Snakebite envenoming is one of the most overlooked tropical diseases worldwide. In 2017, the World Health Organization (WHO) added this condition to the Neglected Tropical Diseases (NTD) list with two objectives: the first one focused on making visible the complexities associated with the management of the snakebites, and the second one related to the development of a global strategy, including the participation of the local governments, international organizations, and the private sector.

In 2009, this condition was included in the NTD list; nevertheless, the WHO decided to delete it without further details.¹ Likewise, it may be argued that the increase in the worldwide antivenom supply generated a seeming safety image during the 2000-2010 decade, which finished when multiple poor-quality products caused a death crisis by envenoming in sub-Saharan Africa and India.

The WHO estimated that by 2019, nearly 5.8 billion people worldwide were at risk of facing any incident related to the venomous snakes and that 7,400 snakebites were registered per day. Likewise, this organization reported that the number of daily deaths ranges between 220 and 380, resulting in about 130,000 annual deaths by this cause.² Despite that most of the cases occur in India and sub-Saharan Africa, snakebite envenomings are also an issue in other regions of the world like the Middle East and Latin America. In this latter, Brazil, Mexico, Venezuela, Peru, Ecuador, Costa Rica, and Colombia are the most affected countries.³

Faced with this panorama, Mexico has been classified, on many occasions, as an outstanding antivenoms manufacturer in the region. Important universities in the country research this topic; nonetheless, reality shows that snakebite epidemiology has been poorly and disjointedly studied. Some factors explaining this issue prevalence in the country are the inadequate hospital coverage in rural areas, the deficiencies in the epidemiological surveillance, and the fact that most cases are treated locally, not in hospitals. Even though Secretaría de Salud reported about 3,700 new cases by 2017, some authors suggest this figure may reach 27,000 per year.³

Dirección General de Epidemiología from Secretaría de Salud is the governing body responsible for counting the snakebite cases. It reported 3,172 new cases in 2017; nearly 3,882 in 2018, and 4,095 new cases in 2019; with an incidence of 3.005 in 2017, 3.112 in 2018, 3.235 cases per 100,000 inhabitants in 2019 (see Results section). The latest research has suggested that factors like urbanization and even changes in biodiversity may explain the increase in the number of cases⁴; nevertheless, it is necessary to make changes in the epidemiological surveillance because it should emphasize the implementation of mechanisms that better identify the implicated species. Thus, the resulting epidemiological information would translate into concrete actions focused on supplying antivenoms and into concentrating the existing resources in the most vulnerable zones.

In Mexico, snakebite envenoming has not been treated as an NTD, and the obstacles the health system in our country faces are similar to the problems registered in other regions of the world; that is to say, under-reporting of cases, antivenom shortages, and the inappropriate administration of treatments. Regarding the available epidemiological data, it is noteworthy to question: how could we translate the epidemiological surveillance results into an efficient public policy to treat snakebites?

State of the Art

Scientific literature about snakebite epidemiology in Mexico is limited. In order to analyze it, it is possible to identify two large groups: the ones explaining the issue nationwide and the others studying the states in particular. As part of the first group, the works of Zúñiga-Carrasco⁵; Siria Hernández⁶, and González-Rivera are relevant.⁷ In the second group, Yáñez has studied this issue in Yucatán⁸ and Veracruz⁹; likewise, Almaraz-Vidal¹⁰ dealt with this problem in Las Grandes Montañas region in Veracruz.

Zúñiga-Carrasco et al. analyze the snakebite cases from 2000-2010 in Mexico. The authors describe that 48.7% of the cases were registered in subjects between 15 and 44 years old, an extensive age group that hinders the data analysis. The authors also found that men represented 64% of the cases, while women only 34%. Thus, they relate this difference with the subjects' occupation; that is to say, 44% of the cases are employed in the agricultural sector, 22% are students, and 17% are in charge of the household work. The authors suggest that the months with the highest mortality are January, February, and November because they coincide with the generalized decrease of temperature nationwide, influencing the snakes' behavior. In conclusion, the authors advocate snakebites be considered a vector-borne disease; consequently, the necessary measures must be taken for their treatment.

Siria Hernández's communications main objective is to describe the snakebite incidence during 2003 and 2007 in Mexico. Siria found that, during the mentioned period, 18,848 cases were registered in all the country; they pointed out that Oaxaca and Veracruz were the most affected states. Besides, she claims that the geographical and climate characteristics in those places enable the interaction between humans and snakes, which explains the high incidence in those states. Siria also identified that Bothrops asper caused nearly 48% of the snakebite cases. The most interesting part of this research is the conclusions because they suggest that snakebites' main problem is not the lack of antivenoms or their effectiveness. The real issue is that the healthcare personnel taking care of these emergencies do not have enough information.

In their article, González Rivera et al. analyze the snakebite incidence in Mexico from 2003 to 2006. To begin with, they emphasize the improvement in the epidemiological surveillance of this condition since 2003. They identify a registry of 15,219 cases in all the states from 2003 to 2006; Oaxaca, San Luis Potosí, Hidalgo, and Puebla are the most affected states. The touchstone of this research is that the snakebites registry is a more neglected issue among infants.

Concerning the states in particular, Yáñez Arenas et al. analyze Yucatán during 2003 and 2012. There were 821 cases in the nine years studied, and although this figure is not so high as the ones registered in other states like Oaxaca, Veracruz, and Guerrero, the authors claim that the endemic presence of snakes of medical importance is one of the most relevant reasons to analyze this state. When disaggregating data by municipalities, the authors found that two towns in Yucatán register higher incidence rates than those reported in Veracruz's municipalities, the most affected state. The authors explain that such circumstances respond to three factors: the small population size in the municipalities with higher incidence, the abundance of venomous snakes in the region, and the economic activities in this area.

Regarding Veracruz, Yáñez Arenas asserts that a factor explaining the high snakebite incidence is that the agricultural activities represent the main economic activity. The author describes 3,765 snakebite cases between 2003 and 2012 with an incidence rate of 49.2 per 100,000 inhabitants. Based on the epidemiological data record, the author points out a mortality decrease of 50% because of that cause compared to the 1980s. Nevertheless, the author also found that the number of new cases remained stable from 2003 to 2013; thus, he concluded that the actions taken by Secretaría de Salud del Estado had not had the expected effect: they have not reduced the number of cases.

Despite the methodological differences, all the research previously analyzed share four common points:

• snakebites are a health issue in Mexico;
• there are several inconsistencies in the recent cases registry, for instance, the snake identification;
• the number of new cases in Mexico has remained stable since 2003;
• there are various obstacles to effectively treat this problem, such as insufficient hospital coverage and the prevalence of non-tested treatments, based on plants.

Epidemiology of Snakebite Cases during 2017-2019

The analyzed data are the number of cases (number and percentage) and the annual incidence (cases per 100,000 inhabitants).

This information was processed using a Microsoft Access database to compare these two variables in 2017, 2018, and 2019. A map was drawn with R Studio's snakebite incidence to represent the cases' geographical distribution better.

The snakebite epidemiological data were taken from Boletín Epidemiológico del Sistema Nacional de Vigilancia Epidemiológica (SINAVE).¹¹ It is important to mention that this research's data are public and can be consulted free of charge. SINAVE generates and processes information from all the institutions affiliated to Sistema Nacional de Salud (according to Secretaría de Salud data, by 2020, SINAVE was composed of nearly 20,005 care units).¹¹ The notifications are processed according to the guidelines of established institutional channels with Comité Nacional de Vigilancia Epidemiológica as the head.

By 2017, 3,712 snakebites were registered in Mexico. The states with more cases that year were Veracruz (411 cases), Oaxaca (363), Puebla (318), San Luis Potosí (241), and Hidalgo (234). The five states with fewer cases were Colima (21), Baja California Sur (17), Baja California (15), Morelos (13), and Aguascalientes (11). Table 1 disaggregates the number of cases by estate, taken from Boletín Epidemiológico from SINAVE.

By 2018, 3,882 cases were registered nationwide, 170 more cases compared to 2017. The five states with more cases were Veracruz (460, +49), Puebla (375, +57), San Luis Potosí (309, +68), Oaxaca (265, -98), and Hidalgo (242, +8). The state with a higher increase of cases was San Luis Potosí, with 68 new cases. The five states with fewer cases were Baja California Sur (25, +8), Querétaro (22, -28), Colima (15, -6), Morelos (14, +1), and Aguascalientes (9, -2). Compared to 2017, Aguascalientes remained the state with fewer registered cases, followed by Morelos.

By 2019 there were 4,095 registered cases nationwide, 213 more cases than in 2018. The five states with more registered cases were Oaxaca (417, +152), Veracruz (401, -59), Puebla (379, +4), San Luis Potosí (367, +58), and Guerrero (289, +65). It is significant that in the three years analyzed, the highest increase was registered in Oaxaca with 152 new cases compared to 2018. The states with fewer registered cases were Baja California (23, -3), Colima (16, -6), Morelos (16, +1), Baja California Sur (15, -10), and Aguascalientes (10, +1).

Table 2 shows the rank (in descending order) the Mexican states have concerning the snakebite new cases. The states that remained steady from 2017 to 2018 were Veracruz (#1), Chiapas (#8), Tabasco (#9), Quintana Roo (#11), Morelos (#31), and Aguascalientes (#32). The states that remained steady from 2018 to 2019 were Quintana Roo (#11), Campeche (#23), and Aguascalientes (#32).

Boletín Epidemiológico reports the snakebite new cases per week (Table 3 for years 2017, 2018, and 2019). According to the figures, by 2017, most of the cases were registered in week number 38 (18 -24 September) with 142; in 2018, it was week 41 (9-15 October) with 140 new cases, and finally, in 2019 it was week 28 (10-16 July) with 130 new cases. The average of cases per week in 2017 was 70.75 cases, in 2018 was 71.67, and in 2019 was 76.519 cases. Thus, it is possible to claim an increasing tendency in the number of snakebites registered nationwide. The decrease in Mexico City first ranked 19 in 2917, 25 in 2018, and 24 in 2019 nationwide.

Table 4 shows the incidence comparison of snakebites in the 32 states from 2017 to 2019. In 2017, Oaxaca registered 8.99 cases per 100,000 inhabitants, followed by San Luis Potosí with 8.65, and Hidalgo with 8.03 cases per 100,000 inhabitants. In 2018, San Luis Potosí ranks first with 10.93, followed by Hidalgo with 8.11 cases, and Quintana Roo with 6.72 cases per 100,000 inhabitants. Finally, in 2019, San Luis Potosí remains in the first position with 12.89, followed by Oaxaca with 10.12, and Hidalgo with 8.03 cases per 100,000 inhabitants.

It is important to consider that if the cumulative incidence is considered (Figure 1), in 2017 Veracruz ranks the first with 11.07% of total cases, followed by Oaxaca with 9.79%, and Puebla with 8.56% of the total cases nationwide. In 2018, Veracruz remains the state with the highest proportion of cases nationwide with 11.85%, followed by Puebla with 9.66%, and finally San Luis Potosí with 7.96%. By 2019, Oaxaca occupies the first place with 10.18% of the cases; the second place was Veracruz with 9.79% and the third Puebla with 9.25%. Aguascalientes was the state with the lowest incidence: 0.296, 0.232, and 0.244 by 2017, 2018, and 2019, respectively (Figure 1). The population size may explain those incidences in every state and the decreased number of registered cases.

According to the regional classification of the country taken from Instituto Nacional de Estadística y Geografía (INEGI)¹⁴, it is likely that most of the snakebites cases occur in the Central region, with 40.7% in 2017, 37.25% in 2018, and 31.5% in 2019 (see Table 5). It is interesting that, regarding regions, the percentage remained steady in all of them; the North region and South region registered a slight decrease from 2017 to 2019.

In general, it is possible to claim that most of the snakebite cases in Mexico affect more males. Data of the new disaggregated snakebite cases are shown in Table 6 per gender of the victims. In the annual aggregates, in 2017, nearly 67% of the registered cases were men, compared to 33% women. By 2018, this figure remained stable, and by 2019 the male cases increased 1% to reach 68% and the women cases 32%. After analyzing the disaggregated information per state, this tendency showed the scenario repeats itself in almost all the cases except Tabasco in 2019, where the percentage of the registered female cases was 54%, and the male cases were 46% of the state's total.

Snakebites as a Neglected Tropical Disease

While most of the scientific literature about snakebite epidemiology concurs in asserting that this condition is an NTD, the reality is that the country's health authorities seem not to recognize this category. They consider that snakebites are a solved issue. Beyond being a mere formality, the NTD concept is important because of three reasons:

1. the relationship among NTD, poverty, and marginality;
2. NTD make visible the weaknesses of the healthcare systems in the developing countries;
3. NTD concept underlines the economic and social effects this type of disease has on the population. That is important when considering that snakebites leave permanent sequelae in many cases, directly affecting the family economy and the regions' development from a broader perspective.

Chami and Bundi affirm that high NTD indexes are an indicator of extreme poverty, financial weakness, and social marginality.¹⁵ Likewise, Hotez asserts that besides the economic troubles, the regions with high NTD indexes tend to be more vulnerable to natural disasters and even more to climate change.¹⁶ Aerts, Sunyoto, Tediosi, and Sicuri¹⁷ also sustain that the lack of political responsibility and governance of the health sector significantly affects the NTD management.

It is essential to point out that the acknowledging of snakebites as an NTD has been discussed for over a decade. The WHO recognized that this condition has characteristics of its own, making the overview much more complex. In other words, this is not a condition that may be treated like any other bacterial or vector-borne disease (which also forms part of this group). In this sense, Zúñiga-Carrasco considers that it is necessary to include snakebites in Mexico's vector-borne diseases. This proposal does not ponder that most of the strategies focused on treating this disease are based on the control and eradication of the species causing it. The best example is the diseases transmitted by mosquitoes like dengue, Zika, and chikungunya infection.¹⁸ Therefore, these strategies are incompatible with snakes because one of the government objectives is conservation.

Regarding poverty, it is interesting to analyze the latest data from Consejo Nacional de Evaluación de la Política de Desarrollo Social (CONEVAL) —decentralized public body responsible for measuring poverty in Mexico— about the poverty evolution in the states with higher snakebite incidence. By 2018, nearly 60% of the population in Veracruz was poor; besides, this state registered one of the highest indexes of extreme poverty in the country, just behind Chiapas, Oaxaca, and Guerrero. In Oaxaca, which ranked first in snakebite in 2018, 66.6% of its population was poor. Likewise, Puebla and Hidalgo registered 58.9% and 43.8% of poverty, respectively.¹⁹

All that confirms the fact that snakebites are, at the same time, a sign and a consequence of the poor economic conditions and the institutions' weakness affecting those states. The works of Yáñez-Arenas about the snakebites in Veracruz and Yucatán conclude that the number of new cases per state and the incidence remained constant because the strategies failed to address this problem, or more severely, there are no strategies at all. In this sense, the results of this research suggest that during the government of Enrique Peña Nieto, snakebites were not a central topic in the health agenda. It is worth noting that the current government has not made any effort nationwide to treat this problem.

Mistakes in the Epidemiologic Surveillance

Based on the analysis of Boletín Epidemiológico from SINAVE, corresponding to the 52 weeks in 2017, 2018, and 2019, it was possible to identify a series of errors in the case counting. More than simple mistakes, it is interesting to enhance a direct relationship between the states with more cases and the mistakes from the Boletín. Below are some examples of such mistakes, ranging from reporting 1 case in one week to 30 cases. Sometimes, the mistake seems to be corrected in the subsequent weeks; nevertheless, it is clear that the errors significantly affect the cases' counting in the corresponding states.

There are several questions related to these mistakes, for instance, whether they are a source of error, that is to say, from the various reports of the states, or if they are processing errors made by the state authorities writing the bulletin. The following mistakes do not represent an accurate list of all the bulletin mistakes. Still, it is essential to study the data to enhance the available data's quality to analyze this disease.

During week 29, 9 new cases were registered in Guerrero; the cumulative cases for men were 30, for women was 73. During week 30, there was a 16-case increase, which modified the cumulative cases for men to 86 and for women to 27. During week 31, the authorities reported 11 new cases, but cumulative cases for men decreased to 70 and for women to 29. In this case, the total cumulative cases diminished, and the new cases were not counted in this week. Finally, during week 32, 5 new cases were reported; nevertheless, men's cumulative cases were modified until 100 and 40 for women without any apparent reason.

During week 10, 2 new cases were reported in Oaxaca, which resulted in 9 male cumulative cases and 7 in women. During week 11, 4 new cases were reported in the state, which resulted in 12 cumulative cases in men and 11 in women. That is not possible, unless the total number of cases was 7; thus, the total number is wrong in 3 more cases than the previous week.

During week 18, Sonora reported 1 new case, which resulted in 14 cumulative cases in men and 6 in women. During week 19, no cases were reported; consequently, the male and female cumulative cases should be steady, but women's cumulative cases increased from 6 to 129 cases. In week 20, 3 new cases were reported; that modified the male cumulative cases to 19 and diminished the female ones to 7, clearly representing a mistake in counting the state's cases.

In 2018, 29 errors were identified. Most of the counting errors in snakebite cases were placed in Oaxaca, Jalisco, Hidalgo, Guerrero, Veracruz, and Durango. In 2019, the states with the highest prominence of errors were Guerrero, Jalisco, and Chiapas. Therefore, it is urgent to review the snakebite epidemiological accuracy to identify the errors' source and solve them.