Chagas Disease Control Programme in Brazil: A Study of the Effectiveness of 13 Years of Intervention(*)

Article excerpt

Introduction

Public health services and programmes can be evaluated by different theoretical and methodological approaches which take into account the triad of structure-process-results (1). Since structure and process can rapidly be assessed, the evaluation conclusions can provide important information to programme administrators. On the other hand, only the evaluation of results can identify changes in the mortality and morbidity of populations as a result of the programme's intervention (2, 3). Evaluation of the impact of the programme requires a considerable investment of time in order to observe, analyse and measure the changes in the health indicators being studied (2). Epidemiological studies are often used for evaluating the impact (results) of health programmes, as well as estimating their efficacy and effectiveness, after controlling for extrinsic or confounding factors and identifying other changes (4-6).

The actions of the Chagas Disease Control Programme in Brazil are based on house spraying with insecticide, the objective being to control the Triatoma bug population (intermediate host of Trypanosoma cruzi, the etiological agent of Chagas disease). Until now, the assessment of the programme's impact has been mainly based on entomological indicators, i.e. measuring the reduction of the household triatomine population. The results have shown success in controlling Triatoma infestans, the main vector of T. cruzi in Brazil. However, the replacement of this species by secondary ones in household infestation, which could lead to a possible recrudescence in T. cruzi infection rates, has focused attention on this type of habitat in the transmission of Chagas disease (7, 8) and emphasized the need to evaluate the programme's activities in terms of a reduction in transmission rates. Hence, in addition to the entomological results, serological evaluations of selected cohorts have shown a reduction of T. cruzi infection among those who were born after the start of the programme (9-12). Seroprevalence of Chagas disease in this population is considered to be a sensitive indicator of triatomine household infestation rates, capable of estimating the risk of parasite transmission in the community (3).

A quasi-experimental epidemiological study was conducted in Minas Gerais State in 1987, with the objective of evaluating the effectiveness of the programme. Areas with interventions lasting 5 and 10 years were compared to a control area with no intervention. A comparison of the infection rates found in the study areas, among those born after the programme's implementation, with those published by Chagas Disease Serological Survey showed a decrease in T. cruzi infection rates (cohort of 2-6-year-olds) in the area with 10 years of intervention. However, in the area with only 5 years of intervention (Montalvania), there was an increase in the T. cruzi infection rates in a similar cohort. The authors suggested that 5 years of programme activities were not sufficient to induce changes in the infection rates (13, 14).

The present study was conducted in Montalvania, Minas Gerais State, in 1995 after 13 years of interventions under the Chagas Disease Control Programme. The objective was to investigate (1) the T. cruzi infection transmission pattern in a cohort born after the intervention, and (2) whether the duration of the programme was a determinant factor in inducing changes in the incidences. The panel study was the design chosen in order to evaluate the efficacy of the control programme, a series of cross-sectional studies being carried out in the same population at various time intervals (15). The results of this study were compared with two previous investigations conducted in this area: the Chagas Disease National Serological Survey (1975-1980) (16) and the quasi-experimental study conducted in 1987 (13).

Materials and methods

Study population. This investigation was carried out in the rural area of Montalvania, situated in the north-east of Minas Gerais State, south-east Brazil. The necessary sample size (500) was estimated by assuming that a 50% reduction in T. cruzi infection rate would have occurred as a result of the programme, and accepting as a baseline the rates derived in 1987 (13), with ct = 0.05 and 1 -- [Beta] = 0.90 (17). The sampling unit was the household, identified through the control programme's records. A two-stage sampling scheme was used: a simple random sample of communities within the study counties; and a stratified random sample of houses within each selected community. The following criteria were used in order to obtain better representation of rural households: all houses in communities with less than 10 houses, 50% in communities with 11-30 houses, 30% in communities with 31-60 houses, and 10% in communities with [is greater than] 60 houses (13). All the inhabitants of the selected houses were eligible to be included in the study.

Data collection and laboratory test. The study procedures were approved by the ethical committee of the Institute of Biological Sciences of the Federal University of Minas Gerais. Before data collection, the informed consent of all participants was obtained. The member responsible for the family was then interviewed using a pre-coded questionnaire developed specially for this study. The information collected included not only the respondent, but all family members participating in the survey. The following information was obtained: demographic and social characteristics, knowledge about Chagas disease, household characteristics including all annexes and buildings, any house improvements made, risk factors associated with T. cruzi infection, and factors related to the activities of the control programme. To guarantee reliability in the data collection, all interviews were made by the same interviewer using an instruction manual.

At the interview, a blood sample was collected from all the participants by fingerprick onto filter-paper, according to standard procedures defined by the Brazilian National Health Foundation (18). After drying at room temperature, the filter-papers were stored at 4 [degrees] C before being sent for testing to the serology laboratory at the Department of Parasitology, Federal University of Minas Gerais. Eluates from the filter-papers were tested simultaneously and blindly for anti-T, cruzi antibodies using indirect immunofluorescence assay (IFA) and enzyme-linked immunosorbent assay (ELISA), as previously described (19). The indirect haemagglutination (IHA) test (20) was used when discordant results were obtained. A sample was considered positive when at least two serological tests were reactive: IFA [is greater than or equal to] 1: 40 and IHA [is greater than or equal to] 1: 40; the cut-off point for the ELISA test was the average of negative control titres plus 3 standard deviations (21). Blood samples were tested up to 60 days after collection.

Data on the presence of triatomine bugs in this area were abstracted from the files of the Chagas Disease Control Programme.

Data processing and analysis. The data were analysed using Epi Info software (22) and the following were determined: frequency distribution of collected variables; estimate of the T. cruzi prevalence in the area; T. cruzi incidences, stratified by age groups; correlation between the results obtained in this study and those on triatomine infestation collected by the Chagas Disease Control Programme; the control programme's efficacy, by comparing the T. cruzi infection rates from this investigation with those obtained in the national survey conducted in 1975-1980 and those obtained by the programme evaluation conducted in 1987 (13). Using a relative index, the overall T. cruzi prevalences and incidences, by age group, were compared between the three studies. For this last analysis, both cross-sectional comparisons and cohort analysis were performed for the age groups 2-6 and 7-14 years. The age group comparisons were carried out with the same age group structure used in the National Serological Survey.

Results

Table 1 shows the distributions of the sampling procedures; 156 households were selected and interviewed, and blood samples were obtained from 653 participants out of 655 in the study (99.7%).

Table 1: Numbers sampled and examined in Montalvania, Minas Gerais State, 1995

                         No. in sample   No. in Montalvania

Selected communities           16            150 (10.7)(a)
Households interviewed        156          5 623 (2.8)
Study population              655          8 033(b) (8.2)
Blood samples examined        653          8 033(b) (8.1)

(a) Figures in parentheses are percentages.

(b) Rural population.

The characteristics of the study population can be seen in Table 2. Most participants had no education or incomplete elementary school education. A high proportion (84.3%) were born in Montalvania. Only 1.7% of the subjects reported ever receiving a blood transfusion.

Table 2: Distribution of the demographic variables studied in Montalvania, Minas Gerais State, 1995(a)

                               Number

Sex:
 Male                       325 (49.6)(b)
 Female                     330 (50.4)

Ethnic group:
 Non-White                  510 (77.9)
 White                      145 (22.1)

Education:
 None                       140 (26.0)
 Elementary (incomplete)    363 (65.2)
 Elementary (incomplete      40 (7.2)
  and cursory
 Elementary (complete)        1 (0.2)
 High school (incomplete)     1 (0.2)
 High school                  7 (1.5)

Birth place:
 Montalvania                552 (84.3)
 Another county (MG)         47 (7.2)
 Another state               56 (8.5)

Blood transfusion            11 (1.7)

(a) Data for refusals, "not done" and "don't know" are not shown. The mean age of study participants was 25.5 years.

(b) Figures in parentheses are percentages.

Distribution of the variables used to characterize the houses and their occupants are shown in Table 3. The average time of residence was 11.9 years. Higher proportions of houses were found to have mud walls, dirt floors and tile roofs. Food storage areas, woodpiles, and pictures on the wall, as well as the presence of chickens, dogs and cats inside the dwellings were also reported for most of the houses.

Table 3: Distribution of housing characteristics in the study population, Montalvania, Minas Gerais State, 1995(a)

                                       Number/mean

Number of houses studied:              156 (2.8)(b)
 Duration of residence (mean, years)    11.9
 Persons per house (mean)                5.2
 Rooms per house (mean)                  5.3
 Bedrooms per house (mean)               2.9
 Persons per bedroom (mean)              2.1

Type of walls:
 Brick                                  43 (27.6)
 Mud                                    56 (35.9)
 Adobe                                  44 (28.1)
 Wood and straw                          2 (1.3)
 Adobe and brick                         6 (3.9)

Type of roof:
 Tile                                  112 (71.8)
 Zinc                                    2 (1.3)
 Straw                                   7 (4.5)
 Others                                 35 (22.4)

Type of floor:
 Tile or ceramic                         3 (1.9)
 Cement                                 37 (23.7)
 Dirt                                  105 (67.3)
 Others                                 11 (7.1)

Clothes storage:
 Box                                    55 (35.3)
 Suspended                              82 (52.6)
 Bags                                  101 (64.7)
 Objects on the walls:
 Frame                                 104 (66.7)
 Calendars                             100 (64.1)

Supplies:
 Firewood                               37 (23.7)
 Food storage                          117 (75.0)

Animals indoors:
 Dog                                   110 (70.5)
 Cat                                    89 (57.1)
 Chicken                               148 (94.9)

Type of annex:
 Chicken house                         125 (80.1)
 Pigsty                                 98 (62.8)
 For pile of wood                       50 (32.1)
 For tiles                              34 (21.8)
 For bricks                             36 (23.1)
 For waste                              11 (7.1)

(a) Data for refusals, "not done", and "don't know" are not shown.

(b) Figures in parentheses are percentages.

Table 4 shows the results of the serological tests. A total of 15 participants had two positive serological tests for T. cruzi infection and the overall prevalence was estimated as 2.3%. Among four discordant results between IFA and ELISA, three were confirmed positive by IHA.

Table 4: Proportion of positive serological tests for Trypanosoma cruzi in Montalvania, Minas Gerais State, 1995(a)

                        Number

Blood samples tested    653 (99.7)(a)

IFA:(b)
 Positive                13 (2)
 Negative               640 (98)

ELISA?
 Positive                15 (2.3)
 Negative               638 (97.7)

Positive in two tests    15 (2.3)

(a) Figures in parentheses are percentages.

(b) IFA = indirect immunofluorescence antibody test. ELISA = enzyme-linked immunosorbent assay. The indirect haemagglutination test (IHA) was performed for four discordant test three of them were positive.

The overall prevalences obtained in this study and reported previously from this area are shown in Table 5. The differences are expressed as relative reduction in the infection rates; the total reduction during the thirteen years of the control programme was estimated as 83.5%.

Table 5: Overall prevalence and relative reduction of Trypanosoma cruzi infection observed in Montalvania, Minas Gerais State, 1995

                                               Total
                     Prevalence   Relative    relative
Studies                 (%)       reduction   reduction
                                     (%)         (%)

National survey         13.9         --          --
(1975-80)
Evaluation in 1987       7.8        43.9         --
Evaluation in 1995       2.3        70.5        83.5

Age-specific infection rates were determined using the same age groups as published in the National Survey of 1975-80. Table 6 compares the present results with those from the evaluation conducted in 1987 (prevalences were not available for the national survey). Reductions in the T. cruzi positive seroprevalences, in both cross-sectional and cohort analysis, for almost all age groups were observed. Prevalences were zero in 1995 for the 1-6-and 7-14-year age groups. Table 7 shows the percentage distribution of T. cruzi positive serology, by age group, between the three studies conducted in the area. Whereas an increase was observed in the 2-6-year-old cohort between the National Survey and the 1987 evaluation, the same comparison between 1987 and present evaluations indicates an interruption in parasite transmission. A marked reduction was also observed for the 7-14-year cohort.

Table 6: Trypanosoma cruzi prevalence, by age group, Montalvania, Minas Gerais State, 1987 and 1995

                         %
                    prevalence in:

Age group (years)   1987   1995

 1-6                 2.5      0
 7-14               10.9      0
15-29                8.8    3.1
30-44                5.3    6.6
[is greter than
or equal to] 45      3.9    2.5

Table 7: Trypanosoma cruzi infection rates, by age group, in Montalvania, Minas Gerais State, 1975-80, 1987 and 1995

                         Percentage infection rates

Age group          National survey   Evaluation   Evaluation
(years)            in 1975-80        in 1987      in 1995

2-6                     15.5             5.7          0
7-14                    26.6            54.7          0
15-29                   20.0            22.6         26.6
30-44                   20.0            11.3         53.3
[is greater than
 or equal to] 45        17.7             5.7         20.0

These differences and changes, which were used to estimate the effectiveness of the control programme, are shown in Table 8. The cross-sectional analysis suggested a reduction of 100% for both the 2-6 and 7-14-year age groups; the cohort analysis showed a 100% reduction only for the 2-6-year age group.

Table 8: Relative changes in Trypanosoma cruzi infection rates in Montalvania, Minas Gerais State

Comparisons                  Age group    % positive

Cross-sectional:             2-6 years
 National Survey (1975-80)                   15.5
 Evaluation in 1987                           5.7
 Evaluation in 1995                           0.0

Cross-sectional:             7-14 years
 National Survey (1975-80)                   26.6
 Evaluation in 1987                          54.7
 Evaluation in 1995                           0.0

Cohort for 2-6-year-olds:
 National Survey (1975-80)   2-6 years       15.5
 Evaluation in 1987          7-14 years      54.7
 Evaluation in 1987          2-6 years        5.7
 Evaluation in 1995          7-14 years       0.0

Comparisons                       % change

Cross-sectional:
 National Survey (1975-80)
 Evaluation in 1987           63.2 [down arrow]
 Evaluation in 1995          100.0 [down arrow]

Cross-sectional:
 National Survey (1975-80)
 Evaluation in 1987          105.6 [up arrow]
 Evaluation in 1995          100.0 [down arrow]

Cohort for 2-6-year-olds:
 National Survey (1975-80)
 Evaluation in 1987          248.4 [up arrow]
 Evaluation in 1987
 Evaluation in 1995          100.0 [down arrow]

The entomological indicators (data from the Control Programme) show that large numbers of T. infestans were captured at the start of the intervention; 76.3% of specimens were collected, 57.4% in the surrounding areas. The replacement of this species by T. sordida occurred during the second year of the programme's activities. While percentages of 3.9% and 1.5% were obtained, respectively, indoors and in the areas surrounding the houses at the start of the control programme, current reports indicate 12.6% and 13.7%. T. infestans has not been observed in this area.

Discussion

The results of the present investigation, compared with those obtained in the previous studies in the same area, show that the control programme's effectiveness reached 100% for the age groups 2--6 and 7-14 years. No participants in these age groups, who were born after the control programme started, were identified as infected by T. cruzi. The reduction was confirmed by both cross-sectional analysis (age groups 2-6 and 7-14 years) and cohort analysis (age group 2-6 years). The total decrease observed in infection prevalence, estimated in terms of relative reduction, was 83.5%, when compared to the results of the first investigation. In addition, the 2.3% prevalence found in this study reflects an infection already existing among those born before the intervention programme. It should be noted that although 2.5% of 2-6-year-olds were found to be positive in the 1987 evaluation, no infection was detected in the age group 7-14 years in the present study; a significant reduction in T. cruzi infection rates was also observed in the age group 15-29 years. The most plausible explanation for these findings is the high migration rate to urban centres among young adults searching for better living conditions (23).

This investigation also demonstrated that, for this area, 13 years of control interventions were necessary to induce detectable changes in the transmission of T. cruzi infection. As an earlier evaluation in this area had concluded that 5 years of intervention were not enough to detect changes in the infection rates, an important question arises: for how long should the programme be active in order to induce changes in T. cruzi infection rates in areas similar to Montalvania? It should be emphasized that this area had a very high proportion of houses infested with triatomine bugs at the start of the control programme. Even today, the proportion of houses with suitable conditions for triatomine colonization is still very high. The observed replacement of domiciled T. infestans by secondary vector species in household environs highlights the need for continuing surveillance to prevent recrudescence of T. cruzi transmission.

The effectiveness of health interventions has traditionally been evaluated using the experimental or quasi-experimental design (2, 5, 6). The main advantage of an experimental study is the absolute control exerted by the investigator on the study factor and the random allocation of subjects to guarantee the comparability of the study groups, while ensuring the absence of confounding factors. The quasi-experimental design, which also permits control of the study factor but without the random allocation of subjects, has been proposed as the method of choice to evaluate public health programmes, especially those affecting large populations (24). Only recently, observational studies have been suggested as an alternative method for evaluating health interventions; the major advantages are the reduced cost and the ease of execution (6, 25).

Comparison between areas is crucial for impact evaluation; only by comparing areas with and without the intervention can the observed changes in health indicators be associated with the programme's actions. However, in some situations, a comparison area is not available. In 1995, for example, all the endemic areas in the Minas Gerais State were under the Chagas Disease Control Programme's interventions so that external comparison could not be carried out; an evaluation was possible only by an internal comparison, i.e. studies conducted in the same area at different time intervals (6). In the present investigation, the epidemiological design of choice was the panel study which may be considered as a series of cross-sectional studies, carried out in the same population at various time intervals; unlike conventional cross-sectional studies, longitudinal measurements of individuals or samples are obtained. The design is not affected by absence of the disease at the start of the investigation, as in cohort studies (15, 26). Because time trends can be determinative, changes in the T. cruzi incidence can be attributed to the intervention programme.

The data analysis was designed to identify any distortion that may have occurred during data collection and in the execution of the diagnostic test used in identifying the infection. The data collection methodology was similar to that used in the 1987 evaluation (13). This approach assured high internal comparability. Besides, the interviews were conducted by the same interviewer, using a pre-coded questionnaire and an instruction manual specially developed for this study. The serological tests were carried out, blindly and simultaneously, using two different techniques. Any discordant result was confirmed by a third method.

The construction and internal organization of dwellings were considered to be the main determinant factors for triatomine colonization and consequently T. cruzi human infections (27, 28). This study identified a high proportion of mud houses ("cafuas"), with dirt floors and tile roofs. Food storage, woodpiles, pictures on the wall, and animals were also reported in the houses. A previous investigation has shown a risk of 2.5 for the presence of T. infestans associated with these characteristics (29). In the peridomestic area, the presence of a chicken house, pigsty and woodpile was reported for most of the dwellings; these characteristics are also associated with the presence of triatomines (30).

The households and their surroundings in this investigation were similar to those previously reported from this area (13), which suggests that, during this period, no significant changes related to house improvement were made. Montalvania can still be considered as a high-risk area for triatomine colonization (28). After control of domiciled T. infestans, the area was quickly re-infected by other triatomine species which are considered not to be important in T. cruzi transmission. This fact emphasizes the need for active and continuing surveillance, considering both triatomine presence and T. cruzi infection.

The above results demonstrate the adequacy of the panel design in evaluating the effectiveness of the Chagas Disease Control Programme to interrupt parasite transmission by vectors in this area and to reduce by 100% the incidence rate of infection. It was also shown that the duration of the programme's activities, to be effective, will depend on the baseline characteristics of the area.

Acknowledgements

This investigation was partly supported by Conselho National de Desenvolvimento Cientifico e Tecnologico (CNPq) and Fundacao de Amparo a Pesquisas do Estado de Minas Gerais (FAPEMIG). We are grateful to Fundacao Nacional de Saude-Coordenacao do Estado de Minas Gerais for their cooperation in the field work.

(*) From the Department of Parasitology, Institute of Biological Sciences, Federal University of Minas Gerais, Caixa Postal 486, 31270-901-Belo Horizonte, MG, Brazil. Requests for reprints should be sent to Dr M. Carneiro at this address.

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F.C. Costa(1), R.W.A. Vitor(2), C.M.F. Antunes(3), & M. Carneiro(2)

(1) Doctoral student (Doutoranda).

(2) Assistant Professor.

(3) Professor.

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