Introduction

Trypanosoma cruzi (T. cruzi) is a flagellate protozoan that causes Chagas disease (CD). It is traditionally linked to rural areas of continental Latin America, where it is transmitted by a variety of bug vectors. In recent decades, the epidemiological pattern of this disease has undergone considerable changes [1]. In the endemic countries of Latin America, the regional Chagas programs are working to interrupt vector-borne and transfusional transmission, to control congenital Chagas disease and to support initiatives aimed at improving diagnosis, management and surveillance of the disease [2]. In non-endemic countries that receive immigrants from Latin America or send tourists to endemic areas, CD is an emerging disease and has become a public health problem because it can be transmitted by non-vectorial mechanisms [3], [4].

Spain is a major European host country for people from Latin America. According to the Spanish National Institute of Statistics, in 2009 more than 1.8 million immigrants from Latin America were registered, accounting for 3.85% of the total population [5]. In recent years several studies of CD in non-endemic countries [6]–[9] have focused in particular on non-vectorial transmission mechanisms such as pregnancy and childbirth [10], [11], blood transfusion [12], [13] and organ transplantation [14], [15]. However, when reviewing the literature we found little information on imported CD in non-endemic countries at the primary care level [16], which is ideal for screening the general population [17].

The clinical manifestations of chronic T. cruzi infection include the latent form (the indeterminate chronic form), which occurs in 60% of cases [18], the cardiac form [19], the digestive or cardiodigestive form, and sudden death [20]. Therefore, many diagnoses of CD are based on epidemiological suspicion rather than clinical signs and symptoms.

The objectives of the present study were (1) to assess the prevalence of Trypanosoma cruzi infection in the adult Latin American population treated at a health center in Barcelona, Spain; (2) to analyze the clinical phase of the disease; and (3) to determine whether screening for imported CD in primary care should be recommended.

Methods

Results

A total of 766 persons from continental Latin America were included in the study. The epidemiological data are presented in Table 1 and the countries of origin in Table 2.

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Table 1. Epidemiologic data.

https://doi.org/10.1371/journal.pntd.0001135.t001

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Table 2. Countries of origin.

https://doi.org/10.1371/journal.pntd.0001135.t002

Of the 766 patients analyzed, 27 were reactive to the ICT and 20 of these were reactive in cELISA, rELISA and oELISA. Also, 2 patients of the 101 tested by ICT, cELISA, and rELISa regardless of the result of the first were reactive in cELISA and rELISA. Both were also positive in oELISA, so they were considered positive.

A total of 22 patients were diagnosed with CD, corresponding to a prevalence of 2.87% (95% CI, 1.6–4.12%) in the sample studied. Of these, 21 were from Bolivia; the prevalence of CD in the subgroup of Bolivian patients studied (n = 127) was 16.53% (95% CI, 9.6–23.39%). The remaining patient was from Paraguay.

All the patients infected by T. cruzi were in the chronic phase of CD. The clinical form and the reasons why they visited the health center are presented in Table 3. Four patients (18.2%) had been previously diagnosed in the country of origin, but none of them mentioned it in the primary care visit because they thought it was a health problem proper to their country that would be unknown to the Spanish health staff (this information was obtained when they were asked for informed consent to participate in the study). None of them were aware of their clinical phase and 2 patients had received incomplete treatment.

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Table 3. Clinical phase of Chagas disease (CD) and reasons for visit.

https://doi.org/10.1371/journal.pntd.0001135.t003

Discussion

The prevalence of T. cruzi infection in the sample studied was 2.87% and in the subgroup of Bolivian patients it was 16.53%. In the medical literature we found few studies of similar characteristics to ours (involving screening of the adult Latin American population in primary care) and their results varied [29], [12] due to the heterogeneity of the populations analyzed and the distribution of CD in Latin America.

The laboratory confirmation of a clinical suspicion of CD is based on consistent results of at least 2 different immunological tests [24]. ICTs are attractive in primary care because they are easy to use in routine clinical practice and do not require sophisticated facilities or specialized staff. In the substudy that we performed in 101 patients [25], for the ICT used we found a sensitivity of 92.5% and a specificity of 96.8%. Other studies have evaluated the sensitivity and specificity of ICTs [30], [31] with similar results. The current sensitivity of ICTs must be increased so that they can be used as effective screening tests. Meanwhile, they should be combined with other methods that offer greater sensitivity [25], [31].

The highest prevalence was found among Bolivian patients, in agreement with other studies performed in Spain [9], [16] and other non-endemic countries [12], [32]. No cases were diagnosed among the Peruvian or Ecuadorian patients, who formed 45% of the sample, probably due to the heterogeneous distribution of CD in endemic countries and the lower seroprevalence of T. cruzi estimated in Peru (0.69%) and Ecuador (1.74%) [33].

An epidemiologic history of having lived in rural areas and/or adobe houses showed a significant relationship with T. cruzi infection, consistent with the dominant vector-borne transmission mechanism in the countries of origin. All patients with T. cruzi infection had heard of CD in their countries of origin and approximately 82% knew someone who was affected. These data should be taken into account for establishing CD screening criteria in immigrants from endemic zones, because mere knowledge of the disease may be considered as an indirect indicator of its presence in the region of origin.

In non-endemic countries CD screening programs have been aimed at particularly susceptible groups: in blood banks (France [34], the USA [35] and Spain [36]), and in pregnant Latin American women and their neonates (the Spanish autonomous communities of Catalonia [37] and Valencia [38]). In our study only 9.5% of the patients with T. cruzi infection had visited the health center due to clinical symptoms suggestive of CD. As it is a silent disease that has recently appeared in non-endemic countries, we stress the importance of establishing in these countries health screening programs based on compatible epidemiologic history among the general immigrant population from endemic areas. These programs should be multidisciplinary [3], supported by the best scientific evidence possible, and promoted by the health authorities.

In non-endemic countries, detecting persons infected by T. cruzi is important in order to control the transmission (vertical, by transfusion, or by organ transplant), reduce reactivations in immunodepressed persons, and delay the onset of the chronic cardiac form through antiparasite treatment [39], all of which have a great impact on the persons affected, on public health, and on health systems. Nevertheless, the best solution for CD is a combination of treatment and prevention in endemic countries [40], [41], where many programs and initiatives are underway [2], [42].

The data obtained in this study and the experiences described elsewhere [4], [12], [14], [16], [20], [27] suggest that it is advisable to perform CD screening in non-endemic countries on all patients from continental Latin America who: (1) have a suggestive epidemiologic history (having lived in a rural area, in adobe houses or having knowledge of CD in the country of origin), (2) are pregnant, (3) are immunosuppressed, (4) have symptoms suggestive of CD, or (5) request screening.

Acknowledgments

We thank OPERON S.A. for the disinterested supply of the ICTs. We also thank Silvia Tebar, Antoni Soriano and Lluís Valerio for their collaboration.

Chagas-Clot research group

Physicians: Ignacio Aoiz Linares, Isabel Arias Moliz, Joan Bayó Llibre, Marta Buela, Francesc-Xavier Cano Sana, Ester Casajuana Brunet, Josefina Filomena, Sarai de la Fuente Gilabert, Francisco-Javier García-Alfaro, Carlos Gonzalvo Orero, Laura Haro, MCarmen Igualada Delgado, Fernando Martín González, Elena Mellado, Itsaso Mendizábal Condon, Verónica Moldón, Melania Priego, Ricard Riel Cabrera, Carme Roca Saumell, Núria Sellarés, Rosa Senán Sanz, Mireia Ventura Fontanet, Nieves Vizcay Guruchaga, Josep Lluís Abad Rodríguez, Manel Honrado. Nurses: Teresa Areny Ribera, Gloria Camacho García, Consuelo Cantalapiedra Caicedo, Florencio Cardosa Oliver, Monica Espelt, M.Isabel Fernández Fraga, Josep Manel Grau Granero, Jordi López-Solana, M.Concepción López–Navarro, Esther Montero Moya, Anna Parcerisa Miralles, Marineus Puig García, Gloria Rosillo Sanz, Anna Urpí Fernández, M.José Lapuerta. Clinical assistants: Lurdes Martínez-Vidal, Rosa Fernández. Health Technicians: Josep Maria Escribà Jordana, Isabel Plaza Espuña.