Epidemiology of gastrointestinal parasites of cattle from selected locations in Southern Ghana

S A Squire, H Amafu-Dey and J Beyuo

Animal Health and Food Safety Division, Council for Scientific and Industrial Research-Animal Research Institute,
P. O. Box AH 20, Achimota, Accra, Ghana
sylbinedu@yahoo.com

Abstract

A cross-sectional study was conducted to establish the prevalence and intensity of gastrointestinal parasites of cattle from two institutional farms located in the Coastal Savanna and Transitional zones of Southern Ghana. A total of 309 (different ages, sex and breed) faecal samples were examined using the McMaster and sedimentation techniques.

Overall, the cattle showed a very high prevalence (95.5%) of parasite infections. Out of this percentage, 75.1% had multiple parasites whiles 20.4% had a single parasite infection. Prevalence of Strongyles (63.1%) was highest, followed by Fasciola (51.1%), Dicrocoelium (39.8%), Eimeria (29.4%), Paramphistomum (25.9%), Schistosoma (21.7%), Ascaris (6.1%) and then Moniezia (2.3%). Strongyles, Ascaris, Moniezia and Eimeria infections were significantly higher (p<0.05) in the calves (0-12 months old) whiles Fasciola, Paramphistomum, and Schistosoma infections were higher (p<0.005) in the adults (>24 months old).  In general, most of the animals had low intensity (<500EPG / <10EPC) of infection. There was a wide range of nematodes, cestode and protozoa egg counts (0-47200 OPG, 0-40200 EPG and 0-246000 EPG, respectively). The range of trematodes egg count was 0-52EPC. A wide variety of gastrointestinal parasites were prevalent among cattle in the study area. For effective treatment and control, the variability of parasites would have to be considered. Also, further studies on gastrointestinal parasites dynamics, distribution and impact are proposed.

Key words: coastal savanna zone, intensity, prevalence, transitional zone

Introduction

Cattle forms an integral part of the livestock industry in Ghana, for the purpose of mainly beef and in some cases milk production (Okanta 1992). In some communities, cattle are also used as a source of labour for farming. Thousands of metric tons of beef, milk and pieces of hide are produced from cattle in the country (FAO 2009).These produce are, however, inadequate and hence several live cattle and tons of beef are imported to meet local  demands (VSD 2010).There are about 2,750,185 cattle in the country (GSS 2008).

The extensive system being the main management practice is based mainly on extensive grazing by mostly smallholder herders. The commercial and state institution farms practice varying levels of management systems that are higher than the extensive system (Oppong-Anane et al 2010). In this higher level of practice, cattle may graze on sown pastures as well as natural pastures. All these systems however expose the animals to several diseases including parasitic infections.

Parasitic diseases constitute a major impediment to livestock production in Sub-Saharan Africa; owing to the direct and indirect losses they cause (Harper and Penzhorn 1999; Kagira and Kanyari 2001). The parasites decrease animal production and may cause death (Lebbie et al 1994). In tropical and sub-tropical regions where marginal levels of nutrition exacerbate the detrimental effects of infection, animal deaths due to nematode infections are very common (Ademola and Eloff 2010).The trematodes, cestodes and protozoans are also important parasites that affect ruminant livestock. Some of these are zoonotic and therefore a threat to public health.

In Ghana, gastrointestinal parasites are among the main causes of losses in livestock. An analysis of the conditions diagnosed in 464 sheep of all ages over a 6-year period on the University of Ghana Agricultural Research Station, Nungua, has shown that most deaths (67%) occurred in the 1-6 months age group and that pneumonia, followed by tapeworms and parasitic gastroenteritis, were the main conditions diagnosed (Oppong 1972). Several studies have therefore been conducted on some epidemiological and control aspects of gastrointestinal parasites for effective control measures in mostly sheep and goats (Agyei et al 1991; Agyei 1997; Agyei 1998; Agyei and Ampomah 2001; Agyei 2003; Agyei 2007). Not much, however, has been done with respect to gastrointestinal parasites in cattle.

In the 1960s, Fasciola and Dicrocoelium were found in the liver of cattle from slaughter houses in the northern part the country (Odei 1966). Later, Agyei (1991) made epidemiological observations on helminth infections in calves from Southern Ghana. He reported the presence of Toxocara vitulorum, Strogylates, Strogyloides papillosus and Moniezia benedini in the calves. To complement these findings, this study sought to establish the prevalence of gastro-intestinal parasites in different age groups of cattle and the intensity of the parasites’ infection.

Materials and methods

Study area

The study was conducted at two state institutional farms with similar management systems. The farms were located at Pokuase (latitude 5^o 41´N, longitude 0^o 17´W) and Fafraha (latitude 5^o 43´N, longitude 0^o 08´W) in Southern Ghana. Pokuase is in the forest-coastal savannah transition zone with mean monthly temperature and rainfall of 23.3^oC to 24.7 ^oC and 12.6 mm to 204.6 mm, respectively. The drier Fafraha in the coastal savannah zone had mean monthly temperature and rainfall of 25.7 ^oC to 29.2 ^oC and 0 to 205.7mm, correspondingly. The mean annual temperature at Fafraha (27.7 ± 0.4 ^oC) was higher as compared to Pokuase (24.2 ± 0.1 ^oC) during the period of study. Climatic data was obtained from the Ghana Meteorological Services Department in Accra.

Study population

The study population was made up of 309 cattle (male, 18.1% and female, 81.9%, respectively) of different stages of maturity and breed. The herds were kept in kraals during the early hours of the morning and throughout the evening. The animals grazed on natural pastures supplemented with cultivated pastures during the day. Selective monthly deworming was targeted at the calves (0-12 months old) and sick when needed. The animals were categorised into three age groups: 0-12 months (21.7%), 13-24 months (14.9%) and >24 months (63.4%). The herd consisted of three main breeds; indigenous Ndama (28.2%), Sanga (34%), and Friesian-Sanga crossbreed (37.9%). The Ndamas were located at the Pokuase farm whiles the Sangas and Friesian-Sanga crosses were located at the Fafraha farm.

Sample collection and analysis

Fresh fecal samples were collected per-rectum using sterile plastic gloves from the 309 cattle in a cross sectional study conducted between June and July 2009. The samples were placed in suitable leak-proof plastic containers, tightly closed, labeled and transported to the laboratory for examination.

The fecal samples were examined macroscopically for their consistency as watery, loose, soft or formed and then categorized as either diarrheic or non diarrheic. The sedimentation and floatation technique as described by MAFF (1986) was used to detect the presence of nematode, cestode and trematode eggs, and coccidian oocysts in the samples. Morphological and colour differences were used to distinguish various eggs.

The intensities of nematode and cestode eggs infections were categorized by egg per gram of faeces (EPG) and coccidial infections by oocysts per gram of faeces (OPG) as observed under the x10 microscope objective. The intensity of trematode eggs was however qualitatively classified as egg per long cover slip (EPC). For the purposes of analysis, infections of nematodes, cestode and protozoa (coocidia) in animals were classified as low (< 500 EPG/OPG), moderate (500 - 2000 EPG/OPG) and High (>2000 EPG/OPG) as described by Obonyo et al (2012). Trematode infections were also classified as low (<10EPC), moderate (10-20 EPC) and high (>20 EPC).

Statistical analysis

Animal and laboratory data were analyzed using SPSS 15.00 for Windows (SPSS, 2006). The prevalence of each parasite infection was calculated as the number of animals’ diagnosed positive for a given parasite divided by the total number of animals examined at the particular time (Thrusfield 2005). Chi-square statistics (χ2) was carried out to determine the association of the explanatory variables (sex, age, breed, location of farm and stool/faeces consistency) with the prevalence of parasites. The egg/oocyst count was described in terms of mean, range (minimum and maximum) and standard error of mean. T-tests were performed to compare climatic data. In all the analysis, confidence level was held at 95%, and p<0.05 was set for significance.

Results

Climatic condition

Sampling was done during the major raining or wet season. The mean annual rainfalls (61.7 ± 15.5mm and 54.7 ± 18.2mm) and number of raining days (6.1 ± 1.1days and   4.6 ± 1.2days) for Pokuase and Fafraha farms, respectively were not significantly different (p>0.05) . However, the mean annual temperature at the Fafraha farm (27.7 ± 0.4 ^oC) was significantly higher (p<0.001), compared to that of Pokuase farm (24.2 ± 0.1 ^oC). The major raining season peaked in June during the year. Climatic data for the period of sampling (June and July) indicated the following means; rainfall (205.2 ± 0.5 and 155.7 ± 50.0; p<0.05), number of rain days (10 ± 2 and 12 ± 5; p>0.05) and temperature (24.2 ± 0.4^oC and 26.5 ± 0.6 ^oC; p>0.05) at Pokuase and Fafraha farms respectively.

Overall prevalence of parasites in cattle

Overall, 95.5% of the 309 animals sampled shed helminth eggs and/or coccidia oocysts. Table 1 shows the overall prevalence of gastro-intestinal parasites in the different age groups, sexes, locations, breeds and stool consistencies of cattle. The prevalence was high (98.5%, 97.8% and 94.9%) among all the age groups (0-12 months, 13-24 months and >24 months old, respectively). A similar trend was observed among the various sexes (male and female) and locations (Pokuase and Fafraha) of cattle. The prevalence was also high among both animals with diarrheic stool (93.2%) and normal stool (96.0%). Among the differnt breeds of cattle, the prevalence was highest (p<0.05) in the Ndama (98.9%) followed by the Sangas (97.1%) and then the Friesian Sanga crossbreeds (91.5%).

Prevalence and intensity gastrointestinal parasites

Six varieties of parasites were observed during faecal examination. Out of the 95.5% of animals positive, 75.1% of them had multiple parasites eggs sp, while 20.4% had a single parasite infection. Most of the animals (31.4%) shed eggs from 3 parasites or 2 parasites (27.5%) (Figure1). Only 0.6% of the animals shed eggs from all six gastrointestinal parasite.

Figure 1: Percentage of cattle shedding a given number of parasites

Different classes of parasites (Trematode, Nematode, Cestode and Protozoa) were observed in the faecal examination (Table 2 and 3). The parasites observed were Strongyles (63.1%), Fasciola (51.1%), Dicroceolium (39.8%), Eimeria (29.4%), Paramphistomum (25.9%), Schistosoma (21.7%), Ascaris (6.1%) and Moniezia (2.3%).

Tables 2 and 3 show the intensity of infection with the various parasites. Most of the animals had low infections (<500 EPG/OPG or <10 EPC). The percentage of animals with low infections ranged from 76.7% (Moniezia) to 98.7% (Schistosma). The few animals with severe (>2000 EPG/OPG or >20 EPC) infections ranged from 0 (Schistosoma) to 5.5% (Eimeria).The mean Protozoa (Eimeria) OPG (1273.8±799.8) was high as compared to the other parasites. Among the nematodes, Ascaris showed the highest mean EPG (713.9±269.9) whiles Fasciola showed the highest mean EPC (3.9±0.3) among the trematodes. 

Table 4 shows the prevalence of the various parasites in different categories of cattle. The prevalence of the individual parasites varied significantly (p<0.05) among the various age groups. The prevalence of Strongyles (79.1%), Ascaris (23.9%) and Eimeria (55.2%) was significantly higher (p<0.05) among the calves (0-12 months old) as compared to the older age groups. Moniezia (10.4%) was detected in only calves. In the older animals (>24months), the prevalence of Fasciola (60.2%), Paramphistomum (28.1%) and Schistosoma (28.1%) was significantly higher (p<0.05) than that of the younger animals. There was no significant difference (p>0.05) in the prevalence of Dicrocoelium amongst the various age groups.

In addition, the prevalence of Fasciola, Schistosoma and Eimeria was significantly higher (p<0.05) in the females as compared to the males. The prevalence of Strongyle was however significantly higher (p<0.05) in the males as compared to the females.

There was no significant difference (p>0.05) in infection between animals with diarrhoea (diarrheic) and those without diarrhoea (non diarrheic) (Table 4).

Fasciola was significantly higher (p<0.05) in the animals from Pokuase while Dicroceolium and Schistosoma was significantly higher (p<0.05) at Frafraha (Table 4).

The prevalence of all the trematodes (Paramphistomum, Schistosoma, Dicrocoelium) were highest (p<0.05) in the Sangas, except Fasciola which was highest (p<0.05) in the indigenous Ndamas. Meanwhile, Ascaris and Moniezia were relatively highest (p<0.05) in the Friesian-Sanga crossbreed cattle (Table 4).

Discussion

The current study showed that, cattle from the study area were infected with a wide variety of gastrointestinal parasites including nematodes, cestodes, trematodes and protozoa. The overall prevalence (95.5%) was higher than the prevalence (53.8% and 50.2%) found in similar studies from Nigeria and Ethiopia, respectively (Pam et al 2013; Regassa et al 2006). Majority of the animals in this study had multiple parasites infections, similar to the observations made by Swai et al (2006).

Although cattle in this study were kept under a higher level of management system as described by Oppong-Anane et al (2010), the overall prevalence was high. This could be as a result of high levels parasitic contamination in the pastoral environment and hence for the need for a review of the management system.  In addition, the period of study was in the major raining/wet season during when parasitic infections are relatively high as compared to the dry season. Agyei (1997) observed that, the number of infective larvae on pasture was directly related to the pattern of rainfall but was influenced by the number of raindays in the period. Conversely, most of the animals in the current study recorded low infections (egg counts) as compared to moderate and high infections.

 Among the different age groups, there was no significant difference in the overall prevalence of parasites, despite the fact that calves (0-12 months old) were given prophylaxes (dewormed monthly). Meanwhile, the prevalence of the nematodes (Strogyles and Ascaris), Cestode (Moniezia) and protozoa (Eimeria) was significantly higher in the younger animals and decreased with increasing age group. The high prevalence among the calves could therefore be due to a number of factors including antihelmintic resistance, the quality and dosage of the antihelmintic drug or reinfection. This however needs to be investigated to ensure effective control of the parasites. The trematodes (Fasciola, Paramphistomum and Schistosoma) on the other hand were significantly higher in the adults (>2 years) than the younger animals. The variation in prevalence among the age groups in the present study was similar to the findings by Sadar et al (2006).

The overall parasite prevalence was high in all categories of animals including the various sexes and stool consistencies. Among the sexes, the prevalence of Fasciola, Schistosoma and Eimeria were significantly higher in the females, whiles Strongyle was significantly higher in the males. There reason for this trend is however not clear.  Meanwhile, other studies recorded no association between sex and parasitic prevalence (Fikru et al 2006; Awraris et al 2012).

Although diarrhoea is a main symptom of gastrointestinal parasite infection, there was no significant association between diarrhoea and parasite prevalence in this study. This implies that most of the infected animals were asymptomatic. It could also be as a result of the generally low parasite egg output (EPG/OPG/EPC) by most of the animals.

The overall prevalence among the indigenous Ndama was significantly higher than that of the Sanga and Friesian-Sanga in this study. For the individual parasitic infections however, Fasciola was most prevalent in the Ndama whiles Dicroceolium and Schistosoma were most prevalent in the Sanga. On the contrary, there was no significant difference in the overall prevalence observed at Pokuase and Frafraha despite the fact that the Ndama was kept at Pokuase and the other breeds at Frafraha. This particular finding is therefore inconclusive and needs to be further researched.

The most prevalent parasite was the Strongyles (63.1%) with a mean egg count of 441.8±59.3EPG (ranging from 0 to 8800). The prevalence observed in this study was higher as compared those reported by Swai et al (2006) and Regassa et al (2006) in Tanzania (20.0%) and Ethiopia (47%) respectively. In Ghana, Haemonchus spp., Trichostrongylus spp. and Oesophagostomum spp. were the reported Strongyle genera found cattle (Agyei 1991). Strongyles have been shown to be the most common and economically important gastrointestinal nematodes in Ghana and the tropics (Agyei 1997; Odoi et al 2007).

Fasciola was the second most prevalent (51.1%) gastrointestinal parasite with a mean egg count of 3.9±0.0EPC (ranging from 0 to 30). In comparison, the prevalence in this study was higher than 25.9% from Kenya and 15.4% from Zimbabwe (Mungube et al 2012; Pfukenyi et al 2006). In Ghana, there is insufficient available data on Fasciola infection in livestock. Odei (1966) observed from studies conducted at the slaughter-houses at Wa and other localities in Northern Ghana that only 8.6% of the livers examined were infected with Fasciola. He attributed the low prevalence to restricted number of habitats suitable for the snail host and proposed that as more permanent water-bodies become available the infection may increase. Fasciolosis causes high mortalities especially in small ruminants and calves (Maingi et al 1997, Wamae et al 1998). It also results in losses associated with liver condemnation in slaughtered animals (Kithuka et al 2002, Mungube et al 2006). In Ethiopia, the financial loss due to liver condemnation was estimated to be 106,400 Ethiopian birr (8312.5 USD) per annum (Abebe et al, 2010). Fasciola is also an important parasite in humans (Mas-Coma, 2005).

Dicroceolum (39.8%) with a mean egg count of 3.1±0.3EPC (ranging from 0 to 3) was less prevalent in this study as compared to 66% observed by Ahmadi et al (2010) in Iran. Like Fasciola, not much is known about Dicrocoelium infection among livestock from in Ghana. Odei (1966) in his observations of liver from the abattoir in the North found 58.8% Dicrocoelium hospes infection in cattle. He also found the parasite in the liver of goats. Dicrocoeliasis is mostly asymptomatic, but can in severe cases lead to anaemia and emaciation (Otranto and Traversa 2003). It is one of the leading causes of discarding liver of cattle, sheep and goats for health reasons. Therefore, Dicrocoelium was included in the World Health Organization list of organisms to target with its Food borne Disease Burden Epidemiology Reference Group in 2007 (WHO 2007). The parasite tends to be found in areas that favor the intermediate hosts, such as fields with dry, chalky and alkaline soils (Gideon 2009). 

Eimeria was the only protozoan in this study and had a prevalence of 29.4%. This was close to a prevalence of 26.4% seen in cattle from Nigeria (Pam et al 2013). Eimeria had the highest mean oocyst count (1273.8±799.8OPG) as well as the widest range parasite load (0-246000OPG). From previous studies in this study location, Adjei (2003) reported E. parva, E. pallida, E. faurei, E. ahsata, E. bakuensis, E. intricata, E. granulosa, E. ovinoidalis and, occasionally, E. marsica, E. ovinoidalis in lambs located in the current study area. Eimeria causes coccidiosis in mainly calves and is usually accompanied by diarrhea of varied severity from watery faeces to one containing blood. Dehydration, weight loss, depression, loss of appetite and occasionally death may also be observed in infected animals.

Paramphistomum (25.9%) the next most prevalent parasite after Eimeria had the widest range of egg count (0-52) among the trematodes and a mean of 1.1±0.2EPC. There is very little available data on this parasite in Ghana. Available data include post-mortem reports of 3.87% Paramphistomum cervi in sheep (Oppong 1972). The prevalence observed in this study was lower than 45.3% and 51.1% in native and crossbreed cattle respectively from Bangladesh (Sardaret al 2006). Though the pathogenic importance of the parasite has not been well documented, Kanyari et al (2009) observed that, animals with poor body conditions had higher intensity of Paramphistomum than those with good body conditions.

A prevalence of 21.7% Schistosoma with a mean egg count of 0.8±0.1EPC (ranging from 0-18) was recorded in this study. No data was found on bovine schistosomiasis in Ghana. In Bangladesh, a higher prevalence of 47.5% was reported in cattle by Islam et al (2011). According to De Bont and Vercruysse (1997), about 530 million heads of cattle live in areas endemic for cattle schistosomiasis in Africa and Asia while at least 165 million cattle are infected with schistosomes. This disease is generally chronic in nature and symptoms in majority of animals are insufficient to distinguish the illness from other debilitating infections (De Bont and Vercruysse, 1998).

Ascaris was prevalent in 6.1% of the animals and this was mostly in calves.  Though majority of the animals had low infections, the range of worm load was as wide as 0-47200 EPG with a mean of 713.9±269.9 EPG. The current prevalence was lower as compared to 57% reported by Awraris et al (2012) in Ethiopia. Agyei (1991) found Toxocara vitulorom in his observations in calves from this study area. Toxocara like Ascaris causes ascariasis which results in both direct and indirect losses in animals.

The least prevalent gastrointestinal parasite in this study was Moniezia (2.3%), the only identified cestode. It was found only in calves with a mean egg count of 225.3±148.1, EPG (ranging from 0 to 40200). Comparatively, this prevalence was lower than 8.3% and 9.4% found in native and crossbred cattle respectively by Sadar et al (2006).Moniezia benedini have earlier been observed infections from calves and sheep in the study area (Agyei1991; Agyei2003). The tapeworm is pathogenic and both larval and adult stages suck blood from the digestive system of the host. According to a report by Oppong (1972), tapeworms due to Moniezia expansa were diagnosed in 25% of all deaths in sheep.

In conclusion, gastrointestinal parasites are highly prevalent in cattle from the study area. There was a wide variety of parasites with most animals having multiple parasite infections. The gastrointestinal parasites have economic significance and some are also zoonotic. It is necessary to further determine the infection dynamics of these parasites especially the trematodes for effective control measures. It is also recommended that the economic impact of these parasites on livestock production in Ghana should be established. In addition, it is necessary to assess the current control strategies to improve production.

Acknowledgement

The technical assistance provided by Mr. Emmanuel Pappoe and Mr. Tobias Bonzi of CSIR-Animal Research Institute parasitology laboratory is highly appreciated. The authors are also grateful to the cattle herds’ men and the management of the above mentioned institutes.

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Received 27 April 2013; Accepted 1 June 2013; Published 1 July 2013

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