Ethno-knowledge and attitudes regarding snakebites in the Alto Juruá region, Western Brazilian Amazonia

Journal Pre-proof Ethno-knowledge and attitudes regarding snakebites in the Alto Juruá region, Western Brazilian Amazonia

Ageane Mota da Silva, Mônica Colombini, Ana Maria Moura-da-Silva, Rodrigo Medeiros de Souza, Wuelton Marcelo Monteiro, Paulo Sérgio Bernarde PII:

S0041-0101(19)30718-4

DOI:

https://doi.org/10.1016/j.toxicon.2019.10.238

Reference:

TOXCON 6227

To appear in:

Toxicon

Received Date:

24 June 2019

Accepted Date:

12 October 2019

Please cite this article as: Ageane Mota da Silva, Mônica Colombini, Ana Maria Moura-da-Silva, Rodrigo Medeiros de Souza, Wuelton Marcelo Monteiro, Paulo Sérgio Bernarde, Ethno-knowledge and attitudes regarding snakebites in the Alto Juruá region, Western Brazilian Amazonia, Toxicon (2019), https://doi.org/10.1016/j.toxicon.2019.10.238

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Journal Pre-proof Ethno-knowledge and attitudes regarding snakebites in the Alto Juruá region, Western Brazilian Amazonia Ageane Mota da Silva a, b, Mônica Colombini c, Ana Maria Moura-da-Silva c, Rodrigo Medeiros de Souza d, Wuelton Marcelo Monteiro e, f, Paulo Sérgio Bernarde g, * a Instituto b

Federal do Acre, Campus de Cruzeiro do Sul, Cruzeiro do Sul. Acre, Brazil

Programa de Pós-Graduação Bionorte, Universidade Federal do Acre, Campus Universitário – BR

364, Rio Branco, Acre, Brazil c

Laboratório de Imunopatologia, Instituto Butantan, São Paulo, Brazil

d

Laboratório de Microbiologia, Imunologia e Parasitologia, Centro Multidisciplinar, Campus

Floresta, Universidade Federal do Acre, Cruzeiro do Sul, AC, Brazil e

Universidade do Estado do Amazonas, Manaus, AM, Brazil

f

Fundação de Medicina Tropical Dr. Heitor Vieira Dourado, Manaus, AM, Brazil

g

Laboratório de Herpetologia, Centro Multidisciplinar, Campus Floresta, Universidade Federal do

Acre, Cruzeiro do Sul, AC, Brazil *Corresponding author. Laboratório de Herpetologia, Campus Floresta, Universidade Federal do Acre, Estrada do Canela Fina S/N, 69.980-000 , Cruzeiro do Sul, Acre, Brazil. E-mail address: [email protected] (P.S. Bernarde).

Highlights 

Snakebite is an important cause of morbidity in the Alto Juruá region.

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Most snakebites occur in the rainy season when rivers are full and there is increased activity of snakes and their prey.



Small specimens of lancehead (Bothrops atrox) are responsible for most envenomations.



Half of the victims utilized some kind of inadequate first aid technique.

Abstract Background The Alto Juruá region, located in the extreme western part of the Brazilian Amazonia, possesses an indigenous and riverine population which is involved in agricultural and forest extraction activities, and is a region that stands out for its high incidence of snakebites. Objectives To assess the attitudes of the victims, the characteristics of the snakes and the circumstances of the snakebites which occurred in a region where human populations are highly exposed to snakes. Methods The study was conducted at the Regional Hospital of Juruá in the Municipality of Cruzeiro do Sul (Acre), which regularly attends victims of snakebites in the Alto Juruá region. The snakes that caused the envenomations were identified from clinical and epidemiological diagnosis of the symptoms and signs that patients presented during hospital, and by enzyme immunoassay for venom detection using serum samples of the patients, or by identification of the snake responsible for the envenomation when it was taken to the hospital or photographed. People who suffered or witnessed the snakebite were interviewed to assess the circumstances of the bite, the attitude adopted after the accident and whether they recognized the species of snake that caused the envenomation.

Journal Pre-proof Results There were 133 cases of snakebite (76.24 / 100.000 inhabitants), mainly involving male individuals living in the rural area and who had a low level of education. The most affected groups were farmers (48%) and children and teenagers (39%). It was observed that 8.3% of them presented a history of recurrence for bites. The lower limbs were the most affected anatomical region (84%). The Bothrops atrox snake, mainly small specimens (mostly juveniles), was the main species involved in the envenomations (83.4%). Snakebites occurred mainly in forest areas, backyards of houses in rural areas and near to aquatic environments, during activities (walking, farming, extractivism, hunting). Most of the time, the snake was on the ground and the bite occurred because of the approximation of the individual, either by trampling or by approximation of a hand. Half of the victims performed some kind of inadequate first aid (not drinking water, use of tourniquet, incision at the site of the bite, use of black stone, drinking a compound “Específico Pessoa”). Conclusions Snakebite is an important cause of morbidity in the Alto Juruá region. Bothrops bites are mostly caused by small-sized specimens, probably due to the greater abundance of B. atrox juveniles, and also because small snakes are more difficult for people to see. People are more often bitten on the lower limbs probably due to the size of B. atrox (small and medium) and because the snakes are usually on the ground in most situations. Many victims resort to ineffective actions that can cause complications and also delay serotherapy. A low level of education is a factor that may contribute to worse outcomes in snakebites since it is associated with a lack of knowledge of preventive and first aid measures. Keywords: Snakebite Snakes

Journal Pre-proof Envenomation Ophidism South America

1. Introduction Envenomation by snakes is considered a neglected tropical disease in several countries in Africa, Asia and Latin America, and affects mainly the poorest populations who live in rural areas (Chippaux, 2017; Williams et al., 2019). Snakebites are responsible for a major socioeconomic impact in these regions where there is higher incidence (Kasturiratne et al., 2017), and it is estimated that up to 5,500,000 snakebites occur on the planet each year, which may result in 1,841,000 envenomations and 94,000 deaths (Kasturiratne et al., 2008). However, these estimates may be underestimated or not represent the real dimension of this health impairment, since there is a lack of concrete data in the most affected regions, and also due to the fact that many victims do not have access to or do not seek hospital care (Fry, 2018). In the Brazilian Amazon, the most affected groups are those who work on plantations and also those who live in forests, in places often where there is some difficulty in getting to the hospital units that have the antivenom (Feitosa et al., 2015). In these poorer regions which are a long way from hospital care, due to cultural beliefs and habits, many people turn to household remedies or inadequate forms of treatment (Fita et al., 2010; Fry, 2018; Michael et al., 2018). Some of the practices considered to be inadequate (e.g., tourniquet, incision, black stone) are widely observed in Africa, Asia, and Latin America (Fry, 2018; Michael et al., 2018). These practices may worsen the clinical situation of the victim due to the delay in the search for hospital care and also because some may worsen the situation and may contribute to the onset of infections (e.g., incision) and death of tissues (e.g., tourniquet) (Ribeiro et al., 2001; Fry,

Journal Pre-proof 2018; Michael et al., 2011, 2018). The search for traditional healers is also an alternative in cases of snakebites, especially in communities with difficulties in accessing formal health care, which have certain beliefs about snakes and snake venom, tradition, and trust in the capacity of traditional healers (Schioldann et al., 2018). The delay in receiving antivenom therapy or the non-application of serum is one of the factors responsible for the appearance of complications such as amputations and deaths (Feitosa et al., 2015; Mise et al., 2018; Schioldann et al., 2018). Fry (2018) reviewed the myriad factors of human origin that influence the trajectory of global causes of snakebites and treatment failures, noting that this is both a sociological and economic problem as well as a medical one. Brazil is a country with 406 species of snakes, of which approximately 16% are venomous (Costa and Bérnils, 2018; Bernarde et al., 2018a). The venomous snakes are from the species belonging to the families Viperidae (lanceheads, genus Bothrops and Bothrocophias; rattlesnakes, genus Crotalus; bushmasters, genus Lachesis) and Elapidae (coral snakes, genus Micrurus and Leptomicrurus), which are responsible for 28% of venomous animal envenomations in the country (Chippaux, 2015). In the Brazilian Amazon, the highest number of cases of snakebites in Brazil occur and some municipalities have incidences that are greater than 200 cases per 100,000 inhabitants (Feitosa et al., 2015). The greatest diversity of snakes is also found in this region, around 190 species (Prudente, 2017; Bernarde et al., 2018a), of which 18% of these are venomous, and most of the bites are caused the genus Bothrops (81%), followed by Lachesis (7.3%), Crotalus (4.4%) and Micrurus (0.3%) (Magalhães et al., 2019). The Alto Juruá region, located in the extreme west of the Brazilian Amazon, has many inhabitants (farmers, riverine, extractivists, indigenous) who live in rural areas and forests, a region that stands out due to the high incidence of snakebites (Pierini et al., 1996; Bernarde and Gomes, 2012). The objective of this study was to evaluate the attitudes of the victims, the characteristics of the snakes and the circumstances of the snakebites in this region where there are vulnerable human populations that are frequently exposed to this type of injury.

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2. Materials and methods 2.1 Study area The study was conducted during a 1 year period (July 1st, 2017 to June 30th, 2018) at the Regional Hospital of Juruá in the Municipality of Cruzeiro do Sul (Acre) located in the Alto Juruá region in the western Brazilian Amazon, which regularly treats victims of snakebites from four municipalities (Cruzeiro do Sul, Mâncio Lima and Rodrigues Alves in the state of Acre, and Guajará in the state of Amazonas), and has a population of 137,722 inhabitants (IBGE, 2019) (Fig. 1). The main economic activities of the region are the production of manioc flour, extractivism of forest products (açaí, buriti), agriculture (corn, rice, beans, banana, watermelon, vegetables and fruit), livestock and fishing (ACRE, 2006). The climate of the region is tropical, hot, and humid, with an annual average temperature of 24.5 ºC, with the highest rainfall period from November to April (average rainfall of 2500 mm per year) (Moreira et al., 2016).

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Fig. 1. Location of the Alto Juruá region in Brazil.

2.2 Morbidity rate The morbidity rate (cases per 100,000 inhabitants) was calculated by dividing the number of people who been bitten by a snake by the number of inhabitants of the region during the period and then multiplied by 100,000. For the calculation of the morbidity rate, only the cases that occurred in the municipalities that sent the victims of snakebites regularly to the Juruá Regional Hospital were considered (Cruzeiro do Sul, Mâncio Lima and Rodrigues Alves in the state of Acre and Guajará in the Amazonas state). 2.3 Snake identification The snakes that caused the envenomations were identified from clinical and epidemiological diagnosis of the symptoms and signs that patients presented during hospital admission according to the types of envenomations (bothropic, lachetic and elapidic) that may occur in the region (Oliveira et al., 2018), and by enzyme immunoassay for venom detection of Bothrops atrox and Lachesis muta (Pardal et al., 2004) using serum samples from the patients collected before the antivenom therapy, or by identification of the snake responsible for the envenomation by a herpetologist (Paulo Sérgio Bernarde from UFAC) when it was taken to the hospital or photographed (confirmed cases). The snakes, when taken to the hospital, were identified using the regional snake identification guide (Bernarde et al., 2017). When the snakes were not brought to the hospital, a board containing photographs of snakes was shown to the patient to assess whether they recognized the specimen responsible for the envenomation. This was not a primary criterion for diagnosing the type of envenomation, but served rather as complementary information (See Mota-da-Silva et al., 2019a). The board contained color photographs of 17 common species in the Alto Juruá region

Journal Pre-proof (Bernarde et al., 2017) and was in the order as follows: Boa constrictor, Eunectes murinus, Bothrops bilineatus smaragdinus, Spilotes pullatus, Lachesis muta, B. atrox (adult), Corallus batesii, Micrurus lemniscatus, Oxyrhopus melanogenys, M. hemprichii, M. annellatus bolivianus, B. atrox (juvenile), Epicrates cenchria, Anilius scytale, Oxybelis fulgidus, M. surinamensis, Erythrolamprus aesculapii and E. reginae) which were only indicated by letters from A to R (Table 1). Each of the species of snakes had two photographs, with the exception of B. atrox that featured two pictures of juvenile specimens and two of adult specimens. The cases in which the snakes were not taken to the hospital and the patients were asymptomatic and had no change in blood coagulation time were considered "dry bites" or caused by non-venomous snakes (Silveira and Nishioka, 1992; Nicoleti et al., 2010). Table 1. List and sequence of snake species used on photo boards during interviews. Letter

Species

Family

Brazilian name

English name

Toxicity

A

Boa constrictor

Boidae

Jiboia

Boa constrictor

NV

B

Eunectes murinus

Boidae

Sucuri

Anaconda

NV

C

Bothrops bilineatus

Viperidae

Papagaia

Two-striped

V

smaragdinus D

Spilotes pullatus

forest-pitviper Colubridae

Caninana

Yellow

NV

ratsnake E

Lachesis muta

Viperidae

Pico de jaca

Bushmaster

V

F

Bothrops atrox

Viperidae

Surucucu

Lancehead

V

Boidae

Papagaia

Emerald tree

NV

(adult) G

Corallus batesii

boa H

Micrurus lemniscatus

Elapidae

Cobra-coral

Coral snake

V

Journal Pre-proof I

Oxyrhopus

Dipsadidae

Cobra de buriti

melanogenys J

Micrurus hemprichii

Tschudi's false

NV

coral snake Elapidae

Cobra coral

Hemprichi's

V

coral snake K

Micrurus annellatus

Elapidae

Cobra coral

bolivianus L

Bothrops atrox

Annellated

V

coral snake Viperidae

Jararaca

Lancehead

V

Boidae

Salamanta

Rainbow boa

NV

Aniliidae

Cobra coral

Red pipe snake

NV

Colubridae

Papagaia

Green vine

NV

(juvenile) M

Epicrates cenchria

N

Anilius scytale

O

Oxybelis fulgidus

snake P

Micrurus

Elapidae

Cobra coral

surinamensis Q

Erythrolamprus

Aquatic coral

V

snake Dipsadidae

Cobra coral

aesculapii

Aesculapian

NV

false coral snake

R

Erythrolamprus

Dipsadidae

reginae

Jararaquinha

Royal ground

NV

snake

V = Venomous; NV = Non venomous.

2.4 Venom-specific enzyme immune assays Immuno-enzymatic assays (ELISA) were used to identify and quantify circulating Bothrops atrox or Lachesis muta venoms in serum samples according to Pardal et al. (2004). The test was not conducted for other low incidence snakes because we did not have ELISA available for these species.Venom toxins present in the samples were collected with Bothrops-Lachesis antivenoms

Journal Pre-proof coated on ELISA plates. Plates were then incubated with a second antibody generated in rabbits against B. atrox venom or a specific mouse monoclonal antibody anti-Lachesis muta venom (Colombini et al., 2001) for reaction with bound toxins. This step was followed by incubation with anti-rabbit or anti-mouse IgG-peroxidase conjugates. Reactions were revealed by addition of the enzyme substrates (OPD plus H2O2), and recorded at 492 nm. Values were calculated using standard curves with known concentrations of B. atrox or L. muta venoms. The cut-off level corresponded to the mean plus 2 S.D. values of negative samples obtained from volunteer donors who were accompanying the patients.

2.5 Patient interviews The interviews regarding the circumstances of the snakebites and the patients’ actions were carried out using a semi-structured questionnaire based on a list of free and previously chosen topics; a method that allows the collection of large amounts of information, and reveals both expected and unanticipated aspects (Huntington, 1998). The interviews consisted of an interview script with questions to assess the circumstances of the snakebite, the action taken after the bite (first aid) and whether the victim recognized the snake that caused the bite.

2.6 Ethical aspects This research is part of the project "Venomous snakes and snakebites in Cruzeiro do Sul region in the state of Acre" approved by the Committee of Ethics in Research with Humans of the Tropical Medicine Foundation Dr. Heitor Vieira Dourado (Authorization No. 2,084,630).

3. Results During the period of one year, 133 snakebites were registered (morbidity rate of 76.24 cases per 100,000 inhabitants). Most of these occurred during the rainy season (64.7%) and in the

Journal Pre-proof morning (41.8%) or overnight (38%) (Table 2). The victims were mainly males between the ages of 11 to 20 years (27.8%) and 31 to 40 years (21%), living in the rural area (85.7%), with the most affected groups being farmers (48%) and children and teenagers (39%) (Table 3). The victims had low levels of education, with only 16.4% having a high school diploma and 3.4% having a certificate of higher education (Table 3). The lower limbs, feet (67%) and legs (17%), corresponded to the main anatomical region affected in the snakebites (Table 2). The Bothrops atrox was the main species involved in snakebites, confirmed by clinical and epidemiological diagnosis (56.4%) and confirmed cases (27%) (Tables 4 and 5, Figs. 2 and 3). Bothrops bilineatus smaragdinus was the second most common species cited as being responsible for the bites (5.3%), confirmed by the clinical-epidemiological diagnosis and information from the victims (Tables 4 and 5, Fig. 2). Four species of non-venomous snakes were confirmed in 5.3% of the cases (Tables 4 and 5, Figure 4). Dry bites or possible bites by non-venomous snakes accounted for 6% of cases (Tables 4 and 5). The length of the snakes, which was estimated by the victims or accompanying persons who witnessed the snakebite, followed similar proportions (small = 54.1%, medium = 31.2%, large = 14.7%) to the specimens of Bothrops atrox which were taken to the hospital by the patients (small = 60%, medium = 30%, large = 10%) (Table 5; Fig. 3).

Journal Pre-proof Fig. 2. Live snake specimens: A) “Jararaca” (Botrops atrox – juvenile); B) “Surucucu” (B. atrox – adult); C) “Papagaia” (B. bilineatus smaragdinus). Photos: Paulo Bernarde.

Fig. 3. Dead specimens of Bothrops atrox that caused snakebites: A) Small specimen (30 cm); B) Medium specimen (89 cm); C) Large specimen (165 cm). Photos: Paulo Bernarde.

Journal Pre-proof Fig. 4. Specimens of non-venomous snakes that caused snakebites: A) “Cobra-d’água” (Helicops angulatus); B) “Surucucu-de-brejo” (Hydrops triangularis); C) “Papagaia” (Philodryas viridissima); D) Xenodon rabdocephalus. Photos A and B: Paulo Bernarde; C: Ageane Mota da Silva; D) Isaías Nogueira. Most of the victims saw the snake only after the bite (89.8%) (Table 2). At the time of the bite, the snake was on the ground most of the time (92.1%) and, snakebites occurred mainly when the person was either passing close to a snake that was on the ground (49.6%) (Table 2). Snakebites occurred mainly in forests, backyards of houses in rural areas, river banks or streams and in plantations, and in other types of environments to a lesser extent (Table 2). People were bitten mainly while working or walking, and during other activities types: hunting, fishing, relaxing, collecting açaí in the forest, fetching water, or less frequently in other activities (Table 2). Most were not using proper footwear, such as sandals (65.9%) or barefoot (17.8%) (Table 2). Those using boots (n = 14, 10.8%) were bitten because the snake was either on vegetation (35.8%), or because the snake was large in size (150 cm) and the bite was above the height of the boots (21.4%), or the victim’s hand was close to the snake on the ground (14.3%), or the snake's fangs pierced the boot during the bite (14.3%), or because the snake was in the ravine (1.7%) or on a tree trunk (1.7%) (Table 2). In approximately half of the situations (51.4%), the snake that caused the bite was killed (Table 6). Most of those who did not kill the snake (52.4%) did not know or did not want to answer why they did not kill the snake. The snake was not killed because it fled (26.2%), or because it was not seen (16.4%) or because the victims were unaccompanied children (5%) (Table 6). Eleven people (8.3%) had already been bitten by snakes at least once in their life, some up to three times or more. Bothrops atrox was the main species reported (called a “jararaca” or “surucucu”) (Table 5; Fig. 5). During the study period, one patient was bitten twice, the first time was a suspected case of B. atrox bite and, 40 days later, by a Xenodon rabdocephalus.

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Fig. 5. Necrosis scar on foot from a bite caused by “surucucu” (probably Bothrops atrox) 8 years ago. Patient had been bitten twice in life.

In relation to the first aid carried out by the victims of the snakebites, half (50.7%) did nothing, while the rest, most of the time did something invasive or obviously potentially harmful practice (did not drink water, used a tourniquet, made an incision at the site of the bite, tied the dead snake to the limb) and non invasive which may not be harmful (tied a strip of cotton on the limb and resorted to faith healers and witch doctors) (Table 6) (Fig. 6). Thirty-one of the victims (23.5%), ingested some type of drink (tea, water of the açaí seed, Epecífico Pessoa, tea made scrapings from the board of a pier or with scrapings from the house steps , gray tinamou feather tea, araticum leaf tea, pig hair tea, deer horn tea, bitter coffee, açaí root tea, rue tea, chicory root tea, pearl cichlid fish tea, squirrel tail tea, gunpowder tea, liquid of parasitic plant, cooked purple cotton, ivory palm juice and althaea juice) and 19 (14.4%) applied some type of substance to the location of the bite (buriti sap or oil, paca gall, salt, lemon, banana peel, piper leaf, sugar, Específico Pessoa, tobacco, snake brains, snake guts, pork lard, black stone and gasoline) (Table 6; Fig. 6).

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Fig. 6. A) Salt placed on the wound; B) Strip of cotton tied on the bitten leg; C) Gray tinamou (Tinamus tao) (feathers used to make tea); D) Açaí root (Euterpe precatoria) (tea); E) Pearl cichlid fish (Cichlidae) (tea); F) Squirrel (Sciuridae) (tea made from the tail); G) Paca (Agouti paca) (gall bladder); H) Ladder orpier (tea made with scrapings from a board). Photos: A and B = Ageane Mota da Silva; C = Wanieulli Pascoal; D – H = Paulo Bernarde.

The victims were taken to the hospital mainly by the Mobile Emergency Service ambulance (SAMU) (23%), private car (22.1%), boat and ambulance (19.7%), motorcycle only (9.8% %) and

Journal Pre-proof motorcycle and ambulance (9%) (Table 6). The majority of the victims (65.4%) took more than three hours to reach the hospital, with the following causes being reported: distance and difficult access to the hospital (51.7%), difficulties in arranging transport (13.8%), transferred from other hospital units (12.6%), mild symptoms initially (11.5%), waited to improve (5.7%), danger of navigating at night or without a flashlight (3.5%) and a child who not had reported to the parents the day they were bitten (1.2%) (Table 6).

Table 2. Circumstances of the snakebites in Alto Juruá. CIRCUMSTANCES

FREQUENCY

PERIOD OF DAY (n = 129) Morning (6:00 – 11:59 horas)

54 (41.8%)

Afternoon (12:00 – 17:59 horas)

25 (19.4%)

Evening (18:00 – 23:59 horas)

49 (38%)

Night (0:00 – 5:59 horas)

1 (0.8%)

REGION OF THE BODY THAT WAS BITTEN (n = 133) Foot

89 (67%)

Leg

23 (17%)

Thigh

2 (1.6%)

Hand

13 (10%)

Arm

2 (1.5%)

Forearm

1 (0.7%)

Thorax

2 (1.5%)

Head

1 (0.7%)

WHEN SNAKE WAS SEEN (n = 128) Saw after the bite

115 (89.8%)

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10 (7.8%)

Saw before the bite

3 (2.4%)

WHERE THE SNAKE WAS (n = 127) Ground

118 (92.1%)

On vegetation or tree trunk

8 (6.2%)

Gulley or ravine

1 (1.7%)

HOW THE BITE HAPPENED (n = 127) Passed the snake on the ground.

62 (48.8%)

Stepped on the snake

37(29.1%0

Placed hand close to the ground where the snake was

15 (11.8%)

Passed next to the snake that was on the vegetation

7 (5.5%)

Approached another snake while moving away from one snake he/she

1 (0.8%)

had seen Passed by the snake that was in a ravine or gulley

1 (0.8%)

Stepped on the snake that was on a trunk

1 (0.8%)

Stumbled and fell placing a hand on the snake on the ground.

1 (0.8%)

Trying to capture the snake by hand

1 (0.8%)

Handling the snake thinking it was dead

1 (0.8%)

AREA OF OCCURRENCE (n = 133) Rural

114 (85.7%)

Urban

19 (14.3%)

ENVIRONMENT WHERE THE SNAKEBITE OCURR (n = 129) Forest

29 (22.5%)

Yard in rural

27 (20.9%)

Riverbank or stream

24 (18.6%)

Plantation

19 (14.8%)

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9 (7%)

Dirt track

9 (7%)

Home

3 (2.3%)

Yard in urban

2 (1.5%)

Paved highway

2 (1.5%)

Banks of a weir

2 (1.5%)

Beside a flooded forest

1 (0.8%)

School

1 (0.8%)

Football pitch

1 (0.8%)

WHAT THE VICTIM WAS DOING AT THE TIME OF THE BITE Working

46 (35.8%)

Walking

34 (27.8%)

Hunting

13 (10%)

Relaxing

9 (6.8%)

Fishing

8 (6.2%)

Harvesting açaí

5 (3.9%)

Fetching water (well or stream or river)

5 (3.9%)

Indoors

3 (2.3%)

Going to defecate

2 (1.5%)

Teaching at school

1 (0.8%)

Playing soccer

1 (0.8%)

TYPE OF FOOTWEAR USED (n = 129) Sandals

85 (65.9%)

Barefoot

23 (17.8%)

Boots

14 (10.8%)

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7 (5.5%)

HOW THE PERSON WAS BITTEN WHILE WEARING BOOTS (n = 14) Snake on vegetation

5 (35.8%)

Snake of large size (150 cm) and struck above the boot

3 (21.4%)

Brought hand close to where the snake was

2 (14.3%)

Snake’s fangs (42 and 50 cm snake length) perforated the boot

2 (14.3%)

Approached the snake that was on the trunk

1 (7.1%)

Approached the snake that was in the ravine or gulley

1 (7.1%)

Table 3. Profile of the snakebite victims in the Alto Juruá region. FEATURES

Frequency

SEX OF VICTIM (n = 133) Male

102 (76.7%)

Female

31 (23.3%)

AGE 0 to 10

15 (11.3%)

11 to 20

37 (27.8%)

21 to 30

21 (15.8%)

31 to 40

28 (21%)

41 to 50

19 (14.4%)

51 to 60

8 (6%)

> 60 OCCUPATION (n = 133)

5 (3.7%)

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64 (48%)

Student

33 (25%)

Housewife

5 (4%)

Other

31 (23%)

EDUCATION (n = 128) Illiterate

19 (14.8%)

Incomplete Elementary School

53 (41.5%)

Elementary School

30 (23.4%)

High School

21 (16.4%)

University

5 (3.9%)

Table 4. Method of identifying the snake involved in the snakebites in the Alto Juruá (n = 133). SNAKE

Clinical and

Recognized by

Enzymatic

Snake

epidemiological

photo plates

assay

captured or photographed

B. atrox (111)

75 (56.4%)

79 (59.4%)

28 (21%)

13 (9.8%)

B. bilineatus (7)

7 (5.3%)

6 (4.5%)

0

0

Non-venomous

7 (5.3%)

0

0

7

8 (6%)

0

0

0

(7) Non-venomous or dry bite (8)

Table 5. Snakes involved in bites in the Alto Juruá region. FREQ = frequency.

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FREQ

SNAKE THAT CAUSED THE BITE (n = 133) Bothrops atrox – suspected (by clinic)

75 (56.4%)

B.atrox (Antigenemia, Snake taken to hospital or photographed!)

36 (27%)

B. bilineatus smaragdinus – suspeito (By clinic and recognized on the

7 (5.3%)

photoboard!) Helicops angulatus (Snake taken to hospital or photographed!)

3 (2.2%)

Philodryas viridissima (Snake taken to hospital or photographed!)

2 (1.5%)

Hydrops triangularis (Snake taken to hospital)

1 (0.8%)

Xenodon rabdocephalus (Snake photographed!)

1 (0.8%)

Non-venomous or dry bite

8 (6%)

ESTIMATED SIZE OF THE Bothrops atrox (n = 109): 20 – 165 cm ( 64.8 cm) Small 20 – 50 cm ( 36.2 cm)

59 (54.1%)

Medium 51 – 100 cm ( 80.7 cm)

34 (31.2%)

Large 101 – 165 cm ( 136.2 cm)

16 (14.7%)

SIZE OF Bothrops atrox CAPTURED (n = 10): 25.5 – 165 cm (61.2 cm) Small 20 – 50 cm ( 31.3 cm)

6 (60%)

Medium 51 – 100 cm ( 86.5 cm)

3 (30%)

Large 101 – 165 cm ( 165 cm)

1 (10%)

SNAKES INVOLVED IN PREVIOUS BITES (N = 24) Surucucu

13 (54%)

Jararaca

7 (29.2%)

Jararaca d’água

1 (4.2%)

Journal Pre-proof Jararacuçu

1 (4.2%)

Papagaia

1 (4.2%)

Pico de jaca

1 (4.2%)

Table 6. Pre-hospital actions and behavior adopted by the victims after the snakebite in the Alto Juruá region. ATTITUDES

Frequency

WAS SNAKE KILLED (n = 127) Yes

66 (51.4%)

No

61 (47.6%)

REASON FOR NOT KILLING THE SNAKE Do not know or did not answer

32 (52.4%)

Snake escaped

16 (26.2%)

Not seen

10 (16.4%)

Unaccompanied child

3 (5%)

TYPE OF FIRST AID* (n = 132) No action taken

67 (50.7%)

Did not drink water

42 (31.8%)

Torniquet

7 (5.3%)

Cleaned with soap and water

7 (5.3%)

Tied a strip of cotton on limb

6 (4.5%)

Cleaned with alcohol

4 (3%)

Sought faith healers

2 (1.5%)

Made incision at the site of the bite

1 (0.8%)

Journal Pre-proof Tied the dead snake to the leg

1 (0.8%)

Sought witch doctor

1 (0.8%)

Ingestion Tea (Content unknown!)

6 (4.5%)

Water from the açaí seed (Eurterpe precatoria Mart.)

5 (3.7%)

“Específico Pessoa”

4 (3%)

Tea made with scrapings from the board of a pier or from the house

4 (3%)

steps Gray tinamou feather tea (Tinamus tao) (Aves: Tinamidae)

3 (2.2%)

Custard Apple leaf tea (Annonaceae)

2 (1.5%)

Pig hair tea (Mammalia: Suidae)

2 (1.5%)

Deer horn tea (Mammalia: Cervidae)

2 (1.5%)

Bitter coffee

2 (1.5%)

Açaí root tea (Euterpe precatoria Mart.)

1 (0.8%)

Rue tea (Ruta graveolens L.)

1 (0.8%)

Chicory root tea (Cichorium intybus L.)

1 (0.8%)

Pearl cichlid fish tea (Perciformes: Cichlidae)

1 (0.8%)

Squirrel tail tea (Mammalia: Sciuridae)

1 (0.8%)

Gunpowder tea

1 (0.8%)

Parasitic plant juice

1 (0.8%)

Cooked purple cotton

1 (0.8%)

Ivory palm juice (Phytelephasa equatorialis Spruce)

1 (0.8%)

Althaea juice

1 (0.8%)

Topical concoction on bite Buriti oil or sap (Mauritia flexuosa L.)

3 (2.2%)

Gall bladder from paca (Cuniculus paca) (Mammalia: Cuniculidae)

2 (1.5%)

Journal Pre-proof Salt

2 (1.5%)

Lime (Citrus limon L.)

2 (1.5%)

Banana (Musacea)

1 (0.7%)

Piper leaf (Pothomorphe umbellate L.)

1 (0.7%)

Sugar

1 (0.7%)

Específico Pessoa

1 (0.7%)

Tobacco

1 (0.7%)

Snake brain (Reptilia: Viperidae)

1 (0.7%)

Snake guts (Reptilia: Viperidae)

1 (0.7%)

Pork lard (Mammalia: Suidae)

1 (0.7%)

Black Stone (also known as snakestone)

1 (0.7%)

Gasoline

1 (0.7%)

TYPE OF TRANSPORT (n = 122) Ambulance – SAMU

28 (23%)

Car

27 (22.1%)

Boat + Ambulance

24 (19.7%)

Motorcycle

12 (9.8%)

Motorcycle+ Ambulance

11 (9%)

Boat + Car

6 (5%)

Car + Ambulance

3 (2.5%)

Plane + Ambulance

2 (1.6%)

Hammock + Ambulance

2 (1.6%)

Bus

2 (1.6%)

Taxi

2 (1.6%)

Boat + Motorcycle

1 (0.8%)

Boat + Plane + Ambulance

1 (0.8%)

Journal Pre-proof Boat + Taxi

1 (0.8%)

Cause of delay to hospital (n=87 victims with delay >3 hours) (65.4%) Distance and difficulty in accessing treatment

45 (51.7%)

Difficulties arranging transport

12 (13.8%)

Transferred from other hospital

11 (12.6%)

Mild symptoms initially

10 (11.5%)

Awaited improvement

5 (5.7%)

Danger of navigating at night or without a flashlight

3 (3.5%)

Child did not tell to its parents that it had been bitten

1 (1.2%)

*More than one first-aid measure may have been used

4. Discussion The highest percentage (64.7%) of the snakebites occurred during the period of November to April, which corresponds to the months of higher rainfall (Moreira et al., 2016) and also to the period when the Juruá River is at its highest (Moreira et al., 2019). Amazonian snakes feed mainly on anuran amphibians, lizards and small mammals (rodents and marsupials) (Martins and Oliveira, 1998; Bernarde and Abe, 2006; Bisneto and Kaefer, 2019) and, during the rainy season in the Amazon, there is a greater activity (reproductive and of foraging) of these animals and the emergence of their offspring (Fleck and Harder, 1995; Woodman et al., 1995; Santos-Filho et al., 2006; Bernarde, 2007; Pinheiro and Turci, 2013; Miranda et al., 2015; França et al., 2017), which would be related to a greater number of snakebites in this period. In this period, the Bothrops atrox is also more active and it is when its young are born (Oliveira and Martins, 2001; Turciet al., 2009; Bisneto and Kaefer, 2019), the Bothrops being the principal agent of envenomations in the northern region of the country (Pierini et al., 1996; Pardal et al., 2004; Moreno et al., 2005; Roriz et al., 2018; Mota-da-Silva et al., 2019a). River floods have been cited as one of the causes of increases in

Journal Pre-proof cases of snakebites, since they cause snakes to search for drier areas, which provides a greater possibility of an encounter with humans (Moreno et al., 2005; Waldez and Vogt, 2009; Roriz et al., 2018). In addition to the climatic and ecological factors involved in the higher rate of snakebite cases during the rainy season, certain human activities carried out at that time (e.g., plowing, forest extractivism) also contribute to the greater number of bites during this period (Waldez and Vogt, 2009; Oliveira et al., 2013; Mota-da-Silva et al., 2019b). During the reproductive period of the snakes, some events (combat between males, males seeking females, copulations) increase the activity of snakes, which may contribute to the increase in snakebites (Salomão et al., 1995; Almeida-Santos and Salomão, 2002). The attempted copulation of two males with a female of the second species most involved in snakebites, B. b. smaragdinus, during January in the Alto Juruá was recorded by Turci et al. (2009), which reinforces the hypothesis that the rainy season is the mating period for these species of Bothrops in the region. The period of the day when snakebites mostly occur in the Amazon is related to both the activity of snakes and humans, and thus occur mainly during the day (76% to 83.5% of cases) (Moreno et al., 2005; Waldez and Vogt, 2009; Roriz et al., 2018). In this study, although most of the snakebites were recorded as occurring during the day (61.2%), mainly in the morning (41.8%), a significant portion occurred during the evening (38%). This lower proportion of cases during the day compared to other Amazonian localities (Rio Branco, Moreno et al., 2005; Baixo rio Purus, Waldez and Vogt, 2009; Porto Velho, Roriz et al., 2018), may be due to differences in the composition of species causing the bites and / or in the human activities being carried out and also due to cultural habits. The main causative species in this study, Bothrops atrox, although predominantly nocturnal, may also be active during the day (Oliveira and Martins, 2001). The snake B. bilineatus smaragdinus, although mainly nocturnal, can extend its hunting activity until the early hours of the morning (Fonseca et al., 2019). Bothrops species found during the day are usually found under herbaceous plants and shrubs, between fallen logs and roots (Sazima, 1992; Oliveira and Martins, 2001), sites that may be more protected from predators by camouflage and still in the

Journal Pre-proof mosaic of shade and sun, which is probably associated with thermoregulation activity. The dipsadids, Philodryas viridissima and Xenodon rhabdocephalus, have diurnal habits and are also found in open areas (Bernarde et al., 2017), which corroborates with the snakebites recorded as being caused by these snakes during the day. These daytime snake activities could partly explain accidents during the day, when combined with people's working hours. Several studies on snakebites have shown that the main profile corresponds to male adults and farmers in rural areas (Kasturiratne et al., 2008, Magalhães et al., 2019 and Mise et al., 2019) as ours also did (76.7% male, 48% farmers, 85.7% of the cases in the rural area). The second most affected group were the children and teenagers (39% of the victims), a phenomenon that was also observed in the study by Moreno et al. (2005), who registered that 18% of the cases treated in Rio Branco were students (children), coming or going from schools. The low level of education observed in this study is associated with the fact that most victims are from rural areas, who have greater difficulty in accessing education and lower levels of education (e.g., Arruda et al., 2018). A low level of education was observed in the victims in this study and as in others in the Amazon (e.g., Moreno et al., 2005; Magalhães et al., 2019), and this is linked to worse outcomes in snakebite treatment, since it is associated with the lack of knowledge of preventive and first aid measures (Moura et al., 2010; Bertolozzi et al., 2015; Pandey et al., 2016). As in other studies in the Amazon (Pierini et al., 1996; Pardal et al., 2004; Moreno et al., 2005; Roriz et al., 2018), the Bothrops atrox was the main cause of snakebites in this study (83.4% of the cases), even in reports of those who had been bitten previously. This species of snake is widely distributed in the Amazon and has general, non-specific habits. It feeds on a wide spectrum of prey (rodents, amphibians, lizards, other snakes, birds, etc.) and is found in several types of forested habitats (forests and floodplains), as well as disturbed areas (crops, pastures and cities) (Oliveira and Martins, 2001; Turci et al., 2009; Fraga et al., 2013; Bisneto and Kaefer, 2019). The abundance of this snake in various types of environments, in combination with certain human activities (e.g., plowing, extractivism), increase the possibility of an encounter and therefore bites to

Journal Pre-proof people in rural and forested areas (Waldez and Vogt, 2009; Mota-da-Silva et al., 2019b). The B. bilineatus smaragdinus is a rare species along its geographical distribution in the Western Amazon (e.g., Duellman, 1978; Dixon and Soini, 1986), however, in Alto Juruá it was the second most commonly involved species in snakebites (5.3% of cases), the same observed in other studies in Colombia (Haad, 1980/81) and in Equador (Smalligan et al., 2004). In some lowland riverside forests in Alto Juruá, B. b. smaragdinus is the most commonly encountered snake (Turci et al., 2009; Fonseca et al., 2019), despite this, there are relatively few cases caused by this species. Although it is an abundant species in some forests in the Alto Juruá, B. b. smaragdinusis found on vegetation between heights of 30 cm to 18 m in height, at an average height of 6 m (Fonseca et al., 2019), which would make an encounter between a snake and humans walking in the woods more difficult. During the study period, no lachetic accidents were recorded, which shows that the bites caused by Lachesis muta are infrequent, probably because this species occurs mainly in forests in low population density areas and also due to its relatively less aggressive behavior and large size (easier to be seen) (Mota-da-Silva et al., 2019a). Despite the occurrence of six Micrurus species in the Alto Juruá region (Bernarde et al., 2017), coral snake bites are rare due to the low frequency and more secretive habits of the species and its greater difficulty in inoculating the venom during the bite, often occurring during improper handling (Pardal et al., 2010; Bucaretchi et al., 2016; Strauch et al., 2018). After the period of this study, a case of elapidic envenomation caused by M. annellatus bolivianus was recorded. The victim was bitten on the hand when sorting through saw dust during work in sawmill (Mota-da-Silva et al., 2019c). The snakebites caused by "non-venomous snakes" (Dipsadidae and Colubridae) accounted for 5.3% of the cases and were reported in more detail in a previous study (Mota-da-Silva et al., 2019d), in which the possibility of error of diagnosis of some species is discussed. The coloring pattern of the Helicops angulatus species can be mistaken for B. atrox, as can also happen with Philodryas viridissima and B. b. smaragdinus, in addition to the possibility of pain, edema and

Journal Pre-proof alteration of the blood coagulation time (in the case of H. angulatus) in the patients, which could lead to an erroneous diagnosis of bothropic envenomation (Mota-da-Silva et al., 2019d). Most of the specimens (54.1%) of Bothrops atrox involved in snakebites were small size (between 20 and 50 cm), followed by average (51 to 100 cm, 31.2%) and large (101 to 165 cm, 14.7%). This may be due to the greater abundance of B. atrox juveniles in the environment (Turci et al., 2009; Bisneto and Kaefer, 2019) and also by the fact that small snakes are more difficult to detect and thus more snakebites occur (Sazima, 1988). Interestingly, the sizes of the snakes that were brought to the hospital (small: 60%, medium: 30%, large 10%) was similar to the sizes estimated by the victims, which creates more confidence in the reliability of the results of the interviews. The snake that caused the bite was seen only after the sting most of the time (89.8%), which shows that the camouflage of these animals makes it difficult for them to be spotted in the wild, especially specimens of Bothrops atrox on the ground (Martins and Oliveira, 1998) and B. bilineatus smaragdinus when on the vegetation (Fonseca et al., 2019). In all snakebites, basically people either stepped on, touched or approached the snake, demonstrating that these snakes bite as a defensive response to a potential predator (Sazima, 1988; Martins and Oliveira, 1998). Snakes were found on the ground in most situations (92.1%), which when associated with their size (85.3% were smaller than 1 m), would explain why the feet and legs corresponded to the main anatomical regions that were affected (67% and 17%, respectively). This was also observed in other studies (Pierini et al., 1996; Moreno et al., 2005; Waldez and Vogt, 2009; Bernarde and Gomes, 2012; Roriz et al., 2018; Magalhães et al., 2019). Added to this is the fact that the reach of the strike of the lanceheads (Bothrops spp.) does not exceed the a third of the snake’s body length (Araújo and Martins, 2007). Most of snake bites occurred in forests (22.5% of cases) and in backyards in rural areas (20.9%), which is attributed to the fact that Bothrops atrox is one of the most abundant snakes,

Journal Pre-proof especially in rural areas where human populations are more concentrated (Martins and Oliveira, 1998; Oliveira and Martins, 2001; Turci et al., 2009). This species of snake is also common in the vicinity of aquatic environments (Oliveira and Martins, 2001; Turci et al., 2009; Fraga et al., 2013), which explains why 20.9% of the cases of bites occurred on the margins of rivers, streams, weirs and “igapós”. A similar proportion was observed by Pierini et al. (1996) in an earlier study in the Alto Juruá region, which reported 19% of snakebites occurring along rivers and streams. People being bitten while walking was the situation in which most snake bites occurred (27.8%), similar to that observed (25.7%) by Pierini et al. (1996), which denotes the accidental character of the snake's defensive strike (e.g., Sazima, 1988; Martins and Oliveira, 1998). Working on plantations presents the greatest risk for snakebites (e.g., Pierini et al., 1996; Moreno et al., 2005; Mise et al., 2019), which was observed in 19.4% of cases that occurred during agricultural activities (e.g., land clearing). Activities developed within forests (hunting, açaí harvesting, forestry) accounted for 13.3% of the cases, which is an occupation related to communities that depend on forest resources (Pierini et al., 1996; Waldez and Vogt, 2009). Some studies have reported snakebites occurring during the harvesting of açaí (Waldez and Vogt, 2009; Pardal et al., 2015; Silva and Pardal, 2018), in our study 3.9% of the cases occurred during this activity, and were also detailed in the study by Mota et al. (2019b). In the Alto Juruá region, during the harvesting of açaí, there is a risk of encountering adult specimens of B. atrox on the ground near the trees and B. bilineatus smaragdinus on the vegetation in the trees neighboring the palm tree, probably hunting small mammals that are attracted by the fruits of the açaí palm (Mota-da-Silva et al., 2019b). Rarer situations were also recorded, such as the case of a man who, after cutting a B. atrox juvenile into three parts with a machete, was bitten on the hand when he picked up the body parts (Mota-da-Silva et al., 2019e). Since the main anatomical region which was affected was the feet, the use of suitable footwear could prevent a large part of the snakebites (Moreno et al., 2005; Waldez and Vogt, 2009; Bernarde et al., 2018b), however, most of the victims in this study were wearing sandals (65.9%) or

Journal Pre-proof barefoot (17.8%), with only 10.8% wearing boots at the time of the snakebite. Most (35.8%) of victims wearing boots were bitten by snakes (Bothrops atrox and B. b. Smaragdinus) that were on the vegetation, since these are species that use these substrates (Oliveira and Martins, 2001; Turci et al., 2009) and, by large specimens (150 cm) of B. atrox (21.4%), that managed to strike on the leg above the boot. In four cases (28.5%), the victims placed their hands near a snake that was on the ground (2 cases) or approached a snake that was in a ravine or on a trunk. Martins and Oliveira (1998) reported two specimens (57.8 and 100 cm) of B. atrox that were able to puncture leather gloves and cause envenomation. In our study, we recorded two victims in which this species (42 and 50 cm) perforated boots with their fangs and caused envenomation. Thus, although the use of rubber boots helps to prevent snakebites, it should be remembered that some specimens can pierce them with their fangs during a strike. The use of leather leggings for better protection from snake bites is also recommended. As noted in other studies (e.g., Moreno et al., 2005; Waldez and Vogt, 2009; Roriz et al., 2018), few people (13.5%) took the snake that caused the snakebite or a photograph of it to the hospital, which would greatly facilitate the diagnosis. Although half of the snakes were killed after the snakebite, most people did not bring the dead specimen to the hospital, which indicates the importance of the need for campaigns for this practice to be performed to aid in the diagnosis (Bernarde et al., 2018b). In the Alto Juruá region, Pierini et al. (1996) reported that 13% of the interviewed population (indigenous and extractivist) had been bitten by snakes at least once in their lives, in some cases, several times. Among the patients interviewed in this study, 8.3% reported having previously been bitten at least once, some up to four or ten times. This shows how common snakebites in the Alto Juruá region are and how frequently they are an important cause of morbidity (Pierini et al., 1996). These numbers may still be underestimated, since many victims of snakebites do not seek hospital care (Pierini et al., 1996; Waldez and Vogt, 2009; Fry, 2018).

Journal Pre-proof Half of the victims did not take any first aid measures, while the remainder most often practiced some kind of inappropriate behavior (not drinking water, use of tourniquet, incision at the site of the bite, use of black stone, drinking “Específico Pessoa”) (Fita et al., 2010; Fry, 2018; Michael et al., 2018; Schioldann et al., 2018). Not drinking water, which is also a common belief in the Northeast of Brazil, (e.g., Oliveira et al., 2013), was the main inappropriate action taken by victims of snakebites in this study (31.8% of cases), which may contribute to worsening of the clinical picture, since dehydration may contribute to the onset of renal failure, which is one of the complications that may result in death (Souza et al., 2018). More than 20 years ago, Pierini et al. (1996) also reported a number of actions that were also recorded in this study (use of tourniquets, incision at the site of the bite, “Específico Pessoa”, tea made with scrapings from the board of a pier or from the house steps, Gray tinamou feather tea, gunpowder tea, traditional healers). Some of these practices (e.g., tourniquet, “Específico Pessoa”, black stone), which have already proved not to bring any benefit and may even aggravate the victim's condition (Borges et al., 1996; Ribeiro et al., 2001; Chippaux et al., 2007; Fry, 2018), are still used. In this study we obtained reports of traditional medicine in the form of zooterapy, which constitutes the use of wild animals or part of the body of the animals (squirrel, deer, paca, gray tinamou, fish species and the snakes themselves which caused the envenomation), which is a widespread practice in more isolated communities which are a long distance from medical care in the North and Northeastern regions of Brazil (e.g., Pierini et al., 1996; Fita et al., 2010; Barros et al., 2012). The use of plants was also observed in this study (e.g., Araticum, açaí root and shoots, buriti, piper, ivory palm and Althaea), which is another form of traditional medicine widely used in the Amazon and in the northeastern region of the country (e.g., Pierini et al., 1996; Fita et al., 2010; Vásquez et al., 2014). Resorting to these first aid resources, treatments and healers can cause complications because some practices can aggravate the envenomation and also delay the antivenom therapy, or even cause people not to seek the hospital care due to their beliefs or difficulty of access to such facilities (e.g., Pierini et al., 1996; Pandey et al., 2016; Schioldann et al., 2018).

Journal Pre-proof Despite the importance of the rapid hospitalization so as to receive the antivenom therapy in order to reduce the possibility of complications, consequences and deaths (Souza et al., 2018), the majority (65.4%) of the victims arrived at the hospital three hours after the bite. The victims arrived at the hospital mainly by ambulance (23%) and car (22.1%), but even so, a significant portion (27.1%) needed a boat for at least part of the journey, which demonstrates that a large part of the population which is most vulnerable to snakebites in the Amazon is located in communities in remote areas and is dependent on river or air transportation (Fan and Monteiro, 2018). The majority of the patients who took more than three hours to arrive at the hospital (69%) claimed that the delay was due to difficulties (distance, difficult access, difficulty in getting transportation, danger of navigating during the night or even having no flashlight for nocturnal travel), which demonstrates their vulnerability to snakebites and the difficulty these populations located in more distant communities in the Amazon have when accessing antivenom therapy (e.g., Pierini et al., 1996; Waldez and Vogt, 2009; Fan and Monteiro, 2018). Many patients experience a poor outcome or delay in effective care in a hospital because of their previous use of ineffective treatments (Schioldann et al., 2018). Some victims (17.2%) did not go to the hospital at first because they believed that the symptoms would not worsen. Later, with the onset of worsening symptoms, they sought hospital care.

5. Conclusions Snakebite is an important cause of morbidity in the Alto Juruá region (76.24/100,000 inhabitants and 8.3% of patients had previously been bitten), mainly in rural and forest areas, and this incidence may be underestimated because many victims of snakebites do not seek hospital care. Farmers make up the main victims and the snakebites happen mainly during the work in the fields and in forests (extractivism, forestry, hunting). The main species involved in snakebites is Bothrops atrox, followed by B. bilineatus smaragdinus. Lachetic (Lachesis muta) and elapidic bites

Journal Pre-proof (Micrurus spp.) are less frequent and none were recorded during the study period. Bothropic envenomations are mostly caused by small-sized specimens, probably due to the greater abundance of B. atrox juveniles in the environment and also due to the fact that small snakes are harder to detect by humans. People are more often bitten on the lower limbs probably due to the size (small and medium) of B. atrox and the snakes being on the ground in most situations. Many victims resorted to ineffective actions that can cause complications and also delay antivenom therapy. A low level of education is a factor that may contribute for worse outcomes in snakebites, because it is associated with the lack of knowledge about preventive measures and first aid. Retrospective surveys of snakebite cases are limited since data in medical records may be incomplete and also because it is impossible to obtain and relate diverse information (Saboia and Bernarde, 2019; Blessmann et al., 2018). Prospective studies such as this allow a more complete and valuable study of the circumstances of snakebites, allow a deeper analysis of the clinical and epidemiological information, and are able to more accurately assess the circumstances of the bites and also the attitudes of the victims. For a better understanding of ophidism, it is necessary to evaluate all aspects involved in the epidemiological context (species involved, variables in people, environment, time of day and seasonality), bio-ecology of snakes, circumstances in which snakebite occurred and also victims’ actions after the bite.

Acknowledgements We are grateful to the directors of the Juruá Regional Hospital of Cruzeiro do Sul for their permission for this research and the entire team of doctors, nurses, nursing assistants, and other hospital staff for their support of this study.

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Declaration of interests ☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. ☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:

Respectfully on behalf of all co-authors,

____________________________________________________________________

Paulo Sergio Bernarde

June 24th, 2019