Open Access

Predictors of specific anti-Brucella antibodies among humans in agro-pastoral communities in Sengerema district, Mwanza, Tanzania: the need for public awareness

  • Elifuraha B. Mngumi1,
  • Mariam M. Mirambo2Email author,
  • Sospeter Wilson2 and
  • Stephen E. Mshana2
Tropical Medicine and Health201644:34

DOI: 10.1186/s41182-016-0034-5

Received: 8 July 2016

Accepted: 14 September 2016

Published: 18 October 2016

Abstract

Background

Human brucellosis remains to be a neglected zoonotic disease among agro-pastoral communities where livestock rearing is one of the main economic activities. This study was conducted in different agro-pastoral communities in Sengerema district, Mwanza, Tanzania, to determine seroprevalence and predictors of anti-Brucella antibodies, information that may influence public awareness on the risk factors and strategies to improve the diagnosis of brucellosis in developing countries.

Methods

A cross-sectional community-based study was conducted between July and September 2008 in ten villages of Sengerema district. Sociodemographic and other related information were collected using a standardized data collection tool. Detection of Brucella abortus and Brucella melitensis antibodies were done using rapid Brucella serum agglutination test. Data were analysed by using STATA version 11.0. Adjusted odds ratios (AOR) were calculated using multivariate logistic regression analysis.

Results

A total of 382 adults were enrolled with the median age of 30 (interquartile range 15–40) years. Males formed the majority of the participants 234 (61.5 %). Overall, seroprevalence of anti-Brucella antibodies was found to be 14.1 % (54/382, 95 % CI 10.6–17.5). Seroprevalence of B. melitensis was 11 % (42/382) while that of B. abortus was found to be 7 % (26/282), P = 0.0267. Co-infection of B. melitensis and B. abortus was observed in 3.6 % (14/382, 95 % CI 1.7–5.4) of participants. On a multivariate logistic regression analysis, male sex (AOR 3.2, 95 % CI 1.3–7.5, P = 0.007), touching goat placenta (AOR 2.54, 95 % CI 1.05–6.14, P = 0.012) and agro-pastoralist occupation (AOR 2.07, 95 % CI 1.01–4.24, P = 0.04) were found to predict B. melitensis infection. Males (AOR 3.07, 95 % CI 1.45–6.51, P = 0.003) and agro-pastoralists (AOR 2.98, 95 % CI 1.38–6.43, P = 0.005) were found to be predictors for specific anti-Brucella antibodies.

Conclusions

A significant proportion of the agro-pastoralist male population in agro-pastoral communities in Sengerema district is positive for anti-Brucella antibodies. With the decrease incidence of malaria fever, other causes of fever such as Brucella spp. should be considered of public health concern in Tanzania especially in agro-pastoral communities.

Keywords

B. abortus B. melitensis Brucellosis Anti-Brucella antibodies Sengerema

Background

Human brucellosis is a global public health concern due to its potential in causing morbidity among human population as well as livestock leading to economic loses. Worldwide, over 500,000 human cases of brucellosis are reported annually [1]. Seroprevalence has been found to vary in different countries across Sub-Saharan Africa [1, 2]. In the tropical countries like Tanzania, Brucella infection is endemic especially in agro-pastoral communities [2]. Brucellosis is an occupational disease to slaughterhouse workers, agro-pastoralists, laboratory personnel and veterinarians [3]. Humans can get infection through direct contact with infected farm animals or ingestion of contaminated animal products [4, 5].

Brucella infection is characterized by non-specific symptoms including general body malaise, anorexia, fever, back pain, headache, lethargy and many other clinical presentations that often mimic other diseases causing pyrexia such as malaria and typhoid fever [2, 68]. Its ability to survive and multiply within immune cells such as macrophages results into chronic debilitating disease with poor prognosis in most of the cases [9]. In addition, the treatment requires multiple antibiotics for prolonged duration. Despite being important, zoonotic disease data regarding the epidemiology of Brucella infection among high-risk groups are scarce in developing countries including Tanzania.

Tanzania is a Third World country which has about 51 million people. About 68 % of the Tanzania population is below the poverty line of $1.25 per day [10] and is involved in small-scale agricultural activities. Sengerema district has a total population of 663,034 with the majority of them engaged in agro-pastoralist activities. The poverty and agro-pastoralist activities are risk factors for neglected diseases include brucellosis [11].

This study was conducted to determine seroprevalence and predictors of Brucella infection among agro-pastoral communities in Sengerema district. This information may be useful in influencing public awareness on the possible risk factors for infection as well as considering it in diagnosis of febrile illnesses especially in these communities.

Methods

Data collection and laboratory procedures

A cross-sectional community-based study was carried out between July and September 2008 in ten agro-pastoral villages in Sengerema district namely Kasungamile, Kabusuli, Lubungo, Magutu, Mami, Ngoma A, Ngoma B, Nyalwambu, Sota and Sota Kaningu. Sociodemographic data and other information related to brucellosis (age, sex, keeping cattle, contact with blood, touching animal placenta, consuming raw milk etc.) were collected using a standardized data collection tool. After obtaining written informed consent, about 4 ml of blood samples were collected using plain Vacutainer tubes (Becton, Dickinson and Company, Nairobi, Kenya) and transported to the Bugando multipurpose laboratory whereby sera were separated and stored in cryovials at −80 °C until processing. Sera were tested for the presence of specific Brucella melitensis and Brucella abortus antibodies using commercial rapid agglutination test according to the manufacturer’s instructions (Eurocell A/M® Euromedi equip LTD.UK). The Eurocell A® is specific for B. abortus and Eurocell M® for B. melitensis. The agglutination test has been found to have 95 % sensitivity with specificity of 100 % [12].

Data management and analysis

Data were entered into a computer using Microsoft Office Excel 2007 and analysed using the STATA version 11 (College Station, Texas, USA). Categorical variables were presented as proportions while continuous variables (age) were summarized as median with interquartile ranges. Stepwise regression model was used to determine factors associated with anti-Brucella antibodies. Univariate analysis was done, and factors with P value <0.2 were fitted on multivariate logistic regression analysis. Unadjusted odds ratio (UAOR), adjusted odds ratio (AOR) and 95 % confidence interval (CI) were noted. P value of <0.05 was considered statistically significant.

Results

Baseline characteristics

A total of 382 participants from agro-pastoral communities in different villages of Sengerema district were recruited with the median age of 30 (interquartile range (IQR) 15–40) years. Males 234 (61.5 %) formed the majority of the study population. Out of 382 participants, 117 (30.6 %) and 245 (64.1 %) were students and agro-pastoralists, respectively. A total of 294 (77 %) participants were found to keep cattle (Table 1).
Table 1

Baseline characteristics of 382 adult participants from Sengerema district

Characteristics

Frequency/median

Percent

Age

30 (IQR 15–40)

 

Sex

 Female

148

38.5

 Male

234

61.5

Occupation

 Students

117

30.6

 Agro-pastoralists

245

64.1

 Othersa

20

5.2

Keep cattle

 No

88

23.0

 Yes

294

77.0

aBusinessmen, teachers and fishermen

Prevalence of specific anti-Brucella antibodies

Overall, seroprevalence of brucellosis was found to be 14.1 % (54/382, 95 % CI 10.6–17.5). Seroprevalence of B. melitensis antibodies was found to be 11 % (42/382, 95 % CI 7.8–14.1) while for B. abortus was 7 % (26/282, 95 % CI 4.4–9.5), P = 0.026. Seroprevalence of anti-Brucella antibodies indicative of co-infection with both B. melitensis and B. abortus was found to be 3.6 % (14/382, 95 % CI 1.7–5.4).

Factors associated with the presence of specific anti-Brucella antibodies

The median age of participants who tested positive for B. melitensis antibodies was 30 (IQR 19–40) years compared to 30 (IQR 15–40) years for those tested negative (P = 0.489). Males had significantly higher B. melitensis antibodies than females (14.5 vs. 5.4 %, P = 0.008). On multivariate logistic regression analysis, male sex (AOR 3.2, 95 % CI 1.3–7.5, P = 0.007), touching goat placenta (AOR 2.54, 95 % CI 1.05–6.14, P = 0.012) and agro-pastoralist occupation (AOR 2.07, 95 % CI 1.01–4.24, P = 0.04) were found to predict B. melitensis infection (Table 1).

Regarding B. abortus, there was no significant difference between male and female sex (8.5 vs. 4.1 %, P = 0.097). On univariate logistic regression analysis, agro-pastoralists were more likely to contract B. abortus infection than students (OR 7.3, 95 % CI 1.71–31.51, P = 0.007). Only occupation (OR 7.44, 95 % CI 1.42–38.9, P = 0.02) remained significant predicting B. abortus infection when adjusted for age, touching placenta, touching goat placenta and blood splash (Table 2).
Table 2

Factors associated with B. melitensis seropositivity among 382 adults from agro-pastoral communities in Sengerema district

Characteristics

B. melitensis seropositivity

Unadjusted OR (95 % CI)

P value

Adjusted OR (95 % CI)

P value

Age (years)*

42 (IQR 19–40)

1.0 (0.98–1.02)

0.628

  

Sex

 Female (148)

8 (5.4 %)

1

   

 Male (234)

34 (14.5 %)

2.9 (1.33–6.62)

0.008

3.2 (1.3–7.5)

0.007

Occupation

 Students (117)

10 (8.5 %)

1

   

 Agro-pastoralists (245)

32 (13.1 %)

1.9 (0.90–4.01)

0.088

2.07 (1.01–4.24)

0.04

Keep cattle

 No (88)

9 (10.2 %)

1

   

 Yes (294)

33 (11.2 %)

1.1 (0.5–2.41)

0.793

  

Touch placenta

 No (289)

28 (9.7 %)

1

   

 Yes (93)

14 (15.1 %)

1.65 (0.82–3.29)

0.153

0.75 (0.34–1.67)

0.493

Touch goat placenta

 No (341)

32 (9.4 %)

1

   

 Yes (41)

10 (24.4 %)

3.11 (1.4–6.9)

0.005

2.59 (1.25–6.38)

0.012

Blood splash

 No (360)

37 (10.3 %)

1

   

 Yes (22)

5 (22.7 %)

2.5 (0.89–7.4)

0.079

1.5 (0.47–4.98)

0.47

*Median

Overall, males (18.4 vs. 7.4 %, P = 0.004) and agro-pastoralists (18.0 vs. 8.5 %, P = 0.005) had significantly higher rates of Brucella-specific antibodies than females and students, respectively (Table 3). These factors were independently found to be associated with Brucella infection with either of the two species (Table 4). On multivariate logistic regression analysis, male sex (OR 3.07, 95 % CI 1.45–6.51, P = 0.003) and being agro-pastoralist (OR 2.98, 95 % CI 1.38–6.43, P = 0.005) were found to predict the presence of Brucella-specific antibodies when adjusted to touching placenta and touching goat placenta.
Table 3

Factors associated with B. abortus seropositivity among 382 adults from agro-pastoral communities in Sengerema district

Characteristics

B. abortus seropositivity

Unadjusted OR (95 % CI)

P value

Adjusted OR (95 % CI)

P value

Age (years)*

30 (IQR 23–47)

1.02 (0.99–1.04)

0.069

0.98 (0.96–1.01)

0.489

Sex

 Female (148)

6 (4.05 %)

1

   

 Male (234)

20 (8.5 %)

2.2 (0.87–5.64)

0.097

2.1 (0.753–6.14)

0.152

Occupation

 Students (117)

2 (1.7 %)

1

   

 Agro-pastoralists (245)

24 (9.8 %)

7.3 (1.71–31.51)

0.007

7.44 (1.42–38.9)

0.017

Keep cattle

 No (88)

4 (4.55 %)

1

   

 Yes (294)

22 (7.5 %)

1.69 (0.57–5.07)

0.342

  

Touch placenta

 No (289)

14 (4.84 %)

1

   

 Yes (93)

12 (12.9 %)

2.9 (1.29–6.5)

0.010

1.35 (0.52–3.4)

0.529

Touch goat placenta

 No (341)

20 (5.87 %)

1

   

 Yes (41)

6 (14.63 %)

2.7 (1.04–7.3)

0.042

1.76 (0.59–5.27)

0.307

Blood splash

 No (360)

22 (6.11 %)

1

   

 Yes (22)

4 (18.2 %)

3.4 (1.06–10.9)

0.034

1.89 (0.52–6.88)

0.329

*Median

Table 4

Factors associated with Brucellosis among 382 adults from agro-pastoral communities in Sengerema district

Characteristics

Brucellosis

Unadjusted OR (95 % CI)

P value

Adjusted OR (95 % CI)

P value

Age (years)*

30 (IQR 20–44)

1.01 (0.99–1.02)

0.227

  

Sex

 Female (148)

11 (7.43 %)

    

 Male (234)

43 (18.38 %)

2.80 (1.39–5.63)

0.004

3.07 (1.45–6.51)

0.003

Occupation

 Students (117)

10 (8.5 %)

1

   

 Agro-pastoralists (245)

44 (18.0 %)

2.7 (1.35–5.72)

0.005

2.98 (1.38–6.43)

0.005

Keep cattle

 No (88)

11 (12.5 %)

    

 Yes (294)

43 (14.6 %)

1.20 (0.59–2.43)

0.616

  

Touch placenta

 No (289)

35 (12.1 %)

    

 Yes (93)

19 (20.4 %)

1.86 (1.01–3.45)

0.048

0.86 (0.42–1.75)

0.687

Touch goat placenta

 No (341)

43 (12.6 %)

    

 Yes (41)

11 (26.8 %)

2.5 (1.18–5.44)

0.016

2.10 (0.94–4.71)

0.069

Blood splash

 No (360)

49 (13.6 %)

    

 Yes (22)

5 (22.7 %)

1.87 (0.65–5.30)

0.240

  

*Median

Discussion

Brucellosis is one of the public health concerns due its potential in causing human infection and economic loses among agro-pastoralists [13]. Despite having impact on livelihoods, it is one of the neglected tropical diseases in most of the developing countries. Despite this study being conducted 8 years ago, the situation now is comparable to the time the study was conducted. In the present study, a significant proportion of agro-pastoralists was infected with B. melitensis which is comparable to previous studies [1419]. On the contrary, the prevalence observed in this study is lower as compared to what has been reported earlier in Nigeria, Libya and Kenya [13, 20, 21]. The difference could be attributed by the fact that these previous studies were done among febrile patients and butcher workers which are among high-risk groups for brucellosis. In addition, the seroprevalence of B. abortus in this study was found to be significantly lower than that of B. melitensis which is in agreement with previous study [22].

Among the risk factors assessed, male sex, agro-pastoral occupation and touching goat placenta were found to be associated with B. melitensis infection among agro-pastoral communities which is consistent to previous reports [14, 20, 2327]. Meanwhile, agro-pastoralism was the only factor found to predict B. abortus infection while male sex and agro-pastoralism were found to predict the presence of Brucella antibodies. The finding of touching goat placenta predicting B. melitensis infection confirms its presence in goat and sheep as the main host [28]. On the other side, male sex and agro-pastoralism were found to predict brucellosis as previously observed [29, 30]. Predominance of male sex and agro-pastoralism could be explained by the traditional roles of males in these communities whereby they are much more involved in livestock care as compared to female counterparts. Other studies have documented female sex to be risk factors for brucellosis, and this could be explained by female involvement in agro-pastoral activities, signifying the importance of occupation as the major risk factor for contracting Brucella infection [31].

One of the major limitations of the study is the recall bias; majority of the study participants might have forgotten the previous risk behaviour regarding brucellosis. The other limitation is inability to distinguish past and present infections. Despite these limitations, the information the data obtained will help in improving the diagnosis of other causes of fever in developing countries.

Conclusions

There is high seroprevalence of anti-Brucella antibodies among agro-pastoralists in Tanzania. With a decreased trend in malaria infections, diagnosis of other causes of febrile illnesses should be considered in these agro-pastoral communities.

Abbreviations

AOR: 

Adjusted odds ratio

BMC: 

Bugando Medical Centre

CI: 

Confidence interval

CUHAS: 

Catholic University of Health and Allied Sciences

IQR: 

Interquartile range

UAOR: 

Unadjusted odds ratio

VIC: 

Veterinary Investigation Centre

Declarations

Acknowledgements

The authors would like to acknowledge the technical support provided by Mr. Vitus Silago and all the staff at Veterinary Investigation Centre (VIC) Mwanza, Sengerema district council and Microbiology/Immunology department-CUHAS-Bugando. This study was supported by a research grant from Touch Foundation to EBM.

Funding

This study was supported by a research grant from CUHAS/Bugando to EBM. Funders had no role in this study.

Availability of data and materials

All data have been included in the manuscript.

Authors’ contributions

MMM, EBM and SEM participated in the design of the study. MMM and EBM did the data collection. SW performed the tests. MMM and SEM analysed and interpreted the data. MMM wrote the first draft of the manuscript. SEM and EBM did the critical review of the manuscript. All authors read and approved the final version of the manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

The protocol for conducting the study was approved by the Joint Catholic University of Health and Allied Sciences/Bugando Medical Centre (CUHAS/BMC) research ethics and review committee (CREC) with ethical clearance number CREC/001/07/2007. Written informed consent was obtained from each participant prior recruitment to the study.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Veterinary Pathology, Sokoine University of Agriculture
(2)
Department of Microbiology and Immunology, Weill Bugando School of Medicine, Catholic University of Health and Allied Sciences

References

  1. Pappas G, Papadimitriou P, Akritidis N, Christou L, Tsianos EV. The new global map of human brucellosis. Lancet Infect Dis. 2006;6(2):91–9.View ArticlePubMedGoogle Scholar
  2. McDermott JJ, Arimi S. Brucellosis in Sub-Saharan Africa: epidemiology, control and impact. Vet Microbiol. 2002;90(1):111–34.View ArticlePubMedGoogle Scholar
  3. Pappas G, Akritidis N, Tsianos E. Effective treatments in the management of brucellosis. Expert Opin Pharmacother. 2005;6(2):201–9.View ArticlePubMedGoogle Scholar
  4. Makita K, Fèvre EM, Waiswa C, Kaboyo W, De Clare Bronsvoort BM, Eisler MC, Welburn SC. Human brucellosis in urban and peri‐urban areas of Kampala, Uganda. Ann N Y Acad Sci. 2008;1149(1):309–11.View ArticlePubMedGoogle Scholar
  5. Corbel MJ. Brucellosis in humans and animals. Geneva: World Health Organization; 2006.Google Scholar
  6. Kunda J, Fitzpatrick J, Kazwala R, French NP, Shirima G, MacMillan A, Kambarage D, Bronsvoort M, Cleaveland S. Health-seeking behaviour of human brucellosis cases in rural Tanzania. BMC Public Health. 2007;7(1):1.View ArticleGoogle Scholar
  7. Mutanda L. Selected laboratory tests in febrile patients in Kampala, Uganda. East Afr Med J. 1998;75(2):68–72.PubMedGoogle Scholar
  8. Andriopoulos P, Tsironi M, Deftereos S, Aessopos A, Assimakopoulos G. Acute brucellosis: presentation, diagnosis, and treatment of 144 cases. Int J Infect Dis. 2007;11(1):52–7.View ArticlePubMedGoogle Scholar
  9. Roop II RM, Gaines JM, Anderson ES, Caswell CC, Martin DW. Survival of the fittest: how Brucella strains adapt to their intracellular niche in the host. Med Microbiol Immunol. 2009;198(4):221–38.View ArticlePubMedGoogle Scholar
  10. Kazungu KG, Cheyo MB. Government expenditure on growth strategies and poverty reduction in Tanzania. What have we learned? Afr J Econ Rev. 2014;2(1):38–47.Google Scholar
  11. National Bureau of Statistics IM. Tanzania demographic and health survey 2010. 2011.Google Scholar
  12. Memish Z, Almuneef M, Mah M, Qassem L, Osoba A. Comparison of the Brucella Standard Agglutination Test with the ELISA IgG and IgM in patients with Brucella bacteremia. Diagn Microbiol Infect Dis. 2002;44(2):129–32.View ArticlePubMedGoogle Scholar
  13. Ducrotoy MJ, Bertu WJ, Ocholi RA, Gusi AM, Bryssinckx W, Welburn S, Moriyon I. Brucellosis as an emerging threat in developing economies: lessons from Nigeria. PLoS Negl Trop Dis. 2014;8(7):e3008.View ArticlePubMedPubMed CentralGoogle Scholar
  14. Tumwine G, Matovu E, Kabasa JD, Owiny DO, Majalija S. Human brucellosis: seroprevalence and associated risk factors in agro-pastoral communities of Kiboga District, Central Uganda. BMC Public Health. 2015;15(1):1.View ArticleGoogle Scholar
  15. Ogola E, Thumbi S, Osoro E, Munyua P, Omulo S, Mbatha P, Ochieng L, Marwanga D, Njeru I, Mbaabu M. Seroprevalence of brucellosis in humans and their animals: a linked cross-sectional study in two selected counties in Kenya. Online J Public Health Inform. 2014;6:1.View ArticleGoogle Scholar
  16. Sofian M, Aghakhani A, Velayati AA, Banifazl M, Eslamifar A, Ramezani A. Risk factors for human brucellosis in Iran: a case-control study. Int J Infect Dis. 2008;12(2):157–61.View ArticlePubMedGoogle Scholar
  17. Husseini AS, Ramlawi AM. Brucellosis in the West Bank, Palestine. Saudi Med J. 2004;25(11):1640–3.PubMedGoogle Scholar
  18. Kalaajieh W. Epidemiology of human brucellosis in Lebanon in 1997. Med Mal Infect. 2000;30(1):43–6.View ArticleGoogle Scholar
  19. Elbeltagy K. An epidemiological profile of brucellosis in Tabuk Province, Saudi Arabia. 2001.Google Scholar
  20. Ahmed M, Elmeshri S, Abuzweda A, Blauo M, Abouzeed Y, Ibrahim A, Salem H, Alzwam F, Abid S, Elfahem A. Seroprevalence of brucellosis in animals and human populations in the western mountains region in Libya, December 2006–January 2008. Euro Surveill. 2010;15(30):19625–8.PubMedGoogle Scholar
  21. Muriuki S, McDermott J, Arimi S, Mugambi J, Wamola I. Criteria for better detection of brucellosis in the Narok District of Kenya. East Afr Med J. 1997;74(5):317–20.PubMedGoogle Scholar
  22. Swai ES, Schoonman L. Human brucellosis: seroprevalence and risk factors related to high risk occupational groups in Tanga Municipality, Tanzania. Zoonoses Public Health. 2009;56(4):183–7.View ArticlePubMedGoogle Scholar
  23. Wu G, Yang C. Prevalence study of brucellosis among high-risk people in Xinjiang region, China. Microbiol Discov. 2013;1(1):2.View ArticleGoogle Scholar
  24. Aworh MK, Okolocha E, Kwaga J, Fasina F, Lazarus D, Suleman I, Poggensee G, Nguku P, Nsubuga P. Human brucellosis: seroprevalence and associated exposure factors among abattoir workers in Abuja, Nigeria-2011. Pan Afr Med J. 2013;16:103.View ArticlePubMedPubMed CentralGoogle Scholar
  25. Abdollahi A, Morteza A, Khalilzadeh O, Rasoulinejad M. Brucellosis serology in HIV-infected patients. Int J Infect Dis. 2010;14(10):e904–6.View ArticlePubMedGoogle Scholar
  26. Rahman AA, Dirk B, Fretin D, Saegerman C, Ahmed MU, Muhammad N, Hossain A, Abatih E. Seroprevalence and risk factors for brucellosis in a high-risk group of individuals in Bangladesh. Foodborne Pathog Dis. 2012;9(3):190–7.View ArticlePubMedGoogle Scholar
  27. Tsend S, Baljinnyam Z, Suuri B, Dashbal E, Oidov B, Roth F, Zinstag J, Schelling E, Dambadarjaa D. Seroprevalence survey of brucellosis among rural people in Mongolia. Western Pacific Surveill Res J. 2014;5(4):13.View ArticleGoogle Scholar
  28. Young EJ. Brucella spp. In: Principles and practice of clinical bacteriology. 2nd ed. West Sussex, England: John Wiley & Sons Ltd; 2006. p. 265–72.View ArticleGoogle Scholar
  29. Shirima G, Fitzpatrick J, Kunda J, Mfinanga G, Kazwala R, Kambarage D, Cleaveland S. The role of livestock keeping in human brucellosis trends in livestock keeping communities in Tanzania. Tanzan J Health Res. 2010;12(3):203–7.View ArticleGoogle Scholar
  30. Assenga JA, Matemba LE, Malakalinga JJ, Muller SK, Kazwala RR. Quantitative analysis of risk factors associated with brucellosis in livestock in the Katavi-Rukwa ecosystem, Tanzania. Trop Anim Health Prod. 2016;48(2):303–9.View ArticlePubMedGoogle Scholar
  31. Kansiime C, Rutebemberwa E, Asiimwe BB, Makumbi F, Bazira J, Mugisha A. Annual trends of human brucellosis in pastoralist communities of south-western Uganda: a retrospective ten-year study. Infect Dis Poverty. 2015;4(1):1.View ArticleGoogle Scholar

Copyright

© The Author(s) 2016

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