Prevalence of gastrointestinal parasites in indigenous chickens slaughtered at live bird markets of Nairobi County, Kenya

A N Maina, R M Waruiru¹, P G Mbuthia¹, W K Munyua¹, R O Otieno¹ and M N Mutune¹

Viral and Rickettsial Diseases Department, Naval Medical Research Center, Silver Spring, Maryland, United States of America
rmwaruiru@yahoo.co.uk
¹ Department of Veterinary Pathology, Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Nairobi, P.O. Box 29053-00625, Kangemi-Nairobi, Kenya

Abstract

Endoparasitism is among important causes of reduced productivity of indigenous chickens. This study was undertaken to determine the prevalence and intensity of gastrointestinal (GI) parasites in apparently healthy free range chickens slaughtered at various live bird markets in Nairobi County, Kenya. The 131 sampled chickens of both sexes originated from 8 counties with varying agro-climatic conditions. Worm egg and coccidial oocyst counts were performed on fecal materials from each bird while worms collected from the GI tracts were identified and quantified. Many chickens had adult GI helminths (90%), but only a few of these (14%) had coccidial oocysts. Nematodes were the predominant helminths (89%) followed by cestodes (51.5%) but no trematodes were recovered. The nematodes recovered were: Heterakis isolonche (59.5%), Subulura brumpti (36%), Tetrameres americana (32%),Ascaridia galli (19.8%), Gongylonema ingluvicola (19.1%),Acuaria hamulosa (6.1%), Heterakis gallinarum (5.3%) andCapillaria spp. (2.3%). The cestodes recovered were: Raillietina echinobothrida (37.7%), Hymenolepis carioca (33.6%), Davainea proglottina (6.9%), R. tetragona (6.1%) and R. cesticillus (2.3%). Other endoparasites encountered were the air-sac mite, Cytodites nudus (15.3%), Sacocystis spp. (5.6%) and Syngamus trachea (4%). The results of this study showed that GI parasites are prevalent and may pose health problems in apparently healthy free range chickens. The parasites economic importance should be investigated and control strategies initiated to improve the health and productivity of indigenous chickens in Kenya.

Introduction

Indigenous chickens are defined as a group of heterogeneous native fowls, which have been left to out-cross over the years in rural households (Tuitoek et al 1999) and their importance for rural economy is immense in many countries of the world (Barua and Yoshimura 1997; Vali 2008; Magothe et al 2012). These chickens play a major role for the rural poor with respect to their subsidiary income and also provide them with high protein food (eggs and meat). Their potential is enormous and has not been realized because of many constraints like infectious diseases, parasitism, predation, lack of feed, housing, low genetic potential, lack of marketing policy and inadequate farmer education (Nzioka 2002). Parasitism due to GI helminths and ectoparasites constitutes among the major causes that decrease productivity of chickens, but neglected as they are rarely lethal (Permin et al 1997; 2002; Hunduma et al 2010).

Studies conducted on rural free-range poultry in Botswana (Mushi et al 2000), Ethiopia (Zeryehun and Yohannes 2015), Ghana (Poulsen et al 2000), Morocco (Hassouni and Belghyti 2006), Nigeria (Idika et al 2016), Tanzania (Permin et al 1997; Magwisha et al 2002) and Zimbabwe (Mukaratirwa et al 2001; Permin et al 2002) have shown high prevalence of both external and internal parasites among indigenous chickens. In Kenya, Sabuni et al (2010; 2011; 2013) and Waruiru et al (2017) have shown that ecto- and haemo-parasites are common in free range chickens and ducks. However, few such studies have been done on helminth parasites of poultry in the country (Ondawsy et al. 2000; Irungu et al. 2004; Okech et al 2006; Chege et al 2015).

Scavenging free-range birds are in constant contact with soil which serves as an important reservoir and transmission site for infective larval stages of helminths and arthropods which act as paratenic or intermediate hosts (Pandey and Jiang 1992). These factors explain the presence of wide range of helminths and their impact in the health and growth of scavenging rural chickens (Permin et al 1997; Phiri et al 2007). A study conducted in Kenya by Ndegwa et al (1998) showed that farmers did not deworm their indigenous chickens and were not aware about the existence of parasitism in poultry. This study was designed to investigate the prevalence and intensity of GI parasites in marketed indigenous chickens with the ultimate aim of developing control strategies relevant for free range poultry management.

Materials and methods

Study area and chickens

The chickens were purchased from live bird open-air markets located in various trading centers of Nairobi County, Kenya. These were selected using simple random method and included: Burma/Maziwa (Jogoo road), Kariokor, Nairobi South (B and C) and Westlands trading centers. The free range village chickens are brought in cages from different rural areas of Kenya and are usually sold live. However, some consumers prefer to have the chickens slaughtered at the markets in which facilities are readily available. It was established through a questionnaire administered to the traders that sampled birds came from the former Eastern (Machakos, Makueni and Kitui counties), Rift Valley (Bomet, Kericho and Uasin Gishu counties) and Nyanza (Kisii and Homa bay counties) provinces of Kenya, respectively. Counties in the eastern region are in agro-climatic zones 3 to 6 and with a mean annual rainfall of less than 1100 mm. The other counties are in agro-ecological zones 1 to 3 and with a mean annual rainfall of more than 1700 mm (Sombroek et al 1982).

A total of 75 live chickens, mainly adults and a few growers were purchased while 56 other samples were obtained as parts of GI tracts from slaughter slabs within the trading centers.

Recovery and identification of gastrointestinal parasites

The GI tracts of the live chickens were obtained during the post mortem examination and separated into various parts namely: crop, proventriculus, gizzard, duodenum, small intestines (jejunum and ileum), caecum and large intestines. Each part was opened and contents emptied into separate containers. They were washed with water to retrieve all the worms clinging on the mucosa. The nematodes and cestodes from these parts were collected and put in separate containers with 70% ethanol. All the nematodes from each anatomical location were quantified. The helminths were processed according to procedures outlined by Gibbons et al (1996), and identified using helminthological keys of Soulsby (1982), Permin and Hansen (1998) and Norton and Ruff (2003).

A fecal sample was obtained from the cloaca or the contents of the large intestines from each bird during post mortem examination. This sample was used to determine fecal egg and coccidial oocyst counts using a modified McMaster technique (MAFF, 1986).

Data analysis

The data derived from these procedures was entered in Ms excel and exported to Instat® (2004) for statistical analysis. Analysis of variance using non-parametric one-way ANOVA (Conover 1980) for sex and place of origin was performed. The prevalence of GI parasites was defined as described by (Margolis et al 1982) and a critical probability of 0.05 was adopted as a cut-off point for statistical significance.

Results

Of the 131 chickens sampled, 118 had one or more adult species of GI helminths giving an overall prevalence of 90%. These chickens harbored an average of 37 worms per chicken with a range of 0-374 worms. Nine nematodes species were recovered namely: Heterakis isolonche (59.5%), Subulura brumpti (35.9%), Tetrameres americana (32.3%), Ascaridia galli (19.8 %), Gongylonema ingluvicola (19.1%), Acuaria hamulosa (6.1). H. gallinarum (5.3%) and Capillaria spp. (2.3%). Five cestodes species recovered included: Raillietina echinobothrida (37.4%),Hymenolepis carioca (33.6%), Davainea proglottina (6.9%), R. tetragona (6.1%) and R. cesticillus (2.3%) (Table 1). No trematodes were recovered in this study. Other endoparasites observed were Syngamus trachea (4.0%), which was identified in histological sections of lung tissues, the mite, Cytodites nudus (15.3%) in the air sacs and Sarcocystis spp. (5.6%) was identified in the neck muscles during microscopic examination.

The range of GI nematodes was as follows: T. americana (0-6), A. hamulosa (0-11), A. galli (0-12) and caecal worms ( H. gallinarum, H. isolonche and S. brumpti) 0-374 per chicken. The overall mean intensity of caecal worms was 36.3 and there was a significant difference in mean worm load between counties of bird’s origin (Fig. 1) but not between sexes.

Nineteen percent (25/131) of the fecal samples processed were positive for helminth parasite eggs while 14% (18/131) were positive for coccidial oocysts. The egg types encountered were: Ascaridia spp. (13.3%), Heterakis spp. (13.3%), Capillaria spp. (33.3%) and cestode eggs (40%).

Figure 1. Mean caecal worm counts in chickens originating from eight different counties of Kenya

Discussion

The present study disclosed a high infestation prevalence (90%) of GI parasitism in indigenous chickens in Kenya. These findings are comparable with previous reports (Ondawsy et al 2000; Irungu et al 2004; Okech et al 2006; Chege et al 2015) from different regions of Kenya. The prevalence rate of GI parasites of scavenging chickens was reported to be 90.21% in Ethiopia (Ashenafi and Eshetu 2004) and 100% in Zimbabwe (Jensen and and Pandy 1989). The parasites recorded were mainly helminths and comprised of nematodes and cestodes.

The high prevalence of GI helminth observed in free-range chickens in Kenya may be attributable to the type of production system, as proposed by Magwisha et al (2002). Under this system, local chickens roam from place to place usually seeking for food in the superficial layers of the soil. The soil is often contaminated with living organisms including those that serve as paratenic or intermediate hosts for helminths that infest poultry (Pandey and Jiang 1992; Ashenafi and Eshetu 2004).

Several nematode species as encountered in this study have been reported in variable numbers in indigenous chickens in tropical countries (Permin et al 1997; Poulsen et al 2000; Mukaratirwa et al 2001; Ashenafi and Eshetu 2004; Idika et al 2016) including Kenya (Irungu et al 2004; Chege et al 2015). The most prevalent nematodes were H. isolonche, S. brumpti and T. americana while, A. hamulosa, H. gallinarum and Capillaria spp. were recorded at lower prevalences. This was in contrast to earlier findings of a study conducted in Kakamega County where only four nematode species were reported, with H. gallinarum being the most prevalent followed by A. galli (Ondawsy et al 2000). Five more nematode species (i.e.,H. isolonche, S. brumpti, A. hamulosa. G. ingluvicola and Capillaria spp.) were recorded in the present study of 8 counties in Kenya. Strongyloides avium had been recorded in a previous study in Kenya (Irungu et al. 2004). Heterakis spp. and S. brumpti were isolated from the caecum and large intestines, although their predilection site is the caecum (Norton and Ruff, 2003). This observation was unusual and could be attributed to translocation of the worms from the caecum.

Five tapeworm species were recovered in this study with the most prevalent being R. echinobothrida followed byH. carioca, D. proglottina, R. tetragona and R. cesticillus.This was in agreement with the findings of Chege et al (2015) but differed from those of Ondawsy et al (2000) who encountered only one species, R. tetragona. Other studies conducted in East Africa recorded up to 10 species of tapeworms (Permin et al 1997).

Trematodes were not observed in this study and was in agreement with findings of Chege et al (2015) in Kenya, Yoriyo et al (2008) in Nigeria and Komba et al (2013) in Tanzania. However, other studies conducted in Kenya (Ondawsy et al 2000, Kyalo 2012), Uganda (Ssenyonga 1982) and Bagladesh (Islam et al 2004) recorded the presence of trematodes in chickens.

The study showed that caecal worm loads were significantly higher in warmer counties of Machakos, Makueni and Kitui compared to colder ones of Bomet, Kericho, Kisii and Uasin Gichu. It was also evident that some nematode worms like A. galli. T. americana, S. brumpti, H. isoloche and the cestode, R. echinobothrida were prevalent in all the counties. These variations could be due to differences in local environmental conditions (i.e., temperature, precipitation, humidity etc), which support larval development and facilitate transmission of these helminth parasites (Ashenafi and Eshetu 2004; Kyalo 2012).

The mean intensity of helminth infestations did not differ significantly between male and female chickens as was reported in studies conducted in Nigeria (Yoriyo et al 2008) and Morocco (Hassouni and Belghyti 2006). However, this was in variance with recent findings of Kyalo (2012) in Kenya. Mixed GI helminths and coccidia (Eimeria spp.) infestations were common and this may play a role in early chick mortality and other production losses among adults due to their combined devastating effects on the host metabolism (Nnadi and George 2010).

Conclusions

• This study demonstrated that GI helminths and coccidia were common in marketed indigenous chickens from different agro-ecological zones of Kenya.
• As these parasites may pose health problems, integrated control measures should be put in place to improve the health and productivity of scavenging rural chickens in the country.
• This would enhance smallholder farmer’s livelihoods in rural areas where most of the chickens are produced.

Conflict of interests

Acknowledgements

This study was financially supported by the DANIDA-LHRP funds, Dean’s grant No. 655-466 and ENRECA program on improving the health and productivity of the rural poultry in Africa grant No. 500-661-092.

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Received 22 August 2017; Accepted 27 August 2017; Published 1 December 2017

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