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  • Research Article
  • Open Access

Helminths of veterinary and zoonotic importance in Nigerian ruminants: a 46-year meta-analysis (1970–2016) of their prevalence and distribution

Infectious Diseases of Poverty20187:52

https://doi.org/10.1186/s40249-018-0438-z

  • Received: 7 July 2017
  • Accepted: 9 May 2018
  • Published:

Abstract

Background

The livestock industry plays a vital role in the economy of Nigeria. It serves as a major source of income and livelihood for majority of Nigerians who are rural settlers and contributes about 5.2% to the National Gross Domestic Product (GDP). Helminths however, cause economic losses due to reductions in milk production, weight gain, fertility and carcass quality. Zoonotic helminths of livestock origin cause health problems in humans.

Methods

Using the Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) guidelines, the prevalence and distribution of helminths of veterinary and zoonotic importance in Nigerian ruminants were determined in a meta-analysis of data published between 1970 and 2016. Data were stratified based on regions, hosts, study periods, sample sizes and study types while helminths were phylogenetically grouped into cestodes, nematodes and trematodes.

Results

Data from 44 studies reported across 19 Nigerian states revealed an overall pooled prevalence estimate (PPE) of 7.48% (95% CI: 7.38–7.57) for helminths of veterinary and zoonotic importance from a total of 320 208 ruminants. We observed a significant variation (P < 0.001) between the PPEs range of 1.90% (95% CI: 1.78–2.02) and 60.98% (95% CI: 58.37–63.55) reported across different strata. High heterogeneity (99.78, 95% CI: 7.38–7.57) was observed. Strongyloides papillosus was the most prevalent (Prev: 32.02%, 95% CI: 31.01–33.11), while, Fasciola gigantica had the widest geographical distribution.

Conclusions

Helminths of veterinary and zoonotic importance are prevalent in ruminants and well distributed across Nigeria. Our findings show that helminths of ruminants may also be possible causes of morbidity in humans and economic losses in the livestock industry in Nigeria. High heterogeneity was observed within studies and the different strata. Good agricultural practices on farms, standard veterinary meat inspection and adequate hygiene and sanitation in abattoirs, farms and livestock markets need to be implemented in Nigeria in order to reduce the economic, public health and veterinary threats due to these helminths.

Keywords

  • Cestodes
  • Geographical distribution
  • Helminths
  • Nematodes
  • Nigeria
  • Prevalence
  • Ruminants
  • Trematodes

Multilingual abstracts

Please see Additional file 1 for translations of the abstract into the five official working languages of the United Nations.

Background

Helminths of ruminants refer to a group of complex multicellular eukaryotic parasites which are infective to animals and humans in which case they are called zoonoses [1]. This group of parasites cause serious economic and public health problems in many resource-limited countries across the globe. In Nigeria for instance, these problems are influenced by inadequate veterinary and medical care as well as inadequate policies on disease control among many other factors [2].

Helminth parasites of ruminants are broadly grouped into two phyla, namely nemathelminthes which are nematodes or roundworms such as Haemonchus, Bonostomum, Oesophagostomum and Chabertia and platyhelminthes which include cestodes (e.g. Avitellina, Moniezia, Stilesia and Taenia) and trematodes such as Dicrocoelium, Eurytrema, Fasciola and Paramphistomum [3]. Transmission of these parasites may be through the ingestion of parasitic eggs and infective larvae on contaminated pasture, water, soil, human hands or tissues of infected vertebrate intermediate hosts, skin penetration, transplacental as well as arthropod and gastropod intermediate hosts [4]. Transmission is influenced by factors including poor hygiene and sanitation, indiscriminate and open defecation [5], as well as environmental factors like temperature, humidity, rainfall [6] and soil moisture [7]. Lack of strategic de-worming of livestock [8, 9], poverty and overcrowding [10] are additional factors.

The negative impacts of helminths on livestock productivity still remain a major challenge in the livestock industry globally [11] despite the projected increased dependence on agriculture in the nearest future [12]. These parasites cause serious economic losses in ruminants ranging from growth rate decrease and poor quality of skin and hides to reductions in the production of milk, meat and wool [13]. For instance, evidence revealed that lactating cows may lose 294.8 kg of milk on average per lactation due to helminth parasites [14, 15]. In Nigeria, infection prevalence rates range between 25.6 and 91.4% [1619]. Economic losses caused by the rejection of editable organs of slaughtered food animals during veterinary meat inspections were also documented [2022].

From the public health point of view, reports of zoonotic meta-cestodes; Cysticercus bovis and hydatid cyst [19, 23, 24], nematode; Oesophagostomum [2527] and trematodes; Dicrocoelium dendriticum, Eurytrema pancreaticum and Fasciola gigantica [22, 28] entering the food chain in Nigeria are of great public health concern. Human infections with these parasites may result in diarrhoea, retarded growth, intellectual and cognitive retardation [29], cystic echinococcosis and cysticercosis [30].

The livestock industry plays a vital role in the economy of Nigeria. It serves as a major source of income and livelihood for majority of Nigerians who are rural settlers and contributes about 5.2% of the National Gross Domestic Product (GDP) [31]. In addition, cattle, sheep and goats contribute over 80% of the total meat produced in Nigeria [25, 32]. Despite these benefits, helminth infections still cause serious economic losses in Nigeria as a result of reductions in milk production, weight gain, fertility and carcass quality. The aim of this study was to provide epidemiological information which will help in instituting sustainable control programmes against these parasites, thus reducing economic losses associated with these helminths and maximising the contribution of the livestock industry to Nigeria’s GDP.

Methods

Study areas

We included in the present review studies published on helminths of veterinary and zoonotic importance in ruminants from Nigeria (West Africa; 4–14 ̊N; 3–14 ̊E) which covers a surface area totalling 923 768 km2 (Fig. 1). In Nigeria, there are two seasons; the rainy season which runs from March to November in the Southern region and May to October in the Northern region, as well as the dry season which runs from December to February in the South and November to April in the North [33].
Fig. 1
Fig. 1

Distribution of eligible studies and regional prevalence of helminths in ruminants in Nigeria

Bibliographic search strategy

The study followed the Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) guidelines published by Moher et al. [34], and the three authors conducted independently the literature search. We used the PRISMA checklist (Additional file 2) as the basis for inclusion of relevant information. The outcome of interest was the infection of Nigerian ruminants with helminths species of veterinary and zoonotic importance.

A comprehensive literature search was carried out on PubMed, MEDLINE, Google Scholars, AJOL and references of studies that resulted from the search of databases between September, 2016 and March, 2017. To ensure that relevant studies were not omitted, the search was categorized into three stages as broad, narrow and specific search stages. Under the broad search, combinations like helminths of ruminants in Nigeria, prevalence or occurrence of helminths of ruminants in Nigeria were used. Search combinations employed for the narrow search included, but were not limited to, prevalence or occurrence of cestodes, nematodes or trematodes of ruminants in Nigeria. The combinations used under specific search targeted helminth species of ruminants and included, but were not limited to, prevalence or occurrence of Avitellina ± centripunctata, Taenia ± saginata/Cysticercus ± bovis, Echinococcus/hydatid ± cyst, Moniezia ± expansa ± benedeni, Bunostomum ± phlebotomum, Toxocara ± vitulorum, Haemonchus ± contortus ± placei, Fasciola ± gigantica ± hepatica and Dicrocoelium ± dendriticum in cattle, sheep and goats. Specific searches were also narrowed to regions and states of the Nigerian federation.

Inclusion criteria

Studies identified by any of the three search stages were then screened before selection. A study was considered eligible only if: (i) it was carried out in Nigeria, (ii) it was published in English, (iii) it was published between 1970 and 2016, (iv) it was a cross sectional study, (v) the study specified the location in Nigeria where it was conducted, (vi) the sample size and number of positive cases were clearly stated, (vii) the sample size was ≥50, (viii) it reported helminths species of veterinary and zoonotic importance, (ix) the method of diagnosis was stated, (x) parasites were identified at least to the genus level.

In this study, helminths were considered of veterinary importance if they are naturally infective to animals only while those that are naturally infective to man and animals were considered of zoonotic importance. In order to provide data that would guide veterinarians and public health workers in effective diagnosis and treatment as well as policy makers in policy formulation against helminths in Nigeria, endemic helminths were grouped according to their classes as cestodes, nematodes and trematodes.

Data extraction, collation and analysis

Data pulled out from the eligible studies were: name of author, the year the study was conducted and year it was published, sample size, number of positive cases, state and region of study, study design, type of study, host and helminths species of veterinary and zoonotic importance identified at least to the genus level.

Preliminary analyses including summations, subtractions and divisions were conducted using Microsoft Excel. Statistical and meta-analysis were respectively carried out with Graph-Pad Prism version 4.0 and Comprehensive Meta-Analysis version 3.0. Prevalence for individual studies was determined by multiplying the ratio of cases to sample size by 100. The binomial formula
$$ 95\% CI=\mathrm{p}\pm \mathrm{z}1\hbox{-} \upalpha /2\surd \mathrm{p}\left(1\hbox{-} \mathrm{p}/n\right) $$

was employed to determine the 95% Confidence interval (95% CI). It was assumed that the true effect sizes might differ within eligible studies; therefore the random-effects model was used to determine pooled prevalence estimates [35]. Heterogeneity within studies was evaluated using the Cochran’s Q-test while percentage variation in prevalence estimate due to heterogeneity was quantified using the formula I2 = 100 × (Q-df)/Q, where Q is Chi square and df is the degree of freedom which is the number of studies minus one. In accordance with the report of Higgins and Thompson, [36], I2 values of 0, 25, 50 and 75% were considered as no, low, moderate and high heterogeneities, respectively.

Results

Bibliographic search and eligible studies

The selection process for eligible studies and the list of excluded studies are presented in Fig. 2 and Additional file 3, respectively. Of the 86 studies retrieved, 69 were from databases while the remaining 17 resulted from checking the lists of references of the studies obtained through the search of databases. Twenty nine duplicate studies were removed after scanning through titles. A total of 13 studies were excluded after detailed abstract and full text review for reasons such as: lack of clearly stated numbers of positive cases/sample sizes (n = 6), lack of identification of helminths at least to the genus level (n = 5) and sample size less than fifty (n = 2). A total of 44 studies were finally included in the meta-analysis.
Fig. 2
Fig. 2

Flow diagram for the selection process of eligible studies

Characteristics of eligible studies

The studies analysed were carried out between 1973 and 2016 and published between 1976 and 2016. Ten studies were reported from the North-central, nine from the North-eastern, 11 from the North-western, four each from the South-eastern and South-southern as well as 6 from the South-western regions. A total of 23 937 cases from a sample size of 320 208 were reported. The biological samples collected by the individual studies were blood, faeces and tissues. Thirty two studies reported helminths in cattle, 20 in goats and 12 in sheep. Two of the studies were carried out between 1970 and 1981, three between 1982 and 1993, five between 1994 and 2005 as well as 34 between 2006 and 2016. Twenty eight studies had sample sizes ≤1000, 5 had sample sizes between 1001 and 2000 and 11 had sample sizes greater than 2000. Thirty six, six, and two studies were abattoir-based, farm-based and market-based, respectively, while ten, 31 and three of the studies were diagnosed using macroscopy, microscopy and serology respectively (Table 1).
Table 1

List and characteristics of the 44 eligible studies

Year of study

Region

Host

Type of study

Method of diagnosis

Sample size

Cases

Prev. (%)

Study RN

2002

North-east

G/S

Farm-based

Microscopy

249

126

50.60

[16]

2007

North-west

C/G/S

Abattoir-based

Microscopy

300

100

33.33

[17]

2012/2013

North-central

C/G/S

Farm-based

Microscopy

326

298

91.41

[18]

2013/2014

North-central

C/G/S

Abattoir-based

Microscopy

2508

642

25.60

[19]

2016

North-east

C

Abattoir-based

Microscopy

208

187

89.90

[22]

2008

North-west

C

Abattoir-based

Macroscopy

11 804

315

2.67

[23]

2013

North-west

C

Abattoir-based

Serology

285

69

24.21

[24]

2013

South-west

C

Abattoir-based

Microscopy

397

163

41.06

[25]

2013

South-east

G

Abattoir-based

Microscopy

200

185

92.50

[26]

2013

North-central

G

Abattoir-based

Microscopy

248

183

73.79

[27]

2003/2004

North-west

C/G/S

Abattoir-based

Microscopy

76 702

61

0.08

[28]

2011

South-west

C/G/S

Farm-based

Microscopy

1171

251

21.43

[68]

2012/2013

South-south

C

Abattoir-based

Macroscopy

22 259

382

1.72

[69]

2012

North-west

C

Abattoir-based

Serology

386

66

17.10

[70]

2012

North-east

C

Abattoir-based

Macroscopy

3015

657

21.79

[71]

1973/1974

North-east

C

Abattoir-based

Macroscopy

14 270

4524

31.70

[72]

2012/2013

North-central

G/S

Market-based

Microscopy

1002

552

55.09

[73]

2009/2010

South-south

C

Abattoir-based

Microscopy

251

156

62.15

[74]

2013

North-central

C

Farm-based

Serology

686

536

78.13

[75]

2011/2012

North-west

G/S

Abattoir-based

Microscopy

300

242

80.67

[76]

2015

South-south

C

Abattoir-based

Microscopy

514

35

6.81

[77]

2005

South-west

C

Abattoir-based

Macroscopy

483

75

15.53

[78]

2010–2013

North-east

C

Abattoir-based

Macroscopy

6007

288

4.79

[79]

2016

North-east

C

Abattoir-based

Microscopy

208

62

29.81

[80]

2013

North-west

C

Abattoir-based

Microscopy

224

62

27.68

[81]

2009

North-west

C

Abattoir-based

Microscopy

200

30

15.00

[82]

1986

North-west

C

Abattoir-based

Microscopy

502

156

31.08

[83]

2011

North-west

C

Farm-based

Microscopy

1525

820

53.77

[84]

2009

South-east

C/G

Abattoir-based

Microscopy

1138

525

46.13

[85]

1991/1992

South-west

G

Abattoir-based

Microscopy

1080

896

82.96

[86]

2013

North-central

G

Abattoir-based

Microscopy

248

183

73.79

[87]

2013/2014

South-west

C/G/S

Farm-based

Microscopy

170

132

77.65

[88]

2010

North-west

C

Abattoir-based

Macroscopy

285

5

1.75

[89]

2014

South-west

G

Market-based

Microscopy

400

303

75.75

[90]

1985

South-east

C

Abattoir-based

Macroscopy

942

38

4.03

[91]

1999–2002

South-east

C

Abattoir-based

Macroscopy

25 800

6750

26.16

[92]

2010/2011

South-south

G

Abattoir-based

Microscopy

213

161

75.59

[93]

2015

North-central

C

Abattoir-based

Microscopy

160

55

34.38

[94]

1997–1999

North-central

C

Abattoir-based

Microscopy

14 372

1924

13.39

[95]

1973–1975

North-east

C/G/S

Abattoir-based

Microscopy

3322

1202

36.18

[96]

2012

North-east

C

Abattoir-based

Microscopy

350

122

34.86

[97]

2010

North-central

G/S

Abattoir-based

Microscopy

110

59

53.64

[98]

2006

North-east

G/S

Abattoir-based

Macroscopy

124 888

78

0.06

[99]

2011

North-central

C

Abattoir-based

Microscopy

500

281

56.20

[100]

C: Cattle; G: Goats; S: Sheep; Prev.: Prevalence; RN: Reference number

Regional distribution of eligible studies

The studies were distributed across 19 Nigerian States. Studies were concentrated mostly in the North-western region 11 (25.0%) and Sokoto State five (11.4%), followed by the North-central region 10 (22.7%) as well as Oyo and Rivers States four (9.1%). The least number of studies were reported in the South-southern region, four (9.19%) as well as Adamawa, Imo and Niger States, one (2.3%) as presented in Fig. 1.

Pooled prevalence estimate and heterogeneity analysis

The overall pooled prevalence estimate (PPE), PPEs for different strata and heterogeneities are presented in Table 2. Individual prevalence of eligible studies ranged between 0.06 and 92.50%. The study revealed an overall pooled prevalence estimate of 7.48% (95% CI: 7.38–7.57) from 23 937 cases and 320 208 ruminants. Regional pooled prevalence estimates ranged between 2.08% (95% CI: 1.99–2.18) in the North-western region and 49.18% (95% CI: 47.55–50.80) in the South-western region. PPEs among different host species ranged between 1.90% (95% CI: 1.78–2.02) and 12.55% (95% CI: 12.39–12.72). Based on the period of study, prevalence estimates ranged between 4.49% (95% CI: 4.39–4.58) among studies published between 2006 and 2016 and 43.19% (95% CI: 41.24–45.14) for studies published between 1982 and 1993. Pooled prevalence estimates in relation to sample sizes ranged between 5.52% (95% CI: 5.44–5.60) for studies with sample sizes greater than 2000 and 51.45% (95% CI: 50.17–52.73) for studies with sample sizes between 1001 and 2000. Prevalence estimates in relation to study settings ranged between 6.65% (95% CI: 6.56–6.73) for abattoir-based and 60.98% (95% CI: 58.37–63.55) for market-based studies. PPEs in relation to methods of diagnosis ranged between 6.25% (95% CI: 6.15–6.36) for studies diagnosed using macroscopy and 49.45% (95% CI: 46.75–52.14) for studies diagnosed using serology. The PPEs for helminths of zoonotic importance in Nigerian ruminants were 0.11% (95% CI: 0.09–0.12), 13.60% (95% CI: 12.46–14.80), 13.84% (95% CI: 13.55–14.13) and 15.81% (95% CI: 15.51–16.11) for Echinococcus/hydatid cysts, Oesophagostomum species, Fasciola gigantica and T. saginata/Cysticercus bovis respectively (Table 2).
Table 2

Pooled prevalence estimates of helminths in Nigerian ruminants based on different strata

Variables

No. of Studies

Pooled prevalence estimates

(95% CI)

Heterogeneity

Sample size

Cases

Prev. (%)

I 2 (%)

Q-P

Region

North-central

10

20 160

4713

23.38

22.80–23.97

99.71

0.000

North-east

9

152 517

7246

4.75

4.64–4.86

99.84

0.000

North-west

11

92 513

1926

2.08

1.99–2.18

99.79

0.000

South-east

4

28 080

7498

26.70

26.19–27.22

99.46

0.000

South-south

4

23 237

734

3.16

2.94–3.39

99.83

0.000

South-west

6

3701

1820

49.18

47.55–50.80

99.52

0.000

Hosts

Cattle

32

154 953

19 446

12.55

12.39–12.72

99.75

0.000

Goat

20

113 563

3510

3.09

2.99–3.19

99.60

0.000

Sheep

12

51 692

981

1.90

1.78–2.02

99.55

0.000

Study period

1970–1981

2

17 592

5726

32.55

31.86–33.25

95.93

0.000

1982–1993

3

2524

1090

43.19

41.24–45.14

99.75

0.000

1994–2005

5

117 606

8936

7.60

7.45–7.75

99.87

0.000

2006–2016

34

182 486

8185

4.49

4.39–4.58

99.76

0.000

Sample size

≤1000

28

9345

4070

43.55

42.54–44.57

98.81

0.000

1001–2000

5

5916

3044

51.45

50.17–52.73

99.46

0.000

> 2000

11

304 947

16 823

5.52

5.44–5.60

99.92

0.000

Study type

Abattoir-based

36

314 679

20 919

6.65

6.56–6.73

99.79

0.000

Farm-based

6

4127

2163

52.41

50.87–53.94

99.76

0.000

Market-based

2

1402

855

60.98

58.37–63.55

97.98

0.000

MOD

       

Macroscopy

10

209 753

13 112

6.25

6.15–6.36

99.91

0.000

Microscopy

31

109 098

10 154

9.31

9.14–9.48

99.63

0.000

Serology

3

1357

671

49.45

46.75–52.14

99.49

0.000

Overall

44

320 208

23 937

7.48

7.38–7.57

99.78

0.000

P < 0.001 for all strata; CI: Confidence interval; I2: Inverse variance index; MOD: Method of diagnosis; Prev.: Prevalence; Q-P: Cochran’s P-value

The study revealed an overall high degree of heterogeneity (99.78%, 95% CI: 7.38–7.57, P < 0.001) which persisted even in different strata such as the Northern (99.78%, 95% CI: 5.15–5.32, P < 0.001) and Southern regions (99.78, 95% CI: 17.95–18.60, P < 0.001) as well as hosts like cattle (99.75, 95% CI: 12.39–12.72, P < 0.001), sheep (99.55%, 95% CI: 1.78–2.02, P < 0.001) and goats (99.60%, 95% CI: 2.99–3.19, P < 0.001) as presented in Figs. 3, 4, 5, and 6. Most (48.15%) of the parasites reported in ruminants were nematodes. The most prevalent species of cestode, nematode and trematode were T. saginata/Cysticercus bovis (15.81%), Strongyloides papillosus (32.06%) and Paramphistomum spp. (15.51%) while Taenia spp., Strongyloides papillosus and Fasciola gigantica respectively had the widest geographical distribution (Table 3).
Fig. 3
Fig. 3

Forest plot for the prevalence of helminths of veterinary and zoonotic importance in Nigerian ruminants. RN: Reference number

Fig. 4
Fig. 4

Forest plot for the prevalence of helminths of veterinary and zoonotic importance in ruminants in Northern and Southern Nigeria. RN: Reference number

Fig. 5
Fig. 5

Forest plot for the prevalence of helminths of veterinary and zoonotic importance in Nigerian cattle. RN: Reference number

Fig. 6
Fig. 6

Forest plot for the prevalence of helminths of veterinary and zoonotic importance in goats and sheep in Nigeria. RN: Reference number

Table 3

Pooled prevalence estimates and distribution of helminths species according to class of parasites

Parasites

Number of studies

Pooled prevalence estimates

(95% CI)

Heterogeneity

Sample size

Cases

Prev. (%)

I 2 (%)

Q-P

HVI Cestodes

Moniezia expansa

9

5785

368

6.36

5.75–7.02

99.51

0.000

Avitellina centripunctata

3

712

33

4.63

3.21–6.45

95.01

0.000

Taenia spp.

10

3224

104

3.23

2.64–3.90

99.17

0.000

Moniezia benedeni

4

4643

77

1.66

1.31–2.07

97.62

0.000

Overall (Cestodes)

14 364

582

4.05

3.73–4.39

97.82

0.000

Nematodes

       

Strongyloides papillosus

13

7671

2459

32.06

31.01–33.11

99.90

0.000

Gongylonema spp.

1

248

41

16.53

12.13–21.75

0.00

0.594

Gaigeria spp.

1

248

35

14.11

10.03–19.08

0.00

0.742

Bunostomum phlebotomum

9

4513

407

9.02

8.20–9.89

94.16

0.000

Trichostrongylus spp.

7

3300

287

8.70

7.76–9.71

99.01

0.000

Ostertagia spp.

5

1160

99

8.53

6.99–10.29

0.00

0.436

Trichuris globulosa

8

4930

337

6.84

6.15–7.58

87.56

0.005

Cooperia pectinata

2

2663

173

6.50

5.59–7.50

0.00

0.335

Haemonchus contortus

8

4104

234

5.70

5.01–6.46

98.78

0.000

Chabertia ovina

2

464

25

5.39

3.52–7.85

0.00

0.844

Nematodirus spp.

4

1905

87

4.57

3.67–5.60

89.94

0.002

Toxocara vitulorum

10

6634

283

4.27

3.79–4.78

98.65

0.000

Trichuris ovis

7

4591

71

1.55

1.21–1.95

87.93

0.004

Overall (Nematodes)

42 431

4538

10.70

10.40–10.99

99.67

0.000

Trematodes

       

Paramphistomum spp.

12

9180

1424

15.51

14.78–16.27

91.49

0.001

Eurytrema pancreaticum

3

672

81

12.05

9.69–14.76

98.76

0.000

Schistosoma bovis

6

1926

191

9.92

8.62–11.34

95.54

0.000

Dicrocoelium hospes

5

7809

641

8.21

7.61–8.84

98.57

0.000

Dicrocoelium dendriticum

4

3436

152

4.42

3.76–5.17

71.93

0.059

Gastrothylax spp.

2

464

14

3.02

1.66–5.01

46.71

0.171

Overall (Trematodes)

23 478

2503

10.66

10.27–11.06

98.79

0.000

HZI

       

T. saginata/C. bovis

5

58 925

9315

15.81

15.51–16.11

98.79

0.000

Fasciola gigantica

20

53 402

7390

13.84

13.55–14.13

99.97

0.000

Oesophagostomum spp.

7

3397

462

13.60

12.46–14.80

0.00

0.799

Echinococcus/Hydatid cyst

4

202 160

213

0.11

0.09–0.12

77.86

0.034

Overall (HZI)

 

317 884

17 380

5.47

5.39–5.55

99.95

0.000

CI: Confidence interval; HVI: Helminths of veterinary importance; HZI: Helminths of zoonotic importance; I 2 : Inverse variance index; Prev.: Prevalence; Q-P: Cochran’s P-value

Discussion

Several studies have documented individual divisional, provincial and regional reports on helminth parasites of ruminants in different parts of Nigeria. However, information on the national prevalence of these parasites is lacking. The evidence available shows that this is probably the first meta-analysis to consider endemic helminths of ruminants, their prevalence and distribution across Nigeria. The study was necessary to provide useful epidemiological information required for the institution of control programmes that will help in reducing economic losses and public health problems associated with these helminths.

The overall pooled prevalence estimate of 7.48% observed in Nigerian ruminants is lower than reports of other meta-analysis from Ethiopia [37, 38]. The variations in these PPEs may be attributable to factors including grazing habits, nutritional status, husbandry and production systems, host immunological status [39], availability of intermediate hosts as well as the number of viable infective larvae and eggs in the environment [40]. The differences between time of sample collection and analysis as well as the specificity and sensitivity of the diagnostic methods employed by the various studies may also be possible reasons for the variations in the PPEs. Studies from Ethiopia [41] and Andhra Pradesh, India [42] also reported similar helminth species as those reported in Nigeria during the period under review.

Pooled prevalence estimates in relation to regions was highest in South-western Nigeria probably due to the forested nature, the longer periods of rainfall, lower temperatures, lower humidity and high soil moisture in the region [33]. Failure of control programmes such as adequate sanitation, control of intermediate hosts and strategic deworming due to inadequate funding may also account for the higher prevalence in south-west Nigeria. Majority of Nigerian livestock are raised in Northern Nigeria explaining the higher number of studies reported in the region.

Yearly distribution of studies shows that most of the studies were published between 2006 and 2016 suggesting an increase in research during the last few years out of the four decades reviewed. This may be due to increased awareness and research on animal health. The study revealed a drastic decline in the pooled prevalence of similar helminths from 47.76% during 1982 and 1993 to 4.49% during 2006 and 2016. With the increased specificity and sensitivity of current diagnostic techniques, the recent decline in the prevalence of helminths suggests increased awareness of the socio-economic and public health consequences of these infections by farmers, improvements in quality of veterinary services, management practices as well as improved hygiene and sanitation levels.

Studies with larger sample sizes give more representation of the study population, and are believed to provide more reliable findings. Despite these advantages, over 64% of the studies had sample sizes of 1000 and less. The smaller sample sizes may not be unconnected with the lack of grants for supporting research in Nigeria. The higher prevalence observed in cattle as compared to sheep and goats may be due to factors related to differences in host’s susceptibility, genetic make-up, defence mechanisms and parasite host specificity. The open grazing of cattle in areas used by humans for defecation as opposed the raising of sheep and goats in backyard housing may explain the higher prevalence reported in cattle.

From the economic standpoint, cattle and small ruminants (sheep and goats), serve as major sources of income and livelihood, and contribute 50 and 35% of the total meat produced in Nigeria, respectively [25, 32] despite the fact that over 90% of them are managed traditionally with inadequate veterinary care [43]. Therefore, this study which provides information on the burden of helminth infections in cattle and small ruminants became necessary to curtail economic losses that may be associated with unidentified and uncontrolled helminth infections.

Majority of the reported nematode species are parasites of cattle, sheep and goats with the exception of Toxocara vitulorum and Trichostrongylus spp., which are mainly parasites of cattle. Nematodes like Oesophagostomum spp. may also be of public health concern. The presence of Haemonchus contortus is of particular concern due to its high pathogenecity and economic importance in sheep and goats [44].

The distribution of studies in relation to study settings shows that majority (82.2%) of the studies were abattoir-based, probably due to the ease of collecting samples from slaughtered animals, especially with the challenges of on-farm studies such as unwillingness of herdsmen to allow researchers access to their animals, problems of restraining large animals like cattle and insecurity in the rural areas where most of the livestock is raised. The epidemiological significance of the highest PPE reported in livestock markets is the risk of initiating new endemic foci for these infections especially those of public health concerns like cysticercosis and cystic echinococcosis. The presence of zoonotic helminths in food animals slaughtered for human consumption during this period is of public health concern. To ensure food safety, quality veterinary meat inspection is suggested to curtail the transmission of these helminths to humans.

Cysticercus bovis was the most prevalent (15.81%) of the five species of cestodes reported in Nigeria. This PPE is considerably higher than the ranges documented in other developing countries of Africa (0.2–5.6%) [4547] and elsewhere (0.09–3.0%) [4850]. The occurrence of this metacestode alongside hydatid cysts in food animals that entered the food chain is a threat to public health considering their association respectively with cysticercosis and cystic echinococcosis in humans.

Paramphistomum spp. was the most prevalent of all the species of trematodes reported in Nigeria. This may be due to the massive asexual multiplication of helminths of the genus Paramphistomum in snail intermediate hosts and the long lifespan of these helminths that usually results in a constant source of infection for successive generations of snails [51]. Substantive evidence shows that various genera of these snails (Archachatina, Limicolaria and Oncomelania) are endemic in Nigeria [5255]. These reports have justified the occurrence of different trematodes like Fasciola gigantica, Dicrocoelium spp., Eurytrema pancreaticum and Schistosoma bovis among others across Nigeria. Though there are no documented reports of human infections with zoonotic flukes like Fasciola gigantica, Dicrocoelium dendriticum and Eurytrema pancreaticum in Nigeria, reports elsewhere [5659] showed that they may be potential threats to public health in Nigeria. This suggests the need for studies in humans to determine the status of these parasites in Nigerians.

The grouping of helminths according to their phylogenetic classes was based on the fact that members of these groups share common control measures. For instance, while nematodes of ruminants have direct life cycle and are pasture-borne, cestodes and trematodes that have indirect life cycles are arthropod-borne and gastropod-borne parasites, respectively [3, 60]. Consequently, while nematode control targets rotational grazing of ruminants, the control of cestodes and trematodes usually focus on reducing the numbers of arthropod and gastropods intermediate hosts in the environment. In addition, majority of anthelmintics used for chemotherapeutic control are also classified as anticestodals (e.g. praziquantel, nitroscanate), antinematodals (e.g. piperazine, tetrahydropyrimidines) and antitrematodals (e.g. benzimidazoles, salicylanides) for these phylogenetic classes [6163].

Three diagnostic methods (macroscopy, microscopy and serology) were employed by the 44 studies analyzed. Macroscopy was used basically for the gross identification of cystic conditions caused by larval stages of cestodes like C. bovis and hydatid cyst as well as adult helminths like Fasciola spp. Microscopy was used for the identification of helminth eggs while serology was used for antigen/antibody detection. Though all these techniques are valuable in the diagnosis of helminth infections, they are not without limitations. While macroscopy may easily miss non-prominent lesions during gross examination of tissues, sample preparation for microscopy may be time-consuming, labour intensive and requires expertise. Serology which is the most sensitive and specific of these three diagnostic techniques is associated with false positive results and is limited to the detection of only few helminth species. These limitations may contribute to the low prevalence observed and the inability of some of the studies to identify helminths to the species level. Due to these deficiencies, highly sensitive and specific molecular techniques earlier described [6467] may provide a better understanding of the status of helminths parasites in Nigeria.

The findings of this study have several implications. Looking from the epidemiological point of view, the detection of helminths in congregations of livestock like markets may suggest possible increased risk of transmission of these parasites as majority of farmers buy these animals from the markets and introduce them into their herds without any veterinary care. On the other hand, the presence of these helminths in ruminants on farms may probably cause contamination of grazing pasture and sources of drinking water for these animals resulting in new foci of infections. There are obvious public health implications of finding zoonotic helminths like hydatid cyst, Cysticercus bovis, Fasciola gigantica and Oesophagostomum spp. among others in ruminants. These include the risk of environmental contamination that may result in human infections or of acquiring such infections through the consumption of slaughtered food animals that enter the food chain. These parasites are associated with different conditions in humans ranging from diarrhoea, retarded growth, intellectual and cognitive retardation [29] to cystic echinococcosis and cysticercosis.

Limitations

Though this study provided useful epidemiological information on the prevalence and distribution of endemic helminths in Nigeria, which will be useful in disease control, it is not devoid of limitations. First, there were uneven distributions of studies across states, regions, hosts, study period, study types and sample sizes, This implies that the findings may not accurately represent the situation for Nigeria. Another setback is the fact that despite the distribution of eligible studies across the six Nigerian regions, studies were published from only nineteen of the thirty-six states.

Conclusions

Helminths of veterinary and medical importance are prevalent in Nigeria with overall PPE of 7.48%. There was a 43.3% decline in the pooled prevalence of helminths over a period of 13 years. The highest pooled prevalence estimates were observed in the South-western region and among cattle. Strongyloides papillosus was the most prevalent of all the helminths while Fasciola gigantica had the widest geographical distribution across Nigeria. High degrees of heterogeneity were observed within studies and different strata. On-farm good agricultural practices including effective strategic deworming of livestock according to parasites’ seasonality and abundance, ranching instead of nomadism, standard veterinary meat inspection and adequate hygiene and sanitation in abattoirs and livestock markets will reduce the economic, public health and veterinary threats caused by these parasites.

Abbreviations

AJOL: 

African Journals OnLine

C: 

Cattle

CI

Confidence interval

FCT: 

Federal Capital Territory

G: 

Goat

HVI: 

Helminths of veterinary importance

HZI: 

Helminths of zoonotic importance

I 2

Inverse variance index

MOD: 

Method of diagnosis

PPE(s): 

Pooled prevalence estimate(s)

Prev: 

Prevalence

PRISMA: 

Preferred Reporting Items for Systematic Review and Meta-Analysis

Q: 

Cochran’s heterogeneity statistic

Q-P

Cochran’s P-value

RN: 

Reference number

S: 

Sheep

Declarations

Acknowledgements

The authors are grateful to the Editor-In-Chief of the Nigerian Journal of Parasitology for making available some of the articles included in the meta-analysis.

Availability of data and materials

The data supporting the conclusion of this article are all included within the article and Additional files 2 and 3.

Authors’ contributions

SNK: Conceived and designed the study, SNK, BVM, JKPK: Conducted comprehensive literature search, screened literatures and extracted data, SNK: Carried out statistical and meta-analysis, SNK: wrote the paper. All authors read and approved the final version of the manuscript.

Ethics approval and consent to participate

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Veterinary Public Health and Preventive Medicine, University of Jos, PMB, 2084 Jos, Nigeria
(2)
Department of Veterinary Public Health and Preventive Medicine, Ahmadu Bello University, PMB, 1045 Zaria, Nigeria

References

  1. Garcia HH, Moro PL, Schantz PM. Zoonotic helminth infections of humans: echinococcosis, cysticercosis and fascioliasis. Curr Opin Infect Dis. 2007;20:489–94.View ArticlePubMedGoogle Scholar
  2. Ugbomoiko US, Ariza L, Heukelbach J. Parasites of importance for human health in Nigerian dogs: high prevalence and limited knowledge of pet owners. BMC Vet Res. 2008;4:49.9 pages.Google Scholar
  3. Urquhart GM, Armour J, Duncan JL, Jennings FW. Veterinary Parasitology, second edition, Blackwell publishers, 2003, pp. 157–158.Google Scholar
  4. Greenland K, Dixon R, Khan SA, Gunawardena K, Kihara JH, Smith JL, et al. The epidemiology of soil-transmitted helminths in Bihar state, India. PLoS Neg Trop Dis. 2015;9(5):e0003790.View ArticleGoogle Scholar
  5. Lee AC, Schantz PM, Kazacos KR, Montgomery SP, Bowman DD. Epidemiologic and zoonotic aspects of ascarid infections in dogs and cats. Trends Parasitol. 2010;26(4):155–61.View ArticlePubMedGoogle Scholar
  6. Steinmann P, Zhou XN, Li YL, Li HJ, Chen SR, Yang Z, et al. Helminth infections and risk factor analysis among residents in Eryuan county, Yunnan province, China. Acta Trop. 2007;104:38–51.View ArticlePubMedGoogle Scholar
  7. Cundill B, Alexander N, Bethony JM, Diemert D, Pullan RL, Brooker S. Rates and intensity of re-infection with human helminths after treatment and the influence of individual, household, and environmental factors in a Brazilian community. Parasitology. 2011;138:1406–16.View ArticlePubMedGoogle Scholar
  8. World Health Organization. Prevention and control of schistosomiasis and soil transmitted helminthiasis. World Health Organ Tech Rep Ser. 2002;912(i-vi):1–57. back coverGoogle Scholar
  9. Brooker S, Michael E. The potential of geographical information systems and remote sensing in the epidemiology and control of human helminth infections. Adv Parasitol. 2007;47:245–87.View ArticleGoogle Scholar
  10. Brooker S, Bethony J, Hotez PJ. Human hookworm infection in the 21st century. Adv Parasitol. 2004;58:197–288.View ArticlePubMedPubMed CentralGoogle Scholar
  11. Wilson P. Decomposing variation in dairy profitability: the impact of output, inputs, prices, labour and management. J Agric Sci. 2011;149:507–17.View ArticlePubMedPubMed CentralGoogle Scholar
  12. Herrero M, Thornton PK. Livestock and global change: emerging issues for sustainable food systems. Proc Natl Acad Sci U S A. 2013;110:20878–81.View ArticlePubMedPubMed CentralGoogle Scholar
  13. Qamar MF, Maqbool A, Ahmad N. Economic losses due to haemonchosis in sheep and goats. Sci Intern. 2011;23(4):321–4.Google Scholar
  14. Ploeger HW, Koosterman A, Bargeman G, Wuijokhuise LV, Den Brink R. Milk yield increase after anthelmintic treatment of dairy cattle related to some parameters estimating helminth infection. Vet Parasitol. 1990;35(1–2):103–16.View ArticlePubMedGoogle Scholar
  15. Nodtvedt A, Dohoo I, Sanchez J, Conboy G, DesCôteaux L, Keefe G. Increase in milk yield following eprinomectin treatment at calving in pastured dairy cattle. Vet Parasitol. 2002;105(3):191–206.View ArticlePubMedGoogle Scholar
  16. Nwosu CO, Madu PP, Richards WS. Prevalence and seasonal changes in the population of gastrointestinal nematodes of small ruminants in the semi-arid zone of North-Eastern Nigeria. Vet Parasitol. 2007;144(1–2):118–24.View ArticlePubMedGoogle Scholar
  17. Abunza MD, Ahmad A, Afana S. Prevalence of paramphistomiasis in ruminants slaughtered at Sokoto central abattoir, Sokoto. Nig J basic Appl Sci. 2008;16(2):287–92.Google Scholar
  18. Ibukun AV, Oludunsin F. Prevalence of intestinal helminths and protozoa parasites of ruminants in Minna, north-central, Nigeria. IOSR J Agric Vet Sci. 2015;8(2):62–7.Google Scholar
  19. Odeniran PO, Jegede HO, Adewoga TOS. Prevalence and risk perception of adult-stage parasites in slaughtered food animals (cattle, sheep and goat) among local meat personnel in Ipata abattoir, Ilorin, Nigeria. Vet Med Anim Sci. 2016;4(1):1.View ArticleGoogle Scholar
  20. Biu AA, Ahmed MI, Mshelia SS. Economic assessment of losses due to parasitic diseases common at the Maiduguri abattoir, Nigeria. Afr Sci. 2006;7(3):143–5.Google Scholar
  21. Danbirni S, Ziyauhaq H, Allam L, Okaiyeto SO, Sackey AKB. Prevalence of liver condemnation due to fascioliasis in slaughtered cattle and its financial losses at Kano old abattoir, Nigeria. J Vet Adv. 2015;5(6):1004–9.View ArticleGoogle Scholar
  22. Karshima NS, Bata SI, Bobbo AA. Prevalence, risk factors and economic losses associated with fasciolosis in slaughtered cattle in Bauchi, North-Eastern Nigeria. Alex J Vet Sci. 2016a;50(1):87–93.Google Scholar
  23. Rabiu BM, Jegede OC. Incidence of bovine cysticercosis in Kano state, north-western, Nigeria. Bayero J Pure Appl Sci. 2010;3(1):100–3.Google Scholar
  24. Okolugbo BC, Luka S, Ndams IS. Enzyme linked immunosorbent assay in the serodiagnosis of hydatidosis in camels (Camelus dromedarius) and cattle in Sokoto, northern Nigeria. Int J Infect Dis. 2014;13(1):1–6.Google Scholar
  25. Adedipe OD, Uwalaka EC, Akinseye VO, Adediran OA, Cadmus SIB. Gastrointestinal helminths in slaughtered cattle in Ibadan, South-Western Nigeria. J Vet Med. 2014;2014:923561.View ArticlePubMedPubMed CentralGoogle Scholar
  26. Ani OC, Nshiwu GN. Assessment of intestinal parasites in goats slaughtered at Abakaliki abattoir, Ebonyi state, Nigeria. Nig. J Parasitol. 2015;36(2):81–4.Google Scholar
  27. Nwoke EU, Odikamnoro OO, Ibiam GA, Umah OV, Ariom OTA. Survey of common gut helminths of goats slaughtered at Ankpa abattoir, Kogi state, Nigeria. J Parasitol Vect. Biol. 2015;7(5):89–93.Google Scholar
  28. Magaji AA, Oboegbulem SI, Daneji AI, Garba HS, Salihu MD, Junaidu AU, et al. Incidence of hydatid cyst disease in food animals slaughtered at Sokoto central abattoir, Sokoto state, Nigeria. Vet Wld. 2011;4(5):197–200.Google Scholar
  29. Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S. Current concepts: hookworm infection. N Engl J Med. 2004;351:799–807.View ArticlePubMedGoogle Scholar
  30. Diop AG, de-Boer HM, Mandlhate C, Prilipko L, Meinardi H. The global campaign against epilepsy in Africa. Acta Trop. 2003;87:149–59.View ArticlePubMedGoogle Scholar
  31. Adedipe NO, Bakshi JS, Odegbaro OA, Aliyu A. Evolving the Nigeria Agricultural Research Strategy Plan: Agro-Ecological Inputs, National Agricultural Research Project (NARP), 1996.Google Scholar
  32. Ugwu DS. The role of small ruminants in the household economy of southeast zone of Nigeria. Res. J Appl Sci. 2007;2(6):726–32.Google Scholar
  33. Iloeje NP. A new geography of Nigeria. New revised edition. Nigeria: Longman; 2001.Google Scholar
  34. Moher D, Liberati A, Tetzlaff J, Altman DG. The PRISMA group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.View ArticlePubMedPubMed CentralGoogle Scholar
  35. Hedges LV, Vevea JL. Fixed- and random-effects models in meta-analysis. Psychol Meth. 1998;3:486–504.View ArticleGoogle Scholar
  36. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Meth. 2002;21:1539–58.Google Scholar
  37. Asmare K, Sheferaw D, Aragaw K, Abera M, Sibhat B, Haile A, et al. Gastrointestinal nematode infection in small ruminants in Ethiopia: a systematic review and meta-analysis. Acta Trop. 2016a;160:68–77.View ArticlePubMedGoogle Scholar
  38. Asmare K, Sibhat B, Abera M, Haile A, Degefu H, Fentie T, et al. Systematic review and meta-analysis of metacestodes prevalence in small ruminants in Ethiopia. Prev Vet Med. 2016b;129:99–107.View ArticlePubMedGoogle Scholar
  39. McNeilly TN, Nisbet AJ. Immune modulation by helminth parasites of ruminants: implications for vaccine development and host immune competence. Parasite. 2014;21:51.View ArticlePubMedPubMed CentralGoogle Scholar
  40. Radostits OM, Blood DC, Gay CC. Diseases caused by helminth parasites, in veterinary medicine: a textbook of diseases of cattle, sheep, pigs, goats and horses, 8th ed. London; 1994.Google Scholar
  41. Sissay MM, Uggla A, Waller PJ. Prevalence and seasonal incidence of nematode parasites and fluke infections of sheep and goats in eastern Ethiopia. Trop Anim Hlth Prod. 2007;39(7):521–31.View ArticleGoogle Scholar
  42. Murthy GSS, Rao PV. Prevalence of gastrointestinal parasites in ruminants and poultry in Telangana region of Andhra Pradesh. J Para Dis. 2014;38(2):190–2.View ArticleGoogle Scholar
  43. Tibi KN, Aphunu A. Analysis of cattle market in Delta state: the supply determinants. Afr J Gen Agric. 2010;6(4):199–203.Google Scholar
  44. Mortensen LL, Williamson LH, Terrill TH, Kircher R, Larsen M, Kaplan RM. Evaluation of prevalence and clinical implications of anthelmintic resistance in gastro-intestinal nematodes of goats. J Am Vet Med Assoc. 2003;23:495–500.View ArticleGoogle Scholar
  45. Dzoma BM, Setlhodi EK, Molefe MM, Motsei LE, Bakunzi FR, Ndou RV, et al. Prevalence of bovine cysticercosis in the north West Province of South Africa from 2000 to 2010. J Hum Ecol. 2011;36(1):9–12.View ArticleGoogle Scholar
  46. Emiru L, Tadesse D, Kifleyohannes T, Sori T, Hagos Y. Prevalence and Public health significance of bovine cysticercosis at Elfora, abattoir, Ethiopia. J Public Health Epidemiol. 2015;7(2):34–40.View ArticleGoogle Scholar
  47. Nzeyimana P, Habarugira G, Udahemuka JC, Mushonga B, Tukei M. Prevalence of bovine cysticercosis and age relationship at post-mortem in Nyagatare slaughterhouse. Wld J Agric Sci. 2015;3(1):004–8.Google Scholar
  48. Garedaghi Y, Saber APR, Khosroshahi MS. Prevalence of bovine cysticercosis of slaughtered cattle in Meshkinshahr abattoir. Am J Anim Vet Sci. 2011;6(3):121–4.View ArticleGoogle Scholar
  49. Cueto-González SA, Rodríguez-Castillo JL, López-Valencia G, Bermúdez-Hurtado RM, Hernández-Robles ES, Monge-Navarro FJ. Prevalence of Taenia saginata larvae (Cysticercus bovis) in feedlot cattle slaughtered in a federal inspection type abattoir in north-West México. Foodborne Pathog Dis. 2015;12(5):462–5.View ArticlePubMedGoogle Scholar
  50. Rossi GAM, de Simoni HAS, Lopes WDZ, Almeida HMS, Soares VE. Prevalence and geospatial distribution of bovine cysticercosis in the state of Mato Grosso, Brazil. Prev Vet Med. 2016;130:94–8.View ArticlePubMedGoogle Scholar
  51. Waal T. Paramphistomum - a brief review. Irish Vet J. 2010;63(5):313–5.Google Scholar
  52. Ayanda OI. Prevalence of snail vectors of schistosomiasis and their infection rates in two localities within Ahmadu Bello University campus, Zaria, Kaduna state, Nigeria. J Cell Anim Biol. 2009;3(4):058–61.Google Scholar
  53. Kalu NK, Kalu EO, Ukwe MC, Onyeuwu CN. A survey of freshwater snails: the intermediate hosts of schistosomiasis in Bende LGA, Abia state, Nigeria. Intern J Sci Nat. 2012;3(4):879–82.Google Scholar
  54. Okeke OC, Ubachukwu PO. Urinary schistosomiasis in urban and semi-urban communities in South-Eastern Nigeria. Iran J Parasitol. 2013;8(3):467–73.PubMedPubMed CentralGoogle Scholar
  55. Igbinosa IB, Isaac C, Adamu HO, Adeleke G. Parasites of edible land snails in Edo state, Nigeria. Helminthologia. 2016;53(4):331–5.View ArticleGoogle Scholar
  56. Ishii Y, Koga M, Fujino T, Higo H, Ishibashi J, Oka K, et al. Human infection with the pancreatic fluke, Eurytrema pancreaticum. Am J Trop Med Hyg. 1983;32:1019–22.View ArticlePubMedGoogle Scholar
  57. Jack J, Adusu E, Jelinek T. Human infection with Dicrocoelium dendriticum. Dtsch Med Wochenschr. 2004;129:2538–40. (in German)View ArticleGoogle Scholar
  58. Le TH, De NV, Agatsuma T, Nguyen TG, Nguyen QD, McManus DP, et al. Human fascioliasis and the presence of hybrid/introgressed forms of Fasciola hepatica and Fasciola gigantica in Vietnam. Int J Parasitol. 2008;38(6):725–30.View ArticlePubMedGoogle Scholar
  59. González LC, Esteban JG, Bargues MD, Valero MA, Ortiz P, Náquira C, et al. Hyperendemic human fascioliasis in Andean valleys: an altitudinal transect analysis in children of Cajamarca province, Peru. Acta Trop. 2011;120(1–2):119–29.View ArticlePubMedGoogle Scholar
  60. Zajac AM, Conboy GA. Veterinary clinical parasitology. 7th ed. Iowa, USA: Blackwell Publishers; 2006.Google Scholar
  61. Gilles HM, Hoffman PS. Treatment of intestinal parasitic infections: a review of nitazoxanide. Trends Parasitol. 2002;18:95–7.View ArticlePubMedGoogle Scholar
  62. Lee BH, Clothier MF, Dutton FE, Nelson SJ, Johnson SS, Thompson DP, et al. Marcfortine and Paraherquamide class of anthelmintics: discovery of PNU-141962. Curr Top Med Chem. 2002;2:779–93.View ArticlePubMedGoogle Scholar
  63. Greenwood K, Williams T, Geary T. Nematode neuropeptide receptors and their development as anthelmintic screens. Parasitology. 2005;131:S169–77.View ArticlePubMedGoogle Scholar
  64. Harmon AF, Williams ZB, Zarlenga DS, Hildreth MB. Real-time PCR for quantifying Haemonchus contortus eggs and potential limiting factors. Parasitol Res. 2007;101:71–6.View ArticlePubMedGoogle Scholar
  65. Bott NJ, Campbell BE, Beveridge I, Chilton NB, Rees D, Hunt PW, et al. A combined microscopic-molecular method for the diagnosis of strongylid infections in sheep. Int J Parasitol. 2009;39(11):1277–87.View ArticlePubMedGoogle Scholar
  66. Roeber F, Jex AR, Campbell AJD, Campbell BE, Anderson GA, Gasser RB. Evaluation and application of a molecular method to assess the composition of strongylid nematode populations in sheep with naturally acquired infections. Infect Genet Evol. 2011;11(5):849–854.Google Scholar
  67. Roeber F, Larsen JWA, Anderson N, Campbell AJD, Anderson GA, Gasser RB, et al. A molecular diagnostic tool to replace larval culture in conventional faecal egg count reduction testing in sheep. PLoS One. 2012;7(5):e37327.View ArticlePubMedPubMed CentralGoogle Scholar
  68. Adediran OA, Adebiyi AI, Uwalaka EC. Prevalence of Fasciola species in ruminants under extensive management system in Ibadan South-Western Nigeria. Afr J Med Med Sci. 2014;43:137–41.PubMedGoogle Scholar
  69. Akpabio U. Incidence of bovine fasciolosis and its economic implications at trans-Amadi abattoir port-Harcourt. Nigeria Acta Parasitol Glob. 2014;5(3):206–9.Google Scholar
  70. Aliyu AA, Ajogi IA, Ajanusi OJ, Reuben RC. Epidemiological studies of Fasciola gigantica in cattle in Zaria, Nigeria using coprology and serology. J Public Health Epidemiol. 2014;6(2):85–91.View ArticleGoogle Scholar
  71. Ardo MB, Aliyara YH, Lawal H. Prevalence of bovine fasciolosis in major abattoirs of Adamawa state, Nigeria. Bayero. J Pure Appl Sci. 2013;6(1):12–6.Google Scholar
  72. Babalola DA, Schillhorn VTW. Incidence of fascioliasis in cattle slaughtered in Bauchi (Nigeria). Trop Anim Hlth Prod. 1976;8(4):243–7.Google Scholar
  73. Dantanko H, Idris HS. Helminthosis in livestock slaughtered in Dei-Dei abattoir, F.C.T Abuja. Glob Adv. Res J Agric Sci. 2014;3(9):304–9.Google Scholar
  74. Elele K, Owhoeli O, Gboeloh LB. Prevalence of species of helminth parasites in cattle slaughtered in selected abattoirs in Port Harcourt, south-south, Nigeria. Intern Res Med Sci. 2013;1(2):010–7.Google Scholar
  75. Elelu E, Ambali A, Coles GC, Eisler MC. Cross-sectional study of Fasciola gigantica and other trematode infections of cattle in Edu local government area, Kwara state, north-Central Nigeria. Parasit Vectors. 2016;9(470)Google Scholar
  76. Gana JJ, Makun H, Chiezey NP, Tekdek LB. Epidemiological study on abomasal nematodes in slaughtered small ruminants raised in the Guinea savannah zone of Nigeria. Sok J Vet Sci. 2015;13(2):26–33.View ArticleGoogle Scholar
  77. Gboeloh LB. Occurrence of adult Taenia saginata in cattle slaughtered in major abattoirs in port-Harcourt metropolis, Nigeria. Intern J Biol Biomol Agric Food Biotech Eng. 2015;9(12):1249–52.Google Scholar
  78. Idowu OA, Olorode N, Idowu AB, Sam-Wobo SO. Fascioliasis: Prevalence, protein content and attitude of meat sellers to infected livers of slaughtered cattle in Abeokuta. Nig. J Parasitol. 2007;28(2):125–8.Google Scholar
  79. Karshima NS, Pam VA, Bobbo AA, Obalisa A. Occurrence of Cysticercus bovis in cattle slaughtered at the Ibi slaughter house, Ibi local government area of Taraba state, Nigeria. J Vet Adv. 2013;3(3):130–4.View ArticleGoogle Scholar
  80. Karshima NS, Bata SI, Bobbo AA, Habila A. Prevalence and risk factors of Dicrocoelium dendriticum and Eurytrema pancreaticum infections in slaughtered cattle in Bauchi, Nigeria. Nig J Parasitol. 2016b;37(2):260–4.View ArticleGoogle Scholar
  81. Magaji AA, Kabir I, Salihu MD, Saulawa MA, Mohammed AA, Musawa AI. Prevalence of fascioliasis in cattle slaughtered in Sokoto metropolitan abattoir, Sokoto, Nigeria. Adv Epidemiol. 2014;2014:43–8.View ArticleGoogle Scholar
  82. Musa FM, Damisa D, Ado A. Prevalence of Taenia saginata in cattle slaughtered at Tudun Wada abattoir Kaduna Nigeria. Nig J Parasitol. 2011;32(1):41–3.Google Scholar
  83. Ndifon GT, Betterton C, Rollinson D. Schistosoma curassoni Brumpt, 1931 and S. bovis (Sonsino, 1876) in cattle in northern Nigeria. J Helminthol. 1988;62(1):33–4.View ArticlePubMedGoogle Scholar
  84. Nnabuife HE, Dakul AD, Dogo GI, Egwu OK, Weka PR, Ogo IN, et al. A study on helminthiasis of cattle herds in Kachia grazing reserve (KGR) of Kaduna state, Nigeria. Vet Wld. 2013;6(11):936–40.Google Scholar
  85. Nwigwe JO, Njoku OO, Odikamnoro OO, Uhuo AC. Comparative study of intestinal helminths and protozoa of cattle and goats in Abakaliki metropolis of Ebonyi state, Nigeria. Adv Appl Sci Res. 2013;4(2):223–7.Google Scholar
  86. Nwosu CO, Ogunrinade AF, Fagbemi BO. Prevalence and seasonal changes in the gastro-intestinal helminths of Nigerian goats. J Helminthol. 1996;70(4):329–33.View ArticlePubMedGoogle Scholar
  87. Odikamnoro OO, Uhuo CA, Nwoke EU, Daniel LE, Ebiriekwe SC, Elom MO. Survey of common gut parasites of goat slaughtered at Ankpa abattoir, Kogi state, Nigeria: implication for public health. Intern J Med Sci Clin Invent. 2015;2(5):885–91.Google Scholar
  88. Ogudo US, Oluwole AS, Oladeji MH, Adeniran AA, Alabi OM, Ekpo UF. Gastrointestinal helminth infections in a ruminant livestock farm in Abeokuta, south -western Nigeria. Ann Res Rev Biol. 2015;8(4):1–8.Google Scholar
  89. Okolugbo BC, Luka SA, Ndams IS. Hydatidosis of camels and cattle slaughtered in Sokoto state, Northern-Nigeria. Food Sci Qual Mgt. 2013;21:40–6.Google Scholar
  90. Olanike AO, Olayide AJ, Oludunsin FO, Aderoju OR, Dauda WJ. Prevalence of gastrointestinal parasites of goats in Ibadan, south-west, Nigeria. Wld J Agric Res. 2015;3(2):49–51.Google Scholar
  91. Okolo MI. Studies on Taenia saginata cysticercosis in eastern Nigeria. Intern J Zoon. 1986;13(2):98–103.Google Scholar
  92. Opara MN, Ukpong UM, Okoli IC, Anosike JC. Cysticercosis of slaughter cattle in South-Eastern Nigeria. Ann N Y Acad Sci. 2006;1081:339–46.View ArticlePubMedGoogle Scholar
  93. Owhoeli O, Elele K, Gboeloh LB. Prevalence of gastrointestinal helminths in exotic and indigenous goats slaughtered in selected abattoirs in Port Harcourt, south-south, Nigeria. Chin J Biol. 2014;2014(1):1–8.View ArticleGoogle Scholar
  94. Oyedeji FN. Intestinal helminth parasites of cattle slaughtered in abattoirs in Gwagwalada. Wld Rural Obser. 2016;8(1):23–6.Google Scholar
  95. Qadeer MA. Prevalence of bovine cysticercosis in Jos abattoir. Nigeria Anim Res Int. 2008;5(1):777–9.Google Scholar
  96. Schillhorn VTW, Folaranmi DO, Usman S, Ishaya T. Incidence of liver fluke infections (Fasciola gigantica and Dicrocoelium hospes) in ruminants in northern Nigeria. Trop Anim Hlth Prod. 1980;12(2):97–104.View ArticleGoogle Scholar
  97. Shitta KB, James-Rugu NN. Prevalence of gastro-intestinal helminths of slaughtered cattle at Wukari abattoir Taraba state, North-Eastern Nigeria. Nig J Parasitol. 2013;34(2):55–9.Google Scholar
  98. Solomon-Wisdom GO, Matur BM, Ibe KC. Prevalence of intestinal helminth infections among sheep and goats raised for slaughtering in Gwagwalada abattoir, Abuja, Nigeria. J Glob Pharm Sci. 2014;2(1):12–9.Google Scholar
  99. Tijani AO, Musa HI, Atsanda NN, Mamman B. Prevalence of hydatidosis in sheep and goats slaughtered at Damaturu abattoir, Yobe state, Nigeria. Nig Vet J. 2013;31(1):71–5.Google Scholar
  100. Yohanna JA, Maisaje RD, Nwibari BMW, Njoku CI. Gastro-intestinal helminths among slaughtered cattle at Jos abattoir, Plateau state. Nig J Parasitol. 2012;33(2):141–4.Google Scholar

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