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Ecological and Sociodemographic Determinants of House Infestation by Triatoma infestans in Indigenous Communities of the Argentine Chaco
research-article
Author(s):
M. Sol Gaspe ,
Yael M. Provecho ,
M. Victoria Cardinal ,
M. del Pilar Fernández ,
Ricardo E. Gürtler
*
Publication date (Electronic):
18 March 2015
Journal:
PLoS Neglected Tropical Diseases
Publisher:
Public Library of Science
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Abstract
Background
The Gran Chaco ecoregion, a hotspot for Chagas and other neglected tropical diseases, is home to >20 indigenous peoples. Our objective was to identify the main ecological and sociodemographic determinants of house infestation and abundance of Triatoma infestans in traditional Qom populations including a Creole minority in Pampa del Indio, northeastern Argentina.
Methods
A cross-sectional survey determined house infestation by timed-manual searches with a dislodging aerosol in 386 inhabited houses and administered questionnaires on selected variables before full-coverage insecticide spraying and annual vector surveillance. We fitted generalized linear models to two global models of domestic infestation and bug abundance, and estimated coefficients via multimodel inference with model averaging.
Principal Findings
Most Qom households were larger and lived in small-sized, recently-built, precarious houses with fewer peridomestic structures, and fewer livestock and poultry than Creoles’. Qom households had lower educational level and unexpectedly high residential mobility. House infestation (31.9%) was much lower than expected from lack of recent insecticide spraying campaigns and was spatially aggregated. Nearly half of the infested houses examined had infected vectors. Qom households had higher prevalence of domestic infestation (29.2%) than Creoles’ (10.0%), although there is large uncertainty around the adjusted OR. Factors with high relative importance for domestic infestation and/or bug abundance were refuge availability, distance to the nearest infested house, domestic insecticide use, indoor presence of poultry, residential overcrowding, and household educational level.
Conclusions and Significance
Our study highlights the importance of sociodemographic determinants of domestic infestation such as overcrowding, education and proximity to the nearest infested house, and corroborates the role of refuge availability, domestic use of insecticides and household size. These factors may be used for designing improved interventions for sustainable disease control and risk stratification. Housing instability, household mobility and migration patterns are key to understanding the process of house (re)infestation in the Gran Chaco.
Author Summary
Indigenous peoples are especially affected by Chagas and other neglected tropical diseases. One of the most numerous ethnic groups in the Gran Chaco region of South America is the Qom (Toba) people. The living conditions of Qom households most likely differ substantially from those of Creoles, and their association with house infestation by triatomine bugs has not been investigated. This is important because the major vector species have adapted to thrive in human sleeping quarters, and in addition to housing construction patterns, other ecological and sociodemographic factors may affect house infestation. We found that Qom households had much higher domestic infestation than Creole ones, in conjunction with more precarious housing, fewer poultry and livestock. The unexpectedly high local residential mobility of Qom households combined with the large fraction of recently-built houses (derived from a rapidly increasing population with a very young age structure during recent decades) may explain why domestic infestation was much lower than expected from the lack of recent insecticide spraying campaigns. Domestic infestation and bug abundance increased with overcrowding and refuge availability, and decreased with household education levels and insecticide use. These results are useful for designing improved interventions and household risk stratification.
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Most cited references48
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Indigenous health in Latin America and the Caribbean.
Raul A Montenegro, Carolyn Stephens (2006)
This review is the second in a series on Indigenous health, covering different regions and issues. We look briefly at the current state of Indigenous health in Latin America and the Caribbean, a region with over 400 different indigenous groups and a total population of 45 to 48 million people. We describe the complex history and current reality of Indigenous peoples' situation within the American continent. We discuss the importance of Indigenous health systems and medicines, and look at changing political environments in the region. The paper concludes with a discussion of the changing political and legislative environment in Latin American countries.
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Socio-Cultural Aspects of Chagas Disease: A Systematic Review of Qualitative Research
Laia Ventura-Garcia, Maria Roura, Christopher Pell … (2013)
Introduction According to the World Health Organization (WHO), globally, more than 10 million people are infected with Trypanosoma cruzi. Most live in Latin American countries, where the parasite is endemic [1] and where control strategies were first implemented in the 1940s and 1950s [2]–[3]. Since 2000, due to expanding migration flows and increased funding for research on Neglected Tropical Diseases (NTD), Chagas has become an international health priority. Estimates suggest that between 50,000 and 70,000 are affected in Spain [4], and 300,000 in the USA [5]. The persistence of Chagas disease – as with most NTD – is linked to social, cultural, historical, political and economic processes [6]–[8]. The WHO recognizes Chagas disease as one of the most neglected diseases, mainly found amongst the poorest [9]. Within countries, its unequal distribution illustrates the complex interaction of socio-cultural, biological and environmental factors. The creation of the WHO's Special Programme for Research and Training in Tropical Diseases (TDR) in 1975 saw the social sciences incorporated into the study of NTD [6], [10], [11]. However, a recent bibliographic analysis [7] has shown that social science contributions remain scarce. Hence there is a paradox: although the importance of social and cultural factors is broadly acknowledged, current approaches to NTDs almost always neglect aspects of the socio-cultural - biologically - environment triad [10]. This results in a narrower understanding of Chagas disease and hampers sustainable prevention and control [6]. Since 1990, the number of Chagas-related publications has shown a linear increase [3], [12]. What has qualitative social science research contributed? What are the main research gaps? What are next steps for future research? Under the auspices of the COHEMI project and as part of Work Package 6: Social and Cultural Context to Health Seeking of Latin American Migrants in Europe, this systematic review aims to provide a comprehensive overview of qualitative research on Chagas disease, both in endemic and non-endemic countries. Specific objectives include identifying qualitative studies through a systematic search strategy; describing the state of qualitative research; and synthesizing, analyzing and interpreting themes that have emerged [13]–[14]. This enables the identification of research gaps, contradictory findings and priorities for further research. The review is restricted to English, Spanish and Portuguese language literature. No previous literature review on this topic has been identified. Methods Search strategy Literature was identified using a search strategy available at www.cohemi-project.eu. Ten databases were examined using combinations of terms (see Table 1), and other sources of information, such as the bibliographies of identified articles, were used. The most recent searches were carried out in November 2012. 10.1371/journal.pntd.0002410.t001 Table 1 List of databases and search terms. DATABASE CONCEPTS Embase 1980 to 2012 week14, Ovid MEDLINE 1946 TO MARCH Week 4 2012, Social policy and practice 201201 Chagas.m_titl., Trypanosoma cruzi.m_titl., T.cruzi.m_titl. (Limit to human (not valid in Social Policy and Practice)) qualitative research.af., anthropology.af., ethnology.af., ethnography.af., social sciences.af., beliefs.m_titl., health seeking.m_titl., experienc$.m_titl., practices.m_titl., representations.m_titl., behavior.m_titl LILACS Chagas, Trypanosoma cruzi qualitative, anthropology, ethnography, qualitative research, psychology, social sciences JSTOR ti:(Chagas, Trypanosoma cruzi, T.cruzi) Scopus Chagas, Trypanosoma cruzi, trypanosomiasis (NOT Africa), T.cruzi. (Limit to human) qualitative research, ethnography, ethnology, social sciences, anthropology (all fields) Crochane Plus Chagas, Trypanosoma cruzi, T.cruzi qualitative, anthropology, social sciences TESEO (Chagas, T.cruzi, Trypanosoma cruzi):ti and abstract IME-ISOC (CSIC) Chagas, Trypanosoma cruzi, T.cruzi Citations and abstracts were downloaded into Mendeley and Endnote 6 by two independent researchers, and duplicates were deleted. A preliminary screening of titles and abstracts was performed according to the following inclusion criteria: research related to Chagas disease; employed qualitative methods and findings were derived from qualitative methods; English, Spanish and Portuguese language. Methods considered to be qualitative were interviews, observation or participant observation, focus groups, ethnography, discourse analysis and participatory methods. Of the articles that reported results based on quantitative and qualitative methods, only the latter data were reviewed. Surveys and book reviews were not included. Access to the full text of the remaining articles was sought; seven articles could not be accessed (see Figure 1). 10.1371/journal.pntd.0002410.g001 Figure 1 Flow of search. Analysis A thematic synthesis approach was taken to analyze the literature [13], [14]. Software for qualitative data analysis –AtlasTi– was used to code selected documents. “Descriptive themes” that resulted from this process enabled the generation of “analytical themes”, as a next step of interpretation. Articles were classified by fieldwork site and main topic (see Appendix S1 and Appendix S2). Results Search results Of the thirty-three studies reviewed, the majority (27) were conducted in Latin America: Argentina (12), Brazil (7), Bolivia (2), Peru (2), Venezuela (2), Paraguay (1) and Colombia (1). Of the twelve studies carried out in Argentina, half were by the same author; this was also the case for two articles from Brazil. In non-endemic countries, studies were conducted in Europe: Spain (4) and Italy (1); and one in USA. Most of the studies were based on individual interviews (24). In ten cases, this was the only reported technique for collecting data; twelve articles reported the complementary use of either: individual interviews and participant observation (7); individual and group interviews (2); individual interviews and participatory tools (1); individual interviews and other techniques (2); in three articles, researchers utilized more than two techniques. Finally, four articles reported participatory methods; discourse analysis techniques (2); and focus groups (2). Most of the articles have been published since 2008 (See Table 2). 10.1371/journal.pntd.0002410.t002 Table 2 Year of publication of the articles reviewed. Year published N 2008–2012 16 2003–2007 7 1998–2002 9 1993–1997 1 Qualitative synthesis of findings: Endemic countries The interplay of socio-structural factors and Chagas disease Chagas disease occurs in specific contexts marked by socio-cultural, political, economic, environmental and historical circumstances. Certain structural changes may influence the environment and people's living conditions, which, in turn, may trigger triatomin infestation (the Chagas disease insect vector) and provoke a higher risk of infection. Briceño-León [15] and Mastrangelo [16] described such case in the Amazon Region and Argentina, respectively: a shift in economic development during the 1980s towards industrial production and international trade played an important role determining social and environmental changes, which led to deterioration in living conditions. Land expropriations and deforestation forced families to migrate and engage in wage labor. Triatomins, previously located in more wooded areas, began occupying domestic spaces; and household re-infestation increased, in part because of its precarity. Several reviewed studies focused on migration and stigmatization of infected people as pathways that caused their living conditions to deteriorate. Bayer et al. [17] showed how, in neighboring communities in Peru, vulnerability to triatomine infestation depended on the socio-economic processes underlying migration and settlement patterns. Displacements from endemic rural areas to urban settings or from non-endemic areas to endemic areas - for permanent or temporal labor - contributed to the appearance of infections in urban and non-endemic rural areas [16]–[20]. Other studies explored how the stigmatization of poor and rural populations and the discrimination of infected individuals affected their access to health-care and working conditions. Studies in different parts of Argentina [16], [21]–[22] described the mistreatment and discrimination that ethnic groups experienced in medical contexts, limiting their access to care. Employment-related stigma and discrimination [18], [23]–[24] was highlighted in urban settings [18], [23], [25]–[26], where Chagas disease - even positive serology regardless of symptoms – often resulted in labor exclusion. Chagas sufferers therefore commonly avoided the diagnostic tests that were often a prerequisite for employment, and sought informal sector, which caused deteriorations in living conditions. Chagas-related stigma also affected more socially and economically favored groups [18], [26]–[27]. Chagas disease's association with filth, neglect and misery led such groups to ignore possible infections, avoid testing, and meant that positive diagnosis caused great suffering. Health practices Hygienic habits, household clutter, or cohabitation with domesticated animals were often identified as behaviors influencing Chagas prevention, and the persistence of the triatomine vector in dwellings [16], [18]–[19], [21]–[22], [25]–[26], [28]–[32]. Caballero Zamora et al. [28] and Rojas et al. [29] explained these behaviors in terms of a lack of knowledge about Chagas disease and its transmission. Therefore, as Sanmartino et al. [30] described, greater knowledge of Chagas disease would drive communities to acquire new health-related behaviors. However, this was not always the case, and other authors, including Sanmartino in subsequent research, suggested that increased knowledge of Chagas disease was not always enough to change practices [16], [18]–[19], [25], [28]: “risk perceptions” [16], [18]–[19], [25], [28], and the ways of thinking about Chagas within a population's worldview [16], [18], [21]–[22], [25]–[26], [31]–[32] might explain behaviors. Five studies [16], [18]–[19], [25], [28] suggested that community members' views about the danger of triatomins and Chagas disease often differed from those of policy makers and clinicians. For example, in some highly endemic areas, where living conditions were demanding and the vector very common, Chagas disease was not perceived as a threat or, at least, as a health priority. Therefore, behavior was not always researchers expected. Moreover, an absence of symptoms and of an impact on everyday activities contributed to the naturalization and normalization of Chagas disease [25]–[26], [31], which influenced care seeking [19]. Insight into different ways of thinking about Chagas disease, its socio-cultural representations, was however seen as crucial to understand behavior and explain why knowledge about Chagas disease does not always imply behavior change [16], [18], [21]–[22], [25]–[26], [31]–[32]. For example, taking into account the failure of previous preventive programs based on increasing knowledge amongst indigenous populations in Las Lomitas, Argentina, Sosa-Estani [22] highlighted how, from the indigenous (pilagá) point of view, disease causation was explained in personalistic terms, or as violation of taboos or social norms. Preventive and curative practices may be therefore deeply linked to such representations, rather than the parasite or insect-vector. In Bolivia [28], some indigenous understanding of the vector as bearers of good luck was also a way to explain inaction against triatomines. In “peri-domestic” settings of Argentina's Gran Chaco region, the failures of vector control activities were attributed to differences between the conceptions of “landscape”, “wild” and “domesticated” used in preventive programs and those of the target population [16]. Preventive programs differentiated “domestic” from “peri-domestic” spaces as an indicator of human proximity to the insect vector, whereas the local population conceived these spaces as a continuum, allowing humans, animals and plant material brought from the mountain to cohabit “domestic” spaces. Biomedical understandings of Chagas disease Particular ways of thinking about Chagas disease are not unique to target populations. Scientists' and health professionals' understandings are also developed in specific contexts and can affect their work. Kreimer et al. [3] reflected historically on the production of scientific knowledge on Chagas disease in Argentina: the “problem of Chagas” was defined according to the interests of different stakeholders, which involved recognizing certain facts and neglecting others. Historically, revised definitions of appropriate intervention strategies have also involved re-conceptualizations of Chagas disease: first seen as a problem of precarious living conditions; then as a question of fumigation; and finally, as a matter for basic research, for which molecular biology was prioritized. Ramos et al. [33] addressed the role of Brazilian mass media in the construction of the problem: positive assessments of Chagas' control strategies contributed to the social demobilization of a problem that was not yet under control. Addressing health professionals' understandings of Chagas disease in an Argentinean urban context and in Brazil, Sanmartino [34] and Uchoa et al. [24] highlighted how a lack of relevant training and their own stereotypes affected the care they provided. The patient's experience of Chagas disease Studies that addressed experiences of Chagas disease from the sufferer's perspective showed how social groups described a variety of conceptions about the disease [21], [24], [35]–[37]: local communities do not only have knowledge and specific ways of thinking about “Chagas”, but people also syncretize different kinds of knowledge, producing new hybridized understandings. Evaluating the first Chagas' preventive programs in Brazil, Magnani et al. [35] concluded that the emphasis placed on disease contributed to a rapid and effective response: it provoked awareness of people's responsibility for health and their role in combating the vector, and led to new preventive practices. Nevertheless, prevention programs that neglected those already affected disregarded the meanings attributed to “Chagas”: new meanings, such as associations with death, fear, suffering, distrust, and despair, caused suffering and could affect health seeking behaviors. For example, two studies from Brazil [24], [35] described how some people developed informal yet adaptive strategies, such as denying Chagas disease, when the emotional burden was unbearable. In contrast, studies in Brazil [35] and Argentina [18] described how a positive serology can be enough to consider oneself as ill, even if asymptomatic: although biomedical nosologies classify different degrees of severity of Chagas disease based on symptoms, infection by Trypanosoma was conflated with diagnosis of Chagas disease. A positive serology saw infected individuals identify themselves as sick, was sufficient to promote feelings of discomfort, and caused individual and social suffering. In all these situations, the patient-provider relationship was identified a key element in patients making sense of the disease [16], [18], [24], [35]–[36]. Institutional strategies There is no effective vaccine for Chagas disease and treatments are not 100% effective (in chronic cases effectiveness is unknown, although known to be low). Therefore, in endemic countries, the main strategies to combat the disease involve prevention interventions, control of blood banks and monitoring pregnant women. Preventive strategies have focused on controlling the most common vector through three principal interventions [25]: housing improvements, insecticide spraying, and health education. Many of the reviewed studies were designed to supplement, improve or evaluate Chagas prevention and/or control interventions [16], [18]–[20], [22], [25], [27], [28]–[32], [34]–[40] Four studies [16], [18], [24], [35] highlighted the need for these approaches, but raised the question of whether achievements in vector control led to improvements in social and individual wellbeing. Surveillance and control activities were often dissociated from diagnosis, management and care. Moreover, because Chagas disease was problematized with reference to a narrow biological framing that neglected other political, economical, socio-cultural and individual dimensions, activities focused on infected individuals or those at risk of infection were neglected. Qualitative synthesis of findings: Non-endemic countries Access to health services In non-endemic countries, Chagas control is based on screening protocols for migrants considered at risk of infection. Several studies highlighted the importance of monitoring migrants' access and utilization of health services [41]–[45]. In Europe, migrants' lack of information about services and working constraints were the main barriers to accessing health services [41]–[45]. Immigration policies [41], migrants' mobility and Chagas disease's lack of symptoms [42] were also highlighted. Although one study [42] concluded that a “lack of knowledge” about Chagas disease prevented Latin American migrants from accessing screening services in Madrid, an ethnography conducted in Barcelona [43] revealed that migrants tend to feign ignorance during medical consultation - waiting for information from health personnel - and discuss their experiences and knowledge in other contexts. Although the author highlighted the importance of providing information about Chagas disease, associated fears and meanings explained why some migrants resisted screening. Indeed, meanings of Chagas disease and experiences within the health system in migrants' countries of origin were key to understanding health-seeking in Spain. In USA [45], a lack of awareness about Chagas disease among Latinos and fears of being diagnosed with a disease associated with death were also reported as barriers to testing and treatment, together with reservations about quality of care and costs. Gender relationships and identity also influenced migrants' patterns of healthcare utilization: men were less likely to utilize healthcare services because they associated seeking help with weakness, which challenged their ideals of masculinity. Furthermore, due to their social role as breadwinners, men prioritized their families' economic situation over their own health- [43]–[44]. Indeed, men did not use to seek care until symptoms were unbearable [45]. In contrast, women had closer ties to the health system due to their reproductive role. Mothers' feelings of responsibility and guilt, if their children received a positive diagnosis, led them to use health services to ensure their children received treatment [43]–[45]. Studies emphasized the importance of developing community-oriented programs [41]–[43], as well as the need to consider the wider social determinants of health-care access services and health-related – such as the factors that limit patients' capacity to alter their dietary habits to reduce Chagas-related constipation [46] - into strategies and health recommendations [41], [46]. Migratory goals as incentives for seeking care A study conducted in Madrid [44] described how Bolivian migrants attended a specialized tropical disease unit with chronic symptomatic Chagas disease, and following the death or diagnosis of a friend or relative. Patients were referred by family, friends, or through primary health care facilities. However, migrants' main motivations for seeking care were not only associated with the somatic dimension of Chagas disease; patients' main concerns were linked to their life projects and dying before achieving their migratory goals: ensuring the welfare of relatives, who depended on their income and the health of their children, was essential [43]–[44]. Although social relations, the family and migratory projects were key to understanding health seeking, these motivations contrasted with a disease-centered approach utilized in control interventions and care programs. This contrast was complicated by the mostly asymptomatic nature of the disease, its association with death and severe illness, and the lack of cure or effective treatment. Regarding treatment, some patients claimed that it could lengthen life, and hence was a guarantee of achieving migratory goals [43]–[44]. Other asymptomatic patients considered it an unnecessary risk, assuming that symptoms would only present after achieving their migratory goals [44]. Side effects and uncertain outcome were reasons for refusing or abandonment treatment. Discussion As the work of Bastien [47] and Briceño-León [48] suggest, the literature reviewed illustrates how Chagas disease is embedded in a web of relationships marked by biological, socio-cultural, political, economical, historical and environmental circumstances that shape its incidence and prevalence, as well as population's response. The reviewed articles identified pathways that lead certain social groups into conditions that increase their vulnerability to Chagas disease [15]–[26], [31]. The impacts of macro-economic policies on local communities, national and international economic/labor migration, or the social and political exclusion of poor, rural or ethnic groups were some of the processes described. Nonetheless, wide ranges of social determinants that foster propitious conditions for infection and prevent social group from changing their behavior have been mostly neglected in Chagas disease control strategies. Gaining insights into the processes that increase vulnerability to infection in specific contexts is however fundamental to orient and adapt interventions to local settings. Such an understanding can assist the development of national and international policies and the implementation of the most suitable prevention measures in a given context. With regard to prevention and control activities, behavioral change approaches at an individual and community level have had varying degrees of success. In the reviewed literature, there were two general approaches. In one approach a population's lack of knowledge and its members' beliefs were assumed to be “cultural obstacles” to behavior change or to care seeking [28]–[30], [42]. A second approach however proposed an alternative: knowledge is not enough to change behavior, and populations' understanding of health and Chagas disease - consistent or not with biomedical models - and living conditions play an important role with regard to behavior [16], [18]–[19], [21]–[22], [25]–[26], [28], [31]–[32], [43]–[44]. The reviewed highlights an important question: how can awareness about Chagas disease and triatomines be raised in social groups that do not conceive them as a health threat? Scholars have suggested that people's understandings of Chagas and the social context that influences their living conditions are key to explain the disease not being considered a threat [16], [18]–[19], [21]–[22], [25]–[28], [31]–[32], [43]–[44]. When living conditions are demanding, as is common in endemic rural areas, Chagas disease is not often a priority. However, socially and economically favored groups do not often consider the possibility of infection. Inversely, when Chagas disease is perceived to be a problem, reasons may not be linked to the disease itself, but to its social impact, such as hindering migratory goals or its financial affects on a patient's children. Prevention and care practices are often therefore less disease-specific than clinicians and policy makers' understandings. Moreover, understanding how these processes vary across social groups is key to the design and implementation of appropriately adapted interventions. In relation to local ways of thinking about Chagas disease, a second question arose about how to recognize local knowledge and build bridges with biomedicine [18]. People are not merely recipients of information and, although social groups handle Chagas-related knowledge and meanings based on their socio-cultural worldviews [16], [21], [24], [35]–[37], [44]–[45], these models are not closed and pure. Instead they are syncretic: for example in Brazil [37], where during early prevention programs, new conceptions of Chagas disease were formed based on pre-existing knowledge and the information disseminated. Chagas-related meanings can also change during migration, when they are re-orientated according to the new situation and possibilities [44]–[45]. Preventive interventions and doctor-patient interactions are spaces where new conceptions about Chagas disease are constructed. Inasmuch as people use to react to the meanings associated with Chagas disease and not just to the disease itself [44], messages transmitted in preventive programs, doctor-patient communication, and the coordination of Chagas prevention and control programs with disease management patient care, are fundamental. Transdisciplinary activities that consider the experience and needs of those affected might be a successful way of creating links between biomedical and local understandings, opening new possibilities for Chagas disease prevention and management. Priorities for further research Further research is required to contextualize socio-cultural factors and processes associated with Chagas disease in different countries and amongst different social groups: differentiated by class, ethnicity, geography, gender and age. This necessitates the study of Chagas disease in relation to the socio-cultural, economical, political, historical processes that enable its appearance and persistence, as well as the different experiences of Chagas disease. Research concerning policies and programs to address the socio-structural factors is needed to reduce the burden of Chagas disease; understanding the elements that hinder the development and implementation of such policies is also important. In most countries, there is a general lack of qualitative studies informing locally and nationally appropriate strategies. Contextualized research on migratory flows, how they interact with living conditions, and their links with Chagas incidence is necessary. In addition, research on changing risk behaviors for infection that takes into account the processes that place social groups in different positions of vulnerability is required. Such approaches are rare in research on and interventions for Chagas, though they may be crucial for policy and action guidance. There is a lack of information concerning health seeking behaviors and their underlying processes in endemic countries. As studies described self-care practices [18], [24], [28], [35]–[36],[45], as well as deficiencies in diagnosis, care and treatment for Chagas disease, understanding the processes underlying the specific care seeking steps could contribute to the design and/or re-orientation of prevention, screening and care programs, both in endemic and non endemic countries. A deeper knowledge of experiences of an asymptomatic disease and its relationship with health seeking could also be helpful to understand health seeking processes. Because Chagas disease is considered a zoonosis that cannot be eradicated, long-term entomological surveillance systems are required [49]. Further research on the effects of the organization of health systems, especially to clarify the consequences of Chagas disease control programs within the framework of decentralized health systems existing in almost all Latin America, would be crucial for the implementation and sustainability of effective and permanent epidemiological surveillance. Comparative research across countries would be useful for this purpose. More research to evaluate medium and long-term social and individual effects of preventive programs implemented in endemic countries – whether vertical or participatory - as well as the social and individual impact of control strategies in endemic and non-endemic countries is needed. Evaluating interventions using this broader perspective, and developing research tools to expand the focus of these activities to incorporate socio-cultural aspects of health is key to designing successful long-term programs. Furthermore, research focused on incorporating people's experience and needs into policies and interventions in endemic and non-endemic countries, and the development of preventive and/or control actions, conducted with attention to affected individuals beyond medical spaces, is crucial. Some topics were scarcely addressed in the qualitative research on Chagas. For example, a transnational approach [50], which views places of origin and settlement as continuous rather than disconnected social spaces, was absent. Because migration and health research has highlighted the impact on the health knowledge and practices of the migrant's relatives in the country of origin, the study of social remittances [51] for health is important to understand behavior and orient interventions. Moreover, it is necessary to better understand how conceptions of Chagas disease in endemic countries – for example, resulting from the vertical implementation of prevention programs - might influence how people experience Chagas disease during migration, affecting health seeking behaviors in non-endemic countries. How infected individuals construct their identities as ill or as healthy is also particularly important with regard to understanding the mismatch between the experience of those affected and medical classifications of Chagas disease. Further research on transdisciplinary approaches to addressing Chagas disease is required. Strengths and limitations of the review The review includes papers in three languages, giving a broad overview of research conducted in different contexts, with varied health systems and at different points in the development of Chagas programs. To retrieve literature that is not electronically indexed, grey literature was also searched and incorporated. Screening was carried out in duplicate and discrepancies were solved with consensus between reviewers. Results are limited to the issues raised in the studies reviewed. Exclusion of studies whose full-text could not be accessed may be a limitation. However, because abstracts were checked, and the authors of excluded articles were included in the review through their authorship of other articles, the impact on the themes is probably minimal. Conclusions Biomedical aspects of Chagas disease are embedded in socio-cultural and environmental contexts. The literature reviewed shows how qualitative social science provides key tools to understand this socio-cultural context. This review is a potentially useful resource for policy makers, clinicians, researchers and patients. A number of findings are particularly important for the design and implementation of policies, strategies and programs. Social and structural processes are essential to explain the emergence, persistence and re-emergence of Chagas disease. However, few studies address strategies aimed at influencing the socio-structural context, and there is a general lack transferring their results in practice. Different social groups – influenced by ethnicity, socio-economic status, age, urban/rural context - experience different social conditions that influence their Chagas-related experiences and behaviors. Understanding how socio-cultural processes differentially affect these groups is key to designing and promoting appropriate interventions, adapted to populations and contexts, and considering their specific needs. Behavioral change approaches should consider how social conditions and the local representations of health and disease influence the practices related to Chagas. Chagas disease requires an explicitly multidimensional approach, in which prevention, control and care strategies and programs are designed and implemented jointly, and in which the social and biomedical sciences, together with the experience of those affected, are incorporated and articulated. Supporting Information Appendix S1 List of documents, location of data and main topic. Endemic countries. (TIFF) Click here for additional data file. Appendix S2 List of documents, location of data and main topic. Non endemic countries. (TIFF) Click here for additional data file. Checklist S1 Prisma checklist. (DOC) Click here for additional data file.
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Community Participation in Chagas Disease Vector Surveillance: Systematic Review
Fernando Abad-Franch, M. Celeste Vega, Miriam Rolón … (2011)
Introduction Chagas disease still imposes a heavy burden on most Latin American countries, with about 10–12 million people infected by Trypanosoma cruzi [1], [2]. Multinational control initiatives have since the early 1990s drastically reduced prevalence and incidence, mainly through insecticide-based elimination of domestic vector populations (blood-sucking bugs of the subfamily Triatominae) [3] and systematic screening of blood donors with highly sensitive serological tests [1], [2], [4], [5]. In spite of these advances, vector-borne transmission is estimated to cause about 40,000 new infections per year [6]. Reinfestation of treated households by native vectors as the residual effect of insecticides vanishes is the most likely mechanism underlying such persistent transmission [7]. Similarly, outbreaks of acute Chagas disease have been attributed to the contamination of foodstuffs by infected adult (i.e., winged) triatomines that invade premises where food is processed or stored [8]–[12]. In Amazonia and other humid forest ecoregions, where the bugs rarely colonise inside houses, endemic, low-intensity transmission seems also mediated by adventitious, household-invading triatomines [13]–[15]. In addition, there is growing concern that insecticide-resistant vector populations, such as those detected in southern South America [16], [17], may threaten effective disease prevention. This rapid overview shows why sustained Chagas disease control is believed to require some sort of longitudinal, long-term surveillance system capable of detecting and eliminating household infestation foci [1], [18]. Surveillance typically relies on the periodical inspection of households by trained personnel. Active vector searches are performed with or without the aid of chemical ‘flush-out’ agents such as low-dose pyrethroid dilutions, and infestation foci are eliminated by insecticide spraying when discovered [18]. However, detecting the vectors can be difficult, particularly when only small populations occur within or around households. In fact, vector colonies are expected to become rarer and smaller as control programmes proceed, and managers are progressively less prone to fund costly active surveillance resulting in few detection events. A number of vector-detection devices have been designed in an attempt to enhance surveillance; most consist of boxes that triatomines can use as refuges or of paper sheets or calendars where the typical faecal streaks of the bugs can be identified [19]–[27]. Such ‘sensing devices’ are placed within households or in annex structures and checked periodically for bugs or their traces, supposedly reducing the costs of surveillance while retaining adequate sensitivity [26]–[29]. Finally, and since the early vector control trials, there has been a perception that resident householders may have better chances of discovering bugs in their own homes than a visiting team searching the house for a few minutes every several months [30]–[32]. ‘Community participation’ in entomological surveillance gained extra momentum with the Declaration of Alma Ata [33], [34], which “…encouraged approaches to health care that incorporated community participation and community development” (ref. [34], p. 1). Experiences involving community participation in Chagas disease control have been described in several settings across Latin America [18], [30], [31]; they seem to converge towards an encouraging overall picture, and the Chagas disease example has accordingly been praised in several subjective reviews (e.g., [35], [36]). However, the effectiveness of these diverse strategies for Chagas disease vector surveillance, including community participation, has not been thoroughly and objectively assessed at the continental scale. With the aim of filling this gap, we systematically reviewed the published evidence on this issue, tackling specifically the following major questions: (i) How common and important is the phenomenon of house reinfestation by triatomine bugs after control interventions?; (ii) How effective are different vector surveillance strategies at detecting infestation/reinfestation foci?; (iii) To what extent have community participation and empowerment been effectively promoted?; and, finally, (iv) Can available strategic options be condensed in overarching recommendations for surveillance that apply across the highly diverse ecological and social-cultural settings where the problem is present? Methods The review protocol is available upon request from the corresponding author. This review was carried out in the context of a collaborative project led by the Inter-American Development Bank, and was not formally registered. We searched Medline, ISI Web of Knowledge, Scopus, LILACS, and SciELO; the major query argument was “Triatomin* AND (Control OR Surveillance)”. Searches retrieved records from 1948 to 2009, including additional documents identified by searching bibliographies and in the authors' records. This search strategy aimed at recovering documents describing vector control interventions, with or without surveillance, so that post-control reinfestation trends could also be assessed. Only documents describing field interventions aimed at the control and/or surveillance of domestic Chagas disease vectors were included in the full review process. Descriptive (non-intervention) reports, results of research with laboratory or experimental vector populations, expert reviews, and opinion or commentary pieces were either excluded or used only for the introduction and/or discussion. We were particularly interested in comparing strategies involving institutional (by professional staff) or participatory surveillance. We also compared alternative methods for vector detection, including active searches, vector-detection devices, and community participation. Major outcomes included household infestation/reinfestation indices (or, in some cases, bug catches) and vector detection rates. Inclusion/exclusion of documents was assessed independently by ARdA and FA-F, and discrepancies resolved by consensus. Figure 1 presents the flow diagram of the review process. Data were independently extracted by ARdA and FA-F using predefined data fields inspired by the Guide to Community Preventive Services [37] (www.thecommunityguide.org) and including study quality indicators. FA-F revised data extraction results and resolved inconsistencies by re-checking the original documents. The following items were considered: (1) study classification (study design, intervention components, whether or not the intervention was part of a broader initiative, outcomes); (2) descriptive information, including (2.i) description of the intervention (what was done, how, where and by whom it was done, theoretical basis of the intervention, types of organisation involved, whether or not there was any intervention in a control group), (2.ii) study characteristics (place, time, population, settings, outcome measurement, whether or not there was a measurement of exposure to the intervention), (2.iii) results (primary results, sample and effect sizes), and (2.iv) applicability in settings other than the actual study one (direct and indirect costs, harms and benefits, implementation process, and whether the community participated at each stage of the process – design, pre-implementation, effecting, and evaluation); and (3) study quality, including quality of descriptions, sampling (universe, eligibility and selection of participants, sample size, potential sampling biases), effect measurements, data analyses (statistics, confounders, repeated measures or other sources of non-independence), and interpretation of results (rate of adherence, control and assessment of potential confounders and sources of bias). Relevant references and other details deemed important were also recorded. The protocol required extracting detailed demographic data about intervention and control or indirectly affected populations. Such information was however absent from or incomplete in most studies; this, together with the fact that the outcomes of primary interest refer to households, not individual people, led us to exclude these items from the protocol during the course of the review. 10.1371/journal.pntd.0001207.g001 Figure 1 Flow diagram of the systematic review process. The often important morphological, ecological and behavioural differences among triatomine bug species [3], combined with the likely sensitivity of results to study-specific (methods, research team performance) and site-specific conditions (vector density, household building materials and structure), led us to avoid estimating meta-analytical summary effects from different reports. Inadequate design and/or reporting of several studies were further factors hindering meta-analysis. When enough information was given in the original reports, we nonetheless re-analysed data from studies comparing control strategies (in terms of household infestation rates) and vector detection techniques (in terms of detection rates). Whenever possible, we used McNemar's tests for correlated proportions [38], with odds ratios (OR) estimated as the ratio of discordant results. When independence of observations was likely, or in the absence of complete data on repeated observations, ORs were estimated from standard contingency tables [39]. Approximate OR 95% confidence intervals (95%CI) were calculated by assuming normality of log-odds [39]. The VassarStats online facility (http://faculty.vassar.edu/lowry/VassarStats.html) and Microsoft Office Excel® spreadsheets were used for the analyses. Results Overall results Database searches retrieved 1,342 candidate documents; elimination of duplicates yielded 858 unique records (Figure 1) in English, Spanish, or Portuguese. Assessment of titles and abstracts yielded five groups: (a) documents apparently describing control and/or surveillance interventions (236 records), (b) non-intervention studies, (c) studies with laboratory or experimental vector populations, (d) subjective reviews and opinion pieces, and (e) reports clearly irrelevant to our review. Evaluation of group (a) documents against inclusion criteria identified 93 reports for full data extraction [Supporting Information, List S1]; of the remaining 143 (plus several additional references), 26 studies [Supporting Information, List S2] were also used for partial quantitative assessments, and the rest were considered as supplementary sources of qualitative information for the introduction and/or discussion. The spatial and ecological coverage of our review is represented in Figure 2. Only 11 randomised trials [40]–[50] were identified, with just one crudely assessing a community-based intervention [50] and four describing different aspects of the same trial [44]–[47]. Over half of the studies dealt directly or indirectly with different strategies for household-level vector surveillance. Interventions ranged from insecticide spraying (the most frequent) to educational activities, with a few studies describing alternative control approaches such as environmental management [51]–[58] or insecticide-treated materials [48], [49], [59]. Most studies measured intervention effects as reductions in household infestation rates (through entomological surveys) or as vector detection rates (through detection records). While the quality of the descriptions was generally adequate, analytical procedures were often dubious; for instance, albeit many studies describe results in which the same sampling units were assessed more than once (e.g., before-after, time-series) or by more than one method (e.g., vector-detection studies), only a few apply statistical tests suited for repeated measures or other sources of non-independence of observations. 10.1371/journal.pntd.0001207.g002 Figure 2 Geographical-ecological coverage of studies on Chagas disease vector control and surveillance. Study site locations (black dots) are overlaid on the World Wildlife Fund ecoregional map of Latin America (available with detailed ecoregion legends at www.conserveonline.org/docs/2001/06lac_ecoregions.jpg). Collaborative efforts involving both academic institutions and official public health agencies were common (∼70% of studies), a typical historical trait of Chagas disease vector control [60]. Even though sustainability was discussed in several documents, detailed assessment of the costs (monetary and not) and potential unintended benefits and harms was rare. Forty-eight reports described some sort of ‘community participation’ in the intervention; however, none of them explicitly stated that participation took place at the design stage, and only three describe a participatory evaluation process [47], [58], [61]. In contrast, local residents helped carry out the intervention in 45 studies, mainly by reporting vectors caught in their homes; in 20, the community was also involved in the pre-implementation phase. Control effectiveness and the role of surveillance Since Carlos Chagas historic paper [62], vector control has become the cornerstone of primary Chagas disease prevention [60], [63]. Pioneering attempts involved chemical (including cyanide gas) and physical means (including flamethrowers) [64]. The failure of DDT in controlling triatomines was followed by substantial optimism when HCH (lindane) proved successful in early trials in Brazil [65], [66], Argentina [67], and Chile [68]. The effectiveness of insecticide-based control kept improving as new chemicals and better formulations, with longer residual effects and lower toxicity, were introduced [40]–[42], [45], [69], [70]. Synthetic pyrethroids are now widely used and continue to be very efficient [71]–[75]; yet, recent research suggests that resistance may be widespread among some Triatoma infestans populations [16], [17], and insecticides are less effective in peridomestic environments [43], [76]. The top-quality report (in terms of sample size, design, and data treatment) we retrieved shows that peridomestic T. infestans foci reappear quickly after spraying (albeit with lower-density colonies) and that standard deltamethrin application with manual sprayers performs better than more sophisticated techniques [43]. Table 1 summarises the results of major reports on Chagas disease vector control [5],[18],[44],[57],[61],[63],[71]–[73],[77]–[113]. Overall, these studies unequivocally show that household insecticide spraying has successfully reduced infestation rates throughout Latin America, but also that reinfestation of dwellings by native vector species is common, spatially widespread, and temporally persistent. In many cases, the elimination of introduced populations was closely followed by the occupation of vacant niches by ‘secondary’ vector species, suggesting that the former had displaced the latter upon introduction [114], [115]. 10.1371/journal.pntd.0001207.t001 Table 1 Chagas disease vector control interventions: effectiveness, reinfestation trends, and the replacement of introduced species by native vectors. Ref. Comparison Intervention Vectors Setting Units, size Main results, comments and caveats [77] Before-after HCH Ti*, Pm Brazil (Cerrado, Bahia Interior Forests) Infestation rates, 324 DUs Infestation odds ∼6 (3 to 12) times lower after treatment; treated DUs near non-treated localities were ∼5 times less protected. (Analyses assume observations in each DU and time-point are independent) [78] Time-series (1951–64) HCH yr 6–8 Ti*, Pm Brazil (Cerrado, Bahia Interior Forests) Capture events by control agents and bugs captured by control agents Median annual capture events before-during-after treatment: Ti, 95-13-24; Pm, 31-14-36.5. Median number of bugs captured before-during-after treatment: Ti, 4,405-1,802-274; Pm, 138-72-186. (No information on number of DUs studied each year) [79] Time-series (1950–54; 1960–69) HCH Ti*, Pm Brazil (Alto Paraná Atlantic Forest, Cerrado) Number of bugs captured in DUs Median annual capture (range) 1950–54: Ti, 1,330 (167–1,850); Pm, 14 (0–775). Median annual capture (range) 1960–69: Ti, 27 (3–440); Pm, 1,506 (678–3,741). (No information on number of DUs studied each year) [80] Before-after HCH Ti*, Ts, Pm Brazil (Cerrado) Vector presence, ∼500 localities Ti virtually disappears; Ts persists in DUs of ∼45% of localities; Pm presence rises from 26% to 41% of localities [63] Time-series (1983; 1986–99) Mainly Deltamethrin Ti*, several native spp. Brazil (several ecoregions across the country) Number of bugs captured by control agents per yr countrywide Ti falls from >84,000 (in 1983) to 60,000 in 1953 to 0 in 2000, with the last focus (131 bugs) eliminated in 1999; Ts reaches a maximum of >114,000 in 1968, then steadily decreases to ∼7,000 bugs/yr from 1990 on; Pm reaches a maximum of >10,500 in 1968, then decreases to ∼2,800 bugs/yr in the 80s, ∼1,100 in the 90s, and ∼500 bugs/yr in 2000–2008. The number of DUs searched each year varied markedly: >600,000/yr up to 1973, ∼450,000/yr 1974–84, ∼20,000/yr 1985–88, and 35% up to 1971 to 25% in 1972, ∼15% in 1973–76, 5–10% in 1974–84, and 30% in the last assessment. (Approximate values taken from Figure 1A in the reference) [96] Before-after Deltamethrin Ti Argentina (Dry Chaco) Infestation rates, 533 DUs initially; 89 localities Pre-treatment infestation rate: 48.2%; 1 yr later, 383 DUs searched (only peridomicile) and 108 found infested (28.2%). Infestation of localities: 53% before, 39% after (McNemar OR 0.5, 95%CI 0.3–1.02) [18] Time-series (1984–2006) Mainly Deltamethrin, fumigant canisters Ti Argentina (Dry Chaco) Infestation rates, ∼300 DUs Pre-treatment infestation 88%; 6 mo after 0%; recovery to pre-treatment levels in 5–7 yr; new interventions (community-based surveillance and selective control) reduce infestation to 25% 4 yr later; thereafter, and for 7 more yr, infestation remains ∼10% on average [5], [97] Time-series (1980–2000) National control programme Mainly Ti (partly*) Argentina (all ecoregions north of parallel 46S) Overall DU infestation rates ∼30% infested DUs in 1980; >6% in 1992; 100,000 DUs/yr between 1991 and 2000; >820,000 DUs were under surveillance by 2000 [97] Time-series (1964–2000) National control programme Mainly Ti (partly*) Argentina (all ecoregions north of parallel 46S) Province-specific DU infestation rate classes The percentage of provinces with infestation rates >20% fell from 68.2% in 1964 to 60% (1982), 58.3% (1987), 22.2% (1992), and 5.5% (2000); for provinces with rates below 20%, the figures were 31.8%, 40%, 41.7%, 77.8%, and 94.4% for the same years. (N = 22, 15, 12, 18, and 18 provinces surveyed in each evaluation year) [57], [72] Before-after and follow-up at 6-mo intervals for 18 mo Lambda-cyhalothrin, housing improvement, and both combined Ti, Ts Paraguay (Humid Chaco) Infestation rates, 185 DUs initially Houses: pre-treatment: 42.3% infested; post-treatment: insecticide alone 2.4%, insecticide+housing 16.4%, housing improvement alone 3.4% (all effects reported as significant after McNemar tests). Peridomiciles: initially 13.9%; after treatments, 0%, 3.5%, and 1.7%, respectively (only the combined treatment reported as significant after McNemar tests). Infestation recovered to >6% in 18 mo. Housing improvement costs were >24 times higher than those of insecticide [98] Time-series (1977–2000) Mainly pyrethroids Mainly Ti, Ts Paraguay (Dry and Humid Chaco, Alto Paraná Atlantic Forests, Paraná Flooded Savanna) DU infestation rates Overall infestation fell from 39.5% (1977) to 14% (1985) and 10% (1996); assessment of ∼170,000 DUs in 1999–2001 yielded an infestation rate of 0.73%, but much higher rates (∼37%) are common in indigenous communities of the Chaco [99] Before-after (2 surveys) National control programme Ti*, Trv Uruguay (Uruguayan Savanna) Infestation rates, ∼240,000 DUs Pre-intervention: overall rate 2.4% (up to 6.3% in 1 department); by 1992, overall 0.5% (up to 2.7%); by 1999, overall rate 0.1% (up to 0.7%). Ti was virtually eradicated from the country [100] Before-after HCH (2 rounds) Ti* Chile (Valdivian Temperate Forests, Chilean Matorral) Infestation rates, >32,700 DUs in 199 localities Observed infestation: pre-treatment 3%, post-treatment 0.3%. Infestation as reported by dwellers: pre-treatment 18.7%, post-treatment 3% [101] Time-series (1982–95) “Pyrethroids”, with no specification Ti* Chile (Chilean Matorral) DU infestation rates, ∼480 DUs per assessment Pre-intervention (1982): 73.3% of DUs infested; 1992, 24.1%; 1993, 3.9%; 1994, 2.8%; 1995, 4%. (Community-based surveillance started in 1992 after a massive spraying campaign [1988–91]) [102] Before-after National control programme Ti* Chile (Valdivian Temperate Forests, Chilean Matorral) DU infestation rates Pre-intervention overall rate was >35% in 1980; systematic control and surveillance from 1993 onwards reduced infestation to 60% by NR. (Unclear data presentation precluded further analyses) [32] NR vs. AS Mainly Ts, Pm Brazil (Serra do Mar Coastal Forests, Alto Paraná Atlantic Forests, Cerrado) Detection events in variable DU numbers from 1990 to 1995 Houses: 1990–91, OR 7.2, 95%CI 6.1–8.6, N>31,000; 1992–93: OR 5.8, 95%CI 5–6.7, N>47,500; 1994–95: OR 4.1, 95%CI 3.5–4.8, N = 36,500. Peridomiciles: 1990–91, OR 2.6, 95%CI 2.4–2.9, N∼28,000; 1992–93: OR 2.6, 95%CI 2.4–2.8, N∼43,500; 1994–95: OR 2.15, 95%CI 1.96–2.4, N>33,600. (Analyses assume that all observations are independent, which was likely the case in most instances) [132] NR vs. ASfo Ti Argentina (Dry Chaco) Detection events in 98 DUs (1993–96) Houses: McNemar OR 7, 95%CI 2.1–23.5. Peridomestic areas: McNemar OR 0.2, 95%CI 0.08–0.5 (i.e., ASfo performed better than NR at detecting peridomestic infestation) [107] NR vs. AS and DDgn Mainly Rp, also Tmac, Pg, Rpic Venezuela (Llanos) Detection events in 550 DUs NR vs. AS: McNemar P 1 indicate a positive effect of the first method in the comparison; see Table 2 for details. Vector-detection devices Several ‘passive’ vector surveillance methods have been devised and tested over the years. As defined here, they differ from the traditional, ‘active’ surveillance approach in that control programme agents do not search the whole residence to determine whether it is infested; instead, they rapidly check for bugs (or their traces) in a ‘detection device’. Table 3 summarises the main results of major comparative studies [20]–[22], [26]–[28], [130], [132], [134]–[140]. In general, the sensitivity of vector-detection devices does not seem to be superior to that of active searches, but (i) both methods appear to complement each other, with only one of them revealing infestation in many instances (see also ref. [141]), and (ii) the costs of the passive approach are, in general, lower (but see ref. [28]). Several studies with small sample sizes favour sensing devices, whereas the results of larger trials tend to show that they perform equally or worse than active searches (Figure 4). The evidence in relation to vector-detection devices remains therefore inconclusive, and further research is needed; below (Conclusions and outlook) we provide methodological suggestions to this end. 10.1371/journal.pntd.0001207.g004 Figure 4 Detection of Chagas disease vectors by vector-detection devices vs. alternative methods: estimated odds ratios and 95% confidence intervals. AS, active searches by vector control staff (ASfo, using a flushing-out agent; ASkd, using full insecticide application to ‘knock-down’ the bugs); DD, vector-detection devices (DDgn, Gómez-Núñez boxes; DDmb, ‘María’ boxes; DDb, box; DDps, paper sheet; DDp, plastic boxes); (p), results in the peridomestic area; the reference number and sample size are indicated in parentheses; studies were ranked by mean effect size; effects are significant at the 95% level when the CI does not cross the dashed line; point estimate values >1 indicate a positive effect of the first method in the comparison; see Table 3 for details. 10.1371/journal.pntd.0001207.t003 Table 3 Chagas disease vector surveillance: performance of different vector-detection devices across regions and triatomine species. Ref. Comparison Vectors Setting Units, size Main results, comments and caveats [135] DDgn vs. AS (nd) Rp Venezuela (La Costa Xeric Shrublands, Llanos) Detection events, 42 DUs, 5 monthly assessments Overall, DDgn were about 7.5 times more likely to detect infestation than AS (95%CI ∼1.7–33) (Approximate values taken from detection rates averaged over assessments) [136] DDgn vs. AS (nc) Ti Brazil (Alto Paraná Atlantic Forests, Serra do Mar Coastal Forests) Detection events, 27 houses and peridomestic annexes McNemar OR 1.25, 95%CI 0.34–4.7; in 5 cases, only DDgn detected infestation, and in 4 cases only AS did so [137] DD vs. AS (nc) Ts Brazil (Cerrado) Detection events, 72 houses and peridomestic annexes McNemar OR 0.24, 95%CI 0.09–0.63; in 21 cases, only AS detected infestation, and in 5 cases only DD did so [130] DDgn vs. AS (c) Ti Chile (Valdivian Temperate Forests, Chilean Matorral) Detection events in 43 DUs known to be infested by combining AS, DDgn and NR McNemar OR 6, IC95% 1.3–26.8. This positive effect of DDgn on detection only became apparent after several weeks of DDgn operation [138] DDgn vs. ASfo (nc/c) Ti Brazil (Cerrado, Atlantic Dry Forests) Detection events, 104 DUs DDgn performed significantly worse than ASfo: McNemar OR 0.06, 95%CI 0.014–0.25 [139] DDgn vs. AS (nc/c) Pm Brazil (Bahia Interior Forests) Detection events, 247 DUs DDgn performed significantly worse than AS: McNemar OR 0.26, 95%CI 0.11–0.6 [20] DDmb vs. ASfo (nc) Ti Argentina (Dry Chaco) Detection events, 38 DUs ASfo performed slightly better than DDmb (McNemar OR 0.5, 95%CI 0.13–2); Wisnivesky-Colli et al. [29] suggest that DDmb costs are 4 times lower [28] DDmb vs. AS (c) Ts Brazil (Atlantic Dry Forests, Caatinga, Cerrado, Bahia Interior Forests) Detection events, 225 DUs Infestation rates ascertained with DDmb were about one order of magnitude lower than those reported by control programme agents using AS. AS-based surveillance costs were estimated to be ∼1/4 of those of the DDmb-based strategy, mainly because of the need for several visits per year to check the devices [21] DDsf vs. DDmb (nd) Ti Argentina (Dry and Humid Chaco) Detection events, 63 DUs McNemar OR 14, IC95% 1.8–107. DDsf cheaper than DDmb [27] DDb and DDps vs. ASfo (nc) Ti Argentina (Dry Chaco) Detection events, 45 DUs DDb vs. ASfo: McNemar OR 9, 95%CI 1.14–71. DDps vs. ASfo: OR 3.5, 95%CI 0.73–16.9 [132] DDb vs. ASkd (c) Ti Argentina (Dry Chaco) Detection events, 60 DUs After 1 yr of DD operation: McNemar OR 4.5, 95%CI 1.5–13.3. After 2 yr of DD operation: McNemar OR 1.9, 95%CI 0.7–4.7. The results suggested that AS sensitivity depended on vector density – as measured by the number of faecal streaks in DDb. A previous trial [141] suggested that ASfo perform better than ASkd (McNemar OR 5, 95%CI 1.5–17.3), but bug removal by ASfo may have distorted subsequent ASkd results [134] DDp vs. AS (nc) Ti Argentina (Dry Chaco) Detection events, 56 peridomestic structures After 11 mo of DDp operation: McNemar OR 6.3, 95%CI 1.9–21.4. The cost of DDp was also lower [22] DDtb vs. AS (nc) Ti Argentina (Dry Chaco) Detection events, 51 peridomestic structures No differences in performance, but DDtb cost said to be about 12–20% that of AS [26] DDgn and DDps vs. AS (nc) Rec Peru (Peruvian Yungas, Tumbes-Piura Dry Forests) Detection events, 207 DUs in 19 localities DDgn vs. AS: McNemar OR 11.1, 95%CI 3.3–33.3; in 3 DUs infestation was only detected by AS, while in 33 DUs only the DDgn revealed bug presence. DDps and AS were similarly sensitive (McNemar OR 1.2, 95%CI 0.5–2.7) but complemented each other (infestation detected by just one method in 22 DUs) [140] DDmb vs. AS (nc) Mainly Td Nicaragua (Central American Dry Forests) Detection events, 99 DUs in 2 communities DDmb non-significantly more sensitive (McNemar OR 1.9, 95%CI 0.95–3.85); however, AS detect infestation in 12 DUs negative by DDmb Ref., reference; in the “Comparison” column, letters in parentheses indicate whether the study area was (c) or was not (nc) under chemical vector control; (nc/c) indicates that some, but not all, houses had been recently sprayed, and (nd) that no data on spraying were provided; AS, active searches by vector control staff (ASfo, using a flushing-out agent, generally a low-concentration pyrethroid solution; ASkd, using full insecticide application to ‘knock-down’ the bugs); DD, vector-detection devices (DDgn, Gómez-Núñez boxes; DDmb, ‘María’ boxes; DDsf, ‘Santa Fe’ boxes; DDb, box; DDps, paper sheet; DDp, plastic boxes; DDtb ‘tetra-brick’ recycled boxes; whenever several designs [or an undescribed one] were used, no specification is given); Rp, Rhodnius prolixus; Ti, Triatoma infestans; Ts, Triatoma sordida; Pm, Panstrongylus megistus; Rec, Rhodnius ecuadoriensis; mo, month(s); yr, year(s). In the “Setting” column, the ecoregions included in each study are given in parentheses. Discussion In the long run, Chagas disease prevention will depend on keeping households free of T. cruzi vectors [60], [116], [142]. Insecticide-based control campaigns have been extremely successful, but there is compelling evidence that persistent reinfestation of a fraction of treated households is the pattern to be expected across Latin America; reinfestation, in turn, can result in disease transmission re-emergence [18], [105], [106], [143], [144]. These well-supported findings clearly substantiate the view that long-term vector surveillance will be critical for the interruption of Chagas disease transmission [5], [7], [18], [35], [142], [145], [146]. Entomological surveillance primarily aims at detecting (then eliminating) household infestation foci; it thus allows for monitoring reinfestation trends in areas under control [5], [92], [94], [95], [147]–[151]. This is of fundamental importance for both (i) eliminating residual foci of introduced species targeted for local eradication and (ii) keeping reinfestation by native species at levels below disease transmission thresholds [73], [115], [152], [153]. We note, however, that ‘native’ vector species may be equally or more efficient than introduced ones at transmitting T. cruzi, and that even the most notorious ‘primary’ vectors, T. infestans and Rhodnius prolixus, are native (and reinfest treated households) [18], [143], [154]–[158] in their original ranges. Thus, entomological surveillance has a major role to play in most of Latin America even after introduced vector populations have been eliminated; in areas under surveillance, rapid diagnostic tests could be used to discover residual or re-emergent transmission foci [142]. But in order to attain these goals, vector detection must be as effective as possible, and the evidence we have reviewed shows that available vector-detection techniques all work far from perfectly. What would be, then, the best strategy to meet the permanent challenge of detecting reinfestation? Our appraisal yields strong support to the view that notification of suspect vectors by residents is the most sensitive among the several detection approaches tested to date – and that it is also probably the cheapest. Furthermore, the difference in performance seems to widen as vector population density declines, which is the typical situation in post-control settings. Such an austere ‘participatory’ strategy signals the minimum degree of community involvement required to effectively enhance surveillance: residents are just asked to report suspect insects found in their homes, and a response is mounted by professional staff, often related to decentralised health services [142], [154], [159], [160], to eliminate infestation when needed [18], [145], [161]. An educational/communication component tailored to the social-cultural background of the community is obviously required to stimulate notification [4], [35], [162], [163], but our review suggests that very simple interventions can be effective enough. Perhaps the main challenge here is to sustain community awareness in the face of even rarer infestation events; continuous education, a clearly defined channel for communication between residents and control agents, and an opportune response to any notification (including those involving insects other than triatomines) are probably the key to long-term success [35], [73], [152], [159], [164]–[166]. This is not to say that more sophisticated approaches would not perhaps bring further benefits to people living under risk conditions. For instance, we found that most community-based experiences in Chagas disease vector surveillance are merely utilitarian, with little or no participation of the community in the design, planning, and evaluation of interventions. Effective involvement of all stakeholders along the whole process would no doubt foster true empowerment, and this could in itself result in improved health and living standards [33], [34], [167]–[171]. Still, we underscore that, in the absence of adequate resources for comprehensive community-based programmes, stimulating vector notification by residents may suffice to boost the efficiency of entomological surveillance across highly diverse ecological and socio-economic settings. Finally, our review revealed that there is plenty of room for improvement of both methodological and reporting standards in the Chagas disease control/surveillance literature. In many cases, the results were reported incompletely and/or confusingly, sometimes precluding data extraction; in several instances, the data in the text, tables, and figures were incongruent. Indeed, just a few of the reviewed studies followed high-quality designs (e.g., with some sort of randomisation) and used sound analytical approaches, particularly in relation to the non-independence of observations; these reports tended to rely on small sample sizes and/or have limited spatial scope. Apart from the obvious need for using adequate design and analytical procedures, several guidelines for good reporting practices are readily available (e.g., the STROBE statement [172]); researchers and journal editors share the responsibility of improving the standards of published reports on Chagas disease control and prevention. Indeed, we believe that the main limitations of our review relate to the quality of the original reports, even if the breadth of our appraisal probably lightens the effects of individual study drawbacks. We did not test formally for publication bias, but deem it unlikely that any major study was overlooked; the possibility that such a bias exists should however be kept in mind when interpreting our results, particularly in relation to vector-detection devices. In an attempt to overcome possible study-level biases, we made every effort to extract and re-analyse the data in each document, without taking reported results at face value, but this does not alleviate design or data collection bias. However, we are confident that our main findings (that reinfestation by triatomines is common and widespread and that householder involvement in vector reporting enhances surveillance) are not bias-induced artefacts. We also note that our assessment focused on the initial stage of surveillance – the detection of infestation foci. The responses triggered by detection events, the monitoring of infestation trends, and the analysis and dissemination of epidemiological data are also essential components of disease surveillance [173], but their appraisal was beyond the scope of this review. Conclusions and outlook Entomological surveillance is and will remain crucial to contain Chagas disease transmission; yet, the zoonotic nature of the parasite's life cycle implies that eradication is unfeasible [1]. The enduring challenge of household reinfestation by locally native vectors can only be met by means of horizontal strategies – and these work better when the community takes on a protagonist role. Even very simple forms of participation, such as encouraging vector notification by residents, can substantially enhance the effectiveness of surveillance. Control programmes should therefore incorporate community-based approaches as a strategic asset from inception; such approaches must include a timely, professional response to every notification, and would very likely benefit from a strengthened focus on community empowerment. It must finally be emphasised that, in practice, vector detection failures are unavoidable, particularly when bug population density is low [174]. It may then be argued that infestation rates are virtually always underestimated and that, because these rates are the foremost indicator used in decision-making [175], imperfect detection can seriously misguide Chagas disease control programme management. We consequently suggest that a critical area for future research relates to the reliable estimation of vector detection probabilities. This is somewhat more difficult in the absence of a ‘gold-standard’ technique, but by no means unworkable: repeated-sampling approaches [176]–[178] readily yield detection probability estimates (with confidence intervals) that can in addition be modelled as a function of covariates – such as, for instance, alternative detection methods, different fieldwork teams, different vector species, or physically diverse ecotopes. These approaches have been successfully applied in wildlife [179] and disease ecology studies [180], [181], and can also help enhance Chagas disease vector research [182]. Supporting Information Abstract S1 Spanish and Portuguese translations of the abstract. (DOC) Click here for additional data file. Checklist S1 PRISMA checklist. (DOC) Click here for additional data file. List S1 93 documents submitted to full data extraction. (DOC) Click here for additional data file. List S2 27 documents used in partial quantitative assessments but not submitted to full data extraction. (DOC) Click here for additional data file.
Author and article information
Contributors
Audrey Lenhart: Role: Editor
Journal
Journal ID (nlm-ta): PLoS Negl Trop Dis
Journal ID (iso-abbrev): PLoS Negl Trop Dis
Journal ID (publisher-id): plos
Journal ID (pmc): plosntds
Title:
PLoS Neglected Tropical Diseases
Publisher:
Public Library of Science
(San Francisco, CA USA
)
ISSN
(Print):
1935-2727
ISSN
(Electronic):
1935-2735
Publication date
(Electronic):
18
March
2015
Publication date Collection:
March
2015
Volume: 9
Issue: 3
Electronic Location Identifier: e0003614
Affiliations
Author notes
Conceived and designed the experiments: MSG REG. Performed the experiments: MSG YMP MdPF. Analyzed the data: MSG MVC MdPF REG. Contributed reagents/materials/analysis tools: MSG YMP MVC MdPF REG. Wrote the paper: MSG MVC MdPF REG.
* E-mail:
gurtler@
123456ege.fcen.uba.ar
Article
Publisher ID: PNTD-D-14-01399DOI: 10.1371/journal.pntd.0003614
PMC ID: 4364707
PubMed ID: 25785439
SO-VID: 7f5addae-bce4-4732-942e-cee7dca3d986
Copyright statement:
Copyright @
2015
License:
This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited
History
Date
received
: 13
August
2014
Date
accepted
: 11
February
2015
Page count
Figures: 3,
Tables: 4,
Pages: 26
Funding
This study was supported by awards from Tropical Disease Research (UNICEF/PNUD/WB/WHO)(No.
A70596;
http://www.who.int/tdr), Agencia Nacional de Promoción Científica y Tecnológica (PICT 2011–2072 and PICTO-Glaxo
2011-0062;
http://www.agencia.mincyt.gob.ar), and the University of Buenos Aires (20020100100-944;
http://www.uba.ar) to REG. The funders had no role in study design, data collection and analysis, decision
to publish, or preparation of the manuscript.
Categories
Subject:
Research Article
Custom metadata
Data Availability All relevant data used in this paper is available in
S4 Table.
ScienceOpen disciplines: Infectious disease & Microbiology
Data availability:
ScienceOpen disciplines: Infectious disease & Microbiology