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Faculty of Medicine, Kilimanjaro Christian Medical University College, Moshi, TanzaniaNational Institute for Medical Research, Amani Research Centre, Muheza, Tanzania
Risk factors associated with dengue and chikungunya in North-Eastern Tanzania has not been investigated.
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Understanding risk factors of infection is vital for targeting control interventions.
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Environmental are associated with chikungunya IgM seropositivity.
Abstract
Background
Dengue and chikungunya are mosquito-borne viral diseases of major global health concern. In Tanzania, information on risk factors for dengue and chikungunya is limited. We investigated individual, household, socio-economic, demographic and environmental risk factors for dengue and chikungunya seropositivity.
Methods
A cross sectional study was undertaken which included a total of 1003 participants from North-Eastern Tanzania, to determine the sero-prevalence of dengue and chikungunya and to investigate associated risk factors. Logistic regression models were used to determine the risk factors for dengue and chikungunya seropositivity.
Results
Environmental factors such as living in a house with uncovered containers within the compound had higher odds of being chikungunya IgM seropositive (OR = 2.89; 95% CI: 1.76–4.76). Also, participants who kept hoofed animals in their home and who lived in a house surrounded by vegetation (<100 m) had higher odds of chikungunya IgM seropositivity ({OR = 1.67; 95% CI: 1.11–2.51} and {OR = 181; 1.10–3.00} respectively). Due to few dengue seropositive, dengue was excluded in the bi-and multivariate analysis. However, dengue IgM seropositivity was associated with G6PD status (p = 0.03) while there was no apparent association between genetic factors (G6PD, HbB or alpha-thalassemia) and chikungunya seropositivity.
Conclusion
Public health education on environmental management practices is needed to eliminate the identified risks such as simple removal of uncovered containers that may serve as breeding sites for mosquitoes, avoiding animal husbandry in the peri-domestic environment and clearing of vegetation surrounding houses. More studies are needed to investigate the association of dengue and G6PD deficiency.
Dengue and chikungunya are mosquito-borne viral diseases considered global public health threats due to their wide geographic spread and potential for acute onset of large-scale epidemics with attack rates as high 90% and 85%, respectively [
]. Several epidemics have been documented in urban and semi urban areas throughout the tropical and sub-tropical areas of the world including the on-going pandemic of chikungunya which started in Kenya in 2004 [
]. Risk factors for dengue and chikungunya infections are typically categorized into individual factors, household factors, environmental factors and viral genetic factors [
Emergence of chikungunya seropositivity in healthy Malaysian adults residing in outbreak-free locations: chikungunya seroprevalence results from the Malaysian Cohort.
]; including age, sex and level of education. The age distribution of individuals infected with dengue may vary in different epidemiological and geographical settings, as in some settings dengue is seen exclusively as a childhood disease [
]. Hence, human genetic factors such as hemoglobinopathies and G6PD deficiency could be important individual risk factors for dengue virus infection and perhaps that of other arboviruses including chikungunya. Infection with any of the four-dengue virus serotypes may elicit cross reactive but non-neutralizing immune responses capable of enhancing subsequent heterotypic dengue infection, with an increased risk of severe disease. As such, host immune status can be a risk factor for infection as well as increased pathogenicity [
], living in rented housing, living near uncovered sewers, and living near open sewers and untreated water discharging directly into nearby ponds/lakes have been associated with dengue [
Emergence of chikungunya seropositivity in healthy Malaysian adults residing in outbreak-free locations: chikungunya seroprevalence results from the Malaysian Cohort.
] have also been associated with increased risk of chikungunya virus infection. Notably, some of these risk factors (such as area of residence and housing quality) may vary between different geographical settings, even between neighboring areas in urban settings [
Environmental factors, including the presence of anthropogenic breeding sites for the primary vector Aedes (Ae) aegypti within the perimeters of residential areas have been associated with dengue seropositivity [
Evidence of dengue virus transmission and factors associated with the presence of anti-dengue virus antibodies in humans in three major towns in Cameroon.
Individual genotypes and strains of each dengue serotype may present different virulence levels in terms of infectivity of host and/or vector as shown in vitro and in epidemiological studies [
] and has been implicated as a risk factor of increased transmission of chikungunya virus when introduced into areas already infested by Ae. albopictus [
]. There has been a significant research interest in dengue in Asia, the Pacific and the Americas for the past several decades and in chikungunya since the onset of the on-going pandemic 12 years ago; nevertheless the general epidemiology and risk factors for the two diseases remain poorly understood in the African context. Recent declines in malaria transmission as observed throughout most of Sub Saharan Africa have, however, placed an increased focus on non-malarial fevers, including arboviral diseases such as dengue and chikungunya. The occurrence of large-scale dengue epidemics in Cape Verde (2009), Senegal (2009) [
] underscores the urgency of informed decisions and priority setting in terms of arboviral control in the Sub Saharan Africa.
A small number of sero-prevalence studies have provided limited information on the transmission and risk factors of dengue and chikungunya in East African countries [
Seroprevalence of Anti-Dengue Virus 2 Serocomplex antibodies in out-patients with fever visiting selected hospitals in rural parts of western Kenya in 2010–2011: a cross sectional study.
Understanding risk factors of dengue and chikungunya infection is important for targeting control interventions. In North-Eastern Tanzania; information on risk factors for dengue and chikungunya is not available, therefore this study aimed at identifying individual, household, environmental and socio-economic risk factors associated with dengue and chikungunya seropositivity in three different areas of North-Eastern Tanzania.
Methods
Study design and setting
Community-based cross sectional studies were conducted in May, 2013, November 2013 and May 2014 at Bondo, Hai and Lower Moshi respectively as described in Ref. [
Prevalence of Dengue and Chikungunya virus infections in north-eastern Tanzania: a cross sectional study among participants presenting with malaria-like symptoms.
]. Bondo village is located in Handeni District (population size: 276,646) in Tanga Region, Hai town is located in Hai District (population size: 210,533) and Lower Moshi is located in Moshi Rural District (population size: 466,737) both in Kilimanjaro Region [
] (Fig. 1). Bondo is lowland rural area is covered by bush land, palm gardens and sisal plantations. The area normally has two annual rainy seasons; the ‘long rains’ (March–June) and the ‘short rains’ (October–November) with an annual rainfall of more than 1000 mm [
]. Hai District is an inland rural area, classified as tropical savannah, although the climate varies considerably due to the influence of Mount Kilimanjaro. On average, the district receives 700 mm of rainfall in the lowlands, 1250 mm in the mid zone and 1750 mm in the upper zone [
] during the long rains (March–June) and the short rains (November–December). Moshi Rural District is located inland in a lowland rural area characterized by several water streams across the area that form irrigation channels for rice cultivation and sugarcane plantations. Moshi Rural District has two rainy seasons; the long rains (March–May) and the short rains (November–December) with an average annual rainfall of 900 mm.
Figure 1Tanzanian map showing the study area in North-Eastern Tanzania (shown in green). Areas shown in violet color are the selected districts (study sites) in Kilimanjaro and Tanga regions, (Created using Arc-GIS). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Prevalence of Dengue and Chikungunya virus infections in north-eastern Tanzania: a cross sectional study among participants presenting with malaria-like symptoms.
]. Briefly; community sensitization was done through community leaders prior to initiation. Community members were encouraged to visit their local health facility for enrollment. Participants aged 2–70 years were included in the study. The health facilities included Bondo Dispensary, Hai Hospital and TPC hospital in Lower Moshi. On presentation each person was screened for malaria (using RDTs) and malaria positive cases were treated according to National treatment guidelines.
Clinical information was recorded for each participant during the health facility visit using a structured questionnaire, while a blood sample (0.5 ml) was taken for screening of IgM/IgG anti-dengue and anti-chikungunya antibodies. Two drops of blood were spotted onto filter paper (Whatman 3MM) and air dried at room temperature overnight before storage in sealed bags with desiccant at 4 °C. Dried blood spots were further used for human genotyping of G6PD, HbB or alpha-thalassemia. Each participant was subsequently interviewed on potential risk predictors during a household visit, while direct observations were completed for the household and the peri-domestic environment. In the case of participants being less than 12 years, a parent or guardian was interviewed on their behalf.
Predictor variables assessed for individual risk of seropositivity included sex, age and level of education. Household predictors included information on the presence and structure of windows, bed net use (by participant), and number of persons per household room. Environmental predictors included uncovered containers/car tires and other water receptacles, as well as animals (cattle, goat or sheep) kept in the peri-domestic environment or in the immediate neighborhood. Vegetation (trees, grasses etc.) within 100 m of the household and proximity to water bodies (e.g. rivers, streams or wells) were also included as possible environmental predictors.
Number of assets in household was included as predictors for socio-economic status, whereas education, age and travel history were used as demographic predictors.
Notably, the “Eleven household asset index” was used as a proxy for socio-economic status as described by Sissoko et al. (2008) and TDHS, (2010). The index was constructed on the basis of availability of electricity (1 point), television set (1 point), radio (1 point), motorcycle (1 point), bicycle (1 point), mobile phone (1 point), possession of land (1 point), toilet facility in the house (no facility = 0 point, pit latrine with no cement = 1 point, pit with cement slab = 2 points, flush to septic sewer = 3 points), source of water (private 1 point) material used for house construction (mud blocks = 1 point, cement blocks = 2 points) material used for house roofing (grass = 0 point, corrugated metal = 1 points). The study sample was divided into three grades, namely low, medium and high socio-economic status based on the sum of items for each household, and the distribution of the household asset index score across the total study sample using the Principal Component Analysis [
Participant sera were tested for the presence of anti-dengue and anti-chikungunya antibodies using commercial enzyme-linked immunosorbent assays (ELISA), as described and presented previously [
Prevalence of Dengue and Chikungunya virus infections in north-eastern Tanzania: a cross sectional study among participants presenting with malaria-like symptoms.
]. Briefly; Anti-Dengue (both IgM & IgG) were analyzed using SD Capture-Elisa (SD Inc, Gyeonggi-do, Korea) and anti-Chikungunya IgM were analyzed using SD indirect sandwich Elisa (SD Inc, Gyeonggi-do, Korea), while anti-Chikungunya IgG were analyzed using chikungunya IgM capture Elisa (IBL international, Hamburg, Germany). All assays were performed according to the manufacturers' instructions.
All patient samples were screened for G6PD deficiency and hemoglobin A and S were detected using a high throughput combined PCR-ELISA assay followed by a sequence-specific oligonucleotide probe ELISA (SSOP- ELISA) [
Rapid screening for glucose-6-phosphate dehydrogenase deficiency and haemoglobin polymorphisms in Africa by a simple high-throughput SSOP-ELISA method.
]. Dengue seropositive case was defined as either IgM or IgG positive.
Statistical analysis
The association between categorical predictors and the presence of IgM and/or IgG seropositivity was presented as odds ratios (OR) with 95% confidence intervals (95% CIs) using logistic regression. Predictors significantly associated with seropositivity in the bivariate analysis (set to p ≤ 0.1) were selected for multivariate analyses in order to test for statistically significant (p < 0.05) associations in a final model. The multivariate analysis did not include dengue due to low numbers of seropositives. The Chi-square test (χ2) or Fisher exact test were used to compare categorical data such as proportions of IgM and/or IgG seropositivity and genetic factors (Wild type vs. Heterozygote and Homozygote). All data were analyzed using SPSS 20.0 software (SPSS Inc., Chicago, IL, USA).
Ethics approval and consent to participate
Ethical approval for the study was obtained from the Kilimanjaro Christian Medical University College Research Ethics Review Committee (Certificate No. 658). For inclusion in the study, a written informed consent as to participate in the study was obtained from participants aged ≥18 years or parents/guardians of those under 18 years. If the legal guardian was illiterate, signed consent was sought from another literate witness chosen by the guardian. Confidentiality was maintained throughout the study.
Results
A total of 1003 participants were recruited from Hai hospital (n = 240), TPC hospital (n = 261) and Bondo dispensary (n = 502). The detailed seroprevalence among febrile and afebrile participants has been reported previously [
Prevalence of Dengue and Chikungunya virus infections in north-eastern Tanzania: a cross sectional study among participants presenting with malaria-like symptoms.
], in brief, the overall prevalence of dengue IgM and IgG seropositives was 1.0% (10/1003), respectively while the prevalence of chikungunya IgM and IgG was 13.5% (135/1003) and 4.9% (49/1003), respectively (Fig. 2). Few participants presented both seropositive of IgM and IgG simultaneously. Only 2.2% (3/135) presented both IgM and IgG for chikungunya virus and 10% (1/10) presented both IgM and IgG for dengue virus. All individuals positive for dengue IgM and/or dengue IgG were categorized together as dengue seropositive. Only 20 dengue seropositive cases were detected thus dengue was excluded in the bi- and multivariate analysis.
Figure 2Seroprevalence of IgG and IgM against chikungunya virus and dengue virus, respectively. IgM: Immunoglobulin M, IgG: Immunoglobulin G, DENV: Dengue virus, CHIKV: Chikungunya virus.
Out of 1003 samples, 985 (98.2%), 995 (99.2%) and 993 (99.0%) were successfully genotyped for G6PD deficiency, sickle cell and alpha-thalassemia, respectively.
Out of 985 tested for G6PD deficiency, in the dengue seropositives (n = 19), 63.2% (12/19) were G6PD wild type, 21.1% (4/19) were heterozygotes and 15.8% (3/19) were homozygotes. In the dengue sero-negative group (n = 966) the G6PD wild types were 76.4% (738/966) while the heterozygotes and homozygotes were lower in frequency, at 19.3% (186/966) and 4.3% (42/966), respectively (Fischer's Exact test = 4.96, p = 0.06 for comparison of wild type versus heterozygote + homozygotes between dengue seropositives and sero-negatives). Out of 995 tested for sickle cell, in the dengue seropositives, 78.9% (15/19) were wild type, 21.1% (4/19) were heterozygotes and none were homozygotes while for the dengue sero-negatives, the prevalence was 85.7% (836/976), 14.2% (139/976) and 0.1% (1/976), respectively (Fischer's Exact test = 3.14, p = 0.35). Out of 993 tested for alpha thalassemia, in the dengue seropositives, 73.7% (14/19) were wild type, 26.3% (5/19) were heterozygotes and none were homozygotes while in the sero-negative group, the prevalence were 52.6% (512/974), 31.1% (303/974) and 16.3% (159/974), respectively (Fischer's Exact test = 4.95, p = 0.07).
For G6PD deficiency, among the Chikungunya IgM seropositives 79.3% (107/135) were G6PD wild type, 17.0% (23/135) were heterozygotes and 3.7% (5/135) were homozygotes. Among the chikungunya IgM sero-negative group the G6PD wild types were 75.6% (643/850), 19.6% (167/850) were heterozygotes and 4.7% (40/850) were homozygotes (χ2 test = 0.68, p = 0.72). Chikungunya IgM seropositive among participants tested for Sickle cell, wild types were 82.2% (111/135), and heterozygous were 17.8% (24/135) while none 0 (0) were homozygous. Among chikungunya IgM sero-negatives, 86.0% (740/860) were wild types, 13.8% (119/860) were heterozygous and 0.1% (1/860) were homozygous (Fischer's Exact test = 2.13, p = 0.33).
While for alpha-thalassemia, in the chikungunya IgM seropositives 51.9% (70/135) were wild type, 31.9% (43/135) were heterozygotes and 16.3% (22/135) were homozygotes. In the chikungunya IgM sero-negative group, 53.1% (456/858) were wild type, 30.9% (265/858) were heterozygotes and 16.0% (137/858) were homozygotes (χ2 test = 0.11, p = 0.95). For G6PD deficiency, in the Chikungunya IgG seropositives 75.7% (37/49) were G6PD wild type, 20.4% (10/49) were heterozygotes and 4.1% (2/49) were homozygotes. In the chikungunya IgG sero-negative, the G6PD wild types were 76.2% (713/936), heterozygotes were 19.2% (180/936) and homozygotes were 4.6% (43/936) (Fischer's Exact test = 0.10, p = 0.95). Chikungunya IgG seropositive among participants tested for Sickle cell, wild types were 79.6% (39/49), heterozygous were 20.4% (10/49) while none were homozygous while among the IgG sero-negatives, the prevalence were 85.8% (812/946), 14.1% (133/946) and 0.1% (1/946), respectively (Fischer's Exact test = 2.98, p = 0.25). Lastly for alpha-thalassemia, in the chikungunya IgG seropositive group, 40.8% (20/49) were wild type, 36.7% (18/49) were heterozygotes and 22.4% (11/49) were homozygotes while in the chikungunya IgG sero-negative group the prevalence were 53.6% (506/944), 30.7% (290/944) and 15.7% (148/944), respectively (χ2 test = 3.31, p = 0.19) (Table 1).
Table 1Individual risk factors (genetics factors) with dengue and chikungunya. Results of Chi-square and Fisher's Exact test analysis.
Bi and multivariate analysis of the association between individual, household, environmental and socio-economic/demographic risk factors and chikungunya IgM and IgG seropositivity
The results of the bi- and multivariate analyses of the association between selected predictors and chikungunya IgM seropositivity are shown in Table 2. Only variables that presented a significant association with seropositivity in the bivariate analysis (set to p ≤ 0.1) are presented below with respect to the multivariate analysis.
Table 2The associations between selected predictors and chikungunya IgM and IgG seropositivity. Results of bivariate and multivariate analysis (n = 1003).
Based on the household asset index [21,70]. Only variables that were predictors of chikungunya IgM and IgG seropositivity (set in the bivariate analysis to P ≤ 0.1) were included in multivariate analysis.
. Only variables that were predictors of chikungunya IgM and IgG seropositivity (set in the bivariate analysis to P ≤ 0.1) were included in multivariate analysis.
c Adjusted for level of education, window screening, number of persons per room, uncovered containers, animal keeping and vegetation.
Participants with uncovered container/car tires around their houses had higher odds of being chikungunya IgM seropositive as compared to those without (OR = 2.89; 95% CI: 1.76–4.76). Also, participants who kept animals (mainly cattle, sheep or goat) in their home had higher odds of chikungunya IgM seropositivity as compared to those who did not (OR = 1.67; 95% CI: 1.11–2.51). Likewise; participants who lived in a house surrounded by vegetation (within 100 m) had higher odds of chikungunya IgM seropositivity as compared to participants who lived in a household with no surrounding vegetation (OR = 1.81; 95% CI: 1.10–3.00).
Finally, inhabitants who resided in Lower Moshi (TPC) had lower odds of being chikungunya IgM seropositive as compared to Bondo and Hai (OR = 0.47, 95% CI = 0.23–0.94), Table 2.
The results of the bi- and multivariate analysis of the association between selected predictors and chikungunya IgG seropositivity are also shown in Table 2. In the bivariate analyses only age, bed net use, SES and site of study qualified for further multivariate analysis (set to p ≤ 0.1). However, in multivariate analysis none of the predictors displayed a statistically significant association with IgG seropositivity.
Discussion
The objective of the present study was to determine risk factors associated with dengue and chikungunya seropositivity in North-Eastern Tanzania. Due to the low number of dengue seropositive cases this study mainly reports on risk factors for chikungunya seropositivity, as a follow-up to previous studies confirming chikungunya seropositivity in the region [
Prevalence of Dengue and Chikungunya virus infections in north-eastern Tanzania: a cross sectional study among participants presenting with malaria-like symptoms.
]. Chikungunya IgM are detectable 2–3 days after the onset of symptoms and persist up to three months while chikungunya specific IgG appear soon after IgM antibodies (2–3 days) and persist for several years [
We found an association between higher dengue seropositivity and G6PD deficiency (p = 0.03). This finding supports in vitro studies showing that monocytes obtained from G6PD-deficient patients display higher dengue virus infection rates than those of normal controls [
]. Since this finding is limited with few numbers of dengue seropositive cases, there is need for further investigations into the association between G6PD and dengue risk and the underlying mechanisms. We did not find any association between sickle cell and alpha-thalassemia traits with dengue seropositivity. However; according to two cases reported elsewhere [
] sickle cell trait are associated with more severe manifestations, whereas in vitro studies suggest that thalassemia trait carriers have reduced susceptibility to dengue virus infection [
]. Furthermore, there was no association between chikungunya seropositivity and any of the genetic factors we studied. To the best of our knowledge no previous studies have examined potential associations of chikungunya infection with genetic factors, as such more detailed investigations are needed.
Environmental risk factors
Dengue and chikungunya viruses are transmitted by common mosquito vectors of the genus Aedes (Ae.), particularly Ae. aegypti and Ae. albopictus [
Risk factors for the presence of chikungunya and dengue vectors (Aedes aegypti and Aedes albopictus), their altitudinal distribution and climatic determinants of their abundance in Central Nepal.
]. In our study area, both vectors were present but Ae. aegypti was recognized as the most dominant species (data not shown).
We observed a significant association between the presence of uncovered containers/used car tires in the surrounding area of the households and chikungunya IgM seropositivity. Artificial/uncovered water receptacles including used car tires are widely recognized breeding sites for Ae. aegypti mosquitoes [
Evidence of dengue virus transmission and factors associated with the presence of anti-dengue virus antibodies in humans in three major towns in Cameroon.
] as simple vector control strategies for the control of Chikungunya.
We observed an association between chikungunya IgM seropositivity and animal keeping; those with animals had higher odds of being seropositive. Animal keeping increases the density and survival of mosquito vectors by providing alternative and/or additional blood-sources and breeding sites [
]. Ae. aegypti is highly anthropophilic; the high positivity rates among individuals with animals in their home surrounding is therefore most probably due to increased availability of breeding sites resulting from animals hoof prints. On the other hand, although to a lesser degree, several authors have reported Aedes mosquitos being attracted to and feeding on other non-human hosts [
]. Additionally, Ae. formosus, a sub-species of Ae. aegypti that is less anthropophilic and therefore capable of feeding on non-human hosts exists in forests and vegetated African fields [
] and Kaaya et al. reported presence of this species in Moshi (unpublished data). This is to say, in addition to providing breeding sites through hoof prints, animal keeping in this study may have placed humans at an increased risk by attracting mosquitoes, which, when close to human houses, ended biting humans and not animals. Our findings suggest for further studies to explore the impact of peridomestic animals in arboviral transmission as this could help in the planning of future integrated prevention and control programs.
In this study, participants with vegetation within 100 m from their house had higher odds of chikungunya IgM seropositivity. In a recent study conducted in Dar Es salaam, Tanzania, it was shown that a high vegetation cover provided shade for the oviposition and development of the aquatic stages of mosquitoes including Ae. aegypti [
]. Furthermore, the most common breeding sites reported for Ae. aegypti in Tanzania are discarded plastic containers, unused car tires and vegetation, the latter including tree holes, leaf axils, flower bracts, fallen leaves [
Our findings highlight the need to consider establishing and maintaining an Aedes mosquito surveillance and control program in the study area or Tanzania as a whole. Notably, vector control remains the most effective of available measures for integrated control of several arboviruses as well as malaria. For the study area in particular, the elimination of Aedes breeding sites and removal of livestock from the peri-domestic environment [
This study has some limitations. We did not determine yellow fever vaccine status to exclude cross reactivity with dengue virus. However, dengue prevalence was low, therefore it is unlikely that the observed dengue sero-prevalence is due to cross reactivity. The sensitivity and specificity of standard diagnostic Elisa test range was reported to be 84% and 91% in a convalescent phase [
]. Therefore we may have underestimated the true chikungunya seropositivity in this study.
We conducted a one time sampling as a community cross sectional study, therefore we did not collect a second sample to correctly estimate the persistence of IgM in participants as this was not the scope of the present study. Chikungunya IgM antibodies are detectable 5 or more days after onset of illness/symptoms in and may persist for 2 or 3–6 months [
]. In another study it was observed that the persistent IgM may be due to response to viral persistence as chikungunya RNA has been detected in joint tissue in humans [
]. Therefore, further studies are needed to study the persistence of chikungunya IgM in the body. We did not observe any severe case of dengue or chikungunya, therefore the reported association of seropositivity and host factors should be interpreted with cautions.
Conclusion
We conclude that environmental factors such as living in a house with uncovered containers, keeping hoofed animals and vegetation (<100 m) were associated with chikungunya IgM seropositivity in North-Eastern Tanzania. Public health education on (i) environmental management practices is needed to eliminate the identified risks through simple removal of uncovered containers that may serve as breeding sites for mosquitoes, avoiding animal husbandry in the peri-domestic environment and clearing of vegetation surrounding houses, (ii) the presence of chikungunya in the North-Eastern Tanzania. Finally, more studies are required as to the potential association between dengue, chikungunya and other relevant arboviruses and human genetic determinants.
Authorship statement
DCK conceived the idea, designed the study, participated in data collection, and performed the experiments, data analysis and interpretation. MM participated in data collection and performed the experiments. KLS participated in drafting and critical review of the manuscript. DWM contributed to the drafting of the manuscript, data interpretation, and critical review of the manuscript. FT performed data analysis, interpretation and participated in critical review of the manuscript. MA designed the study and participated in critical review of the manuscript. FWM contributed to the drafting and critical review of the manuscript. RAK designed the study and critical review of the manuscript.
Conflicts of interest
None to declare.
Funding
Funding for this work was received through the project Danida Fellowship Centre in the Building strong Universities (BSU). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Provenance and peer review
Not commissioned; externally peer reviewed.
Acknowledgments
We acknowledge the district medical officers of Handeni, Hai and Moshi rural for giving us permission to conduct this research. The authors wish to thank the doctors in-charge, nurses and laboratory staff of Bondo Dispensary, Hai and TPC Hospitals for their help in the data collection. We thank Miss Polyxeni Syrianou from Technological Educational Institute of Athens, Aigaleo, Greece, for performing laboratory test. The authors wish to thank BSU for financial support. We candidly acknowledge the community members for participating in this study.
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