Livestock Research for Rural Development 18 (8) 2006 Guidelines to authors LRRD News

Citation of this paper

Prevalence of gastro intestinal parasite infections in Maasai cattle in Ngorongoro District, Tanzania

E S Swai, P F Mtui, A N Mbise, E Kaaya, P Sanka, P M Loomu*

Veterinary Investigation Centre, PO Box 1068, Arusha, Tanzania
pfmtui@yahoo.com   /   emasw@yahoo.co.uk
* District Veterinary Office, PO Box 1, Loliondo, Tanzania

Abstract

A survey of the prevalence of gastro-intestinal tract (GIT) parasite in grazing ruminants (cattle) was conducted in pastoral farming area during the period of March 2004. Data were gathered from 17 herds/farms with a total of 90 cattle in five wards (Sale, Pinyiny, Malambo, Olpiro and Digodigo) of Ngorongoro district. Coccidian oocyst, nematodes and trematodes infections were found in 2.2%, 20% and 56.6% of the cattle, respectively. Most farms (94%) had trematode infections. No single farms had nematode infections in Olpiro and the overall prevalence was estimated to be 47%. Nematodes infection rates were influenced by the age and haemoparasites profiles of the study animals. Trematodes infections were influenced by level of tick infestation and the location of farm. Of the 90 cattle examined, 14.2% young stock (1-3yrs), 35% immature cattle (>3-6yrs) and 21.7% adult cattle (>6yrs) were infected with nematodes.

Most of the animals examined during the present survey had low to moderate strongyle eggs and coccidia oocyst counts, suggesting that the infections were usually sub-clinical. In contrast, trematodes egg counts were relatively high. However, sub-clinical infections may be very important economically leading to retarded growth; reduced productivity and animals are more susceptible to other infections. The animal will also continuously contaminate pastures.

Study surveys suggest, appropriate GIT parasite control approach be explored and tried in order to alleviate the problem of worm burden in the present area of study.

Key words: Africa, gastro intestinal parasites, pastoral livestock production system, prevalence, Tanzania


Introduction

Gastro intestinal tract (GIT) parasites are known to be widespread in Tanzania (Keyyu et al 2002; Makundi 2001) and limit cattle production in many areas and countries (Allonby and Urquhart 1972; Keyyu et al 2005; Maichomo et al 2004). The direct losses caused by these parasites are attributed to acute illness and death, premature slaughter and rejection of some parts at meat inspection. Indirect losses include the diminution of productive potential such as decreased growth rate, weight loss in young growing calves and late maturity of slaughter stock (Hansen and Perry 1994). The infections are either clinical or sub clinical, the latter being the most common and of great economic importance (Allonby and Urquhart 1972; Msanga 1985; Makundi et al 1998). Although clinical parasitism has received considerable attention as a result of obvious severity, the study of parasitism in herds without clinical signs of infection has been largely neglected.

A review of the literature, however, indicates that only a limited number of studies have been undertaken to provide information on the prevalence, distribution and epidemiology of various species of parasites in cattle in different agro-climatic zones including Pastoral Maasai range land in Tanzania (Hansen and Perry 1994; Keyyu et al 2003; 2005; Kassuku et al 1986; Makundi 2001). Currently, there is no information on the prevalence of GIT parasites (Strongyle and Fasciola spp) in traditional cattle in Ngorongoro. The information is important in the formulation of parasite control strategies.

A study was designed to determine the prevalence and intensity of GIT helminths in grazing cattle in a wildlife/livestock interface pastoral/agro-pastoral areas of Ngorongoro District, Tanzania.


Materials and Methods

Description of study sites

Ngorongoro district is situated on the northwestern part of Arusha Region, lying between Longitude 35 and 36E and latitude 2 and 4S. The district has heterogenous physical and climatic features varying from cool [Loliondo and Ngorongoro Conservation Area Authority (NCAA)] highlands in the North and South, respectively, to semi-arid plain in the central West and South.  There are two rainy seasons, long rains occurring between December and  May and the short rains between July to November. Rainfall varies widely from 1000 mm in the highlands down to 600 mm in the semi-arid areas. The study was conducted in four administrative wards and in one village of the Ngorongoro district. Mean annual temperatures are between 13C to 28C and mean maximum temperature falls between 10 and 32C. Vegetation cover is mainly grassland interrupted by short bushes and scattered trees. Characteristic of the four wards and village are described as follows:

'Digodigo and Samunge ward'

The ward lies in the northeastern segment of Ngorongoro district, whereby agro-pastoralists land management practices are conducted in a highly unstable environment. The area is surrounded by hills containing bushes. Also it is tsetse-infested area signifying the presence of trypanosomosis. Irrigation in the lowland area is practiced during the dry season.

'Saleward'

The ward is also an agro-pastoralist area. Agriculture depends on rainfall that is sometimes scanty and erratic. Pastoralists keep their cattle in bushy areas with open grazing areas.

'Malambo ward'

This ward is located inland from Digodogo and lies within the Serengeti great plain. The area is dominated by Maasai pastrolists. The ward contains some of the most fertile, volcanic soils capable of producing highly nutritious grasses.

There are two main seasons, the rainy season from November to June and the dry season from July to October. A great variance in rainfall is observed between and within seasons, which lead to a variance in pastoral production typical of the area. . The emigration of wildlife from Serengeti National Park to these areas during the rainy season excludes Maasai cattle from utilizing these forages due to the occurrences of Malignant Catarrhal fever (MCF), a disease transmitted from calving wildebeests to cattle through contamination of pastures.

'Pinyiny ward'

Part of the ward villages that are composed of crystalline, hard and non-porous volcanic rocks is nestled at the base of escarpment. They lie within the Great Rift Valley and the shore of Lake Natron. The area has no eastern wall to the Rift Valley and therefore the flattish area, which is suitable for irrigation, falls into a gentle depression. The water of Lake Natron is highly salty such that it is not fit for drinking neither for human nor animals.

'Endulen ward/Olpiro village'

This ward /village is nestled within Ngorongoro Conservation Area Authority (NCAA). The area is bushy with open grazing areas. It is tsetse-infested area indicating the presence of trypanosomosis. People found in this village are the Tatoga pastoralists and the Hadzabe hunter-gatherers. Each group has its own distinct socio-economic and cultural arrangements. Few Tatoga are agro-pastoralists practicing irrigation as water is abundant. Hunter-gatherers make little discernable impact on the environment but their own lives and lifestyle are extremely vulnerable to land-use restrictions.

Farms and animal selection

Farms used in this study belonged to pastrolist Maasai, Sonjo (agriculturist) and Hadzabe (hunters-gathers) who constitute the majority of the inhabitants of Ngorongoro. A total of 90 animals mainly indigenous short horn zebu of all sexes and ages, categorised by Maasai as: young stock (1-3yrs), immatures (3-6yrs) and adult (>6 yrs) from 17 farms/herds were used in the study. The animals had not been drenched for at least 4 week prior to sampling. The study herd selection was carried out with the help of Community Animal Health Workers (CAHWs) who were trained to carry out veterinary services in their respective wards or villages. The criteria for choosing the farms were that they should comply and have a minimum of 25 animals of all age groups per herd. No formal procedure to secure representative of cattle herds in all administrative and geographical areas could be implemented since the herds were evenly distributed across the district.

Data collection

A questionnaire extensively piloted prior to the start of the survey. It was administered on a single day farm visit and used to collect all information related to animals (age, sex, location, source of animal - homebred or brought - in and owner) and farm management practices. Farm management practices included presence of ticks on the animal body, live body weight (estimated using a tape weigh band [Webo-Denmark]) and history of dipping (not reported here). Due to the absence of written records, the age of animal was estimated by dentition. Jugular blood from each animal was also harvested for serum collection. Obtained sera were subjected to indirect enzyme linked immuno-sorbent assay as described by Katende et al (1990; 1998) in order to evaluate the level of sero-conversion against five major tick borne parasites (TBDs) namely Theileria parva, Cowdria ruminatium, Anaplasma marginale, Babesia bigemina and Babesia bovis. Most of the responses to many of the questionsand laboratory results (sero-conversion status: positive or negative) were used as binary explanatory variables in the analyses described in the following section. The study was conducted during March 2004.

Sampling and faecal analysis

During each visit to the 17 farms, faecal samples were collected from all recruited animals. The faecal samples were collected per rectum with new, unused gloves for each animal. Collected samples were put into faecal pots, labelled and kept cool prior to transportation to the laboratory where they were immediately examined or stored at refrigerated temperature (4 C) for a maximum of one day before processing. The sedimentation and floatation technique as described by MAFF (1986) was used to detect the presence of stomach and liver fluke eggs (trematodes) and strongyle eggs (nematodes) in the samples. The presence of coccidian oocysts was also recorded.

Worm identification through culturing faecal samples could not be carried out due to the local laboratory capacity reasons.

Statistical analysis

Point prevalence was used in this study. The prevalence rates of parasite eggs/oocysts were defined as described by Hansen and Perry (1994). The data were entered and edited in the Epi-info program (Version 6.04b, CDC, Atlanta, USA 1996). Descriptive statistics and graphical results were generated in Statistix (Analytical soft ware). Logistic regression (using Egret for Windows version 2.0, Seattle, USA) was used to investigate the relationship between presence of faecal eggs and individual cattle and farm-level variables such as sex, levels of exposures to TBDs parasite, level of tick infestations and location (as factors).


Results

Farm infection rates

Farm prevalence of infections with nematodes and trematodes by ward is shown in Table 1. In total, 16(94%) farms had at least, one trematode infection. High prevalence rates occurred in all wards excluding Pinyiny, which recorded a lower prevalence rate (66%). The overall nematode infection rates were 47%, with Digo digo ward recording a high infection rate (83%).


Table 1.  Farm prevalence of GIT parasites by ward and worm spp (n =17)

Ward

Nematodes

Trematodes

Number

Screened

% of excreters

Number

Screened

% of

excreters

Digodigo

6

5(83.3)

6

6(100)

Malambo

3

1(33.3)

3

3(100)

Olpiro

3

0(0)

3

3(100)

Pinyiny

3

1(33.3)

3

2(66.6)

Sale

2

1(50)

2

2(100)

Overall

17

8(47.0)

17

16(94.0)


Prevalances of GIT parasite infection in animals
Strongylosis

Table 2a and Figure 1 give the stratified prevalence of strongyle infection in young stocks, immature and adult cattle in the five wards.


Table 2a.  Prevalence of faecal strongyle egg counts (nematodes) in calves, immature and adult on five wards/villages

Ward / or

Village

Calves

Immature

Adult

Overall

Number

examined

%  of

excreters

Number

examined

% of

excreters

Number

examined

% of

excreters

Number

examined

%

excreters

Sale

9

11.1*

5

20**

1

0

15

13.3**

Malambo

9

0

3

50*

3

33.3*

15

13.3*

Pinyiny

9

11.1*

2

0

4

0

15

6.6*

Olpiro

9

0

4

0

2

0

15

0

Digodigo

20

30*

6

83.3*

4

50*

30

43.3*

Overall

56

14.2%

20

35%

14

21.7%

90

20%


Overall, Strongyle eggs were detected in 18 out of 90(20%) samples examined from the five wards indicating that the infection is common in the study area. Of the 56 young stock (calves) examined, 8 (14.2%) were positive for strongyle eggs while out of 20 immature cattle, 7 (35%) were infected. Egg excretion rate was high in Digodigo (43.3%) and worm burden was low in other wards/villages to non-existent in Olpiro (0%).



Figure 1. Animal prevalence of GIT parasites by ward and worm spp (n=90)
(Error bar represents 95% confidence interval of proportion)


Trematodes (Fasciolasis)

Trematodes (mainly Fasciolasis) formed the most prevalent gastrointestinal infection with average prevalence of 56.6%. High prevalence rates occurred in Sale (80%) and Digodigo (80%) (Figure 1 and  Table 2b).


Table 2b.  Prevalence of faecal trematodes egg counts in calves, immature and adult on five wards/villages

Ward / or

Village

Calves

Immature

Adult

Overall

Number

examined

% of

excreters

Number

examined

% of

excreters

Number

examined

% of

excreters

Number

examined

% of

excreters

Sale

9

88.8**

5

60***

1

100*

15

80***

Malambo

9

66.6*

3

0

3

33.3*

15

46.6*

Pinyiny

9

11.1**

2

50**

4

100*

15

26.6**

Olpiro

9

22.2**

4

0

2

100**

15

26.6**

Digodigo

20

75*

6

100*

4

75**

30

80**

Overall

56

57.1%

20

50%

14

64.2%

90

56.6 %

*: Range of egg excretion: 100-250 eggs per g faeces

**: Range of egg excretion: >250 500 eggs per g faeces

 ***: Range of egg excretion:  > 500 eggs per g faeces


As shown in Figure 2, there was an age difference in the distribution of strongyle eggs. Animal aged between 5-7 yrs had few samples with trematode eggs compared to young stocks.


Figure 2.  Age prevalence profiles of nematodes and trematodes infection in Ngorongoro


Coccidiosis

Two percent of all samples collected had coccidial oocysts. Coccidial infection was limited to animals of less than four years old. Oocyst positive animals were observed in Sale and Malambo wards.

Factors associated with trematode and nematode infection

The factors, which were found to be associated with infection of trematodes and nematodes in the multivariable regression models, are shown in Table 3a,b.


Table 3a.  Factors associated with trematodes infection in cattle in Ngorongoro in multivariable logistic regression models adjusted for farm effects

Variable

β

SE

P -value

Constant

-1.38

0.49

 

Digodigo* vs Malambo

                     Pinyiny

                     Olpiro

                     Sale

-1.50

-2.39

-1.50

0.04

0.75

0.80

0.75

0.85

0.044

0.002

0.039

0.032

Tick infested: Yes vs No*

2.10

0.82

0.010

Random term (farm effect)

0.71

0.37

 

* Reference variable, β = Coefficient of regression (or parameter estimate),
SE = Standard error of Coefficient, P = level of significance


Animal located in Sale were significantly (P<0.05) associated with increased risk of trematode infection. Tick infestation was a risk factor to trematode infection. Animals infested with Trypanosomosis and seroconverted to Anaplasma marginale were associated with increased risk of nematode infection. (β = 3.7 and 1.6 for Tryps and Anaplasma marginale, respectively).


Table 3b.  Factors associated with nematode infection in cattle in Ngorongoro in multivariable logistic regression models adjusted for farm effects

Variable

β

SE

P- value

Constant

-3.6

1.20

 

Tryps infected:  Yes vs No*

3.7

1.89

0.045

Anaplasma marginale infected: Yes vs No*

 

0.80

0.051

Random term (farm effect)

1.9

0.70

 

* Reference variable, β = Coefficient of regression (or parameter estimate),
SE = Standard error of Coefficient, P = level of significance


With notable exception of Olpiro ward, the prevalence of strongyle infection did not vary significantly among cattle in the five wards for any of the three age groups (P> 0.05)
 

Discussion

Endo-parasites are highly prevalent in cattle raised in communal wildlife/cattle grazing areas in Ngorongoro district. GIT nematodes and trematodes were almost universally present in all the animals examined. The prevalence was close to that found by Mahlau (1970), and compares with previous reports in the Southern Highlands of Tanzania (Ecimovic and Mahlau 1973; Keyyu et al 2005). It was comparable to the level of 30- 60% infection found in Kenya (Maingi and Gichigi 1992; Waruiru et al 1995), over 30% in Sierra Leone (Asanji and William 1987) and over 40% in Nigeria (Schillhorn Van Veen et al 1980).

The prevalence of trematodes as reflected by egg output appeared to be greater in immature animals than in the young and older age groups. This conforms to earlier observations of other workers (Maingi et al 1993; Waruiru et al 2000; Mbae et al 2004). In contrast, the age prevalence relationship for nematodes was less clear in this study. Trematode infections were consistently higher across all age group- suggesting the parasite to be more prevalent in the study areas.

The presence of nematodes was associated with both Anaplasma marginale and Trypanosomiasis infection. Our observation is that cattle, which are infected by haemoparasites pathogens, had more nematodes eggs. Since we did not do total worm counts we cannot categorically state that cattle infected with haemoparasites are more susceptible to nematode infections, but probably this was the case. More studies are required to further investigate the nematode and haemoparasite relationship observed. However, the observed nematode and haemoparasite link in this study can be explained partly by management in the farms (less tick and tsetse control practices noted) and what has been reported on the epidemiology of haemoparasites (Swai et al 2005). Haemoparasites are associated with red blood destruction leading to anaemia syndrome features and the condition is more important in free grazing animals.

Both location (Malambo, Pinyiny, Olpiro) and level of tick infestation were associated with low and high trematode infection rates, respectively. In these wards, cattle share grazing with wildlife. The weak relationship observed is difficult to explain. Unfortunately, in this study, we were unable to judge the actual period when contact between cattle and wildlife (wild beest) occurs. This coupled with the relatively small number of farms studied, limits our ability to compare between the proportions of cattle with faecal eggs with potential farm level risk factors. The danger from these parasites is undoubtedly greatest where large herds are kept in close contact with wildlife and especially where overstocking occurs. Cross-infection of parasites between wildlife and domestic cattle are likely to occur in such farms (Ocaido et al 1996). Results obtained in this survey and the previous one (Waruiru et al 1995) suggest that GIT parasites are prevalent in cattle and possibly in wildlife as they share grazing. Extensive epidemiological studies on the GIT parasite infections in cattle and other wild life ruminants in various agro-climatic regions in the country now need to be undertaken and a sound control programme formulated.

The observed threshold level of egg numbers in this study may be regarded as low to moderate that mainly manifests as sub-clinical infections (Waruiru et al 2005). The effects of these infections can be aggravated by the frequent drought that occurs in some of the study areas (Anon 2005). This is described as the most economically important form of infection since it occurs in most of the cases leading to unthriftiness and animals are more susceptible to other infections and are continuously contaminating pastures (Ocaido et al 1996). Treatment of such animals is therefore indicated to improve productivity and reduce the chances of infecting the more susceptible young animals.

Coccidial oocysts that were detected in 2.2% of all animals sampled was sporadic and the burden was light. This parasite is probably not an mportant factor affecting the health of cattle in the study area. Coccidiosis is more important where animals are housed or confined in small areas. The disease is also more important in young animals. However, they are sources of stress and weight loss to animals when they occur in large numbers and should be treated as they occur if the economic situation justifies this.

This study was cross-sectional in nature. Therefore, it could not capture worm egg count patterns over seasons. A better and a longer-term monitoring study is proposed in order to address the health and economic impact of these worms in this cattle production system.


Conclusions


Acknowledgements

The authors wish to acknowledge the financial support from DANIDA-ERETO without which this research would not have been possible. Special thanks go to the participating farmers and CAHWs for their considerable cooperation and help. Permission to publish this paper was granted by the Director of Veterinary Service, Tanzania for which we are very much grateful.


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Received 3 May 2006; Accepted 11 June 2006; Published 5 September 2006

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