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

Helminths of veterinary and zoonotic importance in Nigerian ruminants: a 46-year meta-analysis... 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 * Correspondence: torkarshima@yahoo.co.uk Department of Veterinary Public Health and Preventive Medicine, University of Jos, PMB, 2084 Jos, Nigeria Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This 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. Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 2 of 15 Multilingual abstracts result in diarrhoea, retarded growth, intellectual and Please see Additional file 1 for translations of the abstract cognitive retardation [29], cystic echinococcosis and into the five official working languages of the United cysticercosis [30]. Nations. The livestock industry plays a vital role in the economy of Nigeria. It serves as a major source of income and liveli- Background hood for majority of Nigerians who are rural settlers and Helminths of ruminants refer to a group of complex contributes about 5.2% of the National Gross Domestic multicellular eukaryotic parasites which are infective to Product (GDP) [31]. In addition, cattle, sheep and goats animals and humans in which case they are called zoo- contribute over 80% of the total meat produced in Nigeria noses [1]. This group of parasites cause serious economic [25, 32]. Despite these benefits, helminth infections still and public health problems in many resource-limited cause serious economic losses in Nigeria as a result of re- countries across the globe. In Nigeria for instance, these ductions in milk production, weight gain, fertility and problems are influenced by inadequate veterinary and carcass quality. The aim of this study was to provide epi- medical care as well as inadequate policies on disease con- demiological information which will help in instituting trol among many other factors [2]. sustainable control programmes against these parasites, Helminth parasites of ruminants are broadly grouped thus reducing economic losses associated with these hel- into two phyla, namely nemathelminthes which are nema- minths and maximising the contribution of the livestock todes or roundworms such as Haemonchus, Bonostomum, industry to Nigeria’sGDP. Oesophagostomum and Chabertia and platyhelminthes which include cestodes (e.g. Avitellina, Moniezia, Stilesia Methods and Taenia) and trematodes such as Dicrocoelium, Eury- Study areas trema, Fasciola and Paramphistomum [3]. Transmission We included in the present review studies published on of these parasites may be through the ingestion of para- helminths of veterinary and zoonotic importance in ru- sitic eggs and infective larvae on contaminated pasture, minants from Nigeria (West Africa; 4–14 N; 3–14 E) water, soil, human hands or tissues of infected vertebrate which covers a surface area totalling 923 768 km (Fig. 1). intermediate hosts, skin penetration, transplacental as well In Nigeria, there are two seasons; the rainy season which as arthropod and gastropod intermediate hosts [4]. Trans- runs from March to November in the Southern region mission is influenced by factors including poor hygiene and May to October in the Northern region, as well as the and sanitation, indiscriminate and open defecation [5], as dry season which runs from December to February in the well as environmental factors like temperature, humidity, South and November to April in the North [33]. rainfall [6] and soil moisture [7]. Lack of strategic de- worming of livestock [8, 9], poverty and overcrowding Bibliographic search strategy [10] are additional factors. The study followed the Preferred Reporting Items for The negative impacts of helminths on livestock prod- Systematic Review and Meta-Analysis (PRISMA) guide- uctivity still remain a major challenge in the livestock in- lines published by Moher et al. [34], and the three authors dustry globally [11] despite the projected increased conducted independently the literature search. We used dependence on agriculture in the nearest future [12]. the PRISMA checklist (Additional file 2) as the basis for These parasites cause serious economic losses in rumi- inclusion of relevant information. The outcome of interest nants ranging from growth rate decrease and poor quality was the infection of Nigerian ruminants with helminths of skin and hides to reductions in the production of milk, species of veterinary and zoonotic importance. meat and wool [13]. For instance, evidence revealed that A comprehensive literature search was carried out on lactating cows may lose 294.8 kg of milk on average per PubMed, MEDLINE, Google Scholars, AJOL and refer- lactation due to helminth parasites [14, 15]. In Nigeria, in- ences of studies that resulted from the search of data- fection prevalence rates range between 25.6 and 91.4% bases between September, 2016 and March, 2017. To [16–19]. Economic losses caused by the rejection of edit- ensure that relevant studies were not omitted, the search able organs of slaughtered food animals during veterinary was categorized into three stages as broad, narrow and meat inspections were also documented [20–22]. specific search stages. Under the broad search, combina- From the public health point of view, reports of zoo- tions like helminths of ruminants in Nigeria, prevalence notic meta-cestodes; Cysticercus bovis and hydatid cyst or occurrence of helminths of ruminants in Nigeria were [19, 23, 24], nematode; Oesophagostomum [25–27] used. Search combinations employed for the narrow and trematodes; Dicrocoelium dendriticum, Eurytrema search included, but were not limited to, prevalence or pancreaticum and Fasciola gigantica [22, 28]entering occurrence of cestodes, nematodes or trematodes of ru- the food chain in Nigeria are of great public health minants in Nigeria. The combinations used under spe- concern. Human infections with these parasites may cific search targeted helminth species of ruminants and Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 3 of 15 Fig. 1 Distribution of eligible studies and regional prevalence of helminths in ruminants in Nigeria included, but were not limited to, prevalence or occurrence while those that are naturally infective to man and ani- of Avitellina ± centripunctata, Taenia ± saginata/Cysticercus mals were considered of zoonotic importance. In order ± bovis, Echinococcus/hydatid ± cyst, Moniezia ± expansa ± to provide data that would guide veterinarians and public benedeni, Bunostomum ± phlebotomum, Toxocara ± health workers in effective diagnosis and treatment as well vitulorum, Haemonchus ± contortus ± placei, Fasciola ± as policy makers in policy formulation against helminths gigantica ± hepatica and Dicrocoelium ± dendriticum in in Nigeria, endemic helminths were grouped according to cattle, sheep and goats. Specific searches were also nar- their classes as cestodes, nematodes and trematodes. rowed to regions and states of the Nigerian federation. Inclusion criteria Data extraction, collation and analysis Studies identified by any of the three search stages were Data pulled out from the eligible studies were: name of then screened before selection. A study was considered author, the year the study was conducted and year it was eligible only if: (i) it was carried out in Nigeria, (ii) it was published, sample size, number of positive cases, state and published in English, (iii) it was published between 1970 region of study, study design, type of study, host and hel- and 2016, (iv) it was a cross sectional study, (v) the study minths species of veterinary and zoonotic importance specified the location in Nigeria where it was conducted, identified at least to the genus level. (vi) the sample size and number of positive cases were Preliminary analyses including summations, subtrac- clearly stated, (vii) the sample size was ≥50, (viii) it re- tions and divisions were conducted using Microsoft Excel. ported helminths species of veterinary and zoonotic im- Statistical and meta-analysis were respectively carried out portance, (ix) the method of diagnosis was stated, (x) with Graph-Pad Prism version 4.0 and Comprehensive parasites were identified at least to the genus level. Meta-Analysis version 3.0. Prevalence for individual stud- In this study, helminths were considered of veterinary ies was determined by multiplying the ratio of cases to importance if they are naturally infective to animals only sample size by 100. The binomial formula Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 4 of 15 removed after scanning through titles. A total of 13 studies 95%CI ¼ p  z1‐α=2√p1ðÞ ‐p=n were excluded after detailed abstract and full text review was employed to determine the 95% Confidence interval for reasons such as: lack of clearly stated numbers of (95% CI). It was assumed that the true effect sizes might positive cases/sample sizes (n = 6), lack of identification differ within eligible studies; therefore the random-effects of helminths at least to the genus level (n =5) and sam- model was used to determine pooled prevalence estimates ple size less than fifty (n = 2). A total of 44 studies were [35]. Heterogeneity within studies was evaluated using the finally included in the meta-analysis. Cochran’s Q-test while percentage variation in prevalence estimate due to heterogeneity was quantified using the Characteristics of eligible studies formula I =100 ×(Q-df)/Q, where Q is Chi square and df The studies analysed were carried out between 1973 and is the degree of freedom which is the number of studies 2016 and published between 1976 and 2016. Ten studies minus one. In accordance with the report of Higgins and were reported from the North-central, nine from the Thompson, [36], I values of 0, 25, 50 and 75% were North-eastern, 11 from the North-western, four each considered as no, low, moderate and high heterogeneities, from the South-eastern and South-southern as well as 6 respectively. from the South-western regions. A total of 23 937 cases from a sample size of 320 208 were reported. The bio- Results logical samples collected by the individual studies were Bibliographic search and eligible studies blood, faeces and tissues. Thirty two studies reported The selection process for eligible studies and the list of helminths in cattle, 20 in goats and 12 in sheep. Two of excluded studies are presented in Fig. 2 and Additional file 3, the studies were carried out between 1970 and 1981, respectively. Of the 86 studies retrieved, 69 were from data- three between 1982 and 1993, five between 1994 and 2005 bases while the remaining 17 resulted from checking the as well as 34 between 2006 and 2016. Twenty eight studies lists of references of the studies obtained through the had sample sizes ≤1000, 5 had sample sizes between 1001 search of databases. Twenty nine duplicate studies were and 2000 and 11 had sample sizes greater than 2000. Fig. 2 Flow diagram for the selection process of eligible studies Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 5 of 15 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 Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 6 of 15 Thirty six, six, and two studies were abattoir-based, farm- Pooled prevalence estimate and heterogeneity analysis based and market-based, respectively, while ten, 31 and The overall pooled prevalence estimate (PPE), PPEs for three of the studies were diagnosed using macroscopy, mi- different strata and heterogeneities are presented in croscopy and serology respectively (Table 1). 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) Regional distribution of eligible studies from 23 937 cases and 320 208 ruminants. Regional The studies were distributed across 19 Nigerian States. pooled prevalence estimates ranged between 2.08% (95% Studies were concentrated mostly in the North-western CI: 1.99–2.18) in the North-western region and 49.18% region 11 (25.0%) and Sokoto State five (11.4%), followed (95% CI: 47.55–50.80) in the South-western region. PPEs by the North-central region 10 (22.7%) as well as Oyo among different host species ranged between 1.90% and Rivers States four (9.1%). The least number of (95% CI: 1.78–2.02) and 12.55% (95% CI: 12.39–12.72). studies were reported in the South-southern region, Based on the period of study, prevalence estimates ranged four (9.19%) as well as Adamawa, Imo and Niger between 4.49% (95% CI:4.39–4.58) among studies pub- States, one (2.3%) as presented in Fig. 1. lished between 2006 and 2016 and 43.19% (95% CI: Table 2 Pooled prevalence estimates of helminths in Nigerian ruminants based on different strata Variables No. of Pooled prevalence estimates (95% CI) Heterogeneity Studies Sample size Cases Prev. (%) I (%) 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; I : Inverse variance index; MOD: Method of diagnosis; Prev.: Prevalence; Q-P: Cochran’s P-value Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 7 of 15 41.24–45.14) for studies published between 1982 and 95% CI:17.95–18.60, P < 0.001) as well as hosts like cattle 1993. Pooled prevalence estimates in relation to sam- (99.75, 95% CI: 12.39–12.72, P < 0.001), sheep (99.55%, ple sizes ranged between 5.52% (95% CI:5.44–5.60) 95% CI:1.78–2.02, P < 0.001) and goats (99.60%, 95% for studies with sample sizes greater than 2000 and CI:2.99–3.19, P < 0.001) as presented in Figs. 3, 4, 5, 51.45% (95% CI: 50.17–52.73) for studies with sample and 6. Most (48.15%) of the parasites reported in rumi- sizes between 1001 and 2000. Prevalence estimates in nants were nematodes. The most prevalent species of relation to study settings ranged between 6.65% (95% cestode, nematode and trematode were T. saginata/Cysti- CI:6.56–6.73) for abattoir-based and 60.98% (95% CI: cercus bovis (15.81%), Strongyloides papillosus (32.06%) 58.37–63.55) for market-based studies. PPEs in rela- and Paramphistomum spp. (15.51%) while Taenia spp., tion to methods of diagnosis ranged between 6.25% Strongyloides papillosus and Fasciola gigantica respect- (95% CI:6.15–6.36) for studies diagnosed using ively had the widest geographical distribution (Table 3). macroscopy and 49.45% (95% CI: 46.75–52.14) for studies diagnosed using serology. The PPEs for hel- minths of zoonotic importance in Nigerian ruminants Discussion were 0.11% (95% CI:0.09–0.12), 13.60% (95% CI: Several studies have documented individual divisional, 12.46–14.80), 13.84% (95% CI:13.55–14.13) and 15.81% provincial and regional reports on helminth parasites of (95% CI:15.51–16.11) for Echinococcus/hydatid cysts, ruminants in different parts of Nigeria. However, informa- Oesophagostomum species, Fasciola gigantica and T. sagi- tion on the national prevalence of these parasites is lack- nata/Cysticercus bovis respectively (Table 2). ing. The evidence available shows that this is probably the The study revealed an overall high degree of heterogen- first meta-analysis to consider endemic helminths of rumi- eity (99.78%, 95% CI:7.38–7.57, P < 0.001) which persisted nants, their prevalence and distribution across Nigeria. even in different strata such as the Northern (99.78%, The study was necessary to provide useful epidemiological 95% CI:5.15–5.32, P < 0.001) and Southern regions (99.78, information required for the institution of control Fig. 3 Forest plot for the prevalence of helminths of veterinary and zoonotic importance in Nigerian ruminants. RN: Reference number Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 8 of 15 Fig. 4 Forest plot for the prevalence of helminths of veterinary and zoonotic importance in ruminants in Northern and Southern Nigeria. RN: Reference number programmes that will help in reducing economic losses methods employed by the various studies may also be and public health problems associated with these possible reasons for the variations in the PPEs. Studies helminths. from Ethiopia [41] and Andhra Pradesh, India [42] also The overall pooled prevalence estimate of 7.48% ob- reported similar helminth species as those reported in served in Nigerian ruminants is lower than reports of Nigeria during the period under review. other meta-analysis from Ethiopia [37, 38]. The variations Pooled prevalence estimates in relation to regions was in these PPEs may be attributable to factors including highest in South-western Nigeria probably due to the grazing habits, nutritional status, husbandry and produc- forested nature, the longer periods of rainfall, lower tion systems, host immunological status [39], availability temperatures, lower humidity and high soil moisture in of intermediate hosts as well as the number of viable in- the region [33]. Failure of control programmes such as fective larvae and eggs in the environment [40]. The dif- adequate sanitation, control of intermediate hosts and ferences between time of sample collection and analysis as strategic deworming due to inadequate funding may also well as the specificity and sensitivity of the diagnostic account for the higher prevalence in south-west Nigeria. Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 9 of 15 Fig. 5 Forest plot for the prevalence of helminths of veterinary and zoonotic importance in Nigerian cattle. RN: Reference number Majority of Nigerian livestock are raised in Northern as opposed the raising of sheep and goats in backyard Nigeria explaining the higher number of studies reported housing may explain the higher prevalence reported in in the region. cattle. Yearly distribution of studies shows that most of the From the economic standpoint, cattle and small rumi- studies were published between 2006 and 2016 suggesting nants (sheep and goats), serve as major sources of income an increase in research during the last few years out of the and livelihood, and contribute 50 and 35% of the total four decades reviewed. This may be due to increased meat produced in Nigeria, respectively [25, 32] despite the awareness and research on animal health. The study re- fact that over 90% of them are managed traditionally with vealed a drastic decline in the pooled prevalence of similar inadequate veterinary care [43]. Therefore, this study helminths from 47.76% during 1982 and 1993 to 4.49% which provides information on the burden of helminth in- during 2006 and 2016. With the increased specificity and fections in cattle and small ruminants became necessary sensitivity of current diagnostic techniques, the recent de- to curtail economic losses that may be associated with un- cline in the prevalence of helminths suggests increased identified and uncontrolled helminth infections. awareness of the socio-economic and public health conse- Majority of the reported nematode species are parasites quences of these infections by farmers, improvements in of cattle, sheep and goats with the exception of Toxocara quality of veterinary services, management practices as well vitulorum and Trichostrongylus spp., which are mainly as improved hygiene and sanitation levels. parasites of cattle. Nematodes like Oesophagostomum spp. Studies with larger sample sizes give more representa- may also be of public health concern. The presence of tion of the study population, and are believed to provide Haemonchus contortus is of particular concern due to its more reliable findings. Despite these advantages, over high pathogenecity and economic importance in sheep 64% of the studies had sample sizes of 1000 and less. and goats [44]. The smaller sample sizes may not be unconnected with The distribution of studies in relation to study settings the lack of grants for supporting research in Nigeria. shows that majority (82.2%) of the studies were abattoir- The higher prevalence observed in cattle as compared to based, probably due to the ease of collecting samples sheep and goats may be due to factors related to differ- from slaughtered animals, especially with the challenges ences in host’s susceptibility, genetic make-up, defence of on-farm studies such as unwillingness of herdsmen to mechanisms and parasite host specificity. The open allow researchers access to their animals, problems of grazing of cattle in areas used by humans for defecation restraining large animals like cattle and insecurity in the Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 10 of 15 Fig. 6 Forest plot for the prevalence of helminths of veterinary and zoonotic importance in goats and sheep in Nigeria. RN: Reference number rural areas where most of the livestock is raised. The that entered the food chain is a threat to public health epidemiological significance of the highest PPE reported considering their association respectively with cysticerco- in livestock markets is the risk of initiating new endemic sis and cystic echinococcosis in humans. foci for these infections especially those of public health Paramphistomum spp. was the most prevalent of all concerns like cysticercosis and cystic echinococcosis. the species of trematodes reported in Nigeria. This may The presence of zoonotic helminths in food animals be due to the massive asexual multiplication of helminths slaughtered for human consumption during this period of the genus Paramphistomum in snail intermediate hosts is of public health concern. To ensure food safety, qual- and the long lifespan of these helminths that usually re- ity veterinary meat inspection is suggested to curtail sults in a constant source of infection for successive gen- the transmission of these helminths to humans. erations of snails [51]. Substantive evidence shows that Cysticercus bovis was the most prevalent (15.81%) of various genera of these snails (Archachatina, Limicolaria the five species of cestodes reported in Nigeria. This PPE and Oncomelania) are endemic in Nigeria [52–55]. These is considerably higher than the ranges documented in reports have justified the occurrence of different trema- other developing countries of Africa (0.2–5.6%) [45–47] todes like Fasciola gigantica, Dicrocoelium spp., Eury- and elsewhere (0.09–3.0%) [48–50]. The occurrence of trema pancreaticum and Schistosoma bovis among others this metacestode alongside hydatid cysts in food animals across Nigeria. Though there are no documented reports Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 11 of 15 Table 3 Pooled prevalence estimates and distribution of helminths species according to class of parasites Parasites Number Pooled prevalence estimates (95% CI) Heterogeneity of 2 Sample size Cases Prev. (%) I (%) Q-P studies 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 : Inverse variance index; Prev.: Prevalence; Q-P: Cochran’s P-value of human infections with zoonotic flukes like Fasciola The grouping of helminths according to their phylo- gigantica, Dicrocoelium dendriticum and Eurytrema pan- genetic classes was based on the fact that members of creaticum in Nigeria, reports elsewhere [56–59]showed these groups share common control measures. For in- that they may be potential threats to public health in stance, while nematodes of ruminants have direct life Nigeria. This suggests the need for studies in humans to cycle and are pasture-borne, cestodes and trematodes determine the status of these parasites in Nigerians. that have indirect life cycles are arthropod-borne and Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 12 of 15 gastropod-borne parasites, respectively [3, 60]. Conse- cognitive retardation [29] to cystic echinococcosis and quently, while nematode control targets rotational graz- cysticercosis. ing of ruminants, the control of cestodes and trematodes usually focus on reducing the numbers of arthropod and Limitations gastropods intermediate hosts in the environment. In Though this study provided useful epidemiological infor- addition, majority of anthelmintics used for chemothera- mation on the prevalence and distribution of endemic hel- peutic control are also classified as anticestodals (e.g. minths in Nigeria, which will be useful in disease control, praziquantel, nitroscanate), antinematodals (e.g. pipera- it is not devoid of limitations. First, there were uneven zine, tetrahydropyrimidines) and antitrematodals (e.g. distributions of studies across states, regions, hosts, study benzimidazoles, salicylanides) for these phylogenetic period, study types and sample sizes, This implies that the classes [61–63]. findings may not accurately represent the situation for Three diagnostic methods (macroscopy, microscopy Nigeria. Another setback is the fact that despite the distri- and serology) were employed by the 44 studies analyzed. bution of eligible studies across the six Nigerian regions, Macroscopy was used basically for the gross identification studies were published from only nineteen of the thirty- of cystic conditions caused by larval stages of cestodes like six states. C. bovis and hydatid cyst as well as adult helminths like Fasciola spp. Microscopy was used for the identification Conclusions of helminth eggs while serology was used for antigen/ Helminths of veterinary and medical importance are antibody detection. Though all these techniques are prevalent in Nigeria with overall PPE of 7.48%. There was valuable in the diagnosis of helminth infections, they a 43.3% decline in the pooled prevalence of helminths are not without limitations. While macroscopy may over a period of 13 years. The highest pooled prevalence easily miss non-prominent lesions during gross examin- estimates were observed in the South-western region and ation of tissues, sample preparation for microscopy may among cattle. Strongyloides papillosus was the most preva- be time-consuming, labour intensive and requires expert- lent of all the helminths while Fasciola gigantica had the ise. Serology which is the most sensitive and specific of widest geographical distribution across Nigeria. High de- these three diagnostic techniques is associated with false grees of heterogeneity were observed within studies and positive results and is limited to the detection of only few different strata. On-farm good agricultural practices in- helminth species. These limitations may contribute to the cluding effective strategic deworming of livestock accord- low prevalence observed and the inability of some of the ing to parasites’ seasonality and abundance, ranching studies to identify helminths to the species level. Due to instead of nomadism, standard veterinary meat inspection these deficiencies, highly sensitive and specific molecular and adequate hygiene and sanitation in abattoirs and live- techniques earlier described [64–67] may provide a better stock markets will reduce the economic, public health and understanding of the status of helminths parasites in veterinary threats caused by these parasites. Nigeria. The findings of this study have several implications. Looking from the epidemiological point of view, the de- Additional files tection of helminths in congregations of livestock like markets may suggest possible increased risk of transmis- Additional file 1: Multilingual abstracts in the five official working languages of the United Nations. (PDF 251 kb) sion of these parasites as majority of farmers buy these Additional file 2: Preferred Reporting Items for Systematic Review and animals from the markets and introduce them into their Meta-Analysis (PRISMA) checklist. (DOC 62 kb) herds without any veterinary care. On the other hand, Additional file 3: List of studies excluded from the meta-analysis. the presence of these helminths in ruminants on farms (DOCX 19 kb) may probably cause contamination of grazing pasture and sources of drinking water for these animals resulting Abbreviations in new foci of infections. There are obvious public health AJOL: African Journals OnLine; C: Cattle; CI: Confidence interval; FCT: Federal implications of finding zoonotic helminths like hydatid Capital Territory; G: Goat; HVI: Helminths of veterinary importance; HZI: Helminths of zoonotic importance; I : Inverse variance index; cyst, Cysticercus bovis, Fasciola gigantica and Oesophagos- MOD: Method of diagnosis; PPE(s): Pooled prevalence estimate(s); tomum spp. among others in ruminants. These include Prev: Prevalence; PRISMA: Preferred Reporting Items for Systematic Review and the risk of environmental contamination that may re- Meta-Analysis; Q: Cochran’s heterogeneity statistic; Q-P: Cochran’s P-value; RN: Reference number; S: Sheep sult in human infections or of acquiring such infec- tions through the consumption of slaughtered food Acknowledgements animals that enter the food chain. These parasites are The authors are grateful to the Editor-In-Chief of the Nigerian Journal of associated with different conditions in humans ran- Parasitology for making available some of the articles included in the ging from diarrhoea, retarded growth, intellectual and meta-analysis. Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 13 of 15 Availability of data and materials 18. Ibukun AV, Oludunsin F. Prevalence of intestinal helminths and protozoa The data supporting the conclusion of this article are all included within the parasites of ruminants in Minna, north-central, Nigeria. IOSR J Agric Vet Sci. article and Additional files 2 and 3. 2015;8(2):62–7. 19. Odeniran PO, Jegede HO, Adewoga TOS. Prevalence and risk perception of adult-stage parasites in slaughtered food animals (cattle, sheep and goat) Authors’ contributions among local meat personnel in Ipata abattoir, Ilorin, Nigeria. Vet Med Anim SNK: Conceived and designed the study, SNK, BVM, JKPK: Conducted Sci. 2016;4(1):1. comprehensive literature search, screened literatures and extracted data, 20. Biu AA, Ahmed MI, Mshelia SS. Economic assessment of losses due to SNK: Carried out statistical and meta-analysis, SNK: wrote the paper. All authors parasitic diseases common at the Maiduguri abattoir, Nigeria. Afr Sci. 2006; read and approved the final version of the manuscript. 7(3):143–5. 21. Danbirni S, Ziyauhaq H, Allam L, Okaiyeto SO, Sackey AKB. Prevalence of Ethics approval and consent to participate liver condemnation due to fascioliasis in slaughtered cattle and its financial Not applicable. losses at Kano old abattoir, Nigeria. J Vet Adv. 2015;5(6):1004–9. 22. Karshima NS, Bata SI, Bobbo AA. Prevalence, risk factors and economic Competing interests losses associated with fasciolosis in slaughtered cattle in Bauchi, North- The authors declare that they have no competing interests. Eastern Nigeria. 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Nig J Parasitol. 2012; 33(2):141–4. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Infectious Diseases of Poverty Springer Journals

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

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Medicine & Public Health; Infectious Diseases; Tropical Medicine; Public Health
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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 * Correspondence: torkarshima@yahoo.co.uk Department of Veterinary Public Health and Preventive Medicine, University of Jos, PMB, 2084 Jos, Nigeria Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This 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. Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 2 of 15 Multilingual abstracts result in diarrhoea, retarded growth, intellectual and Please see Additional file 1 for translations of the abstract cognitive retardation [29], cystic echinococcosis and into the five official working languages of the United cysticercosis [30]. Nations. The livestock industry plays a vital role in the economy of Nigeria. It serves as a major source of income and liveli- Background hood for majority of Nigerians who are rural settlers and Helminths of ruminants refer to a group of complex contributes about 5.2% of the National Gross Domestic multicellular eukaryotic parasites which are infective to Product (GDP) [31]. In addition, cattle, sheep and goats animals and humans in which case they are called zoo- contribute over 80% of the total meat produced in Nigeria noses [1]. This group of parasites cause serious economic [25, 32]. Despite these benefits, helminth infections still and public health problems in many resource-limited cause serious economic losses in Nigeria as a result of re- countries across the globe. In Nigeria for instance, these ductions in milk production, weight gain, fertility and problems are influenced by inadequate veterinary and carcass quality. The aim of this study was to provide epi- medical care as well as inadequate policies on disease con- demiological information which will help in instituting trol among many other factors [2]. sustainable control programmes against these parasites, Helminth parasites of ruminants are broadly grouped thus reducing economic losses associated with these hel- into two phyla, namely nemathelminthes which are nema- minths and maximising the contribution of the livestock todes or roundworms such as Haemonchus, Bonostomum, industry to Nigeria’sGDP. Oesophagostomum and Chabertia and platyhelminthes which include cestodes (e.g. Avitellina, Moniezia, Stilesia Methods and Taenia) and trematodes such as Dicrocoelium, Eury- Study areas trema, Fasciola and Paramphistomum [3]. Transmission We included in the present review studies published on of these parasites may be through the ingestion of para- helminths of veterinary and zoonotic importance in ru- sitic eggs and infective larvae on contaminated pasture, minants from Nigeria (West Africa; 4–14 N; 3–14 E) water, soil, human hands or tissues of infected vertebrate which covers a surface area totalling 923 768 km (Fig. 1). intermediate hosts, skin penetration, transplacental as well In Nigeria, there are two seasons; the rainy season which as arthropod and gastropod intermediate hosts [4]. Trans- runs from March to November in the Southern region mission is influenced by factors including poor hygiene and May to October in the Northern region, as well as the and sanitation, indiscriminate and open defecation [5], as dry season which runs from December to February in the well as environmental factors like temperature, humidity, South and November to April in the North [33]. rainfall [6] and soil moisture [7]. Lack of strategic de- worming of livestock [8, 9], poverty and overcrowding Bibliographic search strategy [10] are additional factors. The study followed the Preferred Reporting Items for The negative impacts of helminths on livestock prod- Systematic Review and Meta-Analysis (PRISMA) guide- uctivity still remain a major challenge in the livestock in- lines published by Moher et al. [34], and the three authors dustry globally [11] despite the projected increased conducted independently the literature search. We used dependence on agriculture in the nearest future [12]. the PRISMA checklist (Additional file 2) as the basis for These parasites cause serious economic losses in rumi- inclusion of relevant information. The outcome of interest nants ranging from growth rate decrease and poor quality was the infection of Nigerian ruminants with helminths of skin and hides to reductions in the production of milk, species of veterinary and zoonotic importance. meat and wool [13]. For instance, evidence revealed that A comprehensive literature search was carried out on lactating cows may lose 294.8 kg of milk on average per PubMed, MEDLINE, Google Scholars, AJOL and refer- lactation due to helminth parasites [14, 15]. In Nigeria, in- ences of studies that resulted from the search of data- fection prevalence rates range between 25.6 and 91.4% bases between September, 2016 and March, 2017. To [16–19]. Economic losses caused by the rejection of edit- ensure that relevant studies were not omitted, the search able organs of slaughtered food animals during veterinary was categorized into three stages as broad, narrow and meat inspections were also documented [20–22]. specific search stages. Under the broad search, combina- From the public health point of view, reports of zoo- tions like helminths of ruminants in Nigeria, prevalence notic meta-cestodes; Cysticercus bovis and hydatid cyst or occurrence of helminths of ruminants in Nigeria were [19, 23, 24], nematode; Oesophagostomum [25–27] used. Search combinations employed for the narrow and trematodes; Dicrocoelium dendriticum, Eurytrema search included, but were not limited to, prevalence or pancreaticum and Fasciola gigantica [22, 28]entering occurrence of cestodes, nematodes or trematodes of ru- the food chain in Nigeria are of great public health minants in Nigeria. The combinations used under spe- concern. Human infections with these parasites may cific search targeted helminth species of ruminants and Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 3 of 15 Fig. 1 Distribution of eligible studies and regional prevalence of helminths in ruminants in Nigeria included, but were not limited to, prevalence or occurrence while those that are naturally infective to man and ani- of Avitellina ± centripunctata, Taenia ± saginata/Cysticercus mals were considered of zoonotic importance. In order ± bovis, Echinococcus/hydatid ± cyst, Moniezia ± expansa ± to provide data that would guide veterinarians and public benedeni, Bunostomum ± phlebotomum, Toxocara ± health workers in effective diagnosis and treatment as well vitulorum, Haemonchus ± contortus ± placei, Fasciola ± as policy makers in policy formulation against helminths gigantica ± hepatica and Dicrocoelium ± dendriticum in in Nigeria, endemic helminths were grouped according to cattle, sheep and goats. Specific searches were also nar- their classes as cestodes, nematodes and trematodes. rowed to regions and states of the Nigerian federation. Inclusion criteria Data extraction, collation and analysis Studies identified by any of the three search stages were Data pulled out from the eligible studies were: name of then screened before selection. A study was considered author, the year the study was conducted and year it was eligible only if: (i) it was carried out in Nigeria, (ii) it was published, sample size, number of positive cases, state and published in English, (iii) it was published between 1970 region of study, study design, type of study, host and hel- and 2016, (iv) it was a cross sectional study, (v) the study minths species of veterinary and zoonotic importance specified the location in Nigeria where it was conducted, identified at least to the genus level. (vi) the sample size and number of positive cases were Preliminary analyses including summations, subtrac- clearly stated, (vii) the sample size was ≥50, (viii) it re- tions and divisions were conducted using Microsoft Excel. ported helminths species of veterinary and zoonotic im- Statistical and meta-analysis were respectively carried out portance, (ix) the method of diagnosis was stated, (x) with Graph-Pad Prism version 4.0 and Comprehensive parasites were identified at least to the genus level. Meta-Analysis version 3.0. Prevalence for individual stud- In this study, helminths were considered of veterinary ies was determined by multiplying the ratio of cases to importance if they are naturally infective to animals only sample size by 100. The binomial formula Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 4 of 15 removed after scanning through titles. A total of 13 studies 95%CI ¼ p  z1‐α=2√p1ðÞ ‐p=n were excluded after detailed abstract and full text review was employed to determine the 95% Confidence interval for reasons such as: lack of clearly stated numbers of (95% CI). It was assumed that the true effect sizes might positive cases/sample sizes (n = 6), lack of identification differ within eligible studies; therefore the random-effects of helminths at least to the genus level (n =5) and sam- model was used to determine pooled prevalence estimates ple size less than fifty (n = 2). A total of 44 studies were [35]. Heterogeneity within studies was evaluated using the finally included in the meta-analysis. Cochran’s Q-test while percentage variation in prevalence estimate due to heterogeneity was quantified using the Characteristics of eligible studies formula I =100 ×(Q-df)/Q, where Q is Chi square and df The studies analysed were carried out between 1973 and is the degree of freedom which is the number of studies 2016 and published between 1976 and 2016. Ten studies minus one. In accordance with the report of Higgins and were reported from the North-central, nine from the Thompson, [36], I values of 0, 25, 50 and 75% were North-eastern, 11 from the North-western, four each considered as no, low, moderate and high heterogeneities, from the South-eastern and South-southern as well as 6 respectively. from the South-western regions. A total of 23 937 cases from a sample size of 320 208 were reported. The bio- Results logical samples collected by the individual studies were Bibliographic search and eligible studies blood, faeces and tissues. Thirty two studies reported The selection process for eligible studies and the list of helminths in cattle, 20 in goats and 12 in sheep. Two of excluded studies are presented in Fig. 2 and Additional file 3, the studies were carried out between 1970 and 1981, respectively. Of the 86 studies retrieved, 69 were from data- three between 1982 and 1993, five between 1994 and 2005 bases while the remaining 17 resulted from checking the as well as 34 between 2006 and 2016. Twenty eight studies lists of references of the studies obtained through the had sample sizes ≤1000, 5 had sample sizes between 1001 search of databases. Twenty nine duplicate studies were and 2000 and 11 had sample sizes greater than 2000. Fig. 2 Flow diagram for the selection process of eligible studies Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 5 of 15 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 Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 6 of 15 Thirty six, six, and two studies were abattoir-based, farm- Pooled prevalence estimate and heterogeneity analysis based and market-based, respectively, while ten, 31 and The overall pooled prevalence estimate (PPE), PPEs for three of the studies were diagnosed using macroscopy, mi- different strata and heterogeneities are presented in croscopy and serology respectively (Table 1). 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) Regional distribution of eligible studies from 23 937 cases and 320 208 ruminants. Regional The studies were distributed across 19 Nigerian States. pooled prevalence estimates ranged between 2.08% (95% Studies were concentrated mostly in the North-western CI: 1.99–2.18) in the North-western region and 49.18% region 11 (25.0%) and Sokoto State five (11.4%), followed (95% CI: 47.55–50.80) in the South-western region. PPEs by the North-central region 10 (22.7%) as well as Oyo among different host species ranged between 1.90% and Rivers States four (9.1%). The least number of (95% CI: 1.78–2.02) and 12.55% (95% CI: 12.39–12.72). studies were reported in the South-southern region, Based on the period of study, prevalence estimates ranged four (9.19%) as well as Adamawa, Imo and Niger between 4.49% (95% CI:4.39–4.58) among studies pub- States, one (2.3%) as presented in Fig. 1. lished between 2006 and 2016 and 43.19% (95% CI: Table 2 Pooled prevalence estimates of helminths in Nigerian ruminants based on different strata Variables No. of Pooled prevalence estimates (95% CI) Heterogeneity Studies Sample size Cases Prev. (%) I (%) 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; I : Inverse variance index; MOD: Method of diagnosis; Prev.: Prevalence; Q-P: Cochran’s P-value Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 7 of 15 41.24–45.14) for studies published between 1982 and 95% CI:17.95–18.60, P < 0.001) as well as hosts like cattle 1993. Pooled prevalence estimates in relation to sam- (99.75, 95% CI: 12.39–12.72, P < 0.001), sheep (99.55%, ple sizes ranged between 5.52% (95% CI:5.44–5.60) 95% CI:1.78–2.02, P < 0.001) and goats (99.60%, 95% for studies with sample sizes greater than 2000 and CI:2.99–3.19, P < 0.001) as presented in Figs. 3, 4, 5, 51.45% (95% CI: 50.17–52.73) for studies with sample and 6. Most (48.15%) of the parasites reported in rumi- sizes between 1001 and 2000. Prevalence estimates in nants were nematodes. The most prevalent species of relation to study settings ranged between 6.65% (95% cestode, nematode and trematode were T. saginata/Cysti- CI:6.56–6.73) for abattoir-based and 60.98% (95% CI: cercus bovis (15.81%), Strongyloides papillosus (32.06%) 58.37–63.55) for market-based studies. PPEs in rela- and Paramphistomum spp. (15.51%) while Taenia spp., tion to methods of diagnosis ranged between 6.25% Strongyloides papillosus and Fasciola gigantica respect- (95% CI:6.15–6.36) for studies diagnosed using ively had the widest geographical distribution (Table 3). macroscopy and 49.45% (95% CI: 46.75–52.14) for studies diagnosed using serology. The PPEs for hel- minths of zoonotic importance in Nigerian ruminants Discussion were 0.11% (95% CI:0.09–0.12), 13.60% (95% CI: Several studies have documented individual divisional, 12.46–14.80), 13.84% (95% CI:13.55–14.13) and 15.81% provincial and regional reports on helminth parasites of (95% CI:15.51–16.11) for Echinococcus/hydatid cysts, ruminants in different parts of Nigeria. However, informa- Oesophagostomum species, Fasciola gigantica and T. sagi- tion on the national prevalence of these parasites is lack- nata/Cysticercus bovis respectively (Table 2). ing. The evidence available shows that this is probably the The study revealed an overall high degree of heterogen- first meta-analysis to consider endemic helminths of rumi- eity (99.78%, 95% CI:7.38–7.57, P < 0.001) which persisted nants, their prevalence and distribution across Nigeria. even in different strata such as the Northern (99.78%, The study was necessary to provide useful epidemiological 95% CI:5.15–5.32, P < 0.001) and Southern regions (99.78, information required for the institution of control Fig. 3 Forest plot for the prevalence of helminths of veterinary and zoonotic importance in Nigerian ruminants. RN: Reference number Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 8 of 15 Fig. 4 Forest plot for the prevalence of helminths of veterinary and zoonotic importance in ruminants in Northern and Southern Nigeria. RN: Reference number programmes that will help in reducing economic losses methods employed by the various studies may also be and public health problems associated with these possible reasons for the variations in the PPEs. Studies helminths. from Ethiopia [41] and Andhra Pradesh, India [42] also The overall pooled prevalence estimate of 7.48% ob- reported similar helminth species as those reported in served in Nigerian ruminants is lower than reports of Nigeria during the period under review. other meta-analysis from Ethiopia [37, 38]. The variations Pooled prevalence estimates in relation to regions was in these PPEs may be attributable to factors including highest in South-western Nigeria probably due to the grazing habits, nutritional status, husbandry and produc- forested nature, the longer periods of rainfall, lower tion systems, host immunological status [39], availability temperatures, lower humidity and high soil moisture in of intermediate hosts as well as the number of viable in- the region [33]. Failure of control programmes such as fective larvae and eggs in the environment [40]. The dif- adequate sanitation, control of intermediate hosts and ferences between time of sample collection and analysis as strategic deworming due to inadequate funding may also well as the specificity and sensitivity of the diagnostic account for the higher prevalence in south-west Nigeria. Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 9 of 15 Fig. 5 Forest plot for the prevalence of helminths of veterinary and zoonotic importance in Nigerian cattle. RN: Reference number Majority of Nigerian livestock are raised in Northern as opposed the raising of sheep and goats in backyard Nigeria explaining the higher number of studies reported housing may explain the higher prevalence reported in in the region. cattle. Yearly distribution of studies shows that most of the From the economic standpoint, cattle and small rumi- studies were published between 2006 and 2016 suggesting nants (sheep and goats), serve as major sources of income an increase in research during the last few years out of the and livelihood, and contribute 50 and 35% of the total four decades reviewed. This may be due to increased meat produced in Nigeria, respectively [25, 32] despite the awareness and research on animal health. The study re- fact that over 90% of them are managed traditionally with vealed a drastic decline in the pooled prevalence of similar inadequate veterinary care [43]. Therefore, this study helminths from 47.76% during 1982 and 1993 to 4.49% which provides information on the burden of helminth in- during 2006 and 2016. With the increased specificity and fections in cattle and small ruminants became necessary sensitivity of current diagnostic techniques, the recent de- to curtail economic losses that may be associated with un- cline in the prevalence of helminths suggests increased identified and uncontrolled helminth infections. awareness of the socio-economic and public health conse- Majority of the reported nematode species are parasites quences of these infections by farmers, improvements in of cattle, sheep and goats with the exception of Toxocara quality of veterinary services, management practices as well vitulorum and Trichostrongylus spp., which are mainly as improved hygiene and sanitation levels. parasites of cattle. Nematodes like Oesophagostomum spp. Studies with larger sample sizes give more representa- may also be of public health concern. The presence of tion of the study population, and are believed to provide Haemonchus contortus is of particular concern due to its more reliable findings. Despite these advantages, over high pathogenecity and economic importance in sheep 64% of the studies had sample sizes of 1000 and less. and goats [44]. The smaller sample sizes may not be unconnected with The distribution of studies in relation to study settings the lack of grants for supporting research in Nigeria. shows that majority (82.2%) of the studies were abattoir- The higher prevalence observed in cattle as compared to based, probably due to the ease of collecting samples sheep and goats may be due to factors related to differ- from slaughtered animals, especially with the challenges ences in host’s susceptibility, genetic make-up, defence of on-farm studies such as unwillingness of herdsmen to mechanisms and parasite host specificity. The open allow researchers access to their animals, problems of grazing of cattle in areas used by humans for defecation restraining large animals like cattle and insecurity in the Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 10 of 15 Fig. 6 Forest plot for the prevalence of helminths of veterinary and zoonotic importance in goats and sheep in Nigeria. RN: Reference number rural areas where most of the livestock is raised. The that entered the food chain is a threat to public health epidemiological significance of the highest PPE reported considering their association respectively with cysticerco- in livestock markets is the risk of initiating new endemic sis and cystic echinococcosis in humans. foci for these infections especially those of public health Paramphistomum spp. was the most prevalent of all concerns like cysticercosis and cystic echinococcosis. the species of trematodes reported in Nigeria. This may The presence of zoonotic helminths in food animals be due to the massive asexual multiplication of helminths slaughtered for human consumption during this period of the genus Paramphistomum in snail intermediate hosts is of public health concern. To ensure food safety, qual- and the long lifespan of these helminths that usually re- ity veterinary meat inspection is suggested to curtail sults in a constant source of infection for successive gen- the transmission of these helminths to humans. erations of snails [51]. Substantive evidence shows that Cysticercus bovis was the most prevalent (15.81%) of various genera of these snails (Archachatina, Limicolaria the five species of cestodes reported in Nigeria. This PPE and Oncomelania) are endemic in Nigeria [52–55]. These is considerably higher than the ranges documented in reports have justified the occurrence of different trema- other developing countries of Africa (0.2–5.6%) [45–47] todes like Fasciola gigantica, Dicrocoelium spp., Eury- and elsewhere (0.09–3.0%) [48–50]. The occurrence of trema pancreaticum and Schistosoma bovis among others this metacestode alongside hydatid cysts in food animals across Nigeria. Though there are no documented reports Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 11 of 15 Table 3 Pooled prevalence estimates and distribution of helminths species according to class of parasites Parasites Number Pooled prevalence estimates (95% CI) Heterogeneity of 2 Sample size Cases Prev. (%) I (%) Q-P studies 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 : Inverse variance index; Prev.: Prevalence; Q-P: Cochran’s P-value of human infections with zoonotic flukes like Fasciola The grouping of helminths according to their phylo- gigantica, Dicrocoelium dendriticum and Eurytrema pan- genetic classes was based on the fact that members of creaticum in Nigeria, reports elsewhere [56–59]showed these groups share common control measures. For in- that they may be potential threats to public health in stance, while nematodes of ruminants have direct life Nigeria. This suggests the need for studies in humans to cycle and are pasture-borne, cestodes and trematodes determine the status of these parasites in Nigerians. that have indirect life cycles are arthropod-borne and Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 12 of 15 gastropod-borne parasites, respectively [3, 60]. Conse- cognitive retardation [29] to cystic echinococcosis and quently, while nematode control targets rotational graz- cysticercosis. ing of ruminants, the control of cestodes and trematodes usually focus on reducing the numbers of arthropod and Limitations gastropods intermediate hosts in the environment. In Though this study provided useful epidemiological infor- addition, majority of anthelmintics used for chemothera- mation on the prevalence and distribution of endemic hel- peutic control are also classified as anticestodals (e.g. minths in Nigeria, which will be useful in disease control, praziquantel, nitroscanate), antinematodals (e.g. pipera- it is not devoid of limitations. First, there were uneven zine, tetrahydropyrimidines) and antitrematodals (e.g. distributions of studies across states, regions, hosts, study benzimidazoles, salicylanides) for these phylogenetic period, study types and sample sizes, This implies that the classes [61–63]. findings may not accurately represent the situation for Three diagnostic methods (macroscopy, microscopy Nigeria. Another setback is the fact that despite the distri- and serology) were employed by the 44 studies analyzed. bution of eligible studies across the six Nigerian regions, Macroscopy was used basically for the gross identification studies were published from only nineteen of the thirty- of cystic conditions caused by larval stages of cestodes like six states. C. bovis and hydatid cyst as well as adult helminths like Fasciola spp. Microscopy was used for the identification Conclusions of helminth eggs while serology was used for antigen/ Helminths of veterinary and medical importance are antibody detection. Though all these techniques are prevalent in Nigeria with overall PPE of 7.48%. There was valuable in the diagnosis of helminth infections, they a 43.3% decline in the pooled prevalence of helminths are not without limitations. While macroscopy may over a period of 13 years. The highest pooled prevalence easily miss non-prominent lesions during gross examin- estimates were observed in the South-western region and ation of tissues, sample preparation for microscopy may among cattle. Strongyloides papillosus was the most preva- be time-consuming, labour intensive and requires expert- lent of all the helminths while Fasciola gigantica had the ise. Serology which is the most sensitive and specific of widest geographical distribution across Nigeria. High de- these three diagnostic techniques is associated with false grees of heterogeneity were observed within studies and positive results and is limited to the detection of only few different strata. On-farm good agricultural practices in- helminth species. These limitations may contribute to the cluding effective strategic deworming of livestock accord- low prevalence observed and the inability of some of the ing to parasites’ seasonality and abundance, ranching studies to identify helminths to the species level. Due to instead of nomadism, standard veterinary meat inspection these deficiencies, highly sensitive and specific molecular and adequate hygiene and sanitation in abattoirs and live- techniques earlier described [64–67] may provide a better stock markets will reduce the economic, public health and understanding of the status of helminths parasites in veterinary threats caused by these parasites. Nigeria. The findings of this study have several implications. Looking from the epidemiological point of view, the de- Additional files tection of helminths in congregations of livestock like markets may suggest possible increased risk of transmis- Additional file 1: Multilingual abstracts in the five official working languages of the United Nations. (PDF 251 kb) sion of these parasites as majority of farmers buy these Additional file 2: Preferred Reporting Items for Systematic Review and animals from the markets and introduce them into their Meta-Analysis (PRISMA) checklist. (DOC 62 kb) herds without any veterinary care. On the other hand, Additional file 3: List of studies excluded from the meta-analysis. the presence of these helminths in ruminants on farms (DOCX 19 kb) may probably cause contamination of grazing pasture and sources of drinking water for these animals resulting Abbreviations in new foci of infections. There are obvious public health AJOL: African Journals OnLine; C: Cattle; CI: Confidence interval; FCT: Federal implications of finding zoonotic helminths like hydatid Capital Territory; G: Goat; HVI: Helminths of veterinary importance; HZI: Helminths of zoonotic importance; I : Inverse variance index; cyst, Cysticercus bovis, Fasciola gigantica and Oesophagos- MOD: Method of diagnosis; PPE(s): Pooled prevalence estimate(s); tomum spp. among others in ruminants. These include Prev: Prevalence; PRISMA: Preferred Reporting Items for Systematic Review and the risk of environmental contamination that may re- Meta-Analysis; Q: Cochran’s heterogeneity statistic; Q-P: Cochran’s P-value; RN: Reference number; S: Sheep sult in human infections or of acquiring such infec- tions through the consumption of slaughtered food Acknowledgements animals that enter the food chain. These parasites are The authors are grateful to the Editor-In-Chief of the Nigerian Journal of associated with different conditions in humans ran- Parasitology for making available some of the articles included in the ging from diarrhoea, retarded growth, intellectual and meta-analysis. Karshima et al. Infectious Diseases of Poverty (2018) 7:52 Page 13 of 15 Availability of data and materials 18. Ibukun AV, Oludunsin F. Prevalence of intestinal helminths and protozoa The data supporting the conclusion of this article are all included within the parasites of ruminants in Minna, north-central, Nigeria. IOSR J Agric Vet Sci. article and Additional files 2 and 3. 2015;8(2):62–7. 19. Odeniran PO, Jegede HO, Adewoga TOS. Prevalence and risk perception of adult-stage parasites in slaughtered food animals (cattle, sheep and goat) Authors’ contributions among local meat personnel in Ipata abattoir, Ilorin, Nigeria. Vet Med Anim SNK: Conceived and designed the study, SNK, BVM, JKPK: Conducted Sci. 2016;4(1):1. comprehensive literature search, screened literatures and extracted data, 20. Biu AA, Ahmed MI, Mshelia SS. Economic assessment of losses due to SNK: Carried out statistical and meta-analysis, SNK: wrote the paper. All authors parasitic diseases common at the Maiduguri abattoir, Nigeria. Afr Sci. 2006; read and approved the final version of the manuscript. 7(3):143–5. 21. Danbirni S, Ziyauhaq H, Allam L, Okaiyeto SO, Sackey AKB. Prevalence of Ethics approval and consent to participate liver condemnation due to fascioliasis in slaughtered cattle and its financial Not applicable. losses at Kano old abattoir, Nigeria. J Vet Adv. 2015;5(6):1004–9. 22. Karshima NS, Bata SI, Bobbo AA. Prevalence, risk factors and economic Competing interests losses associated with fasciolosis in slaughtered cattle in Bauchi, North- The authors declare that they have no competing interests. Eastern Nigeria. 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Infectious Diseases of PovertySpringer Journals

Published: May 29, 2018

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