ПАРАЗИТОЛОГИЯ, 2020, том 54, № 6, с. 514-521.

Удк 576.895.2 / 576.32/.36

PREVALENCE OF PARAMPHISTOMUM SPECIES

IN CATTLE SLAUGHTERED AT GWAGWALADA ABATTOIR,

ABUJA, NIGERIA

^aDepartment of Parasitology and Entomology, Faculty of Veterinary Medicine,

University of Abuja, P.M.B 117, Abuja

^bFormerly of School of Sciences, Engineering and Technology Abertay University,

DD1 1HG, Dundee, United Kingdom

* e-mail: balarabemohammed161@yahoo.co.uk

Received 30.03.2020

Received in revised form 15.07.2020

Accepted 09.10.2020

A cross sectional study was carried out in September 2017 April 2018, in Gwagwalada abattoir to

determine prevalence of Paramphistomum spp. in slaughtered cattle. Six hundred and forty eight (648)

cattle were subjected to standard meat inspection procedures for the presence of Paramphistomum spp.

Parasites were determined during initial examination and then determination was clarified microscopically

to appreciate the morphology of adult Paramphistomum spp. The overall prevalence of Paramphistomum

spp. in the study was (59.7 %). The prevalence was higher in male than in female cattle with prevalence of

51.4 % and 48.6 % respectively. A statistically significant difference (P<0.05) in prevalence of

Paramphistomum spp. due to season of sampling, and to cattle species, sex, and age was observed.

The highest infection rate of cattle with Paramphistomum spp. was observed in October. The revealed

high infection rate of cattle with Paramphistomum spp. testifies to an intensive transmission of these

parasites in the region, potentially resulting in immense economical losses in the area examined.

Therefore, it is recommended to cattle breeders to improve feeds provision in order to obtain good

body condition providing sufficient level of resistance against Paramphistomum infections. Integrated

control approach using selected anthelmintic therapy and snail control to reduce the magnitude of the

problem is also recommended.

Keywords: Paramphistomum spp., prevalence, cattle, Gwagwalada, Nigeria

DOI: 10.31857/S123456780606005X

In Nigeria, 13.9 million cattle population provides not only the main source of animal

proteins; by-products, such as bones and skins also play a vital role in economic well-being

514

of the human populace (Sani, 2009; Lawal-Adebowale, 2012). A considerable socio-economic

importance is therefore attached to ownership of these animals that in some cases may be the

only realizable wealth of a rural household (Omeke, 1988; Bettencourt et al., 2015). Their

production is however constrained by a variety of gastrointestinal helminthes, which are

characterized by decrease in milk production, reduced product quality, mortality and other

secondary infections (Saha et al., 2013). Helminthes including trematodes are known to be

potential health hazard to cattle population and are therefore major impediment to efficient

livestock production, characteristically affecting their growth and productive performances

(Bisset, 1994; Charlier et al., 2015).

Among the plethora of Trematodes, Paramphistomum infection is established to have a

devastating effect to cattle production globally, but the highest prevalence has been reported in

tropical and subtropical regions, particularly in Africa including Nigeria (Khedri et al., 2015;

Elelu et al., 2016). The epidemiology of Paramphistomum infection in cattle is determined

by several factors governed by parasite-host-environment interactions (Martinez-Ibeas et al.,

2016). Adults of Paramphistomum are found in the rumen and reticulum whilst immature

parasites are found in the duodenum. Adult Paramphistomum flukes parasitize mainly in the

fore stomachs of cattle causing irregular rumination (ruminitis), lower nutrition conversion,

loss of body condition, decrease in milk production, and reduction of fertility rate (Mogdy

et al., 2009; Ayalew et al., 2016). The immature flukes occur in the upper part of the small

intestine (duodenum and ileum) causing hemorrhage, which leads to anaemia, weight loss,

decreased production; death of animals may also occur (Maitra et al., 2014).

The taxonomy of paramphistomes has been extensively studied by light and electron

microcopy, yet there are still areas where consensus is lacking. The major species that cause

the disease include Paramphistomum cervi (Zeder, 1790), P. cotylophorum (Fischoeder,

1901), P. gotoi Fukui, 1922, P. gracile Fischoeder, 1901, P. hiberniae Willmott, 1950,

P. ichikawai Fukui, 1922, and P. epicitum Fischaedar, 1904. The ones that are predominantly

found in Africa are P. cervi and P. microbothrium Fischoeder, 1901 (Smyth, 1996). Although

Paramphistomum infection outbreaks in different communities have been extensively studied

in different states in Nigeria (Biu, Oluwafunmilayo, 2004; Bunza et al., 2008; Njoku et

al., 2009; Adedipe et al., 2014; Afolabi et al., 2017; Shola et al., 2020), there is paucity

of information on the prevalence of this parasite in the Federal Capital Territory. This

is essential for the design of an effective control strategy. The study was conducted to

determine prevalence of Paramphistomum species in cattle slaughtered at Gwagwalada

abattoir, Abuja, Nigeria.

Materials and methods

The study was carried out in Gwagwalada Area Council, one of the six councils of the Federal

Capital Territory (FCT), Abuja - Nigeria. It is located geographically in the central part of Nigeria

515

between latitude 8°25'-9°9' N and longitude 6°29'-7°45' E. It has a Guinea Savannah type of vegetation,

with rainy season stretching from April to October and dry season from November to March. The climate

of the study area is tropical: non-arid climate with only two seasons throughout the year: wet and dry.

The mean temperature in the study area ranges between 30-37 °C yearly with the highest temperature

in March and the mean total annual rainfall of approximately 1650 mm per annum (NPC, 2006).

A cross sectional study was carried out on slaughtered animals in Gwagwalada abattoir for 3 days

in a week during early dry season (September-December 2017) and 2 days in a week during the late

dry season (January-April, 2018). The animals were randomly selected for sampling. Six hundred and

forty-eight (n = 648) cattle slaughtered in Gwagwalada Area Council abattoir, Abuja, Nigeria were

examined for the presence of Paramphistomum species. Adult worms were collected from the rumen

and reticulum of the animal sampled using a standard meat inspection procedure that involves both

primary and secondary examination.

Ante mortem inspection was carried out in animals before slaughter, to assess them generally.

During the ante mortem examination, detail records about the species, sex, age, and breeding status

of the animals were recorded. Ageing of the cattle was based on rostral dentition as described by

Lasisi et al. (2002). Cattle aged (˂ 3 years old) were classified as young while (> 3 years old) were

considered as adults. Sexual differentiation was based on the appearance of external genitals while

breed identification was based on morphology as described by Yunusa et al. (2013).

Rumen of slaughtered animals selected to be sampled were inspected for the presence of rumen

flukes. The collected flukes were transported to the laboratory in plastic containers with 10 % formalin.

The flukes were washed several times in running tap water to remove debris and ruminal content.

The flukes were later prepared for identification under stereomicroscope. Furthermore, collected flukes

were preserved for further identification.

Rumen and reticula were systematically inspected for the presence or absence of adult

Paramphistomum to estimate fluke burden using standard meat inspection procedures which include

primary and secondary examination. The primary examination includes visualization and palpation.

During the secondary examination further incision of the rumen and reticulum was made to check

presence or absence of Paramphistomum spp. as described by Urquhart et al. (1996).

Rumen flukes were preliminarily identified under microscope using low power magnification

and then slides were prepared for detailed morphological studies and identification. Flukes collected

in Petri dishes were observed using stereoscope to appreciate the morphology. Final identification

of Paramphistomum was done based on morphological features, such as shape, posterior sucker

(acetabulum), anterior sucker, terminal genitalium and tegumental papillae following the standard

guidelines given by Urquhart et al. (1996).

Data Analysis

Data were collected during the study and fed into a computer using Microsoft excel

spreadsheet and analyzed with Statistical software (SPSS - 20.0). Descriptive statistics

was employed and expressed in terms of frequency and simple percentage. Chi square (χ²),

ANOVA (F-Test), and t-test statistics were used to test the relationship between variables.

516

Results

The overall prevalence of Paramphistomum spp. in cattle slaughtered at Gwagwalada

abattoir was 59.1 %. Higher prevalence of Paramphistomum spp. was recorded in adult

cattle (62.0 %) than in young ones (42.1 %). There was statistically significant difference

(P < 0.05) in the prevalence of Paramphistomum between two age groups and female cattle

showed a higher prevalence (61.0 %) than male (57.4 %). Similarly, there was no statistically

significant difference between the breeds examined (P > 0.05) (tabl. 1). Identification result

showed statistically significant variation in prevalence of Paramphistomum spp. between

both sexes (P < 0.05) (tabl. 1).

Table 1. Prevalence of Paramphistomum spp. in cattle slaughtered in Gwagwalada abattoir

Sample parameter

No. examined (%)

No. infected (%)

P- Value

Age

Young

95 (14.7)

40 (42.1)

4.231*

0.001^ª

Adult

553 (85.3)

343 (62.0)

Total

648

383 (59.1)

Sex

Male

343 (52.9)

197 (57.4)

6.114*

0.000^ª

Female

305 (47.1)

186 (61.0)

Total

648

383 (59.1)

Breed

374 (57.7)

216 (57.8)

15.250**

0.762

152 (23.5)

95 (62.5)

70 (10.8)

41 (58.6)

52 (8.0)

31 (59.6)

Total

648

383 (59.1)

*not significant at α = 0.05, ªsignificant at α = 0.05, * t - test, **chi square (χ²).

Key: WF - White Fulani, ND - Ndama, SG - Sokoto Gudali, K - Keteku.

The infection rate is higher during early dry season (October-December), reaching its

peak in the rainy season (tabl. 2).

Table 2. Monthly prevalence of Paramphistomum spp. in cattle slaughtered

at Gwagwalada Area Council abattoir, Abuja

Months

Cattle examined

Infected cattle

September

11.3

79.5

October

14.2

83.7

November

8.8

35.7

December

8.8

45.7

January

11.6

36.0

February

13.3

43.0

March

102

15.7

64.7

April

12.3

76.3

Total

648

36.0

383

59.1

517

Discussion

In this study, the overall prevalence of Paramphistomum spp. was 59.1 %; similar high

prevalence (56 %) was recorded in Sokoto, Northern Nigeria (Bunza et al., 2008), 51.82

% in Ethiopia (Ayalew et al., 2016), and 53.1 % in Bangladesh (Paul et al., 2011). Lower

prevalence rate was however, recorded in Turkey (8.95 %), Spain (18.8 %), and France (20

%) by Ozdal et al. (2010), González-Warleta et al. (2013) and Szmidt-Adjidé et al. (2000),

respectively. The great variability shown in both cases is probably due to ecological and

climatic differences between different locations throughout the continents of Africa, Asia

and Europe. The other most important factors that influence the occurrence of trematodes

in an area include availability of the suitable snail habitat (Dodangeh et al., 2019).

Findings of this study are in accordance with the reports of Davila et al. (2010), Raza

et al. (2010) and Al-Shaibani et al. (2008) who had also revealed higher prevalence of

helminthes in female. In this study, variation in occurrence of such helminthes in males

and females might be due to variation in sample size (Bachal et al., 2002), stress, genetic

resistance of host and insufficient/imbalanced feed against higher needs (Raza et al., 2010).

Higher prevalence among females may be explained by loss of immunity during pregnancy,

birth and lactation (Alade, Bwala, 2015).

The study did not identify any statistically significant difference in the rate of infection

among the breeds (P > 0.05) examined.

Monthly prevalence showed that infection rate was higher in October and gradually

fell down in November and increased in March. Similar work by Gul-E- Nayab et al.

(2017) showed that prevalence of Paramphistomum spp. was highest in cattle in March

and the lowest in November. Similar work by Chaudhri (2000) showed that there was

significant decrease of the rate during raining season. It has been described that the bionomic

requirements for breeding of Planorbis snails and development of intramolluscan stages of

flukes often reach the optimum threshold during the wet months (Radostits et al., 2000).

However, during dry periods, breeding of snails (intermediate hosts) and development of

larval flukes slow down or stop completely and snails undergo the aestivation state (Boray,

1994; Urquhart et al., 1996).

Although a decrease in prevalence was observed along with the advancement of dry

season, relatively high prevalence rates were recorded, this may be due to infections acquired

during previous peak of the snail activity season. The present study agrees with the finding

of Akanda et al. (2014), who reported that parasitic infestation was highest in rainy season

followed by summer and winter season.

518

Conclusion

In this study, Paramphistomum spp. was found to be prevalent in cattle. This will be a

hindrance to the livestock production by causing remarkable direct or indirect losses in the

study area. Moreover, the study area is suitable for the survival of the molluscan hosts that

worsened the situation for the future. Therefore, taking into account the aforementioned

conclusion, integrated control approach using selected anthelmintic therapy and snail control

should be implemented to reduce the magnitude of the problem. In addition, awareness of

the cattle breeders about the disease should be raised to enable them actively participate

in control programs.

Acknowledgements

The authors wish to acknowledge the management and staff of the Gwagwalada Area

Council abattoir and village for their kind permission and coorperation to use their facilities

for the research.

References

Adedipe O.D., Uwalaka E.C., Akinseye V.O., Adediran O.A., Cadmus S.I.B. 2014. Gastrointestinal helminths in

slaughtered cattle in Ibadan, South-Western Nigeria. Journal of Veterinary Medicine 2014: 923561.

Afolabi O.J., Simon-Oke I.A., Ademiloye O.A. 2017. Gastro-intestinal parasites of bovine in Akure abattoirs,

Nigeria. Journal of Entomology and Zoology studies 5: 1381-1384.

Akanda M.R., Hasan M.M.I., Belal S.A., Roy A.C., Ahmad S.U., Das R., Masud A.A. 2014. A survey on prevalence

of gastrointestinal parasitic infection in cattle of Sylhet division in Bangladesh. American Journal of

Phytomedicine and Therapeutics 2: 855-860.

Alade N.K., Bwala M.D. 2015. Gastrointestinal-parasites infestation in Yankasa sheep in a semi-arid environment.

Livestock Research for Rural Development 27: 106.

Al-Shaibani I.R.M., Phulan M.S., Arijo A., Qureshi T.A. 2008. Epidemiology of ovine gastrointestinal nematodes

in Hyderabad distinct, Pakistan. Pakistan Veterinary Journal 28: 125-130.

Ayalew G., Tilahun A., Aylate A., Teshale A., Getachew A. 2016. A study on prevalence of paramphistomum in

cattle slaughtered in Gondar Elfora Abattoir, Ethiopia. Journal of Veterinary Medicine and Animal Health

8: 107-111.

Bachal B., Sharif P., Rahamatullah R., Aijaz H.S. 2002. Prevalence of gastro-intestinal helminths in Buffalo calves.

Journal of Biological Sciences 2: 43-45.

Bettencourt E.M.V., Tilman M., Narciso V., Carvalho M.L.D.S., Henriques P.D.D.S. 2015. The livestock roles in

the wellbeing of rural communities of Timor-Leste. Revista de Economia e Sociologia Rural 53: 63-80.

Bisset S.A. 1994. Helminth parasites of economic importance in cattle in New Zealand. New Zealand Journal of

Zoology 21: 9-22.

Biu A.A., Oluwafunmilayo A. 2004. Identification of some paramphistomes infecting sheep in Maiduguri, Nigeria.

Pakistan Veterinary Journal 24: 187-189.

Boray J.C. 1994. Disease of Domestic Animals Caused by Flukes. Food and Agricultural Organisation of the

Untied Nations, Rome, 49 p.

519

Bunza M.D.A., Ahmad A., Fana S.A. 2008. Prevalence and of paramphistomiasis in ruminants slaughtered at

Sokoto Central Abattoir, Sokoto. Nigerian Journal of Basic and Applied Sciences 16: 287-292.

Charlier J., De Waele V., Ducheyne E., van der Voort M., Velde F.V., Claerebout E. 2015. Decision making on

helminths in cattle: diagnostics, economics and human behaviour. Irish Veterinary Journal 69: 14.

Chaudhri S.S. 2000. Studies on the incidence and epidemiology of paramphistomiasis in sheep. Information

Bulletin 23: 269-274

Davila G., Irsik M., Greiner E.C. 2010. Toxocara vitulorum in beef calves in North Central Florida. Veterinary

Parasitology 168: 261-263.

Dodangeh S., Daryani A., Sharif M., Gholami S., Kialashaki E., Moosazadeh M., Sarvi S. 2019. Freshwater snails

as the intermediate host of trematodes in Iran: a systematic review. Epidemiology and Health 41: e2019001.

Elelu N., Ambali A., Coles G.C., Eisler M.C. 2016. Cross-sectional study of Fasciola gigantica and other trematode

infections of cattle in Edu Local Government Area, Kwara State, north-central Nigeria. Parasites & Vectors

9: 470.

Gul-E-Nayab G., Muhammad I., Niaz S., Ali Z., Kattak S.A. 2017. Prevalence of gastrointestinal parasite,

Paramphistomum in domestic animals (Cows and Buffaloes) of district Swat and Charsadda, KP, Pakistan.

Journal of Entomology and Zoology Studies 5: 907-911.

González-Warleta M., Lladosa S., Castro-Hermida J.A., Martínez-Ibeas A.M., Conesa D., Muñoz F., Mezo M. 2013.

Bovine paramphistomosis in Galicia (Spain): prevalence, intensity, aetiology and geospatial distribution of

the infection. Veterinary Parasitology 191: 252-263.

Khedri J., Radfar M.H., Borji H., Mirzaei M. 2015. Prevalence and intensity of Paramphistomum spp. in cattle

from South-Eastern Iran. Iranian Journal of Parasitology 10: 268-272.

Lasisi O.T, Ojo N.A., Otesile E.B. 2002. Estimation of age of cattle in Nigeria using rostral dentition. Tropical

Veterinarian 20: 204-208.

Lawal-Adebowale O.A. 2012. Dynamics of ruminant livestock management in the context of the Nigerian agricultural

system. In: Jawed K (ed.). Livestock Production. InTech, Rijeka, Croatia, 61-80.

Maitra A., Yadav C.L., Sanjukta R.K. 2014. Seasonal prevalence of paramphistomosis in domestic ruminants in

different agro-climatic zones of Uttarakhand, India. Asian Pacific Journal of Tropical Disease 4: S748-S753.

Martinez-Ibeas A.M., Munita M.P., Lawlor K., Sekiya M., Mulcahy G., Sayers R. 2016. Rumen fluke in Irish

sheep: prevalence, risk factors and molecular identification of two paramphistome species. BMC Veterinary

Research 12: 143.

Mogdy H., Al-Gaabary T., Salama A., Osman A., Amera, G. 2009. Studies on paramphistomosis on ruminants in

Kafrelsheikh. Journal of Veterinary Medicine 10: 116-136.

National Population Commission. 2006 Population Census of the Federal Republic of Nigeria, Abuja. Analytical

Report at the National level. April 2009.

Njoku-Tony R.F., Nwoko B.E.B. 2009. Prevalence of paramphistomiasis among sheep slaughtered in some selected

abattoir in Imo State, Nigeria. Science World Journal 4: 12-15.

Omeke B.C.O. 1988. Improving goat productivity in the humid zone of the tropics. Bulletin of Animal Health

and Production in Africa 36: 126-130.

Ozdal N., Gul A., Deger S. 2010. Prevalence of Paramphistomum infection in cattle and sheep in Van Province,

Turkey. Helminthologia 47: 20-24.

Paul A.K., Talukder M., Begum K., Rahman M.A. 2011. Epidemiological investigation of Paramphistomiasis in cattle

at selected areas of Sirajgonj district of Bangladesh. Journal. Bangladesh Agricultural University 9: 229-232.

520

Radostits O.M., Gay C.C., Blood D.C., Hindicliff I.F.F. (Eds) 2000. Veterinary Medicine (9th edition). W. B.

Saunkr company, London, 1877 p.

Raza M.A., Murtaza S., Bachaya N.A., Hussain A. 2009. Prevalence of Paramphistomum cervi in ruminants

slaughtered in District Muzaffar Garh. Pakistan Veterinary Journal 29: 214-215.

Saha S.S., Bhowmik D.R., Chowdhury M.M.R. 2013. Prevalence of gastrointestinal helminthes in buffaloes in

Barisal district of Bangladesh. Bangladesh Journal of Veterinary Medicine 11: 131-135.

Sani A.B. 2009. Raw material production for export in Northern Nigeria: the experience of the people in the

livestock and allied industries under British rule c. 1900-1960. African Economic History 37: 103-127.

Shola D.O.F., Ganiyu I.A., Rabiu M., Hussain K., Sanda I.M., Baba A.Y., Balogun R.B. 2020. Helminth infections

of great concern among cattle in Nigeria: Insight to its prevalence, species diversity, patterns of infections

and risk factors. Veterinary World 13: 338-344.

Smyth J.D. 1996. Animal Parasitology (3rd edition). Cambridge University Press, Cambridge,

549 p.

Szmidt-Adjidé V., Abrous M., Adjidé C.C., Dreyfuss G., Lecompte A., Cabaret J., Rondelaud D. 2000. Prevalence

of Paramphistomum daubneyi infection in cattle in central France. Veterinary Parasitology 87: 133-138.

Urquhart G.M., Armour J., Duncan J.L., Dunn A.M., Jennings F.W. 1996. Veterinary Parasitology. (2nd edition).

Oxford, Longman Scientific and Technical Press, United Kingdom. 785 p.

Yunusa A.J., Salako A.E., Oladejo O.A. 2013. Morphometric characterization of Nigerian indigenous sheep using

multifactorial discriminant analysis. International Journal of Biodiversity Conservation 5: 661-665.

Зараженность видами Paramphistomum

крупного рогатого скота на скотобойне в Гвагвалада

(Абуджа, Нигерия)

О. Б. Ароволо, Б. Р. Мохаммед, М. Н. Опара

Ключевые слова: Paramphistomum spp., зараженность, крупный рогатый скот,

Гвагвалада, Нигерия

РЕЗЮМЕ

В период с сентября 2017 г. по апрель 2018 г. на скотобойне Гвагвалада было проведено

обследование забитого крупного рогатого скота для определения зараженности Paramphistomum

spp. Стандартной инспекции мясопродуктов на наличие Paramphistomum spp. подвергнуто 648

особей. Найденных паразитов определяли при первичном обследовании и уточняли при микро-

скопировании. Общая зараженность крупного рогатого скота Paramphistomum spp. в период

исследования составила 59.1 %, причем зараженность самцов была выше (51. 4%), чем самок

(48.6 %). Статистически значимые различия (P < 0.05) в зараженности Paramphistomum spp.

животных обнаружены в разные сезоны, а также в зависимости от их вида, пола и возрас-

та. Наибольшее заражение крупного рогатого скота Paramphistomum spp. отмечено в октябре.

Выявленный высокий уровень заражения животных Paramphistomum spp. свидетельствует об

интенсивной трансмиссии этих паразитов в регионе, что может привести к огромным экономи-

ческим потерям. Поэтому животноводам рекомендуется улучшить обеспечение выращиваемых

животных кормами, что позволит повысить их устойчивость к заражению Paramphistomum

spp. При этом необходимо проводить комплексные мероприятия по селективной глистогонной

терапии и борьбе с улитками - промежуточными хозяевами Paramphistomum spp.

521