prevalence of haemonchus contortus infections in sheep and...

Research ArticlePrevalence of Haemonchus contortus Infections in Sheepand Goats in Nyagatare District Rwanda

BordenMushonga1 Dismas Habumugisha2 Erick Kandiwa1 Oscar Madzingira1

Alaster Samkange 1 Basiamisi Ernest Segwagwe3 and Ishmael Festus Jaja4

1 School of Veterinary Medicine Faculty of Agriculture and Natural Resources University of Namibia P Bag 13301Pioneerspark Windhoek Namibia

2School of Animal Sciences and Veterinary Medicine College of Agriculture Environment and Veterinary MedicineUniversity of Rwanda PO Box 57 Nyagatare Rwanda

3Department of Biomedical Sciences Faculty of Medicine University of Botswana P Bag UB0074 Gaborone Botswana4Department of Livestock and Pasture Science University of Fort Hare P Bag X1314 Alice South Africa

Correspondence should be addressed to Alaster Samkange alastersamkangegmailcom

Received 7 June 2018 Accepted 27 August 2018 Published 6 September 2018

Academic Editor William Alberto Canon-Franco

Copyright copy 2018 Borden Mushonga et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

This study investigated the overall prevalence ofHaemonchus contortus infection in sheep and goats from five purposively selectedsubdivisions (sectors) of Nyagatare district from January to December 2014 after a high prevalence of gastrointestinal parasitesand generalized poor productivity was reported in small ruminants in some districts of Rwanda Faecal egg counts (FEC) wereperformed using the Modified Wisconsin Sugar Floatation method and the Fluorescent-labeled peanut-lectin agglutination testwhile enumerations as log (FEC) were done using themodifiedMcMastermethodThe overall prevalenceofH contortus infectionin sheep and goats was 757 (n=949) The overall prevalence ofH contortus infection in sheep (834 n=314) was higher than ingoats (718 n=635) (Odds Ratio [OR] 198 95 Confidence Interval [CI] 140-279 and ple0001)The prevalence of H contortusinfection in female goats (742) was higher than inmale goats (643) (OR 160 95 CI 109-236 and p=001)The prevalence ofH contortus infection in goats fromNyagatarewas higher than in goats fromMatimba (OR325 95CI 176-599 and ple0001) andfrom Katabagemu (OR 367 95 CI 204-659 and ple0001)The prevalence ofH contortus infection in goats from Karangazi washigher than in goats fromMatimba (OR 472 95CI 240-928 and ple0001)The overall meanmonthly log (FEC) forH contortusin sheep and goats were highest in April (189plusmn02 and 1405plusmn01 respectively) and October (1925plusmn 02 and 1375plusmn01 respectively)Though overall sheep in Nyagatare district were at greater risk of H contortus infection and goats from Nyagatare and Karangazisectors were paradoxically at greater risk of H contortus infection It was also apparent that young female goats were at greaterrisk of H contortus infection than young male goats H contortus infection is endemic in small ruminants in Nyagatare districtand possibly other districts in Rwanda Targeted selective treatment (TST) using FAMACHAwith emphasis on low-lying swampypastures and appropriate anthelmintic drugs may be the most economically viable solution in the short term In the long termbreeding ofH contortus resistant small ruminants and strategic grazing using the concept of refugia may bring about considerablerelief from H contortus infection in Nyagatare district in particular and Rwanda at large

1 Introduction

Due to their hardiness and fecundity small ruminants play acrucial role in the cultural and socioeconomic lives of ruralpeople in Africa providing meat milk income and wealth[1ndash4]

Helminth infections are one of the most importantdiseases limiting livestock production in many parts of theworld including Rwanda [5ndash8] Gastrointestinal helminthescause significant economic losses of small ruminant enter-prises through increased susceptibility of animals to otherinfections morbidities and mortalities especially in heavily

HindawiJournal of Veterinary MedicineVolume 2018 Article ID 3602081 9 pageshttpsdoiorg10115520183602081

2 Journal of Veterinary Medicine

parasitized animals and in young animals Furthermore theylead to forced culling carcass and organ condemnations[9] increased cost of veterinary treatments decreased weightgain reduced milk production and reproductive capacitydecreased work capacity diminished food intake reducedanimal growth rates and lower weight gains and treatmentand management costs [8ndash12] Among these gastrointestinalhelminths nematodes are the leading cause of ill-health andproduction losses in sheep and goats worldwide [7 10 13]It would appear that a number of reports point to Tri-chostrongylid nematodes especially Haemonchus contortus(H contortus) (also known as the barberrsquos pole worm) asthe most prevalent parasite identified in small ruminants[8 10 11] According to some reports Haemonchus contortusis themost important gastrointestinal parasite in sheep [5 14]However in a survey in South Eastern Ethiopia Haemonchusspp was not found [15]

H contortus is a helminth parasite of the abomasum ofruminants and in particular sheep and goats It is the mosteconomically important and pathogenic helminth parasite ofsmall ruminants in the warm tropical and subtropical regionsof the world [5 8 13 16 17] Acutely infected sheep andgoats exhibit pale mucous membranes dark colored faecesweakness and edema (bottle jaw) and may die suddenlyChronic disease may manifest as decreased appetite weightloss and anemia [18] Young animals usually carry heavierburdens than adult sheep and goats Occurrence and severityof H contortus infection also depend on the rainfall patternsand temperatures of an area [13] High rainfall and temper-atures promote rapid hatching of eggs on pasture and henceincreased contamination

The prevalence of H contortus infections in a flockprovides a good indication of the parasite burdens andthe magnitude of production losses Ambient temperatureenvironmental humidity grazing behavior of the host andquantity and quality of pasture are some factors responsiblefor the prevalence of gastrointestinal helminths Outbreaksare most common and severe in warm humid climates [19]Other risk factors which include host species sex age bodycondition breed [16] and intensity of worm infections affectthe development of gastrointestinal parasites [20]

Overall prevalence of H contortus infection in smallruminants has been reported variably by different studiesfrom as low as 527 to over 83 [13 15 16 21 22] OneEthiopian study reported a prevalence of 672 and 566 insheep and goats respectively [16] indicating greater suscep-tibility of sheep For instance a study in Ethiopia reportedprevalence of 901-965 in sheep and 818-100 in goats[13] In South Africa the prevalence ofH contortus infectionin sheep has been reported at 68 using the FAMACHAscore and 100 with the Hawkesley microhematocrit reader[23]The same study reported that H contortus was the mostprevalent nematode parasite just as had been reported in anearlier study in that country [1] Reports from other studiesindicate that the prevalence ofH contortus infection is alwayshigher in sheep than in goats in the same geographical area Ina study conducted in Rwanda Haemonchus spp were foundto be the predominant parasite species in small ruminantswith very high infection rates [3]

There are limited reports on the prevalence of gastroin-testinal parasites in Rwanda [3 21] The prevalence hasbeen reported to be around 58 in Bugesera district in theSouthern Province of Rwanda [21] and 889 in kids and733 in lambs in Musanze in the Northern Province ofRwanda [3]

Until today there are very few reports on the prevalenceof nematode parasites in Rwanda and to the best of ourknowledge no studies have been undertaken to assess theburden Haemonchus spp and its implications on smallruminant production on in Nyagatare The objectives of thisstudy were to determine the prevalence of H contortus eggshedding and the prevalence of Haemonchus spp infectionsusing coprocultures in sheep and goats from five selectedsectors of the Nyagatare district where sheep and goatsplay an important part in human livelihood and sustenanceFurthermore the study aimed to determine the significanceof parasite infections and recommend strategic preventiveand control measures with aim of improving the productivityof this sector

2 Materials and Methods

21 Study Area The study area was in Nyagatare district (1∘181015840010158401015840S 30∘ 201015840 010158401015840E) Of the 14 sectors in Nyagatare fivesectors were chosen for this study Karangazi in the EastTabagwe in the West Matimba in the North Katabagemu inthe South and Nyagatare in the centre (Figure 1) There aretwo wet seasons in Nyagatare district the first is from Febru-ary to May and the second from September to NovemberAverage precipitation ranges between 1000mm and 1200mmannually Average temperatures vary between 178∘Cand 21∘C

22 Study Design A cross-sectional study was used wherefive sectors were purposively selected out of the 14 sectorsof Nyagatare district based on location (ie North SouthEast West and Centre) Selection of sheep and goats fromeach sector was done biased towards goats whose populationis roughly double that of the sheep in Nyagatare district Arandom digits table was then used for simple random sam-pling of animals within each sector Male and female sheep(local cross and South African Meat Merino breeds) andthe small East African goat and its crosses with the AlpineAnglo-Nubian and Angora goat breeds raised extensively oncommunal land in the five sectors were sampled [24]

23 Faecal Sample Collection Faecal samples were collectedper rectum monthly from January to December 2014 fromyoung and adult sheep and goats of all sexes raised on naturalpastures in the five sectors A total of 949 faecal samples werecollected from both sheep (n=314) and goats (n=635) Faeceswere scooped from the rectum of small ruminants using agloved index finger in animals restrained in a standing posi-tion Each sample was placed in a separate plastic containerwith a screw cap labeled placed on ice and transported tothe laboratory at the College of Agriculture Environmentand Veterinary Medicine University of Rwanda for analysisSamples that were not tested on the same day were stored at+4∘C

Journal of Veterinary Medicine 3

Figure 1 Map of Nyagatare districtrsquos potentialities wetlands Source httpwwwnyagataregovrwfileadmintemplatesRaportsNyagatarePotentialitiespdf

24 Parasite Identification and Enumeration of H contortusEggs Parasite eggs in faecal samples (3 grams) from eachanimal were isolated using the Modified Wisconsin SugarFloatation method [25] Following centrifugation the super-natant was incubated with Fluorescent-labeled peanut-lectin(Arachis hypogaea) agglutinin (Sigma L7381) to identify andenumerate H contortus eggs [26] Faecal egg counts (FEC)per gram of faeces were performed following the modifiedMcMaster method as described [27] at a sensitivity of 50 eggsper gram (EPG) of faeces

25 Statistical Analysis Descriptive and inferential statis-tics performed in SPSS version 25 Cross-tabulations wereperformed to test differences in occurrence of H contortusinfections between sectors and within species age andsex categories of animals P values le005 were consideredsignificant

3 Results

Overall 757 of the small ruminants under study in Nya-gatare district (n = 949) had H contortus eggs in faeces Theprevalence ofH contortus infection in sheep (834 n = 314)was significantly higher than that in goats of (718 n = 635)(plt005)

As shown in Table 1 the overall prevalence ofH contortusinfection in male and female sheep was 835 and 834respectively and that inmale and female goats was 643 and742 respectively

As shown in Table 2 significant differences existed inthe prevalence of H contortus infection between sheep andgoats (Odds Ratio [OR] 198 95 Confidence Interval [CI]

140-279 and ple0001) There was no difference in theprevalence of H contortus infection when age or sex wasconsidered in sheep Female goats had a higher prevalenceof H contortus infection than male goats (OR 160 95 CI109-236 and p=001) and similarly young female goats had ahigher prevalence of H contortus infection than young malegoats (OR 173 95 CI 101-296 and p=003)

As shown in Table 3 the prevalence of H contortusinfection in sheep fromNyagatare and Karangazi sectors was88 and 90 respectively and that in goats was 854 and895 respectively The prevalence of H contortus infectionin sheep from Tabagwe Matimba and Katabagemu sectorswas 707 738 and 726 respectively and that in goatswas 551 643 and 615 respectively

As shown in Table 4 there was no significant differencein the occurrence of H contortus infections in sheep betweenthe five sectors (pgt005)

As shown in Table 5 the prevalence of H contortusinfection in goats from Nyagatare sector was greater thanin goats from Matimba (OR 325 95 CI 176-599 andple0001) and Katabagemu sectors (OR 367 95 CI 204-659 and ple0001) The prevalence of H contortus infectionin goats fromKarangazi (895)was also greater than in goatsfromMatimba (OR 472 95 CI 240-928 and ple0001)

As shown in Figure 2 two distinct periods of higherlevel of H contortus infection were observed in the firsthalf (February-May) and last half of the year (September-November) A decrease in level of H contortus infec-tion in both sheep and goat was apparent from June toAugust

As shown in Figure 3 a higher level of H contortusinfection in goats was recorded in all sectors from February


Table 1 Prevalence of H contortus infectionin small ruminants of Nyagatare district

Category Positive animals () Negative animals () Total animals ()SheepMale sheep 111 (835) 22 (165) 133 (424)

Adult male 41 (820) 9 (180) 50 (159)Young male 70 (843) 13 (157) 83 (264)

Female sheep 151 (834) 30 (166) 181 (576)Adult female 103 (858) 17 (142) 120 (382)Young female 48 (787) 13 (213) 61 (194)

Overall sheep 262 (834) 52 (166) 314 (1000)GoatsMale goats 99 (643) 55 (357) 154 (243)


Female goats 357 (742) 124 (258) 481 (757)Adult female 221 (742) 77 (258) 298 (469)Young female 136 (743) 47 (257) 183 (288)

Overall goats 456 (718) 179 (282) 635 (1000)Total animals 718 (757) 231 (243) 949 (1000)

Table 2 Comparison of H contortus infections between and within species

Cross-tabulated categories Odds ratio (95 CI) p-valueBetween species

Sheep versus goats 198 (140-279) le0001lowastAdult sheep versus adult goats 206 (128-333) le0001lowastYoung sheep versus young goats 190 (116-313) 001lowast

Within sheepMales versus females 100 (055-183) 056Adult females versus adult males 133 (055-322) 034Young males versus young females 146 (062-342) 026Young males versus adult males 118 (046-301) 045Adult females versus young females 164 (074-365) 016

Within goatsFemales versus males 160 (109-236) 001lowastAdult females versus adult males 144 (080-257) 015Young females versus young males 173 (101-296) 003lowastAdult males versus young males 119 (061-234) 037Young females versus adult females 101 (066-154) 053lowastSignificant difference since ple005

Table 3 Prevalence of H contortus infectionin sheep and goats in the five sectors of Nyagatare district

Category Nyagatare Karangazi Tabagwe Matimba Katabagemu TotalSheepAnimals positive () 73 (880) 55 (902) 41 (707) 48 (738) 53 (726) 262 (834)Animals negative () 10 (120) 6 (98) 11 (190) 12 (185) 13 (178) 52 (166)GoatsAnimals positive () 117 (854) 119 (895) 65 (551) 72 (643) 83 (615) 456 (718)Animals negative () 20 (146) 14 (105) 53 (449) 40 (357) 52 (385) 179 (282)Grand Total 194 194 176 177 208 949


Table 4 Comparison of H contortus infections in sheep between sectors

Cross-tabulated sectors Odds ratio (95 CI) p-valueKarangazi versus Nyagatare 126 (043-366) 045Nyagatare versus Tabagwe 195 (077-500) 012Nyagatare versus Matimba 183 (073-456) 014Nyagatare versus Katabagemu 179 (073-439) 015Karangazi versus Tabagwe 246 (084-720) 008Karangazi versus Matimba 229 (080-657) 009Karangazi versus Katabagemu 225 (080-635) 010Matimba versus Tabagwe 107 (043-269) 053Katabagemu versus Tabagwe 109 (044-269) 051Katabagemu versus Matimba 102 (042-245) 057

Table 5 Comparison of H contortus infections in goats between sectors

Cross-tabulated sectors Odds ratio (95 CI) p-valueKarangazi versus Nyagatare 145 (070-301) 020Nyagatare versus Tabagwe 477 (263-867) 761Nyagatare versus Matimba 325 (176-599) le0001lowastNyagatare versus Katabagemu 367 (204-659) le0001lowastKarangazi versus Tabagwe 693 (358-1344) 472Karangazi versus Matimba 472 (240-928) le0001lowastKarangazi versus Katabagemu 533 (277-1023) 599Matimba versus Tabagwe 147 (086-249) 010Katabagemu versus Tabagwe 130 (079-215) 018Matimba versus Katabagemu 113 (067-190) 037lowastSignificant difference since ple005

0

1

2

3

4

5

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Log(

FEC)

Month

Log(FEC) in sheep Log(FEC) in goats

Figure 2 Monthly log (FEC) trends in sheep and goats for the five sectors in Nyagatare district in 2014

005

115

225

335

445


Log(

FEC)

Month Nyagatare Karangazi Tabagwe Matimba Katabagemu

Figure 3 Mean monthly log (FEC) trends for goats per sector in Nyagatare district in 2014


0

1

2

3

4

5

6

7


Log(

FEC)

Month

Nyagatare Karangazi Tabagwe Matimba Katabagemu

Figure 4 Mean monthly log (FEC) for sheep per sector in Nyagatare district in 2014

to May and from September to November with a decrease inlevel of infection from June to August and in December

As shown in Figure 4 a higher level of H contortusinfection in sheep was recorded in all sectors from Februaryto May and from September to November with a decrease inlevel of infection from June to August and in December

4 Discussion

Table 1 shows that about 76 of small ruminants in this studyshed Haemonchus eggs in their faeces These results indicatea very high level of infection This high level of infectionmay partly explain the low productivity of small ruminants inRwanda as reported in another study [21] This phenomenonof high nematode prevalence is not new in tropical countriesSimilarly high levels of nematode infection like 8308889 and even 100 have been reported in India Rwandaand Pakistan respectively [3 22 28] In the present studysheep and goats were raised under an extensive managementsystem inmostly low-lying pastures where stocking densitieswere high nutrition was limited and veterinary care wasalmost nonexistent One study demonstrated a positive cor-relation between nematode infection and land elevation [28]These factors promote the exposure of livestock to infectivelarvae from pastures and the establishment of infections inanimals [16]

A significantly higher proportion of sheep (834) thangoats (718) had H contortus eggs in their faeces indicatingthat sheep aremore susceptible toH contortus infections thangoats This observation is consistent with the findings of ear-lier work in Ethiopia [13 16] that showed higherH contortusinfection in sheep than in goats However in another studyin a different part of Ethiopia a higher Haemonchus sppinfection in goats (713) than sheep (6757) was reported[29] Studies in neighbouring Uganda have reported theprevalence of goats shedding nematode eggs at 537 [10]which is lower than that reported in this study This may

be explained by the differences in management practicessuch as stocking density and ecoclimatic factors Hot humidareas that receive high rainfall are ideal for reproduction ofnematode parasites contamination of pastures and survivalof infective larvae Higher stocking densities promote pasturecontamination and within-flock transmission of nematodeinfections The results of this study contradicted the findingsof another study undertaken in Bangladesh which reported ahigher occurrence ofH contortus infection in goats (3556)than in sheep (20) in that same study the overall prevalenceof gastrointestinal parasitic infection was also found to behigher in goats (45 than in sheep (40) [30]

The higher prevalence value in sheep than goats arisesfrom the fact that sheep predominantly graze closer tothe ground where infective nematode larvae are prevalentwhile goats are predominantly browsers and feed on shrubsabove the ground where infective larvae are fewer [16]However there are a variety of factors which can convolutethis expectation These factors include host age sex andbreeding status grazing habits the level of education andeconomic capacity of farmers the standard of managementand anthelmintic used [30]

There were no statistically significant differences in theshedding of nematode eggs between male and female sheep(Table 2) These results are in agreement with the findings ofa study from Ethiopia [31] and Bangladesh [32] In contrasta significantly higher number of female than male goats hadnematode eggs in their faeces Previous studies have shownthat female animals are at risk of heavy nematode burdensdue to the immunosuppression associated with pregnancyand periparturient periods [7 15 16 22] In our study thisphenomenon was apparent in goats but not in sheep

Young animals are generally considered to be moresusceptible to nematode infection than adults [6 32] dueto immature active immunity and lack of adaptation in theyoung [6] On the other end immunity also wanes with ageIn our study the differences in nematode infections between


adult and young sheep and goats were not statisticallysignificant (Table 2) Older animals would not influence theresult much because most families sell the biggest (usuallythe oldest) animals in order to raise the most money inRwanda [21] The finding of having no difference in youngthan old animals is in agreement with reports from Ethiopiawhich indicated that helminth infections affect both youngand adult animals equally [31]

The prevalence of sheep and goats that shed nematodeeggs in faeces differed by sector of origin Nyagatare andKarangazi sectors had a significantly higher prevalence ofsheep and goats that shed nematode eggs in faeces than sheepand goats from Tabagwe and Matimba and Katabagemusectors (Figure 4) No significant differences were apparentin the proportions of small ruminants with nematode eggsin faeces between Nyagatare and Karangazi sectors (plt005)These findings are explained by the variations local elevationprecipitation hydrology and pedology between the sectorsFigure 1 shows that Karangazi and Nyagatare both havevery extensive hydrological systems and hence flooding andswamp formation is likely This explains the high infectionrates in these 2 sectors Besides Karangazi is adjacent to agame reserve increasing the likelihood of sharing of parasiteswith game On the other hand Tabagwe Matimba andKatabagemu are generally somewhat mountainous and donot promote H contortus infection due to high elevationwhich favour the growth of browse but not grassland

Figure 3 shows that faecal egg shedding varied with timeof the year in both sheep and goats Higher faecal egg countswere reported from February to May with a peak in Apriland from September to November with a peak in Octobercoinciding with the two rainy seasons that are typical ofthe Nyagatare district Therefore rainfall was an importantdeterminant of nematode infection and burden in the studyareaMoisture plays a supporting role in the development andsurvival of the infective stages of nematodes on pasture [33]Faecal egg counts were significantly higher in the five sectorsin February March April and May than in SeptemberOctober and November The lowest FEC were recorded inJune July August and December coinciding with the periodof low rainfall

Haemonchus contortus eggs were recovered from 834of sheep and 718 goats Our study focused on H contortusparasite because it has been reported in many studies as thepredominant and most pathogenic of sheep and goat parasite[13 16 17] that causes considerable economic losses to thesmall ruminant industry Results from coprocultures corre-lated positively with the faecal egg counts Our findings arewithin the range of prevalence of 696 and 901 reportedin sheep and prevalence of 571 and 818 reported in goats[13]The overall prevalence ofH contortus infection in smallruminants of 757 reported in this study is comparableto overall prevalence of 7103 and 7738 documented byother studies [13] This study showed that small ruminantsharboredH contortus infections throughout the yearwith thehighest prevalence occurring during the rainy seasons

The use of chemicals (mainly anthelminthic drugs) hasbeen standard practice for the control of H contortus inruminants for decades [34] However the efficacy of this

method has been seriously curtailed by the developmentof anthelminthic drug resistance the world over This hasnecessitated the development of alternative techniques suchas rotation of anthelminthic class of drugs [35] breeding foranthelminthic resistance [4] vaccination [34] FAMACHAfor the implementation of targeted selective treatments(TST) copper oxide wire particles (COWP) nematode trap-ping fungi strategic grazing that avoids parasite-laden pas-tures phytotherapy [36 37] and strategic grazing applyingthe concept of refugia [38]

5 Conclusion

Given the high pathogenicity of H contortus compared withother nematode species it can be concluded that sheep andgoat farmers in the Nyagatare district are at a relatively higherrisk of economic loss resulting from reduced productivitymorbidity and possibly mortality in their flocks It is wellknown thatH contortus is a problem in hot humid conditionssuch as occurs in summer in Nyagatare

Data Availability

The data used to support the findings of this study areavailable from the corresponding author upon request

Conflicts of Interest

The authors declare that they have no conflicts of interest

References

[1] F R Bakunzi L K Nkomo L E Motsei R V Ndou and MNyirenda ldquoA survey on anthelmintic resistance in nematodeparasites of communally grazed sheep and goats in a rural areaof North West Province Republic of South Africardquo Life ScienceJournal vol 10 no 2 pp 391ndash393 2013

[2] L Gebresilassie and B Afera Tadele ldquoPrevalence of ovineHaemonchosis in Wukro ethiopiardquo Journal of ParasitologyResearch vol 2015 2015

[3] N Juvenal N Carine S J dArc andM Edward ldquoAn analysis ofthe dynamics of gastro-intestinal nematode infection in smallruminants in the northern region of Rwandardquo InternationalJournal of Animal and Veterinary vol 3 no 3 pp 128ndash134 2011

[4] P I Zvinorova T E Halimani F C Muchadeyi O Matika VRiggio and K Dzama ldquoPrevalence and risk factors of gastroin-testinal parasitic infections in goats in low-input low-outputfarming systems in Zimbabwerdquo Small Ruminant Research vol143 pp 75ndash83 2016

[5] R Sharma and S Ganguly ldquoGastrointestinal Nematodiasis inSmall Ruminants and Anthelmintic Resistance A ReviewrdquoJournal of Immunology and Immunopathology vol 18 no 2 pp100ndash104 2016

[6] M Sohail M Nauman-ul-Islam S S A Shah I A Shah ARaziq andM I Khan ldquoIncidence of gastrointestinal parasites inbeetal goats at District Peshawar Pakistanrdquo Advances in Animaland Veterinary Sciences vol 5 no 5 pp 205ndash207 2017

[7] H M Rizwan M S Sajid Z Iqbal and M Saqib ldquoPointprevalence of gastrointestinal parasites of domestic sheep (Ovis


aries) in district Sialkot Punjab Pakistanrdquo Journal of Animaland Plant Sciences vol 27 no 3 pp 803ndash808 2017

[8] S El-Ashram I Al Nasr R Mehmood M Hu L He and XSuo ldquoHaemonchus Contortus and Ovine Host a RetrospectiveReviewrdquo International Journal of Advanced Research vol 5 no3 pp 972ndash999 2017

[9] I F Jaja B Mushonga E Green and V Muchenje ldquoA quantita-tive assessment of causes of bovine liver condemnation and itsimplication for food security in the eastern cape province SouthAfricardquo Sustainability vol 9 no 5 2017

[10] G Nsereko P Emudong H Mulindwa and J Okwee-AcaildquoPrevalence of common gastro-intestinal nematode infectionsin commercial goat farms in Central Ugandardquo Uganda Journalof Agricultural Sciences vol 16 no 1 pp 99ndash106 2016

[11] I S Elshahawy A M Metwally and D A Ibrahim ldquoAnabattoir-based study on helminthes of slaughtered goats (CaprahircusL 1758) in upperEgypt EgyptrdquoHelminthologia (Poland)vol 51 no 1 pp 67ndash72 2014

[12] I F Jaja B Mushonga E Green and V Muchenje ldquoSeasonalprevalence body condition score and risk factors of bovinefasciolosis in South AfricardquoVeterinary and Animal Science vol4 pp 1ndash7 2017

[13] B Abdo W Tesfaye and T Shibbiru ldquoPrevalence of Haemon-chosis and Associated Risk Factors in Small Ruminants Slaugh-tered at Bishoftu ELFORA Export Abattoirrdquo Journal of NaturalSciences Research vol 7 no 7 pp 48ndash52 2017

[14] S A Fleming T Craig R M Kaplan J E Miller C Navarreand M Rings ldquoAnthelmintic resistance of gastrointestinalparasites in small ruminantsrdquo Journal of Veterinary InternalMedicine vol 20 no 2 pp 435ndash444 2006

[15] K K Elemo and M A Geresu ldquoPrevalence and Risk Factorsof Gastro Intestinal Parasitesof Small Ruminants in Sinana andDinsho Districts of Bale Zonerdquo European Journal of BiologicalSciences vol 9 no 1 pp 01ndash08 2017

[16] T Badaso and M Addis ldquoSmall Ruminants HaemonchosisPrevalence and Associated Risk Factors in Arsi NegelleMunici-pal Abattoir EthiopiardquoGlobal Veterinaria vol 15 no 3 pp 315ndash320 2015

[17] S Blackie ldquoA Review of the Epidemiology of GastrointestinalNematode Infections in Sheep and Goats in Ghanardquo Journal ofAgricultural Science vol 6 no 4 pp 109ndash118 2014

[18] F Roeber A R Jex and R B Gasser ldquoImpact of gastrointestinalparasitic nematodes of sheep and the role of advanced molec-ular tools for exploring epidemiology and drug resistancemdashanAustralian perspectiverdquo Parasites amp Vectors vol 6 no 1 article153 2013

[19] J A Gadahi M J Arshed Q Ali S B Javaid and S I ShahldquoPrevalence of gastrointestinal parasites of sheep and goat inand around Rawalpindi and Islamabad Pakistanrdquo VeterinaryWorld vol 2 no 2 pp 51ndash53 2009

[20] K Tariq M Chishti and F Ahmad ldquoGastro-intestinal nema-tode infections in goats relative to season host sex and age fromthe Kashmir valley Indiardquo Journal of Helminthology vol 84 no01 pp 93ndash97 2010

[21] MManzi J Mutabazi C D Hirwa andD R Kugonza ldquoSocio-economic assessment of indigenous goat production system inrural areas of Bugesera District in Rwandardquo Livestock Researchfor Rural Development vol 25 no 11 2013

[22] E Singh P Kaur L D Singla and M S Bal ldquoPrevalence ofgastrointestinal parasitism in small ruminants in western zoneof Punjab IndiardquoVeterinaryWorld vol 10 no 1 pp 61ndash66 2017

[23] K Rampedi W Smit P Soma B DubeW Luus-Powell and AHalajian ldquoPrevalence of helminth parasites from sheep in theMohlonong village Limpopo Province Preliminary surveyrdquo inProceedings of the South African Society for Animal Science 49thCongress Limpopo South African July 2016

[24] Borden Mushonga Sylvine Twiyizeyimna Gervais Habaru-gira et al ldquoStudy of Incidence of Gross Urogenital Lesionsand Abnormalities on Does Slaughtered at Nyagatare Slaugh-terhouse Eastern Province Rwandardquo Journal of VeterinaryMedicine vol 2017 Article ID 7564019 7 pages 2017

[25] H J Haji Q D Bickle M Ramsan et al ldquoA comparisonof methods for detecting the eggs of Ascaris Trichuris andhookworm in infant stool and the epidemiology of infection inZanzibari infantsrdquo The American Journal of Tropical Medicineand Hygiene vol 76 no 4 pp 725ndash731 2007

[26] M E Jurasek J K Bishop-Stewart B E Storey R M Kaplanand M L Kent ldquoModification and further evaluation of afluorescein-labeled peanut agglutinin test for identification ofHaemonchus contortus eggsrdquo Veterinary Parasitology vol 169no 1-2 pp 209ndash213 2010

[27] HGlennonModifiedMcMasterrsquos Fecal Egg Counting TechniqueNC State Extension Publications 2015 httpwwwcontentcesncsuedu

[28] V Kantzoura M K Kouam H Theodoropoulou H Feidasand G Theodoropoulos ldquoPrevalence and Risk Factors ofGastrointestinal Parasitic Infections in Small Ruminants in theGreek Temperate Mediterranean Environmentrdquo Open Journalof Veterinary Medicine vol 02 no 01 pp 25ndash33 2012

[29] Z Mengist N Abebe G Gugsa and N Kumar ldquoAssessment ofSmall Ruminant Haemonchosis and Its Associated Risk Factorsin and Around Finoteselam Ethiopiardquo Journal of Agriculturaland Veterinary Science vol 7 no 12 pp 36ndash41 2014

[30] M Hossain M J Bhuiyan M S Alam et al ldquoCross sec-tional epidemiological investigation on the prevalence of gas-trointestinal parasites of small ruminants in sullah upazillaof sunamgonj district Bangladeshrdquo Journal of Advances inParasitology vol 2 no 4 pp 100ndash104 2015

[31] M Getachew R Tesfaye and E Sisay ldquoPrevalence and RiskFactors of Gastrointestinal Nematodes Infections in SmallRuminants in Tullo District Western Harerghe EthiopiardquoJournal of Veterinary Science amp Technology vol 08 no 02 pp8ndash11 2017

[32] P R Poddar N Begum M A Alim A R Dey M S Hossainand S S Labony ldquoPrevalence of gastrointestinal helminths ofsheep in Sherpur Bangladeshrdquo Journal of Advanced Veterinaryand Animal Research vol 4 no 3 pp 274ndash280 2017

[33] T Zeryehun ldquoHelminthosis of sheep and goats in andaroundHaramaya SoutheasternEthiopiardquo Journal ofVeterinaryMedicine and Animal Health vol 4 no 3 pp 48ndash55 2012

[34] A F I M D Matos C O R Nobre J P Monteiro C M LBevilaqua D W Smith and M Teixeira ldquoAttempt to controlHaemonchus contortus in dairy goats with Barbervax a vac-cine derived from the nematode gut membrane glycoproteinsrdquoSmall Ruminant Research vol 151 pp 1ndash4 2017

[35] D M Leathwick ldquoManaging anthelmintic resistance-Parasitefitness drug use strategy and the potential for reversion towardssusceptibilityrdquoVeterinary Parasitology vol 198 no 1-2 pp 145ndash153 2013

[36] J G M Houdijk I Kyriazakis A Kidane and S AthanasiadouldquoManipulating small ruminant parasite epidemiology throughthe combination of nutritional strategiesrdquo Veterinary Parasitol-ogy vol 186 no 1-2 pp 38ndash50 2012


[37] T H Terrill J E Miller J M Burke J A Mosjidis and R MKaplan ldquoExperienceswith integrated concepts for the control ofHaemonchus contortus in sheep and goats in the United StatesrdquoVeterinary Parasitology vol 186 no 1-2 pp 28ndash37 2012

[38] S M Muchiut A S Fernandez P E Steffan E Riva and C AFiel ldquoAnthelmintic resistance Management of parasite refugiafor Haemonchus contortus through the replacement of resistantwith susceptible populationsrdquo Veterinary Parasitology vol 254pp 43ndash48 2018

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parasitized animals and in young animals Furthermore theylead to forced culling carcass and organ condemnations[9] increased cost of veterinary treatments decreased weightgain reduced milk production and reproductive capacitydecreased work capacity diminished food intake reducedanimal growth rates and lower weight gains and treatmentand management costs [8ndash12] Among these gastrointestinalhelminths nematodes are the leading cause of ill-health andproduction losses in sheep and goats worldwide [7 10 13]It would appear that a number of reports point to Tri-chostrongylid nematodes especially Haemonchus contortus(H contortus) (also known as the barberrsquos pole worm) asthe most prevalent parasite identified in small ruminants[8 10 11] According to some reports Haemonchus contortusis themost important gastrointestinal parasite in sheep [5 14]However in a survey in South Eastern Ethiopia Haemonchusspp was not found [15]

H contortus is a helminth parasite of the abomasum ofruminants and in particular sheep and goats It is the mosteconomically important and pathogenic helminth parasite ofsmall ruminants in the warm tropical and subtropical regionsof the world [5 8 13 16 17] Acutely infected sheep andgoats exhibit pale mucous membranes dark colored faecesweakness and edema (bottle jaw) and may die suddenlyChronic disease may manifest as decreased appetite weightloss and anemia [18] Young animals usually carry heavierburdens than adult sheep and goats Occurrence and severityof H contortus infection also depend on the rainfall patternsand temperatures of an area [13] High rainfall and temper-atures promote rapid hatching of eggs on pasture and henceincreased contamination

The prevalence of H contortus infections in a flockprovides a good indication of the parasite burdens andthe magnitude of production losses Ambient temperatureenvironmental humidity grazing behavior of the host andquantity and quality of pasture are some factors responsiblefor the prevalence of gastrointestinal helminths Outbreaksare most common and severe in warm humid climates [19]Other risk factors which include host species sex age bodycondition breed [16] and intensity of worm infections affectthe development of gastrointestinal parasites [20]

Overall prevalence of H contortus infection in smallruminants has been reported variably by different studiesfrom as low as 527 to over 83 [13 15 16 21 22] OneEthiopian study reported a prevalence of 672 and 566 insheep and goats respectively [16] indicating greater suscep-tibility of sheep For instance a study in Ethiopia reportedprevalence of 901-965 in sheep and 818-100 in goats[13] In South Africa the prevalence ofH contortus infectionin sheep has been reported at 68 using the FAMACHAscore and 100 with the Hawkesley microhematocrit reader[23]The same study reported that H contortus was the mostprevalent nematode parasite just as had been reported in anearlier study in that country [1] Reports from other studiesindicate that the prevalence ofH contortus infection is alwayshigher in sheep than in goats in the same geographical area Ina study conducted in Rwanda Haemonchus spp were foundto be the predominant parasite species in small ruminantswith very high infection rates [3]

There are limited reports on the prevalence of gastroin-testinal parasites in Rwanda [3 21] The prevalence hasbeen reported to be around 58 in Bugesera district in theSouthern Province of Rwanda [21] and 889 in kids and733 in lambs in Musanze in the Northern Province ofRwanda [3]

Until today there are very few reports on the prevalenceof nematode parasites in Rwanda and to the best of ourknowledge no studies have been undertaken to assess theburden Haemonchus spp and its implications on smallruminant production on in Nyagatare The objectives of thisstudy were to determine the prevalence of H contortus eggshedding and the prevalence of Haemonchus spp infectionsusing coprocultures in sheep and goats from five selectedsectors of the Nyagatare district where sheep and goatsplay an important part in human livelihood and sustenanceFurthermore the study aimed to determine the significanceof parasite infections and recommend strategic preventiveand control measures with aim of improving the productivityof this sector

2 Materials and Methods

21 Study Area The study area was in Nyagatare district (1∘181015840010158401015840S 30∘ 201015840 010158401015840E) Of the 14 sectors in Nyagatare fivesectors were chosen for this study Karangazi in the EastTabagwe in the West Matimba in the North Katabagemu inthe South and Nyagatare in the centre (Figure 1) There aretwo wet seasons in Nyagatare district the first is from Febru-ary to May and the second from September to NovemberAverage precipitation ranges between 1000mm and 1200mmannually Average temperatures vary between 178∘Cand 21∘C

22 Study Design A cross-sectional study was used wherefive sectors were purposively selected out of the 14 sectorsof Nyagatare district based on location (ie North SouthEast West and Centre) Selection of sheep and goats fromeach sector was done biased towards goats whose populationis roughly double that of the sheep in Nyagatare district Arandom digits table was then used for simple random sam-pling of animals within each sector Male and female sheep(local cross and South African Meat Merino breeds) andthe small East African goat and its crosses with the AlpineAnglo-Nubian and Angora goat breeds raised extensively oncommunal land in the five sectors were sampled [24]

23 Faecal Sample Collection Faecal samples were collectedper rectum monthly from January to December 2014 fromyoung and adult sheep and goats of all sexes raised on naturalpastures in the five sectors A total of 949 faecal samples werecollected from both sheep (n=314) and goats (n=635) Faeceswere scooped from the rectum of small ruminants using agloved index finger in animals restrained in a standing posi-tion Each sample was placed in a separate plastic containerwith a screw cap labeled placed on ice and transported tothe laboratory at the College of Agriculture Environmentand Veterinary Medicine University of Rwanda for analysisSamples that were not tested on the same day were stored at+4∘C





3 Results































0

1

2

3

4

5


Log(

FEC)

Month



005

115

225

335

445


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FEC)




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1

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Log(

FEC)

Month





4 Discussion














5 Conclusion


Data Availability




References














































Microbiology












Volume 2018



Agronomy







Volume 2018

Zoology






Volume 2018


Advances in

Virolog y











3 Results































0

1

2

3

4

5


Log(

FEC)

Month



005

115

225

335

445


Log(

FEC)




0

1

2

3

4

5

6

7


Log(

FEC)

Month





4 Discussion














5 Conclusion


Data Availability




References














































Microbiology












Volume 2018



Agronomy







Volume 2018

Zoology






Volume 2018


Advances in

Virolog y




























0

1

2

3

4

5


Log(

FEC)

Month



005

115

225

335

445


Log(

FEC)




0

1

2

3

4

5

6

7


Log(

FEC)

Month





4 Discussion














5 Conclusion


Data Availability




References














































Microbiology












Volume 2018



Agronomy







Volume 2018

Zoology






Volume 2018


Advances in

Virolog y








0

1

2

3

4

5

6

7


Log(

FEC)

Month





4 Discussion














5 Conclusion


Data Availability




References














































Microbiology












Volume 2018



Agronomy







Volume 2018

Zoology






Volume 2018


Advances in

Virolog y














5 Conclusion


Data Availability




References














































Microbiology












Volume 2018



Agronomy







Volume 2018

Zoology






Volume 2018


Advances in

Virolog y













































Microbiology












Volume 2018



Agronomy







Volume 2018

Zoology






Volume 2018


Advances in

Virolog y







prevalence of haemonchus contortus infections in sheep and...

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