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BITES AND ENVENOMATIONS BY COLUBRID SNAKES IN MEXICO AND CENTRAL AMERICA

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©2002 Marcel Dekker, Inc. All rights reserved. This material may not be used or reproduced in any form without the express written permission of Marcel Dekker, Inc. MARCEL DEKKER, INC. • 270 MADISON AVENUE • NEW YORK, NY 10016 BITES AND ENVENOMATIONS BY COLUBRID SNAKES IN MEXICO AND CENTRAL AMERICA Jose ´ Marı ´a Gutie ´rrez 1, * and Mahmood Sasa 1,2 1 Instituto Clodomiro Picado, Facultad de Microbiologı ´a, Universidad de Costa Rica, San Jose ´, Costa Rica 2 Organization for Tropical Studies, San Jose ´, Costa Rica ABSTRACT Information on bites by snakes of the family Colubridae in Mexico and Central America is reviewed. Little is known of the biochemistry and pharmacology of the Duvernoy gland secretion (venom) of colubrids from this region, although some reports describe proteolytic, phosphodiesterase, phospholipase A 2 and hemorrhagic activities. A search of published reports and an effort to obtain reliable unpublished information on colubrid snake bites in the region documented cases inflicted by species of the genera Conophis, Coniophanes, Crisantophis, Erythro- lamprus, Pliocercus, Oxybelis and Dryadophis (= Mastigodryas). The following general pattern emerges from the analysis of these cases: 1) Bites occurred mainly in hands and fingers on people * Corresponding author. Fax: + 506-2920485; E-mail: [email protected] 105 Copyright D 2002 by Marcel Dekker, Inc. www.dekker.com J. TOXICOL.—TOXIN REVIEWS, 21(1&2), 105–115 (2002) Toxin Reviews Downloaded from informahealthcare.com by North Carolina State University on 10/05/12 For personal use only.
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©2002 Marcel Dekker, Inc. All rights reserved. This material may not be used or reproduced in any form without the express written permission of Marcel Dekker, Inc.

MARCEL DEKKER, INC. • 270 MADISON AVENUE • NEW YORK, NY 10016

BITES AND ENVENOMATIONS BYCOLUBRID SNAKES IN MEXICO

AND CENTRAL AMERICA

Jose Marıa Gutierrez1,* and Mahmood Sasa1,2

1Instituto Clodomiro Picado, Facultad de Microbiologıa,

Universidad de Costa Rica, San Jose, Costa Rica2Organization for Tropical Studies, San Jose, Costa Rica

ABSTRACT

Information on bites by snakes of the family Colubridae in

Mexico and Central America is reviewed. Little is known of the

biochemistry and pharmacology of the Duvernoy gland secretion

(venom) of colubrids from this region, although some reports

describe proteolytic, phosphodiesterase, phospholipase A2 and

hemorrhagic activities. A search of published reports and an

effort to obtain reliable unpublished information on colubrid

snake bites in the region documented cases inflicted by species

of the genera Conophis, Coniophanes, Crisantophis, Erythro-

lamprus, Pliocercus, Oxybelis and Dryadophis (=Mastigodryas).

The following general pattern emerges from the analysis of these

cases: 1) Bites occurred mainly in hands and fingers on people

* Corresponding author. Fax: + 506-2920485; E-mail: [email protected]

105

Copyright D 2002 by Marcel Dekker, Inc. www.dekker.com

J. TOXICOL.—TOXIN REVIEWS, 21(1&2), 105–115 (2002)

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©2002 Marcel Dekker, Inc. All rights reserved. This material may not be used or reproduced in any form without the express written permission of Marcel Dekker, Inc.

MARCEL DEKKER, INC. • 270 MADISON AVENUE • NEW YORK, NY 10016

that frequently manipulate colubrids, i.e. herpetologists, herpe-

toculturists and people that take care of these snakes at museums,

exhibits or zoos; and 2) In most cases, only mild local effects

were described, i.e. pain, swelling and, in few cases, ecchymosis.

In only one case by Erythrolamprus bizonus there was ecchy-

mosis beyond the bitten region, whereas persistent bleeding at

the bite site was reported in a Conophis lineatus case. No

systemic alterations were described in any of the cases. Ma-

nagement of colubrid bites in Mexico and Central America

includes cleaning and disinfection of the bitten area, together

with administration of tetanus toxoid. In the case of local

infection, antibiotics are administered. There is no experimental

or clinical evidence supporting the use of Crotalinae antivenoms

in these bites. Despite the lack of systemic alterations in the

cases described, caution should be exercised when manipulating

these snakes, and bitten people should be closely observed for

the potential development of bleeding and coagulopathies, since

these effects have been described in bites by colubrid snakes

from other regions of the world.

Key Words: Coagulopathy; Colubrid snakes; Duvernoy’s

secretion; Edema; Snake bite; Venom

INTRODUCTION

The family Colubridae (order Squamata, suborder Serpentes) is a

polyphyletic group that comprises the majority of extant snake species.[1] A

large number of colubrid species are distributed in Mexico and Central America,

displaying an amazing spectrum of anatomical, physiological and behavioral

adaptations.[1] In this region, the great majority of species are generally

considered non-venomous for humans and, therefore, have received little

attention from the clinical standpoint. However, colubrid species in this region

have Duvernoy glands, located in the posterior supralabial region, which

produce a potentially toxic secretion that reaches the oral cavity via a duct that

opens near enlarged grooved posterior maxillary teeth, in the typical

ophistoglyphous dentition pattern.[2] Other colubrid species also produce a

Duvernoy gland secretion but lack enlarged fangs, having therefore an agly-

phous dentition pattern.

Despite the biological relevance of colubrid snakes in Mexico and Central

America, there is little information concerning the biochemistry and pharma-

cology of their venoms. Moreover, there are few systematic records on the

epidemiological and clinical features of colubrid snake bites in this region. This

106 GUTIERREZ AND SASA

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©2002 Marcel Dekker, Inc. All rights reserved. This material may not be used or reproduced in any form without the express written permission of Marcel Dekker, Inc.

MARCEL DEKKER, INC. • 270 MADISON AVENUE • NEW YORK, NY 10016

review summarizes the information on the bites by colubrid snakes in Mexico

and Central America using published reports as well as reliable personal com-

munications provided by students and researchers.

BIOCHEMISTRY AND PHARMACOLOGY OFDUVERNOY GLAND SECRETIONS

The Duvernoy’s gland secretions of colubrid snakes from other regions of

the world are known to possess a number of enzymatic activities,[3,4] and many

of them contain procoagulant and hemorrhagic components[3,5] which may

induce coagulopathies and local and systemic bleeding in humans. Severe

envenomations have been reported after bites by species of the genera

Thelothornis, Dispholidus and Rhabdophis in Africa and Asia, associated with

coagulopathies and systemic bleeding.[6 – 10] Recently, the presence of a P-III, 65

kDa hemorrhagic metalloproteinase was described in the venom of Dispholidus

typus. This protein cross-reacts immunologically with jararhagin, a potent

hemorrhagic metalloproteinase isolated from the venom of the South American

pit viper Bothrops jararaca.[11] In addition, hemorrhagic and myotoxic activities

have been described in the venom of the South American colubrid Philodryas

olfersii.[12,13]

In contrast, very little information is available on the biochemistry and

pharmacology of venoms from species distributed in Mexico and Central

America. The venom of Leptodeira annulata has weak phospholipase A2 and

phosphodiesterase and high proteolytic activities.[14] It is weakly toxic to mice,

inducing hemorrhagic activity at relatively high doses.[14] The venoms of

various species of the genera Diadophis, Heterodon, Hypsiglena, Salvadora,

Tantilla, Trimorphodon and Pituophis, whose distribution range includes

different regions of Mexico, were recently studied.[4] Most of these secretions

showed proteolytic activity and some also had phosphodiesterase and

phospholipase A2 activities. In particular, the venom of Trimorphodon

biscutatus, a species also present in Central America, has high phospholipase

A2 activity.[4] Vest[15] described hemorrhagic activity in the Duvernoy gland

secretion of the North American species Thamnophis elegans. This genus is

represented in Middle America, and it is likely that Thamnophis sp in this region

may contain hemorrhagic components as well.

BITES BY COLUBRID SNAKES IN MEXICOAND CENTRAL AMERICA

Several epidemiological surveys in the region suggest that a number

of people are bitten by ‘non-poisonous’ snakes[16] which may be colubrids.

ENVENOMATIONS IN MEXICO AND CENTRAL AMERICA 107

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MARCEL DEKKER, INC. • 270 MADISON AVENUE • NEW YORK, NY 10016

However, since the offending snakes are not usually brought to the health center,

and since a correct identification of the snake is not easily performed, it is likely

that some of these cases correspond to bites by snakes of the subfamily

Crotalinae which did not result in envenomation. Thus, there is not reliable

epidemiological information on the actual incidence of colubrid snake bites in

this region.

The following descriptions summarize the information gathered from

various sources, including those reported in the literature and a series of reliable

personal communications by students and researchers:

(a) Genus Conophis: This genus includes various species, mostly

diurnal, having enlarged grooved teeth.[17] Conophis species are

considered ‘aggressive’ and reported to bite while being handled.[17]

Wellman[17] described a number of bites by this colubrid, including a

field colleague bitten in the forefinger by C. lineatus. Other cases

include those of Marineros,[18] the account of D. Janzen (in[19]), and

the unpublished experiences of Manuel Acevedo (personal com-

munication) in Guatemala and one of us (MS) in Costa Rica.

Moreover, a case originally assumed to be caused by Stenorrhina

freminvillei[20] was probably inflicted by C. lineatus.[21] In most

cases, the first effects were pain at the site of the bite and an almost

immediate edema. Pain remained for several hours and there was

local bleeding in some cases. In the cases reported by Marineros,[18]

no effects were described. In few of these bites, local bleeding

persisted for several hours, suggesting an anticoagulant effect,

although the presence of anticoagulant components in the venom of

C. lineatus has not been conclusively demonstrated.

(b) Genus Coniophanes: This genus comprises ca. eight species of small

to moderate size. A report on a bite in a finger by C. imperialis[22]

was characterized by an itching and burning sensation in the area of

the bite. This was followed after a short period of time by numbness

and swelling of the bitten region, as well as by the development of a

red discoloration. Fingers remained swollen for at least three days.

Another bite to the same person produced a sharp and immediate

pain in the interdigital area, where the bite occurred. Within an hour,

the pain extended in the arm up to the level of the elbow. He

described swelling of the hand, with fluid exudating from the bite

punctures and the presence of a red discoloration of the hand.

Twenty five hours after the bite, the pain had subsided, although

swelling and numbness persisted, with a slight soreness in the bitten

area. No hemorrhagic effect was observed. On the other hand, a

specimen of C. schmidtii from Peten, Guatemala, bit Manuel

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MARCEL DEKKER, INC. • 270 MADISON AVENUE • NEW YORK, NY 10016

Acevedo (personal communication) at the base of the left thumb.

Pain was immediate and persisted for over two hours. A slight

edema was evident at the site of the bite. Oscar Lara (personal

communication) reported on a bite in Guatemala by C. piceivittis in

the right thumb, with the development of only slight pain and

swelling which persisted for various days.

(c) Genus Crisantophis: This genus is closely related to Conophis and

includes the species C. nevermanni. A herpetoculturist, Cristian

Guirola, reported the bite on a finger by a juvenile C. nevermanni

in Guatemala (personal communication). A local hematoma de-

veloped shortly after the bite, together with pain and local edema.

No systemic effects were noticed.

(d) Genus Erythrolamprus: This genus includes coral mimics which are

known to produce a toxic Duvernoy gland secretion effective on

other snakes that constitute their diet. One of us (MS) suffered two

bites by E. bizonus from Costa Rica, both at the level of the index

finger. A slight pain was noticed in one of the bites, followed by

local swelling and bleeding, whereas no noticeable effects occurred

in the other bite. A more severe case was documented by Alejandro

Solorzano (personal communication). During a routine cleaning of a

cage at a serpentarium in Costa Rica, an assistant was bitten by an

adult specimen of E. bizonus. The snake, a male of 480 mm snout-

vent length, bit and started a series of chewing movements in the

right index finger for approximately one minute. Pain started im-

mediately, together with swelling in the bitten finger. Between 8–10

hrs after the bite, pain extended to the arm, intensifying when

movements were performed. By 24 hrs, pain and swelling still

persisted, diminishing at 48 hrs. Ecchymotic lesions developed in the

arm, still observed at 72 hrs, together with slight pain. Ecchymosis

persisted for five days, the time at which pain and swelling had

subsided. Thus, this case was associated with a hemorrhagic reaction

developing beyond the site of the bite.

(e) Genus Pliocercus: A bite inflicted by P. elapoides in Mexico in the

left index finger was reported by Seib.[23] The bite lasted only a few

seconds, but nevertheless it caused pain, swelling, lymphadenitis and

ecchymosis in the hand, with no coagulopathies and no systemic

symptoms. Since local incisions were made, a constriction band was

applied and suction was performed, some of the local effects may

have been due to these interventions. However, the development of

ecchymosis is evidence of the toxic effects of the venom.

(f) Other genera: Manuel Acevedo (personal communication) and one of

us (MS) were bitten by Oxybelis aeneus in a thumb and a middle

ENVENOMATIONS IN MEXICO AND CENTRAL AMERICA 109

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©2002 Marcel Dekker, Inc. All rights reserved. This material may not be used or reproduced in any form without the express written permission of Marcel Dekker, Inc.

MARCEL DEKKER, INC. • 270 MADISON AVENUE • NEW YORK, NY 10016

finger. There was swelling in the hands and a slight pain, which

persisted for two days. In addition, the same persons have suffered

several bites by Dryadophis (=Mastigodryas) melanolomus, a

common species in various localities in Central America. In these

cases, the only symptom was a light pain, whereas edema and

hemorrhage were absent. Species of the genus Thamnophis can also

be considered as potentially able to induce mild envenomations in

Mexico and Central America, since cases of bites by T. sirtalis and T.

elegans have been reported in the United States, being associated

with local edema, ecchymosis, lymphangitis and lymphadenitis.[24,25]

From these well-recorded cases, and on the basis of anatomical and

behavioral characteristics of colubrid snakes, it is concluded that most of these

bites occur in people who handle these snakes frequently, i.e. herpetologists

and people taking care of snakes at museums, animal exhibits and zoos,

although a reduced number of cases may also occur in agricultural workers.

Thus, it is suggested that the groups at risk of suffering colubrid snake bites

differ from those at risk of pit viper (family Viperidae) bites. The latter are

usually agricultural workers who are bitten on the job,[16,26] whereas co-

lubrid bites are associated mainly with people who are taking care of or

studying the snakes. As a consequence, the anatomical region of the bite

also differs between these groups. Most pit viper bites occur in feet (approx-

imately 50%), whereas only 30% take place in hands.[16,27] In contrast, most

colubrid bites referred to above occurred in hands and fingers while mani-

pulating the snakes.

The high incidence of colubrid bites in hands may be also related to

anatomical constraints of the snakes since, due to the size of their mouth and

to the fact that fangs are located in the back of the maxillary bone, it is rather

difficult for most colubrid snakes in this region to bite and inject their venom

in anatomical regions other than hands and fingers. Moreover, an additional

factor differentiates pit viper and colubrid bites. In the former, the snake

delivers the venom in an extremely fast action, rapidly releasing the bitten

region in a typical ‘strike and release’ pattern.[1] In the case of colubrid

snakes, the Duvernoy gland secretion is injected into the prey more slowly and

the snake has to hold during the bite for a period of time in order to promote

an effective injection. Thus, the longer a colubrid snake maintains its bite, the

greater possibility it has to inject its venom and, therefore, to induce patho-

physiological alterations in the victim.

In addition, a behavioral difference between colubrids and pit vipers may

have implications in the incidence of snake bites. Most colubrid species in this

region are active hunters and are moving constantly. When threatened by

humans, most of them quickly escape and do not attempt to bite the person.

110 GUTIERREZ AND SASA

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Some of them may bite only when caught or handled, whereas there are several

forms (Imantodes, Geophis, Sibon, etc.) that never attempt to do so. In contrast,

most pit vipers are ambush hunters of relatively low mobility.[1] When

threatened by humans, they may move or, alternatively, display a series of

defensive behaviors which include biting. These differences may partially

explain the higher incidence of pit viper bites, despite the fact that colubrids

outnumber crotaline snakes in the forests and agricultural fields of Mexico and

Central America.

From the observations presented above it is evident that most cases of

colubrid snake bites are associated only with mild local effects, i.e. swelling,

pain, erythema and, in few cases, ecchymosis, whereas there is a conspicuous

lack of systemic alterations. As pointed out by Ribeiro et al.[28] in a study of

bites by the South American colubrid P. olfersii, it is likely that some local

manisfestations in colubrid bites are due to the mechanical trauma associated

with the bite and not to the action of Duvernoy gland secretion, although other

signs and symptoms are evidently associated with local toxicity exerted by this

secretion. Moreover, the few follow-up observations performed on people

bitten by colubrid snakes in Mexico and Central America clearly demonstrate

an absence of permanent tissue damage and other serious sequelae.

Thus, the available evidence strongly suggests that bites by colubrid snakes

in Mexico and Central America do not result in significant pathophysiological

alterations, being mainly characterized by mild local manifestations. This

fragmentary information agrees with some observations in South America on

bites by the colubrid species P. olfersii,[28] Clelia clelia[29] and Erythrolamprus

bizonus.[30] These bites were associated with mild local effects and there were no

systemic alterations. However, since it is likely that Duvernoy gland secretions of

Mexican and Central American colubrids may contain hemorrhagic metallopro-

teinases and procoagulant enzymes, as has been described in other species and

was evident in some of the cases described, and since the pharmacology of

Duvernoy secretions of these species is poorly known at present, caution should

be exercised when handling these snakes and when dealing with their bites.

Moreover, a word of caution seems appropriate since there is a growing number

of snake exhibits in the region, some of which may in the future import exotic

colubrids from Africa or Asia. It should be kept in mind that species of the genera

Thelothornis, Dispholidus, Boiga and Rhabdophis may inflict severe envenoma-

tions in humans and have to be considered, therefore, as truly venomous snakes.

MANAGEMENT OF COLUBRID BITES

In order to reduce the possibilities of a bite, people handling colubrid

snakes need to be aware that such accidents may take place and that these

ENVENOMATIONS IN MEXICO AND CENTRAL AMERICA 111

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snakes have to be manipulated with care. In addition, when a bite occurs, it is

important to avoid allowing the snake to hold on to the bitten region for a

prolonged time, since in these circumstances there is more probability of

injection of Duvernoy gland secretion. It is important to make a correct

diagnosis of a colubrid snake bite, and to differentiate it clearly from bites

inflicted by crotaline or elapid venomous snakes. Since colubrid bites may

cause pain and mild local swelling, unexperienced health personnel may

interpret these mild local effects as corresponding to a pit viper bite. If the

offending snake is brought to the health facility, differential diagnosis should

be made readily, mainly on the basis of the absence of loreal pits in co-

lubrids. If the snake is not available, clinical parameters must be used.

Despite the fact that colubrid snake bites may be associated with edema and

pain, these effects are usually very mild. Consequently, it should be evident

that the bite did not result in significant envenomation and, therefore,

antivenom should not be administered.

Regarding first aid in colubrid snake bites, the affected person must be

reassured by explaining that such a bite is not going to result in a serious

envenomation. If there are persons capable of correctly identifying a colubrid

snake, i.e. herpetologists, naturalists or other people who can make an

unequivocal identification, it is not necessary to take the person to a health

center. However, if there are doubts about the identification of the offending

snake, it is recommended to transport the person to the nearest hospital or health

facility for observation. In case of doubt, it is recommended that specialized

professional personnel perform the diagnosis. Harmful first aid procedures, such

as incisions, tourniquet application, cryotherapy and suction should be com-

pletely avoided.

Management of colubrid bites must include consideration of the pos-

sibility of secondary infection as a consequence of introduction of bacteria from

the skin or the snake oral cavity through the bite. Careful cleaning and dis-

infection of the bitten region is recommended, together with administration of

tetanus toxoid. The routine use of prophylactic antibiotics is not necessary in

these cases, although the bitten region should be observed for evidence of

infection, i.e. redness and enlarged lymph nodes. In the case of infection, these

signs usually appear after 24 hr and not immediately after the bite. If such

secondary infection develops, antibiotics should be administered. Regarding the

administration of polyvalent (Crotalinae) antivenom in colubrid snake bites, an

experimental study demonstrated that Bothrops antivenoms neutralized hemor-

rhagic activity of the venom of P. olfersii.[12] However, with the exception of

this study, there is no solid clinical and experimental basis in support of the use

of bothropic or polyvalent antivenoms in the treatment of colubrid snake bites in

America. Therefore, antivenom therapy should not be considered in patients

bitten by colubrid snakes in Mexico and Central America. In the eventuality of a

112 GUTIERREZ AND SASA

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MARCEL DEKKER, INC. • 270 MADISON AVENUE • NEW YORK, NY 10016

colubrid bite associated with systemic effects, i.e. coagulopathies and bleeding,

management should be based on the administration of fluids, plasma expanders

and, when necessary, transfusions.

CONCLUSIONS

The study of Duvernoy gland secretions of snakes of the family

Colubridae has received very little attention in Mexico and Central America.

Information on the biochemistry and pharmacology of these secretions is only

preliminary, but the scant data available suggest that these secretions constitute a

rich source on novel compounds with great potential significance. The frag-

mentary information on the epidemiological and clinical aspects of colubrid

snake bites in the region has been reviewed. The picture that emerged is one in

which bites occur mainly in people who frequently handle snakes. The available

information indicates that these bites are not associated with systemic en-

venomation, and that most bitten people develop only mild local effects, such as

swelling, pain and, in few cases, bleeding. Increased study of the generally

neglected subject of colubrid snake venoms in Mexico and Central America will

help to provide a better understanding of the composition of these venoms and

the symptoms produced upon envenomation.

ACKNOWLEDGMENTS

The authors thank Alejandro Solorzano, Manuel Acevedo, Oscar Lara and

Cristian Guirola for communicating their experiences with colubrid snake bites.

Thanks are also due to Vicerrectorıa de Investigacion, Universidad de Costa

Rica, for support.

REFERENCES

1. Greene, H.W. Snakes. The Evolution of Mystery in Nature. University of

California Press: Berkeley, 1997; 351 pp.

2. Meier, J.; Stocker, K.F. Handbook of Clinical Toxicology of Animal

Venoms and Poisons; Meier, J., White, J., Eds.; CRC Press: Boca Raton,

Florida, 1995; 367–412.

3. Weinstein, S.A.; Kardong, K.V. Properties of Duvernoy’s secretions from

opistoglyphous and aglyphous colubrid snakes. Toxicon 1994, 32, 1161–1185.

4. Hill, R.E.; Mackessy, S.P. Characterization of venom (Duvernoy’s

ENVENOMATIONS IN MEXICO AND CENTRAL AMERICA 113

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MARCEL DEKKER, INC. • 270 MADISON AVENUE • NEW YORK, NY 10016

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