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Epidemiology of accidents involving venomous animals in the State of Ceará, Brazil (2007-2019)

Abstract INTRODUCTION: Envenomation remains a neglected public health problem in most tropical countries. Epidemiological studies on accidents caused by venomous animals are scarce in the Northeast region of Brazil, mainly in the state of Ceará. The present study aimed to describe the epidemiological features of envenomation cases involving venomous animals in the State of Ceará, Northeastern Brazil, from 2007 to 2019. METHODS: The online Notifiable Diseases Information System was consulted for data on all envenomation cases involving venomous terrestrial animals. Data collected were evaluated for the number of accidents/year, number of accidents/zoological group, antivenom therapy, zone of occurrence, sex, age-group distribution, and deaths. RESULTS: A total of 54,980 cases were recorded, with the highest incidence being that of scorpion stings (67.2%), predominantly in women (52.4%; odds ratio=3.6; 95% confidence interval=3.5-3.8), equally affecting people aged 10-19 years and 40-59 years (21.4%), in the urban areas (odds ratio=10.3; 95% confidence interval=9.9-10.8), especially in the rainy months. Snakebites (16.7%) had an incidence of 8.1/100,000 inhabitants, but the highest case-fatality rates were observed in bee stings (1.3%) and spider bites (0.5%). Regarding therapeutic variables, a small percentage of people had access to serotherapy (5.3%). CONCLUSIONS This study highlights the accidents caused by terrestrial venomous animals as a public health problem that must be monitored in Ceará. Thus, our findings suggest that preventive actions against scorpion and bee stings should be intensified during the months of higher incidence to improve public policies for patient care.


INTRODUCTION
Due to the process of urban expansion, the shared spaces between humans and venomous animals are increasing, thereby increasing the risk of injuries 1 . Accidents caused by venomous animals occur frequently and represent a serious public health problem in tropical countries. Given this situation, permanent health surveillance actions should be implemented 2 .
Data from the National Toxic-Pharmacological Information System (Sistema Nacional de Informação Tóxico-Farmacológica -SINITOX) reveal that venomous animals are the second-largest agent of human intoxication in Brazil. However, the lack of clinics, laboratories, and qualified technical staff contribute to the still high number of cases 2,3 . Accidents caused by venomous animals, considered as a neglected condition in the world, are increasing every year 4 . In 2010, accidents due to venomous animals was included in the compulsory disease notification list (LNC) in Brazil 5,6 . Despite the high numbers, the real magnitude of epidemiological data is still inconsistent in Brazil due to the high rate of underreporting and the omission of data while filling out the notification/investigation forms 1 .
Accidents caused by venomous animals have a major impact on health as they compromise work activities, lead to socioeconomic damage, and impair the quality of life due to the possibility of sequelae and temporary or permanent disability. Thus, knowledge of the profile of the injury is essential to institute adequate vigilance in the prevention of cases and, consequently, deaths 7 . Epidemiological studies related to accidents involving venomous terrestrial animals are still very scarce in the state of Ceará. Considering this aspect, we aimed to describe the epidemiological profile of accidents caused by venomous animals that occurred in Ceará between 2007 and 2019.

Study area
The state of Ceará, located in the Northeast region of Brazil, is composed of 184 municipalities, with a population of 9,132,078 inhabitants in 2019, with approximately 75% living in urban areas 8 . Its territory covers an area of 148,894.7 km² and it is located in the "Polígono da Seca," characterized by reduced rainfall, high temperatures, caatinga vegetation, and generally fine and salty soils 8 .

Data collection
This was a retrospective study to describe and analyze the epidemiological characteristics of cases of accidents caused by terrestrial venomous animals, using the Notifiable Disease Information System (SINAN) platform for collecting data covering the period from 2007 to 2019, available on the DATASUS website (SUS Department of Informatics, maintained by the Brazilian Ministry of Health) (Ministério da Saúde, 2019). These data were made available for us by Coodenadoria de Promoção e Proteção à Saúde/COVIG of the Ceará State Health Department. We used the following variables: sex, age-group distribution, zone of occurrence, month of occurrence, time from bite until assistance, antivenom therapy, deaths, and case evolution. Data on deaths caused by venomous animals were obtained from the Mortality Information System (Sistema de Informações sobre Mortalidade -SIM) using the search for death category ICD-10 (from external causes), grouped with the codes X20 (venomous snakes and lizards), X21 (spiders), X22 (scorpions), and X23 (bees).

Ethics Statement
Strict ethical and professional aspects were followed, maintained, and respected as established in the Resolution of the National Health Council no. 466 of December 12, 2012, which recommended that research involving only secondary data in the public domain, without nominal identification of the research participants, does not require analysis by a research ethics committee.

Data analysis
The data were compiled and tabulated to determine the simple frequencies (n) and relative frequencies (%), and the results are presented in the form of contingency tables and graphs made using the Microsoft Excel 2016 program. The incidence, mortality, and case-fatality rates were also calculated. Demographic and population data from the Brazilian Institute of Geography and Statistics (IBGE) were used to calculate the incidence rates in Ceará for every 100,000 inhabitants. Fisher's test was used, and odds ratios (OR) were calculated to evaluate the association between the demographic variables and the venomous animal types involved in the envenomation 9 .

RESULTS
In the state of Ceará, there was a marked increase in the number of accidents due to terrestrial venomous animals over the last decade, jumping from 1,492 cases in 2007 to 9,629 cases in 2019 10 . A total of 54,980 cases involving venomous animals were recorded between 2007 and 2019 in Ceará. Of these, 37,606 (68.4%) were caused by scorpions, 9,193 (16.7%) by snakes, 4,375 (8.0%) by bees, 1,551 (2.8%) by spiders, 362 (0.7%) by caterpillars, and 1,272 (2.3%) by other species (Figure 1). Accidents caused by venomous animals occur throughout the year, following seasonal variations based on the aggressor species. In Ceará, the number of cases of scorpion stings increased from October to January, while envenomation incidents involving caterpillar and snake bites increased between June and July, and bee stings increased between August and September (Figure 2).

DISCUSSION
Brazil is one of the countries with the most experience in the diagnosis and treatment of cases involving venomous animals. There are four notification systems for registering envenomations and case-fatality rates in the country. Currently, the SINAN is the most-used tool for analyzing these cases 11,12 , but SIM remains the most appropriate system for analyzing mortality data 13,14 .
The SINAN has recorded a progressive increase in the number of notifications involving venomous animals every year in Brazil 4 . Our data reveal an upward trend in the number of incidents involving venomous animals in Ceará. However, it is not possible to analyze whether there has been a real increase in the number of cases over the years or an improvement in the reporting system. This growth trend in cases involving venomous animals is corroborated by studies in other states in the Northeast Region, such as Rio Grande do Norte 15 , Paraíba 2 , and Piauí 16 .
Previous epidemiological studies have confirmed the influence of human and environmental factors on the occurrences of incidents involving venomous animals in Northeast Brazil 17 , especially in the rainiest months 15,16,18 , corroborating our data. In our study, women were more vulnerable, and these results are in line with those of other epidemiological studies involving incidents caused by venomous animals in Brazil 19 and in the Northeast region 15,17,[20][21][22] . The predominance of men usually reveals their greater exposure to areas where there are risks of snakebites, and this is especially true for those performing manual civilian work, such as agricultural workers 15 . However, women and children are more exposed to scorpions, spiders, and caterpillars in the residential environment 23 .
Disorganized urban growth and industrialization, irrational use of natural resources, and ecological imbalance predispose the proliferation of venomous animals and promote overlap between the spaces used by humans and animals 24 . The increase in the population in Ceará probably impacted the occurrence of snakebites and scorpion stings, considering the increase in the volume of domestic waste 15 .
Previous studies in Ceará revealed a high incidence of scorpion bites that may have resulted from the high population density in the capital and from climatic conditions (high temperatures) and urban conditions (accumulation of waste and inadequate sanitation) that would facilitate the adaptation of scorpions to life in urban areas 20 . Thus, the implementation of educational programs for the prevention and treatment of envenomation by scorpions, offered to community and health agents, can be an effective measure of public policy to reduce the growing number of cases. Source: Sesa/Nuvep/Sinannet (2020) and SIM (2020) to death records. *There were two deaths from scorpion bites in the historical series, resulting in zero mortality. and case-fatality rates. **There were no reported lethal cases involving caterpillars in the period. Mortality due to envenomation by venomous animals is due to the toxicity of the venom, the amount inoculated, and the precocity and effectiveness of the treatment administered to the victim 25 . Children, adolescents, and the elderly are more vulnerable to snakebites and scorpion stings, with higher case-fatality rates 19 . In previous studies conducted in Ceará, it was found that the majority of incidents involving venomous animals occurred in an urban areas 15,20 . Our data reveal that bee stings changed the epidemiological picture of Ceará, which shows the importance of studies with this venom and that of updating the notification data so that public policies can be directed to the injured. In previously sensitized people, a single sting of a hymenopteran insect, such as a honeybee, can result in rapid death 26 . However, even in non-atopic people, multiple stings can lead to death due to the higher dose of injected venom 27,28 .
In case of incidents involving venomous animals that occur in the rural areas of many tropical countries in Africa, Asia, New Guinea, and South America, there are difficulties in accessing conventional medical treatment in hospitals, due to delays in transporting the victim or because of the preference for treatment by local traditional healers 28 . Hospitalization occurs in moderate and critical cases that require specialized care due to their prolonged symptoms and the possibility of death 29 . An important factor to note is that most incidents involving venomous animals occur in regions that are far from referral hospitals (rural areas), and delayed care can aggravate cases, possibly resulting in systemic sequelae, the need for amputations, and even death of the victim in a few hours 1 . Such situations that result in death outside the health facilities are not entered in the notification records of the Ministry of Health. Thus, in most cases, the numbers do not portray the reality 28 .
Treatment time is associated with the severity of the envenomation; therefore, victims must have early access to medical care and antivenom therapy, thus resulting in better prognosis 30,31,32 . Studies carried out in the states of Bahia 30 and Piauí 33 showed an improvement in the information provided to the population about the urgency of medical assistance in these cases.
A previous study 18 revealed that a total of 1,307 cases of bee stings were registered by Ceará in the SINAN, with only four deaths and a case-fatality rate of 0.3%, a value well below that found in our study (1.9%) using SIM death records. Such differences in the notifications of deaths may result from discrepancies in the updating of the mandatory notification systems (SIM and SINAN), which is a problem since SINAN identifies a marked increase in the number of deaths due to scorpion stings. The SIM shows a greater increase in the number of deaths due to bee stings, thus making it difficult to construct epidemiological scenarios 34 .
The underreporting of incidents involving venomous animals has been stated by several studies 17,35 . However, the increase in the number of cases over the years may reflect an improvement in the reporting system. Although Brazil has four national systems for recording, the information is still dissociated, resulting in data that may not represent the reality of this public health problem 35 . Thus, there is a need to analyze and periodically evaluate these notification systems, considering their strategic importance in decision-making in health service routines, public policies, and research 34,36 .
Up-to-date regional information is important for the development of epidemiological surveillance. A better understanding of the epidemiology of incidents caused by venomous animals in the state of Ceará should facilitate their prevention and management. Thus, more detailed studies are needed to clarify the clinicoepidemiological profile of envenomations, which will assist in the implementation of educational health care measures seeking to improve the assistance provided to victims.

ACKNOWLEDGMENTS
The authors express their gratitude to Coordenadoria de Vigilância em Saúde da Secretaria Estadual de Saúde do Ceará (COVIG/SESA/CE) and Núcleo de Vetores do Ceará (NUVET) for providing the epidemiological data.

FINANCIAL SUPPORT
Secretaria de Saúde do Estado do Ceará.

AUTHORS' CONTRIBUTION
MMCS and IMLAM conducted the survey and analysis of the data; LEMF performed statistical analysis and graphs; JRMB and RJBJ were involved in writing, edition, and improvement the manuscript. All authors discussed the final results and contributed to the final version.