scholarly journals Tsetse blood-meal sources, endosymbionts, and trypanosome infections provide insight into African trypanosomiasis transmission in the Maasai Mara National Reserve, a wildlife-human-livestock interface

Author(s):  
Edward Edmond Makhulu ◽  
Jandouwe Villinger ◽  
Vincent Owino Adunga ◽  
Maamun M. Jeneby ◽  
Edwin Murungi Kimathi ◽  
...  

AbstractBackgroundAfrican trypanosomiasis (AT) is a neglected disease of both humans and animals caused by Trypanosoma parasites, which are transmitted by obligate hematophagous tsetse flies (Glossina spp.). Understanding of AT transmission is hampered by limited knowledge on interactions of tsetse flies with their vertebrate hosts and the influence of endosymbionts on vector competence, especially in wildlife-human-livestock interfaces. We identified the tsetse species, their blood-meal sources, and the correlation between endosymbiont and trypanosome infection status in the trypanosome-endemic Maasai Mara National Reserve (MMNR) of Kenya.Methodology/Principal FindingsAmong 1167 tsetse flies (1136 Glossina pallidipes, 31 Glossina swynnertoni) collected from 10 sampling sites, 28 (2.4%) were positive by PCR for trypanosomes, majority (17/28) being Trypanosoma vivax. Blood-meal analyses based on high-resolution melting analysis of mitochondrial cytochrome c oxidase 1 and cytochrome b gene PCR products (n = 345) identified humans as the most common vertebrate host (37%), followed by hippopotamus (29.1%), African buffalo (26.3%), elephant (3.39%), and giraffe (0.84%). Trypanosome-infected flies had fed on hippopotamus and buffalo. Additionally, PCR analysis revealed that tsetse flies were more likely to be infected with trypanosomes if they were infected with the Sodalis glossinidius endosymbiont (P = 0.0022 Fisher’s exact test).Conclusions/SignificanceDiverse species of wildlife hosts may contribute to the maintenance of tsetse populations and/or persistent circulation of African trypanosomes in the MMNR. Although the African buffalo is known to be a key reservoir of AT, the higher proportion of hippopotamus blood-meals in trypanosomes-infected flies identified here indicates that other wildlife species may also be important to transmission cycles. No trypanosomes associated with human disease were identified, but the high proportion of human blood-meals identified are indicative of human African trypanosomiasis transmission risk. Furthermore, this work provides data showing that Sodalis endosymbionts can is associated with increased trypanosome infection rates in endemic ecologies.Author summaryHuman and animal African trypanosomiasis are neglected tropical diseases with potential to spread to new areas. Wild animals are important reservoirs for African trypanosomes and crucial in the emergence and re-emergence of AT. Vertebrate host-vector-parasite interactions are integral to trypanosome transmission. We investigated the vertebrate blood-meals and trypanosomes-endosymbionts co-infections in tsetse flies, which have been associated with reservoirs and vector competence, respectively, on AT transmission in Kenya’s Maasai Mara National Reserve. We identified tsetse fly diversity, trypanosome and endosymbiont infection status, and vertebrate blood-meal hosts to infer potential transmission dynamics. We found that Glossina pallidipes was the major tsetse fly vector and that Trypanosoma vivax was the main trypanosome species circulating in the region. Humans, hippopotamus, and buffalo were the most frequented for blood-meals. Buffalo and hippopotamus blood-meals were identified in trypanosome infected flies. Feeding of the flies on both humans and wildlife may potentiate the risk of the human trypanosomiasis in this ecology. Additionally, we found that the endosymbiont Sodalis glossinidius is associated with higher trypanosome infection rates in wild tsetse flies. These findings emphasize the importance of understanding the interaction of tsetse flies with vertebrate blood-meal sources and their endosymbionts in the transmission and control of AT.

2021 ◽  
Vol 15 (1) ◽  
pp. e0008267
Author(s):  
Edward Edmond Makhulu ◽  
Jandouwe Villinger ◽  
Vincent Owino Adunga ◽  
Maamun M. Jeneby ◽  
Edwin Murungi Kimathi ◽  
...  

African trypanosomiasis (AT) is a neglected disease of both humans and animals caused by Trypanosoma parasites, which are transmitted by obligate hematophagous tsetse flies (Glossina spp.). Knowledge on tsetse fly vertebrate hosts and the influence of tsetse endosymbionts on trypanosome presence, especially in wildlife-human-livestock interfaces, is limited. We identified tsetse species, their blood-meal sources, and correlations between endosymbionts and trypanosome presence in tsetse flies from the trypanosome-endemic Maasai Mara National Reserve (MMNR) in Kenya. Among 1167 tsetse flies (1136 Glossina pallidipes, 31 Glossina swynnertoni) collected from 10 sampling sites, 28 (2.4%) were positive by PCR for trypanosome DNA, most (17/28) being of Trypanosoma vivax species. Blood-meal analyses based on high-resolution melting analysis of vertebrate cytochrome c oxidase 1 and cytochrome b gene PCR products (n = 354) identified humans as the most common vertebrate host (37%), followed by hippopotamus (29.1%), African buffalo (26.3%), elephant (3.39%), and giraffe (0.84%). Flies positive for trypanosome DNA had fed on hippopotamus and buffalo. Tsetse flies were more likely to be positive for trypanosomes if they had the Sodalis glossinidius endosymbiont (P = 0.0002). These findings point to complex interactions of tsetse flies with trypanosomes, endosymbionts, and diverse vertebrate hosts in wildlife ecosystems such as in the MMNR, which should be considered in control programs. These interactions may contribute to the maintenance of tsetse populations and/or persistent circulation of African trypanosomes. Although the African buffalo is a key reservoir of AT, the higher proportion of hippopotamus blood-meals in flies with trypanosome DNA indicates that other wildlife species may be important in AT transmission. No trypanosomes associated with human disease were identified, but the high proportion of human blood-meals identified are indicative of human African trypanosomiasis risk. Our results add to existing data suggesting that Sodalis endosymbionts are associated with increased trypanosome presence in tsetse flies.


2020 ◽  
Author(s):  
Robert Opiro ◽  
Robert Opoke ◽  
Harriet Angwech ◽  
Esther Nakafu ◽  
Francis A. Oloya ◽  
...  

Abstract Background: African trypanosomiasis, caused by protozoa of the genus Trypanosoma and transmitted by the tsetse fly, is a serious parasitic disease of humans and animals. Reliable data on the vector distribution, feeding preference and the trypanosome species they carry is pertinent to planning sustainable control strategies.Methodology: We deployed 109 biconical traps in 10 villages in two districts of northwestern Uganda to obtain information on the apparent density, trypanosome infection rates and blood meal sources of tsetse flies. A subset (272) of the collected samples was analyzed for detection of trypanosomes species and sub-species using a nested PCR protocol based on primers amplifying the Internal Transcribed Spacer (ITS) region of ribosomal DNA. 34 blood-engorged adult tsetse midguts were analyzed for blood meal sources by sequencing of the mitochondrial cytochrome c oxidase 1 (COI) and cytochrome b (cytb) genes. Results: Out of the 109 traps deployed, we captured 622 Glossina fuscipes fuscipes tsetse flies (269 males and 353 females). Apparent density (AD) ranged from 0.6 to 3.7 flies/trap/day in the two districts. 29 (10.7%) of the flies were infected with one or more trypanosome species. Infection rate was not significantly associated with neither age group (χ2 = 5.001, df=2, 0.082), sex of the fly (χ2 = 0.099, df = 1, p = 0.753), district of origin (χ2= 0.629, df = 1, p = 0.428) nor village (χ2= 9.252, df = 9, p = 0.414). Nested PCR revealed several species of trypanosomes: T. vivax (6.62%), T. congolense (2.57%), T. brucei and T. simiae each at 0.73%. Blood meal analyses revealed five principal vertebrate hosts, namely, cattle (Bos taurus), humans (Homo sapiens), Nile monitor lizard (Varanus niloticus), African mud turtle (Pelusio schapini) and the African Savanna elephant (Loxodonta africana).Conclusion: We found an infection rate of 10.78 %, with all infections attributed to trypanosome species that are causative agents for the animal disease only. However, more verification of this finding using large-scale passive and active screening of human and tsetse samples should be done. Cattle and humans appear to be the most important tsetse hosts in the region and should be considered in the design of interventions.


2021 ◽  
Vol 17 (1) ◽  
Author(s):  
Robert Opiro ◽  
Robert Opoke ◽  
Harriet Angwech ◽  
Esther Nakafu ◽  
Francis A. Oloya ◽  
...  

Abstract Background African trypanosomiasis, caused by protozoa of the genus Trypanosoma and transmitted by the tsetse fly, is a serious parasitic disease of humans and animals. Reliable data on the vector distribution, feeding preference and the trypanosome species they carry is pertinent to planning sustainable control strategies. Methodology We deployed 109 biconical traps in 10 villages in two districts of northwestern Uganda to obtain information on the apparent density, trypanosome infection status and blood meal sources of tsetse flies. A subset (272) of the collected samples was analyzed for detection of trypanosomes species and sub-species using a nested PCR protocol based on primers amplifying the Internal Transcribed Spacer (ITS) region of ribosomal DNA. 34 blood-engorged adult tsetse midguts were analyzed for blood meal sources by sequencing of the mitochondrial cytochrome c oxidase 1 (COI) and cytochrome b (cytb) genes. Results We captured a total of 622 Glossina fuscipes fuscipes tsetse flies (269 males and 353 females) in the two districts with apparent density (AD) ranging from 0.6 to 3.7 flies/trap/day (FTD). 10.7% (29/272) of the flies were infected with one or more trypanosome species. Infection rate was not significantly associated with district of origin (Generalized linear model (GLM), χ2 = 0.018, P = 0.895, df = 1, n = 272) and sex of the fly (χ2 = 1.723, P = 0.189, df = 1, n = 272). However, trypanosome infection was highly significantly associated with the fly’s age based on wing fray category (χ2 = 22.374, P < 0.001, df = 1, n = 272), being higher among the very old than the young tsetse. Nested PCR revealed several species of trypanosomes: T. vivax (6.62%), T. congolense (2.57%), T. brucei and T. simiae each at 0.73%. Blood meal analyses revealed five principal vertebrate hosts, namely, cattle (Bos taurus), humans (Homo sapiens), Nile monitor lizard (Varanus niloticus), African mud turtle (Pelusios chapini) and the African Savanna elephant (Loxodonta africana). Conclusion We found an infection rate of 10.8% in the tsetse sampled, with all infections attributed to trypanosome species that are causative agents for AAT. However, more verification of this finding using large-scale passive and active screening of human and tsetse samples should be done. Cattle and humans appear to be the most important tsetse hosts in the region and should be considered in the design of control interventions.


2020 ◽  
Author(s):  
Robert Opiro ◽  
Robert Opoke ◽  
Harriet Angwech ◽  
Esther Nakafu ◽  
Francis A. Oloya ◽  
...  

Abstract Background: African trypanosomiasis, caused by protozoa of the genus Trypanosoma and transmitted by the tsetse fly, is a serious parasitic disease of humans and animals. Reliable data on the vector distribution, feeding preference and the trypanosome species they carry is pertinent to planning sustainable control strategies.Methodology: We deployed 109 biconical traps in 10 villages in two districts of northwestern Uganda to obtain information on the apparent density, trypanosome infection rates and blood meal sources of tsetse flies. A subset of the collected samples was analyzed for detection of trypanosomes species and sub-species using a nested PCR protocol based on primers amplifying the Internal Transcribed Spacer (ITS) region of ribosomal DNA. 34 blood-engorged adult tsetse midguts were analyzed for blood meal sources by sequencing of the mitochondrial cytochrome c oxidase 1 (COI) and cytochrome b (cytb) genes. Results: Out of the 109 traps deployed, we captured 622 Glossina fuscipes fuscipes tsetse flies (269 males and 353 females). Apparent density (AD) ranged from 0.6 to 3.7 flies/trap/day in the two districts. 29 (10.7%) of the flies were infected with one or more trypanosome species, with infection rate significantly associated with age group (χ2 = 29.733, df = 2, p < 0.05) but not with sex (χ2 = 0.43, df = 1, p = 0.835) and district of origin (χ2 = 1.374, df = 1, p = 0.241). Nested PCR revealed several species of trypanosomes: T. vivax (62.1%), T. congolense (24.14 %), and T. brucei and T. simiae each at 6.89%. Blood meal analyses revealed five principal vertebrate hosts, namely, cattle (Bos taurus), humans (Homo sapiens), Nile monitor lizard (Varanus niloticus), African mud turtle (Pelusio schapini) and the African Savanna elephant (Loxodonta africana).Conclusion: We found a moderately high infection rate at 10.78%, with all infections attributed to trypanosome species that are causative agents for the animal disease only. However, more validation using large-scale passive and active screening of human and tsetse samples should be done. Cattle and humans appear to be the most important tsetse hosts in the region and should be considered in the design of interventions.


2020 ◽  
Author(s):  
Robert Opiro ◽  
Robert Opoke ◽  
Harriet Angwech ◽  
Esther Nakafu ◽  
Francis A. Oloya ◽  
...  

Abstract Background: African trypanosomiasis, caused by protozoa of the genus Trypanosoma and transmitted by the tsetse fly, is a serious parasitic disease of humans and animals. Reliable data on the vector distribution, feeding preference and the trypanosome species they carry is pertinent to planning sustainable control strategies.Methodology: We deployed 109 biconical traps in 10 villages in two districts of northwestern Uganda to obtain information on the apparent density, trypanosome infection rates and blood meal sources of tsetse flies. A subset (272) of the collected samples was analyzed for detection of trypanosomes species and sub-species using a nested PCR protocol based on primers amplifying the Internal Transcribed Spacer (ITS) region of ribosomal DNA. 34 blood-engorged adult tsetse midguts were analyzed for blood meal sources by sequencing of the mitochondrial cytochrome c oxidase 1 (COI) and cytochrome b (cytb) genes. Results: Out of the 109 traps deployed, we captured 622 Glossina fuscipes fuscipes tsetse flies (269 males and 353 females). Apparent density (AD) ranged from 0.6 to 3.7 flies/trap/day in the two districts. 29 (10.7%) of the flies were infected with one or more trypanosome species. Infection rate was not significantly associated with age group (χ2 = 5.001, df=2, p = 0.082), sex of the fly (χ2 = 0.099, df = 1, p = 0.753), district of origin (χ2= 0.629, df = 1, p = 0.428) and village of origin (χ2= 9.252, df = 9, p = 0.414). Nested PCR revealed several species of trypanosomes: T. vivax (6.62%), T. congolense (2.57%), T. brucei and T. simiae each at 0.73%. Blood meal analyses revealed five principal vertebrate hosts, namely, cattle (Bos taurus), humans (Homo sapiens), Nile monitor lizard (Varanus niloticus), African mud turtle (Pelusio schapini) and the African Savanna elephant (Loxodonta africana).Conclusion: We found an infection rate of 10.78 %, with all infections attributed to trypanosome species that are causative agents for the animal disease only. However, more verification of this finding using large-scale passive and active screening of human and tsetse samples should be done. Cattle and humans appear to be the most important tsetse hosts in the region and should be considered in the design of interventions.


mBio ◽  
2022 ◽  
Author(s):  
Caroline E. Dewar ◽  
Aitor Casas-Sanchez ◽  
Constentin Dieme ◽  
Aline Crouzols ◽  
Lee R. Haines ◽  
...  

African trypanosomes cause disease in humans and their livestock and are transmitted by tsetse flies. The insect ingests these parasites with its blood meal, but to be transmitted to another mammal, the trypanosome must undergo complex development within the tsetse fly and migrate from the insect's gut to its salivary glands.


2021 ◽  
Vol 6 ◽  
pp. 213
Author(s):  
Manun Channumsin ◽  
Marc Ciosi ◽  
Dan Masiga ◽  
Harriet Auty ◽  
C. Michael Turner ◽  
...  

Background: Changes in climate and land use can alter risk of transmission of parasites between domestic hosts and wildlife, particularly when mediated by vectors that can travel between populations. Here we focused on tsetse flies (genus Glossina), the cyclical vectors for both Human African Trypanosomiasis (HAT) and Animal African Trypanosomiasis (AAT). The aims of this study were to investigate three issues related to G. palldipes from Kenya: 1) the diversity of vertebrate hosts that flies fed on; 2) whether host feeding patterns varied in relation to type of hosts, tsetse feeding behaviour, site or tsetse age and sex; and 3) if there was a relationship between trypanosome detection and host feeding behaviours or host types. Methods: Sources of blood meals of Glossina pallidipes were identified by sequencing of the mitochondrial cytochrome b gene and analyzed in relationship with previously determined trypanosome detection in the same flies. Results: In an area dominated by wildlife but with seasonal presence of livestock (Nguruman), 98% of tsetse fed on single wild host species, whereas in an area including a mixture of resident domesticated animals, humans and wildlife (Shimba Hills), 52% of flies fed on more than one host species. Multiple Correspondence Analysis revealed strong correlations between feeding pattern, host type and site but these were resolved along a different dimension than trypanosome status, sex and age of the flies. Conclusions: Our results suggest that individual G. pallidipes in interface areas may show higher feeding success on wild hosts when available but often feed on both wild and domesticated hosts. This illustrates the importance of G. pallidipes as a vector connecting the sylvatic and domestic cycles of African trypanosomes.


BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Miguel Medina Munoz ◽  
Caitlyn Brenner ◽  
Dylan Richmond ◽  
Noah Spencer ◽  
Rita V. M. Rio

Abstract Background Tsetse flies are the obligate vectors of African trypanosomes, which cause Human and Animal African Trypanosomiasis. Teneral flies (newly eclosed adults) are especially susceptible to parasite establishment and development, yet our understanding of why remains fragmentary. The tsetse gut microbiome is dominated by two Gammaproteobacteria, an essential and ancient mutualist Wigglesworthia glossinidia and a commensal Sodalis glossinidius. Here, we characterize and compare the metatranscriptome of teneral Glossina morsitans to that of G. brevipalpis and describe unique immunological, physiological, and metabolic landscapes that may impact vector competence differences between these two species. Results An active expression profile was observed for Wigglesworthia immediately following host adult metamorphosis. Specifically, ‘translation, ribosomal structure and biogenesis’ followed by ‘coenzyme transport and metabolism’ were the most enriched clusters of orthologous genes (COGs), highlighting the importance of nutrient transport and metabolism even following host species diversification. Despite the significantly smaller Wigglesworthia genome more differentially expressed genes (DEGs) were identified between interspecific isolates (n = 326, ~ 55% of protein coding genes) than between the corresponding Sodalis isolates (n = 235, ~ 5% of protein coding genes) likely reflecting distinctions in host co-evolution and adaptation. DEGs between Sodalis isolates included genes involved in chitin degradation that may contribute towards trypanosome susceptibility by compromising the immunological protection provided by the peritrophic matrix. Lastly, G. brevipalpis tenerals demonstrate a more immunologically robust background with significant upregulation of IMD and melanization pathways. Conclusions These transcriptomic differences may collectively contribute to vector competence differences between tsetse species and offers translational relevance towards the design of novel vector control strategies.


2018 ◽  
Author(s):  
Brian L. Weiss ◽  
Michele A. Maltz ◽  
Aurélien Vigneron ◽  
Yineng Wu ◽  
Katharine Walter ◽  
...  

AbstractTsetse flies (Glossina spp.) vector pathogenic trypanosomes (Trypanosoma spp.) in sub-Saharan Africa. These parasites cause human and animal African trypanosomiases, which are debilitating diseases that inflict an enormous socio-economic burden on inhabitants of endemic regions. Current disease control strategies rely primarily on treating infected animals and reducing tsetse population densities. However, relevant programs are costly, labor intensive and difficult to sustain. As such, novel strategies aimed at reducing tsetse vector competence require development. Herein we investigated whether an Enterobacter bacterium (Esp_Z), which confers Anopheles gambiae with resistance to Plasmodium, is able to colonize tsetse and induce a trypanosome refractory phenotype in the fly. Esp_Z established stable infections in tsetse’s gut, and exhibited no adverse effect on the survival of individuals from either group. Flies with established Esp_Z infections in their gut were significantly more refractory to infection with two distinct trypanosome species (T. congolense, 6% infection; T. brucei, 32% infection) than were age-matched flies that did not house the exogenous bacterium (T. congolense, 36% infected; T. brucei, 70% infected). Additionally, 52% of Esp_Z colonized tsetse survived infection with entomopathogenic Serratia marcescens, compared with only 9% of their wild-type counterparts. These parasite and pathogen refractory phenotypes result from the fact that Esp_Z acidifies tsetse’s midgut environment, which inhibits trypanosome and Serratia growth and thus infection establishment. Finally, we determined that Esp_Z infection does not impact the fecundity of male or female tsetse, nor the ability of male flies to compete with their wild-type counterparts for mates. We propose that Esp_Z could be used as one component of an integrated strategy aimed at reducing the ability of tsetse to transmit pathogenic trypanosomes.Author SummaryTsetse flies transmit pathogenic African trypanosomes, which are the causative agents of socio-economically devastating human and animal African trypanosomiases. These diseases are currently controlled in large part by reducing the population size of tsetse vectors through the use of insecticides, traps and sterile insect technique. However, logistic and monetary hurdles often preclude the prolonged application of procedures necessary to maintain these control programs. Thus, novel strategies, including those aimed at sustainably reducing the ability of tsetse to transmit trypanosomes, are presently under development. Herein we stably colonize tsetse flies with a bacterium (Enterobacter sp. Z, Esp_Z) that acidifies their midgut, thus rendering the environment inhospitable to infection with two distinct, epidemiologically important trypanosome strains as well as an entomopathogenic bacteria. In addition to inducing a trypanosome refractory phenotype, colonization of tsetse with Esp_Z exerts only a modest fitness cost on the fly. Taken together, these findings suggest that Esp_Z could be applied to enhance the effectiveness of currently employed tsetse control programs.


Author(s):  
Imna I. Malele ◽  
Johnson O. Ouma ◽  
Hamisi S. Nyingilili ◽  
Winston A. Kitwika ◽  
Deusdedit J. Malulu ◽  
...  

This study was conducted to determine the efficiency of different tsetse traps in 28 sites across Tanzania. The traps used were biconical, H, NGU, NZI, pyramidal, S3, mobile, and sticky panels. Stationary traps were deployed at a distance of 200 m apart and examined 72 h after deployment. The results showed that 117 (52.2%) out of the 224 traps deployed captured at least one Glossina species. A total of five Glossina species were captured, namely Glossina brevipalpis, Glossina pallidipes, Glossina swynnertoni, Glossina morsitans, and Glossina fuscipes martinii. Biconical traps caught tsetse flies in 27 sites, pyramidal in 26, sticky panel in 20, mobile in 19, S3 in 15, NGU in 7, H in 2 and NZI in 1. A total of 21 107 tsetse flies were trapped, with the most abundant species being G. swynnertoni (55.9%), followed by G. pallidipes (31.1%), G. fuscipes martinii (6.9%) and G. morsitans (6.0%). The least caught was G. brevipalpis (0.2%). The highest number of flies were caught by NGU traps (32.5%), followed by sticky panel (16%), mobile (15.4%), pyramidal (13.0%), biconical (11.3%) and S3 (10.2%). NZI traps managed to catch 0.9% of the total flies and H traps 0.7%. From this study, it can be concluded that the most efficient trap was NGU, followed by sticky panel and mobile, in that order. Therefore, for tsetse fly control programmes, NGU traps could be the better choice. Conversely, of the stationary traps, pyramidal and biconical traps captured tsetse flies in the majority of sites, covering all three ecosystems better than any other traps; therefore, they would be suitable for scouting for tsetse infestation in any given area, thus sparing the costs of making traps for each specific Glossina species.Keywords: tseste; traps; densties; Glossina; mobile; stationary; Tanzania


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