Integrative Zoology 2008; 3: 21-26 doi: 10.1111/j.1749-4877.2008.00071.

ORIGINAL ARTICLE

Rodents as reservoirs of parasites in India

Lachhman D. SINGLA,1 Neena SINGLA,3 Vir R. PARSHAD,3 Prayag D. JUYAL1 and Naresh K.
SOOD2
Departments of 1Veterinary Parasitology and 2Veterinary Pathology, Guru Angad Dev Veterinary and Animal
Sciences University, Ludhiana, India and 3Department of Zoology, Punjab Agricultural University, Ludhiana,
India

Abstract
We monitored the prevalence of endoparasitic infections of rodents in Punjab State, India, between January 2004
and December 2005. Three species of wild rodents, namely the house rat, Rattus rattus (n = 42), the lesser
bandicoot rat, Bandicota bengalensis (n = 34) and the Indian gerbil, Tatera indica (n = 15), were live-captured from
houses and crop fields. Examination of various organs revealed that the highest rates of endoparasitic infection
occurred in R. rattus (40.5%), followed by B. bengalensis (35.3 %) and then T. indica (20.0%), with an overall
infection rate of 35.2%. All three rodent species were found naturally infected with one or more species of
helminths. Metacestodes (1–6) of Cysticercus fasciolaris (larvae of Taenia taeniaeformis) were found in all three
rodent species (in the liver). In one male T. indica, numerous robust T. taeniaeformis metacestodes were found in
oval sacs attached to the mesentery and the abdominal wall, an unusual site. The cauda epididymal fluid of the
same gerbil was also found to be infected with a very rare species of strongylid nematode, which could not be
identified to genus or species level. It is possible that this nematode is transmitted sexually and thus may affect the
reproductive potential of gerbils. This appears to be the first report of this phenomenon. In one B. bengalensis
individual, the intestine was found to be obstructed with an acanthocephalan, Moniliformis moniliformis, with
concurrent infection with C. fasciolaris in the form of multiple cysts in the liver. Although no natural protozoan
infection was found in these field rodents, experimental Trypanosoma evansi infection has been established in all
three species with high pathogenicity, and the possibility of sexual transmission was supported by the presence of T.
evansi in the cauda epididymal fluid of male rats.
Key words: helminth, India, parasite, reservoir, rodent.

INTRODUCTION 1999). Their predatory and depredatory habits have a

Rodents constitute the largest and most successful
group of mammals worldwide. They have a high rate of
reproduction, are cosmopolitan in distribution and have
the ability to adapt to a wide variety of habitats (Parshad
Correspondence: Lachhman Das Singla, Department of Veterinary
Parasitology, College of Veterinary Science, Guru Angad Dev
Veterinary and Animal Sciences University, Ludhiana 141004,
India. Email: ldsingla@rediffmail.com
pronounced impact on human economies, and, poten-
tially more seriously, they are major vectors of human
and domestic animal diseases worldwide (Anantaraman
1966; Huq et al. 1985). There are more than 20 diseases
that are known to be directly transmitted by rodents to
humans, usually through the agency of blood-sucking
parasites such as fleas, ticks and mites (Khatoon et al.
2004). Wild rodents act as definitive and/or intermediate
hosts of many endoparasites, several species of which are
common to domestic animals, humans and rodents. Some
naturally occurring rodent parasites are epidemiologi-

© 2008 GADVASU, PAU 21

L. D. Singla et al.

cally important and prevalent parasites of humans and
domestic animals. The eggs of parasites are passed out in
rodent droppings in fields, grain stores and amongst
foodstuffs in houses, and are responsible for disease
spread (Khatoon et al. 2004). The close association that
rodents have with humans and their livestock on one
hand and their exposure to blood-sucking arthropods,
beetles, cockroaches and other invertebrates on the other,
enlarges the scope for transmission of parasites. The
parasitic infections that rodents harbor and convey to
human or animal populations have not been as thor-
oughly investigated as the microbial infections, espe-
cially in India. The objective of the present study was to
monitor the prevalence of endoparasites of rodents from
Punjab State, India, with special reference to the cestode,
nematode, trematode, acanthocephalan and protozoan
parasites found in different wild rodent species.
MATERIALS AND METHODS
A total of 91 individuals of three species of wild ro-
dents (the house rat, Rattus rattus, Linnaeus, n = 42; the
lesser bandicoot rat, Bandicota bengalensis, Gray and
Hardwicke, n = 34; and the Indian gerbil, Tatera indica,
Hardwicke, n = 15) were live-captured from houses and
crop fields using single- and multi-catch traps between
January 2004 and December 2005. Trapping in the
houses was carried out by placing traps along the walls
and on rodent runways. Trapping in the crop fields was
carried out by placing traps near rodent burrows and
other activity sites. A mixture of cracked wheat, pow-
dered sugar and ground nut oil (96:2:2) was used as
in the single-catch traps. After capture, all the animals
were brought to the laboratory on the same day. They
were kept individually in laboratory cages for 10–15 days
and were provided with food and water ad libitum prior
to initiation of the experiment.
In the laboratory, all animals were anaesthetized with
diethyl ether and dissected. The viscera were exposed via
a midventral incision and inspected macroscopically. The
liver, small and large intestine, and reproductive tract
were examined for the presence of parasites. Livers with
Cysticercus fasciolaris parasitic larval cysts were col-
lected in normal physiological saline, then the numbers
and dimensions of the cysts were recorded. Representa-
tive liver samples with cysts in situ were fixed in 10%
formol saline and processed for histopathological
examination. Paraffin-embedded sections were cut at 4–5
μm and stained with hematoxylin and eosin. To study the
morphology of larvae for identification purposes, the
cysts were opened via a small slit to release the parasites.
The length of the larvae was also measured. These larvae
and other parasites found in the intestine and reproduc-
tive tract were preserved in 10% formol saline for later
identification after staining with borax carmine (cestodes
and acanthocephalans) and clearing in lactophenol
(nematodes). To collect parasites from the intestine, the
intestinal contents were transferred to several large Petri
dishes containing saline solution. The contents were
examined both with the naked eye and under a dissecting
microscope. Blood and fecal examinations were carried
out to check for any protozoan infections.

Table 1 Prevalence of parasites in different rodent species

Total No. Percentage Animals Percentage of Percentage of total
Species Parasites found
examined infected infected infected infected individuals individuals
T. taeniaeformis 14 82.4 33.3
Rattus rattus 42 17 40.5 H. diminuta 2 11.8 4.8
Trichuris spp. 1 5.88 2.38
T. taeniaeformis 11 91.7 32.4
Bandicota
34 12 35.3 M. moniliformes 2 16.7 5.9
bengalensis
Mixed infection† 1 8.3 2.9
T. taeniaeformis 3 100.0 20.0
Tatera indica 15 3 20.0 Strongylid 1 33.3 6.7
Mixed infection‡ 1 33.3 6.7
Total 91 32 35.2
†
Mixed infection with T. taeniaeformis and M. moniliformes; ‡Mixed infection with T. taeniaeformis and a strongylid.
bait in the multi-catch traps, and bread pieces were used

22 © 2008 GADVASU, PAU


RESULTS AND DISCUSSION
All three rodent species were found to be naturally
infected with one or more species of helminths. Out of
the 42 R. rattus, 34 B. bengalensis and 15 T. indica
individuals examined, the rate of infection was highest in
R. rattus (40.5%), followed by B. bengalensis (35.3%),
then T. indica (20.0%), with an overall infection rate of
35.2% (Table 1).
Metacestodes of Cysticercus fasciolaris (larvae of
Taenia taeniaeformis) in the form of whitish raised single
to multiple (1–6) parasitic cysts in the liver were recorded
in all three rodent species studied, with highest preva-
lence of 33.3% in R. rattus, followed by 32.4% and
20.0% in B. bengalensis and T. indica, respectively.
Anantharaman (1966), however, reported a higher
prevalence of this parasite in bandicoots than in rats. The
sizes of the cysts varied from 4 to 12 mm in diameter.
Each cyst contained a single, live, characteristic stro-
bilocercus larva. The larvae measured 12 to 20 cm in
length. The armed invaginated rostellum of the larvae
had a double row of hooks. Histopathologically, the
larvae of C. fasciolaris were encapsulated by a thick
fibrous tissue capsule (Fig. 1). Fatty degeneration and
atrophy was evident in the hepatocytes surrounding the
cysts. There was marked infiltration of lymphocytes and
in places there was congestion and dilation of sinusoids.
Despite heavy infection with these parasites, all rats
appeared healthy and agile, suggesting a well-established
host–parasite relationship. The cats in the areas from
where these rodents were captured were found to have
Figure 1 Section of Bandicota bengalensis liver showing fibrous
tissue encapsulation (FTE) and fatty change (FC) around a
Cysticercus fasciolaris larva (L).
© 2008 GADVASU, PAU
Rodents as reservoirs of parasites
eggs of T. taeniaeformis in their feces. Taenia taeniae-
formis adults were also identified in the intestine of a
dead kitten. The high infection rate of this parasite in rats
may be due to the presence of cats in the area.
Contamination of feed with the feces of stray cats may be
the major source of infection. Cysticercus fasciolaris, the
larval stage of T. taeniaeformis, is a common parasite of
rodents in India (Soulsby 1982): its occurrence in
laboratory and wild rodent species has been reported by
many workers (Nama & Parihar 1976; Tyagi & Mishra
1978; Somvanshi et al. 1994; Jithendran & Somvanshi
1999; Bhelonde & Ghosh 2002; Sivakumar et al. 2003;
Singla et al. 2003a). Rodents act as its intermediate host,
whereas cats act as definitive hosts, which pass embryo-
nated eggs in their feces. When ingested by a suitable
rodent, embryonated eggs hatch in the small intestine,
and the embryos pass to the liver, where they develop
into infective larvae in about 30 days. Transmission to the
definitive host is via the ingestion of infective rodent liver.
The occurrence of larvae of T. taeniaeformis in R. rattus
and T. indica has also been reported in countries other
than India (Namue & Wongsawad 1997; Mafiana et al.
1997; Sadjjadi & Massoud 1999).
Hymenolepis diminuta infection was found only in R.
rattus (4.8%). Although H. diminuta is a zoonotic patho-
gen, its public health importance rarely considered, as
few human infections occur. The occurrence of H. di-
minuta only in R. rattus in the present study justifies the
assumption that in storehouses and grocery shops where
R. rattus is found, rat–beetle contact is relatively high,
which leads to the transmission of this parasite
(Anantaraman 1966). Infection with H. diminuta has also
been reported from Rattus spp. caught in Kuala Lumpur
(Leong et al. 1979), Nigeria (Mafiana et al. 1997), Iran
(Sadjjadi & Massoud 1999) and the Philippines (Claveria
et al. 2005).
During the present study, Trichuris sp. eggs were
found in the feces of one R. rattus individual. The aver-
age size of the eggs was 66 µm × 35 µm, closely resem-
bling those of T. muris.
The prevalence of mixed infection with different
species of cestodes, nematodes and acanthocephalan
worms varied according to the rodent species (Table 1).
In one male T. indica, robust metacestodes (12–15 cm in
length) of T. taeniaeformis were found encapsulated in
four oval sacs (2–3 cm in diameter) attached to the
mesentery and abdominal wall (Fig. 2), which is an un-
usual site. There were 20–27 parasites per sac rather than
the single strobilocercus that is found in liver infections.
The total volume of the oval sacs was equivalent to the
23
L. D. Singla et al.
Figure 2 Irregular oval sacs (left side of demarcating line)
containing numerous robust metacestodes of Taenia taeniaeformis
found attached to the mesentery and abdominal wall. Note that the
total volume of oval sacs was equivalent to the total volume of the
abdominal organs (on the right side of the demarcating line). The
metacestodes recovered were 12–15 cm in length.
total volume of the abdominal organs. The cauda
epididymal fluid of the same gerbil contained appro-
ximately 90 parasites (0.7–0.8 mm; average 0.71 ± 0.04
mm) of a very rare species of strongylid nematode that
could not be identified to genus or species level (Fig. 3).
The epididymal fluid of this gerbil had a very low
spermatozoa count (0.4 million mL–1) as compared with
normal animals of the same species (486 million mL–1;
Singla & Parshad 2000). The possibility that this species
is sexually transmitted, and has an effect on the repro-
ductive potential of rodents cannot be ruled out. Based on
our search of the literature, this seems to be the first re-
port of its kind for T. indica. However, another tricho-
strongylid nematode, Hepatojarakus bandicoti, has been
24
Figure 3 Cauda epididymal fluid from an Indian gerbil (Tatera
indica), containing strongylid nematodes.
previously found in the bile passages of the liver in T.
indica from Punjab State, India (Sood & Parshad, 1973).
Similarly, a strongylid nematode has been found in the
epididymides of wood mice, Apodemus sylvaticus, in the
UK (Clarke et al. 2004) and Italy (Casiraghi & Ferraguti
2005), indicating that sexual transmission is likely. These
researchers placed this parasite within the bursate nema-
todes (order Strongyloida) through 18S rDNA analysis,
and suggested that it was an undetermined metastrongy-
loid nematode. The possibility that this parasite is
transmitted sexually opens up an intriguing field of re-
search because sexually transmitted metazoan parasites
are known to occur only in invertebrates.
Trematode infections are very rare among rodents
(Anantharaman 1966). Only two species have been re-
ported from rats (Yamagutti 1958; Niphadkar & Rao
Figure 4 The acanthocephalan parasite Moniliformes moniliformis
emerging from the ruptured intestine of Bandicota bengalensis,
with concurrent infection with Cysticercus fasciolaris in the form
of multiple cysts in the liver.
© 2008 GADVASU, PAU
 Rodents as reservoirs of parasites

1966). In the present study, no trematode infection was

found.
In the present study, the intestines of two of the B.
bengalensis individuals were found to be obstructed with
a number of worms of an acanthocephalan, Moniliformis
moniliformis (5.9%), with concurrent infection with T.
taeniaeformis larvae in the form of multiple cysts in the
liver of one bandicoot (Fig. 4). The M. moniliformis
worms were up to 32 cm in length and appeared to have
pseudosegmented bodies. These worms were seen out of
the intestine probably due to rupture and were initially
misdiagnosed as tapeworms.
Rodents are poor hosts of acanthocephalans, given that
Figure 5 Rats drinking milk from inside a large pot kept at
parasites of only a few genera have so far been reported.
Desnokh Temple in Bikaner, Rajasthan, India.
Species of the genus Moniliformis are the most common.
Moniliformis moniliformis is a cosmopolitan parasite of
rats recorded in India (Bhalerao 1935). Its natural infec-
tion in R. rattus is frequently observed in Madras enhance the chances of parasitic infections spreading
(Anantharaman 1966). Sita (1949) traced its develop- from rodents to humans.
ment through cockroaches and suggested that rodents The information presented here improves our under-
infesting sewers, granaries and storehouses were more standing of the major parasitic infections that rodents
susceptible to infection than field rodents, as darkness harbor and can transmit to human and animal populations
and moisture favored cockroach populations. Crushed in India. Further research is needed to determine the role
insects from grocery shops were found to contain live of different helminth species in regulating rodent po-
infective larvae, which would scatter infection around pulation dynamics and their effect on the reproduction of
(Anantharaman 1966), and contamination of grains and different rodent species. Studies should be conducted to
cereals with these could result in human infection. In the determine the infection rates of these parasites in humans
present study, however, no infection of M. moniliformis and livestock populations. Rodent control efforts to
was reported from R. rattus. minimize human and domestic animal exposure to rodent
In the R. rattus population in the present study, all rats
infestations, combined with surveillance and monitoring
infected with helminths were infected with a single spe- in local problem areas, can help prevent rodent-borne
cies, whereas 2.9% of B. bengalensis and 6.7% of T.
diseases (Taylor et al. 2007) becoming more widespread.
indica were found to be infected with two helminth spe-
cies. Infection with more than two helminth species, as
reported in Funanmbulus pennanti in Jodhpur, India ACKNOWLEDGMENTS
(Parihar & Nama 1978), was not detected in the present The authors are grateful to the Indian Council of Agri-
studies. cultural Research, New Delhi, for providing financial
Although no natural protozoan infection was reported assistance and to the Professor and Head of the Depart-
from field rodents in the present study, experimental ment of Zoology, Punjab Agricultural University, Ludhi-
Trypanosoma evansi infection has been established in R. ana and the Professor and Head of the Department of
rattus and B. bengalensis with high pathogenicity, and Veterinary Parasitology, Guru Angad Dev Veterinary and
the possibility of sexual transmission is supported by the Animal Sciences University, Ludhiana, Punjab, India for
presence of T. evansi in the cauda epididymal fluid of the facilities provided.
male rats (Singla et al. 2003b).
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© 2008 GADVASU, PAU 25

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