Zoonotic diseases directly affect animals and humans, and can also be transmitted between animals and humans. The etiologic agents of zoonoses include bacteria, viruses, fungi, and parasites . The mode of transmission also varies. While some of the pathogens are vector-borne, others are transmitted via aerosol, direct contact through body fluids, contact with inanimate objects (fomites), or food-borne (including water borne). Zoonotic diseases are usually associated with pets (dogs and cats), livestock (cattle), domestic birds, and other vertebrate pests of human dwellings (rats) [2–4].
The unusual changes in the interactions between humans, animals, and the environment that are caused by climate change, increase in global migration, and international trade drive an increased risk of emerging health threats across the globe [5,6]. Greater than one-half of existing infectious diseases are zoonotic and up to 75% of emerging infections can be traced to animal origins . This finding implies that as the overall prevalence of infectious diseases declines among the human population, more animal pathogens adapt to human systems.
Although zoonoses can be transmitted by both wild and domestic animals (livestock and pets), geographic regions with a high density of livestock keepers have a high potential for zoonoses transmission and are so regarded as zoonotic “hotspots” . Nigeria ranks second in the global ranking of countries harbouring poor livestock keepers. Moreover, Nigeria also ranks first among countries with the highest prevalence of endemic zoonoses .
Parasites (helminthes and protozoans) account for more zoonotic diseases among mammals than bacteria or viruses . Despite mass drug administration (MDA) and parasite eradication campaigns, many parasitic zoonoses of public health and veterinary importance continue to cause significant morbidity and mortality worldwide [9,10]. Among parasites, enteric parasites, which are mostly transmitted through ingestion, account for a greater zoonotic burden ; however, enteric parasites receive disproportionately less attention from public health officials .
Ungulates are the most important non-human host of zoonotic pathogens. In fact, ungulates harbour more zoonotic pathogens and are responsible for more of the emerging and re-emerging zoonotic species . Cattle are one of the most common domesticated ungulates. Cattle provide essential sources of meat, milk, other dairy products, manure for crops, clothing, and animal traction. These products and services continue to be vital in the lives of the most economically-challenged humans because cattle are often an important source of food security and revenue.
People who engage in extensive mobile livestock production involving grazing and the use of water across a rangeland as their livelihood are known as pastoralists . Pastoralists share the environment with their livestock, often in large numbers, that requires an occupational interaction . The close interaction between cattle pastoralists, cattle, and cattle products, such as milk and cheese, provides the best opportunity for zoonotic disease transmission [15,16].
The Upper Benue Trough in the Adamawa State of northeastern Nigeria is one of the major pastoralist activity centres in Nigeria. Although a few studies have separately evaluated zoonotic diseases among livestock  and humans  around the Upper Benue Trough, none has reported on concurrent zoonotic diseases or pathogens among humans, animals and/or the environment in the Upper Benue Trough.
Documentation of the zoonotic enteric parasite (ZEP) distribution, which included Entamoba spp., Cryptosporidium spp., Giardia intestinalis, Fasciola spp., Taenia spp., and Trichostrongylus spp. among humans, livestock, and the environment in the current study, is important for an objective appraisal of the ZEP burden and will form the basis for developing more effective integrated intervention programmes towards addressing human and veterinary health within the concept of One Health. We report herein the distribution of and correlation between ZEPs among pastoralists, cattle, and soil with respect to geography and other socio-demographic variables within Adamawa State segment of the Upper Benue Trough.
MATERIALS AND METHODS
The Upper Benue Trough in Adamawa State is one of the most notable livestock zones in Nigeria. Nomadic, semi-nomadic, and sedentary pastoralists occupy several rural communities and temporary camps scattered in almost all localities within and near the Benue and Gongola River valleys. Cattle are the principal livestock of the pastoralists, although pastoralists also engage in raising small ruminants and birds. The sedentary or semi-sedentary pastoralists also engage in some small-scale crop cultivation around their dwellings.
This study focused on the cattle pastoralist communities in Demsa, Girei, and Yola South local government areas (LGAs), all of which are located within Adamawa State segment of the Upper Benue Trough. The study area is located between latitudes 9.187465°N and 9.593930°N, and between longitudes 12.023074°E and 12.555911°E (Fig 1). Although the estimated combined population of the 3 LGAs is 724,100 , there is no data on the population of pastoralists in the study area. It has been estimated, however, that Adamawa State, which has an estimated population of 4.2 million, harbours approximately 450,000 cattle pastoralists . The cattle population in the State has also been estimated at 3.3 million .
Study site, population, and environmental samples
Twelve accessible pastoralist communities were purposively selected based on the consideration that they would yield an adequate number of participants to meet the required sample size. The selection was also done in such a way to generate a relatively proportionate representation of the Fulani clans (Kiri, Uda, Bodi’en, Jahun, and Wiiti), husbandry practices (nomadic, semi-nomadic, and sedentary), and spread across the three LGAs around the trough. The study covered two sets of population groups (human [cattle pastoralists] and livestock populations [cattle in possession of the pastoralist]). The environmental samples reported here are soil samples collected from the pastoralist homes.
Sample and sampling technique
Surveys system (www.systemsurveys.com), a web-based sample size calculator by Creative Research Systems , was used to calculate the sample size with an assumed population of 100,000 pastoralists in the 3 LGA included in the study. At a 95% confidence level and confidence interval of 5, the required sample size was 383. This sample size estimate was further increased to target 500 to compensate for anticipated data inconsistencies and allow for some degree of stratification during the analysis. The same sample size was targeted for the cattle population.
Owing to the small populations of the selected settlements and frequent absenteeism of some household members at the time of data collection, a complete coverage of selected communities was adopted. All members of eligible households who consented or assented (in the case of minors) were included in the survey.
Based on availability, cattle faecal samples were collected from five cattle from the herd of each household included in the survey. Home soil was also collected from each participating household.
The survey data collection entailed administration of a structured questionnaire (reported elsewhere), faecal sample collection from human participants and cattle subjects, and collection of soil samples. All tools and procedures for data collection were pilot-tested in a pastoralist community (not included in the main study) prior to the actual data collection exercise.
Stool sample collection
A labelled, sterile, stool sample container was given to each member of the eligible household, who consented to providing the stool sample and the procedure for collection of the stool was described to the participant or caregiver. The stool samples were collected by the team the next day so that the samples did not remain in possession of the participants. The demographic details of each participant were documented under the same identifier as the sample container label given.
Targeting the same sample size as for humans and assuming an average household size of five in Nigeria, stool samples were collected from five cattle from the herd of each household. Cattle inclusion in sampling was based on the availability of faeces around the anal/rectal area or freshly voided faeces during the time of field visits by team members. An approximate 10-gram faecal sample was collected into a labelled container directly from the rectum or at the time a cow or bull was defecating, the freshly voided droppings were carefully collected immediately in such a way that averted contamination. The animal’s sex, age, and other cattle identifiers were also documented to correspond with the label on the respective sample containers.
All faecal samples were preserved in 10% formalin immediately after retrieval and conveyed to the Infectious Diseases of Poverty Laboratory at Modibbo Adama University in Yola for storage. Faecal samples were stored in the refrigerator at 4° Celsius in the laboratory until processed for microscopy. Environmental samples were kept at room temperature.
Soil sample collection
Home soil samples were collected in each household at a place adjudged to have most contact with humans (i.e., the children’s playground). Approximately 50 grams of topsoil (3 cm deep) was collected at 1 spot per household using a clean hand trowel and the sample was placed in a clean polythene bag for further laboratory processing.
Preparation of samples
Preserved faecal samples from humans and cattle were similarly processed using a formalin-ether sedimentation technique (mainly for detection the of helminthe eggs, but not ignoring protozoan ova and cysts), then a zinc sulphate floatation technique for the detection of protozoan ova and cysts, as described by the World Health Organisation  with modifications adopted from Arora & Arora . Two smears were made from each floatation preparation. One of the smears was directly examined and the other smear was negatively-stained with malachite green. To enhance detection of Cryptosporidium spp., malachite green stain was prepared by dissolving 5 grams of malachite green in 100 ml of distilled water and stirring for 30 min. The solution was filtered to remove any undissolved crystals. The filtrate was then used for staining smears by placing a drop on the slide and mixing with the sample prior to examination. Although Taenia spp. eggs are not normally found in cattle faecal samples, no specific technique was used for detection of cysticercosis in cattle.
Approximately 50 grams of soil sample was immersed in distilled water and filtered through a strainer with 500-μm pores to remove large particles. The filtrate was allowed to passively sediment overnight in a straight-sided container. A portion of the supernatant was decanted until approximately 10 ml of the content at the base of the container. The content was swirled and transferred into a 15-ml centrifuge tube. The content was centrifuged at 2000 rpm for 2 min. After centrifugation, the supernatant was decanted and the sediment was kept in a rack to settle. The sediment was subsequently agitated by shaking and apportioned as follows: one portion was examined after formalin-ether sedimentation; and the other portion was used for the zinc sulphate floatation procedure. The portion for flotation was further aliquoted; one aliquot was examined directly and the other aliquot was stained with malachite green, as described for stool samples.
Faecal and environmental sample microscopy
Each smear (the formol-ether sedimentation preparation, and the stained and unstained smears of the zinc sulphate floatation preparations) was examined under a light microscope at 10X, 40X, and 100X by 2 investigators. In cases in which the results of the same specimen from the two investigators disagreed, a third more experienced investigator examined the slide and adjudicated on inconsistencies. The results were documented on data forms.
Data collected was entered into EpiData (www.epidata.dk) and analysed using IBM-SPSS 20 (IBM). Simple percentages were used to present the infection prevalence and the distribution across socio-demographic variables (community, gender, age group, clan and husbandry practice). A chi-square test was used to determine the association between ZEP infections and socio-demographic variables. The Pearson correlation was used to measure the direction and degree of correlation between the distribution of ZEP infectiosn among human cattle and soil across communities.
Stool samples and demographic information from 504 human participants across 12 pastoral communities were analysed (Table 1). The participants included 50.4% males and 49.6% females of different ages (range, 6 months-59 years), and 5 Fulani clans (Kiri, Jahun, Bodi’en, Uda, and Wiiti) who engage in nomadic, sedentary, or semi-sedentary husbandry practices (Table 2). Faecal samples were also collected from 599 cattle (40.1% males and 59.9% females) between 4 months and 9 years of age across the same 12 communities in 3 LGAs. Soil samples were collected from 114 homes in the 12 communities that were included in the study (Table 1).
|Community||Number of human participants (%)||Number of cattle sampled (%)||Number of home soil samples (%)|
|Bilingo||62 (12.3)||55 (9.2)||11 (9.6)|
|Yolde||60 (11.9)||54 (9.0)||10 (8.8)|
|Lugga||11 (2.2)||18 (3.0)||3 (2.6)|
|Gindin Dutse||27 (5.4)||50 (8.3)||8 (7.0)|
|Veterinary||18 (3.6)||39 (6.5)||6 (5.3)|
|Wuro Ardo Yerima||48 (9.5)||65 (10.9)||13 (11.4)|
|Wuro Ardo Saleh||64 (12.7)||78 (13.0)||16 (14.0)|
|Wuro Nduroi||40 (7.9)||34 (5.7)||7 (6.1)|
|Yolde Ginnaji||67 (13.3)||89 (14.9)||16 (14.0)|
|Yolde Na'i||53 (10.5)||39 (6.5)||8 (7.0)|
|Changala 1||36 (7.1)||45 (7.5)||9 (7.9)|
|Changala 2||18 (3.6)||33 (5.5)||7 (6.1)|
|Total||504 (100.0)||599 (100.0)||114 (100.0)|
|>2 but <5 years||209||34.9|
|5 years & above||215||35.9|
Distribution of ZEP infections
The distribution of ZEP infection among humans, cattle, and soil across the study communities
The ZEP infections in the study included Cryptosporidium spp. (prevalence of 14.1% in humans, 17.9% in cattle, and 37.7% in soil), Entamoeba spp. (prevalence of 12.3% in humans, 14.9% in cattle, and 24.6% in soil), Giardia intestinalis, (prevalence of 12.1% in humans, 14.9% in cattle, and 31.6% in soil), Fasciola spp. (prevalence of 1.8% in humans, 6.3% in cattle, and 3.5% in soil), Taenia spp. (prevalence of 3.0% in humans, 0.5% in cattle, and 7.0% in soil), and Trichostrongylus spp. (prevalence of 3.2% in humans, 6.7% in cattle, and 8.8% in soil).
The overall prevalence of ZEP infections among humans in the study area was 40.3%. The prevalence in Yolde Na’i (54.7%) was the highest, followed by Changala I, (52.8%); Gindin Dutse was shown to have the lowest ZEP infections at 29.6%. The overall prevalence of ZEP infections were not significantly different across communities (P=0.05; Table 3). Among cattle, the overall prevalence of ZEP infections was 48.2% and the highest prevalence of ZEP infections was recorded in Lugga (66.7%), while the lowest prevalence of ZEP infections was in Gidin Dutse (34%). Overall, the prevalence of ZEP infections was significantly different across communities (P=0.05; Table 3). The overall prevalence of ZEP infections in home soil samples was 74.6%, with the highest community prevalence of ZEP infections at 100% in Lugga and the lowest prevalence of ZEP infections at 54.3% in Bilingo. The prevalence of ZEP infections in home soil was not significantly different across communities (P=0.05; Table 3).
|Community||Prevalence of ZEPs|
|Among humans||Among cattle||In home soil|
|Number examined||% positive||Number examined||% positive||Number examined||% positive|
|Wuro Ardo Yerima||48||37.5||65||50.8||13||92.3|
|Wuro Ardo Saleh||64||45.3||78||55.1||16||87.5|
|P value (X2 test)||0.134||0.025*||0.390|
*= significant at a P=0.05.
Distribution of ZEP infections by gender, age group, clan, and husbandry practice
Of the 504 participants examined, 42.1% were males and 38.4% were females; however, the difference in prevalence between male and female participants was not statistically significant (P=0.05). Participants < 5 years of age had the highest prevalence of ZEP infections (50%), while the group 40-59 years of age had the lowest prevalence of ZEP infections (21.4%). A chi-square test showed that the prevalence of ZEP infections was significantly associated with age group (P=0.005). With respect to the 5 clans included in the study, the prevalence of ZEP infections differed significantly across clans, as follows: Bodi’en, 52.1%; Wiiti, 45.5%; Jahun, 44.6%; Uda, 39.2%; and Kiri, 30.5%. The pastoralists with a semi-nomadic husbandry practice had the highest proportion of ZEP infections (41.1%), followed by the nomadic and sedentary practices (40% and 35.4%), respectively (P =0.005; Table 4). With respect to cattle subjects, The difference in prevalence of ZEP infections between males (52.1%) and females (45.7%) was not statistically significant; however, the prevalence of ZEP infections in younger cattle (≤ 2 years of age) was significantly higher (62.9%) than the older category (>2 and < 5 years of age) which had a ZEP infection prevalence of 49.8%. Cattle that were ≥ 5 years of age had the lowest prevalence of ZEP infections (34.9%; Table 4).
|Variable/values||Number enrolled||% positive||P value (X2 test)|
|>2 but <5 years||209||49.8|
|5 years & above||215||34.9|
*= significant at a P=0.05; **= significant at a P=0.005.
Correlation between ZEP infections among humans, cattle, and soil
Pearson correlation analysis was performed to determine the correlation between the prevalence of ZEP infections in humans and cattle within the study area. There was a strong positive correlation (R = 0.750) between the overall prevalence of ZEP infections among humans and cattle with respect to the study communities (P=0.005; Fig 2).
Bivariate Pearson correlations between the prevalence of specific ZEP types among humans and cattle were also analysed (Fig 3). Figure 3(A) shows a strong positive correlation (R=0.770) between Cryptosporidium spp. among humans and cattle in the studied communities (P=0.005). Figure 3(B) also shows a very strong positive correlation (R = 0.840) between Entamoeba spp. among humans and cattle in the studied communities at the 99.5% confidence level. Similarly, Fig 3(C) shows a very strong positive correlation (R =0.902) between G. intestinalis among humans and cattle across the study communities at the 99.5% confidence level. Figure 3(D) also shows a strong positive correlation (R =0.706) between Fasciola spp. among humans and cattle across the communities at the 95% confidence level. Figure 3(E) shows a very strong positive correlation (R = 830) between the prevalence of Taenia spp. among humans and among cattle across the study communities (P = 0.001). Also, Fig 3(F) shows a weak positive correlation (R = 0.260) between the prevalence of Trichostrongylus spp. among humans and cattle in the study communities; the correlation was not statistically significant (P=0.05; Fig 3).
The bivariate Pearson correlation between the prevalence of ZEP infections among humans and home soil was moderately positive (R = 0.484), but not statistically significant (P = 0.05). There was a strong positive correlation (R = 0.677) between the prevalence of ZEP infections among cattle and home soil samples (P = 0.05; Fig 4). A multivariate representation of the correlation between the prevalence of ZEP infections in 3 sample categories (humans, cattle, and home soil) also showed a significant (P = 0.005), strong positive correlation (R = 0.750; Fig 5).
Six ZEPs were identified across human participants, cattle, and soil samples in the study area. The overall prevalence of the parasites was within the ranges of findings from similar studies conducted in Nigeria. Specifically, a review of the intestinal parasite prevalence among human populations in Nigeria reported the overall prevalence of intestinal helminthes was approximately 40% . A study of intestinal parasites among school children in Rivers State of Nigeria found an overall prevalence of 27.4% , while a similar study in Oshodi of Lagos State reported an overall prevalence of 58.3% . A study in the Plateau State of central Nigeria determined that the prevalence of gastrointestinal parasites among cattle was 46% ; however, several other studies have reported a prevalence of 70%-100% in different parts of Nigeria [29–31]. In another study conducted among pastoral Fulani in the Zamfara State of Nigeria, the prevalence of gastrointestinal parasites was 67% .
The most prevalent ZEP among humans was Cryptosporidium spp., followed by Entamoeba spp. and Giardia intestinalis (14.1%, 12.3%, and 12.1% respectively). This order of prevalence is similar, but with a relatively narrower disparity to a study among children in Lagos, in which the prevalence of the parasites were 17.1%, 9.5%, and 4.8%, respectively . It is noteworthy that similar trends in the prevalence of ZEPs were found among cattle and other environmental samples. The similarity in prevalence of different ZEPs across different study samples can be regarded as a subtle indicator of zoonotic transmission. The least prevalent ZEP in the study was Fasciola spp., with a prevalence much higher in cattle (4.7%) than humans (1.8%). The difference in the prevalence can be explained by the fact that the transmission of Fasciola spp. requires an aquatic intermediary host (the snail). Moreover, the infective stage (cercariae) is usually found on aquatic vegetation where the infective stage is much more likely to be ingested by cattle than by humans. For cattle, because only faecal samples were examined, the proper diagnostic method for Taenia spp. was not carried out and hence only 3 (0.5%) of the faecal samples were shown to be positive for Taenia spp. Because Taenia spp. is not known to lay eggs in its intermediate host (cattle) the few Taenia eggs detected in cattle faecal samples might be attributable to contamination during collection, processing, or some non-viable ingested egg passing through the faeces.
There was a strong positive correlation (R=0.750; P<0.005) between the overall prevalence of ZEP infections among humans and cattle across the study communities. Similar trends of correlations in prevalence were also observed with respect to all but one (Trichostrongylus spp.) of the parasite types. This finding is a strong indicator of an ongoing zoonotic transmission of the parasites.
Although the positive correlation between the prevalence of ZEP infections among humans and in home soil across communities was only moderate (R = 0.484) and not statistically significant (P = 0.05). The positive correlation between the prevalence of ZEP among cattle and home soil was strong (R = 0.677) and statistically significant. Also, the multivariate correlation involving the prevalence of ZEP infections with respect to the three sample categories (humans, cattle, and home soil) was also strongly positive (R = 0.750) and statistically significant (P = 0.005). These positive correlations of prevalence, which were stronger between humans and cattle than between humans and soil or cattle and soil, further strengthens the indication that there is an ongoing zoonotic transmission of ZEPs in the study area.
The current study showed that the prevalence of ZEPs in all the three categories of samples collected from the study area were moderately high in relation to reported prevalence in similar settings. The prevalence of ZEP infections was 40.3% among humans, 48.2% among cattle, and 74.6% in home soil. Although the prevalence of ZEP infections across communities was not markedly the same for each of the sample categories, the differences across communities were not statistically significant, except among cattle in which some slightly significant difference was observed (P = 0.05).
There was a strong positive correlation between prevalence of ZEP infections among humans and cattle (R=750), and between cattle and soil (R=677) across the study communities. This finding strongly suggests ongoing zoonotic disease transmission in the study area.
Efforts to control infectious diseases, and more specifically zoonoses among pastoralists should consider integrated approaches that attend to livestock health as well because many of the pathogens are shared between humans and livestock.
Further research should explore the strengthening of evidence for ongoing zoonotic disease transmission by determining the genetic associations between zoonotic infectious agents in humans and cattle. Further research with a different or broader scope to include zoonotic infections other than enteric parasites will also be useful in highlighting the extent of the problem.