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Table of Contents
Year : 2021  |  Volume : 58  |  Issue : 2  |  Page : 148-153

Chagas’ disease among school students from Chiapas, Mexico: Two cases of Chagasic cardiomyopathy

1 Instituto de Ciencias Biológicas, UNICACH, Chiapas, Mexico
2 Laboratorio de Biología de Parásitos, Facultad de Medicina, UNAM, Mexico City, Mexico
3 Facultad de Medicina, UNACH, Chiapas, Mexico

Date of Submission09-Aug-2019
Date of Acceptance24-Dec-2019
Date of Web Publication13-Jan-2022

Correspondence Address:
Dr Salazar-Schettino Paz María
Laboratorio de Biología de Parásitos, Edificio A, 2° piso, Facultad de Medicina, Circuito Interior, Ciudad Universitaria, Avenida Universidad 3000, Ciudad de México, México. C.P. 04510
Torres Gutiérrez Elia
Laboratorio de Biología de Parásitos, Edificio A, 2° piso, Facultad de Medicina, Circuito Interior, Ciudad Universitaria, Avenida Universidad 3000, Ciudad de México, México. C.P. 04510
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0972-9062.325639

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Background & objectives: Chagas disease is a vector-borne life-threatening illness originally confined to the Americas. Seroprevalence studies have been reported in the Mexican state of Chiapas; nevertheless, no clinical/cardiological studies have been conducted to detect underage cases. The aim of the present work was to detect underage cases in the Mexican state of Chiapas.
Methods: A serological screening by ELISA was conducted on 1556 blood samples from school pupils; seropositiv- ity was confirmed by indirect ELISA and indirect immunofluorescence. Seropositive cases were clinically assessed in a hospital, and electrocardiographic and echocardiographic studies were performed. Descriptive statistics were used for analysis.
Results: Seropositivity was confirmed in three cases in the population under study (0.19%). Cardiological studies confirmed the presence of alterations associated to Chagasic cardiomyopathy in two of the three patients.
Interpretation & conclusion: The conditions for an active transmission of T. cruzi infection are met in the rural localities under study. Additionally, the presence of Chagasic cardiomyopathy in underage patients highlights the relevance of an early detection of cases to provide specific treatment at the onset of the infection and to implement epidemiological surveillance as suggested by PAHO/WHO.

How to cite this article:
Guadalupe VLD, Martha BT, Margarita CB, Elia TG, Adelina SGM, Adrián PV, María SSP. Chagas’ disease among school students from Chiapas, Mexico: Two cases of Chagasic cardiomyopathy. J Vector Borne Dis 2021;58:148-53

How to cite this URL:
Guadalupe VLD, Martha BT, Margarita CB, Elia TG, Adelina SGM, Adrián PV, María SSP. Chagas’ disease among school students from Chiapas, Mexico: Two cases of Chagasic cardiomyopathy. J Vector Borne Dis [serial online] 2021 [cited 2022 Aug 10];58:148-53. Available from: https://www.jvbd.org/text.asp?2021/58/2/148/325639

  Introduction Top

Chagas’ disease is a zoonosis caused by the hemoflagellate protozoon Trypanosoma cruzi, which is mainly transmitted by vector triatomines (family Reduviidae) and is prevalent in large portions of the Americas. In Mexico, the number of reported trypanosomiasis cases has increased, with 100 cases reported in 2000 and 1095 cases reported in 2015. In the 2006–2015, Veracruz was the Mexican state with the highest cumulated number of case reports, totaling 1153 and followed by Yucatán, Oaxaca, Chiapas, and Morelos with 827, 771, 702, and 479 cases, respectively[1].

While epidemiological studies have been conducted in Chiapas since the 1970s[2], the seroprevalence rates reported in recent years have been very variable, ranging from 32% in the rainforest and mountain zones to 1% in the coastline; additionally, the occurrence of active transmission in the state has been demonstrated by the presence of seropositive children under 10 years of age (13%)[3]; seroprevalence rates of 22% and 19% were reported in three localities of the Lacandona region[4] and in Sitalá[5], respectively. Vector transmission is the main mechanism of infection by T. cruzi in Chiapas, and five vector species have been reported in the state, with Triatoma dimidiata standing out among them as an intradomiciliary pest[6].

Three clinical phases have been described in Chagas’ disease: the acute phase, which is usually asymptomatic; the chronic asymptomatic phase, characterized by a positive serological detection and the absence of symptoms; and the chronic phase, which may occur up to 10–20 years after the acute phase and in which 20–30% of infected individuals develop cardiomyopathies that lead to the loss of healthy life years and even death[7]. While Chagasic cardiomyopathy is mainly observed in adult individuals, cases of minors with Chagas-associated cardiac lesions have been reported in rural areas from Mexico. The first Mexican case of Chagasic cardiomyopathy in an underage patient was reported in Oaxaca, in 1938[8]; a four-case series was then reported in Querétaro[9]; 14 underage cases from Querétaro, Veracruz, and San Luis Potosí were reported in 2016[10]; and one case was reported in Yucatán in 2017[11]. This highlights the need of actively searching for cases in minors, especially in risk zones.

Despite being one of the states with the highest number of Chagas’ disease case reports, no studies have been conducted in Chiapas to detect underage cases while providing clinical-cardiological follow-up to detect cardiac alterations compatible with the disease. This work is aimed to determine the seroprevalence of T. cruzi infection in school pupils from two rural localities in Chiapas, and to follow up the seropositive individuals to characterize disease-related clinical and cardiac alterations.

  Material & Methods Top

Study Area

A cross-sectional, descriptive study was conducted, from March 2013 to September 2014 at two localities of Mezcalapa region in the state of Chiapas, México [Figure 1]. San Fernando location is 16° 52’ 15 north latitude and 93° 12’ 25 at an elevation of 880 meters above mean sea level (mamsl). Copainalá location is 17° 06″ north latitude and 93° 17″ west longitude at an elevation of 440 mamsl. Both villages have a subtropical warm climate, with abundant rain in the summer[12].
Figure 1: Mezcalapa region, showing the location and geographical information of the study localities. Modified from INEGI, 2010 (4).

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Population under study

School population whose age ranged from 6 up to 18 yr from both localities was sampled, randomly selecting one school of each level: elementary, secondary, and high school. The total school population in all three levels was 1191 students in San Fernando and 430 students in Copainalá. Teaching staff, parents and all the participants were informed on the aim of our study, and an informed consent letter was signed by the parent or legal guardian of each student before a blood sample was taken. Specimens of triatomine species endemic in the region in all development stages were shown to parents and teaching staff, and a questionnaire was applied to determine the degree of convivence with the vector[13]. The results were summarized and statistically analyzed.

Initial screening to identify suspected T. cruzi infection cases

A blood sample was obtained by digital puncture and collected on filter paper (Whatman No. 1), clearly labeling each sample with the donor’s personal information.

ELISA test.

The presence of anti-T. cruzi (IgG) antibodies were determined in blood samples by enzyme-linked immunosorbent assay (ELISA) tests using two different antigenic extracts. The optic density was measured using an Epoch spectrophotometer (BioTek Instruments, Inc., Winooski, VT, USA). Each prove was performed using two positive controls and a negative control. A sample was considered as reactive for the indirect ELISA screening test when optical density was higher than 0.140.

Serological diagnosis confirmation

The standard approach for T. cruzi infection diagnosis according to the section of the Mexican regulation NOM-032-SSA2-2014[14] is to apply two or more tests that use different techniques and/or that detect antibodies to different antigens. In the present protocol confirmatory tests were performed by ELISA and immunofluorescent antibody test (IFA). All serological tests were previously standardized and validated with serum panels provided by Instituto Nacional de Chagas Dr. Mario Fatala Chabén, Argentina; a sensitivity of 96.0% and a sensitivity of 100% were determined for the ELISA, and a sensitivity of 88.0% and a specificity of 100% were determined for IFA[13].

Peripheral blood samples were taken from each reactive case in the screening and from two seronegative pupils of the same sex and age group. Serum were separated by centrifugation 2000 rpm /15 min. Serum samples were diluted 1:200 using a dilution buffer for ELISA confirmatory tests which were performed following the same procedure as screening test. For interpretation; a sample was considered positive for the indirect ELISA confirmatory test when optical density was higher than 0.180.

Detection of antibodies by IFA

IFA slides visualization was performed in an Olympus BH2-RFCA microscope (Olympus corporation Shinjuku, Tokyo, Japan). A sample was considered as positive for the confirmatory IFA test when reactivity was observed at a dilution equal to or higher than 1:32.

Clinical cases

With permission from each family head, the households of school pupils who were seropositive for both tests were visited to observe their environmental conditions and the possible factors associated to the transmission of T. cruzi infection.

In-hospital studies

School students with double-confirmed seropositivity for T. cruzi, along with seronegative students paired by sex, age, and school attendance were referred to the Children’s Hospital at Tuxtla Gutiérrez to undergo a physical examination, a simple 12-lead electrocardiogram (EKG), and a trans-thoracic echocardiogram (ECHO).

Ethical statement

All participants and/or their legal guardians were informed of the objective of this study and signed an informed consent letter. The study “Clinical and cardiological study on children seropositive to Trypanosoma cruzi in two rural localities in Chiapas, Mexico” was conducted with the approval of the Research and Ethics committees of the Facultad de Medicina, UNAM, (Approval no: 103-2015).

In Mexico, the Health Ministry (Dirección General de Epidemiología, Secretaría de Salud), monitors acute and chronic trypanosomiasis, which must be immediately reported through the National System for Epidemiological Surveillance; etiological treatment is administered by the Diseases Control National Centre (Centro Nacional de Programas Preventivos y Control de Enfermedades - CENAPRECE) and distributed at a state level through vector-transmitted diseases departments that report any confirmed case of Chagas’ disease[14].

  Results Top

A total of 1,556 blood samples from school students whose ages vary from 6 to 17 yr of age were collected on filter paper, 1161 from San Fernando and 395 from Copainalá, representing 96.6% of the population attending the schools under study. The population under study was composed of women and men and although the number of students varied in each community (San Fernando 542w/619m; Copainalá 220w/175m), the total percentage among sexes was close to 50% (49% women/ 51% men). At San Fernando, the most represented age group was 15–18 yrs old 53.4% of the students, while at Copainalá the 10–14 yrs age group represented 38.7% of the students.

Of the population under study, none have been previously diagnosed with Chagas disease or any cardiac disfunction. The questionnaire given to school students indicated that between 66.1% and 75.1% of students in Copainalá identified the vector, and 56 students (14.17%) admitted having been bitten by it; in San Fernando, between 26.3% and 31.5% of students knew the vector, and 15 (1.29%) admitted having been bitten. Local inhabitants know the vector as “talaje”.

Serological diagnosis

From the 1156 blood eluates screened, 4 samples (0.25%) from Copainalá and 6 (0.38%) from San Fernando showed reactivity against T. cruzi. From these samples, only three were confirmed as positive by indirect ELISA and IFA, in accordance with the guidelines by WHO[1] and NOM-032-SSA2-2014[6]. These confirmed cases represent a seropositivity rate of 0.19% in the school population under study (3/1556). The seropositive samples corresponded to two female school pupils from Copainalá and one male student from San Fernando [Table 1]. The houses of the three seropositive students are located outside the urban area of each locality, near to a disturbed rainforest ecosystem.
Table 1: School pupils with double confirmed seropositivity for Trypanosoma cruzi.

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According to EKG and ECHO studies, two sero- positive students (G.R.L.G. and M.H.R.) showed cardiac alterations compatible with Chagasic cardiomyopathy, indicating that 0.13% of the sampled population was in the chronic symptomatic phase of Chagas’ disease; disaggregated by sex, prevalence was 0.12% in male (1/794) and 0.13% in female subjects (1/762). The main clinical and cardiographic findings are described below.

Case G.R.L.G.

Male, 17 yr old from the Monterrey locality, municipality of San Fernando. During clinical questioning, the patient did not recognize the vector, nor recall having shown clinical data compatible with the disease. The parents described that the child suffered from a “hot swelling” in the spleen 11 years before, and that by that time their house had concrete block walls, a tin roof, and dirt floors; the family had domestic animals inside and farmyard animals outside the house.

The EKG trace showed an incomplete right bundle branch block (IRBBB), and the ECHO study showed a normal ventricular function with mild to moderate pulmonary artery hypertension, as well as mild failure of the pulmonary valve. This patient did not show clinical data suggesting cardiac failure, allowing us to infer that the ECHO isovolumetric relaxation time is normal [Figure 2], [Table 2].
Figure 2: Electrocardiographic abnormalities found in the case G.R.L.G., with incomplete right bundle branch block (IRBBB).

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Table 2: Results of electrocardiographic (EKG) and echocardiographic (ECHO) studies on two students seropositive for T. cruzi.

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Case M.H.R.

Female, 16 yr of age from the José María Morelos locality, municipality of Copainalá. During clinical questioning, the patient identified the triatomine named as “talaje”, explaining that the insect is commonly seen in the adobe-wall storage room at her home; she also recalled being bitten in the arm by the insect about four years ago, that the bite left a welt and caused fever. The patient reported heart palpitations and severe effort dyspnea, which started one year before. Her house has wooden walls, a tin roof, and dirt floors, with domestic and barnyard animals inhabiting the house and its surroundings. Specimens of the vector species T. dimidiata were collected in the storage room adjacent to the house.

The EKG trace showed an incomplete right bundle branch block (IRBBB) [Figure 3], [Table 2], and the ECHO study showed a mild failure of the pulmonary artery, mild pulmonary hypertension, and mild failure of the function of the tricuspid valve. All three seropositive students were reported to the Health Ministry to be given specific anti-parasitic treatment (Nifurtimox 12 mg/kg). The treatment was administered in accordance with the guidelines by the Centro Nacional de Programas Preventivos y Control de Enfermedades, Secretaría de Salud (CENAPRECE)[15]. The three seronegative students paired with the seropositive ones by sex, age, and school attendance were referred to the Children’s Hospital in Tuxtla Gutierrez, Chiapas. Their medical history, EKG, and ECHO were within normal limits.
Figure 3: Electrocardiographic abnormalities found in the case M.H.R., with incomplete right bundle branch block (IRBBB).

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  Discussion Top

The presence of seropositive cases in Chiapas has been reported several times. By the end of 2017, the Epidemiological Bulletin of the Sistema Nacional de Vigilancia Epidemiológica de la Secretaría de Salud (SINAVE) reported a cumulative total of 40 and 51 cases of American trypanosomiasis, respectively[1].

Among the causal factors associated to infection by T. cruzi are the construction material of the walls, roof, and floor of the houses, since some material types could allow the invasion and permanence of triatomines inside the house, and therefore could favor the host-vector-environment interaction. A risk factor for Chagas’ disease is the proximity of the vector to human populations[16]. When questioned about the vector insect, 70.6% of school students in Copainalá declared to know it, and 14.2% among them admitted having been bitten by the insect at least once. In contrast, 71.1% of students in San Fernando failed to recognize the vector and only 1.3% among those who knew it recalled having been bitten. This could be because most school students in Copainalá live in localities that are nearby the municipal seat, while most students in San Fernando reported to live at the town center.

In total, 1556 blood samples were obtained from 1591 students enrolled, a sign of the good disposition of education authorities and parents from the six schools selected. All schools were located at the municipal seats, where most houses are built of durable materials like bricks, concrete, and blocks; however, the three underage patients with a double confirmed seropositivity for T. cruzi infection lived in nearby neighborhoods, where very few houses have brick walls and/or concrete roofs; houses in those neighborhoods are mainly built of adobe and wood, with a tin and/or tile roof.

Seropositive school pupils were clinically, electrocardiographically, and echocardiographically assessed at the Children’s Hospital in Tuxtla Gutiérrez, Chiapas; two out of the tree students showed signs of alterations in cardiac conduction and rhythm and were diagnosed with chronic Chagasic cardiomyopathy; these cases amount to 0.13% (2/1556) of the population under study. One of the seropositive students did not show evidence of cardiac alterations and is assumed to be in the chronic asymptomatic phase of Chagas’ disease.

In the areas where Chagas’ disease is known to be present, serodiagnosis for T. cruzi infection is omitted in underage patients with cardiac disorders, instead focusing on the clinical evaluation on the current conditions; thus, a possible infection is often undetected[17]. Chagasic cardiomyopathy has been mainly reported in adult individuals, and cases of underage patients living in Chagas’ disease risk areas in Mexico are very scarce[9],[10],[11]; this stresses the need of strengthening the efforts to diagnose, treat, and monitor the disease in all population segments.

The prevalence of Chagas’ disease and the extent of the active transmission of the infection in Chiapas are still unknown. The presence of infection by T. cruzi in school students is herein confirmed, proving that active transmission is possible in these localities, where the presence of the vector and prevalent socioenvironmental conditions favor the human-triatomine interaction. Our results show, for the first time, the presence of underage patients in the chronic symptomatic phase of Chagas’ disease in Chiapas, highlighting the need of maintaining epidemiological surveillance activities to decrease the risk of triatomine infestation in houses, detect circulating T. cruzi strains in human populations and in domestic and peridomestic reservoirs, and reinforcing educational and health-promoting activities to decrease the risk of T. cruzi transmission.

  Conclusion Top

Seroprevalence values of 0.5% and 0.16% were found for T. cruzi infection in the rural localities of Copainalá and San Fernando, Chiapas, respectively. Two cases of Chagasic cardiomyopathy in underage individuals are reported herein, for the first time in Chiapas; along with housing conditions and the presence of vectors in these regions, this finding highlights the importance of continuing the efforts for case detection to give specific treatment at the onset of the infection, and to implement an efficient epidemiological surveillance, as recommended by PAHO/WHO.

Conflict of interest: None

  Acknowledgements Top

The authors thanks the partial financial support of Facultad de Medicina, UNAM and DGAPA-PAPIIT grants Nos. IN-211613 and IN-227816.

  References Top

Boletin Epidemiológico [Internet]. Secretaria de Salud: Dirección General de Epidemiología. Sistema Nacional de Vigilancia Epidemiológica Sistema Único de Información; Available from: https://www.gob.mx/salud/acciones-y-programas/direccion-general-de-epidemiologia-boletin-epidemiologico (Accessed on Febuary 19, 2019).  Back to cited text no. 1
Goldsmith RS, Kagan IG, Zarate R, Reyes-González MA, Cedeño-Ferreira J. Epidemiologic Studies of Chagas’ Disease in Oaxaca, Mexico. Bull Pan Am Health Organ 1978; 12(3): 236–50.  Back to cited text no. 2
Mazariego-Arana MA, Monteón VM, Ballinas-Verdugo MA, Hernández-Becerril N, Alejandre-Aguilar R, Reyes PA. Sero-prevalence of human Trypanosoma cruzi infection in diferent geografic zones of Chiapas, Mexico. Rev Soc Bras Med Trop 2001; 34(5): 453–8.  Back to cited text no. 3
Sosa-Jurado F, Mazariego-Aranda M, Hernández-Becerril N, Garza- Murillo V, Cárdenas M, Reyes PA, et al. Electrocardiographic findings in Mexican chagasic subjects living in high and low endemic regions of Trypanosoma cruzi infection. Mem Inst Oswaldo Cruz 2003; 98(5): 605–10.  Back to cited text no. 4
Cenalmor-Aparicio C, Ballinas-Verdugo M, Reyes PA. American Trypanosomiasis (Chagas disease) in the municipality of Chilón, Chiapas: a clinicoepidemiologic survey. Salud Publica Mex 2013; 55(2): 145–50.  Back to cited text no. 5
Salazar-Schettino PM, Rojas-Wastavino GE, Cabrera Bravo M, Bucio Torres MI, Martínez-Ibarra JA, Monroy-Escobar MC, Rodas-Retana A, Guevara-Gómez Y, et al. A revision of thirteen species of Triamoniae (Hemiptera:Reduviidae) vectors of Chagas disease in Mexico. J Selva Andin Res Soc 2010; 1(1): 57–80.  Back to cited text no. 6
Estrategia y plan de acción para la prevención, el control y la atención de la enfermedad de Chagas [internet]. Washington D.C. EUA OPS/OMS. Available from: https://www.paho.org/mex/index. php?option=com_docman&view=download&alias=389-estrategia-y-plan-de-accion-para-la-prevencion -el-control-y-la-atencion-de-la-enfermedad-de-chagas&category_slug=vigilancia-prevencion-y-control-de-enfermedades&Itemid=493 (Accessed on Febuary 19, 2019).  Back to cited text no. 7
Salazar Schettino PM, Tay J, Ontiveros A, JImenez J, De Haro I, Bucio MI, et al. Enfermedad de Chagas en México. Presentación de casos clínicos. Rev Fac Med UNAM 1983; 25: 77–82.  Back to cited text no. 8
Salazar-Schettino PM, Perera R, Ruiz-Hernandez A L, Bucio Torres MI, Zamora-Gonzalez C, Cabrera-Bravo M, et al. Chagas Disease as a Cause of Symptomatic Chronic Myocardopathy in Mexican Children. Pediatr Infect Dis J 2009; 28(11): 1011–3.  Back to cited text no. 9
Salazar-Schettino PM, Cabrera-Bravo M, Vazquez-Antona C, Zenteno E, De Alba-Alvarado M, Torres Gutierrez E, et al. Chagas Disease in Mexico: Report of 14 Cases of Chagasic Cardiomyopathy in Children. Tohoku J Exp Med 2016; 240(3): 243–9.  Back to cited text no. 10
Méndez-Domínguez N, Chi-Méndez C, Canto-Losa J, Peniche- Echazarreta A, Canto-Losa JP, Gómez-Carro S. Chagasic Cardiopathy in a child: Case report. Rev Chil Pediatr 2017; 88(5): 647–51.  Back to cited text no. 11
México en Cifras. Chiapas 07 [internet]. Instituto Nacional de Geografía y Estadística. 2017 –. Available from: https://www. inegi.org.mx/app/areasgeograficas/?ag=07#tabMCcollapse- Indicadores. (Accessed on Febuary 19, 2019).  Back to cited text no. 12
Salazar PM, Rojas G, Bucio M, Cabrera M, García G, Ruiz A, et al. Seroprevalencia de anticuerpos contra Trypanosoma cruzi y su asociación con factores de riesgo en menores de 18 años de Veracruz, México. Rev Panam Salud Publica 2007; 22(2): 75–82.  Back to cited text no. 13
Norma Oficial Mexicana para la vigilancia epidemiológica, promoción, prevención y control de las enfermedades transmitidas por vectores NOM-032-SSA2-2014 [internet]. Secretaria de Salud, CENAPRECE.. Available from: http://www.cenaprece.salud.gob.mx/programas/interior/vectores/descargas/pdf/ NOM_032_SSA2_2014.pdf. (Accessed on Febuary 19, 2019).  Back to cited text no. 14
Programa de Acción Específico Prevención y control de la Enfermedad de Chagas 2013-2018 [internet]. Secretaria de Salud. 2014. Available from: http://www.cenaprece.salud.gob. mx/descargas/pdf/PAE_PrevencionControlEnfermedadChagas2013_2018.pdf (Accessed on Febuary 19, 2019).  Back to cited text no. 15
Salazar-Schettino PM, De Haro I, Cabrera-Bravo M. Tres especies de triatominos y su importancia como vectores de Trypanosoma cruzi en Mexico. MEDICINA (Buenos Aires) 2005; 65(1): 63–9.  Back to cited text no. 16
Sierra-Johnson J, Olivera-Mar A, Monteón-Padilla VM, Reyes PA, Vallejo M. Panorama epidemiológico y clínico de la cardiopatía chagásica crónica en México. Rev Saude Publica 2005; 39(5): 754–60.  Back to cited text no. 17


  [Figure 1], [Figure 2], [Figure 3]

  [Table 1], [Table 2]


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