Helminth Fauna of the Golden Hamster
Mesocricetus auratus in Brazil
ROBERTO MAGALHÃES PINTO, DS,* LUCINEIDE GONÇALVES, MS, DELIR CORRÊA GOMES, DS,
AND DELY NORONHA, BS
Helminth fauna of conventionally maintained hamsters from institutional animal houses that supply the research community
with laboratory animals and from an openly kept control group, randomly purchased in a pet shop in the State of Rio de Janeiro,
were evaluated and compared. Necropsied animals from institutional suppliers were infected with the oxyurid nematodes Syphacia
criceti and S. mesocriceti and with the cestode Rodentolepis nana; those from the pet shop were infected with S. mesocriceti and R. nana.
These are the first morphometric data that are based on Brazilian samples of these species parasitizing hamsters. Mesocricetus
auratus is a newly recorded host for S. criceti, previously recovered from Oryzomys subflavus and Calomys callosus in Brazil. The
potential of pet and laboratory hamsters in the spreading of helminth infections to humans is also considered.
Because of the role laboratory animals play in the evaluation
of several biological parameters in scientific research and in light
of the program established to control the sanitary conditions of
Brazilian institutional animal houses, we have developed procedures to provide a reliable survey of the helminth fauna occurring
in several animal models. The models we targeted are commonly
maintained but not often evaluated, considering the few data
on the parasites they may harbor. The present approach is related to nematodes and cestodes collected in hamsters from two
institutional animal houses and a pet shop in Rio de Janeiro.
Hamsters are used mainly in assays related to experimental
infections (1, 2), pathology (3-5), host-parasite relationships (6),
immune responses, immunodiagnoses (7), and drug therapies
(8). In addition, pet shop hamsters were investigated as a comparative outside group, because little attention has been given
to the possibility of acquiring parasitic infections from rodents
obtained from commercial sources. Further, the general population probably is unaware of any threat of helminth infection
from pet rodents. Results obtained thus far add new data to the
previous major studies of helminths that parasitize laboratory
animals in Brazil (9, 10). This report is important because parasites may act as variables, usually unsuspected, in experiments.
Materials and Methods
Animals. We obtained 30 adult male specimens of the golden
hamster Mesocricetus auratus (weight, 70 to 170 g) from two different institutional animal houses and a pet shop in Rio de
Janeiro, Brazil. The animals were allocated into groups A, B,
and C (10 animals/group) according to their source. The original source of institutional animals is unknown, but closed
breeding colonies have been maintained in the institutions for
more than 20 years. Pet shop hamsters were considered as an
outside openly kept control group in the comparison of the prevalence of the various helminths and intensity of parasitism. The
suppliers were not identified by name, because of ethical reasons. The microbiological status of the animals was not specified.
Husbandry. Prior to their arrival at the laboratory, the hamsters from the institutional animal houses (weight, 94.5 to 170
g; age, 10 to 52 weeks) were maintained conventionally in groups
of 10 in 40.0 3 33.0 3 16.0-cm plastic cages with stainless-steel
screened covers and daily changed bedding of pine shavings.
Animals received ad libitum Nuvital pellets (ground whole corn,
Laboratorio de Helmintos Parasitos de Vertebrados, Departmento de Helmintologia, Instituto
Oswaldo Cruz, Av. Brasil 4365, 21045-900 Rio de Janeiro RJ, Brasil
*Corresponding author
Volume 40, No. 2 / March 2001
bran wheat, bran soya, leguminous hay, ground corncob, calcite limestone, bicalcium phosphate, premixed amino acids,
vitamins, and minerals; PR 145300104, Ministry of Agriculture,
Colombo, Paraná, Brazil) and filtered water from nursing bottles
adapted to the covers. Bedding and chow were sterilized (heated
for 20 min at 1108C) only for animals in group A. The temperature of the animal room was maintained at 18 to 228C. Housing
was in accord to Brazilian guidelines for the care and use of
laboratory animals (11).
The hamsters from the pet shop (weight, 70 to 90 g; age, 6 to
9 weeks) were kept together in 95.0 3 51.0 3 35-cm cages similar to those used in the animal houses. They received ad libitum
Labina pellets (corn, wheat bran, soya bran, meat flour, raw rice
bran, calcium carbonate, bicalcium phosphate, salt, premixed
amino acids, vitamins, and minerals; Agribands Purina do Brasil
Ltd., Itaguaí, Rio de Janeiro, Brazil) and untreated water from
glass containers on the bottom of the cage. The cages were openly
maintained at room temperature for 3 days after they were delivered to the pet shop by a farm supplier. Husbandry procedures
at the farm were the same as those adopted in the pet shop.
The husbandry practices at the pet shop involved the presence of open food packages next to the animals for sale.
Considering that the maximum mean temperatures in Rio de
Janeiro always exceed 328C in the hottest sectors, where absolute temperatures higher than 408C commonly occur (12), the
doors of the shop, although closed at night, were designed to
provide a large screened window-like to improve ventilation.
Nevertheless, this floor-level entrance permits the free access of
insects, mice, and rats (attracted by the availability of food) into
the shop, thereby improving the maintenance of the parasite
life-cycles in the study animals.
Parasites. Immediately after their arrival at the laboratory,
hamsters were examined for helminths by using a modified anal
swab technique (10) and sacrificed in an ether chamber according to ethical procedures (11). The procedures for processing
of helminths for study and their classification have been reported
elsewhere (9). “En face” slides were prepared by using jelly
mounts (13). Photomicrographs derived from a Axiophot microphotographic system (Zeiss, Jena, Germany) using T400 CN
film (Kodak, Guadalajara, Jalisco, Mexico). NHR stands for New
Host Record. Studied specimens were deposited in the
Helminthological Collection of the Oswaldo Cruz Institute
(CHIOC) either as whole mounts or wet material.
Results
Descriptions refer only to the main morphological data of the
CONTEMPORARY TOPICS © 2001 by the American Association for Laboratory Animal Science
21
Figure 1. Syphacia criceti. (A) Male, whole body, lateral view. Bar, 0.08 mm. (B) Anterior portion of male, lateral view. Bar, 0.02 mm. (C) Head of
female, “en face” view. Bar, 0.01 mm. (D) Eggs “in utero.” Bar, 0.03 mm. (E) Posterior extremity of male, lateral view. Bar, 0.02 mm. (F) Posterior
portion of male, lateral view. Bar, 0.07 mm. Bar of Fig. A, common to Figs. B-F.
specific diagnosis and are based on the helminths recovered
during the present investigation.
Syphacia criceti Quentin, 1969. (Fig. 1, A-F)
(i) Morphometrics based on 10 specimens, five males and five
females. Oxyuroidea, Oxyuridae. Small, somewhat slender
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CONTEMPORARY TOPICS © 2001 by the American Association for Laboratory Animal Science
worms, white when alive. Great sexual dimorphism. Males: body,
1400 to 1600 (mean, 1500) mm long, 90 to 100 (mean, 94) mm
wide, with three mamelons on the ventral surface, of which the
anterior is less prominent than are the two posterior. Esophagus, with bulb, 250 to 260 (mean, 255) mm long. Nerve ring 110
Volume 40, No. 2 / March 2001
Figure 2. Syphacia mesocriceti. (A) Male, whole body, lateral view. Bar, 0.1 mm. (B) Anterior portion of female, lateral view. Bar, 0.03 mm. (C) Eggs
“in utero.” Bar, 0.02 mm. (D) Head of female, “en face” view. Bar, 0.01 mm. (E) Posterior portion of male, lateral view. Bar, 0.2 mm. Bar of Fig. A,
common to Figs. B-E.
to 144 (mean, 130) mm from anterior end and excretory pore
460 to 470 (mean, 465) mm from anterior end. Single spicule,
78 to 80 (mean, 79) mm long. Gubernaculum 30 to 32 (mean,
31) mm long, with a hook-shaped distal process. Three pairs of
Volume 40, No. 2 / March 2001
caudal papillae present. Cloacal aperture 138 to 140 (mean, 139)
mm from posterior end.
Females: body 3400 to 3800 (mean, 3500) mm long, 210 mm
wide. Esophagus, with bulb, 360 to 370 (mean, 366) mm long.
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23
Figure 3. Rodentolepis nana. (A) Scolex with armed rostelum. Bar, 0.02 mm. (B) Mature proglottids. Bar, 0.07 mm. (C) Gravid proglottids. Bar, 0.07
mm. (D) Eggs “in utero.” Bar, 0.02 mm. Bar of Fig. A, common to Figs. B-D.
Nerve ring 160 to 190 (mean, 173) mm from anterior end and
excretory pore 360 to 540 (mean, 462) mm from anterior end.
Vulva 840 mm from anterior extremity. Eggs 111 to 120 (mean,
116) mm long, 43 to 48 (mean, 46) mm wide. Anus 360 to 390
mm from posterior end.
(ii) Taxonomic summary. Host: Mesocricetus auratus
(Waterhouse, 1839)-NHR. Site of infection: small intestine. Distribution: Brazil. Specimens studied: CHIOC no. 34,205a-f (whole
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CONTEMPORARY TOPICS © 2001 by the American Association for Laboratory Animal Science
mounts) and 33,875 (wet material).
Syphacia mesocriceti Quentin, 1971. (Fig. 2, A-E)
(i) Morphometrics based on 10 specimens, five males and five
females. Oxyuroidea, Oxyuridae. Small, thick worms, white when
alive. Cephalic inflations conspicuous. Great sexual dimorphism.
Males: body 1080 to 1500 (mean, 1300) mm long, 80 to 90 (mean,
85) mm wide, with three prominent mamelons on the ventral
surface of posterior portion. Esophagus, with bulb, 190 to 210
Volume 40, No. 2 / March 2001
(mean, 199) mm long. Nerve ring 82 to 90 (mean, 87) mm from
anterior end and excretory pore 280 to 324 (mean, 302) mm
from anterior end. Single spicule 50 to 65 (mean, 58) mm long.
Gubernaculum 29 to 32 (mean, 30) mm long, with a hook-shaped
distal process. Three pairs of caudal papillae. Cloacal aperture
140 mm from posterior end.
Females: body 3200 to 5200 (mean, 4500) mm long, 150 to
180 (mean, 167) mm wide. Esophagus, with bulb, 280 to 385
(mean, 343) mm long. Nerve ring 125 to 140 (mean, 132) mm
from anterior end and excretory pore 490 to 560 (mean, 526)
mm from anterior end. Vulva 700 to 830 (mean, 776) mm from
anterior extremity. Eggs 130 to 140 (mean, 135) mm long, 40 to
50 (mean, 45) mm wide. Anus 360 mm from posterior end.
(ii) Taxonomic summary. Host: Mesocricetus auratus
(Waterhouse, 1839). Site of infection: small intestine. Distribution: cosmopolitan. Specimens studied: CHIOC no. 34,206a-d
(whole mounts)and 33,876 and 33,877 (wet material).
Rodentolepis nana (Siebold, 1852) Spasskii, 1954. [Hymenolepis
nana, Vampirolepis nana] (Fig. 3, A-D).
(i) Morphometrics based on 10 specimens. Cestoda,
Hymenolepididae, Hymenolepidinae.
Long worms, white when alive. Body flattened. Suckers 50 to
53 (mean, 51) mm long, 50 to 58 (mean, 55) mm wide. Rostelum
well developed, with a circle of about 25 Y-shaped hooks, each
14 to 16 (mean, 15) mm long. Proglottids numerous, transversely
elongated: immature forms 260 to 271 (mean, 266) mm long, 50
to 62 (mean, 57) mm; mature forms 490 to 520 (mean, 503) mm
long, 90 to 130 (mean, 108) mm wide; and gravid forms 490 to
540 (mean, 510) mm long, 210 to 230 (mean, 220) mm wide.
Three testes, 40 to 43 (mean, 41) mm long and 40 to 45 (mean,
42) mm wide, arranged in a transverse line, separated into two
groups by female gonads. Cirrus pouch 70 to 82 (mean, 77) mm
long. Gravid uterus extending transversely. Eggs 68 to 70 (mean,
69) mm long, 50 to 65 (mean, 58) mm wide.
(ii) Taxonomic summary. Host: Mesocricetus auratus
(Waterhouse, 1839). Site of infection: small intestine. Distribution: cosmopolitan. Specimens studied: CHIOC no. 34,247
(whole mount) and 33,867 (wet material).
The prevalence of parasitism was 40% in group A animals
(institutional source A), 70% in group B (institutional source
B), and 100% in group C (pet shop). Positive animals from
group A were parasitized only with S. mesocriceti (133 worms);
those from group B presented the nematode S. criceti (62 worms)
and the cestode R. nana (68 worms) in single or associated infections, whereas all animals of group C were infected with S.
mesocriceti (1325 worms), and three animals also presented R.
nana (41 worms) associated with these oxyurids (Table 1).
Oxyurid eggs were rare in the feces of hosts, and the anal swab
devices we used failed to detect the larvae. Therefore, we needed
to euthanize the animals investigated herein.
Discussion
The first full accounts relating to helminth parasitization of
Brazilian laboratory animals and its influence (because of crossreactions due to parasite associations that are either
misinterpreted or overlooked) have been reported (9, 10). The
prevalence of helminth infections in inbred and outbred mice
conventionally maintained in institutional animal houses in Brazil
has been studied (1), and an adaptation of the anal swab technique used to detection oxyurid infections in mice was proposed
in an attempt to avoid euthanizing these hamsters (10). The
present findings address the helminth species parasitizing hamsters and the comparison of the helminth fauna of conventionally
maintained animals with that of hamsters randomly obtained,
openly kept in a pet shop, and regarded as a control group.
The unusual finding of Syphacia criceti in hamsters, originally
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Table 1. Individual distribution of Syphacia criceti (Sc), S. mesocriceti (Sm), and
Rodentolepis nana (Rn) worm burdens in hamsters of the investigated groups
Hamster
Group A
Group B
Group C
1
55 (Sm)
36 (Sc)
384 (Sm)
2
36 (Sm)
01 (Rn)
125 (Sm)
3
0
20 (Sc), 13 (Rn)
96 (Sm)
4
0
06 (Sc), 05 (Rn)
25 (Sm)
5
02 (Sm)
02 (Rn)
32 (Sm)
6
0
0
16 (Sm)
7
40 (Sm)
45 (Rn)
149 (Sm), 32 (Rn)
8
0
0
143 (Sm)
9
0
02 (Rn)
78 (Sm), 05 (Rn)
10
0
0
277 (Sm), 04 (Rn)
described on the basis of nematodes recovered from Oryzomys
subflavus and Calomys callosus in Brazil (14), and its association
with the cestode Rodentolepis nana in animals of group B may be
due to a possible contamination induced by the animal house
staff. These personnel were often in close contact with wild rodents, mainly the murid Akodon cursor, which the care-takers
captured for the evaluation of its role in the spreading of sylvatic
zoonoses and which are maintained on campus. Furthermore,
common house mice and even brown rats have been observed
in the hamster breeding rooms.
Syphacia mesocriceti commonly parasitizes hamsters and was
described on the basis of specimens recovered from this same
host. The present study confirms its taxonomic status.
In light of morphometrics only, S. criceti and S. mesocriceti are
quite similar; nevertheless, males of the former species are more
slender than those of the latter, even under stereoscope microscopy observation. In addition, if “en face” views are evaluated,
the differentiation of these species is achieved promptly by examining the ventral mamelons or esophagus. The generic name
for the cestode R. nana, previously referred to either as Hymenolepis or Vampirolepis, was adopted according to the differentiation
based on the disposition of internal structures (15).
Interestingly, in a survey of helminths from pet or laboratory
hamsters and mice (16), S. obvelata parasitized both hosts and
was associated with R. nana in the hamsters and with R. nana
and Aspiculuris tetraptera in the mice. Another outstanding aspect of our findings is the presence of S. obvelata in all investigated
animals, as this oxyurid seems to be naturally specific to mice (9,
10). A similar specificity is observed for S. mesocriceti and hamsters, except for unexpected outer interferences in the proper
establishment of the infection by this species. Such an interference may have led to the occurrence of a burden of S. criceti
(present investigation), perhaps due to a contamination of the
evaluated colony. Perhaps S. criceti, which was not adapted to
hamsters when the infection was initiated, was able to induce
high immune responses against S. mesocriceti in the hosts such
that this parasite was unable to infect them.
The role of pet rodent animals in the transmission of helminth infections to humans has been emphasized strongly (16).
Human R. nana infections have been reported (16) and appear
to be due to carelessness resulting from misunderstanding of
the necessary prophylactic procedures for properly handling pet
rodents. Nevertheless, cases of human infections by Syphaciinae
nematodes are based only on personal communications, and
there are no available data on these contaminations, which appear to be accidental. However, the generic diagnosis of Syphacia
refers to these nematodes as parasites of rodents and man (17).
Moreover, because of the lack of morphometric data and of
illustration of internal structures (except for eggs) that would
facilitate reliable identification, the so-called Syphacia obvelata
described in hamsters (16) may be, in fact, S. mesocriceti. That
CONTEMPORARY TOPICS © 2001 by the American Association for Laboratory Animal Science
25
parasite was proposed (18) based on 23 nematode specimens
recovered from Mesocricetus auratus and was redescribed 2 years
later in hamsters from Canada (19). Furthermore, S. obvelata is
very similar to S. mesocriceti, and these organisms are distinguished primarily through analysis of cephalic structures by
using “en face” mounts.
Rodent infections due to the cestode R. nana undoubtedly
are transferred to humans and vice versa, for although the cestode eggs are directly infective to both man and rodents, the
parasite, according to its heteroxenous life-cycle, is transmitted
through many intermediate hosts, including fleas and tenebrionids. These intermediate hosts become infected by feeding on
dried fruit, flour, or cereal that have been contaminated with
rodent feces, and small specimens of infected tenebrioids can
pass unnoticed as they invade cereal containers. The transfer of
Syphacia spp. from pet or laboratory animals to humans probably is not rare, even as an accidental infection—the parasites
likely are overlooked often because of their monoxenous life
cycle and lack of alarming symptoms. This point of view is reinforced by the fact that pet shop animals are seldom maintained
under acceptable sanitary conditions and, when purchased from
wholesalers, are not checked (at least in Brazil) for ecto- and
endoparasites prior to their arrival in the pet shops.
The present findings provide reliable data on the helminth
fauna of a very common pet animal. In addition, in light of the
close contact (including caressing and even kissing) of children
with hamsters, our findings serve as a warning regarding the
procedures to be adopted in an attempt to avoid the eventual
rodent-to-man and man-to-rodent transmission of these parasites.
Considering that hamsters and other rodents are pets in many
homes, the likelihood of cross-infections, particularly involving
children and mainly due to unhygienic habits, is high.
Regarding barriers to infection, we concluded that the practices of animal house A, particularly of sterilizing bedding and
chow, were more effective than those of institutional source B.
Even upon the development of increased parasitic burdens of
the Syphaciinae nematodes, which are monoxenous (20), this
practice prevented the installation of the cestode cycle, which is
heteroxenous (21) and has a low potential of transmission.
Acknowledgments
We thank the institutions for supplying the hamsters, Genilton José
Oliveira and Heloisa Maria Nogueira Diniz (Departamento de Ensino,
Instituto Oswaldo Cruz, FIOCRUZ) for technical photographic support,
and Dr. Robin Overstreet (University of Southern Mississippi) for a reprint. We dedicate this paper in honor of the Oswaldo Cruz Institute, on
the occasion of the centenary of its foundation, May 25th 1900.
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