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Tanzania Journal of Health Research, Vol. 12, No. 3, 2010 SHORT COMMUNICATIONS The role of livestock keeping in human brucellosis trends
in livestock keeping communities in
Tanzania G.M.
SHIRIMA1*, J. FITZPATRICK2, J.S. KUNDA3, G.S. MFINANGA3, R.R. KAZWALA4, D.M. KAMBARAGE4 and S. CLEAVELAND5 1Central
Veterinary Laboratory, P.O. Box 9254, Dar es Salaam, Tanzania * Correspondence:
Dr. G.M.
Shirima; E-mail: gmalekia@yahoo.com Received
8 February 2010 Code Number: th10027 Abstract: A cross-sectional survey was carried out in
Karatu and Ngorongoro districts in Arusha region and Babati, Hanang and Mbulu
districts in Manyara region involving 20 agro-pastoral and 9 pastoral villages,
to establish the magnitude of human brucellosis in relation to livestock
brucellosis. A multistage random sampling was used to select villages,
sub-village administrative units, ten cell leadership units and animal keeping
households. A total of 460 humans from 90 families (19 pastoral and 71 agro-pastoral
families) and 2723 domestic ruminants from 90 livestock households were sampled
and bled to obtain serum samples for analysis. A competitive enzyme
linked-immunosorbent assay (c-ELISA) was used to analyse these samples to
detect brucella circulating antibodies. The overall livestock seroprevalence
was 5.7% with 32.2% of livestock households being seropositive whereas, human
seropositivity was 8.3% with 28% family households being seropositive. The highest
proportion of seropositive families was observed in Ngorongoro district (46%)
and the lowest in Babati district with no seropositive family household. Family
members in seropositive livestock households were 3.3 (OR) times more likely to
be seropositive than those with seronegative livestock households. However; 25%
of seronegative family households had seropositive livestock households and 48%
seropositive family households had seronegative livestock households. Therefore, Brucella infection is widespread in the
human populations and their livestock in the northern Tanzania and thus humans
may acquire infection from their own animals or from other sources thus prompted
public health awareness creation in such communities. Keywords: undulant fever, brucellosis,
pastoralists, Tanzania Animal
and human health in livestock keeping communities is inextricably linked. Pastoralists
and agropastoralists depend on animals for nutrition and their socio-economic
development, yet these animals can transmit many diseases to humans including
brucellosis. Brucellosis is a major zoonotic disease widely distributed in both
humans and animals especially in the developing countries (WHO, 1997). The
disease is transmitted to humans through ingestion of contaminated animal
products such as cheese, and unpasteurised milk and by direct contact with
infected animals through handling abortions, dystocia and parturitions.
Brucellosis in humans is characterised by intermittent fever with a marked
effect on the musculoskeletal system evidenced by generalised pains (WHO,
1997). However, these clinical signs are non-specific and the disease can be
misdiagnosed and confused with typhoid fever, malaria, relapsing fever and
rheumatic fever. Although, several countries especially the Middle East
region have carried out studies on human brucellosis (Refai, 2002), only few
and limited studies have been conducted in Tanzania. The first report of human
brucellosis in Tanzania was in 1935 (Wilson, 1936). Further reports of human
brucellosis in the country were from the Lake and Western Regions in 1959, 1960
and 1961 where three cases were confirmed (Mahlau & Hamond, 1962). Recent
reports from several hospitals in the Northern zone have shown that the
incidence of the disease is on the increase (G.M. Shirima unpubl.). Minja (2002) conducted a random survey in two districts
of the Northern zone and found a seroprevalence of 0.7% among livestock keepers
with no infection in other occupational groups. Although the geographical distribution of human
brucellosis is closely related to the endemicity of animal infection, husbandry
methods, eating habits and hygienic standards; screening for animal brucellosis
did not go in hand with human screening in Tanzania. Therefore, this study examined the trend of human brucellosis in livestock
keeping districts where human brucellosis cases were frequently reported in
hospitals. The objectives of the study were to establish the
magnitude of co-existence of human and livestock brucellosis in order to raise
awareness about the scale of the problem by: (i) establish the magnitude of
human brucellosis in livestock keeping communities of the Northern zone of
Tanzania; (ii) establish the magnitude of livestock brucellosis at household (herd/flock)
level; and (iii) establish the role of keeping livestock on the trend of human
brucellosis. This study was conducted in the Arusha and Manyara
regions in northern Tanzania from 2002 to 2003. The regions lie between 34.6 to
38.00E and 1.8 to 6.00S. The regions have potential for agriculture, food and cash crops,
livestock, wildlife and mining. Livestock-keeping
households were selected by a process of multistage random sampling. The
sampling frame comprised of all villages in the study area (n=285), which was
made available at district livestock offices. A random sample of 29 villages
was selected using a table of random numbers. Among these 20 were agro-pastoral
and 9 pastoral villages. In each village two sub-village administrative units
were randomly selected A ten-cell leader, (a leader of ten or more households)
was selected at random from each sub-village and all livestock-keeping
households were identified. Finally, two livestock-keeping households were
selected from each ten-cell leader. This achieved a wide geographic coverage
but was considered to be too time-consuming and other resources and the
sampling procedure was therefore revised to include two households from each of
ten-cell leaders. The sample size was calculated as described by Martin et al., (1987) based on the previous seroprevalence
of 5% (a figure that was considered likely on the basis of previous published
studies) with 80% power and 95% confidence to obtain the total number of
animals to be screened from each household. Blood samples were collected from
the jugular vein using a sterile needle and a plain vacutainer (Becton and
Dicknson, UK) and the metal tag was fitted to each animal for subsequent
identification. Sampling of animals at herd level was difficult due to lack of
systematic method of restraint such as crush or race. Therefore, at herd level
animals were restrained on convenience. Permission to collect human serum samples was obtained
from the Ministry of Health, Tanzania. In each household selected, family
members were approached for blood sampling. Where members gave consent, blood
samples were collected from the brachial vein after disinfection using cotton
wool soaked in methylated spirit (Bell chemicals Co. Ltd. Dar es Salaam). Blood
was collected using sterile disposable 5ml syringe and later transferred into a
plain vacutainer. The vacutainer was assigned an identification number and kept
in a tray for serum separation. Serum samples were sent to VLA Weybridge-UK for
c-ELISA analysis as a confirmatory test. Therefore, a livestock household (herd
and or flock) and a family household was considered c-ELISA seropositive, if at
least one individual was seropositive. Data were entered using Microsoft Excel spreadsheet
97 (1993). The Chi-square test was used to compare two or more proportions and
to determine associations. The strength of the association between risk factor
and brucellosis status was examined by odds ratio (OR) and 95% confidence
intervals (95%CI) values. A
total of 2723 domestic ruminants (cattle, goats and sheep) were bled and
subjected to c-ELISA analysis from 90 households. Of these, 155 samples (5.7%)
were seropositive. Seroposititivity was detected in all species although the
difference between cattle (4.9%) and small ruminants (6.5%) was not
statistically significant (χ2 =3.1, df=1, 95%CI=-0.0017, 0.0331, P>0.05). For both herds and flocks,
c-ELISA seropositivity was significantly higher in pastoral than in
agro-pastoral herds (χ2=31.9, df = 1, 95%CI = 0.379, 0.818, P<0.01) and flocks (χ2= 18.28, df=1, 95%CI= 0.250, 0.731, P<0.01). During
the cross-sectional survey, 104 families were visited. Fourteen families were
not bled due to non-compliance. Therefore, 90 families with a total of 460
family members were screened. Within these families however, young children who
were afraid and those individuals failing to comply were not bled. Seventy four
percent of the families had family members ranging from 1-6 who complied for
bleeding. Out
of 460 sera that were tested using c-ELISA, 38 (8.3%) turned to be seropositive.
There was no statistical difference between seropositivity in males and females
(P=0.663). A higher proportion of
human c-ELISA seropositivity was observed in the agro-pastoral farming system
(8.7%) than in the pastoral system (7.4%) though the difference was not
statistically significant (P =
0.631). However, the difference between pastoral and agro-pastoral families
seropositivity was statistically significant ((χ2 =14.98, P<0.05) with high
proportion of seropositivity observed in agro-pastoral families (29%) compared
to pastoral families (25%). Forty
four percent (11/25) of the families that were c-ELISA seropositive had more
than one person that was seropositive. Also among families that were
seropositive, three families had brucella seropositive human cases diagnosed in
health facilities prior to this study. Furthermore,
the highest proportion of human c-ELISA positive families was observed in
Ngorongoro district (46%) and lowest in Babati district (0%). All family
members (n = 56) from 12 families sampled in Babati district were seronegative
(Table 1). Table 1: C-ELISA seropositivity in humans by district,
family and individual level
Fifty
two percent (13/25) of families that were c-ELISA seropositive had infected
herds and flocks whereas 48% (12/25) of families that were c-ELISA seropositive
their herds and flocks were c-ELISA seronegative. In addition 25% (16/65) of
families that were c-ELISA seronegative had infected herds and flocks. There
was a significant association between c-ELISA seropositivity in families and
c-ELISA seropositivity in households (OR = 3.3, 95%CI = 1.26, 8.67, P<0.05) (Figure 1). Family members
in
the c-ELISA positive households were 3.3 (OR) times more likely to be c-ELISA
positive than those in seronegative livestock households.
The
overall c-ELISA seropositivity in humans was 8.3% whereas in livestock was 5.7%.
To-date this is the first and highest human figure to be reported in a
cross-sectional survey in pastoral and agro-pastoral communities in Tanzania.
The cross-sectional study by Minja (2002) found that livestock keepers in
agro-pastoral areas were infected (0.7%) among different groups of people who
handle livestock and livestock products in the area. Therefore, the current
study encompasses both pastoral and agro-pastoral families and had a wider
coverage thus resulting to a higher seroprevalence than the previous studies.
Several studies carried in other countries indicated variable seroprevalences
based on the rate of infection in animals such as 18-24% in humans and 18% in
farms in Uganda (Ndyabahinduka & Chu, 1984), 3.8% in humans and 7% in
cattle in Chad (Schelling et al.,
2003) and 40 cases/100,000 in humans and 15% in animals in Saudi Arabia
(Memish, 2001). The variations of seroprevalence between humans and livestock
could be probably due to the extent of spread of the disease in livestock
populations and risk factors associated with transmission of brucellosis from
animals to humans. The
statistical difference observed between agro-pastoral and pastoral families
c-ELISA seropositivity with high proportion of infected families recorded in
agro-pastoral families may not reflect the true status of the disease as many family
members from pastoral areas were reluctant for screening. It was expected that
pastoral families having higher seropositivity than agro-pastoral families to
conform to the infection in livestock where high infection was observed in the
pastoral herds and flocks compared to agro-pastoral herds and flocks. Another
possible explanation could be the fact that families in agro-pastoral areas
might acquire infection from other sources apart from their livestock. Absence
of c-ELISA seropositive families in Babati district observed in this study was
consistent with the previous studies where the seroprevalence was low compared
to Hanang district (Niwael, 2001). This could be explained by the fact that
domestic ruminants were also c-ELISA seronegative during cross-sectional
screening. This was supported by the fact that human brucellosis occurred when
brucellosis was present in livestock populations. Families with the highest
c-ELISA seropositivity were observed in Ngorongoro district, which is a
pastoral district, followed by other districts which are predominantly
agro-pastoralist. This was expected because in all families that were screened
in Ngorongoro district their herds and flocks were also c-ELISA positive. Close
cohabitation under poor hygiene, eating habits and livestock related activities
performed without protective measures could have resulted in high family
seroprevalence in the district. Assisting with parturition and handling aborted
foeti and retained placenta may be risk factors for human infection. This was
further supported by the fact that there was a significant statistical
association between families with c-ELISA seropositivity and herd c-ELISA
seropositivity. Furthermore,
48% percent of families were c-ELISA seropositive while their herds and flocks
were c-ELISA seronegative. Family members could acquire infection from
neighbours through drinking raw milk, assisting parturitions or handling
aborted materials and in livestock auction markets where people may have access
to raw blood, milk and meat. It was also observed that 25% of families were
c-ELISA seronegative yet their livestock were seropositive. One explanation
could be the fact that in some families not all members were tested resulting
in false negative families. This may mask the real status of the disease at
family level. These families were from agro-pastoral farming systems where some
households kept high numbers of male rather than female animals for transport
and draught purposes. Therefore, risk from infected males is probably minimal
as humans acquire infection through consumption of raw milk and handling foetal
materials and placentae. Also the practice of boiling milk may be common in
these households thus reducing the risk of human infection. Another possible
explanation could be the recent introduction of infected animals into the herd or
flock. Although
keeping livestock was observed to be associated with human brucellosis in the
area, other sources of infection should be identified and quantified as some
families had seronegative herds and flocks. Acknowledgements Authors
wish to thank Department for International Development for financing this
study. The assistance and collaboration from laboratory staff at VLA Weybridge,
UK, Sokoine University of Agriculture and livestock owners is highly
appreciated. References
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