International Research on Medical Sciences Vol.1(2), pp. 010-017, May, 2013 Available online at http://www.apexjournal.org

ISSN 2315-8845© 2013 Apex Journal International

Full Length Research Paper

Prevalence of species of helminthes parasites in cattle slaughtered in selected abattoirs in Port Harcourt,

South-south, Nigeria

Elele, Kingsely1*, Owhoeli, Ovutor2 and Gboeloh, Lebari Barine1

1Department of Biology, Ignatius Ajuru University of Education, Port Harcourt, P.M.B 5047 Port Harcourt, Nigeria.

2Department of Animal and Environmental Biology, University of Port Harcourt, P.M.B 5323 Choba, Rivers State,

Nigeria.

Accepted 8 May, 2013

A total of 251 stool samples were collected from four abattoirs in Port Harcourt metropolis, South-South Nigeria. The study showed that out of 129 exotic cattle (White Fulani) Bos indicus examined between the months of May - September, 2009, 80 were infected while out of 122 exotic cattle (White Sokoto) Bos

indica between the months of October, 2009 - February, 2010, 76, were infected with various species of gastrointestinal helminthes. The formol-ether concentration method was used to analyse the specimens. The study revealed that an overall prevalence of (62.1%) was recorded; out of which 80 (62.0%) and 76 (62.2%) were recorded for months of May - September, 2009 and October 2009 - February, 2010 respectively. The overall prevalence amongst the infected animals was not statistically significant (p>0.05). Species of helminthes revealed from the study were; Haemoncus, Strongyloides, Chabertia, Trichuris, Ostergia, Bunostonium, Trychostrongyloides, Ascaris, Tenia, Avitelina, Fasciola, Eurytrma, Gastrotylax, Schistosoma, Dicrocoelium. Key words: Gastrointestinal helminthes, Bos indicus, Prevalence, Port Harcourt Metropolis.

INTRODUCTION Ruminants; Cattle, Goats and sheep represent an important source of animal protein in many countries of the world, supplying a good percentage of the daily meat and dairy products in cities and villages in such countries including Nigeria (Nwosu et al., 2007). Apart from being the source of animal protein, their wastes are also very important in agriculture (Nawathe et al., 1985; Nwosu et al., 2007). These animals are used in special ceremonies such as wedding and burials in most parts of Nigeria. However, parasitic diseases, coupled with inadequate management hampered the productive husbandry of these animals (Nawathe et al., 1985, Fikru et al., 2006).

Gastrointestinal parasitic infections are world-wide problem for both small and large-scale farmers, but their impact is greater in Sub-Saharan Africa due to the availability of a wide range of agro-ecological factors suitable for diversified hosts and parasite species (Fikru et al., 2006). Gastrointestinal parasites are known to be widespread in Nigeria (Fabiyi, 1973; Eysker and

*Corresponding author. E-mail: kingsley_elele@yahoo.co.uk.

Ogunsusi, 1980) and limit ruminant production in many areas of the country (Eyster and Ogunsusi, 1980; Chiejina, 1987; Keyyu et al., 2005). The direct losses caused by these parasites are attributed to hyper-acuteness and death, premature slaughter and rejection of some parts at meat inspection whilst indirect losses include the reduction in productive potential such as decreased growth rate, weight loss, diarrhea, anorexia and sometimes anaemia (Soulby, 1986; Nahed et al., 2003; Gonzelez and Gonzelez, 2004).

Helminths or worms cause a wide range of health problems to both man and animals (Colley et al., 2001). Helminthiasis, in large part, is caused

by members of the

phyla Nematoda and Platyhelminthes (Kennedy, and Harnett, 2001). Species belonging to both phyla occupy numerous niches within

their mammalian hosts, ranging

from intestinal lumen to intravascular

and even intracellular sites (Littlewood, and Bray, 2001). They are responsible for substantial loss of productivity in the livestock industry. Their harmful effects on these animals range from gastro-enteritis, anorexia, abdominal distention, diarrhoea, emaciation etc, all of which result in serious economic losses to the farmer and the nation in

general (Junaidu and Adamu, 1997). Similarly, they constitute a major impediment to efficient and profitable livestock production (Akerejola et al., 1999).

The prevalence of gastrointestinal helminths is related to the agro-climatic conditions like quantity and quality of pasture, temperature, humidity and grazing behavior of the host (Pal and Qayyum, 1993). However specific parasites may be distributed throughout the world, they have different impact according to production system, management and geo-climatic conditions (Kennedy and Harnett, 2001).

The information on the prevalence and distribution of various species of gastrointestinal parasites of cattle and goats kept by the nomadic Fulani’s in Nigeria and those in Port Harcourt is important in the formulation of control strategies for the nomads and other farmers. MATERIALS AND METHODS Study area The study was conducted in Port Harcourt City; the capital of Rivers State, Nigeria. Obio/Akpor and Port Harcourt city Local governments are commonly referred to as Port Harcourt city (10). It is situated on the bonny River within the Niger Delta, South-South, Nigeria. The study area lies between latitude 4

0 40

1 and 7

0 10

1 to

longitude 70 55

1 east of the Greenwich meridian. It is

situated some 60km from the open sea, which is immediately where the coastal marshes give way to the land of the interior (18). Four abattoirs were selected from Rumuodumaya; Ogbogoro; Eliozu and Aluu communities in the study. Collection of faecal samples Faecal specimens were collected from Cattle in four selected abattoirs in Port Harcourt metropolitan area. Animals were slaughtered between the hours of 6.30 am and 8.00am daily for a period of ten months (May, 2009 to February, 2010). Faecal samples were randomly collected weekly from the intestines of slaughtered animals (Exotic and Indigenous). The samples were collected in clean labeled sterile vials, preserved in 10% formalin and taken to the laboratory for microscopic examination. Laboratory examination The Formol-ether concentration technique (Agyemang et al, 1997) was used to analyze the samples. 1 g of stool sample was emulsified with 4 ml of 10% formol saline in a test tube. The mixture was filtered into a test tube using a cloth gauge and 3-4 ml of diethyl ether was added and

Elele et al 011 shaken vigorously and allowed to stand for two minutes. The mixture was then centrifuged at 1000 revolutions per minutes (1000 rpm) for 3 minutes. Using a glass rod, the faecal debris from the side of the tube was loosened and the tube inverted to pour off the supernatants. The tube was returned to its original upright position and the fluid from the side of the tube allowed draining to the bottom. The deposit was mixed by tapping the tube with the finger and using a Pasteur pipette. A drop of the sediment was applied on a microscope slide; covered with a cover slip and examined under the microscope using ×10 and ×40 objectives. Lugol’s iodine was also used as a stain. RESULTS A total of 129 cattle were examined between the months of May- September 2009. Eighty (80) were infected with various species of gastrointestinal helminths as follows: Haemoncus species 3, 2, 2, 2, 3, Strongyloides spp 2,1,3,2,1, Chabertia spp 1,2,1,1,2, Trichuris spp 0,0,0,1,1, Ostergia spp 0,1,1,2,2, Bunostonium spp 1,1,1,1,2, Trichostrongylus spp 0,0,1,0,1, Ascaris spp 1,1,0,1,0, Tenia 1,0,0,0,1, Monezia spp 0,0,1,1,0, Avitellina spp 0,2,1,0,1, Dicrocoelium spp 1,0,2,1,1, Fasciola spp 2,2,2,2,0, Eurytrema spp 0,0,1,1,1, Gastrotylax spp 1,1,1,1,0, and Schistosoma spp 1,2,0,1,1, for the months of May, June, July, August and September respectively (Table 1).

A total of 122 cattle were examined between the months of October 2009- February 2010. Seventy-six (76) were infected with various species of gastrointestinal helminths as follows: Haemoncus species 3, 2, 2, 2, 3, Strongyloides spp 1,3,2,1,2, Chabertia spp 2,2,1,1,1, Trichuris spp 0,0,0,1,1, Ostergia spp 1,1,1,2,2, Bunostonium spp 1,1,1,1,1, Trichostrongylus spp 2,1,1,0,1, Ascaris spp 0,0,1,2,0, Tenia 2,0,1,1,2, Monezia spp 0,0,1,0,0, Avitellina spp 0,0,0,1,1, Dicrocoelium spp 0,0,0,0,1, Fasciola spp 1,1,0,1,1, Eurytrema spp 1,1,1,1,0, Gastrotylax spp 0,0,1,0,0, and Schistosoma spp 0,2,2,2,2, for the months of October, November, December, January and February respectively (Table 2 and Plates 1 to 3). DISCUSSION The result of the study clearly indicates a high prevalence rate of gastrointestinal helminthes in cattle slaughtered in four selected abbatoirs in Port Harcourt; namely, Eliozu, Ogbogoro, Rumuokoro and Aluu abbatoirs.

The study revealed that 62.1% of the sampled animals within the period were infected with various species of helminthes parasites. The cattle slaughtered between May - September, 2009 had a prevalence rate of 62.0% while October 2009 - February, 2010, had a prevalence rate of 62.2% (Tables 1 and 2 respectively). These

012 Int. Res. Med. Sci. Table 1. Species of helminths in cattle between the months of May 2008-February 2009.

Parasite type Nematodes Cestodes Trematodes

Mo

nth

s

No

. E

xam

ined

No

. In

fecte

d

Haem

on

cu

s

Str

on

gylo

ides

Ch

ab

ert

ia

Tri

ch

uri

s

Oste

rgia

Bu

no

sto

niu

m

Try

ch

ostr

on

gylo

ides

Ascari

s

Ten

ia

Mo

nezi

a

Avit

elin

a

Fascio

la

Eu

rytr

ma

Gastr

oty

lax

Sch

isto

so

ma s

pp

Dic

roco

eliu

m

May 27 14 3 2 1 0 1 0 1 1 0 0 2 0 1 1 1

June 25 15 2 1 2 0 1 1 0 1 0 0 2 2 0 1 2 -

July 24 17 2 3 1 1 1 1 0 0 1 1 2 1 1 0 2

August 29 17 2 2 1 2 1 0 1 0 1 0 2 1 1 1 1

September 24 17 3 1 2 1 2 2 1 0 1 0 1 0 1 0 1 0

Total (%) 129 80(62) 12(9.3) 9(6.9) 7(5.4) 2(1.5) 6(4.6) 6(4.6) 2(1.5) 3(2.3) 2(1.5) 2(1.5) 4(3.1) 8(6.2) 3(2.3) 4(3.1) 5(3.9) 4(3.1)

Table 2. Species of helminthes obtained between the months of October 2008 – February 2009 from exotic cattle.

Parasite Nematode Cestode Trematode

Mo

nth

s

No

. E

xam

ined

No

. In

fecte

d

Haem

on

cu

s

Str

on

gylo

ides

Ch

ab

ert

ia

Tri

ch

uri

s

Oste

rgia

Bu

no

sto

niu

m

Try

ch

ostr

on

gylo

ides

Ascari

s

Ten

ia

Mo

nezi

a

Avit

elin

a

Fascio

la

Eu

rytr

ma

Gastr

oty

lax

Sch

isto

so

ma s

pp

Dic

roco

eliu

m

October 23 14 3 1 2 0 1 1 2 0 2 0 0 1 1 0 0 0

November 23 14 2 3 2 0 1 1 1 0 0 0 0 1 1 0 2 0

December 23 15 2 2 1 0 1 1 1 1 1 1 0 0 1 1 2 0

January 26 17 2 1 1 1 2 1 0 2 1 0 1 1 1 0 2 0

February 25 16 3 2 1 1 2 1 0 0 2 0 1 1 0 0 2 1

Total (%) 122 76(62.2) 12(9.8) 9(7.3) 7(5.7) 2(1.6) 7(5.7) 5(4) 4(3.2) 3(2.4) 6(4.9) 1(0.8) 2(1.6) 4(3.2) 4(3.2) 1(0.8) 8(6.5) 1(0.8)

Elele et al 013

Strongyloides species

Hatching egg of Chabertia species

A B

D E

G

Ostergia species

Ascaris species Trichuris species

C

Chabertia species

F

Haemoncus species

Bunostonium species Trichostongylus spp

HI

Plate 1. Eggs of Nematodes as seen under the X40 objective of the microscope on slides stained with Lugol’s iodine.

Fasciola species Eurytrema species

Dicrocoelium speciesGastrotylax species Schistosoma japonicum

Schistosoma bovis

A B C

DE F

Plate 2. Eggs of Trematodes as seen under the X40 objective of the microscope on slides stained with Lugol’s iodine.

014 Int. Res. Med. Sci.

Moniezia benedeni Moniezia expansaAvitellina species

Tenia species

AB C

D

B

Plate 3. Eggs of Cestodes as seen under the X40 objective of the microscope on slides stained with Lugol’s iodine.

results are consistent with findings of different researchers in the semi-arid zone of North-Eastern and South-Eastern Nigeria (Anene et al., 1994a; Fakae, 1990; Fakae and Chiejina, 1993; Nwosu et al., 2007).

The helminthes community consisted of sixteen parasitic species, eight (8) nematodes (Haemonchus, Strongyloides, Chabertia, Trichuris, Ostergia, Bunostonium, Trichonstrongylus and Ascaris), three (3) Cestodes (Taenia, Moniezia and Avitellinium) and five (5) (Dicrocoelinum, Fasciola, Eurytrema, Gastrotylax and Schistosoma). Haemonchus species have the highest prevalence in all the samples analyzed that were positive. Fakae (1990) studies the epidemiology of helminthosis in ruminants under the traditional husbandry system in eastern Nigeria and reported prevalence of Haemonchus species as (87.1), higher than other helminthes species. It has been suggested that Haemonchus species can acquire resistance faster than any other gastrointestinal nematodes, like Trichostrongylus, because of its high biotic potential (Torres-Acosta et al., 2003). The area of study shows how vulnerable workers in the abbatoir and people who consume the intestinal parts of the animals may be vulnerable to infections especially to Taenia and Fasciola which are zoonotic and were observed in course of study. Globally, parasitic and other endemic diseases continue to be a major constraint on profitable livestock production. They are rarely associated with high mortality and easily identifiable clinical signs and their effects are usually characterized by lower outputs of animal

products, by products, manure and traction; all contributing to production and productivity losses. Conclusion Various gastrointestinal parasites have been found in cattle in the study area. Hence, the high prevalence rate of helminthiases in livestock needs to be checked periodically. Regular control measure should be practiced and farmers educated in proper use of anthelminthes. Epidemiological facts suggest that high standard of sanitation in modern animal husbandry will prevent exposure of livestock to graze in deteriorated and environmentally polluted range lands will be effective in controlling disease. REFERENCES

Adejinmi JO, Harrison JS (1996) Parasitic Nematodes of

domestic ruminants in Nigeria. Epidemiology. Trop Vet., 14: 3-15.

Agyei AD (1997). Seasonal changes in the level of infective strongylate nematode larvae on pasture in the coastal savanna of Ghana. Veterinary Parasitology 70: 175–182.

Agyemang K, Dwinger RH, Little DA, Rowlands GJ (1997). Village N’Dama cattle production in West

Africa: Six years of research in the Gambia. ILRI

(International Livestock Research Institute), Nairobi, Kenya. 131 pp

Akerejola OO, Schillborn Van Veen TW, Njoku CO, (1999). Ovine and Caprine diseases in Nigeria a review of economic losses. Bull. Anim. Hlth Prod. Afr. 27: 65-70.

Akpoghomeh O (2001). Street map of Port Harcourt and its environs. Kraft books Ibadan, pp. 214-312.

Anderson RC (2000). Nematode parasites of vertebrates: their development and transmission. Oxford, UK: Oxford

Anene BM, Onyekwodiri EO, Chime AB, Anika SM (1994a). Gastrointestinal parasites in sheep and goats of south-eastern Nigeria. Small Ruminant Research 13:187–192.

Anene BM, Onyekwodiri EO, Chime AB, Anika SM (1994b). A survey of gastrointestinal parasites in cattle of southeastern Nigeria. Preventive. Vet. Med. 20: 297–306.

Anene BM, Onyekwodiri EO, Chime AB, Anika SM (1994). Small Ruminant Research, 13: 187-192.

Anonymous (1991). Report of the FAO Expert Consultation on the Helminth Infections of Livestock in Developing Countries. AGA-815 Rome, 23–27 September 1991 Food and Agriculture Organisation of the United Nations, Rome.

Armour J (1980). The epidemiology of helminth disease in farm animals. Vet. Parasitol., 6: 7-46.

Asanji MF (1988). Journal of Helminthology, 62: 243-249. Ashton-Jones E (1998). Human ecology of the Niger

Delta. An Environmental Right Action (ERA) publication, Benin City. Pp10-24

Barger IA (1995)The statistical distrubution of Trichostrongylid nematodes in grazing lambs. Int J Parasitol.;15:645–649. doi: 10.1016/0020-7519(95)90010-4.

Blood DC, Radostits OM, Henderson JA, Arundel JH,

Gay CC (1990). Veterinary Medicine. 7th

edn., The English Language Book Society and Bailliere Tindall. Chambers, P.G. (1990) Zimbabwe Veterinary Journal, 21: 44-45.

Cheesbrough, M. (2005). District laboratory Practice in tropical Countries, Part 1 (2

nded). Cambridge

University Press. Pp 194-202. Cheruiyot, H.K. (1980) Bulletin of Animal Health and

Production in Africa, 28: 139-143 Chiejina, S. N., (1987), Parasitic gastroenteritis in cattle

and small ruminants: Pathogenesis, diagnosis and treatment, Zariya. Vet,2 (2): 45-64.

Chiejina, S.N., (1995). The current status and priorities of research on the epidemiology and control helminth infections of ruminants in West Africa. 6th symposium on Tropical Animal Health and Production. Helminth diseases of ruminants: diagnosis, epidemiology and control.

Colley DG, LoVerde PT, Savioli L (2001). Medical

Elele et al 015

helminthology in the 21st century. Science 293:1437-

1438. Connor RJ, Munyuku AP, Mackyao E, Halliwell RW

(1990). Tropical Animal Health and Production, 22: 1-6. Coop RL, Kyriazakis I (1999). Nutrition-parasite

interaction. Vet Parasitol.; 84: 187–204. doi: 10.1016/S0304-4017(99)00070-9.

Dwinger RH, Agyemang K, Kaufmann AS, Grieve AS, Bah ML (1994). Effects of trypanosome and helminth infections on health and production parameters of village N’Dama cattle in the Gambia. Veterinary Parasitology 54:353–365.

Eysker M, Ogunsusi RA (1980). Observation on epidemiological and clinical aspects of gastro-intestinal helminthiasis of sheep in Northern Nigeria during rainy season. Res. Vet. Sci. 28: 58-62.

Fabiyi JP (1973). Seasonal fluctuations of nematode infestations in goats in the savanna belt of Nigeria Bull. Epizootic Dis, Afr., 21: 227-286

Fakae BB (1990). The epidemiology of helminthiasis in small ruminants under the traditional husbandry system in eastern Nigeria. Vet. Res. Commun., 14(5): 381-391.

Fakae BB, Chiejina SN (1993). The prevalence of concurrent trypanosome and gastrointestinal nematode infections in West African dwarf sheep and goats in Nsukka area of eastern Nigeria. Vet. Parasitol., 49: 313-318.

Familton AS, McAnulty RW (1995). The epidemiology of gastrointestinal parasites

Familton AS, McAnulty RW (1997). Life cycles and development of nematode parasites of ruminants. In: Sustainable control of internal parasites in ruminants. Ed. G.K. Barrell. Animal Industries Workshop, Chapter 6: 67-80.

Faye D, Leak S, Nouala S, Fall A, Losson B, Geerts S (2003). Effects of gastrointestinal helminth infections and plane of nutrition on the health and productivity of F1 (West African Dwarf × Sahelian) goat crosses in The Gambia. Small Ruminant Res. 2003;50:153–161. doi: 10.1016/S0921-4488(03)00108-1.

Fikru R, Teshale S, Reta D, Yosef K (2006). Epidemiology of gastrointestinal parasites of ruminants in western Oromia, Ethiopia. Int.J. Applied. Res. Vet. Med., 4: 51-57.

Food and Agricultural Organisation (FAO), (2000) Distribution and impact of helminth diseases of livestock in developing countries. FAO corporate document repository Agriculture and Consumer protection

Food and Agricultural Organisation (FAO), (2001) Sustainable approaches for managing haemonchosis in sheep and goats. FAO Animal Production and Health Paper. p. 90.

Frittsche T, Kaufmann J, Pfister K (1993). Parasite spectrum and seasonal epidemiology of gastrointestinal nematodes of small ruminants in the Gambia. Vet.

016 Int. Res. Med. Sci.

Parasitol. 49: 2-4. Gonçalves VSP (1995). Livestock production in Guinea-

Bissau: Development potentials and constraints. PhD thesis, University of Reading. p. 226.

Gonzalez R, Gonzalez AC (2004). Alternatives for the control of gastrointestinal nematodes in sheep. Conf. EEPF Matanzas, Cuba.

Hansen J, Perry B (1994). The Epidemiology, Diagnosis and Control of Helminth Parasites of Ruminants. International Livestock Centre for Africa, Addis Ababa. International Livestock Centre for Africa (1979) Small Ruminant Production in the Humid Tropics ILCA Systems Study 3. ILCA, Addis Ababa, pp. 40-76.

Hayat CS, Hussain SM, Iqbal Z, Hayat B, Akhtar M (1996). Effect of parasitic nematodes on haematology and productivity of sheep. Pakistan. Vet. J., 16: 81-83.

Holmes PH (1995). Pathogenesis of trichostrongylosis. Vet. Parasitol., 18: 89-101.

Hussain Q (1985). Studies on the Incidence of Gastrointestinal Parasites and Efficacy of Bismith-II against Nematodes in Buffalo Calves. MSc Thesis. University of Agriculture, Faisalabad.

Iqbal Z, Akhtar M, Khan MN, Riaz M. (1993). Prevalence and economic significance of haemonchosis in sheep and goat slaughtered at Faisalabad abattoirs. Pakistan. J. Agric. Sci., 30: 51-53.

Jacquiet PJ, Gabaret ML, Dia, Chelkh D (1998). Host range and the maintenance of Haemonchus spp. In arid climate. Int. J. Paras 28:253-261

Jacquiet PJ, Gabaret ML, Dia, Chelkh D, Thiam E (1996). Adaptation to arid environment: Haemonchus longistipes in dromedaries of Sahara-sahelien areas of Mauritania. Vet. Paras., 66:193-204.

Javed, MS, Iqbal Z, Hayat B (1992). Prevalence and economics of haemonchosis in sheep and goats. Pakistan. Vet. J., 12: 36-38.

Jithendran KP, Rao JR (1996). Parasitic zoonoses: Role of migratory sheep and goats in Himachal Pradesh. Hima Paryavaran. 8:6-8.

Junaidu AU, Adamu SG (1997): Survey of Gastrointestinal helminth parasites of dogs of public health importance in Sokoto Metropolis. A paper presented at the 22nd Annlual Conference of the Nigerian society for Animal Production 23 – 27th March, 1997 Abubakir Tafawa Balewa University Press.

Kassuku AA (1985). Tanzanian Veterinary Bulletin, 7: 1-3.

Kaufmann J and Pfister K. (1990). The seasonal epidemiology of gastrointestinal nematodes in N'Dama Cattle in the Gambia Veterinary Parasitology, 37 (1990) 45-54.

Kaufmann J, Dwinger RH, Hallebeek A, van Dijk B, Pfister K (1992). The interaction of Trypanosoma congolense and Haemonchus contortus infection in trypanotolerant N’Dama cattle. Veterinary

Parasitology 43: 157–170. Kaufmann J (1996). Parasitic infections of domestic

animals: a diagnostic manual. Birkhauser, Berlin, p. 423.

Kennedy MW, Harnett W (2001). Parasitic nematodes. CAB International.

Keyyu JD, Monrad J, Kyvsgaard, Kassuky AA (2005). Epidemiology of Fasciola gigantica and Amphistomes in cattle on traditional, small-scale dairy and large dairy farms in south highlands of Tanzanian Trop Animal Health production. 37. 303-314.

Kloosterman A, Verhoeff J, Ploeger HW, Lam TJGM, (1993). Antibodies against nematodes in serum, mil and bulk milk samples as possible estimators of infection in dairy cows. Vet. Parasitol., 47: 267-278

Larry SR, John J (2006). Foundations of parasitology (7th

ed) McGraw Hill Singapore Leathwick DM, McEwan J, Bisset S (1998). Selection for

highly productive sheep which have reduced requirement for anthelmintic treatment. Meat NZ Report on Project 94PR 120/1.1: 50pp.

Littlewood DTJ, Bray RA (2001). Interrelationship of the Platyhelminthes, vol. 60. Taylor & Francis, London, United Kingdom.

Lughano K, Dominic K (1996). Diseases of Small Ruminants: Common diseases of sheep and goats in Sub-Saharan Africa. PP 2-14.

Malczewski A, Jolley WR, Woodard LF (1996). Prevalence and epidemiology of trichostrongylids in Wyoming cattle with consideration of the inhibited development of Ostertagia ostertagi. Veterinary Parasitology, 64: 285-297.

Mattioli RC, Zinsstag J, Pfister K (1994). Frequency of trypanosomosis and gastrointestinal parasites in draught donkeys in The Gambia in relation to animal husbandry. Tropical Animal Health and Production 26: 102–108.

Merial (2001). The impact of parasites and drench resistance on Newzealand sheep production.Merial NZ Ltd. p. 6.

Michael L, (2002). Biological control in a global perspective – A review with emphasis on Duddingtonia flagrans. In Biological control of nematode parasites of small ruminants in Asia, FAO Animal Production and Health Paper, pp. 19-37.

Mmom PC (2003). Willingness of city dwellers to relocate their residence. Implication for city decongestion. Rivers state journal of social Sciences. 45: 6-17

Muesterman S, Tome NR (1989) Tropical Animal Health and Production, 21: 247- 255.

Nahed, Q. Lopez, G. Mendoza A. A. and Trigo, (2003). Epidemiology of parasitosis in the Trozil sheep production system. Small Rum. Res., 49: 199-206.

Nawathe DR, Sohael AS, Umo I (1985). Health management of a dairy herd on the Jos Plateau (Nigeria). Bull. Anim. Hlth. Prod. Africa, 33: 199-205.

Ndamukong KJN, Ngone MM (1996). Development and

survival of Haemonchus contortus and Trichostrongylus spp. on pasture in Cameroon. Tropical Animal Health and Production, 28: 193–198.

Ndao M, Belot J, Zinsstag J, Pfister K (1995). Epidemiology of gastrointestinal Helminthiasis in small ruminants in the tree-cropping pasture zone in Senegal. Netherlands, 6 October, Vet. Res., 26(2): 132-139., pp. 8-14..

Nfi N, Ndamukong K (1997). Health problems in small ruminant farms of North-West Province, Cameroon. World Animal Review, 88: 56–58.

Njombe AP (1993). Small Ruminant Production in Tanzania. Proceedings of the Tanzania Society of Animal Production, 20: 130-145.

Nwosu CO, Madu PP, Richards WS (2007). Prevalence and seasonal changes in the population of gastrointestinal nematodes of small ruminants in the semi-arid zone of north-eastern Nigeria. Vet Parasitol, 15; 144(1/2): 118-124

Ogba CO (2002). Problem of Urban Slum: A case study of Port Harcourt City. Unpublished M.sc Thesis. Enugu state university of technology. Enugu. p.102

Onyali IO, Onwuliri COE (1989). Gastrointestinal helminths of camels in Nigeria. Tropical Animal Health and Production 21:245–246.

O'Sullivan BM, Donald AD.(1990). A field study of nematode parasite populations in the lactating ewe. Parasitol.;61: 301–315.

Pal RA, Qayyum M (1993). Prevalence of gastrointestinal nematodes of sheep and goats in upper Punjab, Pakistan. Pakistan Veterinary Journal, 13: 138-141.

Pedreira J, Silva AP, Andrade RS, Suarez JL, Arias M, Lomba C, Diaz P, Lopez C, Banos PD, Morrondo P (2006). Prevalences of gastrointestinal parasites in sheep and parasite control practices in North- West Spain. Preventive Veterinary Medicine, 75: 56-62.

Rahman MF and Ahmed Z (1991). Final report of “Pilot project for the control of parasitic disease of animals in Bangladesh”, Bangladesh Livestock Research Institute, Dhaka.

Rahman WA, Collins GH (1992). Veterinary Parasitology, 43: 85-91.

Rattray, PV (2003). Helminth Parasites in the New Zealand Meat & Wool Pastoral Industries: A Review of Current Issues.

Elele et al 017 Sharkhuu T (2001). Helminths of goats in Mongolia. Vet

Parasitol, sheep - back to basics. Proceedings of the 25

th Seminar, Sheep & Beef Cattle. 101(2): 161-169.

Sissay MM, Uggla A, Waller PJ, (2007). Epidemiology andseasonal dynamics of gastrointestinal nematode infections ofsheep in a semi-arid region of eastern Ethiopia. Vet Parasitol,143(3-4): 311-321.

Society of the NZ Veterinary Association: 67-74. Soulsby EJL (1986). Helminths, Arthropods and Protozoa

of Domestic Animals. 7th

edn., The English Language Book Society and Bailliere Tindall, London

Tembley S, Diarra PA, Waigalo Y, Koumaré A, Vassiliades G (1992). Preliminary observations on helminth parasite populations of the dromedary in northern Mali. Veterinary Parasitology 44:339–342.

Tibor K (1999). Veterinary Helminthology, Butterworth, Oxford., UK.

Torres-Acosta JFJ, Dzul-Canche U, Caballero AJA, Vivas RIR (2003). Prevalence of benzimidazole resistant nematodes in sheep flocks in Yucatan, Mexico. Vet. Parasitol., 114: 33–42.

Vlassoff A, Leathwick DM, Heath AGC (2001). The epidemiology of nematode infections of sheep. NZ Veterinary. J. 49: 213-221.

Waller PJ (2006). Sustainable nematode parasite control strategies for ruminant livestock by grazing management and biological control. Animal Feed Science and Technology. 126: 277-289.

Wamae LW, Ihiga MAK (1991). Bulletin of Animal Health and Production in Africa, 39: 257-269.

Wikipedia, (2009) Helminthiasis. www.wikipedia.org. Wymann MN, Bonfoh B, Traore K, Tembely S, Zinsstag J

(2007). Species diversity and acquisition of gastrointestinal parasites in calves aged 0-13 months in periurban livestock production in Mali. Vet Parasitol, 19;143(1): 67-73.

Zinsstag (1997). Gastrointestinal Nemtodes of livestock in the Gambia: Epidemiology and control. (s)

Zinsstag J, Kaufmann H, Fritsche T, Ndao M (1991). ITC/University of Berne Helminthiasis Project. Fourth Progress Report. 1st May 1991.