305

Neotrop. Helminthol., 8(2), 2014

2014 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

OCCURRENCE OF GASTROINTESTINAL NEMATODES ASPICULURIS TETRAPTERA

(NITZSCH, 1821) SCHULZ, 1927 AND SYPHACIA OBVELATA RUDOLPHI, 1802 ON MUS

MUSCULUS LINNAEUS, 1758 FROM RESEARCH VIVARIA IN MEXICO

OCURRENCIA DE NEMATODOS GASTROINTESTINALES ASPICULURIS TETRAPTERA

(NITZSCH, 1821) SCHULZ, 1927 Y SYPHACIA OBVELATA RUDOLPHI, 1802 EN MUS

MUSCULUS LINNAEUS, 1758 EN BIOTERIOS DE INVESTIGACION EN MEXICO

1,2

Grano-Maldonado, Mayra I.

Abstract

Keywords: Aspiculuris tetraptera - Mexico - Mus musculus - Syphacia obvelata - vivaria mice.

Suggested citation: Grano-Maldonado, M. 2014. Occurrence of gastrointestinal nematodes Aspiculuris tetraptera (Nitzsch,

1821) Schulz, 1927 and Syphacia obvelata Rudolphi, 1802 on Mus musculus Linnaeus, 1758 from research Vivaria in Mexico.

Neotropical Helminthology, vol. 8, n°2, jul-dec, pp. 305-312.

1,2 1

Grano-Maldonado, Mayra I. Ecophysiology Laboratory, Faculty of Marine Sciences, Autonomous University of Sinaloa, Paseo Claussen s / n. A. P. 610.

Mazatlan, Sinaloa, Mexico Tel/Fax: + 52 669 982 86 56. CCMAR-CIMAR L.A., Centro de Ciencias do Mar, Universidade do Algarve, Faro, Portugal

E-mail: grano_mayra@hotmail.com; mgmaldonado@ualg.pt

Laboratory mice Mus musculus Linnaeus, 1758 are commonly used as important models in

veterinary and biomedical research. Forty laboratory mice were collected in four different vivaria

at the National Autonomous University of Mexico and evaluated for parasites. Examination of

intestinal organs revealed nematode Aspiculuris tetraptera (Nitzsch, 1821) Schulz, 1927 (n=104)

and Syphacia obvelata Rudolphi, 1802 (n=1582). A statistical study was performed to determine

host sex preference of infection. Cestode parasites, Rodentolepis nana (Siebold, 1852)

synonymous (Hymenolepis nana and Vampirolepis nana) including a potential cause of human

cestodiasis, with an emphasis on those pathogens with zoonotic potential. Evident ectoparasites

were not present. A review reporting parasites on rodents employed on vivaria in Mexico was

elaborated from a database at the National Helminths Collection of the Institute of Biology of the

National Autonomous University of Mexico. This is the first report of the occurrence of these

nematodes, A. tetraptera and S. obvelata, on M. musculus used and their known geographical

distribution.

Grano-Maldonado

Helminths in Vivaria mice

306

Resumen

Palabras clave: bioterios - Aspiculuris tetraptera - Mexico - Mus musculus - Syphacia obvelata.

El ratón común Mus musculus Linnaeus, 1758 es empleado comúnmente como modelo de

investigación en las ciencias veterinarias y biomédicas. Cuarenta organismos fueron colectados

en cuatro diferentes bioterios de la Universidad Nacional Autónoma de México y fue evaluada la

presencia de parásitos. La examinación intestinal reveló al nematodo Aspiculuris tetraptera

(Nitzsch, 1821) Schulz, 1927 (n=104) y Syphacia obvelata Rudolphi, 1802 (n=1582). El análisis

estadístico determinó que no hay preferencia parasitaria por sexo del hospedero. Se registró al

cestodo Rodentolepis nana (Siebold, 1852) sinónimos (Hymenolepis nana y Vampirolepis nana)

que son causantes de cestodiasis en el humano. Este trabajo tiene un énfasis en estos helmintos

debido a su potencial zoonótico. No se detectó la presencia de ectoparasitos. Se elaboró un

reporte del registro de parásitos en roedores de bioterio en México obtenido de una base de datos

de la Colección Nacional de Helmintos del Instituto de Biología de la Universidad Nacional

Autónoma de México. Este es un primer registro preliminar de la ocurrencia del nematodo A.

tetraptera y S. obvelata en el ratón común M. musculus en cuatro bioterios en la ciudad de

México. Este trabajo amplía la distribución geográfica y contribuye también, a un nuevo registro

del parásito.

INTRODUCTION prevalence of these pathogens may represent

unwanted variables in research (Vogelweid,

1998; Parker et al., 2009) performed an

extended research report describing the

infectious agents in laboratory mouse at

University level in the same way, revealed the

main infection centre may be wild rodents

around laboratory facilities at the university.

And monitoring these animals for

parasitological infestations is important in order

to exclude infectious agents requiring constant

routine studies.

Several authors (Seward, 2001; Olfert &

Godson, 2000; Roble et al., 2012) underline the

potential for laboratory animal personnel to

serve as mechanical vectors of unwanted

infective agents may increase when these

persons handle infected mice at work or acquire

self infected. The aim of the current study was to

expand knowledge on the presence of helminth

parasite and their taxonomical identification

from laboratory mice kept on vivaria which are

employed for different research studies. Data of

abundance and the prevalence of parasites

commonly found in populations of mice on the

University campus in Mexico City are evaluated

Mice are the most commonly used mammalian

research model with hundreds of strains

(Frasierand & Talka, 2005). They are primarily

employed because they are mammals relatively

easy to maintain and handle, reproduce rapidly,

and share a high degree of homology in humans

(Bronson et al., 1989; CCAC, 1998). Proper

housing and management of animal facilities are

essential to i) provides animal well-being and

maintain good health, ii) obtain quality of

research data minimizing variations that can

affect research results, iii) keep safe the health

and safety of personnel (CCAC, 1998; Seward,

2001; Frasier & Talka, 2005; Pritt & Duffee,

2007). A parasitised animal may alter host

physiology, making the host inappropriate for

many experimental uses.

The most common rodent in house laboratory or

vivaria is the common mice Mus musculus

Linnaeus, 1758. However, many of pathogens

of these laboratory mice may alter host

physiology, making in some cases the mice host

not fitting for many research works. Some

Neotrop. Helminthol., 8(2), 2014

slide for further identification.

The taxonomic keys used were Yamaguti

(1961), CIH key to the parasite nematodes

(Anderson et al., 1974-1983) and Keys to the

cestode parasite of vertebrates (Khalil et al.,

1994). The prevalence was calculated by

dividing the number of infected hosts with a

particular parasite species by the total number of

hosts of one species examined, expressed as a

percentage. The average abundance was

calculated by dividing the total number of

individuals of a particular species of parasite by

total number of hosts of one species examined

(both infected and uninfected) of nematodes was

determined according to the procedures of

Margolis et al., (1982). This study also sets out to

examine the parasitic preference between male

versus female parasitized mice using an x test to

assessment for an association between parasite

infection and mice sex.

The examined specimens of M. musculus ranged

in size from 370 to 510 (429 ± 53.47 mm) total

length (TL). A total of 1686 nematodes were

found in Mus musculus belonging to the

As pi culuris tetrapt er a ( Ox yurida:

Heteroxynematidae) and Syphacia obvelata

(Oxyurida: Oxyuridae) in four vivaria (Table 1).

These nematodes showed certain specificity for

particular host organs and were found in the

intestine only. One nematode A. tetraptera was

found only in the mesentery, whereas the cestoda

Rodentolepis nana (Siebold, 1852) were

exclusive of intestine and cecum (Table 2). With

reference to the mice's parasitism by the host

sex, this study showed that there was no parasitic

preference between the 40 parasitized mice; we

established 20 females and 20 males (c = 0.023,

table 3.84; df = 0.1, alpha = 0.05).

This initial study was undertaken to identify

parasites on four different vivaria on the mice M.

musculus employed to different experimental

and are discussed in the context of possible

infectious disease outbreaks in campus vivaria.

A total of 40 random picked up live mice were

donated from four different vivaria. Live mice

(20 males and 20 females) were transported in

cardboard containers to the laboratory where

they were euthanized using an overdose of

anaesthetic ether solution. All animals were

sacrifice in accordance with an approved

institutional animal care ethical protocol

(CCAC,1998). Mice were measured (mm) and

total length (TL) registered. An evaluation for

ectoparasites was performed under the

stereomicroscope (LEICA MZ 9.5, Wetzlar,

Germany).

For endoparasite examination, an abdominal

dissection was performed using a sterile scalpel

form the mouth thru the anus. The following

major internal organs were collected: heart,

lungs, pancreas, spleen, liver, kidneys, stomach,

and intestine. Each organ was placed in

individual Petri dishes with physiological saline

solution 8.5% for further examination.

Collections of nematodes were elaborated using

small paintbrush placing the specimens on the

saline solution. Fixation was elaborated using

hot Berland liquid (19 glacial acetic acid parts

and 1 formalin part) allowing the full body

extension of the nematodes, after that each

specimen were placed in vial with 70% alcohol

to preserve specimens for further taxonomical

examination. Nematodes were placed in slides

with lactophenol of Amman (According with

Lamothe-Argumedo, 1997) between cover slide

and slide allowing the specimen to be

transparent. Cephalic region and the extreme

caudal of each specimen were cut using a scalp

on a slide using drops of glycerine for better

managing. All samples were evaluated

microscopically using an optical microscope

(LEICA DMLB 10 Wetzlar, Germany) and

camera appliance for drawing taxonomic value

features. Cestodes were collected and the

cephalic region (scolex) were cut and put in a

MATERIAL AND METHODS

RESULTS

DISCUSSION

307

Grano-Maldonado

Helminths in Vivaria mice

Table 1. Prevalence (%) and Abundance of nematode parasites on specimens of Mus musculus (n=40) collected at

four different vivaria in Mexico.

Vivaria/

Faculty

Aspiculuris sp.

(n= 104)

Prevalence Abundance Syphacia sp.

(n= 1582)

Prevalence Abundance

Science

196 60 39.2

Medicine

6.8

930 100 186

Veterinary

11.6 308 100 61.6

Bio medics

2.4

148 100 29.6

Mean 26

5.2

395.5 90 79.1

SD 25.56 30 5.11 362.50 20 72.51

Table 2. Helminths reported in rodents employed in house laboratories (vivaria) in Mexico. *(The National

Helminths Collection of the Institute of Biology of the National Autonomous University of Mexico (CNHE-

IBUNAM)).

Host Parasite Habitat

Geographical

Location Reference

Mus

musculus

TREMATODA

Centrocestus

formosanus

Intestine

Mexico City

Arizmendi-Espinosa (1989);

(1992)

Echinochasmus

zubedakhaname

Intestine

Yucatan Lamothe-Argumedo et al.

(1991); Aguirre-Macedo

(1989)

Posthodiplostonum

minimum

Intestine

Patzcuaro

Perez Ponce de

Leon (1992),

(1995); Aguirre-Macedo

(1989)

Phagicola angrensis

Intestine

Yucatan

Aguirre-Macedo (1989)

NEMATODA

Aspiculuris tetraptera

Intestine

Mexico City

In the present study

Syphacia obvelata

Intestine

Mexico City

In the present study

CESTODA

Taenia taeniaeformis

Liver

Mexico City

Caballero (1938)

(CNHE)*

Vampirolepis nana

Intestine

Mexico City

García-Prieto (1986)

Rattus

norvergicus

TREMATODA

Echinostoma

ochoterenci Intestine Mexico City

(Chapultepec) Zerecero (1943)

Echinostoma

revolutum Intestine Cienega Lerma

(Edo. Mexico) Larios-Rodríguez (1940)

Continues table 2.

308

Neotrop. Helminthol., 8(2), 2014

Fibricola caballeroi

Paragonimus

mexicanus

Lungs

Mexico City

Larios-Rodríguez (1940);

Ramirez (1986)

(experimental)

CESTODA

Taenia taeniaeformis

(cists)

Intestine

Morelia, Mich.

Zerecero (1943)

Vampirolepis nana

Intestine

Mexico City,

Morelia, Mich.

Caballero (1939),

(1942); Hierro-Huerta

(1992)

ACANTHOCEPHALA

Moniliformis

moniliformis

Intestine

Morelia, Mich.

Hierro (1992)-Huerta

NEMATODA

Capillaria sp

Bladder

Morelia, Mich.

Hierro (1992)-Huerta

Heterakis spumosa

Intestine

Mexico city

(Chapultepec)

Caballero (1939)

Morelia, Mich.

Hierro (1992)-Huerta

Gongylonema

neoplasticum

Stomach

Morelia, Mich.

Hierro (1992)-Huerta

Nipposstrongylus

brasilensis

Intestine

Morelia, Mich.

Hierro (1992)-Huerta

Trichuris muris

Intestine

Mexico city

Zerecero (1943)

Rattus rattus

TREMATODA

Paragonimus

mexicanus

Lung

Mexico city

Ramírez (1986)

(experimental)

Schistosoma mansoni

Liver,

spleen

Puerto Rico

No data registered

Rattus sp. NEMATODA

Trichuris muris Intestine Mexico city Osorio (CNHE)

TREMATODA

Clonorchis sinensis - Japan Donation, data no

publish

Paragonimus

miyazakii Lung Japan Donation, data no

publish

Continues table 2

(Baker, 1998). This author provides as extend

research work concerning some pathogens and

their direct effect on valid data research.

Experimental studies are required to evaluate the

outline of infective agents in these mammals.

Like all animals, even mice housed facilities are

subject to infection (Olfert & Godson, 2000;

Roble et al., 2012), as well as mice sold as pets or

feed other animals (Roble et al., 2012).

According with Hoag & Meier (1989) infections

biological, medical, biomedical and veterinary

studies on the University campus.

Helminthological survey results of rodents in

this study showed intestinal parasites present in

laboratory mouse colonies at the University

campus in Mexico City were unknown and none

documented by the Laboratory Animal

Diagnostic employers. Researchers using mice,

rats, and rabbits in biomedical experimentation

should be aware of the profound effects that

many of these agents can have on research

309

Grano-Maldonado

Helminths in Vivaria mice

herpesvirus 3) (Parker et al., 2009). Further

studies concerning virus and bacteria may be

included during surveillance healthy programs

in the university vivaria. Although the

endoparasitic burdens found on this study were

similar than other studies (most notably

nematodes) (Parker et al., 2009). Outbreaks

infections present in laboratory mouse colonies

in vivaria are well documented, despite

improvement in detection these activities should

be remain continuous for research institutions.

However, their infection way is not always

known.

The present study is an initial research which

would assist further studies on the basic biology

of the parasites and vivaria management. The

helminth species reported in this studies were

known to Parasitology discipline previously, but

none had been reported in individual of M.

musculus had been examined for parasites

before this study research vivarium in Mexico

City. This work showed the first approach to

identify the helminth parasite from four different

laboratory mice kept on vivaria which are

employed for different research studies at

University campus in Mexico City.

Hymenolepis sp. can infect humans, and

highlights the importance of a more robust need

for parasite control in the vivaria facilities and

increasing the number of other vivaria facilities

in other universities merit further study. The

employees may proceed to provide

antihelmintic medication regularly in the

context of possible infectious disease outbreaks.

Thanks to Rafael Lamothe-Argumedo and Luis

Garcia-Prieto at the National Helminths

Collection of the Institute of Biology of the

National Autonomous University of Mexico

(CNHE-IBUNAM), for his help in acquiring

specimens for taxonomical identification and

literature. Special thanks to Fernando Garcia-

Vargas for his editorial comments. This paper is

dedicated to the late, Rafael Lamothe-

Argumedo who sadly passed away during the

writing of this manuscript.

with the various helminths rarely produce

clinical signs and are only potentially important

as producing unpredictable variables in animals

used in research. Mouse colonies are often

infected with the oxyurids (pinworms) S.

obvelata and A. tetraptera (Parker et al., 2009;

Roble et al., 2012) and in the latest study, other

nematode parasites morphologically compatible

with Gongylonema spp. were found in the

gastrointestinal tract however was not found in

the present study. Scott and Gibbs (1986)

described the population dynamics of pinworms

S. obvelata and A. tetraptera in mice. In Hidalgo

state, Mexico, Pulido-Flores et al. (2005)

reported these nematodes in wild rodents in,

however, these authors reported that Aspiculuris

sp. was the most intense and abundant. Allymehr

et al. (2012) reported S. obvelata (prevalence

42%), A. tetraptera (prevalence 19%) in house

mice from poultry houses in Iran. In the present

study, S. obvelata was the most abundant

agreeing with Allymehr et al. (2012), these

results may be favoured by the vivaria

conditions. These mouse pinworms have a direct

life cycle and spread through a colony rapidly

because of the large numbers of eggs excreted

and carried by the wind. Some mouse colonies

may be infected with R. nana (the dwarf

tapeworm) (Parker et al., 2009; Roble et al.,

2012). The life cycle of this parasite does not

involve any secondary hosts, with infection

taking place directly from eggs excreted in

faeces. Heavily infected animals are below

norms in weight and may be anaemic. Parker et

al. (2009) conclude that wild rodents living near

vivaria in some way transmit infections to and

between the laboratory colonies and could serve

as a source of infection or infestation in

laboratory mouse colonies, although little is

known about the prevalence of infectious

diseases in wild mouse populations in

Philadelphia in particular. Is well documentated,

the wild mouse (M. domesticus) populations in

Australia revealed a high prevalence of minute

virus of mice (MVM), epizootic diarrhea of

infant mice (EDIM), and Theiler mouse

encephalomyelitis virus (TMEV), murine

cytomegalovirus (MCMV), as well as

significant seroprevalence of mouse adenovirus

(MAV), parvovirus, and thymic virus (murid

ACKNOWLEDGMENTS

310

Neotrop. Helminthol., 8(2), 2014

Aguirre-Macedo, M. 1 9 8 9 .

Allymehr, M, Tavassoli, M, Manoochehri, M, &

Ardavan, D. 2012.

Anderson, R, Chabaud, A, & Willmott, S. 1974-

1983.

Arizmendi-Espinosa, M.A. 1989.

Arizmendi-Espinosa, M. A. 1992.

Baker,D.1998.

Bronson, F, Dagg, H, Charles, P & Snell G.

1989.

Caballero, E. 1939.

S o m e

metacercarias parasitizing Cichlasoma

urophthalmus in different localities in the

southeaster of México. BSc Thesis,

Universidad Nacional Autónoma de

México. México, D.F.

Ectoparasites and

gastrointestinal helminths of house mice

(Mus musculus) from poultry houses in

Nor thw e st I r an. C omp arat ive

Parasitology, vol. 79, pp. 283-287.

CIH keys to the nematode parasites

of vertebrates. Commonwealth

Agricultural Bureaux, Farnham Royal,

Bucks: England, vol. pp. 1-10.

Contribution

of the life cycle of Centrocestus

formosanus Nishigori, 1924 in the carp

Mylopharyngodon piceus in Tezontepec

de Aldama, Hidalgo, México. BSc Thesis,

Universidad Nacional Autónoma de

México. México, D.F. Descripción

de algunas etapas larvarias y de la fase

adulta de Centrocestus formosanus de

Tezontepec de Aldama, Hidalgo. Anales

del Instituto de Biología, Universidad

Nacional Autónoma de México, Série

Zoología, vol. 63, pp. 1-11.

Natural pathogens of laboratory

mice, rats, and rabbits and their effects on

research. Clinical Microbiology Review,

vol. 11, pp. 231–266.

Reproduction. In E L Green, (eds.)

Biology of the Laboratory Mouse. Maine,

USA. Consultado el 10 Marzo de

2014,<http://www.informatics.jax.org>

Algunos endoparásitos de

Rattus rattus norvegicus y de Rattus

norvegicus albinus, del Laboratorio de

Investigaciones Médicas del Hospital

General de la Ciudad de México. Anales

del Instituto de Biología, Universidad

Nacional Autónoma de México, Série

Zoología, vol. 10, pp. 285-291.

BIBLIOGRAPHIC REFERENCES CCAC. 1998.

Frasier, D, & Talka, J. 2005.

García-Prieto, L. 1986.

Hierro-Huerta, P. 1992.

Hoag, W, & Meier, H. 1989.

Khalil, L, Jones, A, & Bray R. 1994.

Lamothe-Argumedo, R, & Aguirre-Macedo,

M L . 1 9 9 1 .

LamotheArgumedo, R. 1997.

Larios-Rodríguez, I. 1940.

Margolis, L, Esch, G, Holmes, J, Kuris, A, &

Schad, G. 1982.

Guidelines on choosing an

appropriate endpoint in experiments

using animals for research, teaching and

testing. Consultado el 5 de mayo de 2014

<http://Ottawa.w.ccac.ca/en/CCAC_Pro

grams/Guidelines_Policies/gdlines/endpt

s/appopen.htm> Facility design

considerations for select agent animal

research. Institute for Laboratory Animal

Research Journal, vol. 46, pp. 23-33.

Taxonomic study of

some cestode in vertebrates in Mexico.

BSc Thesis, Universidad Nacional

Autónoma de México. México, D.F.

Helmintofauna of the rat

Rattus norvegicus Erxleben, 1777, in

Morelia, Michoacán, México. B S c

Thesis, Escuela de Biología, UMSNH.

Morelia, Michoacán, Mexico. Infectious

Diseases. In EL Green, (eds.) Biology of

the Laboratory Mouse. Maine, USA.

Consultado el 10 de Marzo de 2014

<http://www.informatics.jax.org/greenbo

ok/frames/frame11.shtml> Keys to the

cestode parasites of vertebrates. 3

edition. CAB International. Wallingford,

Oxon.

M e t a c e r c a r i a o f

Echinochasmus zubedakhaname parásite

of Cichlasoma urophthalmus in Celestún,

Yucatán, México. Anales del Instituto de

Biología, Universidad Nacional

Autónoma de México, Série Zoología,

vol. 62, pp. 139-149. Manual de

técnicas para preparar y estudiar los

parásitos de animales silvestres. 3

edition AGT Editor, México.

Echinostoma

revolutum (Froelich, 1802) (Trematoda:

Echinostomatidae) studied for the first

time in México parasitizing humans. BSc

Thesis, Universidad Nacional Autónoma

de México. México, D.F.

The use of ecological

311

Grano-Maldonado

Helminths in Vivaria mice

terms in parasitology (report of an ad hoc

committee of the American Society of

P a r a s i t o l o g i s t s ) . J o u r n a l o f

Parasitolology, vol. 68, pp. 131-133.

Humane

endpoints for infectious disease animal

models. Institute for Laboratory Animal

Research Journal, vol. 41, pp. 99-104.

Infectious diseases in wild mice

(Mus musculus) collected on and around

the University of Pennsylvania

(Philadelphia) Campus. Comparative

Medicine, vol. 59, pp. 424–430.

Systematic of

Posthodiplostomum Dubois, 1936 and

some aspects on Postodiplostomiasis in el

Lago de Pátzcuaro, Michoacán, México.

PhD thesis. México, D.F. Universidad

Nacional Autónoma de México.

A host-induced

morphological variability in adult

Posthodiplostomum minimum (Digenea:

Neodiplostomidae). Journal of

Parasitology, vol. 2, pp. 818-820.

Training strategies

for animal care technicians and

veterinary technical staff. Institute for

Laboratory Animal Research Journal, vol.

48, pp.109-119.

Helminths of rodents (Rodentia:

Muridae) from Metztitlán, San Cristóbal,

and Rancho Santa Elena, Hidalgo,

Mexico.

Olfert, E, & Godson, D. 2000.

Parker, S, Malone, S, Bunte, R, & Smith, A.

2009.

Pérez-Ponce De León, G. 1992.

Pérez-Ponce De León, G. 1995.

Pritt, S, & Duffee, N. 2007.

Pulido-Flores, G, Moreno-Flores, S & Monks S.

2005.

Ramírez-López, S. 1986. Migration route of the

metacercaria of Paragonimus mexicanus

Miyazaki e Ishii, 1968, in Rattus

norvegicus. BSc Thesis, Universidad

Nacional Autónoma de México. México,

D.F.

Roble, G, Gillespie, V, & Lipman, N. 2012.

Scott, M. & Gibbs, H. 1986.

Seward, J. 2001.

Vogelweid, C. 1998.

Yamaguti, S. 1961.

Zerecero, C. 1943a.

Zerecero, C. 1943.

Infectious disease survey of Mus

musculus from pet stores in New York

City. Journal of the American Association

for Laboratory Animal Science, vol. 51,

pp. 37–41. Long-term

population dynamics of pinworms

(Syphacia obvelata and Aspiculuris

tetraptera) in mice. The Journal of

Parasitology, vol. 72, pp.652–662.

Medical surveillance of allergy

in laboratory animal handlers. Institute

for Laboratory Animal Research Journal,

vol.42, pp.47-54. Developing emergency

management plans for university

laboratory animal programs and

facilities. Contemporary Topics in

Laboratory Animal Science, vol. 37, pp.

52-56. Systema Helminthum. III.

Nematodes. Interscience Publishers Inc,

New York, USA.

Algunos tremátodos de las

ratas domésticas de la Ciudad de

México. Anales del Instituto de Biología,

Universidad Nacional Autónoma de

México, Série Zoología, vol. 14, pp. 507-

526. Some helminths of

domestic and wild rats in México,

describing two new species. MSc Thesis.

Universidad Nacional Autónoma de

México. México, D.F.

Received June 20, 2014.

Accepted September 22, 2014.

312