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Prevalence of helminths infestation in indigenous free-ranging chickens in different ecological zones in Zambia

I Chilinda, J C N Lungu, I K Phiri1, O C Chibinga and J Simbaya

Department of Animal Sciences, School of Agricultural Sciences, University of Zambia, P O Box 32379, Lusaka, Zambia
oschibinga@gmail.com
1 Department of Clinical Studies, School of Veterinary Medicine, University of Zambia, P O Box 32379, Lusaka, Zambia

Abstract

A study was conducted to determine the prevalence of helminths in free ranging indigenous chickens from three different agro-ecological zones in Zambia: Region 1 in Siavonga district, Region 2 in Chibombo district and Region 3 in Mpongwe district. Examination of helminths from gastrointestinal tracts of 96 chickens revealed a 95.8% prevalence rate. The helminths species and their prevalences were: Tapeworm (Raillietina spp) (70.8%), Allodopa suctoria (66.7%), Tetramere americana (54.2%), Heterakis gallinarium (53.1%), Gongylonema ingluvicola (42.7%), and Ascaridia galli (40.6%). The intensity of helminths was lower in birds from agro-ecological zone I (13.5%) compared to birds from region II (43.9%) and region III (42.7%) (P>0.05). These results confirm the higher prevalence of helminths infections in free range indigenous chickens as well as the differences of infections in different agro-ecological zones. Because of this high prevalence rate there is need to integrate appropriate control strategies in each ecological zone in order to improve the indigenous chicken productivity and improve livelihoods of local farmers

Key words: agro ecological zones, endo parasites, indigenous chickens


Introduction

The Indigenous Village Chicken population in Zambia is estimated at 15,391,150 and constitute 56.97% of the poultry population (MFL 2018). Village chicken production is widespread among rural farmers in Zambia because such chickens provide immediate proteins and cash to poor rural communities (Syakalima et al 2017). Indigenous 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) (Maina et al 2017). The potential of indigenous village chickens is enormous in meeting the needs of the local people. However, their potential 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 2000). 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 (Chege et al 2015). Most traditional village poultry is free range and scavenging therefore, there is permanent contact with soil and insects. Soil, especially when humid and warm, may serve as an important reservoir and transmission site for external larval stages of helminths (Permin et al 1997; Horning et al 2003). The exposure to this kind of environment may be responsible for high prevalence of helminths in free ranging chickens. Parasitism due to gastrointestinal 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 on indigenous free range birds have shown high prevalence of both external and internal parasites (Sabuni et al 2013; Idika et al 2016: Waruiru et al 2017). However, few studies have been conducted on the prevalence and intensity of helminth in different ecological zones. The aim of this study was therefore to determine the type, prevalence and intensity of endoparasites affecting free range indigenous chickens from three agro-ecological zones in Zambia.


Materials and methods

Study area

This study covered the three agro-ecological zones in the country. The research area included one district, from each of the three agro-ecological zones in Zambia; namely Siavonga district in agro-ecological region I, Chibombo district in agro-ecological region II, and Mpongwe district in agro-ecological region III. The agro-ecological region I lies in the Southern parts of Western, Southern and Eastern provinces and the mean annual rainfall in this region is low and does not exceed 800mm (Nambeye and Chibinga 2016). It is characterized by relative high temperatures and during growing season, mean daily temperatures may vary from 20 ºC to 25 ºC. The mean are as high as 38 ºC in October and in the cold season may expect mild to severe frost (Muliokela 1995). Region II covers the central part of Zambia extending from east to west. The region receives medium annual rainfall of between 800 and 1000mm. The mean daily temperatures during the growing season range from 23 ºC to25 ºC. The agro-ecological region III covers Northern, Luapula, Copperbelt and North western Provinces. The mean annual rainfall in the region exceeds 1000mm and the mean monthly temperatures during the growing season vary from 16 ºC to 28 ºC. The selection of the district in each region was based on the availability of the free-ranging indigenous rural poultry population.

Study subjects

The chickens collected from the three districts were indigenous breeds reared traditionally. From each district, representing an agro ecological zone 32 birds were purchased. A total of 96 chickens were examined to ascertain the influence of agro ecological zone on prevalence of helminthes. The chickens were slaughtered, dissected and checked for helminths in various parts of the gut. The digestive tract of each chicken was divided into esophagus, crop, proventriculus, gizzard, small and large intestines and caecum. Each part was opened in separate containers. The helminths were identified and counted.

Recovery and identification of gastrointestinal parasites

Each chicken was slaughtered and the intact gastrointestinal tract was extracted. The segments were then opened and observed washed according to the different gastrointestinal segments, (being gullet, crop, the proventriculus, the gizzard, the intestines and the caecum). The contents were then examined under a stereomicroscope for the collection, counting and identification of the nematodes (Permin and Hansen 1999). The mucosae of the various parts of the intestines were scrapped off using a forceps, into a sedimentation beaker. Nodules on the gizzard, when present, were opened under a stereoscopic microscope and worms removed. Nematodes were observed and identified from the washings and scrapings using a stereoscopic microscope. All parasites collected were preserved in 70 % ethanol for later identification using morphological parameters and the helminthological keys according to Soulsby (1982) and Permin and Hansen (1999) and Norton and Ruff (2003).

Data analysis

Data from the study were entered in Ms- Excel and later exported to SPSS (SPSS Institute, Chicago, IL, USA) for descriptive statistical analysis. Kruskal Wallis one-way analysis of variance (Minitab Edition 3) was used to analyze the influence of three agro-ecological zones on the prevalence and parasite burden (intensity). The prevalence of parasites was defined as the total number of chickens infested with parasites divided by the total number of chickens examined at a point in time (Margolis et al 1982). The intensity of the infection as defined as the number of parasite per chickens (Bush et al., 1997). A critical probability of 0.05 was adopted throughout as a cut-off point for statistical significance between groups compared.


Results

Out of the ninety six (96) chickens that were examined ninety two (92) or 95.8% were infected with gastro intestinal helminths. A total of six (6) helminthes species were found in the chickens. The prevalence of the parasites was Raillietina spp (Tapeworms) 70.8%, Allodapa suctoria 66.7%, Tetramere Americana 54.2%, Heterakis gallinarium 53.1%, Gongylonema inguluvicola 42.7% and Ascaridia galli 40.6%, (Figure 1).

Figure 1. Prevalence of various helminths found in indigenous chickens

The results revealed that there were significant differences among agro ecological zones in the prevalence of parasites as shown in Table 1. The prevalence of Gongylonema ingluvicola, Tetramere americana, Ascaridia galli and Raillietina spp (Tape worms) were significantly lower in region one compared to the other two regions (p<0.05). The prevalence of Allodopa suctoria was similar in regions I and II but was significantly lower than in region III (p<0.05) while the prevalence of Heterakis gallinarium was similar in all the regions (p>0.05).

Table 1. Parasite prevalence by percentage (%) in each ecological zone

Helminth

Region I
(%)

Region II
(%)

Region III
(%)

p

Gongylonema ingluvicola

18.7a

46.9b

62.5b

<0.002

Tetramere americana

6.25a

78.1b

78.1b

<0.001

Ascaridia galli

18.7a

46.9b

56.2b

<0.006

Raillietina spp

46.9a

81.2b

84.4b

<0.001

Allodopa suctoria

62.5a

50.0a

84.4b

<0.014

Heterakis gallinarium

59.4

43.8

56.2

0.45

ab Means without common superscripts are different at p <0.05

Furthermore, each parasite species was counted and the total was recorded in order to compare the intensity of the internal parasites by region..Ascaridia galli had5 the lowest number of ninety eight (98) while Allodopa suctoria had the highest number (1133) as shown in Table 2.

Table 2. Helminths intensity (number of parasites) by region counted in the different sections of gastrointestinal tract

Parasite

Region I

Region II

Region III

Total

Gongylonema ingluvicola

8

60

105

173

Tetramere americana

2

244

363

609

Ascaridia galli

43

32

23

98

Raillietina spp

46

85

59

190

Allodopa suctoria

141

560

432

1133

Heterakis gallinarium

103

136

104

343

343

1117

1086

2546

Ecological share of helminthes by percentage showed that region one (1) had the smallest intensity (13.5%) share while regions two (2) and three (3) had almost the same percentage of 43.9% and 42.7% respectively as shown in Figure 2.

Figure 2. Eco-regional Intensity of helminthes found in indigenous chickens


Discussion

The results of this study show that the prevalence of helminths in indigenous fee range chickens is 95.83 %. This figure is similar to what Phiri et al (2007) reported of 95.2 % in central Zambia. Similar observation of such high prevalence of endoparasites have been reported in other tropical African countries such as Kenya (Ondawsy et al 2000; Okech et al 2006; Chege et al 2015), Ethiopia (Ashenafi and Eshetu 2004) and Zimbabwe (Jensen and Panday 1989). This high incidence of helminths is as a results of the management system whereby birds are left fend for themselves and are exposed to conditions supporting their infection. They feed on one place to another and sought their food in the surface layer of the ground. This latter is generally infected with a large variety of living organisms including insects and worms which could be intermediate hosts of certain parasites (Slimane 2016). The chickens scavenge for food and water in an environment infested with a number of gastrointestinal parasites and other disease-causing pathogens to such an extent that they are continuously feeding on different and infective stages of parasites (Permin et al 2002). Abdu 1987, also indicated that, the intensity of worms in the gastrointestinal tracts of the birds might be due to continuous ingestion of infested droppings or infested intermediate hosts of organisms such as beetles, cockroaches, earthworm, flies and grasshoppers in poorly managed stocks. Lack of control measures towards these parasites is a possible factor contributing to the high prevalence of the parasites.

These helminths encountered in this study have also been reported in variable numbers in indigenous free range chickens in tropical countries (Ashenafi and Eshetu 2004; Chege et al 2015; Idika et al 2016) and the same number of helminths was also reported in central Zambia by Phiri et al (2007). The most prevalent helminth was Raillietina spp (70.83%) and the least prevalent was Ascaridia galli (40.6%). The intestinal helminthes appear to be highly prevalent in the local chickens as observed from this study but receive little attention as compared to the bacterial and viral diseases because the impact of diseases is noticed outright. There were no parasites found in the trachea and the gizzard and this is in line with findings described by other researchers in Zambia (Chota 2009; Phiri 2007).

Ascaridia galli is one of the most common helminth species in chickens, it is important to mention that despite certain species (Allodopa suctoria) having a high number they are relatively smaller in size while Ascaridia galli is relatively larger and as such tend to cause much more damage. Ascaridia galli shows high prevalence especially in free range chickens in rural areas (Wilson et al.1994). The observed prevalence (40.6 %) of Ascaridia galli in the current study was lower than the prevalence reported in guinea fowls in Nigeria (Jajere et al 2018). Ascaridia galli causes blood-tinged diarrhea, loss of appetite, increased thirst, birds looking dropsy, head nodding down wards, puffing or ruffled feathers and shivering emaciated and dirty cloacal region, as reported by several researchers (Negesse 1991) In heavy infection of Ascaridia spp this leads to obstruction, dilation and mild to necrotic ulcer in small intestine.

The nematode, Heterakis gallinarum is non-pathogenic, but a vector for Histomonas meleagridis which is highly pathogenic etiologic agent of “Black-head” disease lethal to chickens, turkeys, pheasants and other fowls. The presence of this parasite in free-range backyard chickens may cause severe debility and morbidity, while mortality may occur in extreme cases (Adang et al 2008).

The prevalence rate of Raillietina spp was determined at 70.83% in local chickens in the current study, a study done in Shibuyunji area in Lusaka (Ziela 2000) recorded 100% prevalence. The high prevalence of Raillietina spp. could be attributed to the wide spread and accessibility of intermediate hosts (dung beetles, ants) to the local chickens. Dung beetles and ants were commonly observed in study areas referred to in this study. Dung being a breeding home for beetles is readily available and as such Beetles are rampant and so escalate the survival of tapeworms. Although cestodes in poultry are known to cause retarded growth, enteritis, diarrhoea, haemorrhages and hypovitaminosis B, heavy infections may also be associated with mortality in young birds and the loss of egg production in laying chickens. Furthermore, Raillietina spp is considered as an infectious agent in chickens (Soulsby 1982).

The study showed that the helminths loads were higher in wetter regions of the country compared to the drier region. This exhibition significant differences across regions and this can be attributed to the differences in the climatic conditions obtaining in the three (3) agro-ecological zones which have an effect on the survival of both the parasites as well as the intermediate hosts for the parasites that require an intermediate host. The variation in the prevalence rates reported in this study can be ascribed to variation in geographical location and climate of the different districts from which birds were sampled. There was a geographical pattern with regard to the overall distribution of the species with region two and three being on the higher side. The high intensity (43.9% and 42.7%) of helminthes in regions II and III can be attributed to high rainfall leading to high humidity, dense vegetation cover and conducive temperatures for the survival of helminthes as compared to region I (13.5%), which has lower rainfall and extreme temperatures. This means that differences between the climates influence the biological cycle of these helminths and depends on the creation of micro-environment favourable for the survival and transmission of the infesting larvae and eggs of the parasites (Slimane 2016) and the finding in this study is in agreement. Soil, especially when humid and warm, may serve as an important reservoir and transmission site for external larval stages of helminths (Permin et al 1997; Horning et al 2003). Increased precipitation levels could prevent desiccation of eggs/larvae thus allowing greater survival rates of these parasites and similarly, increased humidity levels would increase larval survival in soil (Weaver et al 2010). Muchadeyi et al (2007) also indicated that the agro-ecological zone influences the type of feed animals’ have as well as disease and parasite pathogen profiles.


Conclusions


Acknowledgements

This study was financially supported by Organic Institute for Sub-Sahara Africa (OISSA) for their financial support towards this research.


References

Abdu P A 1987 Infectious bursal disease in pullet chicks. Avian Dis. 1987;31:204–205. doi: 10.2307/1590797.

Adang K L, Oniye S J, Ajanusi J O, Ezealor A U and Abdu P A 2008 Gastrointestinal Helminths of the Domestic Pigeons. Columba livia domestica Gmelin, 1789 Aves:Columbidae in Zaria, Northern Nigeria. Publication of Faculty of Science, Kaduna State University; World Journal no. 3: 33–37.

Ashenafi H and Eshetu 2004 Study on gastrointestinal helminths of local chickens in Central Ethiopia. Revue de Médecine Vétérinaire 10 504-507.

Bush A O, Lafferty K D, Lotz J M and Shostak A W 1997 Parasitology meets ecology on its own terms: Margolis et al. revisited Journal of Parasitology, 83 (1997), pp. 575-583

Chege H W, Kemboi D C, Bebora L C, Maingi N, Mbuthia P G, Nyaga P N, Njagi LW and Githinji J 2015 Studies on seasonal prevalence of ecto- and endo-parasites in indigenous chicken of Mbeere Subcounty, Kenya. Livestock Research for Rural Development. Volume 27, Article #113. Retrieved June 10, 2020, from http://www.lrrd.org/lrrd27/6/cheg27113.htm..

Chota A, Sikasunge C S, Phiri A M, Musukwa M N, Haazele F and PhiriI K 2010 A Comparative Study of the Efficacy of Piperazine and Carica Papaya for the Control of Helminth Parasites in Village Chickens in Zambia. Tropical Animal Health Production. 42(3):315-8. doi: 10.1007/s11250-009-9432-6

Horning G, Rasmussen S, Permin A and Bisgaard M 2003 Investigations on the Influence of Helminth Parasites on Vaccination of Chickens against Newcastle Disease Virus under Village Conditions. Tropical Animal Health and Production 35, 415–424 (2003). https://doi.org/10.1023/A:1025863412078

Hunduma D, Regassa C, Fufa D, Endale B and Samson L 2010 Major constraints and health management of village poultry production in Rift Valley of Oromia, Ethiopia. American-Eurasian Journal of Agriculture and Environmental Sciences 9: 529-533.

Idika I K, Obi C F, Ezeh I O, Iheagwam C N, Njoku I N and Nwosu C O 2016 Gastrointestinal helminth parasites of local chickens from selected communities in Nsukka region of south eastern Nigeria. Journal of Parasitic Diseases40 (4) 1376–1380.

Jajere S M1, Lawal J R2, Atsanda N N3, Hamisu T M4Goni M D5 2018 Prevalence and burden of gastrointestinal helminthes among grey-breasted helmet guinea fowls (Numida meleagris galeata) encountered in Gombe state, Nigeria.International Journal of Veterinary Science and Medicine, 17 May 2018, 6(1):73-79. DOI: 10.1016/j.ijvsm.2018.04.007.

Jensen J and Pandy V S 1989 Observation on helminths parasites of domestic fowls in Zimbabwe. Zimbabwe Veterinary Journal 20 (1):15-17

Maina A N, Waruiru R M, Mbuthia P G, Munyua W K, Otieno R O and Mutune M N 2017 Prevalence of gastrointestinal parasites in indigenous chickens slaughtered at live bird markets of Nairobi County, Kenya. Livestock Research for Rural Development. Volume 29, Article #233. Retrieved June 4, 2020, from http://www.lrrd.org/lrrd29/12/rmwa29233.html

Margolis L, Esch, G W, Holmer J C, Kuris A M and Schad G A 1982 The use of ecological terms in parasitology. (Report of an ad hoc Committee of the American Society of Parasitologists. Journal of Parasitology 68: 131-133.

Ministry of Fisheries and Livestock (MFL) 2018 Central Statistical Office The 2017/18 Livestock and Aquaculture Census Report. Ministry of Fisheries and Livestock Lusaka Zambia

Muchadeyi F C, Wollny C B A, Eding H, Weigend S, Makuza S M and Simianer H 2007 Variation in village chicken production systems among agro-ecological zones of Zimbabwe. Tropical Animal Health and Production. Volume 39, pp 453-461.

Muliokela S 1995 Zambia Seed Technology Handbook, Ministry of Agriculture, Food and Fisheries. Lusaka Zambia.

Nambeye E and Chibinga O 2016 Nutritive value of some selected indigenous livestock browse species in the drylands of Southern Province, Zambia . International Journal of Applied and Pure Science and Agriculture 2 (1)

Negesse T 1991 Survey of internal parasitesof local chickens of southern Ethopia. Indian journal of poultry scienceVolume 22 Issue 2 pp 128- 129.

Norton R A and Ruff M D 2003 Nematodes and acanthocephalans . In: Saif YM, Barnes Glisson H. J, J. R, Fadly A. M, McDougald L. R., Swayne D. E. Disease of Poultry. 11, Ames, USA: Iowa State University Press pp 931-961.

Nzioka M 2000 Indigenous poultry production in the Katumani mandate District. Constraints and prospects. In: Proceedings of the End of Project Conference. Kenya Agricultural Research Institute headquarters, Nairobi, Kenya. 29 th Nov-1st Dec. 2000. pp. 213-226.

Okech B A, Irungu L W and Cooper J E 2006 Helminthiasis in free-range indigenous domestic poultry in Kenya. Bulletin of Animal Health and Production in Africa 54: 92-99.

Ondawsy H O, Okitoi L O, Obali M P, Simwa S M and Wakhusama, S M 2000 Epidemiology of helminthes in indigenous chicken in western Kenya: Proceedings of the 7th scientific conference, collaborative research for sustainably improved livelihoods. 13th -17th Nov. 2000. pp. 407-412.

Permin A, Esmann J B, Hoj C H, Hove T and Mukatirwa S 2002 Ecto-, Endo- and Haemo-parasites in free-range chicken in Gorombozi District in Zimbabwe. Preventive Veterinary Medicine, 54: 213-224.

Permin A and Hansen J W 1998 Epidemiology, Diagnosis and Control of Poultry Parasites. FAO, Rome, Italy.

Permin A, Magwisha H, Kassuku A A, Nansen Bisgarrd M and Gibbons L 1997 A cross-sectional study of helminths in rural scavenging poultry in Tanzania in relation to season and climate. Journal of Helmintholology, 71: 233-240

Phiri I K, Phiri A M, Ziela M Chota A Masuku M and Monrad J 2007 Prevalence and distribution of gastrointestinal helminths and their effects on weight gain in free-range chickens in Central Zambia. Tropical Animal Health and Production 39 (4): 309-315.

Sabuni Z A, Mbuthia P G, Maingi N, Nyaga P N, Njagi L W, Bebora L C and Michieka J N 2013 Skin lesions associated with ectoparasitic infestation in indigenous chickens in Eastern Province of Kenya. Research Journal of Poultry Sciences 6: 53-58.

Slimane B B 2016 Prevalence of the gastro-intestinal parasites of domestic chicken Gallus domesticus Linnaeus, 1758 in Tunisia according to the agro-ecological zones. Journal of Parasitic Diseases. 2016 Sep; 40(3): 774–778. doi: 10.1007/s12639-014-0577-5

Soulsby E J L 1982 Helminths, Arthropods and Protozoa of Domesticated Animals. 7th ed. Baillière Tindall & Cassell Ltd, London, England: pp. 333 -351.

Syakalima M, Simuunza M and Zulu V 2017 Chicken diseases and their ethno-botanical treatments among the rural poor in southern Zambia, Africa. Livestock Research for Rural Development. Volume 29, Article #13. Retrieved June 9, 2020, from http://www.lrrd.org/lrrd29/1/syak29013.htm.

Waruiru R M, Mavuti S K, Mbuthia P G, Njagi L W, Mutune M N and Otieno R O 2017 Prevalence of ecto- and haemo-parasites of free-range local ducks in Kenya. Livestock Research for Rural Development. Volume 29, Article #126. Retrieved June 11, 2020, from http://www.lrrd.org/lrrd29/7/stek29126.htm..

Weaver HJ, Hawdon JM, Hoberg EP 2010 Soil-transmitted helminthiases: implications of climate change and human behavior. Trends Parasitol. 2010;26:574–581.

Wilson KI, Yazwinski TA, Tucker CA, Johnson ZB 1994 A survey into the prevalence of poultry helminths in Northwest Arkansas commercial broiler chickens. Avian Dis. 1994;38:158–160. doi: 10.2307/1591850.

Ziela Moses 2000 A comparison study of gastro intestinal nematode infection in traditional and commercial chickens and effect of anthelmitic treatment on production. Master of Science, Veterinary Medicine Thesis, University of Zambia, School of Veterinary Medicine, Lusaka.