Original Research | Published: 16 April 2024
open-url

Epidemiological and sociodemographic description of snakebite envenoming cases in Paraguay reported between 2015 and 2021

https://doi.org/10.1136/bmjph-2023-000359

Request reuse permissionopen-url
This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) licenseopen-url

Abstract

Introduction Snakebite envenoming (SBE) is a public health problem in Paraguay where the presence of 15 medically important snake species has been reported. Blessed with large forested areas, its economy largely relies on agricultural production which increases the exposure of outdoor workers to the morbidity and mortality of SBE. Lack of sufficient and accurate epidemiological data highlights the importance of drawing an updated picture of SBE burden in the country.

Methods We performed a retrospective descriptive study on secondary SBE data reported to the national surveillance system between 2015 and 2021. We addressed the availability and quality of the data and assessed its epidemiological and sociodemographic burden in Paraguay over that time period.

Results In total, 1651 cases of SBE were reported between 2015 and 2021 representing an average of 235 cases per year (3.33 cases per 100 000 population). Overall, young males (68%, n=1125) of productive age (25 years old, IQR 29) in agricultural and/or livestock settings (47%, n=653) were the most affected population. Departments with a higher number of notifications were San Pedro (12%, n=191), Caazapá and Alto Paraná (10%, n=163). Regarding data quality, variables about clinical outcomes, treatment administration and case management were the worst reported.

Conclusion SBE is a public health issue that affects young workers in rural areas in Paraguay. It mostly remains unattended and improvements in its reporting need to be done in order to gain a better insight into both the health and social burden of this neglected disease.

What is already known on this topic

  • In Paraguay, snakebite envenoming (SBE) represents a public health problem considering the presence of large forested areas in the country, its close relationship with agricultural activities, the morbidity it causes and the cost of antivenoms. This, together with the lack of sufficient and accurate epidemiological data, makes it important to have an accurate picture of the burden of SBE.

What this study adds

  • The epidemiological trend and geographical distribution of SBE in Paraguay has remained stable in the last two decades. Young males of productive age in agricultural and/or livestock settings have been the most affected, suggesting that SBE in Paraguay is an occupational disease and that more prevention measures should be applied at the workplace and households.

How this study might affect research, practice or policy

  • This work shows a reasonable estimation of the epidemiological and sociodemographic picture of SBE in Paraguay between 2015 and 2021. It is the first to include clinical, case management and treatment characteristics and to report the quality and availability of data coming from the notification system. Moreover, it shows the importance of quality mandatory reporting on better characterisation of the disease burden, improvement of patient care and the planning of resource allocation.

Introduction

Snakebite envenoming (SBE) results from the injection of the toxic secretion (venom) by a venomous snake into tissue or the bloodstream. The bite of the venom is usually accidental and it can result in a syndrome with a wide range of clinical manifestations denominated ophidism that constitutes a medical emergency due to severe sequelae and life-threatening consequences if not treated timely.1

SBE was recently included in the group of neglected tropical diseases (NTDs).2 Although the exact number of accidents by SBE is not yet known because of systematic under-reporting, it is estimated that every year between 1.8 and 2.7 million envenoming accidents occur worldwide. Moreover, SBE alone is the cause of around 94 000 deaths yearly and around triple the cases of amputations and permanent disabilities globally.3 4

The inclusion of SBE in the WHO’s NTD portfolio gave powerful attention to this disease. In 2019, the ‘Global Strategy for Prevention and Control of Snake Envenoming’5 was issued setting the goal to reduce mortality and disability from SBE by 50% before 2030.

In the Americas, it is estimated that between 80 229 and 129 084 cases of SBE and 560 to 2298 related deaths occur annually.6 Particularly, regions of eastern Paraguay and southeastern Brazil have been identified as SBE hotspots with the highest incidence of snakebites in the continent.7

In Paraguay, SBE is both an occupational and environmental problem. Vulnerable populations are mostly located in rural areas, where it is a disease of young agricultural workers and a hazard for indigenous nomadic tribes and homeless populations.8 The Ministry of Health and Social Welfare has included SBE among the zoonoses that are considered neglected,9 and it certainly represents a public health concern considering the presence of large forested areas, its close relationship with agriculture and livestock activities, its associated morbidity and the lack of access to safe and affordable treatment.7 It is estimated that snakebite accidents caused 258 years of life lost in 2019,10 and currently there are more than 227 000 people at risk living in areas with described presence of one or more venomous snake species of medical importance and a travel time longer than 3 hours to urban centres.11

The lack of updated epidemiological figures and accurate information on SBE cases is a recognised global problem.1 5 In most Latin American countries, including Paraguay, the systematisation of epidemiological data collection of these events is recent.12 In 2007, the Pan American Health Organisation (PAHO/WHO) encouraged the countries of the region to declare SBE as a mandatory notifiable event in order to gain a more accurate picture of the health and social impact of this health problem.13 Yet, the mortality and the morbidity translated in disability linked to snakebites in the Americas is still estimated from medical and scientific literature, which may lack precision and representativeness.8 13 This is as well the situation in Paraguay, where information on the health and social impact of SBE is very limited.7

SBE is among the notifiable diseases in Paraguay as established by the General Directorate of Disease Surveillance (GDDS), the ministerial body in charge of the National Epidemiological Surveillance System (NESS).14 According to the most recent published data based on notified cases of SBE in the country, between 2004 and 2015 the average number of SBE accidents was 250 cases per year with an incidence of 3.7 cases per 100 000 inhabitants and a case fatality rate of 2%.12 15 16 Most cases were reported in northern and eastern Paraguay and men of productive age working in the agricultural sector in rural areas were the most affected population. The majority of SBE cases in the country are caused by Bothrops sp and Crotalus sp (family Viperidae) and to a lesser extent by Micrurus sp (family Elapidae).17 18

Taking into account the importance of this disease at a public health level and the lack of recent and reliable data on its burden, the aim of this study is to describe the epidemiological profile of SBE cases notified in Paraguay between 2015 and 2021. Furthermore, by assessing the availability and quality of the data, our analysis also incorporates sociodemographic, clinical and treatment information of SBE as well as case management characteristics during that time frame.

Methods

Data collection

A descriptive observational study was conducted using secondary data obtained through the NESS mandatory case reporting system on snakebite cases in Paraguay. All notified SBE cases through the NESS during the period 2015–2021 were included for the analysis.

The type of surveillance of SBE in Paraguay is universal and it is mandatory for health providers (ie, health facilities including primary care centres and hospitals from public and private systems) to report cases according to the definition of a suspected case (any person who was bitten by a snake) and confirmed case (those cases where the species involved in the accident could be identified). After the form is filled on admission of the patient, it is sent to the GDDS, whose staff is responsible for manually entering the data into databases.14

The notification form is filled out manually by health professionals on arrival of the patient to the health facility. The variables collected can be grouped according to their characteristics in the following categories: epidemiological (department of notification, year, month, place, time of the day of the accident, snake species involved), sociodemographic variables (age, sex, occupation, ethnicity), clinical variables (anatomical place of bite, local and generalised signs and symptoms, sequelae, death, severity), treatment variables (antivenom administration, time between SBE and treatment administration, adverse reaction to antivenom) and clinical management variables (health facility level of complexity, inpatient admission, facility referral, intensive care unit (ICU) admission).19

Authorisation for the transfer and use of their data was requested from the GDDS and the National Zoonosis Program and Anti-Rabies Center (SBE disease control programme directly dependent on the GDDS). The databases containing the information collected by the individual notification forms for snakebite cases were anonymised and later transferred through a secure server by the GDDS in Microsoft Excel format. Then, the information was transferred to a Microsoft Excel spreadsheet for data cleaning and validation and subsequent analysis.

Data on the population of Paraguay for the period 2015–2021 and for each department were extracted from the latest national census data available at the National Statistics Institute of Paraguay web page.20

Data quality assessment

A description of the available variables, both in the notification forms and the database, and a later comparison between them was carried out. From those variables included in the GDDS database and therefore available for a potential analysis, the quality of data was assessed through the calculation of the percentage of missing observations (number of missing observations/total number of observations during the 2015–2021 period). This study considers that a variable has good quality when it presents less than 10% of missing observations as the proportion of missing data is directly related to the quality of statistical inferences.21

Data analysis

We used the STATA V.17.0 package22 for the descriptive statistics analysis on epidemiology, sociodemographics, clinical, medical treatment and management data. We report absolute and relative frequencies of categorical data, and mean, SD, median and IQR for continuous variables. Univariate analysis was performed using CI at the 95% level. Tables and figures were made using both STATA and Microsoft Excel. For the heat map we used http://www.heatmapper.ca/geomap/.23

Those variables not available in the database provided by the GDDS (not entered from the notification forms into the GDDS database) and those that showed high levels of missing observations (>70%) were not included for the descriptive analysis.

Results

Between 2015 and 2021, a total of 1651 cases of SBE were reported in Paraguay, representing an average of 235 cases per year (0.3 cases per 10 000 population). The highest prevalence was observed in 2017 (0.6 cases per 10 000 population). From that year the number of reported cases decreased to a prevalence of 0.2 in both 2020 and 2021 (figure 1).

Figure 1
Figure 1

Year-specific distribution of snakebite cases (cases per 10 000 population) reported between 2015 and 2021 in Paraguay.

Of the total number of reported cases (n=1651), most of them were reported in the eastern region of Paraguay (86%, n=1414). The departments with the most notifications were San Pedro (11.6%, n=191), Caazapá and Alto Paraná both with 163 cases (10%), and Concepción (9%, n=153). The highest snakebite rate (cases per 10 000 population) over the 7 years was observed in the departments of Alto Paraguay (49.5) and Ñeembucú,11 followed by Presidente Hayes (9.2) and Caazapá (8.7) (figure 2).

Figure 2
Figure 2

Department-specific distribution of reported snakebite cases during the 2015–2021 period.

The median age of the victims was 25 years (IQR 44–15). Males accounted for 68% of the cases (n=1125). Taking into account that the occupation of the victims is notified only since 2021 (reported cases, n=170), the group of agricultural and livestock workers was the most affected (28%, n=47/170), followed by that of the students (21%, n=35/170) and domestic workers (18%, n=31/170) (table 1).

Table 1
|
Distribution of SBE cases according to age group (years) (2015–2021), patient occupation and ethnicity (2021)

Snake species involved in the accident were not identified or not reported in about 57% of the cases (n=933 cases). Remarkably, snakes within the genus Bothrops were responsible for around 34% (n=563 cases) of the accidents, those from the genus Crotalus for the 7% (n=121) and involvement of Micrurus sp was reported in 0.1% (n=2 cases) of the cases. Also, 2% (n=32) were reported as ‘Other species’. The most frequent places where snakebite accidents occurred were farms or ranches (40%, n=653) and households (34%, n=560). In terms of time of day, we observed that the majority of cases occurred in the afternoon (12:00–19:00), with 27% of reported cases (n=451). This was followed by the morning (06:00–12:00) with 21% (n=350) and the evening (20:00–00:00) with another 21% of reported cases (n=353), as shown in table 1.

The highest proportion of cases during the 2015–2021 period happened during the summer season and beginning of autumn in the southern hemisphere, with the proportion of cases beginning to increase in the spring months from October to December (5.8–8.3%, n=97–137 out of 1651) culminating with the highest number of accidents (41%, 684/1651) being reported between January and March (13.3–14.2%, n=220–234). In the autumn and winter seasons the proportions were the lowest, especially in the months of June and July (4.2–4.5%, n=69–74) coinciding with the dry season in Paraguay (figure 3).

Figure 3
Figure 3

Distribution of snakebite notified cases according to month and seasonality between 2015 and 2021 in Paraguay.

Regarding the clinical characteristics presented by those affected, most bites occurred on the lower limb (81%, n=1296). In the case of local signs and symptoms, pain was the predominant symptom (92%, n=1377) while oedema at the bite site was the predominant sign in 985 cases (66%), erythema in 408 cases (27%) and abrasions at the bite site in 134 cases (9%). General manifestations were not reported or were absent in 68% (n=1137) of the patients. When reported, the most frequent symptoms were generalised pain (60%, n=352) and coagulopathies (53%, n=308). Haemorrhage was also reported in 79 cases (13%) and blurred vision in 76 cases (13%). About 18% of the cases where general clinical manifestations were reported (104/514) met the clinical criteria for severity, that is, presence of haemorrhage, shock, renal failure, respiratory failure or haematuria. Between 5% and 11% of cases (n=65–71) were reported to be asymptomatic, maybe due to dry bites (table 2).

Table 2
|
Distribution of cases according to anatomical place of bite, local and general clinical manifestations, administration of antiophidic treatment, time elapsed between SBE and its administration and the notifying health facility complexity level

About 75% of the patients (n=1233) needed inpatient hospitalisation. The majority of them (45%, n=744 cases) were first seen at a third level of complexity health centre, followed by a 38% of notified cases (n=621) who were attended for the first time in second-level facilities and only 98 patients (5.4%) who sought care at primary care level (table 2).

Regarding treatment, 93% (n=1543) of the notified cases and 95% (1423/1494) of those who reported presenting any local or general symptom received antiophidic treatment. The notified time elapsed between the snakebite and its administration was between 0 and 3 hours after the accident occurred for the majority of cases (57%, n=937). In 13% of the cases (n=220), the elapsed time was 6 hours or more. Only five cases (0.3%) reported receiving treatment after 24 hours or more (table 2).

In terms of data quality, among the 23 variables used to assess the SBE burden in the country, which were burden in the country, which were systematically collected through notification forms from 2015 to 2021,13 9 out of 23 variables (39%, 9/23) exhibited <10% of missing or unreported observations. These included "Age" (1% missing observations, 18/1651), "Sex" (0%, 0/1651), "Department of notification" (0%, 0/1651), "Year of notification" (0.3%, 5/1651) and "Month of notification" (0.2%, 4/1651). Additionally, 8 variables (35%, 8/23) had missing values raging between 15% and 69% (see tables 1 and 2) and 6 variables (26%, 6/23) showed missing values rates in between 70% and 100% of the total observations (n =1651). These variables predominantly fell into three categories: clinical outcomes, namely "Physical-psychological sequelae" (95%, 1574/1651), "Death" (96%, 1592/1651), "Clinical severity" (91%, 1137/1651), treatment outcomes, including "Adverse reaction to antivenom" (91%, 1507/1651) and clinical management, such as "Facility referral" (87%, 1430/1651) and "ICU admission" (98%, 1619/1651).

Discussion

According to the observations made from SBE notified cases between 2015 and 2021, the 1651 reported cases in Paraguay with an average of 236 cases per year are similar to that observed between 2004 and 2015 (250 cases/year), which indicates that the incidence has remained stable and is similar to the trend of the rest of the region.12 This highlights the lack of national policies for SBE control in Paraguay during the last decade and the need to implement new strategies to improve the situation. When compared with its neighbouring countries, the incidence in Paraguay appears lower than in Brazil (1.3 cases per 10 000 population) and Bolivia (1 per 10 000 population) but higher than in Argentina (0.2 cases per 10 000 population).12 24 At subnational level, the departments of Paraguay, Bolivia and Argentina that are parts of the Gran Chaco region, are the regions with the highest SBE incidence in each country (0.5–5 per 10 000 population in the Bolivian and Paraguayan Chaco and 0.5–15 per 10 000 in the Argentine Chaco) (figure 2).12 This highlights the need to consider the SBE phenomenon within geographical areas with the same ecosystem and not by political divisions.25

Demographically, men in their productive age were the most affected. The most frequently reported occupations in 2021 were agricultural and livestock workers, as well as domestic workers. This underscore the concept of SBE as an occupational disease.1 3 8 11–13 Providing a more detailed report of the victims’ occupations could enhance our understanding of the accident contexts and facilitate the implementation of preventive measures in the workplace.1 5 26

Notably, most of the cases were reported to happen during daytime and in farms and households. This goes in line with the observations by other studies carried out in Paraguay15 16 27 and could be explained by the fact that the presence of humans in snake habitats (open natural areas such as field crops, orchards and gardens, and rural areas) and during the hours with undergoing human activity increases the frequency of human–snake contact.28 29

The most reported genus of snakes responsible for the bites was that of Bothrops sp, which is consistent with the wide distribution and diversity of their species in the country and their aggressiveness when disturbed.17 Remarkably, non-reporting of the snake genus involved in the accident occurred in as much as 56% of cases (933/1651), which implies a significant increase from the 6% reported between 2004 and 200615 but stands at similar levels as it was reported between 2010 and 2015.16 27 This poor level of identification of the snake responsible for the bite, which compromises the selection of the most adequate antivenom treatment, could indicate a lack of technical knowledge of the health personnel and the general population. Still, it is difficult to discern whether this figure is due to the inability to identify the snake’s species or to actual underfilling of the variable in the notification form since it was observed that this variable lacked the answer option ‘Unknown’ in the collection tool used for notification.

Between 2015 and 2021 most accidents were reported in the summer and spring seasons, coinciding with most of the rainy season and increasing at the end of the dry season. This concurs with what has been reported in previous years12 15 16 and is in line with the natural behaviour of the snake species distributed in the country which are more active in hot and rainy seasons.4 17 Geographically, a majority of cases were reported in the northwestern and eastern regions of Paraguay, which are the areas with most agricultural activity in the country and agree with what has been formerly observed.12 15 16 Even so, the risk of suffering an SBE is higher in the western part of the country (the Paraguayan side of the Gran Chaco region), especially in the department of Alto Paraguay (49.5 cases per 10 000 people), which can be explained by the very low population density of the region (2% of the population of Paraguay) and for the large rural areas present in the area.

As in most studies at regional and national levels,8 27 28 involvement of the lower extremities and local clinical manifestations were the most reported clinical features. This may be due to lack of adequate protection during working hours (eg, wearing boots and long trousers, using light when walking at night, clearing bushes around workplace, etc).30 Recent assessment on the knowledge about snakebite prevention in SBE endemic countries has shown that among general population there is a high level of knowledge about snakebite prevention (73% of respondents, 95% CI 52% to 93%, p<0.001).31 Still, the maintained prevalence of snakebite at population level suggests that whether the preventive methods are not being adequately put into practice or people do not perceive SBE a threat of high severity.32

Coagulopathy and generalised pain are commonly reported symptoms that align with the typical effects of envenomation by Bothrops sp snakes.1 7 18 From 2010 to 2015, the same signs and symptoms were reported as the most frequent,15 27 but they differ with what had been observed during the period 2004–2010,33 where the most reported general involvement was renal failure. The percentage of 5–11% of cases not reporting any sign of symptoms is in agreement with the range of asymptomatic SBE in the American region which has been estimated to be between 10% and 40% of the cases.12

The majority of notifications happened in second-level and third-level facilities (38–45%). This could also explain the high levels of admissions shown in this study (93%) that suggest that most patients are admitted, after referral or not, in health facilities with inpatient capacity. This percentage of admission was also observed by Alonso et al,16 who hypothesised that this could indicate the presence of a high number of complications, whether mild or severe. Still, this study cannot conclude that this number is a reliable estimate of the severity of cases reported during 2015–2021 since it is possible that severe cases are being more often reported than mild cases since they are more prompt to seek care.

The time between a snakebite and antivenom treatment administration is of utmost importance since there is a directly proportional relationship between this and the number of complications and sequelae.1 26 30 Slightly more than half of the patients receive antivenom treatment timely. However, 15% of the patients received the treatment after six or more hours of the bite. Such a feature is in line with the fact that the largest burden of SBE lies on departments with large rural areas where it is necessary to travel long distances in order to reach a health facility. Means of transportation or the unavailability of treatment are known risk factors for late access to antiophidian treatment and thus for suffering complications.16 17 31

Observations obtained through this study might lead to an underestimation of the real burden of SBE. This study is based on secondary data from health facilities reporting which can only keep track of those SBE cases who sought healthcare. Moreover, as is known in highly endemic countries and as this study also suggests, the majority of people who suffer from SBE live and work in rural areas where health-seeking behaviour, health beliefs and access to healthcare are not optimal.1–4 8 11 31 A better characterisation of the real burden of SBE in Paraguay would thus imply both passive and active surveillance (eg, household survey).4 5

Due to the significant number of variables collected through the NESS with a high rate of missing observations (10–98% missing data), no further statistical analysis could be performed in this study. In general, lack of standardisation of the collection tool (notification form) and digitalisation of the information flow, including the processes of data entry at ministerial level, together with the low adherence to the surveillance guidelines at the notification points, were all observed to be determinants of the low quality of the available data, which in turn comprises its validity and reliability.

In addition, it was observed that information on victims mortality, presence of sequelae, adverse effects of treatment, as well as further information on patient clinical management had the highest missing data (87–98%). Most of these outcomes are observed during the follow-up of the cases, which usually occurs after filling out the notification form on arrival of the SBE to the health centre. This, together with the fact that single-centre prevalence studies based on clinical records present better data on this group of variables,27 33 suggests that the current information flow established by the NESS does not allow for the collection of information on patient’s clinical progress after admission. Improving the reporting of clinical outcomes, especially mortality and sequelae prevalence, will be of utmost importance since they are indispensable for the correct measurement of the impact of SBE in the country, and because they are part of the indicators established by the WHO’s SBE prevention and control 2030 goal.1 4 5 Moreover, improvements in the reporting of pharmacovigilance data and the volume of demand of treatment are also needed considering the many limitations on the production, distribution and access to safe and effective antivenoms encountered in Paraguay.8 34

Such encountered limitations encourage the Paraguayan NESS to establish more reliable notification workflow, improve the data collection tool including more detailed and standardised variables on epidemiological and clinical characteristics and to enhance the adherence to the notification system among healthcare workers through information and educational measures.

Despite this, to the best of our knowledge, this is the first work to aggregate GDDS data over 7 years and analyse their contents availability and quality. Moreover, it brings the most recent reasonable estimation of the SBE epidemiological situation in the country incorporating to the analysis and data assessment all the groups of variables collected through the notification forms.

Conclusion

Young males of productive age in agricultural and/or livestock settings represent the most reported cases, suggesting that SBE in Paraguay is an occupational disease and that more prevention measures should be applied at the workplace and households. The epidemiological and sociodemographic characteristics of SBE cases in Paraguay during the 2015–2021 period have not changed when compared with the 2004–2014. SBE is an unattended public health issue in Paraguay and improvements in the reporting need to be done in order to gain a better insight of both the health and social burden. This work shows the importance of improving information and its analysis and the direct impact that it can have on better patient care through proper planning of interventions, allocation of therapeutic resources and training of healthcare personnel.