Med Clin (Barc).
2015;144(3):132–136
www.elsevier.es/medicinaclinica
Special article
Changes in viper bite poisonings夽
Novedades en el envenenamiento por mordedura de víbora
Cristina Martín a,∗ , Santiago Nogué b
a
Mutua ASEPEYO, Teruel, Spain
b
Servicio de Urgencias, Hospital Clínic, Barcelona, Spain
a r t i c l e i n f o
Article history:
Received 26 May 2014
Accepted 12 June 2014
Available online 26 September 2015
Introduction
Snakebites are rarely reported in the emergency departments
of our local hospitals but when a case arrives it always produces
great expectancy. For years, clinical manifestations and treatment
have been grouped together but recently there have been signifi-
cant changes in some of the symptoms of envenomation produced
by certain snakes in Europe. These changes bring about modifica-
tions in the way patients are treated and force us to take serious
precautions in controlling their evolution.
New species and new classification
In recent years, new snake species have been discovered in the
world. The number of different species has grown to 3432, which
has led to a new classification in the order Ophidia and in the respec-
tive families, subfamilies, genera, species and subspecies1 .
Regarding the subfamily Viperinae, which includes the European
viper, there have also been changes in the genera in which the
different species and subspecies are classified. Table 1 shows the
main genera in this subfamily, and the main European species and
subspecies, as well as their location2–7 .
Epidemiology
The epidemiological work on snakebites by Swaroop and
Grab8 has served as a worldwide reference in epidemiology for
decades. But the most up-to-date figures are those presented by
夽 Please cite this article as: Martín C, Nogué S. Novedades en el envenenamiento
por mordedura de víbora. Med Clin (Barc). 2015;144:132–136.
∗ Corresponding author.
E-mail address: martinsierramc@hotmail.com (C. Martín).
2387-0206/© 2014 Elsevier España, S.L.U. All rights reserved.
Chippaux9,10 , which indicate that 5.4 million people are bitten by
snakes in the world, causing 2.7 million envenomations and 125
000 deaths every year. In a subsequent meta-analysis, the same
author provides figures for Europe (including Turkey and Russia up
to the Ural Mountains and Caucasus): of a total of about 8000 cases
per year, 1000 are severe and 4 are fatal in Europe11 .
The Spanish case study that most closely approaches the real
problem of snakebites is that presented by the Instituto de la Salud
Carlos III (Health Insititute Carlos III)12,13 as it collected all hospital
discharges from 1997 to 2012, with a mean of 133 cases per year
and a mortality of 1.2 cases per year. Of all the autonomous com-
munities, Catalonia provides the largest number of cases, followed
by Castile and León, Galicia and Andalusia. The distribution of cases
shows prevalence in male subjects (68.6%) and an age range of 5-14
years (31% in the whole series) as the target population for these
accidents.
Characteristics of the venom
Snake venom is one of the most complex toxins developed
by nature. Its composition and activity vary between families,
genera, species and even subspecies, but the nearer they are
phylogenetically, the more similar their characteristics will be.
The macroscopic characteristics of these venoms differ little,
although they do differ in protein composition14 . Methods of
protein analysis such as reversed-phase chromatography, two-
dimensional electrophoresis, and transcriptome and proteome
analyses have revealed that the proteins of these venoms belong
to 10-12 families15–17 , including enzymes (serine protease, Zn2+ -
metalloprotease, phospholipase A2 , L-amino acid oxidases) and
proteins without enzymatic activity (natriuretic peptides, disinte-
grins, Kunitz-type protease inhibitor, cystatin, C-type lectins and
specific of galactose, nerve, vascular and endothelial growth factor
and CRISP toxins). These proteins present multiple isoforms and
 C. Martín, S. Nogué / Med Clin (Barc). 2015;144(3):132–136 133

Table 1
Species and subspecies of European snakes and geographic areas of distribution.

Subfamily Viperinae (genera: Atheris, Bitis, Causus, Cerastes, Daboia, Echis, Eristicophis, Macrovipera, Montatheris, Montivipera, Proatheris, Pseudocerastes, Vipera)

European species Described subspecies Distribution

Vipera berus (Balkan viper) V.b.berus All Eurasia, from France to the north of the Arctic Circle
V.b.bosniensis and to the Pacific Ocean.
V.b.sachalinensis In all Europe, except the Iberian Peninsula and Ireland.
Partially excluded from Italy and Greece
Macrovipera or Daboia lebetina Ml lebetina North Africa, Middle East and Asia.
(viper from the East) Ml obtusa In Europe, in Cyclades islands, Milos and Cyprus
Ml turanica
Ml cernovi
Ml trasmediterranea
Montivipera or Daboia xanthina Eastern zone of Greece, the European part of Turkey
(Turkish viper) and islands of the Aegean Sea
Vipera ammodytes (horned viper) Va ammodytes Eastern Europe, particularly in the Balkans, Italy,
Va montandoni Romania and extended to the south to Greece and the
V.a.meridionalis Cyclades. Also in Armenia, Georgia, Turkey and Libya
V.a.gregorwallneri
V.a. transcaucasia
Vipera ursinii (Ursini’s viper or Of discontinuous distribution, it appears in isolated
meadow viper) and generally small populations in South-eastern
France, the centre of Italy, Hungary, Romania, Bulgaria,
Croatia, Bosnia-Herzegovina, Montenegro, Serbia,
Macedonia, central Asia, Turkey and Iran.
Vipera aspis (aspic viper) V.a.aspis North East of the Iberian Peninsula, centre of Europe
V.a.zinnikeri and the islands of Elbe, Sicily and Montecristo
V.a.francisciredi
V.a.hugyi
V.a.atra
V.a.montecristi
Vípera latastei (snub-nosed viper) V.l.latastei The Iberian Peninsula, with the exception of the north
V. l.gaditana
Vípera seoannei (viper of Seoane) V.s.seoanei Green Spain and the northwest of the Iberian Peninsula
V.s.cantabrica

contribute to the complexity of the venoms and the diversity of
their effects.
Frequently, the venom of European vipers has been described
to have cytotoxic and haemotoxic activities, above all affecting
the coagulation system, both procoagulant and anticoagulant func-
tions. The venom of the horned viper (Vipera ammodytes) is an
exception, characterised by its neurotoxic, cytotoxic and haemo-
toxic effects. But in the last 20 years, the unusual has become
the norm and the neurological manifestations after bites from one
of the European asp species (V.aspis aspis, V.aspis zinnikeri) and
and the Balkan cross adder (V.berus bosniensis) have become the
norm. Several countries in the region have noticed the severity of
these manifestations. This neurotoxicity is thought to be the action
of phospholipase A2 (PLA2 )18–24 . The different PLA2 isoenzymes
may provoke haemolysis, myotoxicity, presynaptic neurotoxicity
and postsynaptic neurotoxicity, cardiotoxicity, oedemas and pro-
coagulant and anticoagulant activities. Table 2 shows neurotoxins
described in the European species.
The causes of this versatile presentation of protein isoforms
and the variations in the effects of the venoms are not clear. It is
believed that changes in the ecological niche (human movements
that force the animals out of their usual habitats), in food (changes
in diet), individual factors (sex, age, season), environmental fac-
tors (higher temperatures, changes in precipitation patterns) or
maybe hybridization among species obliged to share territories,
could determine changes in venom activity. Or perhaps it is only
another step in the Darwinian evolution of the species 15–17,25,26 .
Clinical Manifestations
The first signs and symptoms of viper envenomation are usu-
ally pain and oedema in the region of the bite. Minute by minute,
the intensity of pain tends to increase and to radiate towards the
root of the extremity, while oedema progresses. These symptoms
indicate envenomation. Ecchymosis can be seen at the site of the
bite with a similar tendency to progress, not necessarily associ-
ated with a clotting disorder but with the capillary-permeability
alterations that allows the red blood cells to escape27 .
Hour by hour, systemic manifestations can appear. Neurological
manifestations usually start to appear in the first 4-12 h, palpe-
bral ptosis being the most frequent symptom28 . Other symptoms
can include ophthalmoplegia, diplopia, accommodation deficit, and
dysarthria, paralysis of the sphincter oris, dysphagia and other
general manifestations like lethargy, vertigo, dyspnoea and even
paresthesia29,30 . In France, a Guillain-Barré syndrome has been
described after a vipera aspis bite, although without a full descrip-
tion of the pathogenic mechanism (direct or indirect neurotoxicity
of the venom)28 . It is mentioned as a characteristic feature of viper
envenomation with neurological manifestations, and usually starts
with scarce local symptoms; this should serve as a warning of the
possible appearance of neurological manifestations.
New grading of envenomation
The Audebert grading scale to classify the degree of envenoma-
tion from the European species is used as a therapeutic guideline31 .
But the appearance of neurological manifestations has forced a
change in the grading of viper envenomations. Thus, regardless of
the local reaction, which usually indicates the progression of the
symptoms (pain and oedema), the appearance of neurological man-
ifestations directly classifies the envenomation as grade ii, with the
corresponding consequences regarding treatment (table 3).
Obsolete therapeutic interventions
A consensus exists among professionals from different countries
about those practices that should be avoided. Thus, the use of
tourniquets, cauterizations, amputations of the injured body part,
134 C. Martín, S. Nogué / Med Clin (Barc). 2015;144(3):132–136

Table 2
Species and subspecies with neurotoxic activity observed.

Vipers Subspecies Neurotoxin Effect

Va ammodytes V.ammodytes ammodytes Ammodytoxin A, B, C Presynaptic toxin

Vipoxin Postsynaptic toxin
V.ammodytes meridionalis Vipoxin Postsynaptic toxin
V.aspis V.aspis aspis Ammodytoxin A, B, C Presynaptic toxin
Vaspin Postsynaptic toxin
V.aspis zinnikeri PLA2-I Postsynaptic toxin
V.a.francisciredi Not studied Not studied
V.berus V.berus berus Not found Not found
V.berus bosniensis Not studied Not studied

incision and suction of the wound (with the mouth, extrac-
tors or syringes), the application of homemade remedies (plants,
whiskey, gunpowder, dragonfly infusions or bugs mixed with
turtle blood) are techniques that must be eradicated, not only
because they are not indicated, but also because they are clearly
contraindicated28,32–34 . It is surprising that on some health web-
sites consulted to write this review, the use of some of these
techniques is still recommended.
First aid measures
After a bite, it is essential to ask for help, particularly if signs
of progressive, fast envenomation are observed (calling the emer-
gency line 112 is recommended). The patient should be prevented
from tiring themselves by walking since this could facilitate a
quicker distribution of the venom through the organism. Avoid the
consumption of any type of food or stimulating products (either by
digestive or respiratory tract, much less intravenously). Any cloth-
ing that might apply pressure to the zone near the bite should be
removed, as well as any personal jewellery (bracelets, watches,
rings, piercings) that could produce a tourniquet effect, in case of
oedema28,35–37 .
The objective of local treatment is only to clean and disinfect the
injured area. Cleaning should be with soap and water. Any anti-
septic that might unnecessarily colour the skin must be avoided.
If available, a slightly constricted bandage can be applied follow-
ing the classic guidelines, i.e., from distal to proximal. Elevation of
the limb and application of indirect cold will help to diminish the
oedema.
It is important to gather information about the place (province,
nearby town or city, surroundings, altitude), the hour of the day,
the general description of the snake (the characteristic aspects of
the European vipers are a triangular head with multiple, small
scales, vertical pupil, zigzag pattern on the back, thick, short body,
well-marked short tail, and elusive attitude) to try to identify the
species2–6,36,37 .
Out-of-hospital treatment
If first aid is performed in a health or emergency centre, the
measures to put into practice will be those previously described. It
is important to manage the progression of the envenomation stage,
assess the evolution of local pain, oedemas and ecchymosis, as well
as the appearance of signs and symptoms of systemic envenoma-
tion. In addition, treatment with analgesics and anxiolytics can be
started, if necessary. Salicylates should be avoided. The anti-tetanus
prophylaxis must be checked and transportation arranged to the
nearest hospital or facility with antiophidic serum.
The use of antibiotics or low-molecular-weight heparin is not
recommended. The use of adrenaline, antihistamines and corti-
costeroids is recommended only in the case of an anaphylactic
reaction, which is highly exceptional28,37 .
In-hospital treatment
Transfer to a hospital for medical assessment and treatment is
mandatory in this type of emergency. An initially simple clinical
condition could worsen significantly putting the patient at risk.
Once in the hospital, the procedure will be to check vital signs,
to make a physical examination and to run some complemen-
tary tests: electrocardiogram, haemogram, haemostasis (platelets,
prothrombin time, international normalised ratio [INR], fibrino-
gen, fibrinogen degradation products [FDP]), biochemistry (liver
and kidney functions) and urine analysis (haematuria and urine
protein)28,37 . The pharmacological treatment will depend on the
degree of envenomation and its progression.
• In grade 0 snakebites, observation of the patient in the emergency
department for a minimum of 6 h is necessary, since neurolog-
ical manifestations can take several hours to appear. Clean the
wound, apply indirect cryotherapy, raise the limb, administer
anti-tetanus prophylaxis if applicable, and start antibiotic and
analgesia administration if necessary. If there is no progression,
admission is not necessary. Rest is recommended for some hours

Table 3
Clinical manifestations of the different envenomation degrees.

Grade 0 (no envenomation)
Grade I (mild envenomation)
Grade II (moderate envenomation)
[1,0] Grade III (severe envenomation)
Absence of local or systemic reaction. Only tooth marks and mild or scarce pain. Probable bite of an aglyphous or
opisthoglypha snake, or a viper that has not inoculated venom (“dry” bite)
There are tooth marks from the bite, intense pain, moderate local oedema that can progress to blisters, but that do not go
beyond the limb. There are no systemic symptoms.
In addition to the grade I injuries, there are oedema progression, ecchymosis, lymphangitis, adenopathys or systemic
manifestations such as moderate arterial hypotension, nausea, vomiting, diarrhoea, abdominal pain, dizziness, general
discomfort or asymptomatic haemato-haemostatic alterations (leukocytosis, thrombocytopaenia, hypofibrinogenaemia)
Neurological symptoms: palpebral ptosis, accommodation deficit, ophthalmoplegia, diplopia, dysarthria, dysphagia, paralyses
of the sphincter oris, lethargy, vertigo or paresthesia
In addition to the grade ii lesions, greater regional oedema that can go beyond the injured limb, very intense pain and severe
systemic manifestations (rhabdomyolysis, scattered intravascular coagulation, bleeding tendency, acute renal failure,
respiratory failure, shock, haemolysis, fluid and electrolyte imbalance)
Severe neurological symptoms
 C. Martín, S. Nogué / Med Clin (Barc). 2015;144(3):132–136
and the patient should return for medical assessment in case of
any changes.
• In grade isnakebites, admission to hospital for 24 h to check the
evolution of the envenomation (oedema, pain, haematological or
neurological alterations). The examination should be repeated
periodically. It is recommended that the initial location of oedema
should be marked with a marker pen in order to follow its evo-
lution. Clean the wound, immobilize and raise the limb, apply
indirect cryotherapy; the patient should rest, preferably in bed;
review the anti-tetanus prophylaxis, administer therapy with
antibiotics and intravenous treatment for pain if necessary. Com-
plete fasting and serum therapy as a maintenance therapy.
• In grade ii and iiisnakebites, patient should be admitted to hospital.
Serial blood tests should be performed. Continuous assessment of
the local progression of envenomation and of the appearance of
possible neurological or haematological complications. Admin-
istration of intravenous antiophidic serum (dissolved in saline)
is added to grade i measures. This serum should be adminis-
tered early to pregnant women and if compartment syndrome
develops; in children, the dose will be the same as in adults.
Assess patient admission to intensive care unit (ICU) and con-
sider surgical treatment of necrosis in the perilesional area or
if compartment syndrome does not respond to the antiophidic
serum.
One of the more controversial treatments is antibiotic
therapy28,37–39 . It should not be forgotten that the mouth of the rep-
tile hosts germs, among them Salmonella, Clostridium, Escherichia
coli and Klebsiella, in addition to pentastomid parasites from the
family Porocephalidae, like Armillifer armillatus, A.moniliformis and
A.grandis, arthropods that inhabit the mouth and respiratory tract
of snakes and can pass to humans through the bite. The antibiotic
treatment suggested, as first choice, is amoxicillin-clavulanic treat-
ment, replaced by erythromycin or clindamycin in case of allergy.
Viperfav® serum (Laboratory Sanofi-Pasteur, Lyon, France) is
used in hospitals in Spain. It was used for the first time at the begin-
ning of 2000 but had already been used in neighbouting countries
and its safety had been confirmed24,32,40,41 . This is a third gener-
ation antivenom, i.e., composed of horse antibodies against the
venom of several snake species (V.aspis, V.ammodytes and V.berus),
subsequently treated with pepsins to obtain the F(ab)2 fragment
from the FC fragment of the antibodies. This last fragment is respon-
sible for the anaphylactic (grade i) and immune-complex (grade
iii) Reactions. Hence, these complications are no longer expected
to appear19,28,40,41 . For the same reason, it is no longer recom-
mended to perform a hypersensitivity test prior to administering
the antidote or corticosteroid treatment after the administration
of the antidote to prevent the appearance of serum sickness. The
antidote must be administered under strict medical supervision,
intravenously in a limb other than that which has been bitten.
Compartment syndrome after snake envenomation
Although exceptional, it is possible to develop secondary
compartment syndrome after the venom inoculation, with the pro-
gressive appearance of the clinical manifestations described as the
6 Ps: paresthesias, pain, pressure, pallor, paralysis and pulseless42 . In
these cases, as initial treatment, physical measures are suggested
(raising the limb, indirect cryotherapy) and intravenous adminis-
tration of the antiophidic serum. Fasciotomy is necessary if high
intracompartment pressure persists43–45 . Experiments in animals
indicate that initial management with antiophidic serum is the
guideline to be followed but no prospective clinical studies have
confirmed the effectiveness or value of an extra dose of antivenom
for this syndrome.
135
If compartment syndrome is suspected, the following thera-
peutic scheme has been proposed46 . Measure intracompartment
pressure and verify whether or not it is high (>30 mmHg). Apply
physical measures, such as raising the injured limb. Administer
intravenous mannitol at a dose of 1-2 g/kg and one vial of intra-
venous antiophidic serum. Hourly assessment of the evolution and,
if these measures failed to normalise pressure within 4 h, urgent
fasciotomy is recommend.
Conflict of interest
The authors declare that there are no conflicts of interest.
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