Global Distribution, Host Range and Prevalence of Trypanosoma Vivax: A Systematic Review and Meta-Analysis

DOI: https://doi.org/10.21203/rs.3.rs-93405/v1

Abstract

Background Trypanosomosis caused by Trypanosoma vivax is one of the diseases threatening the health and productivity of livestock in Africa and Latin America. T. vivax is mainly transmitted by tsetse flies; however, the parasite has acquired the ability to be also transmitted mechanically by hematophagous dipterans. Understanding its distribution, host range and prevalence is a key step in local and global efforts to control the disease.

Methods The study was conducted according to the methodological recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist. A systematic literature search was conducted on three search engines, namely Pubmed, Scopus and CAB Direct, to identify all publications reporting natural infection of T. vivax across the world. All the three search engines were screened using the search term Trypanosome vivax without time and language restrictions. Publications on T. vivax that met our inclusion criteria were considered for systematic review and meta-analysis.

Result The study provides a global database of T. vivax, consisting of 899 records from 245 peer reviewed articles in 41 countries. A total of 232,6277 tests were performed on 97 different mammalian hosts, including a wide range of wild animals. Natural infections of T. vivax were recorded in 39 different African and Latin American countries and 47 mammalian host species. All the 245 articles were included into the qualitative analysis, while information from 186 cross-sectional studies was used in the quantitative analysis mainly to estimate the pooled prevalence. Pooled prevalence estimates of T. vivax in buffalo, cattle, dog, dromedary camel, equine, pig, small ruminant and wild animals were 30.6%, 6.4%, 2.6%, 8.4%, 3.7%, 5.5%, 3.8% and 12.9%, respectively. Stratified according to the diagnostic method, the highest pooled prevalences were found with serological techniques in domesticated buffalo (57.6%) followed by equine (50.0%) and wild animals (49.3%).

Conclusion The study provides a comprehensive dataset on the geographical distribution and host range of T. vivax and demonstrates the potential of this parasite to invade other countries out of Africa and Latin America.

Introduction

Trypanosomes are protozoan parasites belonging to the family of Trypanosomatidae and the genus Trypanosoma (T.). The genus Trypanosoma comprises many species such as T. brucei, T. congolense, T. equiperdum, T. evansi, T. simiae, T. suis and T. vivax, that cause diseases called trypanosomoses in different mammalian hosts including humans [1]. Trypanosomoses are widely distributed in Africa, Latin America and Asia [2, 3].

T. vivax is one of the most important Trypanosoma species known to infect both domestic and wild ungulates [4, 5]. T. vivax is reported from cattle, dromedary camel, [6], goat, sheep, pig, dog [7], horse, donkey [8], buffalo, warthog, hippopotamus, reedbuck, waterbuck [9], antelope [10], giraffe [11], rhinoceros [12], rodents, pangolin, primates, reptiles and different wild ungulates and carnivores [13]. In Sub-Saharan Africa, T. vivax is mainly transmitted by tsetse flies (Diptera: Glossinidae) in which the parasite can multiply and remain infective throughout the insect’s life [14]. The parasite has acquired the ability to be also transmitted mechanically by hematophagous flies like Tabanus spp., Stomoxys calcitrans and Haematobia irritans, which are responsible for the spread of T. vivax in tsetse free areas of Africa and in Latin America [4, 1518]

T. vivax infection can be suspected by clinical and/or serological evidence and can be confirmed by parasitological or molecular methods [19]. Reported prevalences of T. vivax show considerable variation with geography, abundance of tsetse or blood sucking flies, and host species. In tsetse infested areas of tropical Africa, the T. vivax prevalence is typically reported between 5–15% and often accounts for up to half of the total trypanosome prevalence. Outside of the tsetse belt, T. vivax prevalence is lower between 2–10% and it is related to local and seasonal variation in biting fly abundance [20].

Trypanosomosis caused by T. vivax is an important cause of economic losses related to morbidity, mortality, reproductive issues and decreased production [4]. For example, economic losses associated with bovine trypanosomosis have been estimated to be around US$5 billion a year in Africa and the continent spend at least $30 million every year to control bovine trypanosomosis in terms of curative and prophylactic treatments [21]. Estimates outside Africa indicate that more than 11 million head of cattle with a value of more than US$ 3 billion are at risk from T. vivax infection in the Brazilian Pantanal and Bolivian lowlands, with potential losses in excess of US$ 160 million [16].

Large numbers of studies have been conducted on T. vivax over the past 100 years. Studies before 1950's focused more on the morphology and taxonomy [22, 23], pathogenicity [24] and treatment [25, 26]. However, since the 1950's, a considerable number of epidemiological studies have been conducted. Notwithstanding the excellent review on livestock trypanosomoses and their vectors in Latin America [18] and a recent general review on T. vivax [20], a systematic literature review on the global distribution, prevalence and host range of T. vivax is lacking. Moreover, no information on the global distribution of T. vivax is available at the World Animal Health Information System of the World Health Organisation

(https://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/Diseasedistributionmap). Thus, this study was conducted to provide the global distribution of T. vivax and to estimate the pooled prevalence of trypanosomosis caused by T. vivax in naturally infected domestic and wild animals.

Methods

The systematic review and meta-analysis were conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist [27]. Screening and data extraction were performed by two authors (SL and EF) independently. All disagreements were discussed and resolved by consensus. A third author (PB) was also involved in the search for full text papers to ensure that all relevant publications were included.

Literature search

On 30th August 2019, a systematic literature search was conducted on three databases to identify all publications reporting natural infection of T. vivax across the world. Pubmed, Scopus and CAB Direct were screened using the search term Trypanosome vivax without time and language restrictions. All references found were imported into Mendeley Desktop, reference manager software.

Inclusion and exclusion criteria

To be considered articles were required to meet the following inclusion criteria: (1) should be observational studies, published in indexed journals, reporting any natural infection of T. vivax using any diagnostic test or tests available; (2) the study design, sample size, sample type, diagnostic methods, and number of T. vivax infected individuals or prevalence, including 0%, must be provided; (3) species of animals with T. vivax infections must be provided. Experimental studies, publications which fail to describe diagnostic tools, study design and/or sample sources and reports solely based on clinical signs were removed despite reporting the prevalence of the disease. In addition, studies reporting T. vivax from multiple species without stratifying the report at species level were removed.

Data extraction

All relevant information such as author names, year of publication, study period, country, region, province, district, latitude, longitude (if provided or if they can be retrieved), host species, number of samples analyzed, type of samples collected, diagnostic method used, number of positives and prevalence or percentage were extracted to a pre-prepared Microsoft Excel spreadsheet (Microsoft Corp., Redmond, Washington, USA). When publications only reported the number of animals tested and the prevalence, the numbers of positives were calculated. When publications only reported the number of animals tested and the number of positives, prevalence values were calculated. Publications in other languages than English were translated using Google Translate.

Data analysis

Owing to heterogeneity within and between studies, random-effects meta-analysis was used to estimate the pooled prevalence and its 95% confidence interval (CI) in different hosts [28]. The estimation was carried out after categorization of the results according to the diagnostic tests used and the host species tested. Accordingly, diagnostic tests were categorized into three categories: (i) parasitological methods, including wet blood smear, stained blood smear, and microhematocrit concentration; (ii) serological methods, including enzyme-linked immunosorbent assay (ELISA) both antigen and antibody based, indirect fluorescence antibody test (IFAT) and antigen detection LATEX agglutination; (iii) molecular methods, including reverse line blot hybridization assay, real-time and conventional polymerase chain reaction (PCR). Species-wise, sheep and goat were categorized into “small ruminants”, horse, donkey and mule into “equine”, water buffalo and buffalo into “buffalo” and all studied wild animals including Cape buffalo into “wild animals”. For cattle, dromedary camel, pig and dog, pooled prevalence was estimated without categorization.

Heterogeneity between studies was evaluated through the Cochran’s Q test (reported as p value) and the inverse variance index (I2). I2 describes the percentage of observed total variation between studies that is due to heterogeneity rather than to random error (intra-study variation). I2 values less than 25% correspond with low heterogeneity, up to 50% with moderate and up to 75% with high heterogeneity [29]. Sub-group analysis using the variable test method was performed to determine the potential sources of heterogeneity among studies. The across study bias was examined by a funnel plot and Egger’s regression asymmetry test. Funnel plot was used to visually examine the presence of publication bias and Egger’s regression asymmetry test was used to test whether the bias is statistically significant or not [30]. The unbiased estimates were calculated using Duval and Tweedie non-parametric ‘fill and trim’ linear random method [31].

The meta-analysis was done using ‘meta’ package of R statistical software version 3.6.2 (R Foundation for Statistical Computing). The map representing the global distribution of T. vivax was created, using Quantum GIS software version 3.4.5 (Open Source Geospatial Foundation, Boston, USA).

Results

Literature search selectionand data extraction

A total of 1691 publications were retrieved, 348 from PubMed, 1269 from Scopus and 74 from CAB Direct (Figure 1). After removal of 390 duplicates, the remaining 1301 publications were screened based on their titles and abstracts. Reviews and articles reporting on laboratory and field experiments (n=993) were excluded of further analysis. Articles without abstract or without sufficient information to take a decision were left for full text review. Of the remaining 308 articles, 11 the full text file remained inaccessible [32,33,42,34–41]. Finally, one additional reference, missed by the systematic literature search, was included. Full text papers of 298 articles were retrieved online or via the library of the Institute of Tropical Medicine Antwerp and eligibility assessed according to the pre-established inclusion/exclusion criteria. A further 53 articles were excluded thus leaving 245 articles fulfilling all inclusion criteria for the meta-analysis [4,5,43,133–142,44,143–152,45,153–162,46,163–172,47,173–182,48,183–192,49,193–202,50,203–212,51,213–222,52,223–232,6,53,233–242,54,243–252,55,253–262,56,263–272,57,273–277,58–62,7,63–72,8,73–82,9,83–92,10,93–102,12,103–112,13,113–122,14,123–132]. Among these 245 articles published between 1958 and 2019, 10 are case reports, 186 report on a cross sectional study, 35 on a longitudinal study and 14 on an outbreak investigation. All relevant data from these articles were recorded, according to diagnostic method and host species, in a Microsoft Excel file thus containing 899 records used in the meta-analysis (Supplementary file S1).

Of these 245 articles, 187 reported on studies conducted in 27 African countries, with Ethiopia taking the lead with 43 articles, followed by Nigeria with 29, Uganda with 21 and Kenya with 15 articles. Studies conducted in Latin America (including the French departments Martinique and French Guiana) were reported in 57 articles of which 32 from Brazil, 9 from Venezuela and 6 from Colombia.

Geographic distribution

All the studies conducted in the 27 African countries reported the presence of T. vivax in at least one host species; natural T. vivax infections were found in 12 of the 13 studied Latin American countries (Figure 2 and Table 1). In Martinique, Alonso and co-workers didn't find clinical nor serological evidence of T. vivax in cattle on this island [50]. One article mentions a cross-sectional study on 300 equines in Pakistan, but all animals were negative in molecular tests for T. vivax [231]. We couldn't find any other reports on the presence of T. vivax in Asia, Antarctica, Australia, Europe and North America.

Host range

A total of 232,627 tests were performed and 24,420 of them were positive for natural infection of T. vivax. Trypanosoma vivax was reported from 9 domestic animal species: buffalo, cattle, dog, donkey, dromedary camel, goat, horse, pig and sheep. Among them, cattle were the most studied species with 198,593 tests performed on cattle in 36 countries and two territories (192 publications) and 20,964 were positive for T. vivax. Next to cattle, goat, sheep, pigs and donkey were the most frequently studied species. The protozoal parasite was also reported from wild animals including diverse species of antelopes, Cape buffalo, hippopotamus, black rhinoceros, pangolin and warthog. Trypanosoma vivax was reported from 39 wild fauna species, including many antelope species and Cape buffalo (Table 2 and 3).

Pooled prevalence estimates according to host species and type of diagnostic test

Pooled prevalence estimates by test methods for different hosts are presented in Table 4 and funnel plots of the meta-analysis and the subgroup analyses can be found in Supplementary files S2 and S3. Substantial heterogeneity was observed in the pooled estimate except for dog, which remained significant even after sub-group analysis.

Cattle: a total of 145 cross-sectional studies from 32 countries were included in estimation of natural infection of T. vivax in cattle. The random effect model indicates the pooled prevalence to be 6.4% (5.7-7.2, 95% CI). High in between studies heterogeneity was observed with 96.8% Higgins I2 test and P=0 Cochran’s Q test. Small ruminants: pooled prevalence of T. vivax estimated from 33 studies in 16 countries was found to be 3.8% (2.5-5.6, 95% CI). The 93.2% I2 and P<0.0001 Cochran’s Q test values indicate high in between studies heterogeneity. Equines: a total of 15 studies from ten different countries were used to estimate the pooled prevalence of T. vivax in equines. The random effect model estimates the pooled prevalence to be 3.7% (2.0-6.8, 95% CI). High in between studies heterogeneity was observed with 88.9% I2 test value and P<0.0001 Cochran’s Q test. Camel: pooling the prevalence of T. vivax in camels was estimated from four studies in three different countries. The model estimates a pooled prevalence of 8.4% (3.4-19.3, 95% CI) with 94.8% I2 statistics and P<0.0001 Cochran’s Q test which indicates high in between studies heterogeneity. Pig: a total of 12 studies from eight different countries were included in the estimation of pooled prevalence in pigs which was found to be 5.5% (3.0-10.1, 95% CI). High in between studies heterogeneity was observed by 90.1% I2 statistic test and P<0.0001 Cochran’s Q test. Dog: five studies from five countries were used in the estimation pooled prevalence of T. vivax in dogs. The pooled prevalence was estimated to be 2.6% (1.0-6.3% 95% CI). Low in between studies heterogeneity is indicated with 5.9% I2 and P=0.3859 Cochran’s Q test values. Buffalo: three studies reported natural infection of T. vivax in domestic buffaloes from Venezuela and the random effect model estimates a pooled prevalence of 30.6% (14.2-54.1, 95% CI) with high in between studies heterogeneity of 98.4% I2 and P<0.0001 Cochran’s Q tests. Wild animals: a pooled prevalence of 12.9% (9.9-16.6, 95% CI) was estimated from six studies in five countries. High in between studies heterogeneity was indicated in 76.7% I2 Higgin’s test and P<0.0001 Cochran’s Q test value.

Subgroup pooled prevalences estimated according to the type of diagnostic test, as represented in Table 4, were lowest with parasitological techniques (from 1.1% in pigs to 13.2% in wild animals) and highest with serological techniques (from 13.8% in small ruminants to 57.6% in buffalo).

Publication bias

The presence of publication bias was analyzed only in five species since there were not enough publications to discuss its possible influence in camel, buffalo and dogs. Possible publication bias was demonstrated by visualization of asymmetry in funnel plots for cattle (Figure 3A), small ruminants (Figure 3B), equines (Figure 3C), pigs (Figure 3D) and wild animals (Figure 3E). It was further confirmed by ‘metabias’ test (Egger’s test) with p value less than 0.05. The `trimfill` method imputed 170, 43, 30, 27 and 11 studies to obtain symmetry in funnel plots in cattle, wild animals, equines, small ruminants and pigs respectively. The new estimated prevalence equals to 14.8% for cattle, 26.8% for wild animals, 21.6% for equines, 9.5% for small ruminants and 24.5% for pigs.

Discussion

This study presents the first systematic review of published literature since the 1950s describing global distribution, host range and prevalence of trypanosomosis caused by T. vivax. Not surprisingly, most publications report on T. vivax infections in domestic mammalian species, in particular in cattle and small ruminants, while few publications describe natural infections in wildlife.

Looking at the T. vivax distribution map (Fig. 1), there is an evident data gap for some sub-Saharan African countries where tsetse flies are present and therefore T. vivax may be endemic. Although our formal search strategy couldn't retrieve any publication on these "missing" countries, conventional Google search confirms the presence of T. vivax in South Sudan and Zimbabwe [285, 286] and Genevieve et al [287] reported on the presence of potential vectors in Central African Republic. Since Angola, the Central African Republic and the Republic of Congo are endemic for human African trypanosomosis, the presence of T. vivax in these countries is likely [288]. Due to its adaptation to mechanical transmission, T. vivax is also present outside the tsetse belt in Africa, e.g. in Ethiopia and Sudan [114, 289]. As a consequence, the trypanosomosis control efforts with focus on tsetse eradication might have little effect on T. vivax. Also, economic impact assessments that are solely based on tsetse distribution alone could seriously underestimate the problem of trypanosomosis due to T. vivax.

Out of Africa, T. vivax is present in Latin America but not in North America, Australia, Asia and the Pacific regions. T. vivax is believed to be introduced into Latin America in cattle and horse imported from Africa, possibly in the 16th century and spread to different Latin American countries including Brazil, Colombia, French Guiana, Guadeloupe, Guyana, Martinique, Panama, Suriname and Venezuela [18]. Stephen [290] reviewed the presence of the parasite in Costa Rica, Ecuador, El Salvador, Paraguay, and Peru and according to Gardiner et al [15], T. vivax was present in the Caribbean thus posing a threat to the livestock industries. From our literature search we can only confirm T. vivax to be endemic in 12 Latin American countries of which 7 (Argentina, Bolivia, Brazil, Colombia, Guyana, Peru, Venezuela) are also endemic for T. evansi [291]. Apparently, T. vivax has never spread into Asia, unlike T. evansi although similar to the latter; it can be mechanically transmitted by bloodsucking flies. Unless there is a particular biological or environmental factor preventing T. vivax to invade the Middle East and Asia, as well Northern Africa, North America and Europe, we must remain alert about the risk of importing T. vivax into non-endemic countries as it happened with Latin America.

This review suggests that T. vivax has a very diverse host range, including 9 domestic mammals and almost 40 wild fauna species. Regarding the latter however, data should be interpreted with caution. Diagnostic tests, whether parasitological, serological or even molecular, have their limitations. For examples, by sequencing of PCR amplicons, Auty and co-workers [11] clearly demonstrate that wildlife may harbor a diversity of trypanosomes, including taxonomically undefined species. Therefore, it is likely that many reports on T. vivax infection in wildlife and tsetse in fact deal with other trypanosome species that are not necessarily pathogenic for domestic animals.

The pooled prevalence of trypanosomosis in different hosts varies significantly depending on the detection methods; significantly higher estimates were reported in publications using serological techniques. Higher estimates using serological technique could be due to the persistence of antibody over several months after curative treatment and the possibility of low undetectable parasitemia in parasitological techniques [20, 93, 292, 293]. Moti et al [187] compared the percentage positivity obtained with different diagnostic techniques and showed that relative to the microhaematocrit centrifugation technique, the percent positivity increased by 50 and 250% when using PCR-RFLP. Also Garcia et al [118] reported that the detection of trypanosomes, PCR-based assays are twice as sensitive as parasitological techniques such as the microhaematocrit centrifugation.

The study has the following limitations. The literature search was almost exclusively based on electronic databases whereby some older literature must have been missed. The data showed a large degree of heterogeneity among studies, which remain significant after sub-group analysis. There is a significant publication bias which could be due to incomplete or inaccurate information provided in the publications. In addition, studies were conducted between 1956 and 2017 and the result may not accurately reflect the current epidemiological situation and therefore could limit interpretation of the result to some degree. Furthermore, we suspect numerous data gaps mainly because of two reasons. Firstly, due to lack of a country level monitoring and reporting system for trypanosomosis, most of the data included in this analysis is from research activities. Secondly, trypanosomosis diagnosis in most endemic countries relied to a great extent on low-sensitivity parasitological methods, while more sensitive molecular tools are rarely used. Thus, prevalences presented here may significantly underestimate the real situation and the economic impact of T. vivax trypanosomosis in Africa and Latin America.

Conclusion

With this study, we intended to provide comprehensive information on the geographical distribution, host range and prevalence of trypanosomosis caused by T. vivax worldwide. The results confirm the wide geographical distribution and a diverse host range of T. vivax. The parasite parasitizes almost all domestic mammals and many wild animal species thus suggesting the potential to get established in other countries with favorable environmental conditions, e.g. in the Middle East, Asia and Australia. The meta-analysis showed a high degree of variability in estimated prevalence values. The variability can be attributed to diagnostic tests used and the species of the animal infected.

Declarations

Funding

No funding was available for this study

Availability of data and materials

All data analyzed in this paper are provided as supplementary file.

Authors╩╝ contributions

P.B. and F.R. conceived the research and S.L. designed the research, and E.F. and S.L. drafted the manuscript. E.F., S.L. and P.B. extracted and compiled the data. All authors read and approved the final version.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

References

  1. Stevens J., Brisse S. Systematics of Trypanosomes of Medical and Veterinary Importance. In: Maudlin I, Holmes P., Miles M., editors. Trypanos. CABI Publishing; 2004. p. 1–19.
  2. Luckins AG, Dwinger RH. Non-tsetse-transmitted Animal Trypanosomiasis. In: Maudlin I, Holmes PH, Miles MA, editors. Trypanos. CABI Publishing; 2004. p. 269–79.
  3. Cecchi G, Paone M, Feldmann U, Vreysen MJB, Diall O, Mattioli RC. Assembling a geospatial database of tsetse-transmitted animal trypanosomosis for Africa. Parasit Vectors. 2014;7:1–10.
  4. Vieira OLE, Macedo LO de, Santos MAB, Silva JABA, Mendonca CL de, Faustino MA da G, et al. Detection and molecular characterization of Trypanosoma (Duttonella) vivax in dairy cattle in the state of Sergipe, northeastern Brazil. Rev Bras Parasitol Vet. Brazil; 2017;26:516–20.
  5. Kassian EN, Simuunza MC, Silayo RS, Moonga L, Ndebe J, Sugimoto C, et al. Prevalence and risk factors of bovine trypanosomosis in Kilwa district, Lindi region of southern Tanzania. Vet Parasitol Reg Stud Reports. 2017;9:1–5.
  6. Birhanu H, Fikru R, Said M, Kidane W, Gebrehiwot T, Hagos A, et al. Epidemiology of Trypanosoma evansi and Trypanosoma vivax in domestic animals from selected districts of Tigray and Afar regions, Northern Ethiopia. Parasit Vectors. 2015;8:212.
  7. Nimpaye H, Njiokou F, Njine T, Njitchouang GR, Cuny G, Herder S, et al. Trypanosoma vivax, T. congolense “forest type” and T. simiae: prevalence in domestic animals of sleeping sickness foci of Cameroon. Parasite. 2011;18:171–9.
  8. Pinchbeck GL, Morrison LJ, Tait A, Langford J, Meehan L, Jallow S, et al. Trypanosomosis in the Gambia: Prevalence in working horses and donkeys detected by Whole Genome Amplification and PCR, and evidence for interactions between trypanosome species. BMC Vet Res. 2008;4.
  9. Anderson NE, Mubanga J, Fevre EM, Picozzi K, Eisler MC, Thomas R, et al. Characterisation of the wildlife reservoir community for human and animal trypanosomiasis in the Luangwa Valley, Zambia. PLoS Negl Trop Dis. 2011;5.
  10. Guedegbe B, Verhulst A, Van Meirvenne N, Pandey VS, Doko A. Serological evidence of the existence of a wild reservoir of Trypanosoma brucei gambiense in the Pendjari biosphere reservation in the Republic of Benin. Ann Soc Belg Med Trop. 1992;72:113–20.
  11. Auty H, Anderson NE, Picozzi K, Lembo T, Mubanga J, Hoare R, et al. Trypanosome Diversity in Wildlife Species from the Serengeti and Luangwa Valley Ecosystems. PLoS Negl Trop Dis. 2012;6.
  12. Mihok S, Otieno LH, Tarimo CS. Trypanosome infection rates in tsetse flies (Diptera: Glossinidae) and cattle during tsetse control operations in the Kagera River region of Rwanda. Bull Entomol Res. 1992;82:361–7.
  13. Njiokou F, Simo G, Nkinin SW, Laveisseìre C, Herder S. Infection rate of Trypanosoma brucei s.l., T. vivax, T. congolense “forest type”, and T. simiae in small wild vertebrates in south Cameroon. Acta Trop. 2004;92:139–46.
  14. Suh PF, Njiokou F, Mamoudou A, Ahmadou TM, Mouhaman A, Garabed R. Bovine trypanosomiasis in tsetse-free pastoral zone of the far-North region, Cameroon. J Vector Borne Dis. 2017;54:263–9.
  15. Gardiner PR, Pearson TW, Clarke MW, Mutharia LM. Identification and isolation of a variant surface glycoprotein from Trypanosoma vivax. Science (80- ). 1987;235:774–7.
  16. Jones TW, Dávila AMR. Trypanosoma vivax - Out of Africa. Trends Parasitol. 2001. p. 99–101.
  17. Davila AM, Silva RA. Animal trypanosomiasis in South America: Current status, partnership, and information technology. Ann N Y Acad Sci. 2000;916:199–212.
  18. Desquesnes M. Livestock Trypanosomoses and Their Vectors in Latin America, CIRAD-EMVT publication, OIE, Paris, France, 2004.
  19. Osório ALAR, Madruga CR, Desquesnes M, Soares CO, Ribeiro LRR, Da Costa SCG, et al. Trypanosoma (Duttonella) vivax: Its biology, epidemiology, pathogenesis, and introduction in the New World - A review. Mem Inst Oswaldo Cruz. 2008;103:1–13.
  20. Dagnachew S, Bezie M. Review on Trypanosoma vivax. African J Basic Appl Sci. 2015;7:41–64.
  21. Angara TE., Ismail A., Ibrahim A. An Overview on the Economic Impacts of Animal Trypanosomiasis. Glob J Res Anal. 2012;3:275–6.
  22. Hoare CA, Broom JC. Morphological and taxonomic studies on mammalian trypanosomes. Trans R Soc Trop Med Hyg. 1938;31:517–34.
  23. Hoare CA, Broom JC. Morphological and taxonomic studies on mammalian trypanosomes. vii.—differentiation of Trypanosoma uniforme and T. vivax in mixed infections. Trans R Soc Trop Med Hyg. 1939;32:629–32.
  24. Hornby HE. The pathogenicity to cattle of Trypanosoma vivax. Vet Rec. 1946;58:178.
  25. Schwetz J. Treatment of Trypanosoma vivax infection. Trans R Soc Trop Med Hyg. 1929;23:109.
  26. Fiennes RNTW. The treatment experiments with Trypanosoma vivax (Ziemann) disease of cattle. Vet Rec. 1948;60:302.
  27. Moher D, Liberati A, Tetzlaff J, Altman D, Group TP. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA Statement. PLoS Med. 2009;6:e1000097.
  28. Hedges L, Vevea J. Fixed- and random-effects models in meta-analysis. Psychol Methods. 1998;3:486–504.
  29. Higgins JPT, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–58.
  30. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple graphical test. BMJ. 1997;315:629–34.
  31. Duval S, Tweedie R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000;56:455–63.
  32. Baptista Filho LCF, Fernandes AC de C, Silva TIB da, Souza ACM de, Sandes HMM, Alves LC, et al. Trypanosoma vivax infection in dairy cattle raised in the State of Pernambuco: case report. Veterinária e Zootec. 2011;18:919–22.
  33. Bolívar AM, Rojas A, Rosales D, Torres Y, García-Lugo P. Detection of hemotropic agents in a livestock farm using PCR and DGGE. Rev Salud Anim. La Habana: Centro Nacional de Sanidad Agropecuaria; 2014;36:53–7.
  34. Carvalho AU, Abrão DC, Facury Filho EJ, Paes PRO, Ribeiro MFB. Occurrence of Trypanosoma vivax in Minas Gerais state, Brazil. Arq Bras Med Vet e Zootec. 2008;60:769–71.
  35. Fidelis Junior OL, Cadioli FA, Barnabé P de A, Machado RZ, Teixeira MMG, Marques LC. Trypanosomiasis in dairy cattle in São Paulo state. Veterinária e Zootec. 2011;18:879–82.
  36. Gonzales JL, Jones TW, Picozzi K, Cuellar HR. Evaluation of a polymerase chain reaction assay for the diagnosis of bovine trypanosomiasis and epidemiological surveillance in Bolivia. Kinetoplastid Biol Dis. 2003;2.
  37. Kalu AU, Uzoukwu M, Ikeme M. Prevalence of tsetse fly and ruminant trypanosomosis in Katsina-Ala Local Government Area, Nigeria. Roum Arch Microbiol Immunol. 1996;55:341–52.
  38. Kamani J, Sannusi A, Egwu OK, Dogo GI, Tanko TJ, Kemza S, et al. Prevalence and significance of haemoparasitic infections of cattle in North- Central, Nigeria. Vet World. 2010;3:445–8.
  39. Katunguka-Rwakishaya E. The prevalence of trypanosomosis in small ruminants and pigs in a sleeping sickness endemic area of Buikwe County, Mukono district, Uganda. Rev Elev Med Vet Pays Trop. 1996;49:56–8.
  40. Magona JW, Mayende JSP. Occurrence of concurrent trypanosomosis, theileriosis, anaplasmosis and helminthosis in Friesian, Zebu and Sahiwal cattle in Uganda. Onderstepoort J Vet Res. 2002;69:133–40.
  41. Plagemann O. Epidemiological survey of trypanosomiasis in cattle in Northern Uganda. Berl Munch Tierarztl Wochenschr. 1974;87:352–5.
  42. Suárez C, García F, Román D, Coronado A, Perrone T, Reyna A, et al. Factores de riesgo asociados a la tripanosomosis bovinaen explotaciones ganaderas de Venezuela. Zootec Trop. 2010;27:363–72.
  43. Abebe R, Wolde A. A cross-sectional study of trypanosomosis and its vectors in donkeys and mules in Northwest Ethiopia. Parasitol Res. 2010;106:911–6.
  44. Abebe R, Gute S, Simon I. Bovine trypanosomosis and vector density in Omo-Ghibe tsetse belt, South Ethiopia. Acta Trop. 2017;167:79–85.
  45. Acapovi-Yao G, Cisse B, Koumba CRZ, Mavoungou JF. Trypanosome infections in cattle in farms of different departments in Côte d’Ivoire. Rev Med Vet (Toulouse). 2016;167:289–95.
  46. Adam Y, Marcotty T, Cecchi G, Mahama CI, Solano P, Bengaly Z, et al. Bovine trypanosomosis in the Upper West Region of Ghana: Entomological, parasitological and serological cross-sectional surveys. Res Vet Sci. 2012;92:462–8.
  47. Ahmed HA, Picozzi K, Welburn SC, MacLeod ET. A comparative evaluation of PCR- based methods for species- specific determination of African animal trypanosomes in Ugandan cattle. Parasit Vectors. 2013;6:316.
  48. Ali D, Bitew M. Epidemiological study of bovine trypanosmosis in Mao-Komo special district, Benishangul Gumuz regional state, Western Ethiopia. Glob Vet. 2011;6:402–8.
  49. Alingu RA, Muhanguzi D, MacLeod E, Waiswa C, Fyfe J. Bovine trypanosome species prevalence and farmers’ trypanosomiasis control methods in south-western Uganda. J S Afr Vet Assoc. 2014;85:1–5.
  50. Alonso M, Camus E, Rodriguez Diego J, Bertaudière L, Tatareau JC, Liabeuf JM. Current status of bovine haemoparasitic diseases in Martinique (French West Indies). Rev Elev Med Vet Pays Trop. 1992;45:9–14.
  51. Alves WP, Cuglovici DA, Furtado LF V, Da Silveira JAG, Facury-Filho EJ, Ribeiro MFB, et al. Comparison of three methods for diagnosis of Trypanosoma (Duttonella) vivax in cattle. Genet Mol Res. 2017;16.
  52. Anene BM, Chime AB, Jibike GI, Anika SM. Prevalence of trypanosomiasis in Zebu cattle at Obudu ranch - a tsetse-free zone in Nigeria. Prev Vet Med. 1991;10:257–60.
  53. Anene BM, Chime AB, Jibike GI, Anika SM. Comparative study of clinical signs, haematology and prevalence of trypanosomiasis in Holstein Friesian and White Fulani Zebu cattle exposed to natural infection in a rain forest zone of Nigeria. Angew Parasitol. 1991;32:99–104.
  54. Angwech H, Nyeko JHPP, Opiyo EA, Okello-Onen J, Opiro R, Echodu R, et al. Heterogeneity in the prevalence and intensity of bovine trypanosomiasis in the districts of Amuru and Nwoya, Northern Uganda. BMC Vet Res. 2015;11:1–8.
  55. Applewhaite LM. Small ruminant trypanosomiasis in Guyana-A preliminary report. Br Vet J. 1990;146:93–4.
  56. Ashcroft MT. An attempt to isolate Trypanosoma rhodesiense from wild animals. Trans R Soc Trop Med Hyg. 1958;52:276–82.
  57. Balyeidhusa ASP, Kironde FAS, Enyaru JCK. Apparent lack of a domestic animal reservoir in Gambiense sleeping sickness in northwest Uganda. Vet Parasitol. 2012;187:157–67.
  58. Bastos TSA, Faria AM, Madrid DM de CM, Bessa LC de, Linhares GFC, Fidelis OLJ, et al. First outbreak and subsequent cases of Trypanosoma vivax in the state of Goias, Brazil. Rev Bras Parasitol Vet. 2017;26:366–71.
  59. Batista JS, Riet-Correa F, Teixeira MMG, Madruga CR, Simoes SD V, Maia TF. Trypanosomiasis by Trypanosoma vivax in cattle in the Brazilian semiarid: Description of an outbreak and lesions in the nervous system. Vet Parasitol. 2007;143:174–81.
  60. Batista JS, Oliveira AF, Rodrigues CMF, Damasceno CAR, Oliveira IRS, Alves HM, et al. Infection by Trypanosoma vivax in goats and sheep in the Brazilian semiarid region: from acute disease outbreak to chronic cryptic infection. Vet Parasitol. 2009;165:131–5.
  61. Batista JS, Rodrigues CMF, Olinda RG, Silva TMF, Vale RG, Camara ACL, et al. Highly debilitating natural Trypanosoma vivax infections in Brazilian calves: epidemiology, pathology, and probable transplacental transmission. Parasitol Res. 2012;110:73–80.
  62. Batista JS, Freitas CIA, Silva JB da, Cavalcante TV, Paiva KAR de, Lopes FC, et al. Clinical evaluation and reproductive indices of dairy cows naturally infected with Trypanosoma vivax. Semin Ciências Agrárias. 2017;38:3031–8.
  63. Behnke JM, Chiejina SN, Musongong GA, Nnadi PA, Ngongeh LA, Abonyi FO, et al. Resistance and resilience of traditionally managed West African Dwarf goats from the savanna zone of northern Nigeria to naturally acquired trypanosome and gastrointestinal nematode infections. J Helminthol. 2011;85:80–91.
  64. Bejano S, Kifle T, Bireda W. Study on the prevalence of bovine trypanosomosis in Assosa district of the BenishanGulgumuz region, West Ethiopia. Livest Res Rural Dev. 2016;28.
  65. Bengaly Z, Kanwe AB, Duvallet G. Evaluation of an antigen detection-ELISA test for the diagnosis of trypanosomiasis in naturally infected cattle. Trop Med Parasitol. 1995;46:284–6.
  66. Bett B, Orenge C, Irungu P, Munga LK. Epidemiological factors that influence time-to-treatment of trypanosomosis in Orma Boran cattle raised at Galana Ranch, Kenya. Vet Parasitol. 2004;120:43–53.
  67. Biryomumaisho S, Melville SE, Atunguka-Rwakishaya E, Lubega GW. Detection of natural Trypanosoma vivax infections in pigs with microhaematocrit centrifugation and amplification of ITS1 rDNA. Onderstepoort J Vet Res. 2009;76:285–9.
  68. Biryomumaisho S, Rwakishaya E-K, Melville SE, Cailleau A, Lubega GW. Livestock trypanosomosis in Uganda: Parasite heterogeneity and anaemia status of naturally infected cattle, goats and pigs. Parasitol Res. 2013;112:1443–50.
  69. Bishaw Y, Temesgen W, Yideg N, Alemu S. Prevalence of bovine trypanosomosis in Wemberma district of West Gojjam zone, North West Ethiopia. Ethiop Vet J. 2012;16:41–8.
  70. Bitew M, Amedie Y, Abebe A, Tolosa T. Prevalence of bovine trypanosomosis in selected areas of jabi tehenan district, West Gojam of Amhara regional state, Northwestern Ethiopia. African J Agric Res. 2011;6:140–4.
  71. Bittar JFF, Bassi PB, Moura DM, Garcia GC, Martins-Filho OA, Vasconcelos AB, et al. Evaluation of parameters related to libido and semen quality in Zebu bulls naturally infected with Trypanosoma vivax. BMC Vet Res. 2015;11:261.
  72. Cadioli FA, Barnabé P de A, Machado RZ, Teixeira MCA, André MR, Sampaio PH, et al. First report of Trypanosoma vivax outbreak in dairy cattle in São Paulo state, Brazil. Rev Bras Parasitol Veterinária. 2012;21:118–24.
  73. Camejo MI, Aso PM, Gonzatti MI, Pérez-Rojas Y. Relationship between asymptomatic infections with Anaplasma marginale, Babesia spp. and Trypanosoma vivax in bulls and testosterone levels. Rev Cient la Fac Ciencias Vet la Univ del Zulia. 2016;26:13–9.
  74. Chanie M, Arega C, Bogale B. Hematopathology and hematological parametric alterations in indigenous cattle due to trypanosomosis. Glob Vet. 2012;9:546–51.
  75. Cherenet T, Sani RA, Panandam JM, Nadzr S, Speybroeck N, van den Bossche P. Seasonal prevalence of bovine trypanosomosis in a tsetse-infested zone and a tsetse-free zone of the Amhara Region, north-west Ethiopia. Onderstepoort J Vet Res. 2004;71:307–12.
  76. Cherenet T, Sani RA, Speybroeck N, Panandam JM, Nadzr S, Van den Bossche P. A comparative longitudinal study of bovine trypanosomiasis in tsetse-free and tsetse-infested zones of the Amhara Region, northwest Ethiopia. Vet Parasitol. 2006;140:251–8.
  77. Clausens P-H, Wiemann A, Patzelt R, Kakaire D, Poetzsch C, Peregrine A, et al. Use of a PCR assay for the specific and sensitive detection of Trypanosoma spp. in naturally infected dairy cattle in peri-urban Kampala, Uganda. Ann. N. Y. Acad. Sci. 1998. p. 21–31.
  78. Connor RJ, Halliwell RW. Bovine trypanosomiasis in Southern Tanzania: Parasitological and serological survey of prevalence. Trop Anim Health Prod. 1987;19:165–72.
  79. Cordon-Obras C, Berzosa P, Ndong-Mabale N, Bobuakasi L, Buatiche JN, Ndongo-Asumu P, et al. Trypanosoma brucei gambiense in domestic livestock of kogo and mbini foci (Equatorial Guinea). Trop Med Int Heal. National Centre of Tropical Medicine, Institute of Health Carlos III, Madrid, Spain; 2009;14:535–41.
  80. Cossic BGA, Adjahoutonon B, Gloaguen P, Dibanganga GL, Maganga G, Leroy P, et al. Trypanosomiasis challenge estimation using the diminazene aceturate (Berenil) index in Zebu in Gabon. Trop Anim Health Prod. 2017;49:619–24.
  81. Costa VM de M, Ribeiro MFB, Duarte ALL, Mangueira JM, Pessoa AFA, Azevedo SS, et al. Seroprevalence and risk factors for cattle anaplasmosis, babesiosis, and trypanosomiasis in a Brazilian semiarid region. Rev Bras Parasitol Vet. 2013;22:207–13.
  82. Cox AP, Tosas O, Tilley A, Picozzi K, Coleman P, Hide G, et al. Constraints to estimating the prevalence of trypanosome infections in East African zebu cattle. Parasites and Vectors. 2010;3.
  83. Cuglovici DA, Bartholomeu DC, Reis-Cunha JL, Carvalho AU, Ribeiro MFB. Epidemiologic aspects of an outbreak of Trypanosoma vivax in a dairy cattle herd in Minas Gerais state, Brazil. Vet Parasitol. 2010;169:320–6.
  84. Silva AS Da, Perez HAG, Costa MM, Da Silva AS, Garcia Perez HA, Costa MM, et al. Horses naturally infected by Trypanosoma vivax in southern Brazil. Parasitol Res. 2011;108:23–30.
  85. da Silva AS, Costa MM, Polenz MF, Polenz CH, Teixeira MMG, Lopes STA, et al. First report of Trypanosoma vixax in bovines in the State of Rio Grande do Sul, Brazil. Cienc Rural. 2009;39:2550–4.
  86. Dagnachew S, Girma H, Abebe G. A cross-sectional study on bovine trypanosomosis in Jawi district of Amhara Region, Northwest Ethiopia. Ethiop Vet J. 2011;15.
  87. Dagnachew S, Tsegaye B, Awukew A, Tilahun M, Ashenafi H, Rowan T, et al. Prevalence of bovine trypanosomosis and assessment of trypanocidal drug resistance in tsetse infested and non-tsetse infested areas of Northwest Ethiopia. Parasite Epidemiol Control. 2017;2:40–9.
  88. Danbirni S, Okaiyeto SO, Kudi AC, Pewan SB. Bovine trypanosomosis and tuberculosis in a nomadic herd in sabon gari local government area of Kaduna state, Nigeria. J Anim Vet Adv. 2010;9:1285–8.
  89. Daniel AD, Joshua RA, Kalejaiye JO, Dada AJ. Prevalence of trypanosomiasis in sheep and goats in a region of northern Nigeria. Rev Elev Med Vet Pays Trop. 1994;47:295–7.
  90. Dayo G-KK, Bengaly Z, Messad S, Bucheton B, Sidibe I, Cene B, et al. Prevalence and incidence of bovine trypanosomosis in an agro-pastoral area of southwestern Burkina Faso. Res Vet Sci. 2010;88:470–7.
  91. De Araujo Melo S, Barros ACE, Costa FB, De Carvalho Neta AV, De Candanedo Guerra RDMN, Abreu-Silva AL. Bovine trypanosomiasis an emerging disease in Maranhão State-Brazil. Vector-Borne Zoonotic Dis. 2011;11:853–6.
  92. Degneh E, Shibeshi W, Terefe G, Asres K, Ashenafi H. Bovine trypanosomosis: changes in parasitemia and packed cell volume in dry and wet seasons at Gidami District, Oromia Regional State, western Ethiopia. Acta Vet Scand. 2017;59:59.
  93. Delafosse A, Thebaud E, Desquesnes M, Michaux Y. Epidemiology of Trypanosoma vivax infection in cattle in the tse-tse free area of Lake Chad. Prev Vet Med. 2006;74:108–19.
  94. de Melo Barbieri J, Blanco YAC, Bruhn FRP, Guimaraes AM. Seroprevalence of Trypanosoma vivax, anaplasma marginale, and babesia bovis in dairy cattle. Cienc Anim Bras. 2016;17:564–73.
  95. Desquesnes M, Gardiner PR. Epidemiology of bovine trypanosomiasis (Trypanosoma vivax) in French Guiana. Rev Elev Med Vet Pays Trop. 1993;46:463–70.
  96. Dhollander S, Jallow A, Mbodge K, Kora S, Sanneh M, Gaye M, et al. Equine trypanosomosis in the Central River Division of The Gambia: A study of veterinary gate-clinic consultation records. Prev Vet Med. 2006;75:152–62.
  97. Dillmann JSS, Townsend AJ. A trypanosomiasis survey of wild animals in the Luangwa Valley, Zambia. Acta Trop. 1979;
  98. Dinka H, Abebe G. Small ruminants trypanosomosis in the southwest of Ethiopia. Small Rumin Res. 2005;57:239–43.
  99. Doko A, Guedegbe B, Baelmans R, Demey F, N’Diaye A, Pandey VS, et al. Trypanosomiasis in different breeds of cattle from Benin. Vet Parasitol. 1991;40:1–7.
  100. Drager N, Mehlitz D. Investigations on the prevelance of trypanosome carriers and the antibody response in wildlife in Northern Botswana. Tropenmed Parasitol. 1978;29:223–33.
  101. Duguma R, Tasew S, Olani A, Damena D, Alemu D, Mulatu T, et al. Spatial distribution of Glossina sp. and Trypanosoma sp. in south-western Ethiopia. Parasites and Vectors. 2015;8.
  102. Dwinger RH, Agyemang K, Kaufmann J, Grieve AS, Bah ML. Effects of trypanosome and helminth infections on health and production parameters of village N’Dama cattle in the Cambia. Vet Parasitol. 1994;54:353–65.
  103. Efrem DB, Yacob HT, Hagos AT, Basu AK. Bovine trypanosomosis in gimbi district of Western Oromia, Ethiopia. Anim Biol. 2010;60:123–31.
  104. Ehizibolo DO, Kamani J, Ehizibolo PO, Egwu KO, Dogo GI, Salami-Shinaba JO. Prevalence and significance of parasites of horses in some states of northern Nigeria. J Equine Sci. 2012;23:1–4.
  105. Enwezor FNC, Samdi SM, Ijabor O, Abenga JN. The prevalence of bovine trypanosomes in parts of Benue state, north-central Nigeria. J Vector Borne Dis. 2012;49:188–90.
  106. Enwezor FNC, Bello B, Kalgo A, Zaria LT. Surveillance and management of trypanosomiasis in cattle herds in Kauru area, Kaduna State, Nigeria. Livest Rearing, Farming Pract Dis. 2011. p. 145–62.
  107. Eyob A, Mekuria S, Regassa A, Abebe R. A cross-sectional study of equine trypanosomosis and its vectors in Wolayta zone, Southern Ethiopia. J Vet Med Anim Heal. 2011;3:21–6.
  108. Ezeani MC, Okoro H, Anosa VO, Onyenekwe CC, Meludu SC, Dioka CE, et al. Immunodiagnosis of bovine trypanosomiasis in Anambra and Imo states, Nigeria, using enzyme-linked immunosorbent assay: Zoonotic implications to human health. J Vector Borne Dis. 2008;45:292–300.
  109. Fajinmi AO, Faleke OO, Magaji AA, Daneji AI, Gweba M, Fajinmi, AO., Faleke, OO., Magaji, AA., Daneji, AI., Gweba M. Presence of Trypanosome species and determination of anaemia in trade cattle at Sokoto Abattoir, Nigeria. Res J Parasitol. 2011;6:31–42.
  110. Fakae BB, Chiejina SN. The prevalence of concurrent trypanosome and gastrointestinal nematode infections in West African Dwarf sheep and goats in Nsukka area of eastern Nigeria. Vet Parasitol. 1993;49:313–8.
  111. Fall A, Diack A, Diaite A, Seye M, D’Ieteren GDM, Diaité A, et al. Tsetse challenge, trypanosome and helminth infection in relation to productivity of village Ndama cattle in Senegal. Vet Parasitol. 1999;81:235–47.
  112. Fávero JF, Da Silva AS, Biazus AH, Volpato A. Trypanosoma vivax infection in goat in west of Santa Catarina state, Brazil. Comp Clin Path. 2016;25:497–9.
  113. Fentahun T, Tekeba M, Mitiku T, Chanie M. Prevalence of bovine trypanosomosis and distribution of vectors in Hawa Gelan district, Oromia region, Ethiopia. Glob Vet. 2012;9:297–302.
  114. Regassa F, Goddeeris BM, Delespaux V, Moti Y, Tadesse A, Bekana M, et al. Widespread occurrence of Trypanosoma vivax in bovines of tsetse- as well as non-tsetse-infested regions of Ethiopia: a reason for concern? Vet Parasitol. 2012;190:355–61.
  115. Regassa F, Andualem Y, Getachew T, Menten J, Hasker E, Merga B, et al. Trypanosome infection in dromedary camels in Eastern Ethiopia: Prevalence, relative performance of diagnostic tools and host related risk factors. Vet Parasitol. 2015;211:175–81.
  116. Galiza GJN, Garcia HA, Assis ACO, Oliveira DM, Pimentel LA, Dantas AFM, et al. High mortality and lesions of the central nervous system in trypanosomosis by Trypanosoma vivax in Brazilian hair sheep. Vet Parasitol. 2011;182:359–63.
  117. Ganyo EY, Boampong JN, Masiga DK, Villinger J, Turkson PK. Haematology of N’Dama and West African Short Horn cattle herds under natural Trypanosoma vivax challenge in Ghana. F1000Research. 2018;7:314.
  118. Garcia H, Garcia M-E, Perez H, Mendoza-Leon A. The detection and PCR-based characterization of the parasites causing trypanosomiasis in water-buffalo herds in Venezuela. Ann Trop Med Parasitol. 2005;99:359–70.
  119. García H, García M-EE, Pérez G, Bethencourt A, Zerpa É, Pérez H, et al. Trypanosomiasis in Venezuelan water buffaloes: Association of packed-cell volumes with seroprevalence and current trypanosome infection. Ann Trop Med Parasitol. 2006;100:297–305.
  120. García H, Rangel-Rivas A, Contreras I, García M-E, García F, Perrone T. Molecular characterization of Trypanosoma vivax in naturally-infected sheep from two farms at San Fernando and Biruaca Counties, Apure State, Venezuela. Rev Cient la Fac Ciencias Vet la Univ del Zulia. 2009;19:230–7.
  121. Garcia HA, Ramirez OJ, Rodrigues CMF, Sanchez RG, Bethencourt AM, Del M Perez G, et al. Trypanosoma vivax in water buffalo of the Venezuelan Llanos: An unusual outbreak of wasting disease in an endemic area of typically asymptomatic infections. Vet Parasitol. 2016;230:49–55.
  122. Girmay G, Arega B, Tesfaye D, Berkvens D, Muleta G, Asefa G. Community-based tsetse fly control significantly reduces fly density and trypanosomosis prevalence in Metekel Zone, Northwest, Ethiopia. Trop Anim Health Prod. 2016;48:633–42.
  123. Gonzales JL, Chacon E, Miranda M, Loza A, Siles LM. Bovine trypanosomosis in the Bolivian Pantanal. Vet Parasitol. 2007;146:9–16.
  124. González JR, Meléndez RD. Seroprevalence of bovine trypanosomosis and anaplasmosis by Elisa at Juan Jose Mora County, Carabobo State, Venezuela. Rev Cient la Fac Ciencias Vet la Univ del Zulia. 2007;17:449–55.
  125. Guedes Junior DS, Araújo FR, Silva FJMM, Rangel CP, Barbosa Neto JD, Fonseca AH. Frequency of antibodies to Babesia bigemina, B. bovis, Anaplasma marginale, Trypanosoma vivax and Borrelia burgdorferi in cattle from the Northeastern region of the State of Pará, Brazil. Rev Bras Parasitol Vet. 2008;17:105–9.
  126. Guerra RDMSNDC, Feitosa Jr. AB, Santos HP, Abreu-Silva AL, Dos Santos ACG, Feitosa AB, et al. Biometry of Trypanosoma vivax found in a calf in the state of Maranhão, Brazil. Cienc Rural. 2008;38:833–5.
  127. Guerra NR, Monteiro MFM, Sandes HMM, Da Cruz NLN, Ramos CAN, De Assis Santana VL, et al. Detection of IgG antibodies against Trypanosoma vivax in cattle by indirect immunofluorescence test. Pesqui Vet Bras. 2013;33:1423–6.
  128. Gueye A, Mbengue M, Diouf A. Ticks and hemoparasitoses of livestock in Senegal. III. The Northern Sudan area. Rev Elev Med Vet Pays Trop. 1989;42:411–20.
  129. Gueye A, Mbengue M, Diouf A, Sonko ML. Ticks and hemoparasitoses in livestock in Senegal. V. The northern Guinea area. Rev Elev Med Vet Pays Trop. 1993;46:551–61.
  130. Haji IJ, Malele I, Namangala B. Occurrence of haemoparasites in cattle in Monduli district, northern Tanzania. Onderstepoort J Vet Res. 2014;81:1–4.
  131. Haji IJ, Sugimoto C, Kajino K, Malele I, Simukoko H, Chitambo H, et al. Determination of the prevalence of trypanosome species in cattle from Monduli district, northern Tanzania, by loop mediated isothermal amplification. Trop Anim Health Prod. 2015;47:1139–43.
  132. Hall MJR, Kheir SM, Rahman AHA, Noga S. Tsetse and trypanosomiasis survey of southern darfur province, Sudan - I. Bovine trypanosomiasis. Trop Anim Health Prod. 1983;15:191–206.
  133. Hamill LC, Kaare MT, Welburn SC, Picozzi K. Domestic pigs as potential reservoirs of human and animal trypanosomiasis in Northern Tanzania. Parasites and Vectors. 2013;6.
  134. Idehen CO, Ishola OO, Adeyemi IG, Abongaby G, Olaleye OO, Aluma AL, et al. Prevalence of African trypanosomosis in cattle and sheep in Bassa Local Government Area of Plateau State, Nigeria. Sokoto J Vet Sci. 2018;16:11–7.
  135. Jaimes-Dueñez J, Triana-Chávez O, Mejía-Jaramillo AM. Spatial-temporal and phylogeographic characterization of Trypanosoma spp. in cattle (Bos taurus) and buffaloes (Bubalus bubalis) reveals transmission dynamics of these parasites in Colombia. Vet Parasitol. 2018;249:30–42.
  136. Jaimes-Dueñez J, Zapata-Zapata C, Triana-Chávez O, Mejía-Jaramillo AM. Evaluation of an alternative indirect-ELISA test using in vitro-propagated Trypanosoma brucei brucei whole cell lysate as antigen for the detection of anti-Trypanosoma evansi IgG in Colombian livestock. Prev Vet Med. 2019;169:104712.
  137. Joshua RA. Occurrence of human serum-resistant Trypanosoma congolense in goats and sheep in Nigeria. Vet Parasitol. 1989;31:107–13.
  138. Kalu AU, Oboegbulem SI, Uzoukwu M. Trypanosomosis in small ruminants maintained by low riverine tsetse population in central Nigeria. Small Rumin Res. 2001;40:109–15.
  139. Kalu AU. Prevalence of trypanosomiasis among Trypanotolerant cattle at the lower Benue River area of Nigeria. Prev Vet Med. 1995;24:97–103.
  140. Kalu AU. Current status of tsetse fly and animal trypanosomosis on the Jos Plateau, Nigeria. Prev Vet Med. 1996;27:107–13.
  141. Karimuribo ED, Morrison LJ, Black A, Turner CMR, Kambarage DM, Ballingall KT. Analysis of host genetic factors influencing African trypanosome species infection in a cohort of Tanzanian Bos indicus cattle. Vet Parasitol. 2011;179:35–42.
  142. Kassaye BK. Prevalence of bovine Trypanosomosis and apparent density of tsetse flies in Sayonole district Western Oromia, Ethiopia. J Vet Sci Technol. 2015;6:254.
  143. Kayang BB, Bosompem KM, Assoku RKG, Awumbila B. Detection of Trypanosoma brucei, T. congolense and T. vivax infections in cattle, sheep and goats using latex agglutination. Int J Parasitol. 1997;27:83–7.
  144. Kebede N, Fetene T, Animut A. Prevalence of Trypanosomosis of small ruminants in Guangua district of Awi Zone, northwestern Ethiopia. J Infect Dev Ctries. 2009;3:245–6.
  145. Kidanemariam A, Hadgu K, Sahle M. Parasitological prevalence of bovine trypanosomosis in Kindo Koisha district, Wollaita zone, south Ethiopia. Onderstepoort J Vet Res. 2002;69:107–13.
  146. Kihurani DO, Nantulya VM, Mbiuki SM, Mogoa E, Nguhiu-Mwangi J, Mbithi PM. Trypanosoma brucei, T. congolense and T. vivax infections in horses on a farm in Kenya. Trop Anim Health Prod. 1994;26:95–101.
  147. Kimaro EG, Toribio J-AALML, Gwakisa P, Mor SM. Occurrence of trypanosome infections in cattle in relation to season, livestock movement and management practices of Maasai pastoralists in Northern Tanzania. Vet Parasitol Reg Stud Reports. 2018;12:91–8.
  148. Kouadio IK, Sokouri D, Koffi M, Konaté I, Ahouty B, Koffi A, et al. Molecular characterization and prevalence of Trypanosoma species in cattle from a northern livestock area in Côte d’Ivoire. Open J Vet Med. 2014;4:314–21.
  149. Laohasinnarong D, Thekisoe OMM, Malele I, Namangala B, Ishii A, Goto Y, et al. Prevalence of Trypanosoma sp. in cattle from Tanzania estimated by conventional PCR and loop-mediated isothermal amplification (LAMP). Parasitol Res. 2011;109:1735–9.
  150. Laohasinnarong D, Goto Y, Asada M, Nakao R, Hayashida K, Kajino K, et al. Studies of trypanosomiasis in the Luangwa valley, north-eastern Zambia. Parasites and Vectors. 2015;8:1–8.
  151. Lefrançois T, Solano P, De La Rocque S, Bengaly Z, Reifenberg JM, Kabore I, et al. New epidemiological features on animal trypanosomiasis by molecular analysis in the pastoral zone of Sideradougou, Burkina Faso. Mol Ecol. 1998;7:897–904.
  152. Lelisa K, Shimeles S, Bekele J, Sheferaw D. Bovine trypanosomosis and its fly vectors in three selected settlement areas of Hawa-Gelan district, western Ethiopia. Onderstepoort J Vet Res. 2014;81:1–5.
  153. Lema AA, Maigoro MA, Said M, Marwana AM, Nuraddeen W. Prevalence of bovine trypanasomosis in katsina central abattoir, Katsina state. Niger J Parasitol. 2018;39:226–9.
  154. Lopes STP, Prado B da S, Martins GHC, Beserra HEA, Sousa Filho MAC de, Evangelista LS de M, et al. Trypanosoma vivax in dairy cattle. Acta Sci Vet. 2018;46:287.
  155. Luckins AG, Mehlitz D. Evaluation of an indirect fluorescent antibody test, enzyme-linked immunosorbent assay and quantification of immunoglobulins in the diagnosis of bovine trypanosomiasis. Trop Anim Health Prod. 1978;10:149–59.
  156. Madruga CR, Araujo FR, Cavalcante-Goes G, Martins C, Pfeifer IB, Ribeiro LR, et al. The development of an enzyme-linked immunosorbent assay for Trypanosoma vivax antibodies and its use in epidemiological surveys. Mem Inst Oswaldo Cruz. 2006;101:801–7.
  157. Maganga GD, Mavoungou J-FF, N’dilimabaka N, Moussadji Kinga IC, Mve-Ondo B, Mombo IM, et al. Molecular identification of trypanosome species in trypanotolerant cattle from the south of Gabon. Parasite. 2017;24:4.
  158. Magona JW, Kakaire DW, Mayende JSP. Prevalence and distribution of animal trypanosomosis on Buvuma Islands in Lake Victoria, Uganda. Trop Anim Health Prod. 1999;31:83–7.
  159. Magona JW, Greiner M, Mehlitz D. Impact of tsetse control on the age-specific prevalence of trypanosomosis in village cattle in southeast Uganda. Trop Anim Health Prod. 2000;32:87–98.
  160. Magona JW, Mayende JSP, Walubengo J. Comparative evaluation of the antibody-detection ELISA technique using microplates precoated with denatured crude antigens from Trypanosoma congolense or Trypanosoma vivax. Trop Anim Health Prod. 2002;34:295–308.
  161. Magona JW, Mayende JSP, Olaho-Mukani W, Coleman PG, Jonsson NN, Welburn SC, et al. A comparative study on the clinical, parasitological and molecular diagnosis of bovine trypanosomosis in Uganda. Onderstepoort J Vet Res. 2003;70:213–8.
  162. Magona JW, Walubengo J, Odimim JJ. Differences in susceptibility to trypanosome infection between Nkedi Zebu and Ankole cattle, under field conditions in Uganda. Ann Trop Med Parasitol. 2004;98:785–92.
  163. Magona JW, Walubengo J, Odiit M, Okedi LA, Abila P, Katabazi BK, et al. Implications of the re-invasion of Southeast Uganda by Glossina pallidipes on the epidemiology of bovine trypanosomosis. Vet Parasitol. 2005;128:1–9.
  164. Magona JW, Walubengo J, Odimin JT. Acute haemorrhagic syndrome of bovine trypanosomosis in Uganda. Acta Trop. 2008;107:186–91.
  165. Magona JW, Walubengo J, Odimim JT. Differences in prevalence of trypanosomosis in nkedi zebu, ankole and crossbred cattle under tethering and open grazing management systems in uganda. Livest Res Rural Dev. 2011;23:141.
  166. Majekodunmi AO, Fajinmi A, Dongkum C, Picozzi K, Thrusfield M V, Welburn SC. A longitudinal survey of African animal trypanosomiasis in domestic cattle on the Jos Plateau, Nigeria: prevalence, distribution and risk factors. Parasit Vectors. 2013;6:239.
  167. Makumyaviri AM, Ngarambe M. Parasitological and serological diagnosis of trypanosomiasis in cattle in the Northern-Kivu province, Congo. Rev Med Vet (Toulouse). 1997;148:809–12.
  168. Makumyaviri A, Mehlitz D, Kageruka P, Kazyumba GL, Molisho D. Animal reservoir hosts of Trypanosoma brucei gambiense in Zaire: Trypanosome infections in two foci in Bas-Zaire. Trop Med Parasitol. 1989;40:258–62.
  169. Mamabolo M V, Ntantiso L, Latif A, Majiwa PAO. Natural infection of cattle and tsetse flies in South Africa with two genotypic groups of Trypanosoma congolense. Parasitology. 2009;136:425–31.
  170. Mamoudou A, Njanloga A, Hayatou A, Suh PF, Achukwi MD. Animal trypanosomosis in clinically healthy cattle of north Cameroon: Epidemiological implications. Parasites and Vectors. 2016;9.
  171. Manuel Tafur T, Amanda Chávez V, Eva Casas A, Enrique Serrano M. Prevalence of Trypanosoma vivax in cattle in high forest of the province of Chachapoyas, Amazonas. Rev Investig Vet del Peru. 2002;13:94–7.
  172. Masiga RC, Nyang’ao JMN. Identification of trypanosome species from camel using polymerase chain reaction and procyclic transformation test. J Camel Pract Res. 2001;8:17–22.
  173. Mattioli RC, Faye JA, Jaitner J. Estimation of trypanosomal status by the buffy coat technique and an antibody ELISA for assessment of the impact of trypanosomosis on health and productivity of N’Dama cattle in The Gambia. Vet Parasitol. 2001;95:25–35.
  174. Mbahin N, Affognon H, Andoke J, Tiberius M, Mbuvi D, Otieno J, et al. Parasitological prevalence of bovine trypanosomosis in Kubo division of Kwale County of coastal: Baseline survey. Am J Anim Vet Sci. 2013;8:28–36.
  175. Mbewe NJ, Namangala B, Sitali L, Vorster I, Michelo C. Prevalence of pathogenic trypanosomes in anaemic cattle from trypanosomosis challenged areas of Itezhi-tezhi district in central Zambia. Parasit Vectors. 2015;8:638.
  176. Mehlitz D. Trypanosome infections in domestic animals in Liberia. Tropenmed Parasitol. 1979;30:212–9.
  177. Mekata H, Konnai S, Witola WH, Inoue N, Onuma M, Ohashi K. Molecular detection of trypanosomes in cattle in South America and genetic diversity of Trypanosoma evansi based on expression-site-associated gene 6. Infect Genet Evol. 2009;9:1301–5.
  178. Mekibib B, Manegerew M, Tadesse A, Abuna F, Megersa B, Regassa A, et al. Prevalence of haemoparasites and associated risk factors in working donkeys in Adigudem and Kwiha districts of Tigray region, northern Ethiopia. J Anim Vet Adv. 2010;9:2249–55.
  179. Mekonnen B, Regassa V, Kahsay AG. Epidemiology of trypanosomosis in goats in Abelti, Bede and Ghibe valley, south West Ethiopia. Int J Trop Med. 2014;9:10–4.
  180. Mekuria S, Gadissa F. Survey on bovine trypanosomosis and its vector in Metekel and Awi zones of Northwest Ethiopia. Acta Trop. 2011;117:146–51.
  181. Mekuria S, Eyob A, Regassa A, Tadesse A, Mekibib B, Abebe R. A cross-sectional study of equine trypanosomosis and its vectors in Wolayta zone, Southern Ethiopia. J Anim Vet Adv. 2010;9:2061–6.
  182. Melese M, Alemu S, Kemal J, Muktar Y, Abraha A. Vector identification and bovine trypanosomosis in edja district, South Ethiopia. Livest Res Rural Dev. 2017;29.
  183. Mihok S, Olubayo RO, Moloo SK. Trypanosomiasis in the black rhinoceros (Diceros bicornis Linnaeus, 1758). Rev Sci Tech. 1992;11:1169–73.
  184. Mihret A, Mamo G. Bovine trypanosomosis in three districts of East Gojjam Zone bordering the Blue Nile River in Ethiopia. J Infect Dev Ctries. 2007;1:321–5.
  185. Moll G, Lohding A, Young AS. Epidemiology of theilerioses in the Trans-Mara division, Kenya: Husbandry and disease background and preliminary investigations on theilerioses in calves. Prev Vet Med. 1984;2:801–31.
  186. Mossaad E, Salim B, Suganuma K, Musinguzi P, Hassan MA, Elamin EA, et al. Trypanosoma vivax is the second leading cause of camel trypanosomosis in Sudan after Trypanosoma evansi. Parasites and Vectors. 2017;10.
  187. Moti Y, Fikru R, Büscher P, Van Den Abbeele J, Duchateau L, Delespaux V. Detection of african animal trypanosomes: The haematocrit centrifugation technique compared to PCR with samples stored on filter paper or in DNA protecting buffer. Vet Parasitol. 2014;203:253–8.
  188. Mugittu KN, Silayo RS, Majiwa PAO, Kimbita EK, Mutayoba BM, Maselle R. Application of PCR and DNA probes in the characterisation of trypanosomes in the blood of cattle in farms in Morogoro, Tanzania. Vet Parasitol. 2001;94:177–89.
  189. Muhanguzi D, Mugenyi A, Bigirwa G, Kamusiime M, Kitibwa A, Akurut GG, et al. African animal trypanosomiasis as a constraint to livestock health and production in Karamoja region: A detailed qualitative and quantitative assessment. BMC Vet Res. 2017;13.
  190. Muhanguzi D, Picozzi K, Hattendorf J, Thrusfield M, Kabasa JD, Waiswa C, et al. The burden and spatial distribution of bovine African trypanosomes in small holder croplivestock production systems in Tororo District, south-eastern Uganda. Parasites and Vectors. 2014;7:603.
  191. Mulaw S, Addis M, Fromsa A. Study on the prevalence of major trypanosomes affecting bovine in tsetse infested Asosa District of Benishangul Gumuz Regional State, Western Ethiopia. Glob Vet. 2011;7:330–6.
  192. Mungube EO, Vitouley HS, Allegye-Cudjoe E, Diall O, Boucoum Z, Diarra B, et al. Detection of multiple drug-resistant Trypanosoma congolense populations in village cattle of south-east Mali. Parasites and Vectors. 2012;5.
  193. Musinguzi SP, Suganuma K, Asada M, Laohasinnarong D, Sivakumar T, Yokoyama N, et al. A PCR-based survey of animal African trypanosomosis and selected piroplasm parasites of cattle and goats in Zambia. J Vet Med Sci. 2016;78:1819–24.
  194. Mwambu PM, Mayende JSP. Salivarian trypanosome infections in cattle in Ikoma, South Mara district, Tanzania. Parasitology. 1973;66:381–5.
  195. Mwambu PM. Prevalence of Trypanosoma vivax infection in cattle in Teso District, Eastern Uganda. Bull Epizoot Dis Afr. 1969;17:395–402.
  196. Mwangi EK, Stevenson P, Gettinby G, Reid SW, Murray M. Susceptibility to trypanosomosis of three Bos indicus cattle breeds in areas of differing tsetse fly challenge. Vet Parasitol. 1998;79:1–17.
  197. N’Djetchi MK, Ilboudo H, Koffi M, Kaboré J, Kaboré JW, Kaba D, et al. The study of trypanosome species circulating in domestic animals in two human African trypanosomiasis foci of Côte d’Ivoire identifies pigs and cattle as potential reservoirs of Trypanosoma brucei gambiense. PLoS Negl Trop Dis. 2017;11:1–16.
  198. Nakayima J, Nakao R, Alhassan A, Mahama C, Afakye K, Sugimoto C. Molecular epidemiological studies on animal trypanosomiases in Ghana. Parasites and Vectors. 2012;5.
  199. Nakayima J, Nakao R, Alhassan A, Hayashida K, Namangala B, Mahama C, et al. Genetic diversity among Trypanosoma (Duttonella) vivax strains from Zambia and Ghana, based on cathepsin L-like gene. Parasite. 2013;20:24.
  200. Nantulya VM, Lindqvist KJ, Stevenson P, Mwangi EK. Application of a monoclonal antibody-based antigen detection enzyme-linked immunosorbent assay (antigen ELISA) for field diagnosis of bovine trypanosomiasis at Nguruman, Kenya. Ann Trop Med Parasitol. 1992;86:225–30.
  201. Ng’ayo MO, Njiru ZK, Kenya EU, Muluvi GM, Osir EO, Masiga DK. Detection of trypanosomes in small ruminants and pigs in western Kenya: Important reservoirs in the epidemiology of sleeping sickness? Kinetoplastid Biol Dis. 2005;4.
  202. Ngomtcho SCH, Weber JS, Ngo Bum E, Gbem TT, Kelm S, Achukwi MD. Molecular screening of tsetse flies and cattle reveal different Trypanosoma species including T. grayi and T. theileri in northern Cameroon. Parasites and Vectors. 2017;10:1–16.
  203. Nonga HE, Kambarage DM. Prevalence of Bovine trypanosomosis in Morogoro, Tanzania. Pakistan J Nutr. 2009;8:208–13.
  204. Nyimba PH, Komba EVG, Sugimoto C, Namangala B. Prevalence and species distribution of caprine trypanosomosis in Sinazongwe and Kalomo districts of Zambia. Vet Parasitol. 2015;210:125–30.
  205. Ocaido M, Otim CP, Okuna NM, Erume J, Ssekitto C, Wafula RZOO, et al. Socio-economic and livestock disease survey of agropastoral communities in Serere County, Soroti District, Uganda. Livest Res Rural Dev. 2005;17.
  206. Ode S, Adamu M, Taioe M, Thekisoe O, Adamu S, Saror DI. Molecular occurrence of trypanosomes, erythrocyte and serum sialic acid concentrations of Muturu and Bunaji cattle in Benue State, Nigeria. Vet Parasitol. 2017;242:10–3.
  207. Odeniran PO, Macleod ET, Ademola IO, Welburn SC. Molecular identification of bovine trypanosomes in relation to cattle sources in southwest Nigeria. Parasitol Int. 2019;68:1–8.
  208. Odongo S, Delespaux V, Ngotho M, Bekkele SM, Magez S. Comparative evaluation of the nested ITS PCR against the 18S PCR-RFLP in a survey of bovine trypanosomiasis in Kwale County, Kenya. J Vet Diagn Invest. 2016;28:589–94.
  209. Okech G, Dolan RB, Stevenson P, Alushula H, Watson ED, Luckins AG, et al. The effect of trypanosomosis on pregnancy in trypanotolerant Orma Boran cattle. Theriogenology. 1996;46:441–7.
  210. Oliveira JB, Hernández-Gamboa J, Jiménez-Alfaro C, Zeledón R, Blandón M, Urbina A, et al. First report of Trypanosoma vivax infection in dairy cattle from Costa Rica. Vet Parasitol. 2009;163:136–9.
  211. Omoogun GA, Akinboade OA. Tsetse and bovine trypanosomosis incidence at egbe in the derived savanna zone of nigeria. Insect Sci its Appl. 2000;20:215–9.
  212. Ono MSB, Souto PC, Cruz JA, Guerra NR, Guimarães JA, Dantas AC, et al. Trypanosoma vivax outbreak in cattle in the ‘Zona da Mata’’ of the state of Pernambuco.’ Med Vet. 2017;11:96–101.
  213. Osaer S, Goossens B, Kora S, Gaye M, Darboe L. Health and productivity of traditionally managed Djallonke sheep and West African dwarf goats under high and moderate trypanosomosis risk. Vet Parasitol. 1999;82:101–19.
  214. Osiyemi TIOO, Agbonlahor DEAA. Incidence of protozoan blood parasites in livestock in northern Nigeria. Trop Anim Health Prod. 1980;12:115.
  215. Otte MJ, Abuabara JY, Nieto MI, Gutierrez JR. Incidence of Trypanosoma vivax infection on three cattle farms on the north coast of Colombia. Acta Vet Scand Suppl. 1988;84:104–6.
  216. Pagabeleguem S, Sangaré M, Bengaly Z, Akoudjin M, Belem AMGG, Bouyer J. Climate, Cattle Rearing Systems and African Animal Trypanosomosis Risk in Burkina Faso. PLoS One. 2012;7.
  217. Paoletta MS, López Arias L, de la Fournière S, Guillemi EC, Luciani C, Sarmiento NF, et al. Epidemiology of Babesia, Anaplasma and Trypanosoma species using a new expanded reverse line blot hybridization assay. Ticks Tick Borne Dis. 2018;9:155–63.
  218. Pereira De Almeida PJLL, Ndao M, Goossens B, Osaer S. PCR primer evaluation for the detection of trypanosome DNA in naturally infected goats. Vet Parasitol. 1998;80:111–6.
  219. Pereira HD, Simões SVDD, Souza FAL, Silveira JAG, Ribeiro MFB, Cadioli FA, et al. Clinical and epidemiological aspects and diagnosis of Trypanosoma vivax infection in a cattle herd, state of Maranhão, Brazil. Pesqui Vet Bras. 2018;38:896–901.
  220. de Souza Pimentel D, do Nascimento Ramos CA, Ramos RADNRA, de Araújo FR, Borba ML, da Gloria Faustino MA, et al. First report and molecular characterization of Trypanosoma vivax in cattle from state of Pernambuco, Brazil. Vet Parasitol. 2012;185:286–9.
  221. Ávila Pulgarín LS, Acevedo Restrepo A, Jurado Guevara JA, Polanco Echeverry D, Velásquez Vélez R, Zapata Salas R, et al. Hemoparasite infection in goats and sheep at five municipalities in north and northeastern Antioquia (Colombia). Rev CES Med Vet y Zootec. 2013;8:11–21.
  222. Patricia Quispe A, Amanda Chávez V, Eva Casas A, Antonio Trigueros V, Francisco Suárez A. Prevalence of Trypanosoma vivax in cattle from the Coronel Portillo province, Ucayali. Rev Investig Vet del Peru. 2003;14:161–5.
  223. Rahman AHA. Observations on the trypanosomosis problem outside the tsetse belts of Sudan. Rev Sci Tech. 2005;24:965–72.
  224. Ramírez-Iglesias JR, Eleizalde MC, Reyna-Bello A, Mendoza M. Molecular diagnosis of cattle trypanosomes in Venezuela: evidences of Trypanosoma evansi and Trypanosoma vivax infections. J Parasit Dis. 2017;41:450–8.
  225. Ravel S, Mediannikov O, Bossard G, Desquesnes M, Cuny G, Davoust B. A study on African animal trypanosomosis in four areas of Senegal. Folia Parasitol (Praha). 2015;62.
  226. Reis M de O, Souza FR, Albuquerque AS, Monteiro F, Oliveira LFDS, Raymundo DL, et al. Epizootic Infection by Trypanosoma vivax in Cattle from the State of Minas Gerais, Brazil. Korean J Parasitol. 2019;57:191–5.
  227. Robson J, Rickman LR. Results of a field trial for the improved detection of Trypanosoma vivax in domestic animals. Bull Epizoot Dis Afr. 1972;20:297–9.
  228. Rodrigues CMF, Batista JS, Lima JM, Freitas FJC, Barros IO, Garcia HA, et al. Field and experimental symptomless infections support wandering donkeys as healthy carriers of Trypanosoma vivax in the Brazilian Semiarid, a region of outbreaks of high mortality in cattle and sheep. Parasit Vectors. 2015;8:564.
  229. Roeder PL, Scott JM, Pegram RG, Prod H. Acute Trypanosoma vivax infection of ethiopian cattle in the apparent absence of tsetse. Trop Anim Health Prod. 1984;16:141–7.
  230. Rowlands GJ, Leak SG, Peregrine AS, Nagda SM, Mulatu W, D’Ieteren GD. The incidence of new and the prevalence and persistence of recurrent trypanosome infections in cattle in southwest Ethiopia exposed to a high challenge with drug-resistant parasites. Acta Trop. 2001;79:149–63.
  231. Sabir N, Chaudhry ZI, Aslam A, Muhammad K, Shahid M, Hussain A, et al. A study on prevalence and molecular characterization of trypanosomal species infecting equines in Lahore region, Pakistan. J Parasit Dis. 2018;42:96–101.
  232. Salas RZ, Zuluaga EAC, Vélez JR, Chávez OT, García VHP, Osorio LAR, et al. Bovine trypanosomiasis in dairy farming in the high tropics: first report of Haematobia irritans as the main vector for T. vivax and T. evansi in Colombia. Rev Med Vet (Bogota). 2017;21–34.
  233. Salim B, Bakheit MA, Sugimoto C. Molecular detection of equine trypanosomes in the Sudan. Vet Parasitol. 2014;200:246–50.
  234. Samdi S, Abenga JN, Fajinmi A, Kalgo A, Idowu T, Lawani F. Seasonal variation in trypanosomosis rates in small ruminants at the Kaduna abattoir, Nigeria. African J Biomed Res. 2008;11:229–32.
  235. Samdi SM, Abenga JN, Wayo B, Mshelia WP, Musa D, Haruna MK, et al. The complementary roles of biting flies and reservoirs of infection: In the resurgent of African animal trypanosomosis in Keffi local Government area of Nassarawa state, Nigeria. Asian J Anim Vet Adv. 2010;6:316–21.
  236. Samdi SM, Fajinmi AO, Kalejaye JO, Wayo B, Haruna MK, Yarnap JE, et al. Prevalence of trypanosomosis in cattle at slaughter in Kaduna central Abattoir. Asian J Anim Sci. 2011;5:162–5.
  237. Sanni TM, Onasanya GO, Adefenwa MA, Yakubu A, Ikeobi CON, Adebambo OA, et al. Molecular diagnosis of subclinical African Trypanosoma vivax infection and association with physiological indices and serum metabolites in extensively managed goats in the tropics. Open J Vet Med. 2013;3:39–45.
  238. Seck MT, Bouyer J, Sall B, Bengaly Z, Vreysen MJB. The prevalence of African animal trypanosomoses and tsetse presence in Western Senegal. Parasite. 2010;17:257–65.
  239. Sharma SP, Losho TC, Malau M, Mangate KG, Linchwe KB, Amanfu W, et al. The resurgence of trypanosomosis in Botswana. J S Afr Vet Assoc. 2001;72:232–4.
  240. Sheferaw D, Birhanu B, Asrade B, Abera M, Tusse T, Fikadu A, et al. Bovine trypanosomosis and Glossina distribution in selected areas of southern part of Rift Valley, Ethiopia. Acta Trop. 2016;154:145–8.
  241. Silbermayr K, Li F, Soudré A, Müller S, Sölkner J. A Novel qPCR Assay for the Detection of African Animal Trypanosomosis in Trypanotolerant and Trypanosusceptible Cattle Breeds. PLoS Negl Trop Dis. 2013;7.
  242. Silva RA, da Silva JA, Schneider RC, de Freitas J, Mesquita D, Mesquita T, et al. Outbreak of trypanosomiasis due to Trypanosoma vivax (Ziemann, 1905) in bovines of the Pantanal, Brazil. Mem Inst Oswaldo Cruz. l; 1996;91:561–2.
  243. Silva RA, Morales G, Eulert E, Montenegro A, Ybanez R. Outbreaks of trypanosomosis due to Trypanosoma vivax in cattle in Bolivia. Vet Parasitol. 1998;76:153–7.
  244. Silveira JAG, Rabelo TML, Lacerda ACR, Borges PAL, Tomás WM, Pellegrin AO, et al. Molecular detection and identification of hemoparasites in pampas deer (Ozotoceros bezoarticus Linnaeus, 1758) from the Pantanal Brazil. Ticks Tick Borne Dis. 2013;4:341–5.
  245. Simo G, Asonganyi T, Nkinin SW, Njiokou F, Herder S. High prevalence of Trypanosoma brucei gambiense group 1 in pigs from the Fontem sleeping sickness focus in Cameroon. Vet Parasitol. 2006;139:57–66.
  246. Simukoko H, Marcotty T, Phiri I, Geysen D, Vercruysse J, Van den Bossche P. The comparative role of cattle, goats and pigs in the epidemiology of livestock trypanosomiasis on the plateau of eastern Zambia. Vet Parasitol. 2007;147:231–8.
  247. Simwango M, Ngonyoka A, Nnko HJ, Salekwa LP, Ole-Neselle M, Kimera SI, et al. Molecular prevalence of trypanosome infections in cattle and tsetse flies in the Maasai Steppe, northern Tanzania. Parasites and Vectors. 2017;10.
  248. Sinshaw A, Abebe G, Desquesnes M, Yoni W. Biting flies and Trypanosoma vivax infection in three highland districts bordering lake Tana, Ethiopia. Vet Parasitol. 2006;142:35–46.
  249. Sinyangwe L, Delespaux V, Brandt J, Geerts S, Mubanga J, Machila N, et al. Trypanocidal drug resistance in eastern province of Zambia. Vet Parasitol. 2004;119:125–35.
  250. Snak A, Lara AA, Garcia FG, Pieri EM, Da Silveira JAG, Osaki SC, et al. Prevalence study on Trypanosoma vivax in dairy cattle in the western region on the State of Paraná, Brazil. Semin Ciências Agrárias. 2018;39:425–30.
  251. Solano P, Michel JF, Lefrancois T, de La Rocque S, Sidibe I, Zoungrana A, et al. Polymerase chain reaction as a diagnosis tool for detecting trypanosomes in naturally infected cattle in Burkina Faso. Vet Parasitol. 1999;86:95–103.
  252. Sow A, Sidibe I, Bengaly Z, Marcotty T, Sere M, Diallo A, et al. Field detection of resistance to isometamidium chloride and diminazene aceturate in Trypanosoma vivax from the region of the Boucle du Mouhoun in Burkina Faso. Vet Parasitol. 2012;187:105–11.
  253. Sow A, Ganaba R, Percoma L, Sidibé I, Bengaly Z, Adam Y, et al. Baseline survey of animal trypanosomosis in the region of the Boucle du Mouhoun, Burkina Faso. Res Vet Sci. 2013;94:573–8.
  254. Specht EJK. Prevalence of bovine trypanosomosis in Central Mozambique from 2002 to 2005. Onderstepoort J Vet Res. 2008;75:73–81.
  255. Suárez C, García F, Román D, Coronado A, Perrone T, Reyna A, et al. Risk factors associated with the bovine trypanosomosis of livestock farms in Venezuela. Zootec Trop. 2010;27:363–72.
  256. Swai ES, Kaaya JE. A parasitological survey for bovine trypanosomosis in the livestock/wildlife ecozone of Northern Tanzania. Vet World. 2012;5:459–64.
  257. Tadesse A, Tsegaye B. Bovine trypanosomosis and its vectors in two districts of Bench Maji zone, South Western Ethiopia. Trop Anim Health Prod. 2010;42:1757–62.
  258. Tafese W, Melaku A, Fentahun T. Prevalence of bovine trypanosomosis and its vectors in two districts of East Wollega Zone, Ethiopia. Onderstepoort J Vet Res. 2012;79:E1-4.
  259. Takeet MI, Fagbemi BO, De Donato M, Yakubu A, Rodulfo HE, Peters SO, et al. Molecular survey of pathogenic trypanosomes in naturally infected Nigerian cattle. Res Vet Sci. 2013;94:555–61.
  260. Tamasaukas R, Roa N, Cobo M. Trypanosomosis due to Trypanosoma vivax in two buffalo (Bubalus bubalis) farms of Guárico state, Venezuela. Rev Cient la Fac Ciencias Vet la Univ del Zulia. 2006;16:575–8.
  261. Tarimo-Nesbitt RA, Golder TK, Dransfield RD, Chaudhury MF, Brightwell R. Trypanosome infection rate in cattle at Nguruman, Kenya. Vet Parasitol. 1999;81:107–17.
  262. Tasew S, Duguma R. Cattle anaemia and trypanosomiasis in western Oromia State, Ethiopia. Rev Med Vet (Toulouse). 2012;163:581–8.
  263. Tchamdja E, Kulo AE, Vitouley HS, Batawui K, Bankolé AA, Adomefa K, et al. Cattle breeding, trypanosomosis prevalence and drug resistance in Northern Togo. Vet Parasitol. 2017;236:86–92.
  264. Terefe E, Haile A, Mulatu W, Dessie T, Mwai O. Phenotypic characteristics and trypanosome prevalence of Mursi cattle breed in the Bodi and Mursi districts of South Omo Zone, southwest Ethiopia. Trop Anim Health Prod. 2015;47:485–93.
  265. Tesfaheywet Z, Getnet F, Ayana M. A cross-sectional study on the prevalence of bovine trypanosomosis in Amhara region, Northwest Ethiopia. Livest Res Rural Dev. 2012;24.
  266. Tesfaye D, Ibrahim N. Prevalence of Bovine Trypanosomosis in Assosa District of Benishangul Gumuz Prevalence of Bovine Trypanosomosis in Assosa. Adv Biol Res (Rennes). 2017;11:13–7.
  267. Thumbi SM, Jung’A JO, Mosi RO, McOdimba FA. Spatial distribution of African animal trypanosomiasis in suba and teso districts in Western Kenya. BMC Res Notes. 2010;3.
  268. Trail JC, D’Ieteren GD, Viviani P, Yangari G, Nantulya VM. Relationships between trypanosome infection measured by antigen detection enzyme immunoassays, anaemia and growth in trypanotolerant N’Dama cattle. Vet Parasitol. 1992;42:213–23.
  269. Ukpai OM, Obasi NI. Prevalence of trypanosomiasis in relation to some haematological parameters in cattle, Ohafia LGA, Abia State, Nigeria. Niger J Parasitol. 2017;38:250–2.
  270. Van Den Bossche P, Mudenge D, Mubanga J, Norval A. The parasitological and serological prevalence of tsetse-transmitted bovine trypanosomosis in the Eastern Caprivi (Caprivi District, Namibia). Onderstepoort J Vet Res. 1999;66:103–10.
  271. Van den Bossche P, Shumba W, Makhambera P. The distribution and epidemiology of bovine trypanosomosis in Malawi. Vet Parasitol. 2000;88:163–76.
  272. Vokaty S, McPherson VO, Camus E, Applewhaite L. Ovine trypanosomosis: a seroepidemiological survey in coastal Guyana. Rev Elev Med Vet Pays Trop. 1993;46:57–9.
  273. Waiswa C, Katunguka-Rwakishaya E. Bovine trypanosomiasis in south-western Uganda: packed-cell volumes and prevalences of infection in the cattle. Ann Trop Med Parasitol. 2004;98:21–7.
  274. Wells EA, Betamcourt A, Ramirez LE. Serological evidence for the geographical distribution of Trypanosoma vivax in the new world. Trans R Soc Trop Med Hyg. 1977;71:448–9.
  275. Wijers DJB. The complex epidemiology of Rhodesian sleeping sickness in Kenya and Uganda. Part II: Observations in Samia (Kenya). Trop Geogr Med. 1974;26:182–97.
  276. Yesufu HM, Mshelbwala AS. Trypanosomiasis survey in cattle and tsetse flies along a trade cattle route in southwestern nigeria. Ann Trop Med Parasitol. 1973;67:307–12.
  277. Zanatto DCS, Gatto IRH, Labruna MB, Jusi MMG, Samara SI, Machado RZ, et al. Coxiella burnetii associated with BVDV (Bovine Viral Diarrhea Virus), BoHV (bovine herpesvirus), Leptospira spp., Neospora caninum, Toxoplasma gondii and Trypanosoma vivax in reproductive disorders in cattle. Rev Bras Parasitol Vet. 2019;28:245–57.
  278. Cadioli FA, Barnabe P de A, Machado RZ, Teixeira MCA, Andre MR, Sampaio PH, et al. First report of Trypanosoma vivax outbreak in dairy cattle in Sao Paulo state, Brazil. Rev Bras Parasitol Vet. 2012;21:118–24.
  279. Ganyo EY, Boampong JN, Masiga DK, Villinger J, Turkson PK. Haematology of N’Dama and West African Shorthorn cattle herds under natural Trypanosoma vivax challenge in Ghana. F1000Research. 2018;7:314.
  280. González JR, Meléndez RD. Seroprevalencia de la tripanosomosis y anaplasmosis bovina en el municipio Juan José Mora del estado Carabobo, Venezuela, Mediante la técnica de ELISA. Rev Cient la Fac Ciencias Vet la Univ del Zulia. 2007;17:449–55.
  281. Laohasinnarong D, Goto Y, Asada M, Nakao R, Hayashida K, Kajino K, et al. Studies of trypanosomiasis in the Luangwa valley, north-eastern Zambia. Parasites and Vectors. 2015;8:1–8.
  282. Lopes STP, Prado B da S, Martins GHC, Beserra HEA, Sousa Filho MAC de, Evangelista LS de M, et al. Trypanosoma vivax em bovino leiteiro. Acta Sci Vet. 2018;46:1–5.
  283. Wijers DJB. The complex epidemiology of Rhodesian sleeping sickness in Kenya and Uganda. 1. The absence of the disease on Mfangano island (Kenya). Trop Geogr Med. 1974;26:58–64.
  284. Mihok S, Munyoki E, Brett RA, Jonyo JF, Röttcher D, Majiwa PAO, et al. Trypanosomiasis and the conservation of black rhinoceros (Diceros bicornis) at the Ngulia Rhino Sanctuary, Tsavo West National Park, Kenya. Afr J Ecol. 1992;30:103–15.
  285. Thon MGA. Prevalence of Trypansomosis in Cattle in Juba Area, Central Equatoria State, Sudan. MTAH thesis, Department of Preventive Medicine Faculty of Veterinary Medicine University of Khartoum. Department of Preventive Medicine Faculty of Veterinary Medicine University of Khartoum; 2009.
  286. Shereni W, Anderson NE, Nyakupinda L, Cecchi G. Spatial distribution and trypanosome infection of tsetse flies in the sleeping sickness focus of Zimbabwe in Hurungwe District. Parasites and Vectors. 2016;9.
  287. Genevieve A-Y, Bakary C, Mavoungou JF, Silas Lendzele S, Abdallah NE. Preliminary study on vectors of bovine trypanosomosis in the central African republic one decade after the socio-military crisis. J Anim Plant Sci. 2019;39:6487–94.
  288. Franco JR, Cecchi G, Priotto G, Paone M, Diarra A, Grout L, et al. Monitoring the elimination of human African trypanosomiasis: Update to 2014. PLoS Negl Trop Dis. 2017;11:1–26.
  289. Ahmed SK, Rahman AH, Hassan MA, Salih SEM, Paone M, Cecchi G. An atlas of tsetse and bovine trypanosomosis in Sudan. Parasit Vectors. 2016;9:194.
  290. Stephen LE. Trypanosomiasis. A Veterinary Perspective, Pergamon Press. 1986.
  291. Aregawi WG, Agga GE, Abdi RD, Büscher P. Systematic review and meta-analysis on the global distribution , host range , and prevalence of Trypanosoma evansi. Parasit Vectors. 2019;12:67:1–25.
  292. Gardiner PR. Recent Studies of the Biology of Trypanosoma vivax. Adv. Parasitol. 1989. p. 229–317.
  293. Desquesnes M. Evaluation of a simple PCR technique for the diagnosis of Trypanosoma vivax infection in the serum of cattle in comparison to parasitological techniques and antigen-enzyme-linked immuno sorbent assay. Acta Trop. 1997;65:139–48.

Tables

Table 1: Countries with reported T. vivax infection in diverse host species tested with diverse methods

Country

Host species studied

Test method

Number of tests (total = 232,627)

Number of positives (total = 24,420)

References

Argentina

Cattle

Reverse line blot

186

16

[217]

Benin

Buffoon kob, cattle, hartebeest, roan antelope, warthog, waterbuck,

Thin and thick blood smears

312

205

[10,99]

Bolivia

Cattle

Thin blood smear, Giemsa stained blood smear, PCR

1520

311

[123,177,243]

Botswana

Cape buffalo, cattle, donkey, goat, greater kudu, impala, lechwe, reedbuck, sable antelope, tsessebe

MHCT/Woo test, Giemsa stained thick and thin blood smear, IFAT

3040

399

[100,239]

Brazil

Cattle, donkey, goat, horse, pampas deer, sheep, water buffalo

MHCT/Woo test, PCR, IFAT, thin and thick blood smear, buffy coat smear, Ab-ELISA, PCR

11468

4079

[4,51,83–85,91,94,112,116,125–127,58,154,156,212,219,220,226,228,242,244,250,59,274,277,60–62,71,72,81]

Burkina Faso

Cattle

Buffy coat smear, Ag-ELISA, Ab-ELISA, PCR

11095

1095

[65,90,151,216,241,251–253]

Cameroon

African civet, black legged mangoose, black striped duiker, blue duiker, bosman potto, brush tailed porcupine, cattle, cloaked mangabey, crested mangabey, crocodile, dark mangoose, de Brazza’s monkey, dog, dwarf guenon, giant forest squirrel, giant rat, goat, golden cat, golden potto, greater cane rat, greater white-nosed monkey, guereza white colobus, long-tailed pangolin, mandrill, mona monkey, monitor lizard, moustached monkey, ogilby’s duiker, Peter’s duiker,pig, red-legged sun squirrel, royal antelope, sheep, sitatunga, small-spotted genet, tree dassie, tree pangolin, two-spotted palm civet, water chevrotain, white-eyelid mangabey, yellow-backed duiker

Buffy coat smear, PCR

4176

406

[7, 13, 14, 170, 202, 245][7,13,14,170,202,245]

Chad

Cattle

Buffy coat smear, Ab-ELISA

1866

435

[93]

Colombia

Cattle, goat, sheep

Blood smear, PCR, IFAT

6712

1699

[135,136,215,221,232,274]

Costa Rica

Cattle

Blood smear, IFAT

642

53

[210,274]

Côte d’Ivoire

Cattle, goat, pig, sheep

MHCT/Woo test, PCR

2185

195

[45,148,197]

Democratic Republic of the Congo

Cattle, dog, goat, pig, sheep

MHCT/Woo test, ELISA

685

41

[167,168]

Ecuador

Cattle

IFAT

310

70

[274]

El Salvador

Cattle

IFAT

100

15

[274]

Equatorial Guinea

Goat, sheep

PCR

559

10

[79]

Ethiopia

Cattle, donkey, dromedary camel, goat, horse, mule, sheep

Giemsa stained blood smear, blood smear, buffy coat smear, MHCT/Woo test, thin and thick blood smear, Ab-ELISA, PCR

55196

2600

[6,43,86,87,92,98,101,103,107,113–115,44,122,142,144,145,152,178–182,48,184,187,191,229,230,240,248,257,258,262,64,264–266,69,70,74–76]

French Guiana

Cattle

Ag-ELISA

3000

870

[95]

Gabon

Cattle

Buffy coat smear, Ag-ELISA, PCR

442

26

[80,157,268]

Gambia

Cattle, donkey, goat, horse, sheep

Buffy coat smear, Giemsa stained blood smear, Ab-ELISA, PCR

5745

1329

[8,96,102,173,213,218]

Ghana

Cattle, goat, pig, sheep

Buffy coat smear, PCR, Ag-latex agglutination test

1786

231

[46,117,143,198]

Guyana

Goat, sheep

MHCT/Woo test, IFAT

467

15

[55,272]

Kenya

Black rhinoceros, cattle, dromedary camel, goat, horse, pig, sheep

Thin and thick blood smear, Giemsa stained blood smear, buffy coat smear, MHCT/Woo test, Ag-ELISA, PCR

5156

845

[66,146,209,227,261,267,275,172,174,183,185,196,200,201,208]

Liberia

Cattle

Giemsa stained blood smear, IFAT, Ab-ELISA

700

327

[155,176]

Malawi

Cattle

Giemsa stained blood smear

9309

9

[271]

Mali

Cattle

Buffy coat smear

796

34

[192]

Martinique

Cattle

IFAT

227

0

[50]

Mozambique

Cattle

Blood smear

16895

1245

[254]

Namibia

Cattle

Giemsa stained thick and thin blood smear, MHCT

1481

15

[270]

Nigeria

Cattle, dog, goat, horse, sheep

Blood smear, Giemsa stained blood smear, MHCT/buffy coat smear, MHCT/Woo test, Ag-ELISA, PCR

20080

2926

[52,53,110,134,137–140,153,166,206,207,63,211,214,234–237,259,269,276,88,89,104–106,108,109]

Pakistan

Donkey, horse, mule

PCR

300

0

[231]

Paraguay

Cattle

IFAT

15

6

[274]

Peru

Cattle

Blood smear, MHCT/Woo test, Giemsa stained blood smear, IFAT, PCR

985

119

[171,177,222,274]

Rwanda

Cattle

Blood smear

3630

36

[12]

Senegal

Cattle, dog, donkey, goat, horse, sheep

Buffy coat smear, blood smears, Ab-ELISA, PCR

4890

365

[111,128,129,225,238]

South Africa

Cattle

PCR

143

30

[169]

Sudan

Cattle, donkey, dromedary camel, horse

Blood smear, Buffy coat smear, PCR

4426

366

[132,186,223,233]

Tanzania

African civet, bohor reedbuck, cattle, Coke’s hartebeest, giraffe, Grant’s gazelle, hunting dog, impala, Kirk’s dikdik, klipspringer, Lichtenstein’s hartebeest, oribi, oryx, ostrich, pig, roan antelope, southern reedbuck, steinbuck, Thomson’s gazelle, tsessebe, warthog, wildebeest, zebra

Blood smear, thin and thick blood smear, Giemsa stained blood smear, buffy coat smear, PCR, PCR-LAMP

9974

431

[5,56,194,203,247,256,78,130,131,133,141,147,149,188]

Togo

Cattle

PCR-RFLP

354

27

[263]

Uganda

Cattle, dog, donkey, goat, pig, sheep

Giemsa stained blood smear, MHCT/Woo test, thick and thin blood smear, buffy coat smear, Ab-ELISA, PCR

28510

1932

[47,49,160–165,189,190,195,205,54,273,57,67,68,77,82,158,159]

Venezuela

Cattle, horse, sheep, water buffalo

MHCT/Woo test, stained blood smear, IFAT, Ab-ELISA, PCR

6328

1373

[73,118–121,124,224,255,260]

Zambia

African civet, baboon, bat, black rhinoceros, bushbuck, cane rat, Cape buffalo, cattle, crocodile, eland, elephant, genet, giraffe, goat, greater kudu, grey duiker, grysbok, hare, hartebeest, hippopotamus, hunting dog, hyena, impala, jackal, leopard, lion, mongoose, pig, porcupine, puku, reedbuck, roan antelope, serval, vervet monkey, warthog, waterbuck, wild cat, wildebeest, zebra

PCR, buffy coat smear

6936

234

[9,97,150,175,193,199,204,246]

Footnote: Ab-ELISA = Antibody enzyme-linked immunosorbent assay, Ag-ELISA= antigen enzyme-linked immunosorbent assay, MHCT = micro hematocrit centrifugation technique, IFAT = immunofluorescence antibody test, PCR = Polymerase chain reaction, PCR-LAMP = Polymerase chain reaction - Loop mediated isothermal amplification, PCR-RFLP= Polymerase chain reaction-restriction fragment length polymorphism

Table 2: Domestic animal species tested for infection with T. vivax. * T. vivax was not observed in Martinique and Pakistan

Species

List of countries

Number of tests

Positive animals

References

Cattle

Argentina, Benin, Bolivia, Botswana, Brazil, Burkina Faso, Cameroon, Chad, Colombia, Costa Rica, Côte d’Ivoire, Democratic Republic of the Congo, Ecuador, El Salvador, Ethiopia, French Guiana, Gabon, Gambia, Ghana, Kenya, Liberia, Malawi, Mali, Martinique*, Mozambique, Namibia, Nigeria, Paraguay, Peru, Rwanda, Senegal, South Africa, Sudan, Tanzania, Togo, Uganda, Venezuela, Zambia

198593

20964

[4,5,48,171,173–177,180,182,184,185,49,187–196,50,197–200,202,203,205–208,51,209–212,214–217,219,220,52,222–227,229,230,232,235,53,236,238–243,246–248,54,249–258,57,259,261–269,58,270,271,273,274,276–281,59,282,283,6,61,62,64–66,68–71,73,12,74–78,80–83,85,14,86–88,90–95,99,40,101–103,105,106,108,109,111,113,114,44,116,118,122,123,125–127,129–131,45,132,134–136,138,139,141–143,145,46,147–149,151–153,155–158,47,159,161–167,169,170]

Dromedary camel

Ethiopia, Kenya, Sudan

1611

133

[6,115,172,186]

Dog

Cameroon, Democratic Republic the Congo, Nigeria, Senegal, Uganda

574

1

[7,137,158,168,214,225]

Donkey

Botswana, Brazil, Ethiopia, Pakistan*, Sudan, Uganda

2713

152

[6,8,233,239,248,43,96,107,178,189,225,228,231]

Goat

Botswana, Brazil, Cameroon, Colombia, Côte d’Ivoire, Democratic Republic of the Congo, Equatorial Guinea, Ethiopia, Gambia, Ghana, Guyana, Kenya, Nigeria, Senegal, Uganda, Zambia

9715

526

[6,7,128,137,140,143,144,150,158,168,179,193,55,197,201,204,211,213,218,221,225,234,237,57,239,246,248,60,63,68,79,98,112]

Horse

Brazil, Ethiopia, Gambia, Kenya, Nigeria, Pakistan*, Senegal, Sudan, Venezuela

3305

857

[8,84,233,96,104,118,146,181,214,225,231]

Mule

Ethiopia, Pakistan*

353

0

[43,181,231,248]

Pig

Cameroon, Côte d’Ivoire, Democratic Republic the Congo, Ghana, Kenya, Tanzania, Uganda, Zambia

2650

233

[7,57,245,246,67,68,133,158,168,197,198,201]

Sheep

Brazil, Cameroon, Colombia, Côte d’Ivoire, Democratic Republic of the Congo, Equatorial Guinea, Ethiopia, Gambia, Ghana, Guyana, Kenya, Nigeria, Senegal, Uganda, Venezuela

6447

455

[6,7,128,134,137,140,143,144,168,197,201,213,55,221,225,234,248,272,57,60,79,98,116,118,120]

Small ruminants

Kenya, Nigeria

988

69

[89,110,227]

Water buffalo

Brazil, Venezuela

2144

509

[116,118,119,121,260]

 

Table 3: Wild animal species tested positive for T. vivax infection

Host species

Scientific name

Country

Number of tests

Positive tests

Positivity rate

References

Black rhinoceros

Diceros bicornis

Kenya

1

1

100

[284]

Black striped duiker

Cephalophus dorsalis

Cameroon

37

3

8.1

[13]

Blue duiker

Cephalophus monticola

Cameroon

290

24

8.3

[13]

Bosman potto

Perodicticus potto

Cameroon

8

3

37.5

[13]

Brush tailed porcupine

Atherurus africanus

Cameroon

106

7

6.6

[13]

Buffoon kob

Kobus kob

Benin

50

1

2

[10]

Bushbuck

Tragolaphus scriptus

Zambia

51

4

7.8

[97]

Cape buffalo

Syncerus caffer

Botswana, Zambia

1105

285

25.8

[9,97,100]

Cloaked mangabey

Cercocebus albigena

Cameroon

12

2

16.7

[13]

Crocodile

Crocodylus niloticus

Cameroon

3

1

33.3

[13]

De Brazza’s Monkey

Cercopithecus neglectus

Cameroon

1

1

100

[13]

Dwarf guenon

Miopithecus tlapoin

Cameroon

55

5

9.1

[13]

Eland

Taurotragus oryx

Zambia

3

1

33.3

[97]

Giant rat

Cricetomys gambianus

Cameroon

135

4

2.9

[13]

Greater kudu

Tragelaphus strepsiceros

Botswana, Zambia

36

26

72.2

[97,100]

Greater white-nosed monkey

Cercopithecus nictitans

Cameroon

155

22

14.2

[13]

Grey duiker

Sylvicapra grimmia

Zambia

7

1

14.3

[97]

Guereza white colobus

Colobus guereza

Cameroon

14

2

14.3

[13]

Hartebeest

Alcelaphus bubalis

Benin

20

1

5

[10]

Hippopotamus

Hippopotamus amphibius

Zambia

29

1

3.4

[9]

Impala

Aepyceros melampus

Botswana

23

14

60.9

[100]

Lechwe

Kobus leche

Botswana

110

39

35.5

[100]

Long tailed pangolin

Manis tetradactyla

Cameroon

34

2

5,9

[13]

Mona monkey

Cercopithecus mona

Cameroon

46

8

17,4

[13]

Monitor lizard

Varanus ornatus

Cameroon

8

1

12,5

[13]

Moustached monkey

Cercopithecus cephus

Cameroon

101

11

10.9

[13]

Oryx

Oryx beisa

Tanzania

1

1

100

[56]

Puku

Kobus vardonii

Zambia

24

1

4.2

[97]

Reedbuck

Redunca sp.

Botswana, Zambia

3

3

100

[9,100]

Sable antelope

Hippotragus niger

Botswana

22

7

31.8

[100]

Sitatunga

Tragelaphus spekei

Cameroon

5

1

20

[13]

Small-spotted genet

Genetta servalina

Cameroon

8

1

12.5

[13]

Southern reedbuck

Redunca arundinum

Tanzania

4

1

25

[56]

Tree pangolin

Manis tricuspis

Cameroon

20

5

25

[13]

Tsessebe

Damaliscus lunatus

Botswana

15

6

40

[100]

Two-spotted palm civet

Nandinia binotata

Cameroon

32

3

9.4

[13]

Warthog

Phacochoerus aethiopicus

Zambia

56

1

1.8

[9]

Waterbuck

Kobus ellipsiprymnus

Zambia

30

19

63.3

[9,97]

White-eyelid mangabey

Cercocebus torquatus

Cameroon

5

2

40

[13]

 

Table 4: Sub group Meta-analysis for different species using different diagnostic methods

Host species

Diagnostic method

Number of publications

Number of tests

Number of positives

Pooled prevalence in %

95% CI

Water buffalo

Parasitological

1

316

36

11.4

8.3-15.4

 

Molecular

Serological

2

2

609

556

127

301

20.9

57.6

17.4-25.0

22.5-86.4

Camel

Molecular

4

1611

133

8.4

3.4-19.3

Cattle

Parasitological

92

102910

5414

4.6

4.0-5.3

 

Molecular

51

31549

3140

7.4

6.2-8.7

 

Serological

23

16469

4495

34.6

28.0-41.9

Dog

Parasitological

3

257

0

3.4

1.1-9.6

 

Molecular

2

189

1

1.2

0.2-8.5

Equine

Parasitological

8

2471

20

1.5

0.9-2.6

 

Molecular

7

1425

251

5.6

2.7-11.3

 

Serological

1

6

3

50.0

16.8-83.2

Pig

Parasitological

4

799

3

1.1

0.4-2.9

 

Molecular

10

1851

230

9.0

4.9-15.9

Small ruminant

Parasitological

19

8990

220

2.3

1.5-3.6

 

Molecular

15

4045

327

5.0

2.7-9.3

 

Serological

3

408

43

13.8

6.1-28.4

Wild animal

Parasitological

Molecular

3

3

1093

1618

75

121

11.8

10.7

7.1-16.9

8.6-13.3

 

Serological

1

748

318

49.3

37.5-61.2