Prevalence and intensity of gastrointestinal helminth infestations of free range domestic ducks in Kenya

R M Waruiru, S K Mavuti¹, P G Mbuthia and L W Njagi

Department of Veterinary Pathology, Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Nairobi, P O Box 29053-00625, Kangemi, Nairobi
rmwaruiru@yahoo.co.uk
¹ Directorate of Veterinary Services, Ministry of Agriculture, Livestock and Fisheries, Kenya

Abstract

This study was undertaken to determine the prevalence and intensity of gastrointestinal (GI) helminths in naturally infested free range domestic ducks in Nairobi and its environs. One hundred and forty five ducks of different age groups and sexes were purchased from owners and post mortems conducted for worm recovery and identification. The data obtained was entered in Microsoft Excel and analyzed using Chi square (χ²), t-test and one way analysis of variance. An overall prevalence of 51.7% (n = 75) of the 145 ducks examined for GI helminths was recorded in this study. Prevalence rates for the various study sites (sub-counties) were 37.3% (Thika), 29.3% (Westlands), 26.7% (Embakasi) and 6.7% (Kasarani) while, ducklings had a prevalence of 40% followed by growers (37.3%) and adults (22.7%). Prevalence for females was 57.3% relative to 42.7% for male ducks.

Six (6) nematode species were recovered from different predilection sites of infested ducks. These were Gongylonema ingluvicola, Heterakis gallinarum, Ascaridia galli, Capillaria contorta, Subulura brumpti and Heterakis isolonche. Hymenolepis spp. was the only cestode recovered in the study. This study documents the occurrence of G. ingluvicola in ducks for the first time in Kenya. Out of 75 infested ducks, 46 (61.3%) were infested with single helminth species while 29 (38.7%) were infested with two or more helminths in varying combinations. The mean helminth worm infestations per duck in different study sites were 18.7 (Embakasi), 12.8 (Westlands), 11.3 (Thika) and 4.8 (Kasarani) while, growers had 17.5 followed by ducklings (9.8) and adults (5.9 worms). Mean worm count of males was 15.3 compared to 9.1 of female ducks. This study provides baseline data on prevalence and species distribution of helminths of domestic ducks in Nairobi and its environs. There is therefore need for further studies on epidemiology and economic significance of helminths of ducks raised under traditional free range management system in Kenya.

Keywords: age, gastrointestinal parasites, Gongylonema ingluvicola, Nairobi, nematodes, sex

Introduction

In Kenya, the livestock sector contributes 23% of the total Gross National Product and 10% of Gross Domestic Product (Kiptarus 2005). Poultry production is mainly subsistence and contributes close to 70% of the national egg and poultry meat output (Nzioka 2000). Poultry also provide enormous opportunity to the rural poor for generating family income and employment opportunities (Mbuthia et al 2003; Bebora et al 2005). The most commonly kept poultry in Kenya are chickens, geese, turkeys and ducks (Mbugua 1990).

Domesticated ducks estimated to be 300,000, form part of the 37.5 million poultry in Kenya (Anonymous 2008). They have a high potential as a source of food and income for rural, peri-urban and urban poor human population and are less susceptible to devastating poultry diseases (Muhairwa et al 2007).

Much emphasis in poultry research and development in East Africa has been placed on chickens (Magwisha et al 2002; Kemboi et al 2013; Nanyeenya et al 2013; Chege et al 2014; Ogada et al 2016) with little information on diseases, parasitism and management constraints of ducks (Cooper and Mellau 1992; Muhairwa et al 2007; Waruiru et al 2017).

Helminth parasites are common among indigenous poultry since they are kept outdoors and are in constant contact with soil (Pandey and Jiang 1992; Magwisha et al 2002) which is a source of infective stages of these parasites. Helminth infestations are associated with unthriftness, poor growth, reduced egg production and fertility and death in acute cases (Phiri et al 2007; Macklin 2018). Several investigations on helminths of chickens in Kenya have been undertaken by Ondawsy et al (2000), Kagira and Kanyari (2002), Irungu et al (2004), Chege et al (2015) and Maina et al  (2017). However, very little has been done to investigate and document important GI parasites of ducks in the country. This study was therefore conducted to investigate the prevalence and intensity of GI helminths of free range domestic ducks in peri-urban areas of Nairobi and Kiambu counties, Kenya.

Materials and methods

Study area

This study was conducted in three sub-counties of Nairobi County (i.e., Embakasi, Kasarani, Westlands) and neighboring Thika Sub-county in Kiambu County. The physiographic and natural conditions of the study area are as described by Anonymous (2014a, b).

Study ducks

One hundred and forty five (77 female and 68 male) ducks bred and raised (together with indigenous chicken) within the slums of the study area were purchased (in-situ) based on the availability of different age groups and sexes and the willingness of the owners to sell some of the birds (duckling, grower and adult) in their flocks. The slums were purposively chosen and sample size of study ducks was calculated as described by Thrustfield (1995). Sub-county distribution of the ducks was 51 (Embakasi), 23 (Kasarani), 37 (Thika) and 34 (Westlands), respectively. They were categorized into ducklings (<2 months), growers (2 to 6 months) and adults (>6 months) according to Magwisha et al (2002). Overall, 47 adults, 50 growers and 48 ducklings were sampled. The ducks were transported alive in cages to the laboratory for postmortem examination and helminth worm recovery.

Post mortem examination

This was done at the Department of Veterinary Pathology, Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Nairobi. The birds were thoroughly examined before being humanely euthanized. They were killed by cervical dislocation, followed by severing of the carotid arteries and jugular veins using a scalpel blade. A thorough post mortem examination was carried out as described by Charlton et al (2006).

Parasitological examination

Each GI tract was spread out on a dissecting board and separated into various segments (esophagus, crop, proventriculus, gizzard, small intestine and caecum). For regional recovery and identification of helminths, each segment was dissected with a scalpel blade to expose the lumen and the mucosa was scraped into a Petri dish containing physiological saline solution and examined under a stereo microscope for the presence of adult worms.

The mucosal scrapings were wet-mounted in glycerin-ethanol and examined under optical microscope at low magnifications of 10 and x40. All helminths recovered were counted before being fixed in 70% ethanol for processing as described by Gibbons et al (1996). Worms recovered were identified using helminthological keys of Permin and Hansen (1998) and Norton and Ruff (2003).

Data analysis

Data was entered in Ms-Excel and later exported to Genstat® Discovery edition 3 for descriptive statistics. The association of prevalence to study sites, age and sex groups was analyzed using Chi-square (χ2) test. A one-way analysis of variance was used to analyze influence of the worm burdens on the three age groups. The prevalence of parasites was defined as the total number of ducks infested with a particular parasite group, divide by the number of ducks examined at a point in time (Margolis et al 1982) . A critical probability of 0.05 was adopted throughout as a cut-off point for statistical significance between test groups.

Results

Prevalence of gastrointestinal tract helminths

Of 145 ducks sampled, 75 had one or more species of GI helminths, giving an overall prevalence of 51.7%. Majority of infested ducks were from Thika Sub-county (37.3%) while, others were from Westlands (29.3%), Embakasi (26.7%) and Kasarani (6.7%) sub-counties, respectively (p< 0.05). Ducklings had a helminth prevalence of 40%, growers 37.3% and adults 22.7% while, female ducks had a higher prevalence of 57.3% relative to males (42.7%). The worm prevalence among duck age groups and sexes was statistically significant (p< 0.05). Mean helminth infestation was 18.7, 12.8, 11.3 and 4.8 worms per duck in Embakasi, Westlands, Thika and Kasarani sub-counties, respectively. Growers had a higher mean worm count (17.5) relative to ducklings (9.8) and adult ducks (5.9). Among the sexes, males had a mean of 15.3 compared to female ducks with a mean of 9.1 worms (Table 1).

Six nematodes (Gongylonema ingluvicola, Heterakis gallinarum, H. isolonche, Capillaria contorta, Subulura brumpti, Ascaridia galli) and one cestode (Hymenolepis spp.) were recorded in this study. Infestation of ducks by Heterakis spp., G. ingluvicola and A. galli were observed in the four sub-counties, while C. contorta and S. brumpti were only observed in Thika and Westlands sub-counties. Hymenolepis spp. was only observed in ducks from Thika sub-county. Helminth infestations occurred either singly (46/75, 61.3%) or as mixed (29/75, 38.7%) infestations of more than one species in various combinations (Table 2).

Gongylonema ingluvicola

This nematode was only recovered from the oesophagi of ducks and had characteristic round or oval thickenings referred to as cuticular plaques or bosses on the cuticle at the anterior aspect. The tail of the male had papillae and spicules with the left spicule being slender and longer than the right one (Figure  1). The worm was recovered singly or as mixed infestation (Table 2) at a prevalence of 34.3% (12/35) in growers and 20% (7/35) in adults (p<0.05). This worm was not grossly observed in ducklings but microscopically, damage due to this worm was observed in 45.7% (16/35) of ducklings. The mean G. ingluvicola worm count was 2 and 1 worm per duck in adults and growers, respectively. Females had a prevalence of 51.4% (18/35) compared to male ducks of 48.6% (17/35) (p>0.05).

Figure 1. Anterior (A) and posterior (B) ends of Gongylonema ingluvicola from a duck showing cuticular bosses (arrow) and a short right spicule (arrow) (x100)

Ascaridia galli

Ascaridia galli worms were recovered from the small intestines of ducks and were the largest nematodes encountered. The worms were semi transparent and possessed three prominent lips around their mouths. The male worms had a prominent preanal sucker and two equal spicules (Fig. 2). Of the 21 ducks that had A. galli as single or mixed infestation (Table 2), 12 (57.1%) were ducklings, 8 (38.1%) growers and 1 (4.7%) adult duck (p<0.05). Males had a prevalence of 66.7% (14/21) relative to female ducks of 33.3% (7/21) (p<0.05).

The overall mean intensity of A galli was 14.7 worms with a range of 0-90 worms per duck. The mean worm count for growers was 29.6, ducklings (7.5) and adults (1.0) (p<0.05). Male worm count was higher (26.8) than in female ducks (7.9) (p<0.05).

Figure 2. Anterior end (A) and posterior end (B) of a male Ascaridia galli from the small intestines of a duck showing three prominent lips around the mouth (arrow) and a prominent preanal sucker (P) and two equal spicules (S) (x100)

Heterakis gallinarum

These were small white worms whose mouths were surrounded by three lips and possessed an oesophageal bulb containing vulvular apparatus (Fig. 3). The males possessed prominent circular pre-cloacal suckers and had two unequal spicules. The female vulva was situated directly behind the middle of the body. A total of 22/145 (15.2%) of the ducks had H. gallinarum. The number of worms per bird ranged from 0-69 worms. This worm had a prevalence of 45.5% (10/22) in growers, 36.4% (8/22) in ducklings and 18.2% (4/22) in adults (p<0.05). Females had a prevalence of 50% (11/22) equal to that of males (p>0.05).

Figure 3. Anterior end (A) and posterior end (B) of Heterakis gallinarum from the caecum of a duck showing oesophageal bulb containing vulvular apparatus (arrow) and prominent circular pre-cloacal sucker (P) and two unequal spicules (S) (x100)

Heterakis isolonche

These were small white worms, with three small prominent lips on the mouth and well developed oesophageal bulb. They were differentiated from H. gallinarum as the male worms had equal or sub-equal spicules (Fig. 4). Five out of 145 (3.5%) of the ducks had H. isolonche in their caeca and worm count per duck ranged from 0 to 6. This worm had a prevalence of 60% (4/5) in growers and 40% (2/5) in adults (p<0.05). Males had a prevalence of 60% (3/5) relative to female ducks of 40% (2/5) (p<0.05).

Figure 4. Posterior end of Heterakis isolonche from the caecum of a duck showing male worm with spicules that are equal (arrow) (x100)

Subulura brumpti

These were small white worms with a dorsally curved anterior end. The oesophagus had a small swelling posteriorly followed by a constriction and then an oesophageal bulb (Fig. 5). The tail of the male worm was ventrally curved with large lateral alae, equal spicules that did not extend beyond the body margin.  Of the 8 ducks that had S.brumpti, 6 (75%) were adult and 2 (25%) were growers (p<0.05). Females had a prevalence of 50% (4/8) equal to that of males (p>0.05).

The overall mean intensity of S brumpti found in the caeca of ducks was 2.6 worms with a range of 0-5 worms per duck. The mean S brumpti worm count was adults 2.6 worms; growers 2.0 worms and ducklings had none (p<0.05). Mean worm count for females was 2.5 while that for male ducks was 2.5 worms (p>0.05).

Figure 5. Anterior (A) and posterior (B) end of Subulura brumpti from the caecum of a duck showing dorsally curved anterior end with a small swelling (S) followed by a constriction (C) and an oesophageal bulb (E) and a ventrally curved tail with equal spicules (arrow) (x100).

Capillaria contorta

These tiny and hair-like worms were found in the oesophagus of ducks. Their body was thread like and was attenuated both anteriorly and posteriorly. The head of this worm was without a cuticular swelling. The isolated females had eggs with bipolar plugs (Figure 6).

Fourteen out of 145 (9.7%) of the ducks had C. contorta occurring either singly or as mixed infestation (Table 2). This worm had a prevalence of 42.9% (6/14) in adults, 42.9% (6/14) growers and 14.2% (2/14) in ducklings (p<0.05). Females had a prevalence of 78.6% (11/14) relative to male ducks of 21.4% (3/14) (p<0.05).

The overall mean intensity of C. contorta was 5.5 worms with a range of 0-31 worms per duck. Adult ducks had a mean worm count of 6.1 relative to growers 4.0 and ducklings 4.0 (p>0.05). Mean worm count for females was 6.0 while that for male ducks was 4.0 (p<0.05).

Figure 6. A part of a gravid Capillaria contorta female with bipolar plugged eggs (arrows)

Discussion

The study demonstrated the occurrence of helminths in different sex and age groups of ducks and prevalence was highest in Thika Sub-county (29.3%) but lowest in Kasarani Sub-county (6.7%). The mean helminth intensity was higher in Embakasi Sub-county (18.7) compared to Kasarani Sub-county with 4.8 worms per duck. The disparity of these findings may have been due to the variations in geo-climatic conditions of the study sites (Ashenafi and Eshetu 2004).

Helminth parasites were recorded at a prevalence of 51.7% with the prevalence and species distribution of nematodes (C. contorta, G. ingluvicola, H. gallinarum, H. isolonche, S. brumpti, A. galli) being higher than that of the cestode, Hymenolepis spp. The prevalence of single helminth species infestation was higher (61.3%) than mixed infestation (38.7%) as was reported by Paul et al (2015) in Nigeria. This study documents the occurrence of G. ingluvicola in ducks which has not been undertaken in Kenya.

Muhairwa et al (2007) found 52% endoparasitic infestation in ducks in Morogoro,Tanzania and demonstrated a total of 14 species of helminths which included A. columba, A. dissimilis, A. galli, C. anatis, C. contorta, C. annulata, H. dispar, H. gallinarum, H. isolonche, Raillietina echinobothridia, R. tetragona , Subulura strongyilina, S. sucturia and S. brumpti. They did not report occurrence of G. ingluvicola and Hymenolepis spp. in Tanzania, while the present study did not observe other species of Ascaridia, Capillaria, Heterakis, Subulura or Raillietina spp.

In Southwestern Nigeria, four different GI helminths were recorded with A. galli being predominant followed by H. gallinarum, Capillaria spp. and Echinuris uncinata (Adejinmi and Oke 2011). The latter worm was not observed in the present study. A total of seven nematode (A. galli, Trichostrongylus tenus, H. gallinarum, S. brumpti, C. contorta, C. annulata, Tetrameres fissipina) and three cestodes (Raillietina echinobothrida, R. tetragona, Hymenolepis cantaniana) species were identified in a recent study in Gombe, Nigeria (Paul et al 2015).

Farjana et al (2008) in Bangladesh reported that 96.6% of ducks were infested with seventeen helminth species which included 11 trematodes, 4 cestodes and 2 nematodes most of which were not found in the present study. Utpal and Biswas (1997) observed 34.3% endoparasitic infestations in ducks in West Bengal India and a total of nine different helminth species. Their study showed that trematodes comprised more than 26% of helminth infestation in the area, whereas cestodes and nematodes comprised 9% and 5%, respectively. They did not report occurrence of G. ingluvicola in Bangladesh and India.

Hymenolepis spp. was the only cestode recovered in the present study at a low prevalence of 1.3%. This was in contrast to Muhairwa et al (2007) who reported Raillietina species at a prevalence of 20.8%, Farjana et al (2008) reported 4 species of cestodes (H. coronula, H. lanceolata, Schillerius longiovum and Fimbriaria fasciolaris) and Utpal and Biswas (1997) found cestodes to comprise 9% of helminth infestation. Trematode helminths were not observed in the present study as was reported in Tanzania (Muhairwa et al 2007 and Nigeria (Adejinmi and Oke 2011) and unlike in India (Utpal and Biswas 1997) and Banglandesh (Farjana et al 2008). The lack of trematodes may be attributed to inavailability of free water in form of rivers, ponds or lakes which are habitats of snail intermediate hosts of trematodes as it was the case in this study (Soulsby 1982).

The helminths encountered in this study are common parasites of free range chickens (Muhairwa et al 2007; Mantur et al 2010) and may be due to the practice of rearing chickens and ducks as mixed flocks in most rural settings (Yakubu 2013). This practice allows them to share the same food, water and habitation which allow sharing of parasitic infestations (Adejinmi and Oke 2011). Also, the ducks' scavenging and amphibious habits expose them to high risk of parasitic infestations (Mantur et al 2010; Paul et al 2015).

In this study, prevalence of A. galli was higher in ducklings (57.1%) and growers (38.1%) relative to adult ducks (4.7%). This was as reported by Muhairwa et al (2007) who recorded a prevalence of 42.7% and 4.2% in ducklings and adult ducks, respectively. Also, they reported the prevalence of H. gallinarum to be 4.2% for ducklings and 24% for adult ducks. This was in contrast to the present study where prevalence was higher in growers (45.5 %) and ducklings (36.4%) relative to adult ducks (18.2%).

The mean worm intensity for A. galli was higher (29.6) in growers compared to ducklings (7.5) and adult ducks (1.0). This was in variance with findings of Muhairwa et al (2007) where mean worm count was higher in adult ducks (14.5) relative to ducklings (4.5). May be the latter compared ducklings and adults but had no grower ducks.

The overall helminth prevalence and intensity in ducklings and growers was significantly higher than that of adult ducks. This was as reported in Tanzania with prevalence of GI worms in ducklings being significant higher compared to adult ducks indicating that younger ducks were more susceptible to GI helminth than adults (Muhairwa et al (2007). Helminth prevalence was slightly higher in female than male ducks while mean worm intensity was higher in males compared to females. Tolossa and Tafesse (2013) recorded no significant difference in prevalence of helminth infestation of chicken between age groups and sexes in Ethiopia. However, this was in contrast with recent findings of Kyalo (2012) in Kenya.

Some of the helminths (i.e., A. galli and H. gallinarum) observed in ducks are pathogenic to chickens (Fowler 1996). Thus, further studies on the health status, blood parameters, feed efficiency conversion and growth rate should be undertaken to determine their economic impact with the aim of developing control measures of these worms to improve the health and productivity of the duck in Kenya.

Conclusions

• The study demonstrated that helminths were prevalent in apparently healthy free range domestic ducks.
  
  
• Single helminth infestation dominated mixed infestation with nematodes being more prevalent relative to cestodes.
  
  
• The study presents the first record of duck helminths in Kenya.
  
  
• Further studies on the importance of these worms in the growth and productivity of ducks under free range management system are indicated.

Conflict of interests

The authors declare that there is no conflict of interest

Acknowledgements

The authors thank Prof Carol J Cardona for availing material support through Avian Flu School, Poultry Health Development Project, University of California, Davis and Global Livestock Collaborative Research Support Program, USAID, for funding this study. We acknowledge Ms. Mary N. Mutune and Richard O. Otieno for their technical assistance and duck owners for their cooperation.

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Received 6 December 2017; Accepted 6 March 2018; Published 1 April 2018

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