All pools that were positive for D. immitis DNA were those of mosquito species known to be competent heartworm vectors [20], so we assume that any positive mosquito pool represents potential transmission. 2017;6:e22053. Data-driven identification of potential Zika virus vectors. The first test compared heartworm prevalence between suburban, natural woodlot and natural field sites with all neighborhood ages collapsed into a single suburban category (three total treatment levels). We also sampled at 6 additional smaller parcels of land composed of undeveloped woodlots and 5 additional smaller parcels of land composed of undeveloped fields. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. Gainsville: University Press of Florida; 2005. salinarius, Ae. Cookies policy. All authors participated in editing and review of the manuscript. Ledesma N, Harrington L. Mosquito vectors of dog heartworm in the United States: vector status and factors influencing transmission efficiency. There did not appear to be any seasonal trends in D. immitis infection within mosquitoes, although we could have missed important dynamics in the spring due to our trapping season beginning in June. Article  Zip codes where mosquitoes were not sampled are denoted NA. Studies on the vector competence of Ae. MRSB and MHR conceptualized the study and its methodology. Modified DNA extraction protocols used with both the DNeasy Blood and Tissue Kit (Qiagen, Venlo, Netherlands) and the ZR Genomic DNA-Tissue MiniPrep (Zymo Research, Irvine, CA, USA). As expected, people of higher socioeconomic status reported greater use of preventative medications, resulting in lower levels of vector-borne pathogens, including D. immitis [22]. Species-level heartworm prevalence by land-use type. Spatial association between malaria vector species richness and malaria in Colombia. The remaining 57% perceived the prevalence … Finally, we performed generalized linear model selection to find the model that best explained within-host heartworm prevalence using all combinations of the following independent variables at the zip code level: presence or absence of heartworm-positive mosquito pools, proportion heartworm-positive mosquito pools, rarefied richness, evenness, Shannon–Wiener diversity, mosquito abundance and median household income. columbiae appears to be a significant contributor to heartworm transmission in suburban Wake County, as it was the only species in the current study to have > 1% D. immitis-positive pools in suburban neighborhoods. An ideal system for further examining the effects of mosquito diversity on vector-borne disease transmission is that of the dog heartworm, Dirofilaria immitis. de Valdez MRW. We approached this question by sampling mosquitoes across Wake County, North Carolina, USA, analyzing the mosquitoes for the presence of D. immitis DNA, and comparing heartworm prevalence rates within the mosquito to heartworm prevalence rates within domestic dogs. Because of their inability to be infectious for D. immitis, we excluded males and nulliparous females from further analysis. The nematode D. immitis is an obligate parasite of mosquitoes and canids. Becker B, Leisnham P, LaDeau SL. Development of Dirofilaria immitis and Dirofilaria repens in Aedes japonicus and Aedes geniculatus. As the percentage of mosquitoes in the area that have previously laid eggs (and therefore previously taken a blood meal) increases, D. immitis presence in mosquitoes also increases, reaffirming that older mosquitoes are the most dangerous from a disease transmission standpoint due to their greater probability of prior pathogen exposure. c While the relationship between within-host heartworm prevalence and mosquito rarefied richness was not significant (F(1, 16)= 4.342, P = 0.054, R2= 0.213), a similar positive trend was found. & Reiskind, M.H. J Med Entomol. Relative suitability of Aedes albopictus and Aedes aegypti in North Carolina to support development of Dirofilaria immitis. As with the Kruskal–Wallis test, we again performed this test for land-use type both with and without neighborhood age categories as levels within the broader suburban category. One possible explanation for this discrepancy is that vector competence within a single mosquito species is susceptible to selection and can vary among geographically distinct populations [20, 41]. 2019;14:e0215485. Within the landscape of North Carolina, this equates to less heartworm disease expected within the host in suburban areas as a function of urbanization-induced mosquito diversity losses. Based on the results of a prior study of heartworm prevalence on an urban to rural gradient [21], we hypothesize that older neighborhoods with less diverse mosquito assemblages dominated by Ae. albopictus. We created categories of neighborhood ages to ensure that neighborhoods of various ages were being sampled: developed before 1993, between 1993–2002, between 2003–2007, between 2008–2012 and from 2013 to present. According to the American Heartworm Society, … To minimize the risk of sample contamination, qPCR was performed at a dedicated workstation that was separate from that utilized for DNA extraction. Any opinions, findings and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation. We cannot assess spatial trends for D. immitis within mosquitoes due to low overall prevalence (Fig. Within-host heartworm prevalence was well modeled by mosquito diversity and household income, further underscoring the effect of mosquito diversity while also illustrating the importance of socioeconomic status, possibly due to differences in administration of preventative medications. Despite high rates of urbanization and ample examples of vector-borne diseases transmitted by multiple species, the effects of urbanization-driven mosquito diversity losses on disease transmission has not been well explored. volume 13, Article number: 12 (2020) Springer Nature. However, when analyzing the 2015 data, percent heartworm-positive mosquito pools was positively correlated with percent parous mosquitoes across the trapping season (Fig. © 2021 BioMed Central Ltd unless otherwise stated. CAS  Prevalence of Heartworm Disease in Ontario According to a study conducted between 2007 and 2016 2 looking at blood samples from dogs, there were 762 positive test results for heartworm in Ontario, with 722 of these occurring in Southern Ontario. McGill E, Berke O, Peregrine AS, Weese JS. Terms and Conditions, With so many known heartworm vectors spanning across multiple genera, the apparent lack of seasonality coupled with a positive correlation with parity could be due to vector mosquitoes having different phenologies, making heartworm transmission potential a nearly constant risk throughout the warmer months in North Carolina. Convergent habitat segregation of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in southeastern Brazil and Florida. Michael H. Reiskind. Visualization of heartworm prevalence by zip code in Wake County, North Carolina. Mosquitoes show habitat fidelity at a much finer scale of less than 100 m [28], leading to a separation of geographical scale between mosquito-level factors and host-level factors that could be obscuring some trends. Together, they indicate that heartworm disease can be found in every populous area. Disease ecology; Diversity; Heartworm; Landscape; Mosquito; Urbanization; Vector. DGE-1746939. The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic précis. Annu Rev Entomol. PubMed  We homogenized the mosquitoes using sterilized pestles in sterilized microcentrifuge tubes and followed modified versions of the standard kit protocols for DNA extraction (full extraction protocols are presented in Additional file 1: Text S1). b Heartworm prevalence within mosquitoes ranged from 0% to 3.09% by zip code. Urbanization is one context in which vector assemblage and diversity vary, potentially with implications for heartworm disease transmission. 2013;7:e2507. In the context of dog heartworm disease, the losses in mosquito diversity seen with suburban development are associated with decreased D. immitis prevalence in both the vectors and the host. Interestingly, our previous work in Wake County did not find any effect of socioeconomic status on mosquito diversity measures [10], so the effect of socioeconomic status detected in the present study is likely due to its impact on host-level factors. Google Scholar. The forecast’s construction and an assessment of its performance are described. Mosquitoes used for analysis in this study were previously sampled and the effects of suburban development on mosquito diversity were previously assessed in Spence Beaulieu et al. ESDA Canine Heartworm … If the local population is indeed refractory to D. immitis infection, that could drive the observed decreased heartworm prevalence in suburban areas, as over 40% of our trapped mosquitoes were Ae. No relationships were noted between within-mosquito and within-host heartworm prevalence. Brown HE, Harrington LC, Kaufman PE, McKay T, Bowman DD, Nelson CT, et al. Parasites & Vectors If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. 2014 Aug;28 Suppl 1:60-7. doi: 10.1111/mve.12069. Google Scholar. PubMed  Background: Mosquitoes are a diverse family of flies that can be pests and vectors of medical and veterinary significance, transmitting a wide array of viruses, protozoans and parasitic nematodes to both humans and animals. In Mississippi, almost 10 percent of dogs tested for heartworms were heartworm … So any pet not on heartworm prevention could have a one-in-ten chance of being infected with heartworm. 2013–2017 American Community Survey. Article  We investigated seasonality of D. immitis transmission within Wake County by plotting the overall percent positive pools across the sampling season. Heartworm prevalence is, overall, low in Canada, with endemic transmission occurring seasonally only in regions of southern British Columbia, Manitoba, Ontario, Quebec, and New Brunswick. Bonizzoni M, Gasperi G, Chen X, James AA. However, with vector diversity being linked to both increased and decreased disease transmission depending on the pathosystem, D. immitis risk as a function of urbanization-induced vector diversity changes is difficult to predict. California Privacy Statement, The two variables were positively correlated (Spearman’s ρ = 0.494, P = 0.027). Spatial association between malaria vector species richness and malaria in Colombia. Figure 1b- Mean prevalence rates in Europe. 2006;135:303–14. We maximized the likelihood function: where \(y_{i\,j}\) is the binary response of whether pool \(j\) in habitat \(i\) was positive for D. immitis, \(n_{i\,j}\) is the number of mosquitoes in pool \(j\) from habitat \(i\), and \(p_{i}\) is the probability that an individual mosquito in habitat \(i\) is positive for D. immitis. Increased mosquito abundance and species richness in Connecticut, United States 2001-2019. We found that the best model to predict heartworm prevalence within dogs at the zip code level is one that includes both mosquito Shannon–Wiener diversity and household income. albopictus. Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, USA, Meredith R. Spence Beaulieu & Michael H. Reiskind, Animal Services Division, Department of Environmental Services, Wake County Animal Center, Raleigh, NC, USA, You can also search for this author in We performed a logit transformation of our within-host heartworm prevalence data to account for its proportional nature [38], and used Akaike information criterion (AIC) as the estimator of model quality in our model selection. PubMed Central  Model selection revealed within-host prevalence was best predicted by a positive relationship with mosquito Shannon-Wiener diversity and a negative relationship with household income. We collected a total of 10,244 mosquitoes over the two years of sampling. Dog heartworm is considered endemic in the contiguous USA, with highest prevalence in the southeastern USA [19]. However, since mosquitoes are responsible for transferring the parasite from dog to dog, some areas do pose a higher risk than others. However, mosquito diversity metrics were positively correlated with host heartworm prevalence. We found an overall decrease in heartworm disease within the vector in suburban areas and a positive correlation between heartworm disease within the host and mosquito diversity measures, which are lower in suburban areas than in undeveloped areas. PeerJ. Large dog relinquishment to two municipal facilities in New York City and Washington, DC: identifying targets for intervention. -, Linthicum KJ, Britch SC, Anyamba A. We thank Paul Labadie, Tommy Pleasant, Hannah Jenkins, Cole Keenan and Dakota Palacio for their work on this project. Heartworm antigen tests are the primary diagnostic and screening tests for heartworm. Nayar JK, Knight JW. Parasit Vectors. Sci Rep. 2016;6:29002. Elife. Prevalence of infectious diseases in cats and dogs rescued following Hurricane Katrina. Geospat Health. PubMed Central  Neighborhood age was not a significant factor, as Kruskal–Wallis test was not significant when incorporating neighborhood age categories. The authors declare that they have no competing interests. 2016;61:395–415. Despite these limitations, shelter data presents a large, readily available dataset that generally cuts across various human demographics, including income and education levels [45], and is the best data currently available with which to test our predictions. To verify that qPCR pools were positive for D. immitis, all positive amplicons were submitted to Eton Bioscience (San Diego, CA, USA) for Sanger sequencing.
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