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Scorpion envenomation in Brazil: Current scenario and perspectives for containing an increasing health problem [1]

['Clara Guerra-Duarte', 'Diretoria De Pesquisa E Desenvolvimento', 'Fundação Ezequiel Dias', 'Belo Horizonte', 'Minas Gerais', 'Rafael Saavedra-Langer', 'Departamento De Bioquímica E Imunologia', 'Icb', 'Universidade Federal De Minas Gerais', 'Alessandra Matavel']

Date: 2023-02 

Opportunistic scorpion species can colonize urban environments, establishing high-density communities that enhance the chances of human accidents. This scenario has been taking place in Brazil, in which some Tityus species have taken city centers, causing an explosion in the number of scorpion envenoming cases. The characteristics of this scorpionism epidemic in Brazil is discussed in the present work. The number of Brazilian scorpion stings has surpassed 120,000 cases in 2017, and has been maintained above this number ever since, representing a more than 3-fold increase in 10 years, which was higher than the number of cases for most of the neglected tropical diseases in the country. The escalation in scorpionism cases is even higher in some regions of Brazil. Fortunately, the proportion of mild cases has also increased in the analyzed period, as well as the number of victims seeking for medical attention within the first hour after the accident. The species Tityus serrulatus, Tityus stigmurus, Tityus bahiensis, and Tityus obscurus are traditionally accountable for most of the scorpion accidents in different regions of Brazil, but other species deserve to be closely watched. Despite scorpionism being a notable health problem in Brazil, accident prevention and pest control regarding this venomous animal have not been properly addressed by the scientific community nor by policy makers. Therefore, this review also aims to point possible fields of research that could help to contain the aggravation of the current scorpionism landscape in Brazil.

The presence of scorpions in Brazilian urban centers has been increasing over the last decade and has led to an important augmentation in the number of human accidents in this country. This review aimed to better understand this scorpionism epidemic in Brazil, analyzing the evolution and dynamics of the accidents per region, the victim’s profile, and the outcomes of the resulting reported cases. The main scorpion species related to these accidents were reviewed, but emerging threatening species are also pointed and discussed. Considering this current medical emergency, it would be expected to have more preventive measures being proposed by the political and scientific community, but this has not been observed. Therefore, this work also suggests different fields that could be important points of action to reduce and contain problems related to scorpionism. These recommendations ranges from improvements in housing and education in all levels to chemical, biological, and genetic forms of control of scorpion populations. The effort made in this review intended to call attention to the scorpion problem in Brazil and to be part of the solution.

Despite the accumulated knowledge, along more than a century, on several aspects of scorpions, ranging from venom composition to ecology, scorpionism is not a solved issue in Brazil. A substantial annual increase in the number of reported incidents, surpassing the mark of 100,000 cases per year since 2017, has been occurring. No effective measures to contain this epidemic have been put in place, and, as a result, the number of accidents and deaths continues to grow. This constant increase in scorpion stings in Brazil raise concerns and demands a deeper understanding of the environmental, demographic, and socioeconomic factors associated, the implications of these incidents, the identification of the scorpion species, and how to better prevent them. This review aims to gather the available information concerning scorpionism in Brazil and proposes future directions to cope with this urban pest.

Brazil is comprised within these scorpionism’ hot spots. Casualties with these arachnids have been described in the country since 1915 [ 11 ], the same period in which antivenom therapy for scorpion stings was also developed locally [ 12 ]. Notwithstanding, scorpionism is likely to be occurring in the area long before that. It has been hypothesized that colonizing incursions in the country’s interior have disturbed the original habitat of some scorpion species, and the foundation of new towns created new exploring possibilities for these animals [ 6 ].

On the other hand, there are opportunistic scorpion species, capable of adapting and colonizing disturbed environments, living in high-density communities. This group can reproduce quickly [ 4 ] and can survive without food for long periods [ 5 ], which warrants them to thrive even amid unnatural conditions, like urban centers [ 6 ]. This life strategy causes the substitution of endemic species by opportunistic ones in disrupted or anthropized environments and can lead to increased chances of human encounters, resulting in harmful accidents [ 4 , 7 – 9 ]. This phenomenon occurs in several places in the world that are afflicted by scorpionism, such as North-Saharan Africa, Middle East, India, Mexico, and South America [ 10 ].

Scorpions are a very ancient group that originated as terrestrial animals approximately 300 million years ago and have persisted ever since [ 1 ]. They are widespread around the globe, present in all continents apart from Antarctica, and are adapted to a variety of environments, including high altitudes, deserts, rainforests, and caves [ 2 ]. Some scorpion species are endemic and dependent of their original habitats’ natural conditions, living in small populations with restrict mobility [ 3 ].

2. The problem: Scorpion envenomation in Brazil

To access epidemiology data of scorpionism in Brazil, the SINAN (Sistema de Informação de Agravos de Notificação) database from Brazilian Ministry of Health, which compiles health data of compulsory notification, was consulted. Data on reported scorpion accidents from 2007 to 2019 were evaluated. This time frame was chosen because the database system was modified in 2007 and the collected information pattern differed from the previous period (2000 to 2006) [13]. Data from 2020 and 2021 are still under revision. However, considering that 2020 was an atypical year due to the Coronavirus Disease 2019 (COVID-19) pandemic, we assumed it would be informative to access preliminary numbers on reported cases and deaths in this year. After 2020, scorpion accidents reported in Espirito Santo state are no longer available in SINAN database, as the state is reporting data on their own platform from thereon, which will compromise future analysis using SINAN data. SINAN was last updated in January 24, 2022.

Even though SINAN is a very important asset to study the epidemiology of scorpionism and other medical conditions in Brazil, inconsistencies in the available database concerning envenoming numbers have been found [14–16]. In addition, there is evident underreporting of scorpionism cases. Even in urban centers, it is estimated that as much as 10% of scorpion stings may not be reported to the official surveillance system [17]. Indeed, Tanajura and colleagues [18] detected that 4.35% of scorpionism cases that received medical attention in the state of Bahia were not reported to the national system. Therefore, the data presented in the following results must be critically analyzed, considering these restrictions.

Fig 1A shows the numbers of scorpion accidents monthly reported in each geographical region of Brazil, from 2007 to 2020. The number of notifications shows a constant increase along the years. The absolute number of accidents were substantially higher in the Southeast and Northeast regions since the beginning of the analyzed time-series, but all regions indicated a constant augmentation, notably in Midwest. The preliminary number of reported scorpion accidents in 2020 did not significantly increase but remained above 100,000 cases in this period. Considering that in 2020, due to the SARS-CoV-2 pandemic, people initially avoided seeking for hospital emergency care for conditions other than COVID-19, resulting in reductions of around 50% in emergency hospital attendance in Brazil [19,20], we hypothesize that the 2020’s accident numbers are likely to be highly underestimated.

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TIFF original image Download: Fig 1. Reported scorpion accidents and related deaths in Brazil from 2007–2020*. (A) Number of reported scorpion accidents per month for each region. (B) Number of reported deaths related to scorpionism per year for each region. Death incidence per 100,000 inhabitants’ values for the years of 2007 and 2020 are written at the curves’ extremities. (C) Brazilian map showing scorpion incidence per federal unit in the year of 2019. Color intensities correspond to incidence rates, according to the legend. (D) Increase of incidence of scorpion accidents between the years of 2007 and 2019 per state. (E) Increase of incidence of neglected tropical diseases of compulsory notification between the years of 2007 and 2019 in Brazil. Graphs were produced using GraphPad Prism 9.0 software, and the map figure was produced using QGis software. The Brazilian map’s shapefile was downloaded from the Instituto Brasileiro de Geografia e Estatística–IBGE website (https://portaldemapas.ibge.gov.br/). Scorpion accidents and other neglected diseases numbers were recovered from the SINAN Database and Brazilian population numbers and estimatives, used for the incidence calculus, and were recovered from Brazilian Institute of Geography and Statistics (IBGE—Instituto Brasileiro de Geografia e Estatística). https://doi.org/10.1371/journal.pntd.0011069.g001

Several studies in Brazil and in other countries have reported seasonality of scorpionism occurrence of [21–31]. According to the data presented in Fig 1A, scorpion accidents present a constant variation, tending to be more frequent in the warmer and rainy seasons. This marked seasonal variation behavior is well observed in the South, Midwest, and Southeast regions, but is less pronounced in Northeast and North, which may reflect the less evident seasons in these areas, as also acknowledged before in epidemiological studies concerning these regions [32–34]. Nevertheless, Monteiro and colleagues [17] observed that the Northern states, which are impacted by river floods in rainy season, have a positive correlation of this period with scorpion stings.

Despite the increase in the number of scorpion accidents, the number of deaths reported up to 2019 for each region did not present the same constant raising pattern, as seen in Fig 1B. However, in the year of 2020, when the number of reported scorpion accidents was lower than in 2019, the number of deaths seems to have skyrocketed. This could be an effect of envenomation complications, since people were avoiding going to emergency rooms due to the COVID-19 pandemic, and it has already been stated that envenoming outcome depends on the time in which medical treatment starts. We stress that numbers from 2020 are still under review, and notification errors could have occurred, as personally communicated by the technical group on venomous animals of Brazilian Ministry of Health, when consulted by email about these numbers. Nevertheless, until the date of this article’s submission (November 2022), numbers had not been updated, remaining as reported here. We calculated the death incidence per 100,000 inhabitants, per region, for the years of 2007 and 2020, using population numbers estimated by the Brazilian Institute of Geography and Statistics (IBGE—Instituto Brasileiro de Geografia e Estatística). The calculated incidence is shown by the numbers at the beginning and at the end of each curve in the graph (Fig 1B). If the real numbers are indeed within the reported range, death incidence per 100,000 habitants may have more than doubled for the regions with the highest number of cases and showed a 6-fold increase in the Midwest.

Fig 1C shows the Brazilian political map colored according to the scorpionism incidence per 100,000 inhabitants in 2019 for each Brazilian state, demonstrating high variability along the territory. Incidence ranged from approximately 4 cases/100,000 inhabitants in the state of Rio de Janeiro (RJ) to 300 cases/100,000 inhabitants in Alagoas (AL) and seems to be higher in the eastern part of Brazil. This map also highlights accidents’ hot spots, represented by the orange spheres. The sphere size is related to the absolute number of accidents occurring within a microregion. It is noteworthy that while in Southeastern states scorpion accidents are distributed more evenly through their territory, in Northeastern states, accidents are more concentrated in the state’s capitals, where most of the states’ population lives.

In face of this concerning rise in scorpionism, we can speculate on the current factors leading to it. According to IBGE (Brazilian Institute of Geography and Statistics) data [35], Brazilian population continues to grow every year. Therefore, it would be reasonable to assume that the increase observed in the number of scorpion stings could be following the population’s growth, and, therefore, the scorpion accident incidence would not change as much over the years. To address this possibility, we have calculated the rates of scorpion accidents incidence increase for each state, comparing the rates reported in 2007 and 2019 (Fig 1D). National average reveals that the number of reported scorpion accidents/100,000 inhabitants increased in all states, with a mean increase of 5.75-fold during this 13-year period, suggesting external factors leading scorpionism increase in the country. The scorpionism incidence in states that are traditionally inflicted by this condition, like Minas Gerais (MG), São Paulo (SP) (Southeast), and Bahia (BA) (Northeast), have grown below the national average range. Other states, despite not having high incidence rates in 2019, deserves attention due to the increase of more than 10-fold in the accident rate, which is the case of Maranhão (MA) and Ceará (CE), in Northeast, and Mato Grosso do Sul (MS) and the Federal District (DF), in Midwest. Also in this region, the state of Goiás (GO) presented a relevant increase, indicating that Midwest may be experiencing the effects of Tityus serrulatus colonization, as further discussed in the session below. The southernmost state of Rio Grande do Sul (RS), where scorpion accident reports increased more than 8-fold, is also a point of attention.

As reporting of scorpion accidents became mandatory in healthcare facilities only since 2010, the increasing number of reported cases could be simply a result of more notifications being processed, and not an increase in the number of accidents by itself. However, this reason alone may not explain the constant rising numbers, especially observed after 2017, as reported accidents with other venomous animals, such as snakes, did not follow the same pattern, with numbers fluctuating around 30,000 accidents per year throughout the analyzed period. Indeed, scorpion accidents is one of the only conditions of compulsory notification that present consistent growth along the years. When compared to other neglected tropical diseases notified to same national system in Brazil (SINAN), scorpionism is the condition with the highest raising trend and one with the highest absolute numbers of notifications (Fig 1E).

Since scorpions are affected by the environment, some studies have claimed that climate factors, such as global warming, could increase scorpion proliferation, maturation, and distribution [36–38], contributing to the observed accidents’ raise. Lacerda and colleagues [39] evaluated geographic and epidemiological characteristics of scorpion envenomation in São Paulo state and identified environmental factors that may be associated with these incidents. All the detected higher-risk areas presented lower precipitation, warmer temperatures, and a lower percentage of natural vegetation coverage, indicating a possible association of these factors with the occurrence of scorpion accidents. Interestingly, the percentage of urbanization was not different between the lower- and higher-risk areas, despite areas with less natural vegetation can be implied to be more urbanized [40]. More studies evaluating the correlation between rates of scorpionism, climate, and other environmental factors are important to predict future trends and to help to cope with the current epidemic [39,40]

Considering the demographic characteristics of envenomed victims, the main profile has not change much between 2007 and 2019 (Fig 2). The proportion of accidents involving adults (20 to 64 years) and the elderly (>65 years) raised about 3%, whereas for the young population (10 to 19 years) and children (0 to 9 years), it has decreased at approximately the same rate (Fig 2A). These changes may reflect a demographic transition, with an observed aging of Brazilian population due to lower fertility and augmentation of life expectancy [41].

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TIFF original image Download: Fig 2. Demographic characteristics of scorpionism victims from 2007 to 2019 in Brazil. Bar graphs show the proportion of scorpionism victims along the years according to (A) age groups, (B) sex, and (C) auto-declared race. Numbers next to the first and the last bars represent the percentage of each analyzed group in the year of 2007 (left) and 2019 (right). Graphs were produced using Microsoft365 Excel software. Scorpion accidents’ information were recovered from the SINAN Database. https://doi.org/10.1371/journal.pntd.0011069.g002

Opposed to what is observed for snakebite, scorpion accidents occurred in both sexes proportionally (Fig 2B). Snakebite is often associated with occupational risk, victimizing mostly agricultural workers, which are male in their majority [42]. As scorpion stings are more likely to occur within households or their surroundings [43], it has affected males and females indistinctively. However, when considering only the North region (S1 Table), the accident profile resembles those for snakebite, affecting more men in rural areas, as described previously [44–46]. On the other hand, women were more frequently stung by scorpions in Rio Grande do Norte (RN), in the Northeast region, which can be possibly related to scorpion urbanization, leading to incidents opportunities when performing housework, which is mostly a female activity in the state [32]. The larger prevalence of scorpion accidents in females was also noted for Bahia [47], Ceará [48], and Sergipe [49], which are also states from the Northeast region of Brazil. This divergency in scorpionism sex prevalence in Brazil demonstrates that assumptions made from combined data must be made carefully, when considering such a large and heterogenous country like Brazil.

According to the reported 2019’s National Household Sample Survey from the Brazilian Institute of Geography and Statistics (IBGE), it is estimated that 42.7% of Brazilians declare their race as White, 46.8% as Mixed (named as “Pardos” locally), 9.4% as Black, and 1.1% as Indigenous or Asian. The “mixed” population seems to be the most hardly hit by scorpionism, in a consistent tendency through the years, as it represents the majority (around 60%) of the scorpionism victims (Fig 2C). This higher incidence among the “mixed” population can be related to the higher social vulnerability of this group, which results in worst habitational conditions, lower access to water, sanitation, and proper waste management, leading to higher exposure to vectors, including scorpions [50]. It is important to underline that, even though the Indigenous population accounts for less than 1% of SINAN reported scorpion accidents, a study made with an indigenous community in the state of Acre (North) found that 14% of them had already been stung by scorpions at least once in their lifetime. This indicates that, although the indigenous group contributes with only a small proportion to the totality of scorpion accidents in Brazil, scorpionism is a relevant issue inside this community [51].

To further characterize the profile of scorpion accidents occurring in Brazil between 2007 and 2019, we accessed the time victims took to search for medical attention, as it is a fundamental parameter to ensure treatment success and prevent aggravation, and the severity grade of the accidents (Fig 3). The proportion of scorpionism victims searching for treatment within the first hour of envenoming has increased over the analyzed period, from 43.7% in 2007 to 59.4% in 2019 (Fig 3A), as already pointed by Chippaux in 2015 [52]. This shift is very positive, as the efficacy of the antivenom treatment is strongly related to the period in which it begins [53,54]. However, a proportional reduction in mortality due to this faster medical care intervention is not observed, but the proportion of mild cases has also increased.

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TIFF original image Download: Fig 3. Medical aspects of scorpion accidents from 2007 to 2019. Bar graphs show the proportion of scorpionism victims along the years according to (A) the time elapsed from the accident until they searched for treatment, (B) the severity grade of envenoming, and (C) the age distribution of scorpionism victims according to accident severity grade and death. Numbers next to the first and the last bars represent the percentage of each analyzed group in the year of 2007 (left) and 2019 (right). Graphs were produced using Microsoft365 Excel software. Scorpion accidents’ information were recovered from the SINAN Database. https://doi.org/10.1371/journal.pntd.0011069.g003

Indeed, although the absolute numbers of accidents in all severity grades have raised unquestionably, the proportion of registered mild cases has increased from 83% to almost 90% of the total cases (Fig 3B). As a result, the percentage of moderate and severe cases were reduced in 2019 when compared to the first year of this time series. We can hypothesize that the substantial growth in the total number of registered scorpion envenoming cases may be due to more people searching for healthcare, even if it turns out to be mild envenoming, as a result of better information of the population about the conduct after a scorpion sting. On the other hand, the higher proportion of mild cases can reflect the faster medical care, as already mentioned. As people would look faster for the treatment, cases would not aggravate.

As it is well known that children are particularly vulnerable to scorpion venom [55], we analyzed case severity and deaths according to victim’s age (Fig 3C). The data show clearly that 0- to 9-year-olds are the group most vulnerable to aggravating envenoming, as this age group correspond to only about 10% to 13% of mild cases but represent almost half of severe cases, in a consistent pattern over the years. Lethality rates are also higher in this group as, although they account for less than 15% of total scorpionism cases, children under 9 represent more than a third of all fatal victims of scorpionism. It is relevant to stress that the proportion of adults in the total number of deaths in 2019, reaching almost half of all fatalities in this year, reveals that the life risk of scorpion envenoming cannot be disregarded in any age group.

Brazil is a country of continental dimensions and is very heterogenous in terms of climate, biomes, economic development, etc. Even inside a same state, broad variation in scorpionism incidence has been reported, as shown in Fig 1D [46,56]. More accurate identification of these scorpionism hot spots within Brazilian territory may be useful for allocating adequate resources for preventing and treating accidents, better reflecting the reality of the populations at greater risk [57]. Amado and colleagues [58] attempted to determine these vulnerable areas, considering not only accident incidence but also climatic niche modeling for all medically relevant species, investments in public health, accessibility to adequate treatment (hospital infrastructure and antivenom availability), and demographic data. This analysis put the North and Northeast regions as the higher priority for health investments. Nevertheless, the high absolute numbers of accidents in the Southeast and the elevated incidence growth observed in the Midwest and South regions contribute to the worrying picture installed in Brazil as a whole.

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