Challenges to Schistosomiasis Control Program in Brazil: setbacks in the control program and critical analysis of the disease notification

ABSTRACT

Background:

In 1970, Brazil implemented the Schistosomiasis Control Program (PCE, Portuguese acronym for Programa de Controle da Esquistossomose) was implemented in Brazil, where, through successive treatment interventions, the epidemiology and transmission of schistosomiasis have changed significantly over time. This study aimed to evaluate the PCE’s effectiveness by critically analyzing the disease notification system.

Methods:

An ecological study was conducted using data on reported schistosomiasis cases in Brazil between 2007 and 2020.

Results:

The highest number of municipalities actively participating in the PCE was 750, recorded in 2007. Conversely, participation reached its lowest point in 2020, with only 259 municipalities involved. Over the past decade, there has been a drastic decline in the number of municipalities with active schistosomiasis control programs. During the same period, there was an observed increase in the number of deaths caused by schistosomiasis, while the number of reported cases decreased. This suggests an inverse correlation.

Conclusions:

The present data suggest that schistosomiasis cases are not correctly diagnosed or reported, reflecting a twisted image of the magnitude of this public health problem in Brazil.

Keywords:
Schistosoma mansoni; Public Health; Epidemiology; Schistosomiasis Surveillance and Control Program; Brazil

INTRODUCTION

Schistosomiasis is a widespread parasitic disease affecting approximately 252 million people, reaching 54 countries, mainly Africa and Asia. These estimates suggest that roughly 770 million people live in areas where the disease is endemic and are at risk of infection^1,2. In Brazil, intestinal schistosomiasis remains an public health problem, infecting approximately 1.5 million people with an additional 25 million living in at-risk areas^3,4.

The Global Burden of Disease Study (2017) estimated that schistosomiasis infections caused 1.4 million disability-adjusted life years (DALYs) in Brazil. This ranked schistosomiasis as the second-leading neglected tropical disease in the country in terms of DALYs^5,6. Furthermore, schistosomiasis was the second most commonly reported parasitic disease in Brazil between 2009 and 2013⁷.

Brazil faces a major public challenge due to schistosomiasis, with a significant number of severe and fatal cases¹, particularly concentrated in the Northeast and Southeast regions⁸. Endemic areas with historically high infection rates were primarily located in the states of Minas Gerais and Bahia. However, the implementation of the Brazilian Schistosomiasis Control Program (PCE Portuguese acronym for Programa de Controle da Esquistossomose), and ongoing treatment interventions have significantly altered the epidemiology and transmission patterns of schistosomiasis^8-10.

The PCE operates in a decentralized manner, with actions planned and organized at the municipal level, and mandated for inclusion in the basic healthcare plan^8,11,12. Brazil utilizes two notification systems for schistosomiasis cases: in endemic areas are registered in the Information System of the Schistosomiasis Surveillance and Control Program (SISPCE) and severe cases are registered in the Information System of the Notification of Diseases (SINAN). In non-endemic areas all cases are registered in the SINAN⁸. This study aims to analyze the effectiveness of the national control program by critically evaluating the notification system, considering the temporal distribution of cases, severe cases, and deaths due to schistosomiasis in Brazil between 2007 and 2020.

METHODS

● Ethical aspects

This Project was approved by the Brazilian Ethical Committee of Research (CEP) under license #38663720.3.0000.5149.

● Study area and epidemiological design

We conducted an ecological descriptive study of schistosomiasis cases reported in Brazil between 2007 and 2020. Data from the secondary database of the National Surveillance System for Notifiable Diseases of the Brazilian Ministry of Health (SINAN - Sistema de Informação de Agravos de Notificação) and the SISPCE were used. Data were grouped by year to examine temporal trends in schistosomiasis prevalence, deaths, and severe cases.

The PCE implements field activities to control the disease, while the SISPCE stores schistosomiasis data and supports PCE management. The 2007-2020 period was chosen because it coincides with a change in SINAN, allowing for synchronized data collection between the two systems.

Severe cases were defined as those presenting with acute, other, or hepatosplenic forms. Intestinal and hepatointestinal forms were classified as non-severe⁸. This classification follows the Brazilian Ministry of Health’s recommendations and aligns with the notification form, where “other forms” encompass neuroschistosomiasis and any other atypical presentations.

For SISPCE data, we calculated an annual positivity rate by dividing the total number of positive cases in each year by the total number of individuals examined. The lethality rate, using only SINAN data, was calculated by dividing the total number of schistosomiasis-related deaths by the total number of positive cases in the corresponding year.

Spearman’s rank correlation coefficients were used to assess correlations between quantitative variables. Statistical analyses were performed using SPSS 25 software.

RESULTS

During the study period, we identified 1,095 Brazilian municipalities actively participating in the PCE. These municipalities were located in the southeastern, northeastern, southern, and northern regions of the country. It is important to note that some states, like Santa Catarina and Rondônia, only provided control program data for two years.

While 1,095 municipalities participated in the program overall, their involvement decreased over time. The highest participation was 750 was observed in 2007, followed by a gradual decrease to 259 by 2020. The year 2016 saw the largest drop in participation, with 179 fewer municipalities compared to the previous year. However, there were fluctuations in this trend, with increases in participation observed in 2009, 2014, 2015, 2017, and 2019 (Table 1 and Figure 1A).

TABLE 1:
Number of Brazilian municipalities actively participating in the Schistosomiasis Control Program (PCE) and schistosomiasis positivity rates from 2007 to 2020. Data are presented by numbers are separated by region, state, and year.

		2007		2008		2009		2010		2011		2012		2013		2014		2015		2016		2017		2018		2019		2020
		%	MC	%	MC	%	MC	%	MC	%	MC	%	MC	%	MC	%	MC	%	MC	%	MC	%	MC	%	MC	%	MC	%	MC
North	Rondônia	0.5	8	0.0	3	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0
	Pará	1.7	6	1.2	7	1.1	5	2.0	5	3.6	6	2.7	3	7.4	1	2.6	1	0.5	1	0.2	1	0.0	0	0.0	0	0.0	0	0.0	0
North East	Maranhão	4.8	45	4.4	36	6.4	41	5.1	40	4.6	40	5.1	35	5.0	33	3.8	33	4.1	35	2.9	32	7.5	25	6.6	28	5.8	25	5.9	18
	Piauí	0.1	3	0.0	1	0.0	0	0.0	1	0.2	1	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0
	Ceará	0.3	30	0.3	25	0.2	24	0.3	25	0.1	36	0.1	37	0.2	23	0.5	27	0.4	22	0.3	9	0.1	13	0.4	11	0.1	12	0.1	9
	Rio Grande do Norte	4.3	15	2.8	14	6.9	12	2.6	16	4.6	15	3.1	14	2.1	15	4.3	15	2.0	10	2.4	6	2.0	10	1.8	12	2.0	11	1.4	5
	Paraíba	4.8	20	6.4	16	13.8	17	7.4	13	6.6	13	6.6	10	8.4	11	10.1	9	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0
	Pernambuco	9.8	45	8.5	49	9.6	53	7.2	55	6.9	57	5.0	53	4.7	57	3.2	108	2.8	111	2.2	111	2.4	100	1.9	102	1.9	97	1.4	61
	Alagoas	7.9	63	8.0	62	9.3	63	6.3	63	6.8	65	5.8	62	5.5	64	5.3	62	4.3	60	3.9	61	4.2	60	3.5	61	3.8	59	2.4	53
	Sergipe	14.5	48	12.4	39	6.9	41	10.4	42	7.2	45	9.2	22	5.4	29	5.5	33	9.2	36	15.2	31	6.2	27	4.0	33	4.4	28	7.3	17
	Bahia	4.1	105	4.5	98	2.7	105	4.5	93	2.8	118	4.0	110	2.3	96	3.2	88	3.0	84	2.5	61	2.9	90	2.6	106	2.4	127	3.7	70
Southeast	Minas Gerais	4.8	297	4.7	265	4.1	244	3.8	228	3.8	221	3.3	189	2.3	141	2.5	116	3.1	175	2.3	47	2.5	43	1.0	22	2.0	26	1.2	17
	Espírito Santo	3.7	47	2.8	43	3.6	36	2.9	41	3.3	41	2.6	39	2.5	26	3.1	28	3.0	28	4.3	24	3.5	21	3.5	14	3.5	14	2.6	9
	Rio de Janeiro	0.4	3	0.7	1	2.8	1	0.7	2	12.6	1	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0
South	Paraná	1.3	13	2.1	11	13.7	8	3.4	7	2.6	1	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0
	SantaCatarina	0.3	2	0.1	1	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0	0.0	0
Total		5.4	750	5.2	671	5.2	650	4.7	631	4.5	660	4.2	574	3.6	496	3.7	520	3.5	562	3.2	383	3.3	389	2.9	389	2.8	399	2.5	259

• MC: Number of municipalities covered; %: Positivity rate for S. mansoni.

Compared to the previous year, 2020 saw the sharpest decline in the number of stool samples examined, with a decrease of 64.4% compared to 2019. The second-largest reduction occurred in 2016, with a decrease of 47.3% (Figure 1B).

FIGURE 1:
(A) Annual changes in the total number of municipalities with an active schistosomiasis control program, Blue bars indicate a decrease, and green bars indicate an increase compared to the previous year. (B) Annual percentage change in the number of stool examinations compared to the previous year. Blue bars indicate a decrease, and green bars indicate an increase.

The decline mirrored a downward trend in the positivity rate for schistosomiasis among the examined population. In 2007, Brazil had a positivity rate of 5.40% (95% CI, 5.27-5.53), with roughly two million individuals examined. By 2020, the positivity rate dropped to 2.83% (95% CI, 2.75-2.93), with only 268,659 examined individuals (Supplementary Material and Figure 2).

FIGURE 2:
Annual positivity rate for schistosomiasis and total number of stool examinations performed annually in municipalities with an active schistosomiasis control program.

In addition to PCE data, we analyzed and compared data from the SINAN for the same period. During this timeframe, SINAN reported 155,008 cases. While the number of notified cases decreased over time, the graph (Figure 3) indicates an increase in the number of deaths. This resulted in a significant negative correlation (r = -0.686, p <0.05) between notified cases and deaths during the study period. This suggests a decrease in the total number of cases, but with a higher proportion resulting in death, leading to an increase in mortality from less than 0.1% in 2007 to approximately 2.5% in 2020. Interestingly, the number of severe cases reported by SINAN remained relatively constant throughout the period, with a total of 7,697 reported cases (Figure 4).

FIGURE 3:
Annual number of notified schistosomiasis cases (black line) and deaths attributed to schistosomiasis (grey line) in Brazil (data from SINAN).

FIGURE 4:
Annual number of severe schistosomiasis cases (black line) and lethality rate (grey line) in Brazil (data from SINAN only).

DISCUSSION

This study examined the effects of the PCE in Brazil from 2007 to 2020. While our results show a decrease in schistosomiasis cases over time, a trend observed in both SISPCE and SINAN data, there’s a concerning aspect regarding PCE performance.

Apesar do sucesso anterior relatado do programa, no Brasil houve uma diminuição nas taxas de positividade ao longo do tempo. No entanto, isto não foi acompanhado por uma diminuição no número de casos graves, resultando num aumento de mortes. The concerted actions of the PCE managed to reducing case numbers through active case finding and treatment¹³, there was a decrease in PCE activity over time, as evidenced by fewer participating municipalities and stool examinations. This raises the possibility that some municipalities may have discontinued their control programs. Potential reasons for program discontinuation could be twofold: i) the perception of a reduction in infection rates, thus prioritizing other health activities, and ii) errors in the notification of the disease.

The decrease in schistosomiasis positivity rate, from 5.4% in 2007 to 2.5% in 2020, suggests success for the PCE. However, this positive trend coincides with a decline in active case-finding efforts, as evidenced by the drop in stool examinations performed (from 2,620,752 in 2007 to 661,497 in 2019, a decrease exceeding 74%).

This reduction might be attributed to a few factors. Inconsistencies in notification systems exist, with discrepancies between the Schistosomiasis Surveillance and Control Program Information System (SISPCE for its initials in Portuguese) and SINAN. Additionally, some municipalities might have under-reported cases as individuals treated in primary healthcare may not consistently inform the PCE team, leading to inaccuracies. This lack of communication between teams makes it difficult to report cases accurately¹⁴.

The year 2020 saw a particularly sharp decline in stool tests, nearly 50% lower than 2019. This can likely be attributed to the impact of the coronavirus disease-2019 (COVID-19) pandemic. Many professionals were redeployed to combat the virus’ spread. Furthermore, the World Health Organization recommended suspending active search activities, mass treatment campaigns, and health education initiatives for neglected tropical diseases during the pandemic’s peak¹⁵. This recommendation likely contributed to the significant drop in stool examinations in 2020. However, concerns have been raised that interrupting control programs for Schistosoma mansoni and S. haematobium could lead to a resurgence of cases in the future¹⁶.

Following decades of control interventions and the implementation of the PCE, areas with low schistosomiasis endemicity have been increasingly common^10,17. The Kato-Katz method remains the primary diagnostic tool used in control programs, even in these low-endemicity settings, due to its practicality and affordability^18,19 However, a significant drawback of this method in these areas is its reduced sensitivity, particularly for individuals with low parasite burden^20,21. Increasing the number of stool samples examined per slide can improve test sensitivity^20-22.

Recent PCE data might suggest a successful program nearing eradication. However, studies using more samples or more sensitivity tests have shown a positivity rate 2.3 times higher²¹. Despite recommendations to increase sample numbers, technical guidelines suggest increasing the number of slides examined per stool sample in low-endemicity areas⁸. However, resource limitations, both financial and human, often hinder the implementation of this approach, making it difficult to identify positive cases in areas with low endemicity or parasite burden^21,23.

Underreporting by municipalities may be another factor contributing to the decrease in reported positive cases. Brazil utilizes two independent notification systems for schistosomiasis: SISPCE and SINAN. This dual system can lead to confusion and underreporting, potentially impacting testing, diagnosis, and notifications. Technical guidelines for schistosomiasis surveillance in Brazil recommend notifying SINAN of all diagnosed cases in. non-endemic areas, regardless of severity. Conversely, in endemic areas, only severe clinical forms should be reported to SINAN, with other cases reported to SISPCE⁸. Additionally, operational data from coproscopic, epidemiological, and malacological surveys are also included in SISPCE reports⁸.

Rondônia is not endemic for schistosomiasis. Despite historical records suggesting its potential endemicity since the 1980s²⁴, active PCE programs successfully controlled the decrease until 2008. At that point, the program was discontinued due to the presumed eradication of transmission within the state. However, reported outbreaks were not caused by local transmission but rather by infected individuals migrating from highly endemic states in southeastern or northeastern Brazil²⁵. This migration risk extends beyond Rondônia, as evidenced by reports of focal transmission in Rio Grande do Sul²⁶. These cases highlight the importance of continuous schistosomiasis monitoring. The absence of schistosomiasis data for São Paulo can be explained by their independent PCE notification system. This utilized its system to track program activities, rendering data incompatible with the national system⁸.

The observed negative correlation between deaths and reported cases suggests a potential consequence of reduced PCE activity. Ideally, trends in severe cases and deaths would mirror trends in reported cases; however, this was not the case in this study. The rise in lethality and continued persistence of severe cases might indicate delayed diagnosis. This, as reported elsewhere, could lead to worsening clinical situations for patients and an increased risk of death during chronic infection^16,27. Additionally, these more severe cases could place a significant burden on the healthcare system due to increased public spending on treatment and patient follow-up.

While data shows a decline in schistosomiasis-positive cases and positivity rates over time, the number of severe cases remained relatively constant between 2008 and 2018, exceeding 500 cases annually. This suggests a potential underdiagnosis of asymptomatic cases or a lack of proper case management. The decrease in severe cases observed in 2019 and 2020 could be attributed to several factors, including the COVID-19 pandemic, competing healthcare priorities, or delays in reporting¹⁶.

Furthermore, the suspected decline in PCE activity in many municipalities is corroborated by the observed increase in deaths and lethality during the study period. This trend coincides with a strong negative correlation between reported positive cases and deaths in the SINAN data.

While schistosomiasis is chronic with a slow progression, the leading causes of death are often related to severe clinical forms like liver cirrhosis, portal hypertension, colitis, pulmonary complications, and neurological issues. These conditions typically develop decades after the initial infection^25,28. The observed rise in lethality, coupled with the negative correlation between lethality and reported cases, suggests potential underreporting or misdiagnosis. Both scenarios are concerning and could represent a setback in Brazil’s fight against schistosomiasis.

The latest National Survey of the Prevalence of Schistosomiasis Mansoni and Soil-Transmitted Helminth Infections (2010-2015) estimated a national schistosomiasis prevalence of 0.9% in Brazil (Katz, 2018). However, this school-based survey had limited coverage in key endemic areas, particularly southeastern and northeastern regions. Additionally, the results weren’t statistically adjusted to account for the reduced sensitivity of the two-slide Kato-Katz method, as documented in other studies^20,21,29. This potentially misleading data might have influenced health policymakers, leading to the downplay of the schistosomiasis problem in Brazil. Consequently, control efforts and financial support for municipal interventions may have been reduced.

A false perception of nearing schistosomiasis elimination, combined with the discontinuation of control activities, could result in a resurgence of the disease in Brazil, as there are still areas with active transmission in several states of the country^30,31. If control activities are not resumed, there may be a significant increase in schistosomiasis infection rates¹². This has already been reported, and the situation might worsen due to the interruption of neglected tropical disease control programs during the COVID-19 pandemic^27,32,33.

Schistosomiasis is a chronic, debilitating disease that imposes a significant burden on the Brazilian public health system. The recent decline in PCE activity coincides with an increase in reported schistosomiasis lethality, leading to higher in public healthcare costs³⁴. In most endemic areas, control primarily relies on diagnosis and preventive chemotherapy for at-risk populations. Therefore, continued PCE efforts are crucial for disease control and achieving the Sustainable Development Goals outlined in the 2030 agenda^35,36.

As this study relied on secondary data, limitations exist regarding data availability and utilization. Endemic areas might have issues with incomplete reporting, leading to missing or unknown schistosomiasis information. Additionally, the ecological study design prevents us from establishing causal relationships. Despite these limitations, the data provided statistically significant insights. It revealed a concerning decline in PCE activity, jeopardizing Brazil’s goal of eliminating schistosomiasis as a public health issue by 2030³⁵.

This decline in PCE activity poses serious public health threats. Without the program’s early diagnosis efforts, the number of severe cases increases, leading to higher healthcare system costs. The gradual decrease in control activities over the past five years has reached worrying levels. It hinders early diagnosis, potentially leading to an expansion of endemic areas, a rise in severe cases, and a significant financial burden on the health sector.

ACKNOWLEDGEMENTS

The authors would like to thank the Ministry of Health for providing the data.

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• Financial Support: Not applicable.

Publication Dates

• Publication in this collection
  29 July 2024
• Date of issue
  2024

History

• Received
  15 Jan 2024
• Accepted
  29 May 2024