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A scoping review on tsetse fly blood meal sources and its assay methods since 1956 to 2022

Parasites & Vectors volume 17, Article number: 52 (2024) Cite this article

Abstract

Background

Tsetse flies (Glossina spp.) are the definitive biological vectors of African trypanosomes in humans and animals. Controlling this vector is the most promising method of preventing trypanosome transmission. This requires a comprehensive understanding of tsetse biology and host preference to inform targeted design and management strategies, such as the use of olfaction and visual cues in tsetse traps. No current review exists on host preference and blood meal analyses of tsetse flies.

Methods

This review presents a meta-analysis of tsetse fly blood meal sources and the methodologies used to identify animal hosts from 1956 to August 2022. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses extension for Scoping Reviews (PRIMA-ScR) was applied. This focused on tsetse-endemic countries, blood meal analysis methodologies and the blood meal hosts identified. The articles were retrieved and screened from databases using predetermined eligibility criteria.

Results

Only 49/393 of the articles retrieved matched the inclusion criteria. Glossina's main hosts in the wild included the bushbuck, buffalo, elephant, warthog, bushpig and hippopotamus. Pigs, livestock and humans were key hosts at the domestic interface. The least studied species included Glossina fuscipleuris, G. fusca, G. medicorum, G. tabaniformis and G. austeni. In the absence of preferred hosts, Glossina fed opportunistically on a variety of hosts. Precipitin, haemagglutination, disc diffusion, complement fixation, ELISA and PCR-based assays were used to evaluate blood meals. Cytochrome b (Cyt b) was the main target gene in PCR to identify the vertebrate hosts.

Conclusions

Tsetse blood meal sources have likely expanded because of ecological changes that could have rendered preferred hosts unavailable. The major approaches for analysing tsetse fly blood meal hosts targeted Cyt b gene for species identification by Sanger sequencing. However, small-fragment DNAs, such as the mammalian 12S and 16S rRNA genes, along with second- and third-generation sequencing techniques, could increase sensitivity for host identification in multiple host feeders that Sanger sequencing may misidentify as “noise”. This review of tsetse fly blood meal sources and approaches to host identification could inform strategies for tsetse control.

Graphical Abstract

Background

Tsetse flies (Glossina spp.) are obligate haematophagous biting insects that are endemic to 38 countries in sub-Saharan Africa. They are the definitive biological vectors of the African trypanosome parasites (genus Trypanosoma). Trypanosome parasites develop within the tsetse fly and transform into infective metacyclic trypomastigotes that cause trypanosomiasis in a wide range of mammalian hosts [1].

Tsetse flies digest blood meals in 1 ½ to 4 days, depending on the amount consumed [2], and they replenish their dwindling abdominal food reserves every 2 to 3 days [3]. Several approaches to analysing blood meals to decipher the hosts have been developed. These methods range from the traditional serological techniques such as precipitin test (PT) and enzyme-linked immunosorbent assay (ELISA) to an advanced molecular approach [4,5,6].

Several studies on tsetse fly blood meal hosts have improved our understanding of the preferred animal hosts and the vector’s potential role in the epidemiology of African trypanosomiasis [7,8,9,10,11]. However, the feeding habits of tsetse fly vectors may change over time depending on the availability of hosts in their habitats. For example, opportunistic feeding behaviour in Glossina palpalis has been shown to shift from rhinoceroses to suids over time, probably because of ecological changes that made the preferred blood meal hosts unavailable [12]. It has been proposed that whenever an environmental change is detected, the feeding sources of tsetse flies may need to be assessed [13]. To surmount this, some of the limitations need to be overcome. For instance, the time taken from sample collection to publication of results on analysis of blood meals cited in the literature ranged from 1 to 16 years [12, 14]. Thus, by the time some studies are published, particularly those documented over a decade later, ecological changes may have occurred and the preferred blood meal hosts might have migrated to alternative locations.

To our knowledge, there is no current review of tsetse fly blood meal analysis and the methodologies used to determine the vector’s propensity for blood meals from potential animal hosts. Thus, we set out to (i) review the published literature on tsetse blood meal sources and methods used for analysis from 1956 to August 2022, (ii) identify tsetse fly species whose feeding preference(s) on hosts are less understood and (iii) identify the strengths and drawbacks of methods used for blood meal analysis.

Methods

Protocol and registration

The scoping review procedure for this study was submitted to the Open Science Framework (OSF) (https://osf.io/yczqp/). It was created using the Preferred Reporting Items for Systematic Reviews and Meta-Analyses extension for Scoping Reviews (PRIMA-ScR) criteria [15].

Eligibility criteria

The set criteria for eligibility of the peer reviewed journal articles for this review included original research publications on tsetse blood meal analysis, articles written in English and articles published up to August 2022. We excluded experimental studies and those in which blood meal hosts were not determined.

Article search strategy from information sources

The article searches were performed using PubMed, Scopus and International System for Agricultural Science and Technology (AGRIS) electronic databases. The key words used in the search for peer reviewed journal information included “blood”, “meal” and “tsetse”.

Selection of sources of the evidence

The PubMed, Scopus and FAO-AGRIS databases were queried individually and fed into Rayyan artificial intelligence software (https://www.rayyan.ai/). The search results were evaluated and duplicates deleted. Titles and abstracts of the peer-reviewed articles were used to determine their eligibility. Two reviewers independently screened the selected articles for inclusion. All studies that did not answer the set research question(s) were disregarded. The selected full-text journal articles in Portable Document Format (PDF) were uploaded to Rayyan software for data extraction. A total of 53 articles were included for the full text screening and data charting (Fig. 1).

Fig. 1
figure 1

Flow chart showing the selection of articles for inclusion in the scoping review. A total of 393 articles were retrieved from PubMed, AGRIS FAO and Scopus electronic databases. After removal of duplicates, 222 articles were screened for relevance and ultimately 53 articles were included. Two articles were in French (abstracts were in English) and two could not be accessed because of subscription access. Finally 49 articles were included in the study.

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Data extraction

Data extraction was performed using a data-charting sheet developed in this review (Additional file 1). The authors, title, year of publication, country, study area, period of sample collection, tsetse fly species studied, number of samples analysed, type of samples collected, diagnostic method used and proportion of samples positively identified were obtained from each publication. The gene and sequencing methods were extracted from articles on molecular approaches to blood meal host identification.

Data analysis

Descriptive data analysis was conducted using R software version 4.3.2 and the results presented as frequencies and percentages. Where appropriate, the data were presented using graphs or tables.

Results

Publication statistics

The initial reference title searches yielded 384 relevant publications. These included 147, 197 and 40 publications from PubMed, Scopus and FAO-AGRIS, respectively. After removal of duplicates, a full text search was done on 213 selected references. Snowballing from the selected references yielded nine more publications, resulting in 222 articles (Fig. 1). The final synthesis included 49 publications (Table 1).

Table 1 Distribution of blood meal studies per nation in Africa
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Methods of identifying vertebrate hosts that tsetse feed on

This review found that molecular detection of the host DNA was used in 77.4% (24/31) of the studies published after the year 2000. ELISA, precipitin test (PT), haemagglutination inhibition test (HIT), disc diffusion or a combination of PT and HIT or ELISA and complement fixation test (CFT) were utilized in studies conducted before 2005. The methods for analysing blood meals are summarized in Fig. 2.

Fig. 2
figure 2

Scatter plot of studies per blood meal method (n = 49). Polymerase chain reaction (PCR), enzyme-linked immunosorbent assay (ELISA), haemagglutination inhibition test (HIT), precipitin Test (PT), gel diffusion (GD) and complement fixation test (CFT) were used. Of the 24/49 (49%) studies which utilized PCR, 1/24 (4.2%) used high-resolution melting (HRM) analysis and 1/24 (4.2%) used multiplex PCR

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Some studies utilized PCR for amplification of the target gene, amplicon sequencing and comparison of the query sequences with information available in the GenBank of NCBI (BLAST) to identify hosts for tsetse blood meals. The mitochondrial cytochrome b (Cyt b) gene was targeted in 21/24 (87.5%) of the studies that employed PCR-based molecular assays. This gene is associated with limited intra-species variability and high inter-species variation. Figure 3 shows the distribution of different genes in the identification of tsetse fly blood meal sources. Sanger sequencing (n = 12/24; 50%) was the most commonly used method followed by heteroduplex hybridization (n = 8/24; 33.3%). Illumina second-generation sequencing accounted for 12.5% (n = 3/24). Only Cameroon (n = 4/7; 57.1%) and the Democratic Republic of Congo (n = 3/7; 41.3%) reported results using heteroduplex hybridization.

Fig. 3
figure 3

Distribution of gene-specific PCR studies for mammalian host blood meals (n = 24). Most of the studies amplified only Cyt b gene 19/24 (79.2%), 2/24 (8.3%) amplified both Cyt b and COI, 2/24 (8.3%) amplified 12S rRNA gene and 1/24 (4.2%) amplified a combination of the three genes

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Tsetse flies species and their blood meal sources

Blood meal hosts were identified in 20 of the 33 tsetse fly species and subspecies present in Africa (Table 2). Glossina pallidipes was the most studied species accounting for 21/87 (24.1%) of the published articles, followed by G. palpalis palpalis at 13.8% (13/87). Glossina fusca, G. medicorum and G. austeni were the least studied at 1/87 (1.1%), 2/87 (2.3%) and 2/87 (2.3%) respectively. Thus, determination of tsetse fly host feeding preferences through blood meal analysis of 13/33 (39.4%) Glossina species and sub-species may not have been fully evaluated.

Table 2 Major and minor blood meal hosts for Glossina spp.
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The blood feeding habits of tsetse flies were influenced by their habitat. This study clustered tsetse flies by collection site. The first group involved ‘human-wildlife’ interface such as the protected national parks and game reserves, while the second group was ‘human-wildlife-domestic animals’ interface such as the edges of protected parks. The third group involved human-domestic-animals interface in human residential areas. Tsetse flies’ blood meal hosts were extracted and summarized by their preferred hosts as shown in Table 2.

Discussion

This study focused on blood meal sources and the methods of blood meal analysis in tsetse flies from 1956 to August 2022. The blood meal sources were mainly dependent on the ecology and the species of tsetse fly vectors. Suids (warthogs, domestic and bush pigs) and bovids (bushbuck and buffalo) were the preferred hosts for most tsetse fly species. Precipitin and haemagglutination tests were the commonly used methods of blood meal analysis from 1956 to 1988. ELISA was predominantly utilized from 1992 to 2008. Most studies after the year 2001 utilized PCR. The traditional serological tests such as PT were less sensitive and could not identify all blood meal hosts of tsetse flies. However, molecular techniques were more sensitive and led to identification of more blood meal hosts.

Kenya recorded the highest number of published research studies focusing on tsetse fly blood meal analysis. This may be due to the existing vibrant research institutions such as International Livestock Research Institute (ILRI), International Centre of Insect Physiology and Ecology (icipe) and Kenya Agricultural and Livestock Research Organization (KALRO)—all of which collaborate in research with Kenyan institutions of higher learning. Additionally, Kenya has active government-led programmes on tsetse fly and trypanosomiasis eradication led by the Kenya Tsetse and Trypanosomiasis Eradication Council (KENTTEC) in conjunction with the aforementioned research institutes for adaptive and operational research.

Most of the studies focused on Glossina pallidipes (24.1%), G. palpalis (13.8%), G. morsitans (13.7%) and G. f. fuscipes (11.5%) [16,17,18,19], which are considered as the main vectors of AAT and HAT in Eastern and Southern Africa and are the predominant species of tsetse flies [20,21,22]. Glossina fuscipes accounts for at least 90% of the HAT transmissions [23]. Regionally unlike the other species of tsetse flies, G. austeni, a vector of AAT, is present only on the east coast countries of the African continent including Somalia, Kenya, Tanzania, Mozambique and north-eastern parts of South Africa and Zimbabwe. From the published studies, only two studies were conducted on blood meal analysis for G. austeni from the tsetse fly samples that were collected between 1982 and 1993 [12] and one from sample data collected between 1950–1955 [24]. Since the Morsitans group have been identified as the major vectors of AAT, there is a need to carry out more blood meal analyses to check the possibility of varying hosts that can be fed on by Morsitans tsetse flies such as G. austeni and the resultant transmission of trypanosomiasis.

There seemed to be an expansion of tsetse flies feeding patterns likely guided by semiochemical cue attraction emanating from the bodies of preferred blood meal hosts from which tsetse flies fed on. The presence of these hosts may, however, be influenced by the ecosystem services and functioning. The grouping of tsetse flies into the five broad groups was based on the blood meal analyses as reviewed by Weitz [25]. Host expansion over time was noted in all the tsetse groups but notable changes in group I, III and V were observed. Among group I, Glossina that feed mainly on Suidae, G. austeni's preference for suids seems to have expanded as recent studies identified the bushbuck as the preferred host [26]. This change could have been influenced by the availability of the vertebrate hosts. For group III, G. pallidipes, which mainly feed on Bovidae, other main hosts included bush pig, elephant and warthog [9]. Recent studies have identified other preferred hosts of G. pallidipes including hippopotamus, human, giraffe, warthog and buffalo [18, 26,27,28], suggesting that different tsetse fly species may not discriminate the hosts so long as they get a blood meal.

Among group V, tsetse flies that feed on human and commonly occurring hosts including bovids, suids, reptiles, canines, elephants and crocodiles, the feeding patterns in this group varied from place to place. For example, in Cameroon, G. palpalis fed more on pigs than on human in Bipindi region yet in Campo region they fed more on humans than on pigs, with sheep and antelopes being minor hosts [29]. Moreover, other studies reported new hosts in the same area including the duiker, monkey and sitatunga [13].

In light of advanced molecular techniques, the tsetse blood meal analysis categories might need to be revised, particularly in terms of genetics, to ensure appropriate classification. Some studies on molecular phylogenetics of tsetse flies, for instance for Palpalis group, reported that the morphology of the female genital plates was used in their grouping. However, some individuals of the fly species were later found to vary outside the ranges that were specified in the standard identification/taxonomic keys, making definitive morphological grouping impossible [30]. The minimum period between collection of tsetse fly samples and blood meal analysis ranged from 1 to 16 years. Tsetse fly host searching behaviour for the exclusive blood meal feeding may be altered as a result of their differential host dependence in response to ecological changes [12]. Thus, it is important to characterize the feeding behavioural host dependence as defined by the presence of different hosts’ blood meals in a single fly in order to detect any potential changes in the epidemiology of AAT. Some studies have confirmed the change in the feeding preference of tsetse flies on hosts [13, 29].

Serological Methods utilized in blood meal analysis

Serological techniques were the earliest methods to be used to unravel tsetse flies’ source of blood for their meals and survival. The serological techniques utilized for blood meal analysis in tsetse flies included precipitin test (PT), haemagglutination inhibition test (HIT), complement fixation test (CFT) and enzyme-linked immunosorbent assays (ELISA). The limitations of precipitin test method included inability to detect highly digested blood meal, and the small amounts of blood consumed by the flies led to a small amount of antigens available for testing [31]. HIT test was more sensitive than PT and thus was better at the identification of individual hosts [8]. The introduction of CFT in tsetse blood meal analysis improved the sensitivity and reliability of blood meal analysis but did not permit absorbance of antisera with cross-reacting antigens [7] and thus it may not be used to differentiate the closely related species. The introduction of ELISA further improved blood meal analysis because of its sensitivity and reliability. The advantages of the ELISA test in blood meal source analysis have been enumerated by Sakamoto and others [32], including the ability to identify mixed blood meals from different species. In addition, it has high specificity and sensitivity as well as high efficiency; it is a simple and eco-friendly procedure given that radioactive substances and large amounts of organic solvents are not required and it uses cheap reagents. However, some of the limitations identified included inability to detect all blood meal sources and decreased sensitivity of the test in highly digested blood meal or small quantities of it [33]. The requirement of specific antisera and cross-reactivity in related species [34] coupled with the need to have the antisera against all possible sources of blood meal in a given target area where tsetse flies are collected are also limiting factors [11, 35].

PCR-based molecular assays

The development of highly sensitive DNA barcoding techniques has helped molecular biologists to understand the parasite Trypanosoma, the tsetse fly species and their hosts [36]. The barcoding process uses short standardized genomic DNA fragments such as COI and Cyt b genes to distinguish among species [37]. The amplification of the mitochondrial proteins COI and Cyt b has proven useful in identifying blood meal sources in tsetse flies [11, 13, 38,39,40].

Cyt b gene is smaller in size than COI gene at 400 bp and 650 bp, respectively. Both Cyt b and COI genes are variable between different organisms but invariable within the same species. Comparatively, Cyt b and COI are similar in identifying intra-species variation but Cyt b is better in the analysis of smaller mammalian fragment samples such as trace or degraded samples [41]. The latter is useful in field-collected samples of hungry tsetse flies with minimal residual blood in the gut. Crushing the insect samples in liquid nitrogen improves the DNA yields [42]. However, other studies have reported that liquid nitrogen may damage to genomic DNA [43]. The COI gene has been less reliable for use in blood meal analysis [27]; hence, most studies use Cyt b gene.

Recently, other genes have been identified and used in the identification of the blood meal hosts. For instance, 12S rRNA gene has been shown to be more sensitive in identifying hosts from highly degraded blood meals [29, 44]. The 150-bp region of the 16S rRNA gene has also been used to identify hosts from highly degraded blood meals where Cyt b gene could not be amplified [45].

With the onset of the utilization of molecular approaches, different sequencing techniques have been used for elucidating the blood meal sources in tsetse flies’ gut including hybridization, Sanger and Illumina [11, 14, 44]. Over time, sequencing techniques have improved tremendously. The first method was heteroduplex hybridization, which uses an ordered array of oligonucleotides to identity a target sequence [46]. This method was successfully used, albeit underlying limitations including the exclusion of repetitive sequences [47]. Hybridization was later replaced by the first-generation Sanger sequencing technique invented by Frederick Sanger in 1977 [48]. Second-generation sequencing techniques, Illumina and Roche 254, have been used to sequence PCR-based amplicons from blood meals in tsetse flies fed from an array of hosts [44, 49, 50].

Tsetse flies prefer to go back to the original vertebrate host species for consecutive blood meals, although during starvation it may feed on any available host [51]. However, second-generation sequencing suggested that most tsetse flies had blood meals from multiple hosts. For example, Gaithuma and colleagues in two tsetse endemic foci, Kafue in Zambia and Hurungwe in Zimbabwe, confirmed the multiple feeding behaviour of these vectors, including feeding upon four different hosts [44, 49]. This raises the question: do tsetse fly species have preferred host(s)? Additionally, since most of the sequencing for determination of hosts has been based on the Sanger sequencing, does this mean it only detects the most abundant blood meal? Furthermore, it is also unclear whether the “dirty” sequences, which are not processed for blast analysis, represent blood from multiple hosts.

Currently, there are second-generation sequencing techniques including 454 pyrosequencing, Illumina and Ion Torrent. Oxford Nanopore and Single Molecule Real Time (SMRT) are considered third-generation sequencing technologies. All these techniques have enriched the accuracy of throughput depth of our scientific understanding at the molecular level as reviewed by different authors [47, 52]. The second- and third-generation sequencing techniques have their benefits and limitations that usually allow for technology advancement. For instance, SMRT can process sequences faster rate with longer reads than the second-generation sequencers, although they can have a high error rate of up to 20% as reviewed by Bleidorn [52]. However, there is a need to further explore the concept of blood meal analysis using the second- and third-generation sequencing techniques, albeit their availability in the African context.

With real-time PCR and PCR coupled with high-resolution melting analysis (PCR-HRM), it is now possible to screen many samples with minimal blood meals in them and reduce the cost of sequencing all the positive samples when appropriate controls are used. PCR-HRM can accurately identify blood meal sources from tsetse flies, including those which fed on multiple hosts [28], and could help overcome the challenge faced with Sanger sequencing, which may not give a clear chromatogram especially in cases of mixed blood meals.

Although speculative, most of the Sanger sequences that are not ‘clean’ enough for BLAST analysis may be feeds from multiple hosts. We hypothesise that the use of PCR-linked HRM and the use of smaller fragments including 12S and 16S rRNA genes could considerably improve blood meal analysis. This is because of PCR-linked HRM's sensitivity in identifying multiple hosts and reducing the cost of sequencing, especially in the African context of limited resources.

Limitation of the scoping reviews

Scoping reviews are important in addressing broad research questions and thus valuable in guiding whether a systematic review will be required. However, due to the breadth of the issue they cover, scoping review results are not conclusive and from the onset may swing towards an area of focus because of limitations in coverage and an absence of quality control unlike systematic studies [53]. This scoping review should therefore be interpreted in light of the above limitations.

Conclusions

The current review mapped out studies on the blood meal analysis in African countries published in English. It found that about half of the African countries endemic for tsetse flies and trypanosomiasis have carried out blood meal analysis. In addition, host-seeking preferences of about two-thirds of the tsetse fly species have been studied. The advent of technological advancement including PCR methods for library preparation and high-throughput sequencing technology in diagnostics has seen old fashioned techniques such as precipitin tests replaced by deterministic molecular diagnostic methods. We recommend that future studies on host preferences of tsetse fly species should deploy small fragment DNA, such as the mammalian 12S and 16S rRNA genes amplified using PCR-HRMA, qPCR or dPCR to enhance efficiency in library preparation and to reduce sequencing costs. Second- or third-generation sequencing approaches are more likely to give accurate results, especially when the vectors have fed on multiple hosts, which may be misidentified by Sanger sequencing as background noise.

Availability of data and materials

All data generated or analysed during this study are included in this published article [and its supplementary information files].

Abbreviations

AAT:

Animal African trypanosomiasis

AGRIS:

International System for Agricultural Science and Technology

BLAST:

Basic Local Alignment Search Tool

CFT:

Complement fixation test

COI:

Cytochrome oxidase I

Cyt b:

Cytochrome b

dPCR:

Digital polymerase chain reaction

ELISA:

Enzyme-linked immunosorbent assay

FAO:

Food and Agricultural Organization

HAT:

Human African trypanosomiasis

HIT:

Haemagglutination inhibition test

ICIPE:

International Centre of Insect Physiology and Ecology

ILRI:

International Livestock Research Institute

KALRO:

Kenya Agricultural and Livestock Research Organization

KENTTEC:

Kenya Tsetse and Trypanosomiasis Eradication Council

OSF:

Open Science Framework

PCR:

Polymerase chain reaction

PCR-HRMA:

Polymerase chain reaction-high-resolution melt analysis

PDF:

Portable Document Format

PT:

Precipitin test

qPCR:

Quantitative polymerase chain reaction

SMRT:

Single molecule real time

References

  1. Langousis G, Hill KL. Motility and more. Nat Rev Microbiol. 2014;12:505–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Mccue MD, Boardman L, Clusella-trullas S, Kleynhans E, Terblanche JS. The speed and metabolic cost of digesting a blood meal depends on temperature in a major disease vector. J Exp Biol. 2016;219:1893–902.

    PubMed  Google Scholar 

  3. Syed Z, Guerin PM. Tsetse flies are attracted to the invasive plant Lantana camara. J Insect Physiol. 2004;50:43–50.

    Article  CAS  PubMed  Google Scholar 

  4. Tempelis CH. Host-feeding patterns of mosquitoes, with a review of advances in analysis of blood. J Med Entomol. 1975;11:635–53.

    Article  CAS  PubMed  Google Scholar 

  5. Service MW, Voller A, Bidwell DE. The enzyme-linked immunosorbent assay (ELISA) test for the identification of blood-meals of haematophagous insects. Bull Entomol Res. 1986;76:321–30.

    Article  Google Scholar 

  6. Kent RJ. Molecular methods for arthropod bloodmeal identification and applications to ecological and vector-borne disease studies. Mol Ecol Resour. 2009;9:4–18.

    Article  CAS  PubMed  Google Scholar 

  7. Staak C, Allmang B, Kampe U, Mehlitz D. The complement fixation test for the species identification of blood meals from tsetse flies. Tropenmed Parasitol. 1981;32:97–8.

    CAS  PubMed  Google Scholar 

  8. Gates DB, Williamson DL. Tsetse fly feeding preference as determined by vehicular trapping in Tanzania. Ann Trop Med Parasitol. 1984;78:301–6.

    Article  CAS  PubMed  Google Scholar 

  9. Snow WWFW, Tarimo SSA, Staak C, Staak B. The feeding habits of the tsetse, “Glossina pallidipes” Austen on the south Kenya coast, in the context of its host range and trypanosome infection rates in other parts of East Africa. Acta Trop. 1988;45:339–49.

    CAS  PubMed  Google Scholar 

  10. Späth J. Feeding patterns of three sympatric tsetse species (Glossina spp.) (Diptera: Glossinidae) in the preforest zone of Cô te d’Ivoire. Acta Trop. 2000;75:109–118. https://doi.org/10.1016/S0001-706X(99)00096-0.

    Article  PubMed  Google Scholar 

  11. Muturi CN, Ouma JO, Malele II, Ngure RM, Rutto JJ, Mithöfer KM, et al. Tracking the feeding patterns of tsetse flies (Glossina genus) by analysis of bloodmeals using mitochondrial cytochromes genes. PLoS ONE. 2011;6:1–6.

    Article  Google Scholar 

  12. Clausen PH, Adeyemi I, Bauer B, Breloeer M, Salchow F, Staak C. Host preferences of tsetse (Diptera: Glossinidae) based on bloodmeal identifications. Med Vet Entomol England. 1998;12:169–80.

    Article  CAS  Google Scholar 

  13. Farikou O, Njiokou F, Simo G, Asonganyi T, Cuny G, Geiger A. Tsetse fly blood meal modification and trypanosome identification in two sleeping sickness foci in the forest of southern Cameroon. Acta Trop. 2010;116:81–8.

    Article  PubMed  Google Scholar 

  14. Simo G, Philemon DM, Kande BVKM, Manzambi EZ, Ollivier G, Asonganyi T, et al. Human African trypanosomiasis transmission, Kinshasa, Democratic Republic of Congo. Emerg Infect Dis. 2006;12:1968–70.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Tricco AC, Lillie E, Zarin W, O’Brien KK, Colquhoun H, Levac D, et al. PRISMA extension for scoping reviews (PRISMA-ScR): checklist and explanation. Ann Intern Med. 2018;169:467–73.

    Article  PubMed  Google Scholar 

  16. Rodrigues CMF, Garcia HA, Sheferaw D, Rodrigues AC, Pereira CL, Camargo EP, et al. Genetic diversity of trypanosomes pathogenic to livestock in tsetse flies from the Nech Sar National Park in Ethiopia: a concern for tsetse suppressed area in Southern Rift Valley? Infect Genet Evol. 2019;69:38–47.

    Article  PubMed  Google Scholar 

  17. Mekata H, Konnai S, Simuunza M, Chembensofu M, Kano R, Witola WH, et al. Prevalence and source of trypanosome infections in field-captured vector flies (Glossina pallidipes) in Southeastern Zambia. J Vet Med Sci. 2008;70:923–8.

    Article  CAS  PubMed  Google Scholar 

  18. Bett B, Irungu P, Nyamwaro SO, Murilla G, Kitala P, Gathuma J, et al. Estimation of tsetse challenge and its relationship with trypanosomosis incidence in cattle kept under pastoral production systems in Kenya. Vet Parasitol. 2008;155:287–98.

    Article  CAS  PubMed  Google Scholar 

  19. Snow W, Wacher T. Observations on the prevalence of trypanosomosis in small ruminants, equines and cattle, in relation to tsetse challenge, in The Gambia. Vet Parasitol Elsevier Vet Parasitol. 1996;66:1–11.

    Article  CAS  Google Scholar 

  20. Okeyo WA, Saarman NP, Bateta R, Dion K, Mengual M, Mireji PO, et al. Genetic differentiation of Glossina pallidipes tsetse flies in Southern Kenya. Am J Trop Med Hyg. 2018;99:945–53.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Shereni W, Neves L, Argilés R, Nyakupinda L, Cecchi G. An atlas of tsetse and animal African trypanosomiasis in Zimbabwe. Parasites Vectors BioMed Central. 2021;14:1–10.

    Google Scholar 

  22. Vreysen MJBB, Seck MT, Sall B, Bouyer J. Tsetse flies: their biology and control using area-wide integrated pest management approaches. J Invertebr Pathol Academic Press. 2013;112:S15-25.

    Article  Google Scholar 

  23. Lindh JM, Goswami P, Blackburn RS, Arnold SEJ, Vale GA, Lehane MJ, et al. Optimizing the colour and fabric of targets for the control of the tsetse fly Glossina fuscipes fuscipes. PLoS Negl Trop Dis. 2012;6(5):e1661. https://doi.org/10.1371/journal.pntd.0001661.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Weitz B, Glasgow JP. The natural hosts of some species of Glossina in East Africa. Trans R Soc Trop mediicine Hyg. 1956;50:593–612.

    Article  Google Scholar 

  25. Weitz B. The feeding habits of Glossina. Bull World Health Organ. 1963;28:711–29.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Ogolla KO, Onyango T, Bwana BK, Otiende MY, Mang’era CM, Ochieng B, et al. Bloodmeal host identities among sympatric Glossina austeni and Glossina pallidipes tsetse flies in Shimba Hills National Reserve, Kwale. Kenya Front Trop Dis. 2023;4:1–7.

    Google Scholar 

  27. Channumsin M, Mable BK, Ciosi M, Masiga D, Auty H, Turner CM, et al. Blood meal analysis of tsetse flies (Glossina pallidipes: Glossinidae) reveals higher host fidelity on wild compared with domestic hosts. Wellcome Open Res. 2021;6:213. https://doi.org/10.12688/wellcomeopenres.16978.1.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Makhulu EE, Villinger J, Adunga VO, Jeneby MM, Kimathi EM, Mararo E, et al. Tsetse blood-meal sources, endosymbionts and trypanosome-associations in the Maasai mara national reserve, a wildlife-human-livestock interface. PLoS Negl Trop Dis. 2021;15:1–18.

    Article  Google Scholar 

  29. Simo G, Njiokou F, Mbida Mbida JA, Njitchouang GR, Herder S, Asonganyi T, et al. Tsetse fly host preference from sleeping sickness foci in Cameroon: Epidemiological implications. Infect Genet Evol. 2008;8:34–9.

    Article  CAS  PubMed  Google Scholar 

  30. Dyer NA, Lawton SP, Ravel S, Choi KS, Lehane MJ, Robinson AS, et al. Molecular phylogenetics of tsetse flies (Diptera: Glossinidae) based on mitochondrial (COI, 16S, ND2) and nuclear ribosomal DNA sequences, with an emphasis on the palpalis group. Mol Phylogenet Evol. 2008;49:227–39.

    Article  CAS  PubMed  Google Scholar 

  31. Weitz B, Buxton PA. The rate of digestion of blood meals of various haematophagous arthropods as determined by the precipitin test. Bull Entomol Res. 1953;44:445–50.

    Article  Google Scholar 

  32. Sakamoto S, Putalun W, Vimolmangkang S, Phoolcharoen W. Enzyme - linked immunosorbent assay for the quantitative/qualitative analysis of plant secondary metabolites. J Nat Med Springer Japan. 2018;72:32–42.

    Article  CAS  Google Scholar 

  33. Wamwiri FN, Nkwengulila G, Clausen P. Hosts of Glossina fuscipes fuscipes and G. pallidipes in areas of Western Kenya with endemic sleeping sickness, as determined using an egg-yolk (IgY) ELISA. Ann Trop Med Parasitol. 2007;101:225–32.

  34. Waiswa C, Picozzi K, Katunguka-Rwakishaya E, Olaho-Mukani W, Musoke RA, Welburn SC. Glossina fuscipes fuscipes in the trypanosomiasis endemic areas of south eastern Uganda: Apparent density, trypanosome infection rates and host feeding preferences. Acta Trop. 2006;99:23–9.

    Article  CAS  PubMed  Google Scholar 

  35. Rurangirwa FR, Minja SH, Musoke AJ, Nantulya VM, Grootenhuis J, Moloo SK. Production and evaluation of specific antisera against sera of various vertebrate species for identification of bloodmeals of Glossina morsitans centralis. Acta Trop Netherlands. 1986;43:379–89.

    CAS  Google Scholar 

  36. Alcaide M, Rico C, Ruiz S, Soriguer R, Muñoz J, Figuerola J. Disentangling vector-borne transmission networks: A universal DNA barcoding method to identify vertebrate hosts from arthropod bloodmeals. PLoS One. 2009;4:1–6.

    Article  Google Scholar 

  37. Ferreira PB, Torres RA, Texeira RHF, Duarte JMB, Barbosa AC, Vargas RC, et al. Diagnostic Cytochrome b gene profiles for the identification of paca (Cuniculus paca) bushmeat: implications for the monitoring of illegal hunting and wildlife trade. Braz J Biol. 2016;76:55–8.

    Article  PubMed  Google Scholar 

  38. Hoppenheit A, Steuber S, Bauer B, Ouma EM, Diall O, Zessin KH, et al. Host preference of tsetse: an important tool to appraise the Nagana risk of cattle in the cotton zone of Mali. Wien Klin Wochenschr. 2010;122:81–6.

    Article  PubMed  Google Scholar 

  39. Hoppenheit A, Bauer B, Steuber S, Terhalle W, Diall O, Zessin KH, et al. Multiple host feeding in Glossina palpalis gambiensis and Glossina tachinoides in southeast Mali. Med Vet Entomol. 2013;27:222–5.

    Article  CAS  PubMed  Google Scholar 

  40. Odeniran POO, Macleod ETT, Ademola IOO, Welburn SCC. Molecular identification of bloodmeal sources and trypanosomes in Glossina spp., Tabanus spp. and Stomoxys spp. trapped on cattle farm settlements in southwest Nigeria. Med Vet Entomol. 2019;33:269–81.

    Article  CAS  PubMed  Google Scholar 

  41. Tobe SS, Kitchener A, Linacre A. Cytochrome b or cytochrome c oxidase subunit I for mammalian species identification-An answer to the debate. Forensic Sci Int Genet Suppl Ser. 2009;2:306–7.

    Article  Google Scholar 

  42. Hunt GJ. Insect DNA extraction protocol. Fingerprinting methods based arbitr primed PCR. 1997;21–4.

  43. Oppert B, Stoss S, Monk A, Smith T. Optimized extraction of insect genomic dna for long-read sequencing. Methods Protoc. 2019;2:1–7. https://doi.org/10.3390/mps2040089.

    Article  CAS  Google Scholar 

  44. Kim JY, Choi JH, Nam SH, Fyumagwa R, Yong TS. Parasites and blood-meal hosts of the tsetse fly in Tanzania: a metagenomics study. Parasites Vectors BioMed Central. 2022;15:1–7.

    Google Scholar 

  45. Bitome-Essono PY, Ollomo B, Arnathau C, Durand P, Mokoudoum ND, Yacka-Mouele L, et al. Tracking zoonotic pathogens using blood-sucking flies as ’flying syringes’. Elife. 2017;6:1–21.

    Article  Google Scholar 

  46. Chee M, Yang R, Hubbell E, Berno A, Huang XC, Stern D, et al. Accessing genetic information with high-density DNA arrays. Science. 1996;274:610–4.

    Article  ADS  CAS  PubMed  Google Scholar 

  47. Bentley DR. Whole-genome re-sequencing. Curr Opin Genet Dev. 2006;16:545–52.

    Article  CAS  PubMed  Google Scholar 

  48. Sanger F, Nicklen S, A.R C. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA. 1977;74:5463–7.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  49. Votýpka J, Rádrová J, Skalický T, Jirků M, Jirsová D, Mihalca AD, et al. A tsetse and tabanid fly survey of African great apes habitats reveals the presence of a novel trypanosome lineage but the absence of Trypanosoma brucei. Int J Parasitol. 2015;45:741–8.

    Article  Google Scholar 

  50. Gaithuma A, Yamagishi J, Hayashida K, Kawai N, Namangala B, Sugimoto C. Blood meal sources and bacterial microbiome diversity in wild-caught tsetse flies. Sci Rep. 2020;10:1–10.

    Article  Google Scholar 

  51. Bouyer J, Pruvot M, Bengaly Z, Guerin PM, Lancelot R, Bouyer J, et al. Learning influences host choice in tsetse. Biol Lett. 2007;3:113–6.

    Article  PubMed  Google Scholar 

  52. Bleidorn C. Third generation sequencing: Technology and its potential impact on evolutionary biodiversity research. Syst Biodivers Taylor & Francis. 2016;14:1–8.

    Article  Google Scholar 

  53. O’Brien KK, Colquhoun H, Levac D, Baxter L, Tricco AC, Straus S, et al. Advancing scoping study methodology: a web-based survey and consultation of perceptions on terminology, definition and methodological steps. BMC Health Serv Res. 2016;16:1–12.

    Article  Google Scholar 

  54. Njitchouang GR, Njiokou F, Nana-Djeunga H, Asonganyi T, Fewou-Moundipa P, Cuny G, et al. A new transmission risk index for human African trypanosomiasis and its application in the identification of sites of high transmission of sleeping sickness in the Fontem focus of southwest Cameroon. Med Vet Entomol. 2011;25:289–96.

    Article  CAS  PubMed  Google Scholar 

  55. Grébaut P, Melachio T, Nyangmang S, Eyenga VE, Njitchouang GR, Ofon E, et al. Xenomonitoring of sleeping sickness transmission in Campo (Cameroon). Parasites Vectors. 2016;9:1–9.

    Article  Google Scholar 

  56. Grébaut P, Mbida JAM, Kondjio CA, Njiokou F, Penchenier L, Laveissière C. Spatial and temporal patterns of human African Trypanosomosis (HAT) Transmission Risk in the Bipindi Focus, in the Forest Zone of Southern Cameroon. Vector-borne Zoonotic Dis. 2004;4(3):230–38. https://doi.org/10.1089/vbz.2004.4.230.

    Article  PubMed  Google Scholar 

  57. Gouteux P, Gboumbi K, Noutoua L, Amico FD, Bailly C, Roungou JB. Man-fly contact in the Gambian trypanosomiasis focus of Nola-Bilolo (Central African Republic). Trop Med Parasitol. 1993;44:213–8.

    CAS  PubMed  Google Scholar 

  58. Simo G, Silatsa B, a, Flobert N, Lutumba P, Mansinsa PD, Madinga JN, et al. Identification of different trypanosome species in the mid-guts of tsetse flies of the Malanga (Kimpese) sleeping sickness focus of the Democratic Republic of Congo. Parasit Vectors. 2012;5:201.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Grébaut P, Bena JM, Manzambi EZ, Mansinsa P, Khande V, Ollivier G, et al. Characterization of sleeping sickness transmission sites in rural and periurban areas of Kinshasa (Réublique Démocratique du Congo). Vector-Borne Zoonotic Dis. 2009;9:631–6.

    Article  PubMed  Google Scholar 

  60. Negash M, Girma M, Seyoum E, Negash M, Girma M, Seyoum E. Epizootiological importance of Glossina morsitans submorsitans (Diptera: Glossinidae) (Newstead) in the Ghibe River Valley Southwest Ethiopia. Acta Trop. 2007;102:100–5.

    Article  Google Scholar 

  61. Kohagne T, M’eyi M, Mimpfoundi R, Louis J. Entomological patterns in the human African trypanosomiasis focus of Komo Mondah. Gabon Afr Health Sci. 2010;10:341–8.

    CAS  PubMed  Google Scholar 

  62. Bitome-Essono P-Y, Ollomo B, line Arnathau C, Durand P, Diamella Mokoudoum N, Yacka-Mouele L, et al. Tracking zoonotic pathogens using blood-sucking flies as “flying syringes.” Elife. 2017;6:e22069. https://doi.org/10.7554/eLife.22069.001

  63. Snow W, Boreham PF. The feeding habits and ecology of the tsetse fly “Glossina morsitans submorsitans” Newstead in relation to nagana transmission in the Gambia. Acta Trop. 1979;36:47–51.

    CAS  PubMed  Google Scholar 

  64. Sasaki H, Kang’Ethe EK, Kaburia HF. Blood meal sources of Glossina pallidipes and G longipennis (Diptera: Glossinidae) in Nguruman Southwest Kenya. J Med Entomol. 1995;32:390–3.

    Article  CAS  PubMed  Google Scholar 

  65. Mihok S, Maramba O, Munyoki E, Kagoiya J. Mechanical transmission of Trypanosoma spp. by African Stomoxyinae (Diptera: Muscidae). Trop Med Parasitol. 1995;46:103–5.

    CAS  PubMed  Google Scholar 

  66. Snow W, Tarimo S, Staak B. The feeding habits of the tsetse, “Glossina pallidipes” Austen on the south Kenya coast, in the context of its host range and trypanosome infection rates in other parts of East Africa. Acta Trop. 1988;45:339–49.

    CAS  PubMed  Google Scholar 

  67. Turner DA. The population ecology of Glossina pallidipes Austen (Diptera: Glossinidae) in the Lambwe Valley, Kenya. I. Feeding behaviour and activity patterns. Bull Entomol Res. 1987;77:317–33.

    Article  Google Scholar 

  68. Snow W, Tarimo S. A quantification of the risk of trypanosomiasis infection to cattle on the south Kenya coast. Acta Trop. 1983;40:331–40.

    CAS  PubMed  Google Scholar 

  69. England EC, Baldry DAT. The hosts and trypanosome infection rates of Glossina pallidipes in the Lambwe and Roo valleys. Bull World Health Organ. 1972;47:785–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Allsopp R, Baldry DA, Rodrigues C. The influence of game animals on the distribution and feeding habits of Glossina pallidipes in the Lambwe Valley. Bull World Health Organ. 1972;47:795–809.

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Rodrigues CMF, Garcia HA, Rodrigues AC, Pereira DL, Pereira CL, Viola LB, et al. Expanding our knowledge on African trypanosomes of the subgenus Pycnomonas: a novel Trypanosoma suis-like in tsetse flies, livestock and wild ruminants sympatric with Trypanosoma suis in Mozambique. Infect Genet Evol. 2020;78:104143. https://doi.org/10.1016/j.meegid.2019.104143.

    Article  PubMed  Google Scholar 

  72. Karshima SN, Lawal IA, Okubanjo OO. Feeding patterns and xenomonitoring of trypanosomes among tsetse flies around the Gashaka-Gumti National Park in Nigeria. J Parasitol Res. 2016; 2016:1591037. https://doi.org/10.1155/2016/1591037.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Auty H, Cleaveland S, Malele I, Masoy J, Lembo T, Bessell P, et al. Quantifying heterogeneity in host-vector contact: Tsetse (Glossina swynnertoni and G. pallidipes) host choice in Serengeti National Park, Tanzania. PLoS One. 2016;11:1–19.

    Google Scholar 

  74. Moloo SK, Kutuza SB, Boreham PFL. Studies on Glossina pallidipes, G. fuscipes fuscipes and G. brevipalpis in terms of the epidemiology and epizootiology of trypanosomiases in south-eastern Uganda. Ann Trop Med Parasitol. 1980;74:219–37.

    Article  CAS  PubMed  Google Scholar 

  75. Opiro R, Opoke R, Angwech H, Nakafu E, Oloya FA, Openy G, et al. Apparent density, trypanosome infection rates and host preference of tsetse flies in the sleeping sickness endemic focus of northwestern Uganda. BMC Vet Res. 2021;17(1):365. https://doi.org/10.1186/s12917-021-03071-w.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Konnai S, Mekata H, Odbileg R, Simuunza M, Chembensof M, Witola WH, et al. Detection of Trypanosoma brucei in field-captured tsetse flies and identification of host species fed on by the infected flies. Vector-Borne Zoonotic Dis. 2008;8:565–73.

    Article  PubMed  Google Scholar 

  77. Newberry K, Boreham PFL, Sheppard M. A preliminary investigation of the effect of age, sex and time of collection on the feeding patterns of Glossina morsitans morsitans Westw. in Zambia. Trans R Soc Trop Med Hyg. 1982;76:79–82.

    Article  CAS  PubMed  Google Scholar 

  78. Okiwelu SN. Host preference and trypanosome infection rates of Glossina morsitans morsitans westwood in the Republic of Zambia. Ann Trop Med Parasitol. 1977;71:101–7.

    Article  CAS  PubMed  Google Scholar 

  79. Boyt WP, MacKenzie PKI, Pilson RD. The relative attractiveness of donkeys, cattle, sheep and goats to Glossina morsitans morsitans Westwood and G. pallidipes Austen (Eiptera: Glossinidae) in a middle-veld area of Rhodesia. Bull Entomol Res. 1978;68:497–500.

    Article  Google Scholar 

  80. Vale GA, Hargrove JW, Jordan AM, Langley PA, Mews AR. Survival and behaviour of tsetse flies (Diptera, Glossinidae) released in the field: a comparison between wild flies and animal-fed and in vitro-fed labora-tory-reared flies. Bull ent Res. 1976;66(4):731-44. https://doi.org/10.1017/S0007485300010786.

    Article  Google Scholar 

  81. Weitz B, Glasgow JP. Transactions of the royal society of South Africa. Trans R Soc South Africa. 1956;50:593–612.

    Google Scholar 

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Acknowledgements

We thank Dr. Simon Kariuki, Mr. Michael Maua and Mr. David Nyaga for the support in the acquisition of the articles and data cleaning.

Funding

This work was partly supported by the Science for Africa (SAF) Foundation through a DELTAS Africa Initiative grant awarded to JLB [DEL-15011] by the Wellcome Trust 107742/Z/15/Z and the UK Foreign, Commonwealth & Development Office. This work was also funded by the Pwani University Research Fund (PURF) awarded to EKS, grant number PURF/02/2017.

The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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Authors and Affiliations

  1. Department of Anatomy and Physiology, School of Health and Human Sciences, Pwani University, P.O. Box 195-80108, Kilifi, Kenya

    Erick Kibichiy Serem

  2. Pwani University Bioscience Research Centre (PUBReC), Pwani University, P.O. Box 195-80108, Kilifi, Kenya

    Erick Kibichiy Serem, David Mwangi Mburu & Osman Abdikarim Abdullahi

  3. Department of Biological Sciences, School of Pure and Applied Sciences, Pwani University, P.O. Box 195-80108, Kilifi, Kenya

    David Mwangi Mburu

  4. Department of Public Health, School of Health and Human Sciences, Pwani University, P.O. Box 195-80108, Kilifi, Kenya

    Osman Abdikarim Abdullahi

  5. Department of Biochemistry, Jomo Kenyatta University of Agriculture and Technology (JKUAT), P.O. Box 62000-00200, Nairobi, Kenya

    Joel Ltilitan Bargul

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EKS: Conceptualization, Formal Analysis, Funding Acquisition, Investigation, Methodology, Project Administration, Validation, Visualization, Writing—Original Draft Preparation, Writing—Review & Editing. JLB: Conceptualization, Formal Analysis, Funding Acquisition, Investigation, Methodology, Resources, Supervision, Validation, Visualization, Writing—Original Draft Preparation, Writing—Review & Editing. OAA: Conceptualization, Formal Analysis, Funding Acquisition, Investigation, Methodology, Project Administration, Resources, Supervision, Validation, Visualization, Writing—Original Draft Preparation, Writing—Review & Editing. DMM: Conceptualization, Formal Analysis, Funding Acquisition, Investigation, Methodology, Project Administration, Resources, Supervision, Validation, Visualization, Writing—Original Draft Preparation, Writing—Review & Editing.

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Serem, E.K., Mburu, D.M., Abdullahi, O.A. et al. A scoping review on tsetse fly blood meal sources and its assay methods since 1956 to 2022. Parasites Vectors 17, 52 (2024). https://doi.org/10.1186/s13071-023-06114-3

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Parasites & Vectors

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