prevalence of gastrointestinal parasites in local and exotic...

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Research Article Prevalence of Gastrointestinal Parasites in Local and Exotic Breeds of Chickens in Pankrono–Kumasi, Ghana Philip Asumang , 1,2 Justice Akoto Delali, 1 Francis Wiafe, 1 Zeba Kamil, 1 Gadafi Iddrisu Balali, 1,2 Vera Afua Dela Gobe, 2 Wilson Nketiah Siaw, 1 and Grace Pinamang 3 1 Department of Science Education, University of Education, Winneba, Ghana 2 Department of eoretical and Applied Biology, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana 3 Department of Science, St Monica’s College of Education, Ghana Correspondence should be addressed to Philip Asumang; [email protected] Received 11 February 2019; Revised 13 June 2019; Accepted 15 July 2019; Published 2 September 2019 Academic Editor: Bernard Marchand Copyright © 2019 Philip Asumang et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. e world’s poultry population is on the ascendency as a result of the high demand for poultry product by consumers. In Africa, poultry meat is estimated to represent almost 25% of all meat, whereas in some areas it covers 100% of the animal protein available. e high demand for poultry products has led to an increase in poultry production in almost all African countries including Ghana, with the domestic chicken being the most kept. e sector has been reported to have recorded a drop in production, partly due to infection of birds by diseases, causing organisms including parasites. e study conducted was to investigate the prevalence of gastrointestinal parasites in local and exotic breeds of chickens in Pankrono–Kumasi in the Ashanti Region of Ghana. Two hundred (200) cloacae of slaughtered birds were collected from slaughtering units in the study area and the faecal samples were examined for the eggs/cysts of gastrointestinal parasites using the simple flotation technique and microscopy. Nematodes and cestodes were recovered in 131 (65.5%) of the samples examined with Ascaridia galli recorded as the most prevalent. Some of the nematodes include Ascaridia galli 65 (32.5%), Heterakis gallinarum 38 (19.0%), and Capillaria spp. 29 (14.5%). Some cestodes were Raillietina spp. 19(9.5%) and Choanotaenia infundibulum 5 (2.5%) with Prosthogonimus spp. 3 (1.5%) being the only trematode recovered. e local breeds recorded a percentage prevalence of 76.0%, making them the most susceptible breed to gastrointestinal parasites. e results obtained attest to the reason behind the reduction in poultry production. It is therefore recommended that farmers are educated on farm managerial practices that will reduce the risk of infection and help increase production to meet the demand of consumers. 1. Introduction e total population of poultry in the world has been estimated by the Food and Agricultural Organization of the UN [1] to be 14.718 million with 1.125M distributed throughout Africa, 1.520M in South America, 6.752M in Asia, 9 M in Oceania, 3.384M in North America, and 1.844M in Europe [2]. e most commonly kept poultry are the domestic chicken (Gallus gallus domesticus) [3, 4]. Based on the number of animals, poultry represent the largest domestic animal stock in the world [5]. is has been demonstrated by the number and fact that during the last three decades, egg production has doubled and poultry meat production has tripled whereas there is no much increment in livestock production due to higher demand for poultry products [6]. In Africa, poultry meat is estimated to represent almost 25% of all meat, whereas in some areas it covers 100% of the animal protein available [7]. Ghana’s overall livestock production has been on the rise since 2000 largely as a result of the exponential growth of the poultry sector in the Southern region [1]. While the total cattle production increased by 8 percent between 2000 and 2007, poultry production increased by more than 80 percent for the same period [7], resulting from the establishment of Hindawi Journal of Parasitology Research Volume 2019, Article ID 5746515, 7 pages https://doi.org/10.1155/2019/5746515

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Page 1: Prevalence of Gastrointestinal Parasites in Local and Exotic …downloads.hindawi.com/journals/jpr/2019/5746515.pdf · 2019-09-02 · In Ghana, the village or backyard poultry production

Research ArticlePrevalence of Gastrointestinal Parasites in Local and ExoticBreeds of Chickens in PankronondashKumasi Ghana

Philip Asumang 12 Justice Akoto Delali1 FrancisWiafe1

Zeba Kamil1 Gadafi Iddrisu Balali12 Vera Afua Dela Gobe2

Wilson Nketiah Siaw1 and Grace Pinamang3

1Department of Science Education University of Education Winneba Ghana2Department of Theoretical and Applied Biology Kwame Nkrumah University of Science and Technology Kumasi Ghana3Department of Science St Monicarsquos College of Education Ghana

Correspondence should be addressed to Philip Asumang asumangphilipyahoocom

Received 11 February 2019 Revised 13 June 2019 Accepted 15 July 2019 Published 2 September 2019

Academic Editor Bernard Marchand

Copyright copy 2019 Philip Asumang et alThis is an open access article distributed under theCreative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

The worldrsquos poultry population is on the ascendency as a result of the high demand for poultry product by consumers In Africapoultry meat is estimated to represent almost 25 of all meat whereas in some areas it covers 100 of the animal protein availableThe high demand for poultry products has led to an increase in poultry production in almost all African countries includingGhanawith the domestic chicken being the most kept The sector has been reported to have recorded a drop in production partly dueto infection of birds by diseases causing organisms including parasites The study conducted was to investigate the prevalence ofgastrointestinal parasites in local and exotic breeds of chickens in PankronondashKumasi in the Ashanti Region of Ghana Two hundred(200) cloacae of slaughtered birds were collected from slaughtering units in the study area and the faecal samples were examinedfor the eggscysts of gastrointestinal parasites using the simple flotation technique and microscopy Nematodes and cestodes wererecovered in 131 (655) of the samples examined with Ascaridia galli recorded as the most prevalent Some of the nematodesinclude Ascaridia galli 65 (325) Heterakis gallinarum 38 (190) and Capillaria spp 29 (145) Some cestodes were Raillietinaspp 19(95) and Choanotaenia infundibulum 5 (25) with Prosthogonimus spp 3 (15) being the only trematode recoveredThelocal breeds recorded a percentage prevalence of 760 making them the most susceptible breed to gastrointestinal parasites Theresults obtained attest to the reason behind the reduction in poultry production It is therefore recommended that farmers areeducated on farm managerial practices that will reduce the risk of infection and help increase production to meet the demand ofconsumers

1 Introduction

The total population of poultry in the world has beenestimated by the Food and Agricultural Organization ofthe UN [1] to be 14718 million with 1125M distributedthroughout Africa 1520M in South America 6752M inAsia 9M in Oceania 3384M in North America and 1844Min Europe [2] The most commonly kept poultry are thedomestic chicken (Gallus gallus domesticus) [3 4] Based onthe number of animals poultry represent the largest domesticanimal stock in the world [5] This has been demonstratedby the number and fact that during the last three decades

egg production has doubled and poultry meat productionhas tripled whereas there is no much increment in livestockproduction due to higher demand for poultry products [6] InAfrica poultry meat is estimated to represent almost 25 ofall meat whereas in some areas it covers 100 of the animalprotein available [7]

Ghanarsquos overall livestock production has been on the risesince 2000 largely as a result of the exponential growth ofthe poultry sector in the Southern region [1] While the totalcattle production increased by 8 percent between 2000 and2007 poultry production increased by more than 80 percentfor the same period [7] resulting from the establishment of

HindawiJournal of Parasitology ResearchVolume 2019 Article ID 5746515 7 pageshttpsdoiorg10115520195746515

2 Journal of Parasitology Research

the integrated poultry project in Accra by the Government ofGhana in the 1960s and the high demand of poultry meat bythe Ghanaian populace [8]

In Ghana the village or backyard poultry productionsystem is the most prevalent one complemented by thecommercial production systemThe countryrsquos village poultrypopulation was estimated at 12 million [9] and in 2005 atover 20 million (FAOSTAT) accounting for 60 ndash 80 of thenational poultry population being kept all over the country inthe rural and periurban areas [10] with theUpper East UpperWest and the Northern regions being the concentratedregions compared to exotic breeds

Research work by [11] avers that commercial poultryproduction has made substantial progress during the lastsixty years in both Western and Central Africa Howeverthe development of vibrant poultry sectors in these countriesis dependent on costly imported day-old chicks from high-performance hybrid stocks balanced feeds drugs and vac-cines For example the 11 hatcheries in Ghana are operatingat only 38 of their total production capacity [12] Thecommercial production system mostly consists of the exoticbreeds which are kept for commercial purposes and aremore abundant in the urban areas of the Greater AccraBrong-Ahafo and Ashanti regions where the market for theirproduct exists and the climatic conditions are favorable [13]

These birds provide man with high nutritional valuesthrough the consumption of their meat andor eggs and othersocioeconomic benefits which cannot be overemphasized[13 14] However the supply of poultry products lags behinddemand With a projected national poultry population of33525369 according to [15] it is estimated that a total of36 184 mt of poultry meat was produced in 2005 Accordingto [16] these data represented between 18 and 24 onlyof the total meat demand of Ghanaians This led to Ghanarsquosnational per capita animal protein consumption being oneof the lowest in Sub-Saharan Africa estimated at some 53 gper day [17] which is lower than the recommended 65 gPoultry meat and eggs together account for only 060 percentof the daily calories consumed [18] It has been estimated thatconsumption of poultry products in Ghana consist of 12kgof meat and 12 eggs per person in a year as compared to theworldrsquos average of 97kg of meat and 154 eggs per person peryear [19] This is partly attributed to the losses encounteredin the poultry industry which have been linked to outbreakof disease causing agents such as viruses bacteria [20] andmostly parasites [21] as it has been estimated that more than750 million chickens guinea fowls and ducklings in Africadie each year as a result of various infections [22]

Poultry production in the Ashanti region accounted for2807 percent of the total poultry production in Ghana in2009 which was second to the Brong-Ahafo region 2962percent [23] This indicates the rise in the consumption ofpoultry product in the region especially the capital city wheremost farmers bring their product for market The region hashowever recorded a decline in production due to infectionsof birds by disease causing agents with parasites being themost prominent ones [24 25] Although some reduction inbirdrsquos parasitic infection has been achieved in commercialproduction system due to improved housing and hygienic

and management practices the prevalence of gastrointestinalparasites is still very rampant [26 27]

The range of feeds fed on by the domestic chicken in thetraditional production system from grains fruits to insectsmay harbor infective stage of parasites thereby predisposingthem to parasitic infections particularly gastrointestinal par-asites [28 29] The famer is equally at risk of cross-infectionas he carries out his managerial practices on the farm [30]

Good knowledge of the parasites of domestic chick-ens species composition and predilection site is essen-tial for prompt disease diagnosis and treatment [31] Thisstudy therefore explored the gastrointestinal parasites of thedomestic chicken (Gallus gallus domesticus) both local andexotic in Kumasi-Pankrono in the Ashanti Region which tothe best of our knowledge is being conducted in the areafor the first time The study seeks to specifically find out (1)the prevalence and types of parasites in the gastrointestinaltract of chickens (2) the breed that is more prevalent togastrointestinal parasites (3) the sex of chickens that is moreprevalent to gastrointestinal parasites

The outcome of the study will serve as a complementto the already existing studies on the subject matter andother related fields Poultry farmers will be enlightenedon the prevalence of gastrointestinal parasites that bothlocal and exotic birds are susceptible to so that measurescan be implemented to improve commercial and free-rangeproduction systems of poultry Finally the public will alsobe informed on the susceptibility of chickens to parasiteinfections and the risk involved in consuming undercookedmeat from poultry

2 Materials and Methods

The study was conducted in Pankrono a suburb of Kumasiin the Ashanti Region It has geographical coordinates of 60451015840 0rdquo North and 10 361015840 0rdquo West It has a population of 60917and is approximately 98km away from the Kumasi CentralBusiness District Most of its inhabitants are civil servantswhiles some are petty traders and a few are being farmers

The study was conducted between January and March2017 For the purposes of the study feacal remains in thelower ends of the large intestine of slaughtered chickens wereconsidered

Two hundred (200) cloacae of slaughtered chickens com-prising of 100 locals (50 males and 50 females) and 100 exotic(50males and 50 females) breeds were collected at random inlabelled sample containers and transported to the Universityof Education Mampong Campus for laboratory examination

In the laboratory the cloacae were cut open and thefaecal samples were scrapped into a universal bottle andanalyzed for eggscyst of intestinal parasites qualitativelyusing supersaturated saline flotation technique [28 32]

The floatation medium was prepared by dissolving 400 gofNaCl in 1000ml of warmdistilledwaterTheprocedurewasconducted by adding 10mls of the floatation medium to thefeacal sample in the universal bottle and stirred with a rodThe mixture was then filtered through double layered gauzeinto a test tube and more media was added until a meniscus

Journal of Parasitology Research 3

was formedA coverslipwas placed gently on the test tube andallowed to stand on a level surface for at least 10 ndash 20minutesThe coverslip was carefully removed and placed on a glassslide and examined immediately for parasite eggs under x10and x 40 objective lens Identification of the eggs was aidedby the addition of Lugolrsquos Iodine solution to the sample onthe glass slide

The data obtained from the laboratory examination ofthe samples were collected using Ms Excel 2015 The Chi-square test (X2) was used for comparison of prevalenceand mean intensity among groups for statistical similaritiesor differences at a significance level of P lt 005 and 95confidence interval

3 Results

Out of the 200 samples examined 131 (655) were infectedwith various species of gastro-intestinal parasites (Figure 3)comprising of 5 species of nematode and 4 species ofcestode and a species of trematodes The nematode parasitesrecorded wereAscaridia galli 65(325)Heterakis gallinarum38 (190) Capillaria spp 29 (145) Tetrameres americana5(25) and Gongylonema ingluvocola 4(20) The ces-todes recovered were Raillietina spp 19(95) Choanotaeniainfundibulum 5(25) Davainea proglottina 4(20) andProsthogonimus spp 3(15) as the only trematode (Table 1)Davainea proglottina was discovered in only female birdsof both breeds whereas all the other parasites were seenin both sexes (Figure 2) Nematodes were the most preva-lent of the three groups present in the samples examinedHowever none of the parasites recovered were known to bezoonotic

Among infected birds (131) A galli H gallinarum andthe Capillaria spp were the most prevalent with a percent-age prevalence of 4963 290 and 2212 respectively(Table 1) The most prevalent among nematodes was Agalli (461) and in cestodes Raillietina spp was the mostprevalent (650)

The overall prevalence of infection in local breeds (760)was significantly higher than the exotic breeds (550)This is not uncommon because of their free range modeof managerial practices which allows them free access tovirtually all types of environment and hence predisposingthem to various forms of infections [33] The three mostprevalent species have yet again showed their dominance inboth breeds with A galli recording a percentage prevalenceof 140 in exotic breeds and 185 in the local breedsH gallinarum 75 and 115 and Capillaria spp with60 and 85 in the exotic and local breeds respectively(Figure 1)

Even though there is no significant difference in theoverall prevalence of the parasites between females (480)and males (380) the parasites showed some degree ofpreference for female birds as higher infection rate wasobserved in females than males in both breeds The preva-lence in the females of the local breed (300) was howeverhigher than observed in the females of the exotic breeds(180)

4 Discussion

The overall prevalence of infection with gastrointestinalparasites recorded in this study was 655 This is in relationto the 636 reported by [26] in Makurdi and slightly above5964 by [34] in Ethiopia The recorded prevalence ishowever lower than the 92 by [35] and 815 reported by[14] in Giwa Kaduna State of Nigeria This could be relatedto the differences in the management system control practicein farms and seasonal differences in the study area [3]

The study revealed nematodes and cestodes as the mostcommon intestinal parasites of chickens This is in accor-dance with the works of [36] in Zaria and [14 36] in whichcestodes and nematodeswere implicated as themajor cause ofhelminth infection in domestic chickens Cestodes generallyundergo an indirect mode of transmission where they makeuse of intermediate host such as ants grasshoppers andbeetles to perpetuate their transmission These organismsserve as food for scavenging birds and hence transmit theinfective stage of the parasites to the bird upon ingestion Thehigh prevalence of nematodes and cestodes recorded in thelocal and exotic breeds gives an indication that neither breedis spared by the raid of gastrointestinal parasites in the studyarea Their prevalence also indicates the availability of theirinfective stages in the study area and the ability of the infectivestages to withstand environmental conditions for a long timebefore they are taken in by the host

Although A galli H gallinarum and Capillaria sppinfested both local and exotic breeds in this study A galli hadthe higher prevalence and this is in consonance with severalstudies which indicate the species as the commonest andmost important helminth infection of poultry [28 37]This isnot surprising as A galli have a direct mode of transmissionand their eggs are very resistant to the environment and cansurvive on the outside for a long timeThe eggs are passed outin the faeces of the host and develop into the infective stage inthe open contaminating feed and water sources New hostsbecome infected when they ingest the infective eggs fromthese sources In the deep litter system the eggs can probablyremain infective for years depending on the temperaturehumidity pH and ammonium concentration and so whereproper managerial practices are not in place feed and watersources of birds can easily be contaminated as farm handlerscan transport the eggs of these parasites from other sourcesto the farm site

The recorded prevalence (760) in the local breeds overthe exotic (550) in the study agrees with previous reportsby [21 37 38] which conforms to the phenomenon thatlocal breeds are more predisposed to infections due to theirroaming and feeding habits where the chickens scavengeduring the daytime with free access to the ground air fruitsleaves roots etc and therefore have greater contact withfaeces and intermediate host organisms such as earthwormsslugs and snails exposing them to a wide range of infectionsUnlike the local breeds the exotic breeds are mostly in aconfinement and so have limited access to these intermediatehosts and are also prone to regular deworming exerciseswhich minimize the risk of infection The duration for thelocal breed to reach table size is much longer compared to

4 Journal of Parasitology Research

00

20

40

60

80

100

120

140

160

180

200

Asca

ridia

gal

li

Het

erak

is ga

llina

rum

Capi

llaria

spp

Raill

ietin

a spp

Choa

nota

enia

infu

ndib

ulum

Tetra

mer

es am

eric

ana

Dav

aine

a pro

glot

tina

Gon

gylo

nem

a ing

luvo

cola

Pro

sthog

onim

us sp

p

Prev

alen

ce (

)

Parasites

Prevalence of Parasites in relation to breed

Prevalence in Exotic Breed ()Prevalence in Local Breed ()

Figure 1 A chat showing prevalence of gastrointestinal helminths of local and exotic breeds of chicken in Pankrono-Kumasi Ghana

Prev

alen

ce (

)

0

2

4

6

8

10

12

14

16

18

Asca

ridia

galli

Het

erak

is ga

llina

rum

Capi

llaria

spp

Raill

ietin

a spp

Ch

oano

taen

ia in

fund

ibul

umTe

tram

eres

amer

icana

Dav

ainea

pro

glot

tina

Gon

gylo

nem

a ing

luvo

cola

Pro

sthog

onim

us sp

p

Parasites

Prevalence of Parasites in relation to sex

FemaleMale

Figure 2 A chat showing the prevalence of gastrointestinal helminth in relation to sex

Journal of Parasitology Research 5

Table 1 Prevalence of gastro-intestinal helminths of local and exotic breeds of chicken in Pankrono- Kumasi Ghana

Parasite No Infected (n=131) Prevalence in population ()Ascaridia galli 65 325Heterakis gallinarum 38 190Capillaria spp 29 145Raillietina spp 19 95Choanotaenia infundibulum 5 25Tetrameres americana 5 25Davainea proglottina 4 20Gongylonema ingluvocola 4 20Prosthogonimus spp 3 15

(a) (b)

(c) (d)

Figure 3 Photographs of some eggs of gastrointestinal helminths of local and exotic breeds of chicken in Pankrono-Kumasi Ghana (a)Capillaria egg (b) H gallinarum (c) Ascarid egg and (d) Choanotaenia infundibulum

the exotic breeds which are fed usually on artificial dietsThis could also be a likely reason for the higher infectionin the local breeds which continue to accumulate parasitesin the system as well as the poor management practicesinherent in free range system [33] It could be said that theexotic breeds were in confinement where good managerialpractices such as regular deworming might have occurredand hence recording a low prevalence This indicates thatin areas where the keeping of local breed is more commonparasite infestation will be a threat to the socioeconomicsurvival of many farmers because there will be a high cost ofproduction with low output [21]

Although the exotic breeds recorded the least prevalencerate in the study area the figure obtained (550) is high fora commercial production systemThis presupposes therefore

that the handling andor management practices at these pro-duction sites are woefully poor The unhygienic conditionsin these sites have created a conducive environment for thesurvival of the larvae of these parasites

The study revealed that female birds recorded manygastrointestinal helminths than the males in both breedseven though there is no significant difference in the figuresobtained This could be by chance or may be related totheir feeding habit as the females are known to be morevoracious in their feeding habits especially during egg pro-duction than the males which remain largely selective [25]Though some zoonotic parasites can be found in chickensthe ones recovered in this study were not zoonotic andtherefore might not pose any risk of infection to han-dlers

6 Journal of Parasitology Research

5 Conclusions

The overall prevalence of gastrointestinal helminths was655 with Ascaridia galli found to be the most prevalentThe helminths discovered were mostly nematodes cestodesand a trematode Local breeds were found to have manygastrointestinal helminths than the exotic breeds as theyrecorded the most prevalence In relation to sex the resultsrevealed that female birds were more prone to the parasitesthan the males as observed in both breeds

6 Recommendations

It is recommended that farmers under the free-range andintensive systems of poultry keeping should be educatedby veterinary extension officers on the various kinds ofgastrointestinal parasites in association with chickens andpoultry as a whole and the dangers they pose

The prevalence level shown by the birds in the studyarea is a clue to the susceptibility of the domestic fowl tomany infectious diseases that may be detrimental to humanconsumption It is therefore recommended that handlersand managers of poultry farms should improve upon theirmanagement skills and issues concerning hygiene Veteri-nary Extension Officers are also requested to pay particularattention to the managerial practices of farmers in the areaand provide the necessary assistance in protecting the healthand wellbeing of poultry as well as contributing to publichealth protection It is also recommended that further studiesshould be carried on the subject matter covering differentmethods and parameters to enhance better results

Data Availability

The data used to support the findings of this study areincluded in the article however the raw data is also availableupon request from the corresponding author

Conflicts of Interest

The authors did not find any conflicts of interest

Authorsrsquo Contributions

The concept of the study was initiated by Philip AsumangHe and Akoto Justice Delali and Wiafe Frimpong Francistogether discussed thoroughly and came up with the designof the study The initial and final draft of the manuscriptwere prepared by Gadafi Iddrisu Balali on the strictest senseafter a discussion with Philip on the definition of intellectualcontent All the authors contributed in the literature searchand manuscript preparation and editing in general howeverPhilip Zeba Kamil and Gadafi did the final literature searchIn the overall preparation of manuscript and editing ingeneral Philip Gadafi Grace Pinamang Vera Afua DelaGobe and Wilson Nketiah Siaw contributed chiefly AlsoPhilip Gadafi Justice Francis and Vera reviewed and edited

the finalmanuscript ORCID ID of the corresponding author0000-0002-2471-9357

References

[1] J Bruinsma World Agriculture Towards 20152030 an FAOStudy Routledge 2017

[2] H K Sebho ldquoExotic chicken status production performanceand constraints in ethiopia a reviewrdquo Asian Journal of PoultryScience vol 10 no 1 pp 30ndash39 2016

[3] O C Jegede P I Bolorunduro and E I Ikani ldquoLevels ofawareness and adoption of disseminated livestock technologiesin Enugu State Nigeriardquo Journal of Food Agriculture andEnvironment (JFAE) vol 5 no 2 pp 185ndash188 2007

[4] J JWMacharia ldquoPhenotypic CharacterizationAndFunctionalPolymorphisms at Prolactin And Vipr1 Genes in EmergingPoultry Species fromWestern Kenyardquo Jkuat-Cohes 2018

[5] M Gilbert G Conchedda T P Van Boeckel et al ldquoIncomedisparities and the global distribution of intensively farmedchicken and pigsrdquo PLoS ONE vol 10 no 7 Article ID e01333812015

[6] C E Bennett R Thomas M Williams et al ldquoThe broilerchicken as a signal of a human reconfigured biosphererdquo RoyalSociety Open Science vol 5 no 12 Article ID 180325 2018

[7] S Barbut Poultry Products Processing An Industry Guide CRCpress 2016

[8] B Y Folitse J Sam L P Dzandu and S K Osei ldquoPoul-try farmersrsquo information needs and sources in selected ruralcommunities in the greater accra region ghanardquo InternationalInformation and Library Review vol 50 no 1 pp 1ndash12 2018

[9] R Osei-Amponsah B Kayang A Naazie M Tiexier-Boichard and X Rognon ldquoPhenotypic characterization of localGhanaian chickens egg-laying performance under improvedmanagement conditionsrdquo Animal Genetic ResourcesResourcesGenetiques AnimalesRecursos Geneticos Animales vol 56 pp29ndash35 2015

[10] M C Brena Y Mekonnen J M Bettridge et al ldquoChangingrisk of environmental Campylobacter exposure with emergingpoultry production systems in Ethiopiardquo Epidemiology andInfection vol 144 no 3 pp 567ndash575 2016

[11] J De Bruyn E Ferguson M Allman-Farinelli et al ldquoFoodcomposition tables in resource-poor settings Exploring currentlimitations and opportunities with a focus on animal-sourcefoods in sub-Saharan Africardquo British Journal of Nutrition vol116 no 10 pp 1709ndash1719 2016

[12] K E Banson G Muthusamy and E Kondo ldquoThe importsubstituted poultry industry evidence from Ghanardquo 2015

[13] H Djang-Fordjour ldquoIdentifying broiler meat production chal-lenges in Ghana focusing on hatchery performancerdquo 2017

[14] H Junaidu S Luka and A Mijinyawa Prevalence of Gas-trointestinal Helminth Parasites of The Domestic Fowl (Gallus-Gallus Domesticus) Slaughtered in Giwa Market Giwa LocalGovernment Area vol 7 Kaduna state Nigeria prevalence 19edition 2014

[15] T Gjedrem N Robinson and M Rye ldquoThe importance ofselective breeding in aquaculture to meet future demands foranimal protein A reviewrdquo Aquaculture vol 350-353 pp 117ndash129 2012

[16] M Tuffour and B A Oppong ldquoProfit efficiency in broilerproduction evidence from greater accra region of ghanardquo

Journal of Parasitology Research 7

International Journal of Food and Agricultural Economics vol2 no 1 p 23 2014

[17] N P Steyn Z Mchiza J Hill et al ldquoNutritional contributionof street foods to the diet of people in developing countriesa systematic reviewrdquo Public Health Nutrition vol 17 no 6 pp1363ndash1374 2014

[18] K Killebrew and R Plotnick Poultry Market in West AfricaGhana Evans School Policy Analysis and Research (EPAR) Briefvol 83 2010

[19] N Yenibehit M Murshed and M Islam ldquoAssessment of tech-nical efficiency of layer production in mampong municipalitystochastic frontier approachrdquo Current Research in AgriculturalSciences vol 6 no 1 pp 20ndash28 2019

[20] A I Youssef and SUga ldquoReview of parasitic zoonoses in EgyptrdquoTropical Medicine and Health 2013

[21] O Agbolade A Arosoye E Akajiugo et al ldquoGastrointestinalparasites of domestic fowls from Ijebu Northrdquo southwesternNigeria Basic Research Journal of Agricultural Sciences vol 3no 7 pp 60ndash64 2014

[22] H Ashenafi and Y Eshetu ldquoStudy on gastrointestinal helminthsof local chickens in central ethiopiardquo Revue de MedecineVeterinaire vol 155 no 10 pp 504ndash507 2004

[23] U FAO ldquoFAOstatrdquo 2014[24] A Organization ldquoThe state of food insecurity in the world 2014

Strengthening the enabling environment for food security andnutritionrdquo Food and Agriculture Organization 2014

[25] E Sonaiya Toward Sustainable Poultry Production in AfricaFAO Expert Consultation on Strategies for Sustainable AnimalAgriculture in Developing Countries Italy Rome 1990

[26] C I Ogbaje E O Agbo and O J Ajanusi ldquoPrevalence ofAscaridia galli Heterakis gallinarum and tapeworm infectionsin birds slaughtered in Makurdi townshiprdquo International Jour-nal of Poultry Science vol 11 no 2 pp 103ndash107 2012

[27] S Satish and M Priti ldquoGastro intestinal helminths parasites oflocal chickens samples from tribal areas of Madhya PradeshrdquoInternational Journal of Life Science vol 1 no 4 pp 284ndash2872013

[28] K Cervantes-Rivera J A Villag A Arroyo-Lara L A Landın-Grandvallet and J A Villagomez-Cortes ldquoA diagnostic surveyof gastroenteric helminths in backyard poultry of a rural villagein Mexican tropicsrdquo 2006

[29] J Yang and Scholten T ldquoDientamoeba fragilis a review withnotes on its epidemiology pathogenicity mode of transmissionand diagnosisrdquo The American Journal of Tropical Medicine andHygiene vol 26 no 1 pp 16ndash22 1977

[30] S Lane and D Lloyd ldquoCurrent trends in research into thewaterborne parasite Giardiardquo Critical Reviews in Microbiologyvol 28 no 2 pp 123ndash147 2002

[31] S Kumar R Garg H Ram P S Maurya and P S Baner-jee ldquoGastrointestinal parasitic infections in chickens of uppergangetic plains of India with special reference to poultrycoccidiosisrdquo Journal of Parasitic Diseases vol 39 no 1 pp 22ndash26 2013

[32] E Soulby helminthes Arthropods and Protozoa of DomesticatedAnimals ( Edu) Bailliere Tindal East Sussex 7th editionhelminthes Arthropods and protozoa of domesticatedAnimals(u) Bailliere Tindal East Sussex

[33] E Matur E Ergul I Akyazi E Eraslan and Z T Cirakli ldquoTheeffects of Saccharomyces cerevisiae extract on the weight ofsome organs liver and pancreatic digestive enzyme activity inbreeder hens fed diets contaminated with aflatoxinsrdquo PoultryScience vol 89 no 10 pp 2213ndash2220 2010

[34] B YehualashetA Study onThe Prevalence of Helminth Parasitesin Free Range (Backyard) Chicken in Selected Small Holder Farmsin And around Haramaya [DVM thesis] College of VeterinaryMedicine Haramaya University Ethiopia 2011

[35] H Mikail and Y Adamu ldquoA survey of the gastrointestinalhelminthes of chickens in SokotoMetropolis NigeriardquoNigerianVeterinary Journal vol 29 no 1 pp 72ndash75 2008

[36] S Luka and I Ndams ldquo(2007) Gastrointestinal parasites ofdomestic chicken Gallus-gallus domesticus Linnaeus 1758 inSamaru Zaria Nigeriardquo ScienceWorld Journal vol 2 no 1 2007

[37] C Ohaeri and C Okwum ldquoHelminthic parasites of domesticfowls in Ikwuano Abia State Nigeriardquo Journal of NaturalSciences Research vol 1 2013

[38] M Mwale and P J Masika ldquoPoint prevalence study of gastro-intestinal parasites in village chickens of Centane district SouthAfricardquoAfrican Journal of Agricultural Research vol 6 no 9 pp2033ndash2038 2011

Hindawiwwwhindawicom

International Journal of

Volume 2018

Zoology

Hindawiwwwhindawicom Volume 2018

Anatomy Research International

PeptidesInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Journal of Parasitology Research

GenomicsInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Hindawiwwwhindawicom Volume 2018

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Neuroscience Journal

Hindawiwwwhindawicom Volume 2018

BioMed Research International

Cell BiologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Biochemistry Research International

ArchaeaHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Genetics Research International

Hindawiwwwhindawicom Volume 2018

Advances in

Virolog y Stem Cells International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Enzyme Research

Hindawiwwwhindawicom Volume 2018

International Journal of

MicrobiologyHindawiwwwhindawicom

Nucleic AcidsJournal of

Volume 2018

Submit your manuscripts atwwwhindawicom

Page 2: Prevalence of Gastrointestinal Parasites in Local and Exotic …downloads.hindawi.com/journals/jpr/2019/5746515.pdf · 2019-09-02 · In Ghana, the village or backyard poultry production

2 Journal of Parasitology Research

the integrated poultry project in Accra by the Government ofGhana in the 1960s and the high demand of poultry meat bythe Ghanaian populace [8]

In Ghana the village or backyard poultry productionsystem is the most prevalent one complemented by thecommercial production systemThe countryrsquos village poultrypopulation was estimated at 12 million [9] and in 2005 atover 20 million (FAOSTAT) accounting for 60 ndash 80 of thenational poultry population being kept all over the country inthe rural and periurban areas [10] with theUpper East UpperWest and the Northern regions being the concentratedregions compared to exotic breeds

Research work by [11] avers that commercial poultryproduction has made substantial progress during the lastsixty years in both Western and Central Africa Howeverthe development of vibrant poultry sectors in these countriesis dependent on costly imported day-old chicks from high-performance hybrid stocks balanced feeds drugs and vac-cines For example the 11 hatcheries in Ghana are operatingat only 38 of their total production capacity [12] Thecommercial production system mostly consists of the exoticbreeds which are kept for commercial purposes and aremore abundant in the urban areas of the Greater AccraBrong-Ahafo and Ashanti regions where the market for theirproduct exists and the climatic conditions are favorable [13]

These birds provide man with high nutritional valuesthrough the consumption of their meat andor eggs and othersocioeconomic benefits which cannot be overemphasized[13 14] However the supply of poultry products lags behinddemand With a projected national poultry population of33525369 according to [15] it is estimated that a total of36 184 mt of poultry meat was produced in 2005 Accordingto [16] these data represented between 18 and 24 onlyof the total meat demand of Ghanaians This led to Ghanarsquosnational per capita animal protein consumption being oneof the lowest in Sub-Saharan Africa estimated at some 53 gper day [17] which is lower than the recommended 65 gPoultry meat and eggs together account for only 060 percentof the daily calories consumed [18] It has been estimated thatconsumption of poultry products in Ghana consist of 12kgof meat and 12 eggs per person in a year as compared to theworldrsquos average of 97kg of meat and 154 eggs per person peryear [19] This is partly attributed to the losses encounteredin the poultry industry which have been linked to outbreakof disease causing agents such as viruses bacteria [20] andmostly parasites [21] as it has been estimated that more than750 million chickens guinea fowls and ducklings in Africadie each year as a result of various infections [22]

Poultry production in the Ashanti region accounted for2807 percent of the total poultry production in Ghana in2009 which was second to the Brong-Ahafo region 2962percent [23] This indicates the rise in the consumption ofpoultry product in the region especially the capital city wheremost farmers bring their product for market The region hashowever recorded a decline in production due to infectionsof birds by disease causing agents with parasites being themost prominent ones [24 25] Although some reduction inbirdrsquos parasitic infection has been achieved in commercialproduction system due to improved housing and hygienic

and management practices the prevalence of gastrointestinalparasites is still very rampant [26 27]

The range of feeds fed on by the domestic chicken in thetraditional production system from grains fruits to insectsmay harbor infective stage of parasites thereby predisposingthem to parasitic infections particularly gastrointestinal par-asites [28 29] The famer is equally at risk of cross-infectionas he carries out his managerial practices on the farm [30]

Good knowledge of the parasites of domestic chick-ens species composition and predilection site is essen-tial for prompt disease diagnosis and treatment [31] Thisstudy therefore explored the gastrointestinal parasites of thedomestic chicken (Gallus gallus domesticus) both local andexotic in Kumasi-Pankrono in the Ashanti Region which tothe best of our knowledge is being conducted in the areafor the first time The study seeks to specifically find out (1)the prevalence and types of parasites in the gastrointestinaltract of chickens (2) the breed that is more prevalent togastrointestinal parasites (3) the sex of chickens that is moreprevalent to gastrointestinal parasites

The outcome of the study will serve as a complementto the already existing studies on the subject matter andother related fields Poultry farmers will be enlightenedon the prevalence of gastrointestinal parasites that bothlocal and exotic birds are susceptible to so that measurescan be implemented to improve commercial and free-rangeproduction systems of poultry Finally the public will alsobe informed on the susceptibility of chickens to parasiteinfections and the risk involved in consuming undercookedmeat from poultry

2 Materials and Methods

The study was conducted in Pankrono a suburb of Kumasiin the Ashanti Region It has geographical coordinates of 60451015840 0rdquo North and 10 361015840 0rdquo West It has a population of 60917and is approximately 98km away from the Kumasi CentralBusiness District Most of its inhabitants are civil servantswhiles some are petty traders and a few are being farmers

The study was conducted between January and March2017 For the purposes of the study feacal remains in thelower ends of the large intestine of slaughtered chickens wereconsidered

Two hundred (200) cloacae of slaughtered chickens com-prising of 100 locals (50 males and 50 females) and 100 exotic(50males and 50 females) breeds were collected at random inlabelled sample containers and transported to the Universityof Education Mampong Campus for laboratory examination

In the laboratory the cloacae were cut open and thefaecal samples were scrapped into a universal bottle andanalyzed for eggscyst of intestinal parasites qualitativelyusing supersaturated saline flotation technique [28 32]

The floatation medium was prepared by dissolving 400 gofNaCl in 1000ml of warmdistilledwaterTheprocedurewasconducted by adding 10mls of the floatation medium to thefeacal sample in the universal bottle and stirred with a rodThe mixture was then filtered through double layered gauzeinto a test tube and more media was added until a meniscus

Journal of Parasitology Research 3

was formedA coverslipwas placed gently on the test tube andallowed to stand on a level surface for at least 10 ndash 20minutesThe coverslip was carefully removed and placed on a glassslide and examined immediately for parasite eggs under x10and x 40 objective lens Identification of the eggs was aidedby the addition of Lugolrsquos Iodine solution to the sample onthe glass slide

The data obtained from the laboratory examination ofthe samples were collected using Ms Excel 2015 The Chi-square test (X2) was used for comparison of prevalenceand mean intensity among groups for statistical similaritiesor differences at a significance level of P lt 005 and 95confidence interval

3 Results

Out of the 200 samples examined 131 (655) were infectedwith various species of gastro-intestinal parasites (Figure 3)comprising of 5 species of nematode and 4 species ofcestode and a species of trematodes The nematode parasitesrecorded wereAscaridia galli 65(325)Heterakis gallinarum38 (190) Capillaria spp 29 (145) Tetrameres americana5(25) and Gongylonema ingluvocola 4(20) The ces-todes recovered were Raillietina spp 19(95) Choanotaeniainfundibulum 5(25) Davainea proglottina 4(20) andProsthogonimus spp 3(15) as the only trematode (Table 1)Davainea proglottina was discovered in only female birdsof both breeds whereas all the other parasites were seenin both sexes (Figure 2) Nematodes were the most preva-lent of the three groups present in the samples examinedHowever none of the parasites recovered were known to bezoonotic

Among infected birds (131) A galli H gallinarum andthe Capillaria spp were the most prevalent with a percent-age prevalence of 4963 290 and 2212 respectively(Table 1) The most prevalent among nematodes was Agalli (461) and in cestodes Raillietina spp was the mostprevalent (650)

The overall prevalence of infection in local breeds (760)was significantly higher than the exotic breeds (550)This is not uncommon because of their free range modeof managerial practices which allows them free access tovirtually all types of environment and hence predisposingthem to various forms of infections [33] The three mostprevalent species have yet again showed their dominance inboth breeds with A galli recording a percentage prevalenceof 140 in exotic breeds and 185 in the local breedsH gallinarum 75 and 115 and Capillaria spp with60 and 85 in the exotic and local breeds respectively(Figure 1)

Even though there is no significant difference in theoverall prevalence of the parasites between females (480)and males (380) the parasites showed some degree ofpreference for female birds as higher infection rate wasobserved in females than males in both breeds The preva-lence in the females of the local breed (300) was howeverhigher than observed in the females of the exotic breeds(180)

4 Discussion

The overall prevalence of infection with gastrointestinalparasites recorded in this study was 655 This is in relationto the 636 reported by [26] in Makurdi and slightly above5964 by [34] in Ethiopia The recorded prevalence ishowever lower than the 92 by [35] and 815 reported by[14] in Giwa Kaduna State of Nigeria This could be relatedto the differences in the management system control practicein farms and seasonal differences in the study area [3]

The study revealed nematodes and cestodes as the mostcommon intestinal parasites of chickens This is in accor-dance with the works of [36] in Zaria and [14 36] in whichcestodes and nematodeswere implicated as themajor cause ofhelminth infection in domestic chickens Cestodes generallyundergo an indirect mode of transmission where they makeuse of intermediate host such as ants grasshoppers andbeetles to perpetuate their transmission These organismsserve as food for scavenging birds and hence transmit theinfective stage of the parasites to the bird upon ingestion Thehigh prevalence of nematodes and cestodes recorded in thelocal and exotic breeds gives an indication that neither breedis spared by the raid of gastrointestinal parasites in the studyarea Their prevalence also indicates the availability of theirinfective stages in the study area and the ability of the infectivestages to withstand environmental conditions for a long timebefore they are taken in by the host

Although A galli H gallinarum and Capillaria sppinfested both local and exotic breeds in this study A galli hadthe higher prevalence and this is in consonance with severalstudies which indicate the species as the commonest andmost important helminth infection of poultry [28 37]This isnot surprising as A galli have a direct mode of transmissionand their eggs are very resistant to the environment and cansurvive on the outside for a long timeThe eggs are passed outin the faeces of the host and develop into the infective stage inthe open contaminating feed and water sources New hostsbecome infected when they ingest the infective eggs fromthese sources In the deep litter system the eggs can probablyremain infective for years depending on the temperaturehumidity pH and ammonium concentration and so whereproper managerial practices are not in place feed and watersources of birds can easily be contaminated as farm handlerscan transport the eggs of these parasites from other sourcesto the farm site

The recorded prevalence (760) in the local breeds overthe exotic (550) in the study agrees with previous reportsby [21 37 38] which conforms to the phenomenon thatlocal breeds are more predisposed to infections due to theirroaming and feeding habits where the chickens scavengeduring the daytime with free access to the ground air fruitsleaves roots etc and therefore have greater contact withfaeces and intermediate host organisms such as earthwormsslugs and snails exposing them to a wide range of infectionsUnlike the local breeds the exotic breeds are mostly in aconfinement and so have limited access to these intermediatehosts and are also prone to regular deworming exerciseswhich minimize the risk of infection The duration for thelocal breed to reach table size is much longer compared to

4 Journal of Parasitology Research

00

20

40

60

80

100

120

140

160

180

200

Asca

ridia

gal

li

Het

erak

is ga

llina

rum

Capi

llaria

spp

Raill

ietin

a spp

Choa

nota

enia

infu

ndib

ulum

Tetra

mer

es am

eric

ana

Dav

aine

a pro

glot

tina

Gon

gylo

nem

a ing

luvo

cola

Pro

sthog

onim

us sp

p

Prev

alen

ce (

)

Parasites

Prevalence of Parasites in relation to breed

Prevalence in Exotic Breed ()Prevalence in Local Breed ()

Figure 1 A chat showing prevalence of gastrointestinal helminths of local and exotic breeds of chicken in Pankrono-Kumasi Ghana

Prev

alen

ce (

)

0

2

4

6

8

10

12

14

16

18

Asca

ridia

galli

Het

erak

is ga

llina

rum

Capi

llaria

spp

Raill

ietin

a spp

Ch

oano

taen

ia in

fund

ibul

umTe

tram

eres

amer

icana

Dav

ainea

pro

glot

tina

Gon

gylo

nem

a ing

luvo

cola

Pro

sthog

onim

us sp

p

Parasites

Prevalence of Parasites in relation to sex

FemaleMale

Figure 2 A chat showing the prevalence of gastrointestinal helminth in relation to sex

Journal of Parasitology Research 5

Table 1 Prevalence of gastro-intestinal helminths of local and exotic breeds of chicken in Pankrono- Kumasi Ghana

Parasite No Infected (n=131) Prevalence in population ()Ascaridia galli 65 325Heterakis gallinarum 38 190Capillaria spp 29 145Raillietina spp 19 95Choanotaenia infundibulum 5 25Tetrameres americana 5 25Davainea proglottina 4 20Gongylonema ingluvocola 4 20Prosthogonimus spp 3 15

(a) (b)

(c) (d)

Figure 3 Photographs of some eggs of gastrointestinal helminths of local and exotic breeds of chicken in Pankrono-Kumasi Ghana (a)Capillaria egg (b) H gallinarum (c) Ascarid egg and (d) Choanotaenia infundibulum

the exotic breeds which are fed usually on artificial dietsThis could also be a likely reason for the higher infectionin the local breeds which continue to accumulate parasitesin the system as well as the poor management practicesinherent in free range system [33] It could be said that theexotic breeds were in confinement where good managerialpractices such as regular deworming might have occurredand hence recording a low prevalence This indicates thatin areas where the keeping of local breed is more commonparasite infestation will be a threat to the socioeconomicsurvival of many farmers because there will be a high cost ofproduction with low output [21]

Although the exotic breeds recorded the least prevalencerate in the study area the figure obtained (550) is high fora commercial production systemThis presupposes therefore

that the handling andor management practices at these pro-duction sites are woefully poor The unhygienic conditionsin these sites have created a conducive environment for thesurvival of the larvae of these parasites

The study revealed that female birds recorded manygastrointestinal helminths than the males in both breedseven though there is no significant difference in the figuresobtained This could be by chance or may be related totheir feeding habit as the females are known to be morevoracious in their feeding habits especially during egg pro-duction than the males which remain largely selective [25]Though some zoonotic parasites can be found in chickensthe ones recovered in this study were not zoonotic andtherefore might not pose any risk of infection to han-dlers

6 Journal of Parasitology Research

5 Conclusions

The overall prevalence of gastrointestinal helminths was655 with Ascaridia galli found to be the most prevalentThe helminths discovered were mostly nematodes cestodesand a trematode Local breeds were found to have manygastrointestinal helminths than the exotic breeds as theyrecorded the most prevalence In relation to sex the resultsrevealed that female birds were more prone to the parasitesthan the males as observed in both breeds

6 Recommendations

It is recommended that farmers under the free-range andintensive systems of poultry keeping should be educatedby veterinary extension officers on the various kinds ofgastrointestinal parasites in association with chickens andpoultry as a whole and the dangers they pose

The prevalence level shown by the birds in the studyarea is a clue to the susceptibility of the domestic fowl tomany infectious diseases that may be detrimental to humanconsumption It is therefore recommended that handlersand managers of poultry farms should improve upon theirmanagement skills and issues concerning hygiene Veteri-nary Extension Officers are also requested to pay particularattention to the managerial practices of farmers in the areaand provide the necessary assistance in protecting the healthand wellbeing of poultry as well as contributing to publichealth protection It is also recommended that further studiesshould be carried on the subject matter covering differentmethods and parameters to enhance better results

Data Availability

The data used to support the findings of this study areincluded in the article however the raw data is also availableupon request from the corresponding author

Conflicts of Interest

The authors did not find any conflicts of interest

Authorsrsquo Contributions

The concept of the study was initiated by Philip AsumangHe and Akoto Justice Delali and Wiafe Frimpong Francistogether discussed thoroughly and came up with the designof the study The initial and final draft of the manuscriptwere prepared by Gadafi Iddrisu Balali on the strictest senseafter a discussion with Philip on the definition of intellectualcontent All the authors contributed in the literature searchand manuscript preparation and editing in general howeverPhilip Zeba Kamil and Gadafi did the final literature searchIn the overall preparation of manuscript and editing ingeneral Philip Gadafi Grace Pinamang Vera Afua DelaGobe and Wilson Nketiah Siaw contributed chiefly AlsoPhilip Gadafi Justice Francis and Vera reviewed and edited

the finalmanuscript ORCID ID of the corresponding author0000-0002-2471-9357

References

[1] J Bruinsma World Agriculture Towards 20152030 an FAOStudy Routledge 2017

[2] H K Sebho ldquoExotic chicken status production performanceand constraints in ethiopia a reviewrdquo Asian Journal of PoultryScience vol 10 no 1 pp 30ndash39 2016

[3] O C Jegede P I Bolorunduro and E I Ikani ldquoLevels ofawareness and adoption of disseminated livestock technologiesin Enugu State Nigeriardquo Journal of Food Agriculture andEnvironment (JFAE) vol 5 no 2 pp 185ndash188 2007

[4] J JWMacharia ldquoPhenotypic CharacterizationAndFunctionalPolymorphisms at Prolactin And Vipr1 Genes in EmergingPoultry Species fromWestern Kenyardquo Jkuat-Cohes 2018

[5] M Gilbert G Conchedda T P Van Boeckel et al ldquoIncomedisparities and the global distribution of intensively farmedchicken and pigsrdquo PLoS ONE vol 10 no 7 Article ID e01333812015

[6] C E Bennett R Thomas M Williams et al ldquoThe broilerchicken as a signal of a human reconfigured biosphererdquo RoyalSociety Open Science vol 5 no 12 Article ID 180325 2018

[7] S Barbut Poultry Products Processing An Industry Guide CRCpress 2016

[8] B Y Folitse J Sam L P Dzandu and S K Osei ldquoPoul-try farmersrsquo information needs and sources in selected ruralcommunities in the greater accra region ghanardquo InternationalInformation and Library Review vol 50 no 1 pp 1ndash12 2018

[9] R Osei-Amponsah B Kayang A Naazie M Tiexier-Boichard and X Rognon ldquoPhenotypic characterization of localGhanaian chickens egg-laying performance under improvedmanagement conditionsrdquo Animal Genetic ResourcesResourcesGenetiques AnimalesRecursos Geneticos Animales vol 56 pp29ndash35 2015

[10] M C Brena Y Mekonnen J M Bettridge et al ldquoChangingrisk of environmental Campylobacter exposure with emergingpoultry production systems in Ethiopiardquo Epidemiology andInfection vol 144 no 3 pp 567ndash575 2016

[11] J De Bruyn E Ferguson M Allman-Farinelli et al ldquoFoodcomposition tables in resource-poor settings Exploring currentlimitations and opportunities with a focus on animal-sourcefoods in sub-Saharan Africardquo British Journal of Nutrition vol116 no 10 pp 1709ndash1719 2016

[12] K E Banson G Muthusamy and E Kondo ldquoThe importsubstituted poultry industry evidence from Ghanardquo 2015

[13] H Djang-Fordjour ldquoIdentifying broiler meat production chal-lenges in Ghana focusing on hatchery performancerdquo 2017

[14] H Junaidu S Luka and A Mijinyawa Prevalence of Gas-trointestinal Helminth Parasites of The Domestic Fowl (Gallus-Gallus Domesticus) Slaughtered in Giwa Market Giwa LocalGovernment Area vol 7 Kaduna state Nigeria prevalence 19edition 2014

[15] T Gjedrem N Robinson and M Rye ldquoThe importance ofselective breeding in aquaculture to meet future demands foranimal protein A reviewrdquo Aquaculture vol 350-353 pp 117ndash129 2012

[16] M Tuffour and B A Oppong ldquoProfit efficiency in broilerproduction evidence from greater accra region of ghanardquo

Journal of Parasitology Research 7

International Journal of Food and Agricultural Economics vol2 no 1 p 23 2014

[17] N P Steyn Z Mchiza J Hill et al ldquoNutritional contributionof street foods to the diet of people in developing countriesa systematic reviewrdquo Public Health Nutrition vol 17 no 6 pp1363ndash1374 2014

[18] K Killebrew and R Plotnick Poultry Market in West AfricaGhana Evans School Policy Analysis and Research (EPAR) Briefvol 83 2010

[19] N Yenibehit M Murshed and M Islam ldquoAssessment of tech-nical efficiency of layer production in mampong municipalitystochastic frontier approachrdquo Current Research in AgriculturalSciences vol 6 no 1 pp 20ndash28 2019

[20] A I Youssef and SUga ldquoReview of parasitic zoonoses in EgyptrdquoTropical Medicine and Health 2013

[21] O Agbolade A Arosoye E Akajiugo et al ldquoGastrointestinalparasites of domestic fowls from Ijebu Northrdquo southwesternNigeria Basic Research Journal of Agricultural Sciences vol 3no 7 pp 60ndash64 2014

[22] H Ashenafi and Y Eshetu ldquoStudy on gastrointestinal helminthsof local chickens in central ethiopiardquo Revue de MedecineVeterinaire vol 155 no 10 pp 504ndash507 2004

[23] U FAO ldquoFAOstatrdquo 2014[24] A Organization ldquoThe state of food insecurity in the world 2014

Strengthening the enabling environment for food security andnutritionrdquo Food and Agriculture Organization 2014

[25] E Sonaiya Toward Sustainable Poultry Production in AfricaFAO Expert Consultation on Strategies for Sustainable AnimalAgriculture in Developing Countries Italy Rome 1990

[26] C I Ogbaje E O Agbo and O J Ajanusi ldquoPrevalence ofAscaridia galli Heterakis gallinarum and tapeworm infectionsin birds slaughtered in Makurdi townshiprdquo International Jour-nal of Poultry Science vol 11 no 2 pp 103ndash107 2012

[27] S Satish and M Priti ldquoGastro intestinal helminths parasites oflocal chickens samples from tribal areas of Madhya PradeshrdquoInternational Journal of Life Science vol 1 no 4 pp 284ndash2872013

[28] K Cervantes-Rivera J A Villag A Arroyo-Lara L A Landın-Grandvallet and J A Villagomez-Cortes ldquoA diagnostic surveyof gastroenteric helminths in backyard poultry of a rural villagein Mexican tropicsrdquo 2006

[29] J Yang and Scholten T ldquoDientamoeba fragilis a review withnotes on its epidemiology pathogenicity mode of transmissionand diagnosisrdquo The American Journal of Tropical Medicine andHygiene vol 26 no 1 pp 16ndash22 1977

[30] S Lane and D Lloyd ldquoCurrent trends in research into thewaterborne parasite Giardiardquo Critical Reviews in Microbiologyvol 28 no 2 pp 123ndash147 2002

[31] S Kumar R Garg H Ram P S Maurya and P S Baner-jee ldquoGastrointestinal parasitic infections in chickens of uppergangetic plains of India with special reference to poultrycoccidiosisrdquo Journal of Parasitic Diseases vol 39 no 1 pp 22ndash26 2013

[32] E Soulby helminthes Arthropods and Protozoa of DomesticatedAnimals ( Edu) Bailliere Tindal East Sussex 7th editionhelminthes Arthropods and protozoa of domesticatedAnimals(u) Bailliere Tindal East Sussex

[33] E Matur E Ergul I Akyazi E Eraslan and Z T Cirakli ldquoTheeffects of Saccharomyces cerevisiae extract on the weight ofsome organs liver and pancreatic digestive enzyme activity inbreeder hens fed diets contaminated with aflatoxinsrdquo PoultryScience vol 89 no 10 pp 2213ndash2220 2010

[34] B YehualashetA Study onThe Prevalence of Helminth Parasitesin Free Range (Backyard) Chicken in Selected Small Holder Farmsin And around Haramaya [DVM thesis] College of VeterinaryMedicine Haramaya University Ethiopia 2011

[35] H Mikail and Y Adamu ldquoA survey of the gastrointestinalhelminthes of chickens in SokotoMetropolis NigeriardquoNigerianVeterinary Journal vol 29 no 1 pp 72ndash75 2008

[36] S Luka and I Ndams ldquo(2007) Gastrointestinal parasites ofdomestic chicken Gallus-gallus domesticus Linnaeus 1758 inSamaru Zaria Nigeriardquo ScienceWorld Journal vol 2 no 1 2007

[37] C Ohaeri and C Okwum ldquoHelminthic parasites of domesticfowls in Ikwuano Abia State Nigeriardquo Journal of NaturalSciences Research vol 1 2013

[38] M Mwale and P J Masika ldquoPoint prevalence study of gastro-intestinal parasites in village chickens of Centane district SouthAfricardquoAfrican Journal of Agricultural Research vol 6 no 9 pp2033ndash2038 2011

Hindawiwwwhindawicom

International Journal of

Volume 2018

Zoology

Hindawiwwwhindawicom Volume 2018

Anatomy Research International

PeptidesInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Journal of Parasitology Research

GenomicsInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Hindawiwwwhindawicom Volume 2018

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Neuroscience Journal

Hindawiwwwhindawicom Volume 2018

BioMed Research International

Cell BiologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Biochemistry Research International

ArchaeaHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Genetics Research International

Hindawiwwwhindawicom Volume 2018

Advances in

Virolog y Stem Cells International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Enzyme Research

Hindawiwwwhindawicom Volume 2018

International Journal of

MicrobiologyHindawiwwwhindawicom

Nucleic AcidsJournal of

Volume 2018

Submit your manuscripts atwwwhindawicom

Page 3: Prevalence of Gastrointestinal Parasites in Local and Exotic …downloads.hindawi.com/journals/jpr/2019/5746515.pdf · 2019-09-02 · In Ghana, the village or backyard poultry production

Journal of Parasitology Research 3

was formedA coverslipwas placed gently on the test tube andallowed to stand on a level surface for at least 10 ndash 20minutesThe coverslip was carefully removed and placed on a glassslide and examined immediately for parasite eggs under x10and x 40 objective lens Identification of the eggs was aidedby the addition of Lugolrsquos Iodine solution to the sample onthe glass slide

The data obtained from the laboratory examination ofthe samples were collected using Ms Excel 2015 The Chi-square test (X2) was used for comparison of prevalenceand mean intensity among groups for statistical similaritiesor differences at a significance level of P lt 005 and 95confidence interval

3 Results

Out of the 200 samples examined 131 (655) were infectedwith various species of gastro-intestinal parasites (Figure 3)comprising of 5 species of nematode and 4 species ofcestode and a species of trematodes The nematode parasitesrecorded wereAscaridia galli 65(325)Heterakis gallinarum38 (190) Capillaria spp 29 (145) Tetrameres americana5(25) and Gongylonema ingluvocola 4(20) The ces-todes recovered were Raillietina spp 19(95) Choanotaeniainfundibulum 5(25) Davainea proglottina 4(20) andProsthogonimus spp 3(15) as the only trematode (Table 1)Davainea proglottina was discovered in only female birdsof both breeds whereas all the other parasites were seenin both sexes (Figure 2) Nematodes were the most preva-lent of the three groups present in the samples examinedHowever none of the parasites recovered were known to bezoonotic

Among infected birds (131) A galli H gallinarum andthe Capillaria spp were the most prevalent with a percent-age prevalence of 4963 290 and 2212 respectively(Table 1) The most prevalent among nematodes was Agalli (461) and in cestodes Raillietina spp was the mostprevalent (650)

The overall prevalence of infection in local breeds (760)was significantly higher than the exotic breeds (550)This is not uncommon because of their free range modeof managerial practices which allows them free access tovirtually all types of environment and hence predisposingthem to various forms of infections [33] The three mostprevalent species have yet again showed their dominance inboth breeds with A galli recording a percentage prevalenceof 140 in exotic breeds and 185 in the local breedsH gallinarum 75 and 115 and Capillaria spp with60 and 85 in the exotic and local breeds respectively(Figure 1)

Even though there is no significant difference in theoverall prevalence of the parasites between females (480)and males (380) the parasites showed some degree ofpreference for female birds as higher infection rate wasobserved in females than males in both breeds The preva-lence in the females of the local breed (300) was howeverhigher than observed in the females of the exotic breeds(180)

4 Discussion

The overall prevalence of infection with gastrointestinalparasites recorded in this study was 655 This is in relationto the 636 reported by [26] in Makurdi and slightly above5964 by [34] in Ethiopia The recorded prevalence ishowever lower than the 92 by [35] and 815 reported by[14] in Giwa Kaduna State of Nigeria This could be relatedto the differences in the management system control practicein farms and seasonal differences in the study area [3]

The study revealed nematodes and cestodes as the mostcommon intestinal parasites of chickens This is in accor-dance with the works of [36] in Zaria and [14 36] in whichcestodes and nematodeswere implicated as themajor cause ofhelminth infection in domestic chickens Cestodes generallyundergo an indirect mode of transmission where they makeuse of intermediate host such as ants grasshoppers andbeetles to perpetuate their transmission These organismsserve as food for scavenging birds and hence transmit theinfective stage of the parasites to the bird upon ingestion Thehigh prevalence of nematodes and cestodes recorded in thelocal and exotic breeds gives an indication that neither breedis spared by the raid of gastrointestinal parasites in the studyarea Their prevalence also indicates the availability of theirinfective stages in the study area and the ability of the infectivestages to withstand environmental conditions for a long timebefore they are taken in by the host

Although A galli H gallinarum and Capillaria sppinfested both local and exotic breeds in this study A galli hadthe higher prevalence and this is in consonance with severalstudies which indicate the species as the commonest andmost important helminth infection of poultry [28 37]This isnot surprising as A galli have a direct mode of transmissionand their eggs are very resistant to the environment and cansurvive on the outside for a long timeThe eggs are passed outin the faeces of the host and develop into the infective stage inthe open contaminating feed and water sources New hostsbecome infected when they ingest the infective eggs fromthese sources In the deep litter system the eggs can probablyremain infective for years depending on the temperaturehumidity pH and ammonium concentration and so whereproper managerial practices are not in place feed and watersources of birds can easily be contaminated as farm handlerscan transport the eggs of these parasites from other sourcesto the farm site

The recorded prevalence (760) in the local breeds overthe exotic (550) in the study agrees with previous reportsby [21 37 38] which conforms to the phenomenon thatlocal breeds are more predisposed to infections due to theirroaming and feeding habits where the chickens scavengeduring the daytime with free access to the ground air fruitsleaves roots etc and therefore have greater contact withfaeces and intermediate host organisms such as earthwormsslugs and snails exposing them to a wide range of infectionsUnlike the local breeds the exotic breeds are mostly in aconfinement and so have limited access to these intermediatehosts and are also prone to regular deworming exerciseswhich minimize the risk of infection The duration for thelocal breed to reach table size is much longer compared to

4 Journal of Parasitology Research

00

20

40

60

80

100

120

140

160

180

200

Asca

ridia

gal

li

Het

erak

is ga

llina

rum

Capi

llaria

spp

Raill

ietin

a spp

Choa

nota

enia

infu

ndib

ulum

Tetra

mer

es am

eric

ana

Dav

aine

a pro

glot

tina

Gon

gylo

nem

a ing

luvo

cola

Pro

sthog

onim

us sp

p

Prev

alen

ce (

)

Parasites

Prevalence of Parasites in relation to breed

Prevalence in Exotic Breed ()Prevalence in Local Breed ()

Figure 1 A chat showing prevalence of gastrointestinal helminths of local and exotic breeds of chicken in Pankrono-Kumasi Ghana

Prev

alen

ce (

)

0

2

4

6

8

10

12

14

16

18

Asca

ridia

galli

Het

erak

is ga

llina

rum

Capi

llaria

spp

Raill

ietin

a spp

Ch

oano

taen

ia in

fund

ibul

umTe

tram

eres

amer

icana

Dav

ainea

pro

glot

tina

Gon

gylo

nem

a ing

luvo

cola

Pro

sthog

onim

us sp

p

Parasites

Prevalence of Parasites in relation to sex

FemaleMale

Figure 2 A chat showing the prevalence of gastrointestinal helminth in relation to sex

Journal of Parasitology Research 5

Table 1 Prevalence of gastro-intestinal helminths of local and exotic breeds of chicken in Pankrono- Kumasi Ghana

Parasite No Infected (n=131) Prevalence in population ()Ascaridia galli 65 325Heterakis gallinarum 38 190Capillaria spp 29 145Raillietina spp 19 95Choanotaenia infundibulum 5 25Tetrameres americana 5 25Davainea proglottina 4 20Gongylonema ingluvocola 4 20Prosthogonimus spp 3 15

(a) (b)

(c) (d)

Figure 3 Photographs of some eggs of gastrointestinal helminths of local and exotic breeds of chicken in Pankrono-Kumasi Ghana (a)Capillaria egg (b) H gallinarum (c) Ascarid egg and (d) Choanotaenia infundibulum

the exotic breeds which are fed usually on artificial dietsThis could also be a likely reason for the higher infectionin the local breeds which continue to accumulate parasitesin the system as well as the poor management practicesinherent in free range system [33] It could be said that theexotic breeds were in confinement where good managerialpractices such as regular deworming might have occurredand hence recording a low prevalence This indicates thatin areas where the keeping of local breed is more commonparasite infestation will be a threat to the socioeconomicsurvival of many farmers because there will be a high cost ofproduction with low output [21]

Although the exotic breeds recorded the least prevalencerate in the study area the figure obtained (550) is high fora commercial production systemThis presupposes therefore

that the handling andor management practices at these pro-duction sites are woefully poor The unhygienic conditionsin these sites have created a conducive environment for thesurvival of the larvae of these parasites

The study revealed that female birds recorded manygastrointestinal helminths than the males in both breedseven though there is no significant difference in the figuresobtained This could be by chance or may be related totheir feeding habit as the females are known to be morevoracious in their feeding habits especially during egg pro-duction than the males which remain largely selective [25]Though some zoonotic parasites can be found in chickensthe ones recovered in this study were not zoonotic andtherefore might not pose any risk of infection to han-dlers

6 Journal of Parasitology Research

5 Conclusions

The overall prevalence of gastrointestinal helminths was655 with Ascaridia galli found to be the most prevalentThe helminths discovered were mostly nematodes cestodesand a trematode Local breeds were found to have manygastrointestinal helminths than the exotic breeds as theyrecorded the most prevalence In relation to sex the resultsrevealed that female birds were more prone to the parasitesthan the males as observed in both breeds

6 Recommendations

It is recommended that farmers under the free-range andintensive systems of poultry keeping should be educatedby veterinary extension officers on the various kinds ofgastrointestinal parasites in association with chickens andpoultry as a whole and the dangers they pose

The prevalence level shown by the birds in the studyarea is a clue to the susceptibility of the domestic fowl tomany infectious diseases that may be detrimental to humanconsumption It is therefore recommended that handlersand managers of poultry farms should improve upon theirmanagement skills and issues concerning hygiene Veteri-nary Extension Officers are also requested to pay particularattention to the managerial practices of farmers in the areaand provide the necessary assistance in protecting the healthand wellbeing of poultry as well as contributing to publichealth protection It is also recommended that further studiesshould be carried on the subject matter covering differentmethods and parameters to enhance better results

Data Availability

The data used to support the findings of this study areincluded in the article however the raw data is also availableupon request from the corresponding author

Conflicts of Interest

The authors did not find any conflicts of interest

Authorsrsquo Contributions

The concept of the study was initiated by Philip AsumangHe and Akoto Justice Delali and Wiafe Frimpong Francistogether discussed thoroughly and came up with the designof the study The initial and final draft of the manuscriptwere prepared by Gadafi Iddrisu Balali on the strictest senseafter a discussion with Philip on the definition of intellectualcontent All the authors contributed in the literature searchand manuscript preparation and editing in general howeverPhilip Zeba Kamil and Gadafi did the final literature searchIn the overall preparation of manuscript and editing ingeneral Philip Gadafi Grace Pinamang Vera Afua DelaGobe and Wilson Nketiah Siaw contributed chiefly AlsoPhilip Gadafi Justice Francis and Vera reviewed and edited

the finalmanuscript ORCID ID of the corresponding author0000-0002-2471-9357

References

[1] J Bruinsma World Agriculture Towards 20152030 an FAOStudy Routledge 2017

[2] H K Sebho ldquoExotic chicken status production performanceand constraints in ethiopia a reviewrdquo Asian Journal of PoultryScience vol 10 no 1 pp 30ndash39 2016

[3] O C Jegede P I Bolorunduro and E I Ikani ldquoLevels ofawareness and adoption of disseminated livestock technologiesin Enugu State Nigeriardquo Journal of Food Agriculture andEnvironment (JFAE) vol 5 no 2 pp 185ndash188 2007

[4] J JWMacharia ldquoPhenotypic CharacterizationAndFunctionalPolymorphisms at Prolactin And Vipr1 Genes in EmergingPoultry Species fromWestern Kenyardquo Jkuat-Cohes 2018

[5] M Gilbert G Conchedda T P Van Boeckel et al ldquoIncomedisparities and the global distribution of intensively farmedchicken and pigsrdquo PLoS ONE vol 10 no 7 Article ID e01333812015

[6] C E Bennett R Thomas M Williams et al ldquoThe broilerchicken as a signal of a human reconfigured biosphererdquo RoyalSociety Open Science vol 5 no 12 Article ID 180325 2018

[7] S Barbut Poultry Products Processing An Industry Guide CRCpress 2016

[8] B Y Folitse J Sam L P Dzandu and S K Osei ldquoPoul-try farmersrsquo information needs and sources in selected ruralcommunities in the greater accra region ghanardquo InternationalInformation and Library Review vol 50 no 1 pp 1ndash12 2018

[9] R Osei-Amponsah B Kayang A Naazie M Tiexier-Boichard and X Rognon ldquoPhenotypic characterization of localGhanaian chickens egg-laying performance under improvedmanagement conditionsrdquo Animal Genetic ResourcesResourcesGenetiques AnimalesRecursos Geneticos Animales vol 56 pp29ndash35 2015

[10] M C Brena Y Mekonnen J M Bettridge et al ldquoChangingrisk of environmental Campylobacter exposure with emergingpoultry production systems in Ethiopiardquo Epidemiology andInfection vol 144 no 3 pp 567ndash575 2016

[11] J De Bruyn E Ferguson M Allman-Farinelli et al ldquoFoodcomposition tables in resource-poor settings Exploring currentlimitations and opportunities with a focus on animal-sourcefoods in sub-Saharan Africardquo British Journal of Nutrition vol116 no 10 pp 1709ndash1719 2016

[12] K E Banson G Muthusamy and E Kondo ldquoThe importsubstituted poultry industry evidence from Ghanardquo 2015

[13] H Djang-Fordjour ldquoIdentifying broiler meat production chal-lenges in Ghana focusing on hatchery performancerdquo 2017

[14] H Junaidu S Luka and A Mijinyawa Prevalence of Gas-trointestinal Helminth Parasites of The Domestic Fowl (Gallus-Gallus Domesticus) Slaughtered in Giwa Market Giwa LocalGovernment Area vol 7 Kaduna state Nigeria prevalence 19edition 2014

[15] T Gjedrem N Robinson and M Rye ldquoThe importance ofselective breeding in aquaculture to meet future demands foranimal protein A reviewrdquo Aquaculture vol 350-353 pp 117ndash129 2012

[16] M Tuffour and B A Oppong ldquoProfit efficiency in broilerproduction evidence from greater accra region of ghanardquo

Journal of Parasitology Research 7

International Journal of Food and Agricultural Economics vol2 no 1 p 23 2014

[17] N P Steyn Z Mchiza J Hill et al ldquoNutritional contributionof street foods to the diet of people in developing countriesa systematic reviewrdquo Public Health Nutrition vol 17 no 6 pp1363ndash1374 2014

[18] K Killebrew and R Plotnick Poultry Market in West AfricaGhana Evans School Policy Analysis and Research (EPAR) Briefvol 83 2010

[19] N Yenibehit M Murshed and M Islam ldquoAssessment of tech-nical efficiency of layer production in mampong municipalitystochastic frontier approachrdquo Current Research in AgriculturalSciences vol 6 no 1 pp 20ndash28 2019

[20] A I Youssef and SUga ldquoReview of parasitic zoonoses in EgyptrdquoTropical Medicine and Health 2013

[21] O Agbolade A Arosoye E Akajiugo et al ldquoGastrointestinalparasites of domestic fowls from Ijebu Northrdquo southwesternNigeria Basic Research Journal of Agricultural Sciences vol 3no 7 pp 60ndash64 2014

[22] H Ashenafi and Y Eshetu ldquoStudy on gastrointestinal helminthsof local chickens in central ethiopiardquo Revue de MedecineVeterinaire vol 155 no 10 pp 504ndash507 2004

[23] U FAO ldquoFAOstatrdquo 2014[24] A Organization ldquoThe state of food insecurity in the world 2014

Strengthening the enabling environment for food security andnutritionrdquo Food and Agriculture Organization 2014

[25] E Sonaiya Toward Sustainable Poultry Production in AfricaFAO Expert Consultation on Strategies for Sustainable AnimalAgriculture in Developing Countries Italy Rome 1990

[26] C I Ogbaje E O Agbo and O J Ajanusi ldquoPrevalence ofAscaridia galli Heterakis gallinarum and tapeworm infectionsin birds slaughtered in Makurdi townshiprdquo International Jour-nal of Poultry Science vol 11 no 2 pp 103ndash107 2012

[27] S Satish and M Priti ldquoGastro intestinal helminths parasites oflocal chickens samples from tribal areas of Madhya PradeshrdquoInternational Journal of Life Science vol 1 no 4 pp 284ndash2872013

[28] K Cervantes-Rivera J A Villag A Arroyo-Lara L A Landın-Grandvallet and J A Villagomez-Cortes ldquoA diagnostic surveyof gastroenteric helminths in backyard poultry of a rural villagein Mexican tropicsrdquo 2006

[29] J Yang and Scholten T ldquoDientamoeba fragilis a review withnotes on its epidemiology pathogenicity mode of transmissionand diagnosisrdquo The American Journal of Tropical Medicine andHygiene vol 26 no 1 pp 16ndash22 1977

[30] S Lane and D Lloyd ldquoCurrent trends in research into thewaterborne parasite Giardiardquo Critical Reviews in Microbiologyvol 28 no 2 pp 123ndash147 2002

[31] S Kumar R Garg H Ram P S Maurya and P S Baner-jee ldquoGastrointestinal parasitic infections in chickens of uppergangetic plains of India with special reference to poultrycoccidiosisrdquo Journal of Parasitic Diseases vol 39 no 1 pp 22ndash26 2013

[32] E Soulby helminthes Arthropods and Protozoa of DomesticatedAnimals ( Edu) Bailliere Tindal East Sussex 7th editionhelminthes Arthropods and protozoa of domesticatedAnimals(u) Bailliere Tindal East Sussex

[33] E Matur E Ergul I Akyazi E Eraslan and Z T Cirakli ldquoTheeffects of Saccharomyces cerevisiae extract on the weight ofsome organs liver and pancreatic digestive enzyme activity inbreeder hens fed diets contaminated with aflatoxinsrdquo PoultryScience vol 89 no 10 pp 2213ndash2220 2010

[34] B YehualashetA Study onThe Prevalence of Helminth Parasitesin Free Range (Backyard) Chicken in Selected Small Holder Farmsin And around Haramaya [DVM thesis] College of VeterinaryMedicine Haramaya University Ethiopia 2011

[35] H Mikail and Y Adamu ldquoA survey of the gastrointestinalhelminthes of chickens in SokotoMetropolis NigeriardquoNigerianVeterinary Journal vol 29 no 1 pp 72ndash75 2008

[36] S Luka and I Ndams ldquo(2007) Gastrointestinal parasites ofdomestic chicken Gallus-gallus domesticus Linnaeus 1758 inSamaru Zaria Nigeriardquo ScienceWorld Journal vol 2 no 1 2007

[37] C Ohaeri and C Okwum ldquoHelminthic parasites of domesticfowls in Ikwuano Abia State Nigeriardquo Journal of NaturalSciences Research vol 1 2013

[38] M Mwale and P J Masika ldquoPoint prevalence study of gastro-intestinal parasites in village chickens of Centane district SouthAfricardquoAfrican Journal of Agricultural Research vol 6 no 9 pp2033ndash2038 2011

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Submit your manuscripts atwwwhindawicom

Page 4: Prevalence of Gastrointestinal Parasites in Local and Exotic …downloads.hindawi.com/journals/jpr/2019/5746515.pdf · 2019-09-02 · In Ghana, the village or backyard poultry production

4 Journal of Parasitology Research

00

20

40

60

80

100

120

140

160

180

200

Asca

ridia

gal

li

Het

erak

is ga

llina

rum

Capi

llaria

spp

Raill

ietin

a spp

Choa

nota

enia

infu

ndib

ulum

Tetra

mer

es am

eric

ana

Dav

aine

a pro

glot

tina

Gon

gylo

nem

a ing

luvo

cola

Pro

sthog

onim

us sp

p

Prev

alen

ce (

)

Parasites

Prevalence of Parasites in relation to breed

Prevalence in Exotic Breed ()Prevalence in Local Breed ()

Figure 1 A chat showing prevalence of gastrointestinal helminths of local and exotic breeds of chicken in Pankrono-Kumasi Ghana

Prev

alen

ce (

)

0

2

4

6

8

10

12

14

16

18

Asca

ridia

galli

Het

erak

is ga

llina

rum

Capi

llaria

spp

Raill

ietin

a spp

Ch

oano

taen

ia in

fund

ibul

umTe

tram

eres

amer

icana

Dav

ainea

pro

glot

tina

Gon

gylo

nem

a ing

luvo

cola

Pro

sthog

onim

us sp

p

Parasites

Prevalence of Parasites in relation to sex

FemaleMale

Figure 2 A chat showing the prevalence of gastrointestinal helminth in relation to sex

Journal of Parasitology Research 5

Table 1 Prevalence of gastro-intestinal helminths of local and exotic breeds of chicken in Pankrono- Kumasi Ghana

Parasite No Infected (n=131) Prevalence in population ()Ascaridia galli 65 325Heterakis gallinarum 38 190Capillaria spp 29 145Raillietina spp 19 95Choanotaenia infundibulum 5 25Tetrameres americana 5 25Davainea proglottina 4 20Gongylonema ingluvocola 4 20Prosthogonimus spp 3 15

(a) (b)

(c) (d)

Figure 3 Photographs of some eggs of gastrointestinal helminths of local and exotic breeds of chicken in Pankrono-Kumasi Ghana (a)Capillaria egg (b) H gallinarum (c) Ascarid egg and (d) Choanotaenia infundibulum

the exotic breeds which are fed usually on artificial dietsThis could also be a likely reason for the higher infectionin the local breeds which continue to accumulate parasitesin the system as well as the poor management practicesinherent in free range system [33] It could be said that theexotic breeds were in confinement where good managerialpractices such as regular deworming might have occurredand hence recording a low prevalence This indicates thatin areas where the keeping of local breed is more commonparasite infestation will be a threat to the socioeconomicsurvival of many farmers because there will be a high cost ofproduction with low output [21]

Although the exotic breeds recorded the least prevalencerate in the study area the figure obtained (550) is high fora commercial production systemThis presupposes therefore

that the handling andor management practices at these pro-duction sites are woefully poor The unhygienic conditionsin these sites have created a conducive environment for thesurvival of the larvae of these parasites

The study revealed that female birds recorded manygastrointestinal helminths than the males in both breedseven though there is no significant difference in the figuresobtained This could be by chance or may be related totheir feeding habit as the females are known to be morevoracious in their feeding habits especially during egg pro-duction than the males which remain largely selective [25]Though some zoonotic parasites can be found in chickensthe ones recovered in this study were not zoonotic andtherefore might not pose any risk of infection to han-dlers

6 Journal of Parasitology Research

5 Conclusions

The overall prevalence of gastrointestinal helminths was655 with Ascaridia galli found to be the most prevalentThe helminths discovered were mostly nematodes cestodesand a trematode Local breeds were found to have manygastrointestinal helminths than the exotic breeds as theyrecorded the most prevalence In relation to sex the resultsrevealed that female birds were more prone to the parasitesthan the males as observed in both breeds

6 Recommendations

It is recommended that farmers under the free-range andintensive systems of poultry keeping should be educatedby veterinary extension officers on the various kinds ofgastrointestinal parasites in association with chickens andpoultry as a whole and the dangers they pose

The prevalence level shown by the birds in the studyarea is a clue to the susceptibility of the domestic fowl tomany infectious diseases that may be detrimental to humanconsumption It is therefore recommended that handlersand managers of poultry farms should improve upon theirmanagement skills and issues concerning hygiene Veteri-nary Extension Officers are also requested to pay particularattention to the managerial practices of farmers in the areaand provide the necessary assistance in protecting the healthand wellbeing of poultry as well as contributing to publichealth protection It is also recommended that further studiesshould be carried on the subject matter covering differentmethods and parameters to enhance better results

Data Availability

The data used to support the findings of this study areincluded in the article however the raw data is also availableupon request from the corresponding author

Conflicts of Interest

The authors did not find any conflicts of interest

Authorsrsquo Contributions

The concept of the study was initiated by Philip AsumangHe and Akoto Justice Delali and Wiafe Frimpong Francistogether discussed thoroughly and came up with the designof the study The initial and final draft of the manuscriptwere prepared by Gadafi Iddrisu Balali on the strictest senseafter a discussion with Philip on the definition of intellectualcontent All the authors contributed in the literature searchand manuscript preparation and editing in general howeverPhilip Zeba Kamil and Gadafi did the final literature searchIn the overall preparation of manuscript and editing ingeneral Philip Gadafi Grace Pinamang Vera Afua DelaGobe and Wilson Nketiah Siaw contributed chiefly AlsoPhilip Gadafi Justice Francis and Vera reviewed and edited

the finalmanuscript ORCID ID of the corresponding author0000-0002-2471-9357

References

[1] J Bruinsma World Agriculture Towards 20152030 an FAOStudy Routledge 2017

[2] H K Sebho ldquoExotic chicken status production performanceand constraints in ethiopia a reviewrdquo Asian Journal of PoultryScience vol 10 no 1 pp 30ndash39 2016

[3] O C Jegede P I Bolorunduro and E I Ikani ldquoLevels ofawareness and adoption of disseminated livestock technologiesin Enugu State Nigeriardquo Journal of Food Agriculture andEnvironment (JFAE) vol 5 no 2 pp 185ndash188 2007

[4] J JWMacharia ldquoPhenotypic CharacterizationAndFunctionalPolymorphisms at Prolactin And Vipr1 Genes in EmergingPoultry Species fromWestern Kenyardquo Jkuat-Cohes 2018

[5] M Gilbert G Conchedda T P Van Boeckel et al ldquoIncomedisparities and the global distribution of intensively farmedchicken and pigsrdquo PLoS ONE vol 10 no 7 Article ID e01333812015

[6] C E Bennett R Thomas M Williams et al ldquoThe broilerchicken as a signal of a human reconfigured biosphererdquo RoyalSociety Open Science vol 5 no 12 Article ID 180325 2018

[7] S Barbut Poultry Products Processing An Industry Guide CRCpress 2016

[8] B Y Folitse J Sam L P Dzandu and S K Osei ldquoPoul-try farmersrsquo information needs and sources in selected ruralcommunities in the greater accra region ghanardquo InternationalInformation and Library Review vol 50 no 1 pp 1ndash12 2018

[9] R Osei-Amponsah B Kayang A Naazie M Tiexier-Boichard and X Rognon ldquoPhenotypic characterization of localGhanaian chickens egg-laying performance under improvedmanagement conditionsrdquo Animal Genetic ResourcesResourcesGenetiques AnimalesRecursos Geneticos Animales vol 56 pp29ndash35 2015

[10] M C Brena Y Mekonnen J M Bettridge et al ldquoChangingrisk of environmental Campylobacter exposure with emergingpoultry production systems in Ethiopiardquo Epidemiology andInfection vol 144 no 3 pp 567ndash575 2016

[11] J De Bruyn E Ferguson M Allman-Farinelli et al ldquoFoodcomposition tables in resource-poor settings Exploring currentlimitations and opportunities with a focus on animal-sourcefoods in sub-Saharan Africardquo British Journal of Nutrition vol116 no 10 pp 1709ndash1719 2016

[12] K E Banson G Muthusamy and E Kondo ldquoThe importsubstituted poultry industry evidence from Ghanardquo 2015

[13] H Djang-Fordjour ldquoIdentifying broiler meat production chal-lenges in Ghana focusing on hatchery performancerdquo 2017

[14] H Junaidu S Luka and A Mijinyawa Prevalence of Gas-trointestinal Helminth Parasites of The Domestic Fowl (Gallus-Gallus Domesticus) Slaughtered in Giwa Market Giwa LocalGovernment Area vol 7 Kaduna state Nigeria prevalence 19edition 2014

[15] T Gjedrem N Robinson and M Rye ldquoThe importance ofselective breeding in aquaculture to meet future demands foranimal protein A reviewrdquo Aquaculture vol 350-353 pp 117ndash129 2012

[16] M Tuffour and B A Oppong ldquoProfit efficiency in broilerproduction evidence from greater accra region of ghanardquo

Journal of Parasitology Research 7

International Journal of Food and Agricultural Economics vol2 no 1 p 23 2014

[17] N P Steyn Z Mchiza J Hill et al ldquoNutritional contributionof street foods to the diet of people in developing countriesa systematic reviewrdquo Public Health Nutrition vol 17 no 6 pp1363ndash1374 2014

[18] K Killebrew and R Plotnick Poultry Market in West AfricaGhana Evans School Policy Analysis and Research (EPAR) Briefvol 83 2010

[19] N Yenibehit M Murshed and M Islam ldquoAssessment of tech-nical efficiency of layer production in mampong municipalitystochastic frontier approachrdquo Current Research in AgriculturalSciences vol 6 no 1 pp 20ndash28 2019

[20] A I Youssef and SUga ldquoReview of parasitic zoonoses in EgyptrdquoTropical Medicine and Health 2013

[21] O Agbolade A Arosoye E Akajiugo et al ldquoGastrointestinalparasites of domestic fowls from Ijebu Northrdquo southwesternNigeria Basic Research Journal of Agricultural Sciences vol 3no 7 pp 60ndash64 2014

[22] H Ashenafi and Y Eshetu ldquoStudy on gastrointestinal helminthsof local chickens in central ethiopiardquo Revue de MedecineVeterinaire vol 155 no 10 pp 504ndash507 2004

[23] U FAO ldquoFAOstatrdquo 2014[24] A Organization ldquoThe state of food insecurity in the world 2014

Strengthening the enabling environment for food security andnutritionrdquo Food and Agriculture Organization 2014

[25] E Sonaiya Toward Sustainable Poultry Production in AfricaFAO Expert Consultation on Strategies for Sustainable AnimalAgriculture in Developing Countries Italy Rome 1990

[26] C I Ogbaje E O Agbo and O J Ajanusi ldquoPrevalence ofAscaridia galli Heterakis gallinarum and tapeworm infectionsin birds slaughtered in Makurdi townshiprdquo International Jour-nal of Poultry Science vol 11 no 2 pp 103ndash107 2012

[27] S Satish and M Priti ldquoGastro intestinal helminths parasites oflocal chickens samples from tribal areas of Madhya PradeshrdquoInternational Journal of Life Science vol 1 no 4 pp 284ndash2872013

[28] K Cervantes-Rivera J A Villag A Arroyo-Lara L A Landın-Grandvallet and J A Villagomez-Cortes ldquoA diagnostic surveyof gastroenteric helminths in backyard poultry of a rural villagein Mexican tropicsrdquo 2006

[29] J Yang and Scholten T ldquoDientamoeba fragilis a review withnotes on its epidemiology pathogenicity mode of transmissionand diagnosisrdquo The American Journal of Tropical Medicine andHygiene vol 26 no 1 pp 16ndash22 1977

[30] S Lane and D Lloyd ldquoCurrent trends in research into thewaterborne parasite Giardiardquo Critical Reviews in Microbiologyvol 28 no 2 pp 123ndash147 2002

[31] S Kumar R Garg H Ram P S Maurya and P S Baner-jee ldquoGastrointestinal parasitic infections in chickens of uppergangetic plains of India with special reference to poultrycoccidiosisrdquo Journal of Parasitic Diseases vol 39 no 1 pp 22ndash26 2013

[32] E Soulby helminthes Arthropods and Protozoa of DomesticatedAnimals ( Edu) Bailliere Tindal East Sussex 7th editionhelminthes Arthropods and protozoa of domesticatedAnimals(u) Bailliere Tindal East Sussex

[33] E Matur E Ergul I Akyazi E Eraslan and Z T Cirakli ldquoTheeffects of Saccharomyces cerevisiae extract on the weight ofsome organs liver and pancreatic digestive enzyme activity inbreeder hens fed diets contaminated with aflatoxinsrdquo PoultryScience vol 89 no 10 pp 2213ndash2220 2010

[34] B YehualashetA Study onThe Prevalence of Helminth Parasitesin Free Range (Backyard) Chicken in Selected Small Holder Farmsin And around Haramaya [DVM thesis] College of VeterinaryMedicine Haramaya University Ethiopia 2011

[35] H Mikail and Y Adamu ldquoA survey of the gastrointestinalhelminthes of chickens in SokotoMetropolis NigeriardquoNigerianVeterinary Journal vol 29 no 1 pp 72ndash75 2008

[36] S Luka and I Ndams ldquo(2007) Gastrointestinal parasites ofdomestic chicken Gallus-gallus domesticus Linnaeus 1758 inSamaru Zaria Nigeriardquo ScienceWorld Journal vol 2 no 1 2007

[37] C Ohaeri and C Okwum ldquoHelminthic parasites of domesticfowls in Ikwuano Abia State Nigeriardquo Journal of NaturalSciences Research vol 1 2013

[38] M Mwale and P J Masika ldquoPoint prevalence study of gastro-intestinal parasites in village chickens of Centane district SouthAfricardquoAfrican Journal of Agricultural Research vol 6 no 9 pp2033ndash2038 2011

Hindawiwwwhindawicom

International Journal of

Volume 2018

Zoology

Hindawiwwwhindawicom Volume 2018

Anatomy Research International

PeptidesInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Journal of Parasitology Research

GenomicsInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Hindawiwwwhindawicom Volume 2018

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Neuroscience Journal

Hindawiwwwhindawicom Volume 2018

BioMed Research International

Cell BiologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Biochemistry Research International

ArchaeaHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Genetics Research International

Hindawiwwwhindawicom Volume 2018

Advances in

Virolog y Stem Cells International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Enzyme Research

Hindawiwwwhindawicom Volume 2018

International Journal of

MicrobiologyHindawiwwwhindawicom

Nucleic AcidsJournal of

Volume 2018

Submit your manuscripts atwwwhindawicom

Page 5: Prevalence of Gastrointestinal Parasites in Local and Exotic …downloads.hindawi.com/journals/jpr/2019/5746515.pdf · 2019-09-02 · In Ghana, the village or backyard poultry production

Journal of Parasitology Research 5

Table 1 Prevalence of gastro-intestinal helminths of local and exotic breeds of chicken in Pankrono- Kumasi Ghana

Parasite No Infected (n=131) Prevalence in population ()Ascaridia galli 65 325Heterakis gallinarum 38 190Capillaria spp 29 145Raillietina spp 19 95Choanotaenia infundibulum 5 25Tetrameres americana 5 25Davainea proglottina 4 20Gongylonema ingluvocola 4 20Prosthogonimus spp 3 15

(a) (b)

(c) (d)

Figure 3 Photographs of some eggs of gastrointestinal helminths of local and exotic breeds of chicken in Pankrono-Kumasi Ghana (a)Capillaria egg (b) H gallinarum (c) Ascarid egg and (d) Choanotaenia infundibulum

the exotic breeds which are fed usually on artificial dietsThis could also be a likely reason for the higher infectionin the local breeds which continue to accumulate parasitesin the system as well as the poor management practicesinherent in free range system [33] It could be said that theexotic breeds were in confinement where good managerialpractices such as regular deworming might have occurredand hence recording a low prevalence This indicates thatin areas where the keeping of local breed is more commonparasite infestation will be a threat to the socioeconomicsurvival of many farmers because there will be a high cost ofproduction with low output [21]

Although the exotic breeds recorded the least prevalencerate in the study area the figure obtained (550) is high fora commercial production systemThis presupposes therefore

that the handling andor management practices at these pro-duction sites are woefully poor The unhygienic conditionsin these sites have created a conducive environment for thesurvival of the larvae of these parasites

The study revealed that female birds recorded manygastrointestinal helminths than the males in both breedseven though there is no significant difference in the figuresobtained This could be by chance or may be related totheir feeding habit as the females are known to be morevoracious in their feeding habits especially during egg pro-duction than the males which remain largely selective [25]Though some zoonotic parasites can be found in chickensthe ones recovered in this study were not zoonotic andtherefore might not pose any risk of infection to han-dlers

6 Journal of Parasitology Research

5 Conclusions

The overall prevalence of gastrointestinal helminths was655 with Ascaridia galli found to be the most prevalentThe helminths discovered were mostly nematodes cestodesand a trematode Local breeds were found to have manygastrointestinal helminths than the exotic breeds as theyrecorded the most prevalence In relation to sex the resultsrevealed that female birds were more prone to the parasitesthan the males as observed in both breeds

6 Recommendations

It is recommended that farmers under the free-range andintensive systems of poultry keeping should be educatedby veterinary extension officers on the various kinds ofgastrointestinal parasites in association with chickens andpoultry as a whole and the dangers they pose

The prevalence level shown by the birds in the studyarea is a clue to the susceptibility of the domestic fowl tomany infectious diseases that may be detrimental to humanconsumption It is therefore recommended that handlersand managers of poultry farms should improve upon theirmanagement skills and issues concerning hygiene Veteri-nary Extension Officers are also requested to pay particularattention to the managerial practices of farmers in the areaand provide the necessary assistance in protecting the healthand wellbeing of poultry as well as contributing to publichealth protection It is also recommended that further studiesshould be carried on the subject matter covering differentmethods and parameters to enhance better results

Data Availability

The data used to support the findings of this study areincluded in the article however the raw data is also availableupon request from the corresponding author

Conflicts of Interest

The authors did not find any conflicts of interest

Authorsrsquo Contributions

The concept of the study was initiated by Philip AsumangHe and Akoto Justice Delali and Wiafe Frimpong Francistogether discussed thoroughly and came up with the designof the study The initial and final draft of the manuscriptwere prepared by Gadafi Iddrisu Balali on the strictest senseafter a discussion with Philip on the definition of intellectualcontent All the authors contributed in the literature searchand manuscript preparation and editing in general howeverPhilip Zeba Kamil and Gadafi did the final literature searchIn the overall preparation of manuscript and editing ingeneral Philip Gadafi Grace Pinamang Vera Afua DelaGobe and Wilson Nketiah Siaw contributed chiefly AlsoPhilip Gadafi Justice Francis and Vera reviewed and edited

the finalmanuscript ORCID ID of the corresponding author0000-0002-2471-9357

References

[1] J Bruinsma World Agriculture Towards 20152030 an FAOStudy Routledge 2017

[2] H K Sebho ldquoExotic chicken status production performanceand constraints in ethiopia a reviewrdquo Asian Journal of PoultryScience vol 10 no 1 pp 30ndash39 2016

[3] O C Jegede P I Bolorunduro and E I Ikani ldquoLevels ofawareness and adoption of disseminated livestock technologiesin Enugu State Nigeriardquo Journal of Food Agriculture andEnvironment (JFAE) vol 5 no 2 pp 185ndash188 2007

[4] J JWMacharia ldquoPhenotypic CharacterizationAndFunctionalPolymorphisms at Prolactin And Vipr1 Genes in EmergingPoultry Species fromWestern Kenyardquo Jkuat-Cohes 2018

[5] M Gilbert G Conchedda T P Van Boeckel et al ldquoIncomedisparities and the global distribution of intensively farmedchicken and pigsrdquo PLoS ONE vol 10 no 7 Article ID e01333812015

[6] C E Bennett R Thomas M Williams et al ldquoThe broilerchicken as a signal of a human reconfigured biosphererdquo RoyalSociety Open Science vol 5 no 12 Article ID 180325 2018

[7] S Barbut Poultry Products Processing An Industry Guide CRCpress 2016

[8] B Y Folitse J Sam L P Dzandu and S K Osei ldquoPoul-try farmersrsquo information needs and sources in selected ruralcommunities in the greater accra region ghanardquo InternationalInformation and Library Review vol 50 no 1 pp 1ndash12 2018

[9] R Osei-Amponsah B Kayang A Naazie M Tiexier-Boichard and X Rognon ldquoPhenotypic characterization of localGhanaian chickens egg-laying performance under improvedmanagement conditionsrdquo Animal Genetic ResourcesResourcesGenetiques AnimalesRecursos Geneticos Animales vol 56 pp29ndash35 2015

[10] M C Brena Y Mekonnen J M Bettridge et al ldquoChangingrisk of environmental Campylobacter exposure with emergingpoultry production systems in Ethiopiardquo Epidemiology andInfection vol 144 no 3 pp 567ndash575 2016

[11] J De Bruyn E Ferguson M Allman-Farinelli et al ldquoFoodcomposition tables in resource-poor settings Exploring currentlimitations and opportunities with a focus on animal-sourcefoods in sub-Saharan Africardquo British Journal of Nutrition vol116 no 10 pp 1709ndash1719 2016

[12] K E Banson G Muthusamy and E Kondo ldquoThe importsubstituted poultry industry evidence from Ghanardquo 2015

[13] H Djang-Fordjour ldquoIdentifying broiler meat production chal-lenges in Ghana focusing on hatchery performancerdquo 2017

[14] H Junaidu S Luka and A Mijinyawa Prevalence of Gas-trointestinal Helminth Parasites of The Domestic Fowl (Gallus-Gallus Domesticus) Slaughtered in Giwa Market Giwa LocalGovernment Area vol 7 Kaduna state Nigeria prevalence 19edition 2014

[15] T Gjedrem N Robinson and M Rye ldquoThe importance ofselective breeding in aquaculture to meet future demands foranimal protein A reviewrdquo Aquaculture vol 350-353 pp 117ndash129 2012

[16] M Tuffour and B A Oppong ldquoProfit efficiency in broilerproduction evidence from greater accra region of ghanardquo

Journal of Parasitology Research 7

International Journal of Food and Agricultural Economics vol2 no 1 p 23 2014

[17] N P Steyn Z Mchiza J Hill et al ldquoNutritional contributionof street foods to the diet of people in developing countriesa systematic reviewrdquo Public Health Nutrition vol 17 no 6 pp1363ndash1374 2014

[18] K Killebrew and R Plotnick Poultry Market in West AfricaGhana Evans School Policy Analysis and Research (EPAR) Briefvol 83 2010

[19] N Yenibehit M Murshed and M Islam ldquoAssessment of tech-nical efficiency of layer production in mampong municipalitystochastic frontier approachrdquo Current Research in AgriculturalSciences vol 6 no 1 pp 20ndash28 2019

[20] A I Youssef and SUga ldquoReview of parasitic zoonoses in EgyptrdquoTropical Medicine and Health 2013

[21] O Agbolade A Arosoye E Akajiugo et al ldquoGastrointestinalparasites of domestic fowls from Ijebu Northrdquo southwesternNigeria Basic Research Journal of Agricultural Sciences vol 3no 7 pp 60ndash64 2014

[22] H Ashenafi and Y Eshetu ldquoStudy on gastrointestinal helminthsof local chickens in central ethiopiardquo Revue de MedecineVeterinaire vol 155 no 10 pp 504ndash507 2004

[23] U FAO ldquoFAOstatrdquo 2014[24] A Organization ldquoThe state of food insecurity in the world 2014

Strengthening the enabling environment for food security andnutritionrdquo Food and Agriculture Organization 2014

[25] E Sonaiya Toward Sustainable Poultry Production in AfricaFAO Expert Consultation on Strategies for Sustainable AnimalAgriculture in Developing Countries Italy Rome 1990

[26] C I Ogbaje E O Agbo and O J Ajanusi ldquoPrevalence ofAscaridia galli Heterakis gallinarum and tapeworm infectionsin birds slaughtered in Makurdi townshiprdquo International Jour-nal of Poultry Science vol 11 no 2 pp 103ndash107 2012

[27] S Satish and M Priti ldquoGastro intestinal helminths parasites oflocal chickens samples from tribal areas of Madhya PradeshrdquoInternational Journal of Life Science vol 1 no 4 pp 284ndash2872013

[28] K Cervantes-Rivera J A Villag A Arroyo-Lara L A Landın-Grandvallet and J A Villagomez-Cortes ldquoA diagnostic surveyof gastroenteric helminths in backyard poultry of a rural villagein Mexican tropicsrdquo 2006

[29] J Yang and Scholten T ldquoDientamoeba fragilis a review withnotes on its epidemiology pathogenicity mode of transmissionand diagnosisrdquo The American Journal of Tropical Medicine andHygiene vol 26 no 1 pp 16ndash22 1977

[30] S Lane and D Lloyd ldquoCurrent trends in research into thewaterborne parasite Giardiardquo Critical Reviews in Microbiologyvol 28 no 2 pp 123ndash147 2002

[31] S Kumar R Garg H Ram P S Maurya and P S Baner-jee ldquoGastrointestinal parasitic infections in chickens of uppergangetic plains of India with special reference to poultrycoccidiosisrdquo Journal of Parasitic Diseases vol 39 no 1 pp 22ndash26 2013

[32] E Soulby helminthes Arthropods and Protozoa of DomesticatedAnimals ( Edu) Bailliere Tindal East Sussex 7th editionhelminthes Arthropods and protozoa of domesticatedAnimals(u) Bailliere Tindal East Sussex

[33] E Matur E Ergul I Akyazi E Eraslan and Z T Cirakli ldquoTheeffects of Saccharomyces cerevisiae extract on the weight ofsome organs liver and pancreatic digestive enzyme activity inbreeder hens fed diets contaminated with aflatoxinsrdquo PoultryScience vol 89 no 10 pp 2213ndash2220 2010

[34] B YehualashetA Study onThe Prevalence of Helminth Parasitesin Free Range (Backyard) Chicken in Selected Small Holder Farmsin And around Haramaya [DVM thesis] College of VeterinaryMedicine Haramaya University Ethiopia 2011

[35] H Mikail and Y Adamu ldquoA survey of the gastrointestinalhelminthes of chickens in SokotoMetropolis NigeriardquoNigerianVeterinary Journal vol 29 no 1 pp 72ndash75 2008

[36] S Luka and I Ndams ldquo(2007) Gastrointestinal parasites ofdomestic chicken Gallus-gallus domesticus Linnaeus 1758 inSamaru Zaria Nigeriardquo ScienceWorld Journal vol 2 no 1 2007

[37] C Ohaeri and C Okwum ldquoHelminthic parasites of domesticfowls in Ikwuano Abia State Nigeriardquo Journal of NaturalSciences Research vol 1 2013

[38] M Mwale and P J Masika ldquoPoint prevalence study of gastro-intestinal parasites in village chickens of Centane district SouthAfricardquoAfrican Journal of Agricultural Research vol 6 no 9 pp2033ndash2038 2011

Hindawiwwwhindawicom

International Journal of

Volume 2018

Zoology

Hindawiwwwhindawicom Volume 2018

Anatomy Research International

PeptidesInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Journal of Parasitology Research

GenomicsInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Hindawiwwwhindawicom Volume 2018

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Neuroscience Journal

Hindawiwwwhindawicom Volume 2018

BioMed Research International

Cell BiologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Biochemistry Research International

ArchaeaHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Genetics Research International

Hindawiwwwhindawicom Volume 2018

Advances in

Virolog y Stem Cells International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Enzyme Research

Hindawiwwwhindawicom Volume 2018

International Journal of

MicrobiologyHindawiwwwhindawicom

Nucleic AcidsJournal of

Volume 2018

Submit your manuscripts atwwwhindawicom

Page 6: Prevalence of Gastrointestinal Parasites in Local and Exotic …downloads.hindawi.com/journals/jpr/2019/5746515.pdf · 2019-09-02 · In Ghana, the village or backyard poultry production

6 Journal of Parasitology Research

5 Conclusions

The overall prevalence of gastrointestinal helminths was655 with Ascaridia galli found to be the most prevalentThe helminths discovered were mostly nematodes cestodesand a trematode Local breeds were found to have manygastrointestinal helminths than the exotic breeds as theyrecorded the most prevalence In relation to sex the resultsrevealed that female birds were more prone to the parasitesthan the males as observed in both breeds

6 Recommendations

It is recommended that farmers under the free-range andintensive systems of poultry keeping should be educatedby veterinary extension officers on the various kinds ofgastrointestinal parasites in association with chickens andpoultry as a whole and the dangers they pose

The prevalence level shown by the birds in the studyarea is a clue to the susceptibility of the domestic fowl tomany infectious diseases that may be detrimental to humanconsumption It is therefore recommended that handlersand managers of poultry farms should improve upon theirmanagement skills and issues concerning hygiene Veteri-nary Extension Officers are also requested to pay particularattention to the managerial practices of farmers in the areaand provide the necessary assistance in protecting the healthand wellbeing of poultry as well as contributing to publichealth protection It is also recommended that further studiesshould be carried on the subject matter covering differentmethods and parameters to enhance better results

Data Availability

The data used to support the findings of this study areincluded in the article however the raw data is also availableupon request from the corresponding author

Conflicts of Interest

The authors did not find any conflicts of interest

Authorsrsquo Contributions

The concept of the study was initiated by Philip AsumangHe and Akoto Justice Delali and Wiafe Frimpong Francistogether discussed thoroughly and came up with the designof the study The initial and final draft of the manuscriptwere prepared by Gadafi Iddrisu Balali on the strictest senseafter a discussion with Philip on the definition of intellectualcontent All the authors contributed in the literature searchand manuscript preparation and editing in general howeverPhilip Zeba Kamil and Gadafi did the final literature searchIn the overall preparation of manuscript and editing ingeneral Philip Gadafi Grace Pinamang Vera Afua DelaGobe and Wilson Nketiah Siaw contributed chiefly AlsoPhilip Gadafi Justice Francis and Vera reviewed and edited

the finalmanuscript ORCID ID of the corresponding author0000-0002-2471-9357

References

[1] J Bruinsma World Agriculture Towards 20152030 an FAOStudy Routledge 2017

[2] H K Sebho ldquoExotic chicken status production performanceand constraints in ethiopia a reviewrdquo Asian Journal of PoultryScience vol 10 no 1 pp 30ndash39 2016

[3] O C Jegede P I Bolorunduro and E I Ikani ldquoLevels ofawareness and adoption of disseminated livestock technologiesin Enugu State Nigeriardquo Journal of Food Agriculture andEnvironment (JFAE) vol 5 no 2 pp 185ndash188 2007

[4] J JWMacharia ldquoPhenotypic CharacterizationAndFunctionalPolymorphisms at Prolactin And Vipr1 Genes in EmergingPoultry Species fromWestern Kenyardquo Jkuat-Cohes 2018

[5] M Gilbert G Conchedda T P Van Boeckel et al ldquoIncomedisparities and the global distribution of intensively farmedchicken and pigsrdquo PLoS ONE vol 10 no 7 Article ID e01333812015

[6] C E Bennett R Thomas M Williams et al ldquoThe broilerchicken as a signal of a human reconfigured biosphererdquo RoyalSociety Open Science vol 5 no 12 Article ID 180325 2018

[7] S Barbut Poultry Products Processing An Industry Guide CRCpress 2016

[8] B Y Folitse J Sam L P Dzandu and S K Osei ldquoPoul-try farmersrsquo information needs and sources in selected ruralcommunities in the greater accra region ghanardquo InternationalInformation and Library Review vol 50 no 1 pp 1ndash12 2018

[9] R Osei-Amponsah B Kayang A Naazie M Tiexier-Boichard and X Rognon ldquoPhenotypic characterization of localGhanaian chickens egg-laying performance under improvedmanagement conditionsrdquo Animal Genetic ResourcesResourcesGenetiques AnimalesRecursos Geneticos Animales vol 56 pp29ndash35 2015

[10] M C Brena Y Mekonnen J M Bettridge et al ldquoChangingrisk of environmental Campylobacter exposure with emergingpoultry production systems in Ethiopiardquo Epidemiology andInfection vol 144 no 3 pp 567ndash575 2016

[11] J De Bruyn E Ferguson M Allman-Farinelli et al ldquoFoodcomposition tables in resource-poor settings Exploring currentlimitations and opportunities with a focus on animal-sourcefoods in sub-Saharan Africardquo British Journal of Nutrition vol116 no 10 pp 1709ndash1719 2016

[12] K E Banson G Muthusamy and E Kondo ldquoThe importsubstituted poultry industry evidence from Ghanardquo 2015

[13] H Djang-Fordjour ldquoIdentifying broiler meat production chal-lenges in Ghana focusing on hatchery performancerdquo 2017

[14] H Junaidu S Luka and A Mijinyawa Prevalence of Gas-trointestinal Helminth Parasites of The Domestic Fowl (Gallus-Gallus Domesticus) Slaughtered in Giwa Market Giwa LocalGovernment Area vol 7 Kaduna state Nigeria prevalence 19edition 2014

[15] T Gjedrem N Robinson and M Rye ldquoThe importance ofselective breeding in aquaculture to meet future demands foranimal protein A reviewrdquo Aquaculture vol 350-353 pp 117ndash129 2012

[16] M Tuffour and B A Oppong ldquoProfit efficiency in broilerproduction evidence from greater accra region of ghanardquo

Journal of Parasitology Research 7

International Journal of Food and Agricultural Economics vol2 no 1 p 23 2014

[17] N P Steyn Z Mchiza J Hill et al ldquoNutritional contributionof street foods to the diet of people in developing countriesa systematic reviewrdquo Public Health Nutrition vol 17 no 6 pp1363ndash1374 2014

[18] K Killebrew and R Plotnick Poultry Market in West AfricaGhana Evans School Policy Analysis and Research (EPAR) Briefvol 83 2010

[19] N Yenibehit M Murshed and M Islam ldquoAssessment of tech-nical efficiency of layer production in mampong municipalitystochastic frontier approachrdquo Current Research in AgriculturalSciences vol 6 no 1 pp 20ndash28 2019

[20] A I Youssef and SUga ldquoReview of parasitic zoonoses in EgyptrdquoTropical Medicine and Health 2013

[21] O Agbolade A Arosoye E Akajiugo et al ldquoGastrointestinalparasites of domestic fowls from Ijebu Northrdquo southwesternNigeria Basic Research Journal of Agricultural Sciences vol 3no 7 pp 60ndash64 2014

[22] H Ashenafi and Y Eshetu ldquoStudy on gastrointestinal helminthsof local chickens in central ethiopiardquo Revue de MedecineVeterinaire vol 155 no 10 pp 504ndash507 2004

[23] U FAO ldquoFAOstatrdquo 2014[24] A Organization ldquoThe state of food insecurity in the world 2014

Strengthening the enabling environment for food security andnutritionrdquo Food and Agriculture Organization 2014

[25] E Sonaiya Toward Sustainable Poultry Production in AfricaFAO Expert Consultation on Strategies for Sustainable AnimalAgriculture in Developing Countries Italy Rome 1990

[26] C I Ogbaje E O Agbo and O J Ajanusi ldquoPrevalence ofAscaridia galli Heterakis gallinarum and tapeworm infectionsin birds slaughtered in Makurdi townshiprdquo International Jour-nal of Poultry Science vol 11 no 2 pp 103ndash107 2012

[27] S Satish and M Priti ldquoGastro intestinal helminths parasites oflocal chickens samples from tribal areas of Madhya PradeshrdquoInternational Journal of Life Science vol 1 no 4 pp 284ndash2872013

[28] K Cervantes-Rivera J A Villag A Arroyo-Lara L A Landın-Grandvallet and J A Villagomez-Cortes ldquoA diagnostic surveyof gastroenteric helminths in backyard poultry of a rural villagein Mexican tropicsrdquo 2006

[29] J Yang and Scholten T ldquoDientamoeba fragilis a review withnotes on its epidemiology pathogenicity mode of transmissionand diagnosisrdquo The American Journal of Tropical Medicine andHygiene vol 26 no 1 pp 16ndash22 1977

[30] S Lane and D Lloyd ldquoCurrent trends in research into thewaterborne parasite Giardiardquo Critical Reviews in Microbiologyvol 28 no 2 pp 123ndash147 2002

[31] S Kumar R Garg H Ram P S Maurya and P S Baner-jee ldquoGastrointestinal parasitic infections in chickens of uppergangetic plains of India with special reference to poultrycoccidiosisrdquo Journal of Parasitic Diseases vol 39 no 1 pp 22ndash26 2013

[32] E Soulby helminthes Arthropods and Protozoa of DomesticatedAnimals ( Edu) Bailliere Tindal East Sussex 7th editionhelminthes Arthropods and protozoa of domesticatedAnimals(u) Bailliere Tindal East Sussex

[33] E Matur E Ergul I Akyazi E Eraslan and Z T Cirakli ldquoTheeffects of Saccharomyces cerevisiae extract on the weight ofsome organs liver and pancreatic digestive enzyme activity inbreeder hens fed diets contaminated with aflatoxinsrdquo PoultryScience vol 89 no 10 pp 2213ndash2220 2010

[34] B YehualashetA Study onThe Prevalence of Helminth Parasitesin Free Range (Backyard) Chicken in Selected Small Holder Farmsin And around Haramaya [DVM thesis] College of VeterinaryMedicine Haramaya University Ethiopia 2011

[35] H Mikail and Y Adamu ldquoA survey of the gastrointestinalhelminthes of chickens in SokotoMetropolis NigeriardquoNigerianVeterinary Journal vol 29 no 1 pp 72ndash75 2008

[36] S Luka and I Ndams ldquo(2007) Gastrointestinal parasites ofdomestic chicken Gallus-gallus domesticus Linnaeus 1758 inSamaru Zaria Nigeriardquo ScienceWorld Journal vol 2 no 1 2007

[37] C Ohaeri and C Okwum ldquoHelminthic parasites of domesticfowls in Ikwuano Abia State Nigeriardquo Journal of NaturalSciences Research vol 1 2013

[38] M Mwale and P J Masika ldquoPoint prevalence study of gastro-intestinal parasites in village chickens of Centane district SouthAfricardquoAfrican Journal of Agricultural Research vol 6 no 9 pp2033ndash2038 2011

Hindawiwwwhindawicom

International Journal of

Volume 2018

Zoology

Hindawiwwwhindawicom Volume 2018

Anatomy Research International

PeptidesInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Journal of Parasitology Research

GenomicsInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Hindawiwwwhindawicom Volume 2018

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Neuroscience Journal

Hindawiwwwhindawicom Volume 2018

BioMed Research International

Cell BiologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Biochemistry Research International

ArchaeaHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Genetics Research International

Hindawiwwwhindawicom Volume 2018

Advances in

Virolog y Stem Cells International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Enzyme Research

Hindawiwwwhindawicom Volume 2018

International Journal of

MicrobiologyHindawiwwwhindawicom

Nucleic AcidsJournal of

Volume 2018

Submit your manuscripts atwwwhindawicom

Page 7: Prevalence of Gastrointestinal Parasites in Local and Exotic …downloads.hindawi.com/journals/jpr/2019/5746515.pdf · 2019-09-02 · In Ghana, the village or backyard poultry production

Journal of Parasitology Research 7

International Journal of Food and Agricultural Economics vol2 no 1 p 23 2014

[17] N P Steyn Z Mchiza J Hill et al ldquoNutritional contributionof street foods to the diet of people in developing countriesa systematic reviewrdquo Public Health Nutrition vol 17 no 6 pp1363ndash1374 2014

[18] K Killebrew and R Plotnick Poultry Market in West AfricaGhana Evans School Policy Analysis and Research (EPAR) Briefvol 83 2010

[19] N Yenibehit M Murshed and M Islam ldquoAssessment of tech-nical efficiency of layer production in mampong municipalitystochastic frontier approachrdquo Current Research in AgriculturalSciences vol 6 no 1 pp 20ndash28 2019

[20] A I Youssef and SUga ldquoReview of parasitic zoonoses in EgyptrdquoTropical Medicine and Health 2013

[21] O Agbolade A Arosoye E Akajiugo et al ldquoGastrointestinalparasites of domestic fowls from Ijebu Northrdquo southwesternNigeria Basic Research Journal of Agricultural Sciences vol 3no 7 pp 60ndash64 2014

[22] H Ashenafi and Y Eshetu ldquoStudy on gastrointestinal helminthsof local chickens in central ethiopiardquo Revue de MedecineVeterinaire vol 155 no 10 pp 504ndash507 2004

[23] U FAO ldquoFAOstatrdquo 2014[24] A Organization ldquoThe state of food insecurity in the world 2014

Strengthening the enabling environment for food security andnutritionrdquo Food and Agriculture Organization 2014

[25] E Sonaiya Toward Sustainable Poultry Production in AfricaFAO Expert Consultation on Strategies for Sustainable AnimalAgriculture in Developing Countries Italy Rome 1990

[26] C I Ogbaje E O Agbo and O J Ajanusi ldquoPrevalence ofAscaridia galli Heterakis gallinarum and tapeworm infectionsin birds slaughtered in Makurdi townshiprdquo International Jour-nal of Poultry Science vol 11 no 2 pp 103ndash107 2012

[27] S Satish and M Priti ldquoGastro intestinal helminths parasites oflocal chickens samples from tribal areas of Madhya PradeshrdquoInternational Journal of Life Science vol 1 no 4 pp 284ndash2872013

[28] K Cervantes-Rivera J A Villag A Arroyo-Lara L A Landın-Grandvallet and J A Villagomez-Cortes ldquoA diagnostic surveyof gastroenteric helminths in backyard poultry of a rural villagein Mexican tropicsrdquo 2006

[29] J Yang and Scholten T ldquoDientamoeba fragilis a review withnotes on its epidemiology pathogenicity mode of transmissionand diagnosisrdquo The American Journal of Tropical Medicine andHygiene vol 26 no 1 pp 16ndash22 1977

[30] S Lane and D Lloyd ldquoCurrent trends in research into thewaterborne parasite Giardiardquo Critical Reviews in Microbiologyvol 28 no 2 pp 123ndash147 2002

[31] S Kumar R Garg H Ram P S Maurya and P S Baner-jee ldquoGastrointestinal parasitic infections in chickens of uppergangetic plains of India with special reference to poultrycoccidiosisrdquo Journal of Parasitic Diseases vol 39 no 1 pp 22ndash26 2013

[32] E Soulby helminthes Arthropods and Protozoa of DomesticatedAnimals ( Edu) Bailliere Tindal East Sussex 7th editionhelminthes Arthropods and protozoa of domesticatedAnimals(u) Bailliere Tindal East Sussex

[33] E Matur E Ergul I Akyazi E Eraslan and Z T Cirakli ldquoTheeffects of Saccharomyces cerevisiae extract on the weight ofsome organs liver and pancreatic digestive enzyme activity inbreeder hens fed diets contaminated with aflatoxinsrdquo PoultryScience vol 89 no 10 pp 2213ndash2220 2010

[34] B YehualashetA Study onThe Prevalence of Helminth Parasitesin Free Range (Backyard) Chicken in Selected Small Holder Farmsin And around Haramaya [DVM thesis] College of VeterinaryMedicine Haramaya University Ethiopia 2011

[35] H Mikail and Y Adamu ldquoA survey of the gastrointestinalhelminthes of chickens in SokotoMetropolis NigeriardquoNigerianVeterinary Journal vol 29 no 1 pp 72ndash75 2008

[36] S Luka and I Ndams ldquo(2007) Gastrointestinal parasites ofdomestic chicken Gallus-gallus domesticus Linnaeus 1758 inSamaru Zaria Nigeriardquo ScienceWorld Journal vol 2 no 1 2007

[37] C Ohaeri and C Okwum ldquoHelminthic parasites of domesticfowls in Ikwuano Abia State Nigeriardquo Journal of NaturalSciences Research vol 1 2013

[38] M Mwale and P J Masika ldquoPoint prevalence study of gastro-intestinal parasites in village chickens of Centane district SouthAfricardquoAfrican Journal of Agricultural Research vol 6 no 9 pp2033ndash2038 2011

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International Journal of

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GenomicsInternational Journal of

Hindawiwwwhindawicom Volume 2018

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The Scientific World Journal

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Hindawiwwwhindawicom Volume 2018

BioinformaticsAdvances in

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ArchaeaHindawiwwwhindawicom Volume 2018

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Hindawiwwwhindawicom Volume 2018

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Hindawiwwwhindawicom Volume 2018

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Nucleic AcidsJournal of

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Submit your manuscripts atwwwhindawicom

Page 8: Prevalence of Gastrointestinal Parasites in Local and Exotic …downloads.hindawi.com/journals/jpr/2019/5746515.pdf · 2019-09-02 · In Ghana, the village or backyard poultry production

Hindawiwwwhindawicom

International Journal of

Volume 2018

Zoology

Hindawiwwwhindawicom Volume 2018

Anatomy Research International

PeptidesInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Journal of Parasitology Research

GenomicsInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawi Publishing Corporation httpwwwhindawicom Volume 2013Hindawiwwwhindawicom

The Scientific World Journal

Volume 2018

Hindawiwwwhindawicom Volume 2018

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Neuroscience Journal

Hindawiwwwhindawicom Volume 2018

BioMed Research International

Cell BiologyInternational Journal of

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Biochemistry Research International

ArchaeaHindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Genetics Research International

Hindawiwwwhindawicom Volume 2018

Advances in

Virolog y Stem Cells International

Hindawiwwwhindawicom Volume 2018

Hindawiwwwhindawicom Volume 2018

Enzyme Research

Hindawiwwwhindawicom Volume 2018

International Journal of

MicrobiologyHindawiwwwhindawicom

Nucleic AcidsJournal of

Volume 2018

Submit your manuscripts atwwwhindawicom