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Snakebite envenoming in Kerala, South India: clinical profile and factors involved in adverse outcomes
N Suchithra, J M Pappachan and P Sujathan Emerg. Med. J. 2008;25;200-204 doi:10.1136/emj.2007.051136

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Original article

Snakebite envenoming in Kerala, South India: clinical profile and factors involved in adverse outcomes
N Suchithra, J M Pappachan, P Sujathan
Department of Medicine, Kottayam Medical College, Kerala, South India Correspondence to: Dr J M Pappachan, Department of Medicine, Kottayam Medical College, Kerala, South India 686008; drpappachan@yahoo. co.in Accepted 5 October 2007

ABSTRACT Background: Snakebite envenoming is an important medical emergency in Kerala, but the factors leading to complications have not been well studied. Objectives: To study the clinical characteristics, factors involved in complications and the outcomes in relation to timing of polyvalent snake antivenom (SAV) administration in patients with snakebite envenoming. Methods: Patients were recruited from cases of snakebites admitted to the emergency care unit of Kottayam Medical College between May 2005 and December 2006. The manifestations of envenoming and complications were recorded. SAV was administered to cases with envenoming. Treated patients were analysed to determine the factors involved in complications and the outcomes in relation to the timing of SAV. Results: 200 (34%) of 586 cases with snakebites had envenoming; 58% were men, 52% were aged 31 50 years and 93% were outdoor bites. The species of snake was identified in 34.5% of the venomous bites. 93.5% had signs of local envenoming. Regional lymphadenitis occurred in 61%. The mortality rate was 3%. Capillary leak syndrome, respiratory paralysis and intracerebral bleeding were the risk factors for mortality. Those who received SAV early (bite to needle time ,6 h) had more severe local envenoming than those who received SAV late (bite to needle time >6 h), but the latter group were more likely to suffer complications. 39.5% had complications, with acute renal failure being the most common (25.5%). Those who received SAV late had a higher risk of developing acute renal failure. Higher rates of complications were seen in those with severe coagulopathy (OR = 8.0), leucocytosis (OR = 3.7) and those who received SAV late. Conclusions: Early administration of SAV reduces the risk of complications. The presence of leucocytosis and severe coagulopathy can predict adverse outcomes.

Snakebite envenoming is a complex medical emergency involving the site of the bite as well as multiple organ systems.4 7 8 The dynamic and erratic course of the envenomation syndrome requires close monitoring of the patient and careful clinical decision-making.9 Most snakebites are nonpoisonous, but clinicians should always be alert to detect the early clinical manifestations of envenoming. The seriousness of the clinical presentation of envenoming depends on the characteristics of the snakes and the victims. Administration of antivenom is the mainstay of treatment.3 4 6 7 911 Proper and timely administration of antivenom and supportive therapy may affect the rate of complications and the outcome in most situations.316 A study was conducted at Kottayam Medical College, the biggest tertiary care teaching institution and referral hospital for five districts of Kerala (Kottayam, Idukki, Pathanamthitta, Alappuzha and Eranakulam) with a population of about 6 million, to examine the demographic details, clinical characteristics, severity of envenoming, likelihood of complications and the factors determining the outcome following treatment in patients admitted to the emergency medicine department with snakebites between May 2005 and December 2006.

METHODS Study subjects

In this prospective cohort study, patients were selected from cases of snakebites admitted to the department of emergency medicine of Kottayam Medical College. Those who were not willing to participate in the study, patients with known systemic diseases (pre-existing renal disease, uncontrolled chronic obstructive airway disease, congestive heart failure and previous myocardial infarction) and those taking diuretics, anticoagulants and antiplatelet drugs were excluded from the study. This is because these illnesses and medications can alter the clinical and laboratory profile of patients with envenoming. An attempt at species identification was done (by the investigators) by inspecting the killed snakes brought by the patients or from their description of the snake involved. Informed consent was obtained from each participant and the study was approved by the ethical committee of the institution. The same team of investigators collected data from each patient using a preformed study sheet.

Snakebite envenoming is a common and lifethreatening medical emergency encountered in tropical and subtropical countries.1 2 Snakebites are estimated to cause 100 000 deaths each year worldwide and disproportionately affect rural populations in resource-poor settings.3 Complications set in fast, and the physician may lose valuable time and the patient unless she/he is very careful. There are about 15 000 deaths from venomous snakebites in India every year.4 5 Of the 3000 species of snakes found worldwide, 15% are considered dangerous and, of the 216 species of snakes found in India, 52 species are reported poisonous.5 However, most of the bites (and consequent mortality) is attributable to five species: namely, king cobra, common cobra, Russells viper, krait and saw-scaled viper.6
200

Study design
A detailed historyincluding the circumstances of the bite, site of the bite, time of the bite and details
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Original article
of treatment received prior to admissionwas obtained from each participant. Clinical examination was performed in each patient to assess the signs of local, regional and systemic envenoming4 8 and for the presence of complications at the time of admission and during treatment. Local signs and symptoms such as oedema, pain, tenderness, oozing from the site, blisters and skin necrosis were considered as evidence of local envenoming, and the degree of severity was categorised as mild, moderate and severe according to standard guidelines.8 Tender lymphadenitis at the draining region of the site of the bite was considered as a sign of regional envenoming.4 All the patients underwent the following investigations at the time of hospitalisation: blood haemoglobin level, total and differential leucocyte counts, platelet count, blood urea, serum creatinine, plasma sugar, sodium and potassium, prothrombin time/international normalised ratio (PT/INR), activated partial thromboplastin time (aPTT), whole blood clotting time, 12-lead ECG and chest radiography. Special tests such as arterial blood gas analysis, echocardiography and CT scanning were performed when considered appropriate for the clinical situation. Clotting time, PT, INR, aPTT and platelet counts were repeated 4-hourly for 24 h and, in those with abnormalities, these tests were repeated at 4-hourly intervals until they became normal. Blood urea, creatinine and electrolyte measurements were repeated every day in all patients with envenoming for 3 days (or longer in those with abnormalities) and more often if necessary. All the laboratory tests were repeated when necessary according to the clinical situation. Vomiting, abdominal pain, hypotension, neurological abnormalities, abnormalities of blood coagulation, renal dysfunction, intravascular haemolysis, capillary leak syndrome, cardiac arrhythmias and acute respiratory distress syndrome were considered as evidence for systemic envenoming. All patients who were found to have signs of envenoming were monitored at 4-hourly intervals by whole blood clotting time assays, and normalisation of the clotting time was used for monitoring the adequacy of antivenom administration. All patients with evidence of envenoming were treated with polyvalent snake antivenom (SAV) manufactured by the Serum Institute of India, Kolkotta (each vial of freeze-dried powder when reconstituted measured 10 ml SAV), useful against Russells viper, cobra, krait and saw-scaled viper envenoming. The dose of SAV administered was based on the standard protocol (determined by the degree of envenoming at the time of hospitalisation and the subsequent abnormalities of coagulation, monitored by whole blood clotting time).4 Other treatments given to the patients included local cleansing of the wound, tetanus toxoid injection and antibiotics according to the severity of the local injury. Supportive treatment was given to those with complications. Allergic reactions to SAV were treated with antihistamines, steroids and epinephrine, when necessary. Patients without evidence of local, regional or systemic envenoming were discharged after 24 h of observation. Those with clinical and/or laboratory evidence of envenoming were managed with SAV and other supportive measures until discharged from hospital or death. Patients treated for envenoming were analysed for factors involved in adverse outcomes in relation to the timing of SAV administration. The relationships between the bite to needle time and the time interval needed for the normalisation of clotting time and coagulopathy, and the relationships between the severity of local envenoming and the development of complications were also analysed. The bite to needle time in
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patients referred from other hospitals who received SAV prior to admission to this institution was determined by consultation with the referring physician, by verifying the referral letter and by cross-verification with the patient.

Statistical methods
x2 test for nominal level measurements, t test for independent samples and the Mann-Whitney U test for the interval ratio measurements were used.

RESULTS
Of the 635 patients admitted with snakebites (219 with envenoming) during the study period, 586 patients who met the inclusion criteria were analysed. Of these, 200 cases were venomous bites of which 98.5% were accidental, 93% were outdoor bites and 81% were in the lower limbs; 58% were men and 52% were aged 3150 years (median age 40 years). Most of the patients were brought to the emergency care unit by ambulances or cars and the average distance travelled was 54 km (range 2164 km). Tourniquets were applied above the bitten area in the limbs by 62 patients (31%) as first-aid, but there was no statistically significant difference in the outcome for these patients. The median duration of hospital stay was 5 days (range 2 42). Six patients (3%) died even after treatment with SAV (median duration of treatment 3 days; range 6 h12 days). Table 1 Local, regional and systemic manifestations and complications of snakebite envenoming
Abnormalities observed in patients with envenoming Local signs of envenoming Oedema of bitten limb Pain at site of bite Tenderness at site of bite Fang marks Local skin necrosis Oozing of blood from bite mark Severe blistering of bite area Regional signs of envenoming Tender regional lymphadenitis Systemic signs of envenoming at time of hospitalisation (total) Vomiting Abdominal pain Anuria/oliguria Hypotension Spontaneous bleeding tendency Neurological signs Syncope Ventricular tachycardia Complications (total) Acute renal failure* Intravascular haemolysis Hypotension requiring ionotropic support Secondary infections Compartment syndrome requiring fasciotomy Intracerebral bleeding Acute respiratory distress syndrome Capillary leak syndrome Respiratory paralysis Ventricular tachycardia without heart disease N (%)

187 151 141 107 81 55 12 122 83 53 44 14 9 8 6 4 1 79 51 39 8 5 4 4 3 2 2 1

(93.5) (75.5) (70.5) (53.5) (40.5) (27.5) (6.0) (61.0) (41.5) (26.5) (22.0) (7.0) (4.5) (4.0) (3.0) (2.0) (0.5) (39.5) (25.5) (19.5) (4.0) (2.5) (2.0) (2.0) (1.5) (1.0) (1.0) (0.5)

*Acute renal failure was defined by the presence of one or more of the following parameters: elevation of creatinine .88.4 mmol/l from the baseline value in 24 h, reduction in urine output to ,400 ml/24 h and baseline creatinine .210 mmol/l in the absence of a previous history of renal disease and subsequent normalisation to ,132 mmol/l after treatment.

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Table 2 Severity of local envenoming: bite to needle time
Severity of local envenoming Mild Moderate Severe Early SAV (,6 h) (n = 156) 41 (26.3%) 103 (66.0%) 12 (7.7%) Late SAV (>6 h) (n = 44) 25 (56.8%) 17 (38.6%) 2 (4.5%) Total (n = 200) 66 (33%) 120 (60%) 14 (7%) x2 = 14.474 p,0.001

Seasonal and diurnal variation was noted in both venomous and non-venomous bites. The peak incidence of snakebites occurred between May and July, the monsoon season in Kerala; 61% of all snakebites and 64% of the venomous bites occurred in the evening hours (18:0022.00 h). Species identification was possible in only 69 cases of the venomous bites (34.5%). Of these, 65 (32.5%) were viper bites, 3 were cobra bites and 1 was a krait bite. Species identification was not possible in the majority of non-venomous bites (67.5%). One krait bite and one cobra bite did not cause any envenoming. The clinical manifestations, laboratory abnormalities and the complications observed in patients with envenoming are shown in table 1. The severity of local envenoming was found to be significantly higher in those patients who were admitted to the emergency unit early (bite to needle time ,6 h) as shown in table 2, but the risk of developing complications was higher in those with less severe local envenoming, many of whom were admitted late (table 3). All the patients with envenoming were treated with SAV, tetanus toxoid injections and appropriate antibiotics. The mean bite to needle time was 5.8 h (range 0.548). Whole blood or blood products (platelet-rich plasma and fresh frozen plasma) were required by 107 cases (53.5%) for correction of anaemia or severe coagulopathy; 25 patients (12.5%) required dialysis for acute renal failure. Only two patients with respiratory paralysis due to neurological signs of envenoming required ventilatory support together with neostigmine and atropine. Thirty cases developed allergic reactions to SAV and eight of them had a severe anaphylactic reaction. In patients with envenoming, the mean dosage of SAV given was 220 ml (range 30620). A total of 156 patients (78%) received SAV early ((6 h); 29 cases received SAV from local hospitals before admission to the emergency unit, and the reason for referral was renal failure in 21 cases and coagulation failure in 8 cases. An abnormal coagulation profile was seen in 142 cases; 103 of these had severe coagulopathy (platelet count ,506109/l, PT .20 s, INR .1.8, aPTT .1 min or blood not coagulable) and 15 had thrombocytopenia (platelet count ,1506109/l) alone in the absence of significant prolongation of clotting time. The mean time taken for normalisation of the abnormal coagulation profile with reference to the bite to needle time was analysed statistically (table 4). There was no significant difference between patients receiving SAV early and those receiving SAV late, but there was a significant difference in the mean time

taken to normalise whole blood clotting time between the two groups (table 4). Of the four patients who developed intracerebral bleeding (all had severe coagulopathy), two patients died (because of cardiorespiratory arrest) despite treatment with SAV and supportive measures. Two patients survived with residual neurological sequelae. Both patients who developed respiratory paralysis from neurotoxic envenoming died (one from cardiac arrest and the other from aspiration pneumonia) despite SAV treatment and ventilatory support. Two patients who developed capillary leak syndrome also died (because of acute respiratory distress syndrome). The relationship between the bite to needle time and the development of complications is shown in fig 1. Of the 51 patients who developed acute renal failure, 25 required haemodialysis. The delay in the administration of SAV following envenoming was associated with a significant risk for the development of acute renal failure (fig 2). Leucocytosis and severe coagulopathy were also associated with high odds for the development of complications (table 5A&B).

DISCUSSION
The high incidence of snakebites in Kerala is related to the occupational characteristics of the population (the majority are engaged in farming), the high population density and also the large number of snakes found in this region. The high literacy rate, easy availability of healthcare and good public transportation systems make Kerala unique compared with the other Indian states in reducing the mortality rates and presumably also from snakebite envenoming.17 18 We also observed a high incidence of non-venomous bites. The lower incidence observed in other studies may be due to under-reporting.6 15 16 Although the male to female sex ratio in cases of venomous bites was comparable to one study from Sri Lanka,19 it was much lower than in some other studies.5 12 20 21 This may be due to the occupational characteristics of the study population (both men and women in Kerala are engaged in agricultural work). The higher rate of snakebites during the evening hours in this study compared with other studies15 16 20 21 may also be explained by this fact. As observed in other studies, 6 20 21 the most common bite sites were the lower limbs. In most cases the clinical characteristics (haemotoxic features) suggested viper bites. The incidence of bites by elapid snakes in our series was surprisingly low compared with other studies.6 15 16 20 The incidence of neurological signs of viper envenoming was also lower than that

Table 3 Severity of local envenoming: snakebite complications

Severity of local envenoming Mild Moderate Severe Complications present (n = 79) 34 (43.04%) 39 (49.37%) 6 (7.59%) Complications absent (n = 121) 32 (26.45%) 81 (66.94%) 8 (6.61%) Total (n = 200) 66 (33%) 120 (60%) 14 (7%) x2 = 6.514 p = 0.039

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Table 4 Relationship between bite to needle time and time needed for reversal of the abnormal coagulation profile, and between bite to needle time and time needed for normalisation of abnormal (.20 min) whole blood clotting time
Bite to needle time n Mean time (h) SD Minimum time (h) Maximum time (h)

Time taken for reversal of abnormal coagulation profile* (n = 142) Early SAV (,6 h) 111 71.8 64.56 Late SAV (>6 h) 31 75.5 73.01

6 12

264.00 240.00

t = 0.275 p = 0.784

Time taken for normalisation of abnormal whole blood clotting time (n = 127) Early SAV (,6 h) 102 37.25 48.875 2 Late SAV (>6 h) 25 54.72 71.505 12

192 240

p = 0.020

SAV, polyvalent snake antivenom. *Prothrombin time, international normalised ratio, activated partial thromboplastin time and low platelet count.

reported by others.21 22 Future epidemiological studies may elucidate the reasons for the low incidence of bites by elapid snakes and also the low rates of neurological features in cases of viper bites in this geographical area. The bite to needle time was lower in our study than that reported by others.20 23 The high awareness among the public in this region about the hazards of snakebite envenoming may be the reason why most patients with snakebites get to the emergency unit quickly. Those who received SAV late had a greater likelihood of developing complications than those who received SAV early. Timely administration of antivenom is the mainstay of treatment for snakebite envenoming, and there is a definite correlation between the development of complications and bite to needle time.3 5 7 1012 20 23 24 High mortality is also related to the delay in treatment.12 15 16 19 23 The early treatment of most cases may be the reason for the low mortality observed in our study. More severe local envenoming and the related symptoms might have been the reason for early admission to hospital in most of those who received SAV early and who therefore had

less chance to develop complications than those who received SAV late. This observation highlights the importance of early hospitalisation of all cases of snakebites, regardless of the symptoms, and observation for a minimum period of 24 h.10 Allergic reactions are the most commonly reported adverse events after administration of SAV, and the reactions are easily managed by a combination of antihistamines, epinephrine and steroids, with prompt resolution of signs and symptoms enabling further dosing of SAV as required.25 Allergic reactions to SAV occurred in 15% of our cases but all were managed easily. The incidence of allergic reactions and the response to treatment was similar to those observed by others.20 Acute renal failure is an important complication of snakebite envenoming. In a recent large-scale study reported from South India, 7.8% of cases of acute renal failure were caused by snakebites.26 The incidence of acute renal failure observed in our study was high, but many of the patients had only mild renal failure. This may also be related to the shorter mean bite to needle time. The significant risk of development of acute renal failure seen in those with higher bite to needle time also

Figure 1 Relationship between timing of polyvalent snake antivenom (SAV) administration after snakebites (bite to needle time, in hours) and the percentage of cases developing complications.
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Figure 2 Relationship between timing of polyvalent snake antivenom (SAV) administration after snakebites (bite to needle time, in hours) and the percentage of cases developing acute renal failure (ARF).
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Table 5 Relationships between severe coagulation abnormality and the development of complications and total leucocyte count and the development of complications
Severe coagulation abnormality Complication Present Absent Total Present 63 (61.2%) 40 (38.8%) 103 (100%) Absent 16 (16.5%) 81 (83.5%) 97 (100%) Total 79 (39.5%) 121 (60.5%) 200 (100%) x2 = 41.712 Total leucocyte count >116109/l ,116109/l 35 (24.4%) 96 (75.6%) 131 (100%) Total 70 (35.0%) 130 (65%) 200 (100%) x2 = 16.5 p,0.001 OR = 3.7 95% CI 1.9 to 7.0

p,0.001 35 (50.7%) OR = 8.0 34 (49.3%) 95% CI 4.09 to 15.53 69 (100%)

supports this conclusion. Although the overall incidence of acute renal failure in our study was comparable to other reports,13 20 the percentage of patients requiring dialysis was lower. The large differences in the incidence and requirement of dialysis in acute renal failure resulting from snakebite envenoming reported from various regions of the world may be related to the species differences in the offending snakes and the differences in the bite to needle time.5 12 13 20 21 23 The 20-min whole blood clotting test is a simple, rapid and reliable test of coagulopathy in snakebite envenoming.16 This test can also be used to monitor venom neutralisation in those treated with SAV. Although monitoring of PT and aPTT may give better evidence of the degree of consumption coagulopathy, the time taken for normalisation of these parameters may be long.27 However, the significant risk of complications in those with severe coagulopathy (OR = 8) mandates monitoring of these parameters for predicting an adverse outcome. The higher rates of complications observed in those with leucocytosis (OR = 3.7) should also alert clinicians managing cases of snakebite envenoming. The significant risks of high mortality in our study were capillary leak syndrome, respiratory paralysis and intracerebral bleeding. Patients with capillary leak syndrome and respiratory paralysis had 100% mortality despite treatment with SAV and supportive measures. Intracerebral bleeding was another complication with a high mortality rate (50%), as noted previously by others.24 Although there are conflicting reports about the usefulness of SAV and its dosage in reversing some of the neurological complications and respiratory paralysis,2 19 22 early administration of SAV might prevent most of these complications. Reversal of coagulopathy and improvement of local signs of envenoming may be seen even after a delay in SAV treatment.28

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15. 16. 17. 18. 19. 20.

CONCLUSIONS
Snakebite envenoming is an important cause of admission to the emergency care unit in Kerala. The case fatality rate is relatively low. Capillary leak syndrome, respiratory paralysis and intracerebral bleeding are the significant predictors of mortality. Delay in the administration of SAV, presence of polymorphonuclear leucocytosis and severe coagulopathy are associated with higher rates of complications. All patients with snakebites, regardless of the degree of local symptoms and signs, should be admitted to hospital early for investigation and for observation and treatment to reduce the likelihood of complications related to envenoming.
Funding: None. Competing interests: None.

21. 22. 23. 24. 25. 26. 27. 28.

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