Studies on seasonal prevalence of ecto- and endo-parasites in indigenous chicken of Mbeere Subcounty, Kenya

H W Chege, D C Kemboi, L C Bebora, N Maingi, P G Mbuthia, P N Nyaga, LW Njagi and J Githinji¹

University of Nairobi P.O. box 29053-0065 Nairobi, Kenya
wambuiche08@gmail.com
¹ Ministry of Livestock, Central Veterinary Laboratories, Private Bag, 00625, Nairobi, Kenya.

Abstract

A study was carried out to determine the seasonality of ecto- and endo-parasites in Mbeere Subcounty, Kenya. A total of 48 chicken were randomly selected and purchased from farms in the study area (24 in wet season and 24 in dry season). The chicken were of different ages (16 chicks, 16 growers and 16 adults) and sexes (19 males and 29 females).

All chicken in the 2 seasons had endoparasites, while ecto-parasites were found in all chicken in wet season and 95.8% of the chicken in dry season. Ectoparasites observed in both seasons were mites, lice, ticks and fleas. Lice were the most prevalent (wet season 100%; dry season 70.4%). In both wet and dry seasons the prevalences of endoparasites were: nematodes 95.8% and 87.5%, cestodes 87.5% and 83.3%, coccidia 20.8% and 0% and haemoparasites 79.2% and 62.5%, respectively. Heterakis species were the most prevalent nematodes. Other detected nematodes were Tetrameres americana and Gongylonema ingluvicola. Raillietina echinobothrida was the most prevalent cestode (wet season 79.2%; dry season 62.5%).  Other cestodes were; Raillietina tetragona, Davaenea proglottina, Hymenolepis cantaniana and Choanotaenia infundibulum. Among the recovered haemoparasites, Plasmodium gallinaceum was the most common (wet season 79.2%; dry season 62.5%). Results indicated that there was no significance difference in occurrence of most ecto- and endo-parasites in both seasons, among the age groups and sexes (p>0.05).

Key words: chicken, prevalence, wet and dry seasons

Introduction

The poultry industry in Kenya has over the years progressed to become an important livestock enterprise particularly in the rural households where over 70% of the country’s poultry keeping is attractive to poor households as they require low capital hence makes an important contribution to their livelihood (MoLD 2008). Endo- and ecto- parasites are common among indigenous chicken since they are kept outdoors where they scavenge and forage and in the process pick up the infective stages of the parasites. These parasites compete with the birds for nutrients; some suck blood causing anaemia, while others cause anorexia or death. Some ecto-parasites are important in transmission of certain pathogens, while others may cause disease such as scaly leg and depluming mange.

Heavy parasite burdens have been recorded in indigenous chicken in Eastern Province of Kenya.  Studies showed that most chicken from this area were infested with ectoparasites such as lice, mites, fleas and ticks as single or mixed infections (Sabuni 2009). The intensity of parasite infection was also significantly different among different age groups but not between sexes of birds. Study carried out by Maina (2005) on indigenous chicken sold at Nairobi markets reported high carriages of endoparasites. Tracing the birds to respective origins, she found that some of the birds were from Eastern province, which encompasses Mbeere Sub County. Previous research on seasonal parasites variation between March 2005 and August 2006 was conducted in Machakos Eastern Kenya (Mungube et al 2008) where endoparasites were found to be more prevalent during the wet season and the ectoparasites were more prevalent during the dry season. The seasonal occurrence of parasite types and intensity of both ecto and endoparasites in Mbeere, Subcounty chicken have not yet been determined. The aim of the present study was to establish parasite types and intensity in village chicken of Mbeere Sub-county in dry and wet seasons.

Materials and Methods

Study area

The research was conducted in Mbeere sub-county, Kenya. It has a bimodal pattern of rainfall with long rains falling between mid-March and June while the short rains occur from October to December. Most parts of the district receive less than 550 mm rainfall per year giving the area a marginal status on land usage for agriculture. The temperature ranges between 20-30^o C (Onduru et al 2002). The area has a high population of indigenous chicken, approximately 165,090 (KBS 2009). The study was conducted during the short rains - wet season (October/November/December) 2011 and in the dry season (January/February/March) 2012.

Study chicken

The target population included chicken of all ages in both  male and female chicks (< 2 months), growers (2-8 months) and adults (> 8 months of age) as described by (Magwisha et al 2002). 

A total of 24 birds were purchased during each of the two seasons (dry and wet) to establish parasite carriage. The birds were obtained from individual farmers using purposive sampling where each homestead sampled had at least 10 birds, managed entirely by free-range manner. All the chicken were transported alive in cages to the Department of Veterinary pathology, Microbiology and Parasitology, University of Nairobi where laboratory examination was done.

Blood smear preparation and Post-mortem examination of birds

Two thin blood smears were prepared and examined under the microscope for haemoparasites (Nemi 1986; Sabuni et al 2010). Post-mortem examination of birds was done as described by Charlton et al (2006).

 Examination of ectoparasites

The ectoparasites were collected from skin of   the body, legs and head. The birds were skinned and the whole skin together with feathers, head, and legs removed and stored in 70% alcohol. The parasites were identified according to their morphological characteristics using entomological keys of Soulsby (1982).

Faecal worm egg and coccidial oocyst counts

Total egg count and coccidial oocyst were performed using modified McMaster technique (MAFF 1986).

Data analysis

Data from the study was entered into Excel spread sheet and analyzed using GenstatR Discovery for descriptive statistics. Unpaired T-test was the stastical method use to assess the difference between the presence of parasites based on seasons. Chi-square statistical method (Fisher’s Exact Test) was used to evaluate association of prevalence to the age and sex based on seasons.

Results

Ectoparasites were found in all bird age groups and sexes during the wet season and in 95.8% (23/24) of the birds in the dry season. The overall seasonal prevalence of ectoparasites species identified in the wet and dry seasons is shown in Table 1.

The study found insignificant difference (p>0.05) for most ecto-parasites between the two seasons, among the age groups and between the sexes.

Adults and growers were 100% infested in both wet and dry seasons, while the chicks had a slightly lower infestation of 88.8% during the dry season. All males and females were all infested with ecto-parasites in the wet while during the dry season all females were infected while males were infected at a rate of 91.7%. Among the ectoparasites, lice were the most prevalent ectoparasites with an overall prevalence of 89.6% and seasonal occurrence of 100% and 79.2% in wet and dry seasons, respectively. There were more lice in the wet season than in the dry season (p<0.05) but not between the chicken ages and sexes (p>0.05). Menacanthus stramineus was the most prevalent louse in both seasons (Table 1).

In both the dry and wet seasons all ages and sexes of birds (100%) had endoparasites. The endo-parasites recovered during the wet and dry seasons are as shown in Table 2.

The most prevalent endoparasites were caecal worms and cestodes. The study found insignificant difference (p>0.05) for most endo-parasites between the two seasons, among the age groups and between the sexes.

The nematodes and cestodes species recovered from the gastrointestinal tracts of birds examined during the dry and wet seasons are shown in Table 3.

The caecal worms (Heterakis species, Heterakis isolonche, Heterakis gallinarum, Subulura brumpti) were the most prevalent nematodes isolated in both seasons (Table 3). The occurrence of caecal worms was slightly higher in the grower chicken [100% (8/8) and 100% (8/8)], than in adult birds [88.9% (8/9) and 100% (7/7)] and in chicks [85.7% (6/7) and 66.7% (6/9)] in wet and dry seasons, respectively. Female birds were more affected in both the wet and dry seasons than male birds. Female birds had 100% infection rate in wet season and 91.7% in the dry season while male birds had 87.5% infection rate in the wet season and 83.3% in the dry season. Most caecal worms occurred in the wet season, although there was no significant difference in occurrence of caecal worms between the two seasons, sexes and among the age groups (p>0.05). Heterakis species were the most prevalent caecal worm recovered in both the wet and the dry seasons (Table 3).

Eighty five percent (85.4%) of the chicken were infected with cestodes in both the wet and dry season. Cestodes were recovered more in adult birds in both wet and dry seasons, at rates of 88.9% (8/9) and 100% (7/7), respectively, compared to 100% (8/8) and 87.5% in growers and 71.4% (5/7) and 77.8% (7/9) in chicks, respectively. Female and male birds were equally affected with cestodes, at a rate of 87.5% each. Raillietina echinobothrida was the most prevalent cestode recovered in both seasons. There was no significant difference in the cestode occurrence among the age groups and between the two seasons and sexes (p>0.05).

Eight percent (4/48) of the faecal samples processed were positive for coccidial oocyst. These were mainly isolated during the wet season. Out of 48 chicken examined in the wet and dry seasons, 34 (70.8%) were infected with haemoparasites.

Four haemoparasite species identified were: Plasmodium gallinaceum 79.2% (19/24) and 62.5% (15/24), Leucocytozoon schoutedeni 29.2% (7/24) and 12.5% (3/24), Aegyptinella pullorum 4.17% (1/24) and 16.7 % (4/24) and Eperythrozoon species 16.7% (4/24) and 4.17% (1/24). The occurrence rates of haemoparasites were 79.2% (19/24) during the wet season and 62.5% (15/24) during the dry season. Adult chicken had prevalence rates of 88.9% (8/9) and 57.1 % (4/7), followed by growers at 87.5% (7/8) and 62.5% (5/8) and chicks at 57.1% (4/7) and 66.7% (6/9) in wet and dry seasons, respectively. Female birds were more infected in the wet season [at rate of 87.5% (14/16)] than male birds [at rate of 62.5% (5/8)] while during the dry season male birds were infected more [at a rate of 75.0% (9/12)] than females [at rate of 50.0% (6/12)]. There was a significant difference in occurrence of haemoparasites between the sexes (p<0.05) but not among the age groups and between the wet and dry seasons (p>0.05).

Discussion

In the present study, it is evident that the village chicken of Mbeere Subcounty had high prevalences of 99.0% for both ecto- and endo-parasites in the wet and dry seasons which indicates that parasitic infection is a common problem in this area. All ages and sexes of chicken were found to be infected with endo- and ecto-parasites. This is due to similar environmental stress factors such as shortage of food, water, extreme temperatures that depress the immune system. Similar observations have been reported in tropical African countries such as Zimbabwe (Permin et al 2002), Malawi (Njunga 2003) and Kenya (Maina 2005; Mungube et al 2008; Sabuni et al 2010 and 2011). In this study, the high prevalence of parasites observed in free range chicken can be attributed to the fact that the birds roam around in the village; hence the birds are in continuous contact with the parasites or the intermediate hosts of the parasites.

In this study, there was no difference in occurrence of both ecto- and endo-parasites between the wet and dry seasons. This is in contrast with previous findings by Mungube et al (2008) who recorded endoparasites as being more in the wet season and ectoparasites more prevalent in the dry season. Variations in the results could be attributed to different climatic conditions; Mbeere lies in Agro Ecological zone 5 while Yathui division (Machakos county) where Mungube et al (2008) did the study lies at Agro Ecological zone 4 and 5 (Jaetzold and Schmidt 1983).This persistent occurrence of the parasites in both seasons in the current study could be explained by the fact that transmission of the respective parasites was not affected by the weather changes in the study area.

In this study, all the chicken in the wet and dry seasons harboured ectoparasites with a prevalence rate of 100% in the wet season and 95.8% in the dry season.  Similar findings have been reported in village chicken in Zimbabwe (Permin et al 2002), and Kenya (Maina 2005; Sabuni et al 2010). The ectoparasites detected in all the age groups and sexes were lice, fleas, ticks and mites. In the wet and dry seasons, all the adult and grower birds were 100% infested. During the dry season the chicks had a slightly lower prevalence of infestation (88.8%). This may be attributed to similar management system hence high prevalences among all the age groups in both seasons. Although there was no significance difference in occurrence of ectoparasites among the age groups; chicks had a low prevalence compared to adults and growers, this could be due to small body size for ectoparasites infestation.

Ectoparasites are associated with poor hygiene in the farm/chicken houses. The poor hygiene conditions, including the fact that all ages of birds are housed together, therefore, facilitate the spread of ectoparasites like lice, mites and ticks. Most farmers do not clean the chicken houses whose litter harbor eggs of some ecto-parasites like fleas and lice. Lice were the most prevalent ectoparasites. This is similar to previous findings in Kashmir valley (Salam et al 2009) and Kenya (Sabuni et al 2010). It is, however, in contrast to previous findings by Maina (2005) and Mungube et al (2008) where the stick tight flea (Echidnophaga gallinacea) was found to be the most prevalent at rates of 56% of 75 chicken and 76.7% of 360 chicken examined (Mungube et al 2008). This could have been attributed to climatic differences in the study areas.

Lice were common in the wet season compared to the dry season. This is in contrast to the previous findings in Kashmir valley (Salam et al 2009) where lice were found to be more prevalent during the dry season than the wet season. In the wet season in Mbeere, chicken tend to hurdle together for warmth which could facilitate the spread of the lice. The high prevalence in the wet season could also be explained by permanent housing during the planting season when the chicken are confined. Menacanthus stramineus was the most prevalent lice in concurrence with previous report of 71.4% (Mungube et al 2008). It is, however, contrary to the findings in Kashmir valley (Salam et al 2009) where Lipeurus caponis was the most prevalent at a rate of 96.9% of 478 chicken examined and in Kenya (Sabuni et al 2010) where this parasite was not recorded but Menopon gallinae was found to be the most prevalent. This may be attributed to difference in the period of study.

The stick tight flea (Echidnophaga gallinacea) was recorded in both wet and dry seasons, at rates of 62.5% and 29.2%, respectively. Mungube et al (2008) and Permin et al (2002) recorded higher rates of 76.7% of 360 chicken and 73% of 100 chicken examined, respectively. The variation in prevalence rates of the flea is likely due to climatic factors between the areas. This flea causes the chicken to become restless and scratches affected area (Taylor et al 2007).

Argas persicus the only tick isolated in both seasons occurred at a rate of 50%; unlike previous reports in Zimbabwe (Permin et al 2002) with prevalences of 6% and 14% for adults and young chicken and in Kenya (Maina 2005; Mungube et al 2008; Sabuni et al 2010) with prevalences of 29.3% of 121, 11.1% of 360 and 5.6% of 144 chicken examined, respectively.  The differences could have probably been due to different environmental factors in the study areas. The nymphs and adults of the tick are temporary obligate parasites and only visit the bird while feeding, indicating the prevalence recorded in this study could have been higher.

All the village chicken had endoparasites in both the wet and dry seasons. Among the nematodes encountered, caecal worms (Heterakis species and Subulura brumpti) were the most prevalent in both the wet and dry seasons. This is in contrast with the previous findings by Mungube et al (2008) who reported Ascaridia galli to be the most prevalent nematode at a rate of 33.3% of 360 chicken examined. In the current study, Ascaridia galli was not isolated because most farmers mainly used piperazine citrate which is effective against it. The findings of this study are however, supported by the report of Maina (2005), who also recorded caecal worms as the most prevalent. Heterakis gallinarum was the least common caecal worm in contrast to a study conducted in semi-arid zone of Kenya (Mungube et al 2008) where he found Heterakis gallinarum to be more common at rate of 22.2% .The differences could have probably been due to different climatic factors in the study areas.

Also, another study carried out in Zimbabwe (Permin et al 2002) documented Heterakis gallinarum was the most common nematode with a prevalence of 64% and 62% in young and adult chicken, respectively. In this study, female birds were affected by caecal worms more than the males in both seasons, although there was no association in occurrence of the caecal worms among the age groups and between the sexes; this, however, needs to be investigated further.  The caecal worms may contribute to poor productivity of village chickens. The high prevalences of caecal worms in the wet and dry seasons may be attributed to constant contact of chicken with the intermediate hosts (earthworms) throughout the two seasons. It was also noted that the farmers were only aware of piperazine citrate (AscarexR) as an anthelmintic for chicken (Chege et al 2014).  The drug does not remove the caecal worms, which could explain the high prevalence of the worms.

Other nematodes recorded with lower rates of prevalence included Tetrameres americana. Both males and females of this parasite were isolated. Maina (2005) who studied the occurrence of helminths in chicken from markets in Nairobi only reported the occurrence of female parasites but no males. The management practice of the source of the sample of birds could have also brought the differences; in this study the birds were entirely managed by free-range manner hence more contact with the intermediate hosts. Infected chicken with Tetrameres americana may lose weight and become anaemic (Permin and Hansen, 1998).

Gongylonema ingluvicola was isolated at a rate of 29.2% and 8.3% in wet and dry seasons, respectively. The parasite was also found in ducks at a rate of 24.1% of 145 ducks examined (Mavuti 2010). It occurred more in the wet season than the dry season due to high population of beetles that act as intermediate hosts.

Cestodes were present in the wet and dry seasons at high prevalences of 87.5% and 83.3% respectively. The high prevalences of cestodes recorded in this study can be attributed to the scavenging diet that includes variety of earthworms that act as intermediated hosts of these parasites. Raillietina echinobothrida and R. tetragona were the two commonly isolated cestodes in the chicken while Hymenolepis cantaniana, Choanotaenia infundibulum, Davainea proglottina were a rare species. Female and male birds were equally infected with cestodes, at a rate of 87.5% each. This could be attributed to similar management system; reproductive system of the bird seems not to be directly related. There was no difference in occurrence of these tapeworms between the wet and dry seasons. This could be attributed to the fact that tapeworms live for extended periods of time in the intestines of untreated hosts (Soulsby 1982). Piperazine citrate, the anthelmintic used by most farmers in the study area, is not effective against cestodes.

Raillietina echinobothrida was the most prevalent cestode at 79.2% and 54.2% in the wet and dry season, respectively. This concurs with previous reports by Maina (2005) and Mungube et al (2008) who reported that the parasite was most prevalent although they recorded lower prevalence rates of 37.4% and 33.3%, respectively. Prevalences of between 34% and 81% have been reported by Permin et al (1997; Poulsen et al (2000); Permin et al (2002); and Irungu et al (2004). Raillietina tetragona had a high prevalence of 54.2% and 37.5% in wet and dry seasons, respectively. In contrast, a study conducted by Kaingu et al (2010) reported a lower prevalence of 13.2% of 710 chicken examined. This variation could be caused by different climatic factors.

In the present study, coccidial oocysts were only reported in the wet season with a low rate of 16.7%. A study conducted in Kenya by Kaingu et al (2010) reported coccidial oocysts at prevalence of 25.6%. The reason why coccidial oocysts were found in the wet season is due to conducive weather conditions that favour their survival.

Haemoparasites were recorded at a rate of 70.8% in both seasons. During the wet season more chicken (79.2%) were infected with haemoparasites than during the dry season (62.5%). This agrees with previous findings in Malawi (Njunga 2003) and in Kenya (Sabuni et al 2011) where prevalences of 71.0% and 79.2%, respectively were recorded. The high prevalence in wet season could be due to favourable climatic conditions for the vectors. There was no difference in occurrence of haemoparasites in the two seasons. This could have been due to presence of vectors of the haemoparasites during both the wet and dry seasons.

Plasmodium gallinaceum was the most prevalent (70.8%) haemoparasite in both seasons. This was slightly higher than 53.7% reported by Sabuni et al (2011) and 14.9% reported by Permin et al (2002). The prevalence of P. gallinaceum was higher during the wet season compared to the dry season. This can be attributed to the fact that mosquito vectors are usually more prevalent during the wet season compared to the dry season. All ages were affected by P. gallinaceum during the two seasons. Plasmodium gallinaceum is highly pathogenic to chicken causing anaemia and paralysis when the number of parasites in blood capillaries is high. Infections can also result in high mortalities in the chickens (Soulsby 1982).

Leucocytozoon schoutedeni had a prevalence of 20.8% in both seasons. This was lower than previous reports in Tanzania (Fallis et al  1973) and Kenya (Sabuni et al 2011), giving prevalence rates of 50% of 150 chicken and 52.1% of 144 chicken examined, respectively. This could have been accounted by different climatic conditions and localities. Leucocytozoon schoutedeni causes anaemia in chicken (Permin and Hansen, 1998).

This study records Aegyptinella pullorum in chicken in Kenya for the first time although it has been reported previously in ducks (Mavuti 2010). The parasite occurred at a rate of 8.33% during both the dry and wet seasons. These results are in agreement with previous findings in Zimbabwe where a rate of 7 and 6% for adults and young chickens was recorded (Permin et al 2002). Aegyptinella pullorum is transmitted by soft ticks mainly Argus persicus which hides in the chicken house and attacks the birds mainly during the night (Soulsby 1982).

This study also records the occurrence of Eperythrozoon species in chicken in Kenya for the first time. The parasite occurred at a rate of 10.4%, which is slightly higher than that previously reported in ducks in Kenya (3.35%) by Mavuti (2010).

Conclusions

• Ecto- and endo-parasites were found to be common in the study area with high prevalences of 97.9% and 100%, respectively in the wet and dry season.

  
  

• There was no difference in occurrence of  ecto- and endo-parasites between the two seasons. In the current study area, sex and age had no significant influence on seasonal prevalence of most ecto- and endo-parasites in chicken.

Recommendations

There is need for vigorous control measures for both ecto- and endo-parasites in chicken in the study area.

Acknowledgements

The authors thank RUFORUM for their sponsorship and funding of the project, the University of Nairobi for providing the work space  and facilities, Richard Otieno, Rose Nyawira and Rebecca Githinji for their technical assistance and the farmers of Mbeere for their cooperation.

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Received 16 April 2015; Accepted 16 April 2015; Published 3 June 2015

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