2Norwegian Veterinary Institute, Oslo, Norway
3Sokoine University of Agriculture, Morogoro, Tanzania
4University of Tromsø, Tromsø, Norway
E-mail:
Keywords: Abortion; Antibody-ELISA; Bovine; Brucella spp; BVDV; N caninum; Pestivirus; Reproductive-Disorders; Serology
Reproductive disorders contribute significantly to suboptimal performance and production in cattle. Studies on reproductive performance including estimation of the frequency of abortion and stillbirth have been reported in different parts of Tanzania but little is known of different risk factors associated with reproductive disorders [1-3]. Causes of reproductive disorders are broadly categorized as infectious and non-infectious. Brucella spp., Bovine Viral Diarrhea Virus (BVDV) and Neospora caninum are known to be among the most common infections associated with reproductive disorders in many parts of the world, but the information about which ones are implicated in reproductive disorders in cattle in Tanzania is scarce [4]. These infections may cause different reproductive disorders including early embryonic death, abortion, stillbirth and fetal malformations [5- 7]. In addition, Brucella is an important zoonotic agent, and its seroprevalence in cattle varies between regions in Tanzania [8- 11]. In Tanzania, the prevalence of antibodies against BVDV has been found to be 12% and 17% in cattle and wildlife populations respectively [12,13]. Neosporosis caused by the protozoan parasite N. caninum, has emerged as one of the most frequently diagnosed causes of abortion in cattle in many parts of the world [14]. In Tanzania, only a few reports exist on N. caninum in cattle and canid populations [15,16].
All three infections are generally considered endemic in the cattle populations in Tanzania, as in the rest of Africa. Climatic factors and the diverse management systems of the cattle industry are likely to influence the epidemiology of these infections, but the impact of these infections on reproductive disorders has received little attention.
The aim of the present study was to investigate the occurrence of selected infections and their impact on reproductive disorders in cattle under different management systems in the southern highlands of Tanzania. Specifically, the study was carried out to establish the i) animal and herd level prevalence of serum antibodies to Brucella spp., BVDV and N. caninum, ii) the association between serostatus and reproductive disorders, and iii) management and other risk factors associated with serostatus and reproductive disorders.
|
Region ( Districts) |
|
Herd size |
Mbeya (Mbarali) |
Njombe (Rural, Urban, Wanging`ombe) |
> 100 cattle |
1 |
0 |
7–100 cattle |
13 |
5 |
1–6 cattle |
28 |
155 |
None of the sampled cattle were vaccinated against the studied infections. Most of the cattle in Mbeya region were kept on pasture during the day and indoors at night, while the majority of cattle in Njombe were confined in open barns with concrete walls or branches of trees with earthened, wooden or concrete floor. For zero grazed animals, roughage was obtained from communal grazing land with little supplementation from agricultural leftovers and industrial by-products. Grazing was on communal land except for a few herds that grazed on the farm.
Disorders (n) |
P=Animal level prevalence (%) |
P=Herd level prevalence (%) |
|||||||
P |
95% CI |
Location |
p |
95% CI |
P |
95% CI |
p |
95% CI |
|
Abortion (38) |
11.3 |
8-16 |
Njombe |
7.0 |
4-11 |
11.6 |
7.7-17 |
7.8 |
4-13 |
Mbarali |
23.4 |
14-35 |
27.8 |
16-45 |
|||||
Retained placenta (51) |
17.2 |
13-20 |
Njombe |
18.2 |
12-25 |
22.6 |
17-29 |
23.4 |
17-31 |
Mbarali |
14.3 |
7-27 |
19.4 |
9-36 |
|||||
Stillbirth (5) |
1.7 |
0.7-4 |
Njombe |
1.4 |
0.4-4 |
2.6 |
1-6 |
1.9 |
0-6 |
Mbarali |
2.6 |
0.6-9 |
5.6 |
1-19 |
|||||
Malformations (4) |
1.4 |
0.5-4 |
Njombe |
1.4 |
0.4-4 |
1.6 |
0.5-5 |
1.9 |
0-5 |
Mbarali |
1.3 |
0.1-8 |
0 |
- |
Risk factors |
Level |
Prevalence (95% CI) |
OR |
95% CI |
p |
Brucella spp. |
|||||
Breed |
Dairy Cross |
1.6 (0.5-5.0) |
1.00 |
- |
- |
Local |
35 (22-51) |
5.34 |
1.22-23.5 |
0.03 |
|
Location |
Njombe |
0.46 (0.07-3.1) |
1.00 |
- |
- |
Mbarali |
22.1 (13.4-34.1) |
21.5 |
1.9–248 |
0.01 |
|
Parity |
Primiparous |
2.3 (0.6-8.3) |
1.00 |
- |
- |
Multiparous |
7.8 (4.0-15.0) |
3.72 |
0.65–21.3 |
0.14 |
|
BVDV |
|||||
Breed |
Dairy Cross |
7.9 (4.6-13.6) |
1.00 |
- |
- |
Local |
50 (37.6-62.3) |
4.9 |
1.76–13.6 |
0.002 |
|
Location |
Njombe |
6.5 (3.1-13.4) |
1.00 |
- |
- |
Mbarali |
33.8 (23.2-46.3) |
2.89 |
0.92–9.1 |
0.09 |
|
Parity |
Primiparous |
10.5 (5.6-18.7) |
1.00 |
- |
- |
Multiparous |
15.1 (10.4-21.5) |
1.44 |
0.69-3.1 |
0.33 |
|
Neospora caninum |
|||||
Breed |
Dairy Cross |
5.2 (2.7-9.6) |
1.00 |
- |
- |
Local |
5.0 (0.7-28) |
0.37 |
0.04-3.53 |
0.38 |
|
Location |
Njombe |
4.2 (2.0-8.7) |
1.00 |
- |
- |
Mbarali |
7.8 (2.9-19.4) |
3.12 |
0.74–13.2 |
0.12 |
|
Parity |
Primiparous |
2.3 (0.6-9.0) |
1.00 |
- |
- |
Multiparous |
6.3 (3-3-11.7) |
3.18 |
0.77–13.2 |
0.11 |
Risk factors |
Level |
Prevalence |
OR |
95% CI |
p |
Brucella spp. |
|||||
Location |
Njombe |
0.63 (0.09-4.3) |
1.00 |
- |
- |
Mbarali |
36.5 (23.3-52.2) |
23.1 |
1.96-292 |
0.013 |
|
Herd size |
Small-scale (≤ 6) |
2.7 (1.1-6.4) |
1.00 |
- |
- |
Medium-scale (6-100) |
61.1 (37.7-80.3) |
14.5 |
2.2–94.4 |
0.005 |
|
Management system |
Indoor |
1.1 (0.3-4.4) |
1.00 |
- |
- |
Outdoor |
63.6 (42.1-80.8) |
22.7 |
3.45-150 |
0.15 |
|
BVDV |
|||||
Location |
Njombe |
6.9 (3.8-12.0) |
1.00 |
- |
- |
Mbarali |
63.4 (47.7-76.7) |
12.7 |
4.7-34.8 |
< 0.001 |
|
Herd size |
Small-scale (≤ 6) |
13.7 (9.4-19.4) |
1.00 |
- |
- |
Medium-scale (6-100) |
66.7 (42.7-84.3) |
2.8 |
0.65–11.8 |
0.17 |
|
Management system |
Indoor |
11.7 (7.7-17.4) |
1.00 |
- |
- |
Outdoor |
72.7 (50.9-87.3) |
2.9 |
0.75-11.3 |
0.12 |
|
Neospora caninum |
|||||
Location |
Njombe |
9.4 (5.7-15.0) |
1.00 |
- |
- |
Mbarali |
9.8 (3.7-23.4) |
0.69 |
0.15-3.1 |
0.62 |
|
Herd size |
Small-scale (≤ 6) |
8.7 (5.4-13.8) |
1.00 |
- |
- |
Medium-scale (6-100) |
16.7 (5.4-41.1) |
2.1 |
0.36-12.2 |
0.40 |
|
Management system |
Indoor |
8.9 (5.5-14.1) |
1.00 |
- |
- |
Outdoor |
13.6 (4.4-35.0) |
1.4 |
0.19–9.9 |
0.74 |
|
Presence of dogs |
Yes |
9.7(5.2-17.1) |
1.05 |
0.4-2.7 |
0.8 |
No |
9.3(4.9-16.9) |
1.0 |
- |
- |
The observed sero-prevalence for Brucella spp. calls for attention, as human brucellosis originates from animals [18]. Veterinary public health measures need to be in place as this is a zoonotic infection and consumption of unpasteurized dairy products is still a practice in some communities in Tanzania. Brucella abortus ,biovar 3 has earlier been isolated from an aborted cattle fetus from the large-scale herd included, illustrating the risk for transmission. Brucella abortus biovar 1 has been detected in the Katavi-Rukwa ecosystem in Tanzania [8,19]. Previous studies have reported the prevalence of brucellosis in cattle to range from 2.2-12.3 % in different regions and management systems in Tanzania [10,11,20,21]. Similarly the present study indicates a difference in sero-prevalence in two geographically very closely areas. Interestingly, Njombe, with a total of 160 herds investigated, had only one seropositive animal, which could be a false positive, and therefore, it is possible to regard the area as Brucella free. This is further supported by information from a local milk factory. They require that farmers test their animals for brucellosis before milk is accepted, and no positive animal has been detected for the past five years (personal communication). The prevalence of brucellosis in Mbarali could be explained by management strategies which allow for more direct or indirect contacts between infected and susceptible animals, as has been observed elsewhere [22]. High prevalence of abortion, strong association with Brucella spp. on both animal and herd level, and isolation of the agent in the same area suggest that Brucella abortus causes abortion in this area.
The prevalence of BVDV was found to be higher than that detected in 18 regions about 25 years ago, but more similar to that observed in the northern parts of the country [13,23]. With this relatively high sero-prevalence, the cattle population most likely also includes Persistently Infected (PI) animals, but such animals are frequently weak-born, unthrifty and underperform and are often eliminated from the herd early in life under these management conditions [24]. Since only animals over six months of age were included in the present study, this might explain why no PI animals were detected. It is not unlikely that BVDV could also has been introduced directly or indirectly from outside as most herds were open, but the general trend of very small herds and little contact probably limits the survival of BVDV in Njombe.
The higher prevalence of both BVDV and Brucella spp. in the two subgroups investigated is interesting, since both subgroups represent particular risk of inter-herd transmission. Breeding males represent a risk because they are commonly moved from herd to herd for natural breeding, and the large-scale herd as it represents typical procedures of replacement heifers for smaller herds.
The low sero-prevalence for N. caninum indicates a different epidemiological pattern from BVDV and Brucella spp. Contrary to our findings, in Ethiopia, a higher sero-prevalence for N. caninum than BVDV and Brucella spp. has been reported, and is regarded as more important for reproductive performance [25,26]. This highlights the difference in epidemiological patterns for these infections in African countries. Presence of infected dogs, which shed infective oocysts in the environment is crucial to dissemination into the cattle population. Investigation of the dog population in the area would have been valuable to explain if a low prevalence in the dogs may be the main reason for the observed low prevalence in cattle. The lack of association between presence of dogs and N. caninum sero-prevalence could be because exposure is more evenly distributed as stray dogs move easily between farms. This lack of association between presence of dogs at farm and N. caninum seropositivity has also been reported in Ireland [27].
The observed association between larger herds and Brucella spp. sero-positivity is in accordance with other observations [28,29]. Evidence suggests that when Brucella spp. is introduced into herds, a large proportion of animals will be infected and the infection will persist for a longer time [30-32]. Sharing of pasture and drinking water facilitate transmission of most infectious diseases, which is in line with the present findings of grazing as risk factor for Brucella and BVDV infections [33]. This might be caused by a higher degree of contact with animals from other herds [34]. In addition the pasture may have been contaminated with infectious agents from animal secretion particularly with Brucella spp. since it is common for cattle to give birth outdoor which contaminate the surrounding environment
The trend in this study that Brucella spp. and BVDV prevalence is linked to breed, has also been observed earlier for Brucella spp. [35]. However, all the zebu cattle herds in the present study were located in the Mbeya region with the higher seroprevalence of Brucella spp. and BVDV so the finding that Zebu cattle was more likely to be seropositiv for these infections should be carefully interpreted. Since breed, location, grazing strategy and management are often interlinked, confounding effects are possible.
The quality of the information gained from the interviews is a concern, as written recordings by farmers are uncommon. The data on reproductive disorders were the only reproductive performance information that was regarded suitable for analysis. Since Brucella spp. typically gives abortion where it is easily observed, the consequences on reproductive performance is most likely better estimated than for BVDV, which often leads to early embryonic death and repeated breeding/prolonged calving interval [36]. The impact of BVDV on reproduction is therefore probably underestimated in the present study.
The present findings indicate that co-infections with BVDV and Brucella spp. may have a greater influence on occurrence of reproductive disorders than mono-infection. Immunosuppressive properties of BVDV is known, and although the mechanisms of abortion caused by BVDV is unclear, it has been speculated that pathological changes induced in the placenta may allow other pathogens to cross the fetal membrane barriers [37,38]. The most likely explanation for the co-infections in this study is, however, that they share the same risk factors.
Serological investigations and cross sectional design has both advantages and disadvantages as methods to establish the prevalence of infection. In the absence of vaccination, seropositivity can be regarded as an earlier infection. For all three infections, animals are generally sero-positive for several years after the infection [39-41]. The risk period for reproductive disorders caused by the agent is only when during pregnancy, and when the agent is actually present. Later, the animal will be fully or partly protected, which leads to underestimation of the association between infection and reproductive performance. Collection of reproductive history for the past three years, as in this study, reduces this challenge.
•EPINAV project through Norwegian State Funds for financial support.
•Technical staff from the Norwegian Veterinary Institute, Oslo, Norway for technical support on serology and virological analysis.
•Veterinary field officers from Njombe, Mbarali and Sokoine University of Agriculture for field work and sample collection.
•Farmers in the study area for their willingness to participate in this study.
•Kassahun Asmare (PhD DVM) and Adis Softic (DVM) for fruitful discussions.
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