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      Improved vector control of Triatoma infestans limited by emerging pyrethroid resistance across an urban-to-rural gradient in the Argentine Chaco

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          Abstract

          Background

          The sustainable elimination of Triatoma infestans in the Gran Chaco region represents an enduring challenge. Following the limited effects of a routine pyrethroid insecticide spraying campaign conducted over 2011–2013 (first period) in Avia Terai, an endemic municipality with approximately 2300 houses, we implemented a rapid-impact intervention package to suppress house infestation across the urban-to-rural gradient over 2015–2019 (second period). Here, we assess their impacts and whether persisting infestations were associated with pyrethroid resistance.

          Methods

          The 2011–2013 campaign achieved a limited detection and spray coverage across settings (< 68%), more so during the surveillance phase. Following community mobilization and school-based interventions, the 2015–2019 program assessed baseline house infestation using a stratified sampling strategy; sprayed all rural houses with suspension concentrate beta-cypermethrin, and selectively sprayed infested and adjacent houses in urban and peri-urban settings; and monitored house infestation and performed selective treatments over the follow-up.

          Results

          Over the first period, house infestation returned to pre-intervention levels within 3–4 years. The adjusted relative odds of house infestation between 2011–2013 and 2015–2016 differed very little (adj. OR: 1.17, 95% CI 0.91–1.51). Over the second period, infestation decreased significantly between 0 and 1 year post-spraying (YPS) (adj. OR: 0.36, 95% CI 0.28–0.46), with heterogeneous effects across the gradient. Mean bug abundance also dropped between 0 and 1 YPS and thereafter remained stable in rural and peri-urban areas. Using multiple regression models, house infestation and bug abundance at 1 YPS were 3–4 times higher if the house had been infested before treatment, or was scored as high-risk or non-participating. No low-risk house was ever infested. Persistent foci over two successive surveys increased from 30.0 to 59.3% across the gradient. Infestation was more concentrated in peridomestic rather than domestic habitats. Discriminating-dose bioassays showed incipient or moderate pyrethroid resistance in 7% of 28 triatomine populations collected over 2015–2016 and in 83% of 52 post-spraying populations.

          Conclusions

          The intervention package was substantially more effective than the routine insecticide spraying campaign, though the effects were lower than predicted due to unexpected incipient or moderate pyrethroid resistance. Increased awareness and diagnosis of vector control failures in the Gran Chaco, including appropriate remedial actions, are greatly needed.

          Graphical abstract

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s13071-021-04942-9.

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          Most cited references61

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          Rings, circles, and null-models for point pattern analysis in ecology

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            Chagas disease: a Latin American health problem becoming a world health problem.

            Political repression and/or economic stagnation stimulated the flow of migration from the 17 Latin American countries endemic for Chagas disease to developed countries. Because of this migration, Chagas disease, an autochthonous disease of the Continental Western Hemisphere is becoming a global health problem. In 2006, 3.8% of the 80,522 immigrants from those 17 countries to Australia were likely infected with Trypanosoma cruzi. In Canada in 2006, 3.5% of the 156,960 immigrants from Latin America whose country of origin was identified were estimated to have been infected. In Japan in 2007, there were 80,912 immigrants from Brazil, 15,281 from Peru, and 19,413 from other South American countries whose country of origin was not identified, a portion of whom may have been also infected. In 15 countries of Europe in 2005, excluding Spain, 2.9% of the 483,074 legal Latin American immigrants were estimated to be infected with T. cruzi. By 2008, Spain had received 1,678,711 immigrants from Latin American endemic countries; of these, 5.2% were potentially infected with T. cruzi and 17,390 may develop Chagas disease. Further, it was estimated that 24-92 newborns delivered by South American T. cruzi infected mothers in Spain may have been congenitally infected with T. cruzi in 2007. In the USA we estimated that 1.9% of approximately 13 million Latin American immigrants in 2000, and 2% of 17 million in 2007, were potentially infected with T. cruzi. Of these, 49,157 and 65,133 in 2000 and 2007 respectively, may have or may develop symptoms and signs of chronic Chagas disease. Governments should implement policies to prevent donations of blood and organs from T. cruzi infected donors. In addition, an infrastructure that assures detection and treatment of acute and chronic cases as well as congenital infection should be developed. 2009 Elsevier B.V. All rights reserved.
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              High resistance to pyrethroid insecticides associated with ineffective field treatments in Triatoma infestans (Hemiptera: Reduviidae) from Northern Argentina.

              Field populations of Triatoma infestans Klug were collected during 2002 from four villages in northern Argentina (El Chorro, La Toma, El Sauzal, and Salvador Mazza), after application of deltamethrin and other pyrethroids was ineffective. High levels of resistance to the pyrethroid insecticides deltamethrin, beta-cypermethrin, beta-cyfluthrin, and lambda-cyhalothrin were detected in all of the evaluated populations. The resistance ratio to pyrethroids determined by topical application ranged from 50.5 (deltamethrin, El Sauzal) to 667.6 (beta-cyfluthrin, Salvador Mazza). None of the pyrethroid-resistant insects was resistant to the organophosphorus insecticide fenitrothion. Topical application of piperonyl butoxide to the most deltamethrin-resistant population (Salvador Mazza) led to slight reduction in levels of resistance. Activity of P450 monooxygenase, measured in individual insects through ethoxycoumarine-O-deethylase, showed a slight but noticeable difference in the distribution of activities between susceptible and resistant populations. The total percentage of insects below 0.48 pmol of 7-OH coumarine/min/ insect was 36.4 for Salvador Mazza population and 64.3 pmol of 7-OH coumarine/min/insect for CIPEIN strain. Whereas a low level of resistance to deltamethrin was previously related to monooxygenase activity in T. infestans, the high levels of resistance shown by these populations seem to involve monooxygenase in combination with other resistance mechanisms, for example, insensitivity of nervous membrane. Research on T. infestans resistance is in progress to improve Chagas vector control programs in Latin America and to implement resistance management strategies.
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                Author and article information

                Contributors
                solgaspe@ege.fcen.uba.ar
                mvcardinal@ege.fcen.uba.ar
                pilar.fernandez@wsu.edu
                cvassena@citedef.gob.ar
                porihuela@citedef.gob.ar
                gfenriquez@ege.fcen.uba.ar
                alvedro@ege.fcen.uba.ar
                manualbert55@gmail.com
                julietanattero@ege.fcen.uba.ar
                lavizcachasp@gmail.com
                nataliam@ege.fcen.uba.ar
                carla@ege.fcen.uba.ar
                hectorfreilij@yahoo.com.ar
                gurtler@ege.fcen.uba.ar
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                28 August 2021
                28 August 2021
                2021
                : 14
                : 437
                Affiliations
                [1 ]GRID grid.7345.5, ISNI 0000 0001 0056 1981, Laboratorio de Eco-Epidemiología, Facultad de Ciencias Exactas y Naturales, , Universidad de Buenos Aires, ; Ciudad Universitaria, C1428EHA Buenos Aires, Argentina
                [2 ]GRID grid.423606.5, ISNI 0000 0001 1945 2152, Instituto de Ecología, Genética y Evolución de Buenos Aires, , Consejo Nacional de Investigaciones Científicas y Técnicas, ; Ciudad Universitaria, C1428EHA Buenos Aires, Argentina
                [3 ]GRID grid.30064.31, ISNI 0000 0001 2157 6568, Washington State University, Paul G. Allen School for Global Animal Health, Allen Center, ; 1155 College Ave., Pullman, WA 99164 USA
                [4 ]Centro de Investigaciones de Plagas e Insecticidas (CIPEIN, CONICET/UNIDEF/CITEDEF), Juan Bautista La Salle 4397, Villa Martelli, CP 1603 Buenos Aires, Argentina
                [5 ]GRID grid.108365.9, ISNI 0000 0001 2105 0048, Universidad Nacional de San Martín, ; Buenos Aires, Argentina
                [6 ]GRID grid.7345.5, ISNI 0000 0001 0056 1981, Cátedra de Química Analítica Instrumental, Facultad de Farmacia y Bioquímica, , Universidad de Buenos Aires, ; Buenos Aires, Argentina
                [7 ]GRID grid.423606.5, ISNI 0000 0001 1945 2152, Servicio de Parasitología, Hospital de Niños Ricardo Gutiérrez, , Instituto Multidisciplinario de Investigación en Patologías Pediátricas, CONICET-GCBA, ; Buenos Aires, Argentina
                Article
                4942
                10.1186/s13071-021-04942-9
                8401064
                34454569
                92bf5876-b530-4cd7-a906-42b4038f6920
                © The Author(s) 2021

                Open AccessThis 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. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. 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. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 17 February 2021
                : 10 August 2021
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003074, Agencia Nacional de Promoción Científica y Tecnológica;
                Award ID: PICT 2015-2921
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100005363, Universidad de Buenos Aires;
                Award ID: UBACYT 20020130100843BA
                Award Recipient :
                Funded by: Universidad de Buenos Aires (AR)
                Award ID: 20020170100779BA
                Award Recipient :
                Funded by: Fundación Bunge y Born (AR)
                Categories
                Research
                Custom metadata
                © The Author(s) 2021

                Parasitology
                gran chaco,sustainability,triatoma infestans,urban,vector control,pyrethroid resistance
                Parasitology
                gran chaco, sustainability, triatoma infestans, urban, vector control, pyrethroid resistance

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