59.33%), Ascaridia galli (45.33%), Davainea proglottina (43.00%), Amoebotaenia cuneata (42.67%), Raillietina cesticillus (38.33%), Hymenolepis sp. 1 (36.00%), Cotugnia spp. (29.67%) and the least was Hymenolepis sp. 2 (21.00%). In month-wise data, highest prevalence was recorded in July (100%), and the highest seasonal prevalence was recorded in summer (90%), followed by monsoon (87%) and winter (84%). No major significant difference in prevalence was noted between males (88.51%) and females (85.53%). Hosts with high body temperature and low GIT pH levels showed increased prevalence and parasite intensity.

Keywords: Country chicken, Gastrointestinal helminth parasites, Prevalence, Intensity, Visakhapatnam

Introduction

The prevalence of most parasitic diseases seems to have reduced significantly in commercial indoor poultry production systems due to improved housing, hygiene and management but continues to be of great threat in deep-litter and free-range commercial systems (Permin and Hansen 1998). The latter consists of country chicken or indigenous domestic fowls (G. gallus domesticus) variously referred to as local or rural chicken, backyard poultry or village chicken, desi chicken, or free-range chicken. In villages, rural farmers mostly rear chicken in a free-range management system or scavenging system. Due to this scavenging habit, country chicken are more prone to all types of infections, particularly GIH parasitic infections compared to birds reared on intensive farming. GIH parasitic infestations are often neglected despite their patho-physiological effects like malnutrition, anorexia, decreased feed conversion ratio, retarded growth, reduced weight gain, decreased egg production, catarrh diarrhoea, intestinal obstruction, morbidity (Dube et al. 2010), infertility and acute worm infestations that sometimes lead to mortality (Katoch et al. 2012). Moreover, these infections are generally influenced by factors such as temperature and humidity, which alter the parasites’ population dynamics resulting in dramatic changes in their prevalence and intensity (Magwisha et al. 2002).

In India, considerable work has been carried out on GIH parasites of country chicken, and several reports are available from different states viz., Karnataka (Puttalakshmamma et al. 2008), Kashmir (Dar and Tanveer 2013), Maharashtra (Naphade and Chaudhari 2013), Madhya Pradesh (Satish and Priti 2013), Tamil Nadu (Sivakumar et al. 2017), Chhattisgarh (Kumari 2018), Telangana (Rao et al. 2018), Rajasthan (Singh and Nama 2018), West Bengal (Ghosh et al. 2019), Meghalaya (Das et al. 2020) and Uttar Pradesh (Jaiswal et al. 2020). In the state of Andhra Pradesh, the prevalence of GIH parasites in country chicken has been reported from Gannavaram by Sreedevi et al. (2014) and from Krishna District by Bandi et al. (2020). The present study constitutes first such epidemiological study on the prevalence of GIH parasites of free range country chicken from Visakhapatnam district, Andhra Pradesh, India (Table 1).

Table 1.

Reports on the prevalence of GIH parasitic infections in country chicken from India

S.no Author Year Area Host Sample P% GIH parasites
1 Puttalakshmamma et al. 2008 Bangalore, Karnataka Desi and Farm Chicken GIT and Faecal 71.00 R. tetragona, R.echinobothrida, A. galli, H. gallinarum, S. brumpti, Strongyloides spp.
2 Katoch et al. 2012 Jammu Backyard Chicken GIT 72.00 R. tetragona, R. echinobothrida, A. galli, H. gallinarum, A. cuneata, Heterakis spp., Capillaria spp., C. hamulosa
3 Satish and Priti 2013 Madhya Pradesh Local and Exotic chicken GIT N/A R. echinobothrida and R. tetragona, H. carioca, A. galli, H. gallinarum, Subulura trachea
4 Naphade and Chaudhari 2013 Maharashtra Desi Chicken GIT and Faecal 84.05 Raillietina spp., Ascaridia spp.
5 Dar and Tanveer 2013 Kashmir Backyard Chicken GIT 85.83 R. tetragona, R. cesticillus, R. echinobothrida, R. spiralis, Choanotaenia infundibulum, C. gondwana, A. cuneata, A. domesticus, D. proglottina
6 Sreedevi et al. 2014 Gannavaram, Andhra Pradesh Desi Chicken GIT and Faecal 63.21 D. proglottina, R. cesticillus, R. echinobothrida, A. galli, Capillaria annulata, H. gallinarum
7 Javaregowda et al. 2014 Shimoga, Karnataka Backyard Chicken GIT and Faecal 73.20 R. tetragona, R. cesticillus, R. echinobothrida, A. galli, H. gallinarum, Capillaria spp., Coccidian spp.
8 Sahu and Sinha 2016 Bihar Desi Poultry Chicken GIT and Faecal 65.39 Raillietina spp., Davainea spp., Ascaridia spp., Heterakis spp.
9 Sivakumar et al. 2017 Tamil Nadu Backyard Chicken GIT N/A A. galli, Dispharynx spiralis, Raillietina spp.
10 Kumari 2018 Chhattisgarh Local and Poultry chicken GIT 46.00 A. galli, Rallietina spp., S. brumpti
11 Singh and Nama 2018 Rajasthan Domestic Chicken GIT 53.33 R. tetragona, A. galli, H. gallinarum
12 Rao et al. 2018 Telangana Domestic Chicken GIT and Faecal 55.79 D. proglottina, R.tetragona, R.echinobothrida, A. galli, H. gallinarum
13 Bandi et al. 2020 Krishna, Andhra Pradesh Backyard Poultry GIT and Faecal 74.22 Raillietina cesticillus, R. echinobothrida and R. tetragona, A. galli, Capillaria spp., H. gallinarum, Strongyloides avium, S. brumpti, Tetrameres mohtedai, D. spiralis
14 Present study 2021 Visakhapatnam, Andhra Pradesh Country Chicken GIT and Faecal 87.32 R. tetragona, R. echinobothrida, R. cesticillus, D. proglottina, A. cuneata, Cotugnia spp., Hymenolepis spp., A. galli, H. gallinarum, Prosthogonimus spp.
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Materials and methods

Study area

The study was carried out in Visakhapatnam district situated between 81°06′ and 83°31′ E, of the Eastern longitudes and 17°15′ and 18°32′ N, of the Northern latitudes (Fig. 1). The boundaries of this district are Vizianagaram in the North-West direction, the East Godavari in the South-West and the Bay of Bengal in the South. The length of the coastline is 135 km. The annual temperatures range between 20 and 38 °C.

Fig. 1.

Fig. 1

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Map of Visakhapatnam District

Sampling

Guts of three hundred (300) country chicken (G. gallus domesticus) were investigated in an annual cycle from January 2021 to December 2021, by taking 25 samples per month. Freshly slaughtered intact GIT samples of chicken were collected from chicken markets covering different locations in Visakhapatnam district. Before slaughtering the chicken, host details like sex, temperature and weight were recorded at the site itself. Collected gut samples were immediately stored in an ice box and brought to the Department laboratory for further analysis (Fig. 2).

Fig. 2.

Fig. 2

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GIT of country chicken as host sample

Parasitological examination

The GIT of each host was slit opened by a longitudinal incision along the duodenum to rectum including caecal tubes and immediately the pH of the GIT was recorded. A macroscopic examination of the different regions of GIT was carried out to collect and separate the visible parasites in petri dishes according to predilection sites for relaxation (Fig. 3). Undetectable parasites were examined through a stereo microscope. Adults and undamaged cestodes and trematodes washed in normal saline (0.9% NaCl) solution were fixed in AFA solution, whereas nematodes were fixed in 70% glycerine alcohol and preserved as permanent mounts (Soulsby 1982; Cable 1957; Belghyti 1994). Parasites were identified based on helminthological keys described by Yamaguti (1959, 1961), Khalil et al. (1994) and Anderson et al. (1974) under a light microscope.

Fig. 3.

Fig. 3

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GIH parasites isolated from their predilection sites

Statistical analysis

Data collected during the present study were tabulated and analysed to show the population and parasite—prevalence, mean intensity, mean abundance, index of infection (total number of parasites of a given species multiplied with total number of samples infected with the same species by square of total number of samples examined) and dominance index (total number of parasites of a given species by total number of parasites collected) of GIH infection in country chicken (Bush et al. 1997). Statistical analysis was performed using one-way ANOVA to understand the significant differences in infection between different GIH parasites and seasons (p > 0.05). The data was analysed using MS Excel 2019 of MSO version 2210 and IBM SPSS Statistics 26.

Result

Prevalence of GIH parasite groups

Overall prevalence

Out of 300 country chicken screened, 261 were found infected with helminth parasites with an overall prevalence of 87.00%. Cestodes and nematodes were more prevalent than trematodes. The highest infection was recorded with cestodes (83.00%) followed by nematodes (70.00%) while the lowest percentage of infection was found with trematodes (0.67%) (Table 2).

Table 2.

Monthly and seasonal prevalence of GIH parasite groups in country chicken

Season Month Total GIH Cestodes Nematodes Trematodes
SE SI P% MI SI P% MI SI P% MI SI P% MI
Summer Mar 25 23 92.00 142.57 23 92.00 110.13 16 64.00 46.63 0 0.00 0.00
Apr 25 22 88.00 155.64 21 84.00 116.33 19 76.00 50.00 1 4.00 31.00
May 25 23 92.00 94.17 22 88.00 47.64 21 84.00 53.24 0 0.00 0.00
Jun 25 22 88.00 143.73 22 88.00 74.91 21 84.00 72.10 0 0.00 0.00
Total 100 90 90.00 133.68 88 88.00 87.18 77 77.00 56.21 1 1.00 31.00
Monsoon Jul 25 25 100.00 182.84 22 88.00 104.77 24 96.00 94.42 0 0.00 0.00
Aug 25 22 88.00 151.00 22 88.00 82.00 20 80.00 75.90 0 0.00 0.00
Sep 25 21 84.00 165.67 18 72.00 144.67 17 68.00 51.47 0 0.00 0.00
Oct 25 19 76.00 163.89 19 76.00 133.63 14 56.00 41.00 1 4.00 1.00
Total 100 87 87.00 166.51 81 81.00 114.22 75 75.00 69.77 1 1.00 1.00
Winter Nov 25 21 84.00 127.52 20 80.00 103.20 15 60.00 40.93 0 0.00 0.00
Dec 25 18 72.00 119.50 18 72.00 88.61 12 48.00 46.33 0 0.00 0.00
Jan 25 22 88.00 120.18 21 84.00 82.14 17 68.00 54.06 0 0.00 0.00
Feb 25 23 92.00 102.78 21 84.00 78.81 14 56.00 50.64 0 0.00 0.00
Total 100 84 84.00 117.11 80 80.00 87.99 58 58.00 48.24 0 0.00 0.00
TOTAL 300 261 87.00 139.29 249 83.00 96.24 210 70.00 58.85 2 0.67 16.00
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SE, Number of samples examined; SI, Number of samples infected; P%, Prevalence; MI, Mean Intensity

Monthly prevalence of infection

Though infection was noted throughout the study period, it varied during different months. Overall infection was maximum in the month of July at 100.00% (182.84) and lowest in December at 72.00% (119.50). Among individual groups, the highest cestode infection was found in March (92.00%) and the lowest in September and December with 72.00% in each month. Whereas nematode infection was highest in July (96.00%) and lowest in December (48.00%). Only two host samples were infected with trematode parasites, in April and October with a prevalence of 4% each (Table 2, Fig. 4).

Fig. 4.

Fig. 4

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Monthly prevalence of GIH parasite groups in country chicken

Seasonal prevalence of infection

High prevalence was noted during summer (90.00%) followed by rainy (87.00%) and winter (84.00%) seasons. Cestode and nematode infections were high during summer at 88.00% and 77.00% and lesser during winter at 80.00% and 58.00% respectively (Table 2, Fig. 5).

Fig. 5.

Fig. 5

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Seasonal prevalence of GIH parasite groups in country chicken

Prevalence of individual GIH parasite species

Overall prevalence

The study recorded ten dominant GIH parasite species, including eight cestode species belonging to six genera and two nematode species belonging to two genera. The nematodes were Ascaridia galli and Heterakis gallinarum, the cestode species were viz. Raillietina tetragona, R. echinobothrida, R. cesticillus, Davainea proglottina, Amoebotaenia cuneata, Cotugnia spp., and Hymenolepis spp. and the trematodes were Prosthogonimus spp. and a new parasite (yet to be identified). The data on the overall prevalence of individual GIH parasites showed highest infection with R. echinobothrida (72.67%), followed by R. tetragona (62.00%), H. gallinarum (59.33%), A. galli (45.33%), D. proglottina (43.00%), A. cuneata (42.67%), R. cesticillus (38.33%), Hymenolepis sp. 1 (36.00%), Cotugnia spp. (29.67%) and Hymenolepis sp. 2 (21.00%). The highest dominance index of 0.29 was noted in the case of H. gallinarum, being the most common species (Table 3).

Table 3.

Ecological indices of individual GIH parasite species in country chicken

GIH species SE SI P% MI MA II DI R SS
R. tetragona 300 186 62.00 12.60 7.81 4.84 0.06 1–47 Small intestine
Raillietina echinobothrida 300 218 72.67 14.46 10.51 7.64 0.09 1–76 Small intestine
R. cesticillus 300 115 38.33 9.83 3.77 1.44 0.03 1–63 Duodenum, Jejunum
D. proglottina 300 129 43.00 37.47 16.11 6.93 0.13 5–105 Duodenum
A. cuneata 300 128 42.67 35.34 15.08 6.43 0.12 6–91 Duodenum
Cotugnia spp. 300 89 29.67 14.27 4.23 1.26 0.03 1–52 Small intestine
Hymenolepis sp. 1 300 108 36.00 39.94 14.38 5.18 0.12 10–247 Duodenum, Jejunum
Hymenolepis sp. 2 300 63 21.00 38.05 7.99 1.68 0.07 15–83 Duodenum, Jejunum
A. galli 300 136 45.33 13.40 6.08 2.75 0.05 1–118 Small Intestine
H. gallinarum 300 178 59.33 59.19 35.12 20.84 0.29 5–492 Caeca
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SE, Number of samples examined; SI, Number of samples infected; P%, Prevalence of infection; MI, Mean Intensity; MA, Mean Abundance; II, Index of Infection; DI, Dominance Index; R, Range; SS, Site Specificity

Monthly prevalence of infection

The data on monthly prevalence of individual GIH parasites showed, R. tetragona to be highest in March (76%) and least in November (48%); R. echinobothrida as highest in March (88%) and least in November and December with 60%; R. cesticillus to be highest in May (52%) and least in September, October and December with 28%; D. proglottina to be highest in October (56%) and least in May and July with 32%; A. cuneata recorded highest in October (60%) and least in May (24%); Cotugnia spp. high in March, June and July with 44% and least in October and November with 12%; Hymenolepis spp. were highest in October (52%); A. galli highest in July (68%) and least in October (16%), and H. gallinarum was highest in July (84%) and least in March and December with 40% (Table 4).

Table 4.

Monthly prevalence of individual GIH parasite species in country chicken

Months SE Cestodes Nematodes
R.t R.e R.c D.p A.c Co Hy 1 Hy 2 A.g H.g
SI P% SI P% SI P% SI P% SI P% SI P% SI P% SI P% SI P% SI P%
Summer
Mar 25 19 76 22 88 12 48 12 48 11 44 11 44 12 48 6 24 15 60 10 40
Apr 25 16 64 20 80 12 48 11 44 11 44 10 40 11 44 6 24 13 52 18 72
May 25 17 68 18 72 13 52 8 32 6 24 9 36 5 20 0 0 14 56 18 72
Jun 25 15 60 21 84 11 44 9 36 7 28 11 44 8 32 0 0 16 64 18 72
Total 100 67 67 81 81 48 48 40 40 35 35 41 41 36 36 12 12 58 58 64 64
Monsoon
Jul 25 15 60 19 76 12 48 8 32 9 36 11 44 6 24 0 0 17 68 21 84
Aug 25 16 64 20 80 12 48 10 40 12 48 9 36 8 32 2 8 13 52 20 80
Sep 25 15 60 16 64 7 28 13 52 10 40 8 32 12 48 11 44 10 40 14 56
Oct 25 13 52 14 56 7 28 14 56 15 60 3 12 13 52 13 52 4 16 11 44
Total 100 59 59 69 69 38 38 45 45 46 46 31 31 39 39 26 26 44 44 66 66
Winter
Nov 25 12 48 15 60 8 32 12 48 12 48 3 12 13 52 7 28 7 28 13 52
Dec 25 13 52 15 60 7 28 10 40 11 44 4 16 8 32 6 24 7 28 10 40
Jan 25 18 72 18 72 8 32 12 48 12 48 5 20 7 28 7 28 12 48 14 56
Feb 25 17 68 20 80 6 24 10 40 12 48 5 20 5 20 5 20 8 32 11 44
Total 100 60 60 68 68 29 29 44 44 47 47 17 17 33 33 25 25 34 34 48 48
TOTAL 300 186 62 218 73 115 38 129 43 128 43 89 30 108 36 63 21 136 45 178 59
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SE, Number of samples examined; SI, Number of samples infected; P%, Prevalence of infection; Rt, R. tetragona; Re, R. echinobothrida; Rc, R. cesticillus; Dp, D. proglottina; Co, Cotugnia spp.; Ac, A. cuneata; Hy1, Hymenolepis sp. 1; Hy2, Hymenolepis sp. 2; Ag, A. galli; Hg, H. gallinarum

Seasonal prevalence of infection

The data on the seasonal prevalence of individual parasites showed that during summer R. echinobothrida (81%) to be highest, R, tetragona (67%) was second and Hymenolepis sp. 2 (12%) was the least prevalent. During monsoon, R. echinobothrida (69%) showed highest prevalence followed by H. gallinarum (66%) and least by Hymenolepis sp. 2 (26%). During winter, R. echinobothrida (68%) showed highest prevalence, followed by R. tetragona (60%) and least Cotugnia spp. (17%) (Table 5, Fig. 6). One-way ANOVA was carried out to understand the significant differences in prevalence between different GIH parasite groups and seasons. The difference was noted to be statistically not very significant (p > 0.05) (Table 6).

Table 5.

Seasonal prevalence of individual GIH parasite species in country chicken

Seasons (P%) SE R.t R.e R.c D.p A.c Co Hy 1 Hy 2 A.g H.g
Summer 100 67 81 48 40 35 41 36 12 58 64
Monsoon 100 59 69 38 45 46 31 39 26 44 66
Winter 100 60 68 29 44 47 17 33 25 34 48
Total 300 62.00 72.67 38.33 43.00 42.67 29.67 36.00 21.00 45.33 59.33
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SE, Number of samples examined; Rt, R. tetragona; Re, R. echinobothrida; Rc, R. cesticillus; Dp, D. proglottina; Co, Cotugnia spp.; Ac, A. cuneata; Hy1, Hymenolepis sp. 1; Hy2, Hymenolepis sp. 2; Ag, A. galli; Hg, H. gallinarum

Fig. 6.

Fig. 6

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Seasonal prevalence of individual GIH parasite species in country chicken

Table 6.

One-way analysis (ANOVA) between parasites and seasons (p > 0.05)

Source of variation Sum of Squares df MS F Sig
Between groups 321.800 2 160.900 0.569 0.573
Within groups 7638.200 27 282.896
Total 7960.000 29
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Effect of various factors on the prevalence of GIH infection

Sex

Out of 300 GIT samples of country chicken examined, 148 males and 152 females were recorded. 131/148 males and 130/152 females were found to be infected with a prevalence and intensity of 88.51% (142.82) and 85.53% (135.73) respectively. The prevalence and intensity of cestode, nematode and trematode infection in males was recorded as 85.81% (95.73), 75.00 (58.74) and 0.68% (31.00) and in females as 80.26% (96.76), 65.13% (58.98) and 0.66% (1.00) respectively. The results showed slightly higher infection in males when compared to females (Table 7).

Table 7.

Prevalence of GIH parasite groups in country chicken based on Sex, Body weight, Body temperature and GIT pH

Host observation Total GIH Cestodes Nematodes Trematodes
SE SI P% MI SI P% MI SI P% MI SI P% MI
Sex
Male 148 131 88.51 142.82 127 85.81 95.73 111 75.00 58.74 1 0.68 31.00
Female 152 130 85.53 135.73 122 80.26 96.76 99 65.13 58.98 1 0.66 1.00
Body Weight (kg)
0.6–1.0 17 17 100.00 142.06 17 100.00 112.41 13 76.47 38.77 0 0.00 0.00
1.1–1.5 128 110 85.94 140.45 104 81.25 91.94 90 70.31 65.40 1 0.78 1.00
1.6–2.0 104 87 83.65 138.08 82 78.85 99.10 70 67.31 55.09 1 0.96 31.00
2.0–2.5 38 36 94.74 140.67 35 92.11 97.37 29 76.32 57.10 0 0.00 0.00
2.6–3.0 8 7 87.50 140.71 7 87.50 99.29 5 62.50 58.00 0 0.00 0.00
3.0–3.5 5 4 80.00 107.00 4 80.00 65.25 3 60.00 55.67 0 0.00 0.00
Body Temperature (°F)
104° 14 9 64.29 44.89 9 64.29 35.56 5 35.71 16.80 0 0.00 0.00
105° 30 23 76.67 82.74 22 73.33 57.05 17 56.67 38.12 0 0.00 0.00
106° 59 44 74.58 96.23 38 64.41 85.05 30 50.85 33.40 0 0.00 0.00
107° 115 104 90.43 135.04 101 87.83 97.76 81 70.43 51.48 0 0.00 0.00
108° 82 81 98.78 194.68 79 96.34 117.49 77 93.90 83.83 2 2.44 16.00
GIT pH level
5.0 73 72 98.63 194.25 72 98.63 121.69 66 90.41 78.67 2 2.74 16.00
5.5 131 128 97.71 137.45 125 95.42 93.66 100 76.34 58.85 0 0.00 0.00
6.0 96 61 63.54 78.28 52 54.17 67.17 44 45.83 29.14 0 0.00 0.00
TOTAL 300 261 87.00 139.29 249 83.00 96.24 210 70.00 58.57 2 0.67 16.00
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SE, Number of samples examined; SI, Number of samples infected; P%, Prevalence of infection; MI, Mean Intensity

Body weight

The body weight of chicken sampled ranged between 0.6 kg and 3.5 kg. To understand the influence of weight on the prevalence and intensity of infection, they were categorized into six groups with a difference of 0.5 kg (kg) weight in each group. The highest prevalence of infection was seen in 0.6–1.0 kg group chicken recording 100% (142.06) and lowest was seen in 3.1–3.5 kg group country chicken recording 80% (107.00). The highest prevalence of cestode and nematode infections was seen in 0.6–1.0 kg group with 100% (112.41) and 76.47 (38.77) respectively, whereas lowest was seen in 3.1–3.5 kg group with 80% (65.25) and 60% (55.67) respectively. Trematodes infections were found highest in the group of 1.6–2.0 kg with 0.96% (31.00) and least in 1.1–1.5 kg with 0.78% (1.00). The results showed that the prevalence and intensity of infection varied with an increase in the weight of the host (Table 7).

Body temperature

The body temperatures of live country chicken from which GIT samples were collected ranged between 104°and 108°F. To study the influence of temperature on the prevalence and intensity of infection, each °F temperature was considered as one group. At each group, the number examined and infected were viz. 104°F (9/14), 105°F (23/30), 106°F (44/59), 107°F (104/115) and 108°F (81/82). The overall prevalence of infection was found to be highest at 108°F with 98.78% (194.68) and lowest at 104°F with 64.29% (44.89). Highest prevalence of cestode, nematode and trematode parasite infections were found at 108°F with 96.34% (117.49), 93.90% (83.83) and 2.44% (16.00) respectively, whereas least infections were recorded at 104°F with 64.29% (35.56), 35.71% (16.80), 0.00% respectively. The results showed that the prevalence and intensity of infection increased with an increase in the host body temperature (Table 7).

pH

The pH taken from the GI tract of the host samples ranged from 5.0 to 6.0, showing infection of 72/73 at 5.0, 128/131 at 5.5 and 61/96 at 6.0 pH. The overall prevalence was highest at 5.0 with 98.63% (194.25) and least at 6.0 with 63.54% (78.28). The prevalence and intensity of cestode, nematode and trematode infection were found to be highest at 5.0 with 98.63% (121.69), 90.41% (78.67) and 2.74% (16.00) respectively, whereas lowest at 6.0 with 54.17% (67.17), 45.83% (29.14) and 0.00% respectively. The results indicated an increase in the prevalence and intensity of infection with a decrease in pH levels (Table 7).

Type of prevalence

As each sample contains more than two to three types of GIH parasites, the infection type was arranged as uninfected, single infection with only one GIH parasite such as cestode (C) or nematode (N) and multiple infections with more than one type of GIH parasite, as (C + N) and (C + N + T). The prevalence of uninfected samples was recorded at 13.00% (39/300), the prevalence and intensity of total single infections (63/300) was 21.00% (76.25), whereas single cestode infection (C) (51/300) was 17.00% (82.92) and single nematode infections (N) (12/300) was 4.00% (47.92). The prevalence of total mixed infections (198/300) was 66.00% (159.34), mixed infections with both cestode and nematodes (C + N) (196/300) was 65.33% (157.88) and mixed infection with all three types i.e., cestodes, nematodes and trematodes (C + N + T) (2/300) was 0.67% (303.00). The results indicated higher prevalence of mixed infections when compared to single infections (Table 8, Fig. 7).

Table 8.

Prevalence of infection types in country chicken

Infection type Sex SE SI P% MI
Uninfected 0 Male 148 17 11.49 0.00
Female 152 22 14.47 0.00
Total 300 39 13.00 0.00
Single C Male 148 20 13.51 76.60
Female 152 31 20.39 87.00
Total 300 51 17.00 82.92
N Male 148 4 2.70 24.00
Female 152 8 5.26 59.88
Total 300 12 4.00 47.92
Total 300 63 21.00 76.25
Mixed C + N Male 148 106 71.62 158.55
Female 152 90 59.21 157.09
Total 300 196 65.33 157.88
C + N + T Male 148 1 0.68 275.00
Female 152 1 0.66 331.00
Total 300 2 0.67 303.00
Total 300 198 66.00 159.34
TOTAL GIH Male 148 131 88.51 142.82
Female 152 130 85.53 135.73
Total 300 261 87.00 139.29
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SE, Number of samples examined; SI, Number of samples infected; MI, Mean Intensity; P%, Prevalence of infection; 0, Uninfected; C, Cestode; N, Nematode; T, Trematode

Fig. 7.

Fig. 7

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Prevalence of infection types in country chicken

Site specificity of GIH parasites

Most of the GIH parasites recorded during the present study exhibited site selection by restricting their habitat to specific GIT areas in the host. Among the GIH parasites recorded, D. proglottina, A. cuneata, Hymenolepis spp., R. cesticillus were found to be more common in the duodenum, R. tetragona, R. echinobothrida, Cotugnia spp., A. galli were mostly seen in the small intestine, whereas H. gallinarum was found in caecum.

It was also observed that most of the infected intestine walls showed the appearance of nodular formations when heavily infected with R. echinobothrida and A. galli. In the case of A. galli, the lumen of the intestine was thickened with the white velvety mucosal formation and intestinal obstruction due to numerous worms of varying sizes was also noticed (Fig. 8). Further studies on the histopathological architecture of intestine tissues will be carried out in due course of time.

Fig. 8.

Fig. 8

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GIT wall of country chicken showing nodular lesions

Discussion

In India, though several reports are available on gastrointestinal parasites of country chicken in general, very little data is available on the occurrence of multiple or mixed parasitic infections that show an effect on chicken health severely, thereby causing death and consequent economic loss. Previous studies indicated the common occurrence of GIH infections in most of the free-ranging country chicken from different geographical regions of India. In the present study also heavy prevalence and intensity of GIH parasites were noted in country chicken. The overall prevalence recorded with GIH parasites in free-range poultry birds during the present study was 87.00% (139.29), which is higher than that reported in previous studies 63.21% (Sreedevi et al. 2014) but less than 100% (Bandi et al. 2020). Most of the reports available from India showed a lesser prevalence of infection in country chicken when compared to the present study viz. 71% (Puttalakshmamma et al. 2008), 72% (Katoch et al. 2012), 52.77% (Sonune 2012), 84.05% (Naphade and Chaudhari 2013), 73.2% (Javaregowda et al. 2014), 65.39% (Sahu and Sinha 2016) and 53.33% (Singh and Nama 2018) (Table 1). However, higher prevalence of infection was recorded in other cases from countries like Kenya 90.78% (Irungu et al. 2004), 89.9% (Hassouni and Belghyti 2006); Nigeria with 87.7% (Yoriyo et al. 2008) and Iran with 93.3% (Mungube et al. 2008); 96% (Eslami et al. 2009) and 94.5% (Butt et al. 2014).

The country chicken act as hosts to a wide variety of helminth parasites, especially cestode, nematode and trematode parasites. It was noted during the present study that cestode infections are much more common than nematodes. A similar situation was noted in other studies reported by Hussen et al. (2012) where a prevalence of 83.00% cestode and 58.00% nematode parasites from country chicken and Ashenafi and Eshetu (2004) recorded a prevalence of 86.32% cestodes and 75.79% nematodes. Trematodes were less in number and showed low prevalences which might be due to less availability of wet habitats for chicken to ingest molluscs that act as the first-intermediate hosts for the hatched trematode larvae to reproduce asexually to generate free-swimming cercariae. No trematode infections were reported in studies carried out elsewhere by Magwisha et al. 2002 and Jaiswal et al. 2020. No acanthocephalan was observed in the present study but few studies were previously reported by Bhalerao (1937), Terregino et al. (1999), Amin et al. (2013) and Yousfi et al. (2013). The variations noted in the prevalence of infection during various studies including the present study, could be due to their distribution in different geographical climates which may restrict the parasite transmissions or survival. However, parasites are said to be more dominant in tropical countries where the climate and environmental conditions favour their survival rate. However, the high prevalence of GIH infections recorded in country chicken during the present study could be due to their free-ranging habit which allows them free access to infective stages of parasites through coincidental ingestion of arthropods like beetles, earthworms, ants etc. which act as intermediate hosts to most of the helminth parasites while in search of feed (Horsfall 1938; Todd and Crowdus 1952; Soulsby 1982).

Studies on the seasonal influence on the prevalence of infections indicated that some parasite species were prevalent during certain seasons and less prevalent during other seasons. In the present study, highest prevalence of GIH parasites was observed during the summer (90%) followed by monsoon (87%) and winter (84%) seasons. Several variations in seasonal prevalence during different investigations in other studies, high helminth infection was reported by Hange et al. (2007), Solanki et al. (2015) and Rehman et al. (2016) during the winter, by Dube et al. (2010) and Sreedevi et al. (2014) during monsoon and Naphade and Chaudhari (2013) and Sheikh et al. (2015) during summer seasons. These variations in parasite exposure and susceptibility could be due to various environmental conditions which favour the survival of the intermediate host and continues its transmission to other hosts so that the parasite completes the lifecycle. During the present investigation, highest prevalence of 100% with 182.84 parasite intensity was recorded in the month of July by nematodes which coincides with the onset of the monsoon. The onset of monsoon triggers mature nematode parasites to actively release eggs through host droppings into the external environment where they remain viable for a long time and get transmitted to definitive hosts while grazing or through contaminated rainwater (Permin and Hansen 1998).

The common GIH parasite species recovered in the present study were R. echinobothrida and R. tetragona in cestodes; A. galli and H. gallinarum in nematodes. R. echinobothrida was also reported to be dominant species by Shah et al. (1999). R. tetragona and A. galli were more common, a similar situation was noted by Puttalakshmamma et al. (2008), Javaregowda et al. (2014) and Rao et al. (2018). R. tetragona was reported high in the month of July by Ghosh et al. (2019). H. gallinarum was the most commonly observed nematode by Permin et al. (2002) and Silva et al. (2016). A. galli species had been reported as the common and most important helminth infection of poultry by Sonune (2012), Satish and Priti (2013), Murthy and Rao (2014) and Sahu and Sinha (2016). Nevertheless, several variations were noted regarding the dominance of various individual parasite infections in previous studies carried out by Pinckney et al. (2008), Katoch et al. (2012), Butt et al. (2014) and Bandi et al. (2020). The results attribute that each GIH parasite species was confined to a particular seasonal month concerning beneficial conditions to expand their maturation and reproduction rate within the host where it abides.

When compared to single infections, mixed infections showed a greater prevalence with different cestode and nematode parasite species. A similar frequency of mixed infections was stated in other cases by Eshetu et al. (2001), Ashenafi and Eshetu (2004) and Hange et al. (2007). On the contrary, single infection was recorded high by Naphade and Chaudhari (2013) and Sreedevi et al. (2014). The variations noted during different studies can be attributed to the food preferences or food availability at a particular time of the year, which to a great extent can influence the establishment of a mixed or single infection. The ability of two or more parasites to survive within the same host may increase the prevalence of mixed infection, but as the number of parasites per host increases, the prevalence decreases due to antagonism with one another within the same host (Reid 1959).

The sex specific prevalence of parasites showed higher prevalence in males than in female country chicken which is similar to those reported in other cases by Radfar et al. (2012), Dar and Tanveer (2013) and Sheikh et al. (2015). This could be because of the fact that females reduce their feeding range during the brooding period and thereby minimising the chances of acquiring infection. Males on the other hand can go far in search of food, increasing the possibility of acquiring parasitic infections.

Studies on the influence of various factors on the prevalence and intensity of infection showed the prevalence and parasite intensity increased with an increase in body temperature whereas both the prevalence and parasite intensity increased with a decrease in pH levels. The reason for an increase in body temperature and pH of GIT can also be due to an invasion of opportunistic secondary bacterial infections which was found along with the primary parasitic infection (Taylor et al. 2005; Salam et al. 2010). So far, no literature is available with regard to the influence of body temperature and pH levels on the prevalence of parasitic infections in GIT. Thus, the present study constitutes first attempt to record.

Different GIH parasites inhabit specific sites of the host’s GIT called predilection sites which favours their growth, where some parasites live in association with other parasite species. In the present study, D. proglottina, A. cuneata and Hymenolepis spp. were found to restrict their habitat to the duodenum, whereas R. tetragona, R. echinobothrida, Cotugnia spp. and A. galli restricted to small intestines and no parasites were recovered from the trachea, oesophagus, crop and gizzard. A similar situation was reported by Puttalakshmamma et al. (2008) and Katoch et al. (2012) while working on R. tetragona, R. echinobothrida, A. galli, H. gallinarum, A. cuneata, Heterakis spp., Capillaria spp. and Cheilospirura hamulosa.

The intestinal and caecal walls showed thickening, mucosa and nodular formations caused by nematodes, A. galli and H. gallinarum. A similar report was made by Rabbi et al. (2006), Bsrat et al. (2014) and Salam (2015). Most of the parasites are restricted to small intestines generally favouring absorption of nutrients through their body surface (Adang et al. 2008). However, more in-depth histopathological studies are required.

Conclusion

The current study documented that the GIT of chicken can be considered as a potential reservoir for a diverse variety of GIH infections. The detailed reports during the present study will help in understanding the parasite recruitment transmission and various factors influencing the prevalence and intensity of parasite infection. The escalated prevalence and intensity of endoparasites during summer months can be expected to the requisite of optimum temperatures for the growth of parasites and diminished resistance of chicken to the parasites during high temperatures resulting in heavy infestations. This primary parasitic infection condition can make the bird more prone to secondary microbial infections thereby lowering its resistance to immunity. The more common appearance of mixed helminth infections, and gross lesions observed in chicken during heavy infections indicated the need to take up further studies on epidemiology and histopathology to understand and implement strategies for disease management. In view of all the above facts, it can be concluded that wholesome studies of this nature would greatly help in understanding the strategies that will enhance the health status of free range country chicken and in turn safe guard human health.

Acknowledgements

The authors are greatly thankful to the Department of Zoology, Andhra University, Visakhapatnam, for providing facilities to undertake the present study. Also, thank the chicken market shopkeepers for providing alimentary tracts as samples for this work and allowing us to carry out the study in their area.

Author contributions

We attest to the fact that all authors listed on the title page have contributed significantly in carrying out the work have read the final manuscript and attest to the validity and legitimacy of the data and its interpretation.

Funding

Self-supported study. No funding was received for conducting the present study.

Data availability

All the data analysed during the current study will be available with the corresponding author upon reasonable request.

Declarations

Conflict of interest

All the authors declare that they have no conflict of interest to disclose.

Consent to participate

We agree to manuscript submission to the Journal of Parasitic Diseases.

Consent to publish

All the Authors affirm the consent for publication in the upcoming issues of the JOPD.

Ethical approval

Not applicable as this is an observational study so no ethical approval is required.

Footnotes

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Data Availability Statement

All the data analysed during the current study will be available with the corresponding author upon reasonable request.

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