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Exploring the interface between diagnostics and maps of neglected parasitic diseases

Published online by Cambridge University Press:  28 March 2014

LAURA RINALDI*
Affiliation:
Section of Parasitology, Department of Veterinary Medicine and Animal Productions, University of Naples Federico II, Naples, Italy
GIUSEPPE CRINGOLI
Affiliation:
Section of Parasitology, Department of Veterinary Medicine and Animal Productions, University of Naples Federico II, Naples, Italy
*
*Corresponding author: Department of Veterinary Medicine and Animal Productions, University of Naples Federico II, Via Della Veterinaria 1, 80137 Napoli, Italy. E-mail: lrinaldi@unina.it
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Summary

Although not new, the ‘One Health’ concept is gaining progressively more importance in parasitology. Now more than ever, veterinary and human perspectives should be closely joined in diagnosis and surveillance of neglected parasitic diseases. We argue that concerted, standardized and harmonized diagnostic and surveillance strategies are needed for the control and/or elimination of animal and human neglected parasitic infections. A key challenge is to integrate parasitological data with available geospatial methods in an accessible and user-friendly framework. We discuss the capability of new diagnostic devices (e.g. Mini-FLOTAC) and geospatial technologies supported by mobile- and electronic-based approaches as one of the research priorities of the new millennium.

Type
Special Issue Article
Copyright
Copyright © Cambridge University Press 2014 

INTRODUCTION

Neglected (from the Latin neglegere = to neglect; nec = not and legere: to select) means ‘not treated with proper attention’. This term is used in human and veterinary medicine to indicate infections/diseases – mostly caused by parasites – often disregarded by the scientific community and health authorities with respect to their diagnosis and surveillance, but also research focus and/or funding.

From a public health perspective, the concept of neglected diseases usually refers to human tropical infections for which the name ‘neglected tropical diseases’ (NTDs) was coined in 2005 (thoroughly reviewed by Utzinger et al. Reference Utzinger, Becker, Knopp, Blum, Neumayr, Keiser and Hatz2012). Among the human NTDs, those caused by helminths predominate and, in particular, soil-transmitted helminths (STHs), i.e. Ascaris lumbricoides, Trichuris trichiura and hookworms (Ancylostoma duodenale and Necator americanus) are a major cause of malnutrition, anaemia and growth and mental delay (Bethony et al. Reference Bethony, Brooker, Albonico, Geiger, Loukas, Diemert and Hotez2006). STHs affect approximately 2 billion individuals worldwide and are a major public health issue in developing countries, predominantly in rural settings with inadequate sanitation especially in the poorest regions of Africa, Asia, Latin America and the Caribbean (Beaumier et al. Reference Beaumier, Gillespie, Hotez and Bottazzi2013). However, the impact of these infections is not confined to tropical settings. Globalization and global movement of people have brought STHs and other human NTDs to the attention of health systems in many ‘developed’ countries, particularly among travellers, expatriates and migrants (Utzinger et al. Reference Utzinger, Becker, Knopp, Blum, Neumayr, Keiser and Hatz2012); as an example, a recent study showed the presence of STHs in about 5% of immigrants in Naples, southern Italy (Gualdieri et al. Reference Gualdieri, Rinaldi, Petrullo, Morgoglione, Maurelli, Musella, Piemonte, Caravano, Coppola and Cringoli2011).

From a veterinarian perspective, among parasitic infections of livestock, gastrointestinal nematodes (GIN), caused by different genera of helminths (e.g. Ostertagia, Teladorsagia, Haemonchus, Trichostrongylus, Cooperia, Nematodirus, etc.) still represent a significant economic and welfare burden to the global ruminant livestock industry (Morgan et al. Reference Morgan, Charlier, Hendrickx, Biggeri, Catelan, von Samson-Himmelstjerna, Demeler, Müller, van Dijk, Kenyon, Skuce, Höglund, O'Kiely, van Ranst, de Waal, Rinaldi, Cringoli, Hertzberg, Torgerson, Wolstenholme and Vercruysse2013). However, as described above for human STHs, GIN infections in grazing ruminants are often neglected and implementation of research, diagnosis and surveillance of these parasites is still poor, mainly in the matter of standardized diagnostic methods and geographical information system (GIS)-based surveillance.

Auspiciously, matters are improving and more attention has been paid in the last few decades toward human and veterinary neglected parasitic infections. For example, over the past 30 years, increased recognition of the impact of the helminth burden on human health has led to an expansion of a number of large-scale control and elimination initiatives against these NTDs (Boatin et al. Reference Boatin, Basáñez, Prichard, Awadzi, Barakat, García, Gazzinelli, Grant, McCarthy, N'Goran, Osei-Atweneboana, Sripa, Yang and Lustigman2012). Concerning animal health, the ranking of GIN as one of the top causes of lost productivity in ruminants by the recent DISCONTOOLS programme (http://www.discontools.eu/home/index) witnesses the EU's increasing consideration of the impact of these parasites upon animal health, welfare and productivity (Vercruysse, present issue).

Veterinary and human perspectives should be united in the diagnosis and surveillance of neglected parasitic infections. Although not new, the ‘One Health’ concept – which states that ‘there should be a seamless interaction between veterinary and human medicine with clinicians, researchers, agencies and governments working together’ (Day, 2011) – is gaining more importance in parasitology. The ‘One Health’ perspective entails a strategy that addresses events at the intersection of human, domestic animal, wildlife and ecosystem health (Zhou, Reference Zhou2012) and close collaboration between veterinarians and tropical disease specialists would improve intervention measures (Demeler et al. Reference Demeler, Ramünke, Wolken, Ianiello, Rinaldi, Gahutu, Cringoli, von Samson-Himmelstjerna and Krücken2013). Hence, in the following sections we emphasize the need for concerted diagnostic and surveillance strategies for the control and/or elimination of animal and human neglected parasitic infections. We also underline that the urgent priority of the new millennium is to accelerate the development and evaluation of novel (and/or standardization of already existing) diagnostics together with harmonized mapping and monitoring systems through GIS and other geospatial tools.

ON DIAGNOSTICS AND DIAGNOSIS

Diagnosis of parasitic infections is of pivotal importance for both individual patient management and population-based studies, such as drug efficacy trials and surveillance of control programmes, in both human and veterinary public health (Cringoli et al. Reference Cringoli, Rinaldi, Maurelli and Utzinger2010).

The general principles put forth by the TDR Diagnostics Tests for infectious diseases (Banoo et al. Reference Banoo, Bell, Bossuyt, Herring, Mabey, Poole, Smith, Sriram, Wongsrichanalai, Linke, O'Brien, Perkins, Cunningham, Matsoso, Nathanson, Olliaro, Peeling and Ramsay2010) indicate that ‘To be useful, diagnostic methods must be accurate, simple and affordable for the population for which they are intended. They must also provide a result in time to institute effective control measures, particularly treatment’. Both the performance characteristics (e.g. sensitivity, specificity, reproducibility, positive predictive value, negative predictive value) and the operational features (e.g. simplicity, ease of use, user acceptability) should be considered whenever a diagnostic test is evaluated (Solomon et al. Reference Solomon, Engels, Bailey, Blake, Brooker, Chen, Chen, Churcher, Drakeley, Edwards, Fenwick, French, Gabrielli, Grassly, Harding-Esch, Holland, Koukounari, Lammie, Leslie, Mabey, Rhajaoui, Secor, Stothard, Wei, Willingham, Zhou and Peeling2012).

Regarding human NTDs, the paper by Becker et al. (Reference Becker, Vogt, Knopp, Panning, Warhurst, Polman, Marti, von Müller, Yansouni, Jacobs, Bottieau, Sacko, Rijal, Meyanti, Miles, Boelaert, Lutumba, van Lieshout, N'Goran, Chappuis and Utzinger2013) has recently provided a comprehensive overview of the reference diagnostic tests (based on microscopy, culture, immunology and molecular biology) presently available for helminths (including STHs) and other infectious pathogens causing persistent digestive disorders in the tropics. Regarding the diagnosis of neglected veterinary parasitic infections, the same approaches (microscopic-/cultural-/immunologic-/molecular-based) described in Becker et al. (Reference Becker, Vogt, Knopp, Panning, Warhurst, Polman, Marti, von Müller, Yansouni, Jacobs, Bottieau, Sacko, Rijal, Meyanti, Miles, Boelaert, Lutumba, van Lieshout, N'Goran, Chappuis and Utzinger2013) can be utilized.

In the present era of genomics, metagenomics, proteomics and bioinformatics (Roeber et al. Reference Roeber, Jex and Gasser2013), diagnosis of STHs in human and GIN in animals still relies predominantly on copromicroscopy (Cringoli et al. Reference Cringoli, Rinaldi, Maurelli and Utzinger2010; Demeler et al. Reference Demeler, Ramünke, Wolken, Ianiello, Rinaldi, Gahutu, Cringoli, von Samson-Himmelstjerna and Krücken2013) and analysis of faecal samples for the presence of helminth eggs is the most widely used diagnostic procedure both in veterinary and human parasitology. Since its foundation by C. J. Davaine in 1857, several copromicroscopic techniques have been developed, in particular quantitative methods based on faecal egg counts (FEC) to determine infection intensity through the assessment of eggs per gram of faeces (EPG).

FEC techniques are considered relatively straightforward and protocols such as the McMaster technique and the Wisconsin flotation technique in the veterinary field, and the Kato-Katz technique and the ether-based concentration method in the human field have been available (and have remained unchanged) for many years (Cringoli et al. Reference Cringoli, Rinaldi, Maurelli and Utzinger2010). However, each of these copromicroscopic techniques shows strengths and limitations. Furthermore, they vary considerably according to their performance and operational characteristics (e.g. analytic sensitivity, accuracy and precision in assessing FEC, timing and ease of use). While copromicroscopy is considered as highly specific, its sensitivity depends on the intensity of infection (Utzinger et al. Reference Utzinger, Becker, Knopp, Blum, Neumayr, Keiser and Hatz2012) and also on the detection limit of the employed technique. The recently introduced use of FLOTAC techniques (Cringoli et al. Reference Cringoli, Rinaldi, Maurelli and Utzinger2010) now theoretically allows sensitivities as low as 1 EPG, i.e. 24 times more than with a single Kato-Katz thick smear and 50 times more than with a single McMaster slide. Several studies have demonstrated that the FLOTAC technique outperformed multiple Kato-Katz thick smears and McMaster for the diagnosis and drug efficacy assessment of STH infections in different settings (e.g. Utzinger et al. Reference Utzinger, Rinaldi, Lohourignon, Rohner, Zimmermann, Tschannen, N'goran and Cringoli2008; Knopp et al. Reference Knopp, Rinaldi, Khamis, Stothard, Rollinson, Maurelli, Steinmann, Marti, Cringoli and Utzinger2009, Reference Knopp, Speich, Hattendorf, Rinaldi, Mohammed, Khamis, Mohammed, Albonico, Rollinson, Marti, Cringoli and Utzinger2011; Glinz et al. Reference Glinz, Silué, Knopp, Lohourignon, Yao, Steinmann, Rinaldi, Cringoli, N'Goran and Utzinger2010; Albonico et al. Reference Albonico, Rinaldi, Sciascia, Morgoglione, Piemonte, Maurelli, Musella, Utzinger, Ali, Ame and Cringoli2013). Furthermore, FLOTAC outperformed McMaster and Wisconsin techniques for the diagnosis and drug efficacy assessment of GIN in ruminants (Levecke et al. Reference Levecke, Rinaldi, Charlier, Maurelli, Morgoglione, Vercruysse and Cringoli2011, Reference Levecke, Rinaldi, Charlier, Maurelli, Bosco, Vercruysse and Cringoli2012; Rinaldi et al. Reference Rinaldi, Coles, Maurelli, Musella and Cringoli2011).

However, a main limitation of FLOTAC is the complexity of the technique, which involves centrifugation of the sample with a specific device, equipment that is often not available in all laboratories, especially in developing countries (Levecke et al. Reference Levecke, Rinaldi, Charlier, Maurelli, Bosco, Vercruysse and Cringoli2012). To overcome these limitations, under the ‘FLOTAC strategy’ (Fig. 1) of improving the quality of copromicroscopic diagnosis, a new simplified tool has been developed, i.e. the Mini-FLOTAC, having an analytic sensitivity of 10 EPG (Cringoli et al. Reference Cringoli, Rinaldi, Albonico, Bergquist and Utzinger2013). It is an easy-to-use and low-cost method, which does not require any expensive equipment or energy source, and can be  used to perform FEC in animals and humans (Cringoli et al. Reference Cringoli, Rinaldi, Albonico, Bergquist and Utzinger2013). It is recommended that Mini-FLOTAC (Fig. 1) be used in combination with Fill-FLOTAC (Fig. 2), a disposable sampling kit, which consists of a container, a collector and a filter. Fill-FLOTAC facilitates the performance of the first four consecutive steps of the Mini-FLOTAC technique, i.e. sample collection and weighing, homogenization, filtration and filling (Cringoli et al. Reference Cringoli, Rinaldi, Albonico, Bergquist and Utzinger2013).

Fig. 1. Devices of the ‘FLOTAC Family’: Mini-FLOTAC, FLOTAC and Fill-FLOTAC.

Fig. 2. Mini-FLOTAC (a) under the Newton NM1 compact portable microscope (note the inverted position) (b). Trichuris egg (d) visualized by a mobile phone (c) adapted to the portable microscope.

Mini-FLOTAC has been already validated in veterinary parasitology for the diagnosis of helminths (e.g. ascarids, hookworms, trichurids, gastrointestinal nematodes) in pets and livestock (Cringoli et al. Reference Cringoli, Rinaldi, Albonico, Bergquist and Utzinger2013; Rinaldi et al. in press). Concerning human parasitic infections, recent experiences from the field in India and Tanzania suggested that Mini-FLOTAC is a valid, sensitive and potentially low-cost alternative technique that could be used in resource-limited settings – particularly for STH diagnosis (Barda et al. Reference Barda, Ianniello, Salvo, Sadutshang, Rinaldi, Cringoli, Burioni and Albonico2013a, Reference Barda, Rinaldi, Ianniello, Zepherine, Salvo, Sadutshang, Cringoli, Clementi and Albonicob, Reference Barda, Zepherine, Rinaldi, Cringoli, Burioni, Clementi and Albonicoc). The advantages of Mini-FLOTAC compared with Kato-Katz, which is the WHO standard recommended technique, is that it can be performed both on fresh and preserved stool samples. This will allow the samples to be processed in subsequent days from their collection with a more efficient quality control. Detailed tutorials of the Mini-FLOTAC techniques on fresh and fixed faeces can be found on the following websites: http://www.youtube.com/watch?v=61C_bpBPbyg (Mini-FLOTAC technique–fresh faeces) and http://www.youtube.com/watch?v=hjMn6mepv_s (Mini-FLOTAC technique–fixed faeces).

It is our hope that further validations of Mini-FLOTAC for diagnosis of helminths parasitizing both animals and humans in different epidemiological settings will demonstrate that this new device meets the standards of a quality-ASSURED (affordable, sensitive, specific, user-friendly, rapid and robust, equipment-free, deliverable) diagnostic test.

LIMITATIONS AND FUTURE OF COPROMICROSCOPIC TECHNIQUES

Although widely used for diagnosis of intestinal parasites, it is well known that copromicroscopy is prone to a number of shortcomings (Utzinger et al. Reference Utzinger, Becker, Knopp, Blum, Neumayr, Keiser and Hatz2012).

First, there is a clear lack of standardization of copromicroscopic techniques and usually each lab uses ‘its own’ method mostly based on the ‘lab traditions’ rather than on the performance or operational characteristics of the technique. However, it is important to underline that different factors may influence the performance of any copromicroscopic technique, especially those based on flotation (e.g. McMaster, Wisconsin, FLOTAC and Mini-FLOTAC) and sedimentation. These can include the choice of fixative used for faecal preservation, the duration of faecal preservation before analyses, the selection of the flotation solution, the concurrent use of ether and many other factors. Therefore, inter-laboratory standardization of techniques, as well as internal and external quality control for parasitological data, are strongly required in human and veterinary parasitology.

Second, the results of any copromicroscopic technique strongly depend on the accuracy of laboratory procedures but also on the experience of the laboratory technicians reading the microscopic fields (Becker et al. Reference Becker, Vogt, Knopp, Panning, Warhurst, Polman, Marti, von Müller, Yansouni, Jacobs, Bottieau, Sacko, Rijal, Meyanti, Miles, Boelaert, Lutumba, van Lieshout, N'Goran, Chappuis and Utzinger2013). Hence, the reliable identification of parasitic infections requires in-depth training for specimen preparation, and expertise and experience for subsequent microscopic examination (Utzinger et al. Reference Utzinger, Becker, Knopp, Blum, Neumayr, Keiser and Hatz2012). Therefore, the ‘human’ factor (i.e. the hands and eyes of technicians) is of fundamental importance for copromicroscopic analyses compared with other diagnostic approaches (i.e. immunological or molecular methods).

Third and most importantly, the main limitation of copromicroscopy is the time and cost to conduct copromicrocopic analysis (in particular FEC) on a representative number of individuals. However, this limitation can be overcome by performing FEC on pooled samples, in which equal amounts of faeces from several individuals are mixed together and a single FEC is used as an index of group mean FEC (Morgan et al. Reference Morgan, Cavill, Curry, Wood and Mitchell2005). Recently, such pooling approaches have been applied to fresh stool samples using the McMaster technique and to fixed faecal samples using the chlorazol black dye for the detection of intestinal parasites in humans and results indicated that this is an efficient and potentially cost-effective strategy (Gaafar, Reference Gaafar2011; Mekonnen et al. Reference Mekonnen, Meka, Ayana, Bogers, Vercruysse and Levecke2013). Similarly, also in the veterinary field, pooling sheep faecal samples using Mini-FLOTAC has been demonstrated as a rapid procedure that holds promise as a valid strategy for assessing GIN infections in ruminants (Rinaldi et al. in press).

Together with pooling, one of the challenges of the future of copromicroscopy is to perform diagnosis of neglected parasitic infections directly in the field by using field portable kits including the new generation of field microscopes. This aspect has had a long track record of development with prior microscope models. As an example, Stothard et al. (Reference Stothard, Kabatereine, Tukahebwa, Kazibwe, Mathieson, Webster and Fenwick2005) reported a field evaluation of a handheld microscope for diagnosis of intestinal schistosomiasis in Ugandan schoolchildren. This handheld microscope was suggested as a pragmatic alternative to the compound microscope, playing an important role in the collection of prevalence data to better guide anthelmintic drug delivery and also empowering the diagnostic capacity of peripheral health centres where compound microscopes are few or absent (Stothard et al. Reference Stothard, Kabatereine, Tukahebwa, Kazibwe, Mathieson, Webster and Fenwick2005). More recently, Bogoch et al. (Reference Bogoch, Andrews, Speich, Utzinger, Ame, Ali and Keiser2013) described the proof of concept that a mobile phone can be converted into a microscope for the point-of-care diagnosis of STHs in resource-constrained settings. It is therefore evident that using portable field microscopes without the need for electricity would be the optimal solution for the diagnosis of helminths in health periphery (for STH) and on farms (for GIN). A closed diagnostic device such as Mini-FLOTAC could be easily ‘attachable’ to such kinds of microscopes supplied with adaptors for mobile phone camera (Fig. 2).

ON MAPPING AND GEOSPATIAL TOOLS

There is increasing consensus that standardized diagnostic techniques should be linked to geospatial tools (e.g. GIS, remote sensing, virtual globes, spatial statistics, ecological niche models) for the integrated mapping, monitoring and surveillance of neglected parasitic infections in humans and animals (Solomon et al. Reference Solomon, Engels, Bailey, Blake, Brooker, Chen, Chen, Churcher, Drakeley, Edwards, Fenwick, French, Gabrielli, Grassly, Harding-Esch, Holland, Koukounari, Lammie, Leslie, Mabey, Rhajaoui, Secor, Stothard, Wei, Willingham, Zhou and Peeling2012; Cringoli et al. Reference Cringoli, Rinaldi, Albonico, Bergquist and Utzinger2013). Now more than ever, we can use the old adage that a picture is worth more than a thousand words (Utzinger et al. Reference Utzinger, Rinaldi, Malone, Krauth, Kristensen, Cringoli and Bergquist2011). Presentation of parasitological results based on interactive, computer-generated maps represents a straightforward way of visualizing large numbers of datasets in a geographical context that could have different spatial scales (local, national, regional and global) (Bergquist and Tanner, Reference Bergquist and Tanner2012; Cringoli et al. Reference Cringoli, Rinaldi, Albonico, Bergquist and Utzinger2013). Geospatial tools have now become an integral part of epidemiology and surveillance by driving systematic collection, analysis and interpretation of health data (Malone and Bergquist, Reference Malone and Bergquist2012; Zhou et al. Reference Zhou, Bergquist and Tanner2013). Translational research has rapidly evolved from approaches requiring specialists in GIS and remote sensing technology to a level where it has become a normal part of health planning and implementation of national disease control programmes (Malone and Bergquist, Reference Malone and Bergquist2012).

Regarding human NTDs, the paper by Clements et al. (Reference Clements, Reid, Kelly and Hay2013) has recently provided a comprehensive overview of the geospatial instruments (along with the application, advantages and disadvantages of each of them) relevant to achieve malaria elimination. The same geospatial approaches can be translated to other neglected parasitic infections of public health and veterinary relevance such as STHs and GIN.

Representation of epidemiological data in the form of a map facilitates interpretation, synthesis and recognition of any changing frequency and pattern of infected cases and the appearance of clusters of parasitological phenomena. Moreover, maps are a convenient tool to foster discussion and dialogue among different stakeholders (Clements et al. Reference Clements, Reid, Kelly and Hay2013; Cringoli et al. Reference Cringoli, Rinaldi, Albonico, Bergquist and Utzinger2013). However, the use of GIS and other geospatial tools for disease mapping, does by no means overcome the major concern of any empirical research, namely (parasitological) data quality. It is noteworthy to stress that disease maps are indissolubly intertwined with diagnostics and further research on geospatial technology and links with standardized diagnostic techniques must take place (Cringoli et al. Reference Cringoli, Rinaldi, Albonico, Bergquist and Utzinger2013). The use of different diagnostics (with differing sensitivity, negative predictive value and/or other performance characteristics) gives rise to distribution maps that can change substantially. As an example, we used the data from our paper by Gualdieri et al. (Reference Gualdieri, Rinaldi, Petrullo, Morgoglione, Maurelli, Musella, Piemonte, Caravano, Coppola and Cringoli2011) where 514 immigrants to Naples (southern Italy) were tested comparing the FLOTAC and the ethyl acetate concentration techniques; combined results of the two techniques served as a diagnostic ‘gold standard’. Regarding STHs, eggs of T. trichiura were found in 20 (3·9%) immigrants when examined by FLOTAC and only in 2 (0·4%) subjects when examined by the concentration technique (Gualdieri et al. Reference Gualdieri, Rinaldi, Petrullo, Morgoglione, Maurelli, Musella, Piemonte, Caravano, Coppola and Cringoli2011). By using this dataset, combined with GIS, the parasitological data were geo-referenced and two distribution maps for T. trichiura were obtained, using the results obtained by FLOTAC (Fig. 3) and by the ethyl acetate concentration (Fig. 4) techniques. From the analysis of these data, it is evident that the map in Fig. 4 is a biased sub-set of the ‘true’ T. trichiura distribution showed in Fig. 3.

Fig. 3. Map of positivity to Trichuris trichiura by FLOTAC. Geo-referenced parasitological results of immigrants tested for intestinal parasites in Naples, southern Italy (data from Gualdieri et al. Reference Gualdieri, Rinaldi, Petrullo, Morgoglione, Maurelli, Musella, Piemonte, Caravano, Coppola and Cringoli2011).

Fig. 4. Map of positivity to Trichuris trichiura by the ethyl acetate technique. Geo-referenced parasitological results of immigrants tested for intestinal parasites in Naples, southern Italy (data from Gualdieri et al. Reference Gualdieri, Rinaldi, Petrullo, Morgoglione, Maurelli, Musella, Piemonte, Caravano, Coppola and Cringoli2011).

Therefore, a key challenge for human and animal neglected parasitic infections is to integrate routinely collected data with available geospatial methods in an accessible and user-friendly framework (Clements et al. Reference Clements, Reid, Kelly and Hay2013; Morgan et al. Reference Morgan, Charlier, Hendrickx, Biggeri, Catelan, von Samson-Himmelstjerna, Demeler, Müller, van Dijk, Kenyon, Skuce, Höglund, O'Kiely, van Ranst, de Waal, Rinaldi, Cringoli, Hertzberg, Torgerson, Wolstenholme and Vercruysse2013). Compared with the past decades, the situation is improving with the development of open-source software for GISs (e.g. QGIS), online data warehouses containing freely available geospatial data and increased training opportunities in geospatial sciences.

Furthermore, the ability to define the distribution of infections at regional, national and sub-national levels has been enhanced greatly by the increased availability of good quality survey data combined with the use of sophisticated model-based geostatistics, enabling spatial prediction in unsampled locations (Magalhães et al. Reference Magalhães, Clements, Patil, Gething and Brooker2011). Hence, Bayesian geostatistical models are increasingly being used in human and veterinary epidemiological studies to estimate parasitic risk profiling at high spatial resolution (e.g. Magalhães et al. Reference Magalhães, Clements, Patil, Gething and Brooker2011; Catelan et al. Reference Catelan, Rinaldi, Musella, Cringoli and Biggeri2012; Chammartin et al. Reference Chammartin, Scholte, Guimarães, Tanner, Utzinger and Vounatsou2013; Scholte et al. Reference Scholte, Schur, Bavia, Carvalho, Chammartin, Utzinger and Vounatsou2013).

Also, WebGIS tools have become increasingly popular as a result of advances in computer technologies, improved and established geographical standards which have helped the dissemination of spatial data to different audiences, and the shift from expert tools to community-based tools that are accessible to a wider range of users (Kienberger et al. Reference Kienberger, Hagenlocher, Delmelle and Casas2013). Closely related to (simple) web-based GIS tools are spatial decision support systems (SDSS), i.e. interactive GIS-based platforms (including integrated database management systems) that are designed to support place-based decision making at the various stages of a planning process (Duncombe et al. Reference Duncombe, Clements, Hu, Weinstein, Ritchie and Espino2012).

In order to stimulate the exchange of information on application of geospatial tools in health research through publications, international conferences, workshops and training courses, GnosisGIS (www.gnosisgis.org) was founded in 2000 as ‘Network On Snail-borne Infections with special reference to Schistosomiasis (GnosisGIS)’. The initial aim was to develop and consolidate collaboration dedicated to validation and use of GIS and other geospatial tools to control schistosomiasis and other snail-borne infections. However, its scope has since been expanded to include other infectious and parasitic diseases of medical and veterinary importance. In 2005 the acronym GnosisGIS was kept, but the network was renamed ‘Global Network for Geospatial Health’. In August 2013, the name was officially changed to ‘International Society for Geospatial Health–GnosisGIS’. It is a dynamic, multinational and multidisciplinary scientific society, bringing together veterinarians, medical doctors, biologists, parasitologists, climatologists, geographers, computer scientists and statisticians. GnosisGIS strives to advance the use of geospatial tools in veterinary and public health. Toward this end, one of the main products of GnosisGIS is its official journal, Geospatial Health, an international, peer-reviewed scientific journal, founded in 2006 (Utzinger et al. Reference Utzinger, Rinaldi, Malone, Krauth, Kristensen, Cringoli and Bergquist2011). Recently, as a unique feature of Geospatial Health, a new section predominantly based on visual presentations, including brief video clips, was introduced in 2010 under the banner of ‘vHealth’ (visual health) (Bergquist and Tanner, Reference Bergquist and Tanner2012). We are convinced that the visual approach will facilitate communication with the wide variety of stakeholders involved in research today, e.g. government offices, funding agencies, etc. However, we should keep in mind that working with policy makers and stakeholders to use the outputs of geospatial analysis in a way that helps their ability to make improved evidence-based decisions will be a very complex challenge (Clements et al. Reference Clements, Reid, Kelly and Hay2013).

CONCLUSIONS AND PERSPECTIVES

There is a broad political commitment towards large-scale control and progressive elimination of a wide variety of parasitic diseases; however, there are some worrying signs for the future, particularly the anticipated declines in funding and coverage of key interventions, and the paucity of novel diagnostic tools and surveillance strategies (Cringoli et al. Reference Cringoli, Rinaldi, Albonico, Bergquist and Utzinger2013). Importantly, ‘improve existing/develop novel diagnostic test’, and ‘update and share data platforms to optimize data management, analysis and modelling (using geospatial technologies), integrating scientists, stake holders and end-users’ are among the priorities identified by the TDR reference group on helminth infections (Boatin et al. Reference Boatin, Basáñez, Prichard, Awadzi, Barakat, García, Gazzinelli, Grant, McCarthy, N'Goran, Osei-Atweneboana, Sripa, Yang and Lustigman2012). Furthermore, for the upcoming calls of Horizon 2020 research funding, transdisciplinary research is strongly recommended by the European Commission. We have already emphasized the need for integrating sound epidemiological designs with innovative diagnostic tools and strategies and high-resolution geospatial tools for mapping neglected parasitic infections of animal and humans considering the ‘One-Health’ perspective (Cringoli et al. Reference Cringoli, Rinaldi, Albonico, Bergquist and Utzinger2013). Recognizing these challenges, standardization of quality procedures and innovating, validating and applying new tools and strategies will foster and sustain long-term control of neglected parasitic infections of human and animals. Indeed, effective and timely public health responses depend upon the ability of health systems to provide accurate and timely information for action (Zhou et al. Reference Zhou, Bergquist and Tanner2013). Use of new technologies supported by mobile- and electronic-based (m- and e-health) approaches as well as improved and more sensitive strategies of diagnosis is considered one of the research priorities to strengthen the surveillance systems within national control/elimination programmes of NTDs (Zhou et al. Reference Zhou, Bergquist and Tanner2013), including neglected parasitic infections of animals and humans.

ACKNOWLEDGEMENTS

The authors acknowledge Drs Antonio Bosco, Ida Guariglia, Davide Ianniello, Maria Paola Maurelli, Maria Elena Morgoglione, Vincenzo Musella, Mario Parrilla, Saverio Pennacchio, Paola Pepe and Mirella Santaniello for their enthusiastic participation in the application and validation of the Mini-FLOTAC technique. The authors acknowledge the help and support from Mr Mike Broderick FRMS, DipM, MCIM (Newton Microscopes Ltd) in the development of the microscopy approach to the Mini-FLOTAC protocol.

FINANCIAL SUPPORT

The authors acknowledge GLOWORM, a project funded by the European Union Seventh Framework Programme FP7-KBBE-2011-5 under grant agreement n° 288975. Laura Rinaldi acknowledges the British Society for Parasitology (BSP) for expenses at attend the 2013 Autumn Symposium on ‘Advances in Diagnostics for Infectious Diseases’.

References

REFERENCES

Albonico, M., Rinaldi, L., Sciascia, S., Morgoglione, M. E., Piemonte, M., Maurelli, M. P., Musella, V., Utzinger, J., Ali, S. M., Ame, S. M. and Cringoli, G. (2013). Comparison of three copromicroscopic methods to assess albendazole efficacy against soil-transmitted helminth infections in school-aged children on Pemba Island. Transactions of the Royal Society of Tropical Medicine and Hygiene 107, 493501.CrossRefGoogle ScholarPubMed
Banoo, S., Bell, D., Bossuyt, P., Herring, A., Mabey, D., Poole, F., Smith, P. G., Sriram, N., Wongsrichanalai, C., Linke, R., O'Brien, R., Perkins, M., Cunningham, J., Matsoso, P., Nathanson, C. M., Olliaro, P., Peeling, R. W., Ramsay, A. and TDR Diagnostics Evaluation Expert Panel (2010). Evaluation of diagnostic tests for infectious diseases: general principles. Nature Reviews Microbiology 8, S17S29.Google Scholar
Barda, B., Ianniello, D., Salvo, F., Sadutshang, T., Rinaldi, L., Cringoli, G., Burioni, R. and Albonico, M. (2013 a). “Freezing” parasites in pre-Himalayan region, Himachal Pradesh: experience with mini-FLOTAC. Acta Tropica 130C, 1116.Google Scholar
Barda, B. D., Rinaldi, L., Ianniello, D., Zepherine, H., Salvo, F., Sadutshang, T., Cringoli, G., Clementi, M. and Albonico, M. (2013 b). Mini-FLOTAC, an innovative direct diagnostic technique for intestinal parasitic infections: experience from the field. PLoS Neglected Tropical Diseases 7, e2344.Google Scholar
Barda, B., Zepherine, H., Rinaldi, L., Cringoli, G., Burioni, R., Clementi, M. and Albonico, M. (2013 c). Mini-FLOTAC and Kato-Katz: helminth eggs watching on the shore of Lake Victoria. Parasites and Vectors 31, e2344.Google Scholar
Beaumier, C. M., Gillespie, P. M., Hotez, P. J. and Bottazzi, M. E. (2013). New vaccines for neglected parasitic diseases and dengue. Translational Research 162, 144155.Google Scholar
Becker, S. L., Vogt, J., Knopp, S., Panning, M., Warhurst, D. C., Polman, K., Marti, H., von Müller, L., Yansouni, C. P., Jacobs, J., Bottieau, E., Sacko, M., Rijal, S., Meyanti, F., Miles, M. A., Boelaert, M., Lutumba, P., van Lieshout, L., N'Goran, E. K., Chappuis, F. and Utzinger, J. (2013). Persistent digestive disorders in the tropics: causative infectious pathogens and reference diagnostic tests. BMC Infectious Diseases 24, 37.Google Scholar
Bergquist, R. and Tanner, M. (2012). Visual approaches for strengthening research, science communication and public health impact. Geospatial Health 6, 155156.CrossRefGoogle ScholarPubMed
Bethony, J., Brooker, S., Albonico, M., Geiger, S. M., Loukas, A., Diemert, D. and Hotez, P. J. (2006). Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367, 15211532.Google Scholar
Boatin, B. A., Basáñez, M. G., Prichard, R. K., Awadzi, K., Barakat, R. M., García, H. H., Gazzinelli, A., Grant, W. N., McCarthy, J. S., N'Goran, E. K., Osei-Atweneboana, M. Y., Sripa, B., Yang, G. J. and Lustigman, S. (2012). A research agenda for helminth diseases of humans: towards control and elimination. PLoS Neglected Tropical Diseases 6, e1547.Google Scholar
Bogoch, I. I., Andrews, J. R., Speich, B., Utzinger, J., Ame, S. M., Ali, S. M. and Keiser, J. (2013). Mobile phone microscopy for the diagnosis of soil-transmitted helminth infections: a proof-of-concept study. American Journal of Tropical Medicine and Hygiene 88, 626629.Google Scholar
Catelan, D., Rinaldi, L., Musella, V., Cringoli, G. and Biggeri, A. (2012). Statistical approaches for farm and parasitic risk profiling in geographical veterinary epidemiology. Statistical Methods for Medical Research 21, 531543.CrossRefGoogle ScholarPubMed
Chammartin, F., Scholte, R. G., Guimarães, L. H., Tanner, M., Utzinger, J. and Vounatsou, P. (2013). Soil-transmitted helminth infection in South America: a systematic review and geostatistical meta-analysis. Lancet Infectious Diseases 13, 507518.Google Scholar
Clements, A. C., Reid, H. L., Kelly, G. C. and Hay, S. I. (2013). Further shrinking the malaria map: how can geospatial science help to achieve malaria elimination? Lancet Infectious Diseases 13, 709718.Google Scholar
Cringoli, G., Rinaldi, L., Maurelli, M. P. and Utzinger, J. (2010). FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nature Protocols 5, 503515.CrossRefGoogle ScholarPubMed
Cringoli, G., Rinaldi, L., Albonico, M., Bergquist, R. and Utzinger, J. (2013). Geospatial (s)tools: integration of advanced epidemiological sampling and novel diagnostics. Geospatial Health 7, 399404.Google Scholar
Day, M. J. (2011). One health: the importance of companion animal vector-borne diseases. Parasite Vectors 4, 49.CrossRefGoogle ScholarPubMed
Demeler, J., Ramünke, S., Wolken, S., Ianiello, D., Rinaldi, L., Gahutu, J. B., Cringoli, G., von Samson-Himmelstjerna, G. and Krücken, J. (2013). Discrimination of gastrointestinal nematode eggs from crude fecal egg preparations by inhibitor-resistant conventional and real-time PCR. PLoS One 19, e61285.Google Scholar
Duncombe, J., Clements, A., Hu, W., Weinstein, P., Ritchie, S. and Espino, F. E. (2012). Geographical information systems for dengue surveillance. American Journal of Tropical Medicine and Hygiene 86, 753755.Google Scholar
Gaafar, M. R. (2011). Use of pooled sodium acetate acetic acid formalin-preserved fecal specimens for the detection of intestinal parasites. Journal of Clinical Laboratory Analysis 25, 217222.CrossRefGoogle ScholarPubMed
Glinz, D., Silué, K. D., Knopp, S., Lohourignon, L. K., Yao, K. P., Steinmann, P., Rinaldi, L., Cringoli, G., N'Goran, E. K. and Utzinger, J. (2010). Comparing diagnostic accuracy of Kato-Katz, Koga agar plate, ether-concentration, and FLOTAC for Schistosoma mansoni and soil-transmitted helminths. PLoS Neglected Tropical Diseases 20, e754.Google Scholar
Gualdieri, L., Rinaldi, L., Petrullo, L., Morgoglione, M. E., Maurelli, M. P., Musella, V., Piemonte, M., Caravano, L., Coppola, M. G. and Cringoli, G. (2011). Intestinal parasites in immigrants in the city of Naples (southern Italy). Acta Tropica 117, 196201.CrossRefGoogle ScholarPubMed
Kienberger, S., Hagenlocher, M., Delmelle, E. and Casas, I. (2013). A WebGIS tool for visualizing and exploring socioeconomic vulnerability to dengue fever in Cali, Colombia. Geospatial Health 8, 313316.Google Scholar
Knopp, S., Rinaldi, L., Khamis, I. S., Stothard, J. R., Rollinson, D., Maurelli, M. P., Steinmann, P., Marti, H., Cringoli, G. and Utzinger, J. (2009). A single FLOTAC is more sensitive than triplicate Kato-Katz for the diagnosis of low-intensity soil-transmitted helminth infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 347354.Google Scholar
Knopp, S., Speich, B., Hattendorf, J., Rinaldi, L., Mohammed, K. A., Khamis, I. S., Mohammed, A. S., Albonico, M., Rollinson, D., Marti, H., Cringoli, G. and Utzinger, J. (2011). Diagnostic accuracy of Kato-Katz and FLOTAC for assessing anthelmintic drug efficacy. PLoS Neglected Tropical Diseases 12, e1036.Google Scholar
Levecke, B., Rinaldi, L., Charlier, J., Maurelli, M. P., Morgoglione, M. E., Vercruysse, J. and Cringoli, G. (2011). Monitoring drug efficacy against gastrointestinal nematodes when faecal egg counts are low: do the analytic sensitivity and the formula matter? Parasitology Research 109, 953957.CrossRefGoogle ScholarPubMed
Levecke, B., Rinaldi, L., Charlier, J., Maurelli, M. P., Bosco, A., Vercruysse, J. and Cringoli, G. (2012). The bias, accuracy and precision of faecal egg count reduction test results in cattle using McMaster, Cornell-Wisconsin and FLOTAC egg counting methods. Veterinary Parasitology 188, 194199.Google Scholar
Magalhães, R. J., Clements, A. C., Patil, A. P., Gething, P. W. and Brooker, S. (2011). The applications of model-based geostatistics in helminth epidemiology and control. Advances in Parasitology 74, 267296.CrossRefGoogle ScholarPubMed
Malone, J. B. and Bergquist, N. R. (2012). Mapping and modelling neglected tropical diseases and poverty in Latin America and the Caribbean. Geospatial Health 6, S1S5.CrossRefGoogle ScholarPubMed
Mekonnen, Z., Meka, S., Ayana, M., Bogers, J., Vercruysse, J. and Levecke, B. (2013). Comparison of individual and pooled stool samples for the assessment of soil-transmitted helminth infection intensity and drug efficacy. PLoS Neglected Tropical Diseases 16, e2189.Google Scholar
Morgan, E. R., Cavill, L., Curry, G. E., Wood, R. M. and Mitchell, E. S. (2005). Effects of aggregation and sample size on composite faecal egg counts in sheep. Veterinary Parasitology 131, 7987.Google Scholar
Morgan, E. R., Charlier, J., Hendrickx, G., Biggeri, A., Catelan, D., von Samson-Himmelstjerna, G., Demeler, J., Müller, E., van Dijk, J., Kenyon, F., Skuce, P., Höglund, J., O'Kiely, P., van Ranst, B., de Waal, T., Rinaldi, L., Cringoli, G., Hertzberg, H., Torgerson, P., Wolstenholme, A. and Vercruysse, J. (2013). Global change and helminth infections in grazing ruminants in Europe: impacts, trends and sustainable solutions. Agriculture 3, 484502.CrossRefGoogle Scholar
Rinaldi, L., Coles, G. C., Maurelli, M. P., Musella, V. and Cringoli, G. (2011). Calibration and diagnostic accuracy of simple flotation, McMaster and FLOTAC for parasite egg counts in sheep. Veterinary Parasitology 177, 345352.Google Scholar
Rinaldi, L., Levecke, B., Bosco, A., Ianello, D., Pepe, P., Charlier, J., Cringoli, G. and Vercruysse, J. (2014). Comparison of individual and pooled faecal samples in sheep for the assessment of gastro-intestinal strongyle infection intensity and anthelmintic drug efficacy using McMaster and Mini-Flotac. Veterinary Parasitology (in press).Google Scholar
Roeber, F., Jex, A. R. and Gasser, R. B. (2013). Next-generation molecular-diagnostic tools for gastrointestinal nematodes of livestock, with an emphasis on small ruminants: a turning point? Advances in Parasitology 83, 267333.Google Scholar
Scholte, R. G. C., Schur, N., Bavia, M. E., Carvalho, E. M., Chammartin, F., Utzinger, J. and Vounatsou, P. (2013). Spatial analysis and risk mapping of soil-transmitted helminth infections in Brazil, using Bayesian geostatistical models. Geospatial Health 8, 97110.Google Scholar
Solomon, A. W., Engels, D., Bailey, R. L., Blake, I. M., Brooker, S., Chen, J. X., Chen, J. H., Churcher, T. S., Drakeley, C. J., Edwards, T., Fenwick, A., French, M., Gabrielli, A. F., Grassly, N. C., Harding-Esch, E. M., Holland, M. J., Koukounari, A., Lammie, P. J., Leslie, J., Mabey, D. C., Rhajaoui, M., Secor, W. E., Stothard, J. R., Wei, H., Willingham, A. L., Zhou, X. N. and Peeling, R. W. (2012). A diagnostics platform for the integrated mapping, monitoring, and surveillance of neglected tropical diseases: rationale and target product profiles. PLoS Neglected Tropical Diseases 6, e1746.CrossRefGoogle ScholarPubMed
Stothard, J. R., Kabatereine, N. B., Tukahebwa, E. M., Kazibwe, F., Mathieson, W., Webster, J. P. and Fenwick, A. (2005). Field evaluation of the Meade Readiview handheld microscope for diagnosis of intestinal schistosomiasis in Ugandan school children. American Journal of Tropical Medicine and Hygiene 73, 949955.Google Scholar
Utzinger, J., Rinaldi, L., Lohourignon, L. K., Rohner, F., Zimmermann, M. B., Tschannen, A. B., N'goran, E. K. and Cringoli, G. (2008). FLOTAC: a new sensitive technique for the diagnosis of hookworm infections in humans. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 8490.Google Scholar
Utzinger, J., Rinaldi, L., Malone, J. B., Krauth, S. J., Kristensen, T. K., Cringoli, G. and Bergquist, R. (2011). Geospatial health: the first five years. Geospatial Health 6, 137154.CrossRefGoogle ScholarPubMed
Utzinger, J., Becker, S. L., Knopp, S., Blum, J., Neumayr, A. L., Keiser, J. and Hatz, C. F. (2012). Neglected tropical diseases: diagnosis, clinical management, treatment and control. Swiss Medical Weekly 142, w13727.Google Scholar
Zhou, X. N. (2012). Prioritizing research for “One health – One world”. Infectious Diseases of Poverty 1, 1.Google Scholar
Zhou, X. N., Bergquist, R. and Tanner, M. (2013). Elimination of tropical disease through surveillance and response. Infectious Diseases of Poverty 3, 1.Google Scholar
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Fig. 1. Devices of the ‘FLOTAC Family’: Mini-FLOTAC, FLOTAC and Fill-FLOTAC.

Figure 1

Fig. 2. Mini-FLOTAC (a) under the Newton NM1 compact portable microscope (note the inverted position) (b). Trichuris egg (d) visualized by a mobile phone (c) adapted to the portable microscope.

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Fig. 3. Map of positivity to Trichuris trichiura by FLOTAC. Geo-referenced parasitological results of immigrants tested for intestinal parasites in Naples, southern Italy (data from Gualdieri et al.2011).

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Fig. 4. Map of positivity to Trichuris trichiura by the ethyl acetate technique. Geo-referenced parasitological results of immigrants tested for intestinal parasites in Naples, southern Italy (data from Gualdieri et al.2011).