Occurrence of Listeria species in different captive wild animals of Nandankanan Zoo, Baranga, Odisha, India
Laxmi Narayan Sarangi1 & Hemanta Kumar Panda 2
1,2 Department of Bacteriology
and Virology, College of Veterinary Science and Animal Husbandry, Odisha University of Agriculture and Technology,
Bhubaneswar, Odisha 751003, India
1 laxmisarangi@gmail.com (corresponding author), 2 drpanda.hk@gmail.com
doi:http://dx.doi.org/10.11609/JoTT.o3175.122 | ZooBank: urn:lsid:zoobank.org:pub:A028441D-1331-4166-9B50-905712F50184
Editor: Ulrike Streicher,
Fauna & Flora International, Hanoi, Vietnam. Date
of publication: 26 January 2013 (online & print)
Manuscript details: Ms #
o3175 | Received 22 April 2012| Final received 11 December 2012 | Finally
accepted 29 December 2012
Citation: Sarangi, L.N. & H.K. Panda (2013). Occurrence
of Listeria species in different captive wild animals of Nandankanan Zoo, Baranga, Odisha, India. Journal of Threatened Taxa5(1): 3542–3547; doi:10.11609/JoTT.o3175.122
Copyright: © Sarangi & Panda 2013. Creative
Commons Attribution 3.0 Unported License. JoTT allows unrestricted use of this article in any medium,
reproduction and distribution by providing adequate credit to the authors and
the source of publication.
Funding: The
facilities was provided by OUAT, Bhubaneswar at department of Microbiology, C.V.Sc. & A.H., OUAT. No
external funding was availed for this work.
Competing Interest: Authors
declare that they have no competing interest.
Acknowledgements: The authors are thankful to Chief
Wildlife Warden, Odisha, Director, Nandankanan Zoological park, Barangafor necessary permission to carry out the research work, Dean, Odisha Veterinary College, for providing necessary
facilities, Senior Veterinary Officer, Veterinary Assistant Surgeon and staffs
of Nandankanan Veterinary Hospital and zoo keepers
for their kind help and cooperation during sample collection and also to Dr. Lala A.K. Singh, Senior Research Officer at Government of
Orissa, Dr. S.V.S. Malik, Principal Scientist, Division of VPH, I.V.R.I., Izatnagar and Dr. A. Dalai, Former Director, Department of
Biotechnology, Ravenshaw University for their
valuable suggestions and kind help during the course of the study.
Abstract: Listeria species were isolated from faecal samples collected from different captive wild
animals of Nandankanan Zoo, Baranga,Odisha, using selective enrichment medium. The isolates were characterized based on
their cell morphology, biochemical and sugar fermentation characteristics as
well as culture morphology. Further, in vitro and in vivo pathogenicity tests were carried out to
assess the pathogenic potential of the isolates. Listeria were found in 24 (23.07%) of the
total 104 faecal samples. Listeria were isolated from the
samples of tiger, bear, hyena, leopard, zebra, elephant, jackal, lion, barking
deer, porcupine, chital, monkey and wild boar. Out of the 24 Listeria isolates
11 were confirmed as L. monocytogenes. The other 13 isolates included L. innocua, L. seeligeri, L. welshimeri and L. ivanovii. The pathogenicity study revealed
that only four isolates were pathogenic. Three of these were L. monocytogenes isolated
from tiger, hyena and elephant and one was L. ivanovii isolated from leopard. Antibiotic sensitivity of the 24 isolates was high towards
ciprofloxacin, levofloxacin, amoxicillin, azithromycin and enrofloxacin. The isolates showed resistance towards oxytetracyclin, gentamicin, cephadroxil,
penicillin- G and nalidixic acid.
Keywords: Captive wild animals, Listeria,L. monocytogenes, L. ivanovii, Nandankanan Zoo, Prevalence.
Listeriosis is an important emerging zoonotic disease caused by pathogenic
strains of Listeria species particularly L. monocytogenesand L. ivanovii. The disease is distributed worldwide and
has been reported in countries of six continents. The significance of the pathogen lies in
its ubiquitous nature (Low & Donachie 1997) and
wide host range, which includes 40 mammals, 20 birds, crustaceans, ticks and
fishes (Sonnenworth 1980). The organism is commonly found in water,
soil, vegetative materials and faecal samples of
animals (Sheehan et al. 1994). The
pathogenic potential of Listeria is well known as it causes abortion,
mastitis, infertility, encephalitis and septicaemiain animals, but its spectrum of diseases is much broader and ranges from
asymptomatic infection and silent carriage to cutaneous lesions or infections
like conjunctivitis, urethritis, endocarditis, pneumonia, pericarditis and
disturbance in gait, followed by death (Malik et al. 2010).
The
number of animals in the wild is decreasing rapidly and many of the animals
living in zoos represent endangered species. Proper care and management of such
animals must be of prime importance. There is a high risk of infection to the captive animals in zoos as
large numbers of animals are kept in a restricted area (Bowens et al.
2003). Listeria spp.have the ability to survive for a long period in the soil and are also possibly
excreted in the faeces of asymptomatic carrier
animals and pose a great risk of infection to other animals, zoo keepers and
also to the visitors. This study
was undertaken to determine the occurrence of Listeria species in faecal samples of wild animal species in the Nandankanan Zoo, Baranga, Odisha, India.
Materials and Methods
Test strains: The standard strains of Listeria monocytogenes (MTCC 1143), Listeria ivanovii (MTCC 7056), Staphylococcus aureus (MTCC 1144) and Rhodococcus equi (MTCC 1135) were obtained from the Microbial
Type Culture Collection and Gene Bank (MTCC), Institute of Microbial Technology
(IMTECH), Chandigarh, India. The
strains were tested for their purity as well as for their morphological and
biochemical characteristics. The L.monocytogenes strain was also tested for its
pathogenicity in vitro and in vivo. All the strains were maintained by sub culturing them in Brain Heart
Infusion (BHI) at 15 days interval.
Collection of samples: One hundred and four faecal samples were either collected from an individual
animal, if it was kept in a separate enclosure (noted as individual samples) or
from several animals if they were housed together in one enclosure (noted as
pooled samples). All the samples
were collected in the morning hours non invasively (Table 1).
Isolation method and media used: Listeria were isolated per USDA
method described by McClain & Lee (1988) with slight modifications. Therefore, the samples were enriched in
a two-step enrichment procedure and were then plated onto a selective medium as
follows.
The
swabs were directly transferred into sterile test tubes containing University
of Vermont Medium 1 (UVM-1, Hi-Media) and were incubated at 370C for
24hr. 0.1ml of the enriched
inoculum was then transferred to University of Vermont Medium 2 (UVM-2,
Hi-Media) and incubated at 370C for 48hr. The enriched medium was streaked on Polymyxin Acriflavin Lithium
chloride Ceftazidime Esculin Mannitol agar (PALCAM, Hi-Media). The streaked plates
were incubated at 370C for 48hr. The typical grey-green colonies with
black centre and a black halo around the colonies
were presumptively identified to be Listeria.
Confirmation of the isolates: The isolates were
characterized by cell morphology, Gram’s staining, catalase test, oxidase test,
tumbling motility at 20–25 0C, MR-VP test, DLABN test and
fermentation of sugar [rhamnose, xylose, maltose and mannitol] (Seeliger & Jones
1986; Low & Donachie 1997). In vitro pathogenicity was tested with
blood agar and Christie, Atkin, Munch-Petersen (CAMP)
test with Staphylococcus aureus and Rhodococcus equi. In vivo pathogenicity
was tested by inoculating mice and chicken embryos.
In vitro pathogenicity tests
Haemolysis on sheep blood agar (SBA) plate: Listeria isolates
were tested for the type and degree of haemolysis on
SBA. Detection of haemolysin allows to discriminatebetween virulent and avirulent Listeria species. The isolates were streaked onto SBA
plates, incubated at 370C in a humidified chamber for 24hr and
examined for haemolytic zones around the
colonies. The characteristic wide
and clear zone of β-haemolysis suggested L. ivanovii, while a narrow zone of β-haemolysis was characteristic for L. monocytogenes(McKellar, 1994).
Christie, Atkin, Munch-Petersen (CAMP) test: CAMP test was conducted
following the standards of the Bureau of Indian Standards (BIS 1994) with some
modifications. The standard strains of Staphylococcus aureusand Rhodococcus equiwere cultured for 24hr on SBA plates at 370C. The cultured inoculates of each strain
were streaked onto freshly prepared 7% SBA plates in parallel streaks with
considerable space between streaks. Afterwards, the Listeria isolates were streaked onto these plates
at 900 angle and 3mm apart from S. aureusand R. equi streaks. The inoculated plates
were incubated at 370C for 24hr. The plates were examined for enhancement
of haemolytic zone; in case of a CAMP- positive
reaction the haemolytic zone between a Listeriastrain and the S. aureus or R. equi strain was enhanced due to the synergistic
effect of their haemolysins. All the Listeriaisolates with CAMP-positivity against S. aureusor R. equi were characterized as L. monocytogenes and L. ivanovii respectively (McKellar 1994).
In vivo pathogenicity
tests
Mice inoculation test: The pathogenicity of the Listeriaisolates was tested by inoculating mice according to the method described by Menudier et al. (1991) with suitable modifications. The test isolates of Listeriawere grown on Brain Heart Infusion (BHI) slants at 370C for
24hr. The bacterial growth was harvested
with sterile normal saline solution (NSS) and the opacity of solution was
adjusted to McFarland Nephelometric tube number
1. Mice of either sex weighing
18–20 g were inoculated intraperitoneally with
a volume of 0.4ml of the solutions containing approximately 107 colony forming units (cfu) of the
test organism per ml. The
inoculated mice were observed for mortality over a period of 72hr.
Chick embryo inoculation
test: The
pathogenicity of Listeria isolates was also tested by inoculating
chicken embryos following the method described by Notermanset al.(1991). The blood vessel-free
surface of the chorioallantoic membrane (CAM) of two precandled 10-day old embryonatedchicken eggs was inoculated with 0.1ml of the test culture in BHI broth. Control eggs were inoculated with 0.1ml
of BHI broth. All eggs were sealed
with molten paraffin and were horizontally placed at 370C for 3
days. The eggs were examined twice
a day by transillumination for embryo death. A test isolate causing embryo mortality
after 24 hours of inoculation was considered to be pathogenic.
Antibiotic sensitivity test: The antibiotic sensitivity of
each of the Listeria isolates was tested applying the Bauer-Kirby
diffusion method (Bauer et al. 1966) using antibiotic discs (Hi-Media). The concentrations of antimicrobial
agents used were as follows: levofloxacin 5μg/disc, enrofloxacin5μg/disc, ciprofloxacin 5μg/disc, penicillin-G 10units/disc,
amoxicillin 10μg/disc, chloramphenicol 30μg/disc, ceftriaxone
30μg/disc, cephotaxime 30μg/disc, cephadroxil 30μg/disc, cephalexin 30μg/disc,
gentamicin 10μg/disc, oxytetracycline30μg/disc, amikacin 30μg/disc, tobramycin
30μg/disc, azithromycin 30μg/disc, nalidixicacid 30μg/disc.
Results
Out
of 104 examined faecal samples 24 (23.07%) samples were
found to be Listeria positive. Listeria isolates were recovered
from the faecal sample of tiger, bear, hyena,
leopard, zebra, elephant, jackal, lion, barking deer, porcupine, chital, monkey
and wild boar. Out of 24 Listeria isolates 11 were identified as L. monocytogenes, six as L. innocua,
four as L. seeligeri, two as L. welshimeri and one L. ivanovii (Table 1). Only four of the Listeriaisolates were found to be pathogenic. These were three isolates of L. monocytogenes which were from tiger, hyena and
elephant and one isolate of L. ivanovii from leopard (Table 2).
TheListeria isolates were tested in vitro for their sensitivity to
different antibiotics. The obtainedantibiogram revealed a high sensitivity towards
ciprofloxacin and levofloxacin (100%). High sensitivity was also observed towards amoxicillin, azithromycin
(87.5%) and enrofloxacin (79.1%). Moderate sensitivity was observed
towards chloramphenicol (66.7%) and amikacin(58.3%). The isolates were
resistant towards oxytetracyclin, gentamycin and cephadroxil (both 75%), penicillin-G and tobramycin (both
62.5%), cephotaxim and cephalexin (both 45.8%) and
ceftriaxone (33.3%). All isolates were resistant to nalidixicacid.
Discussion
Listeria monocytogenes is ubiquitous in nature and
has been isolated from numerous sites, including soil, sewage water and
decaying plant materials etc. Its
viability is remarkable, with survival in soil or silage for more than two years. Studies have shown that about 50% of faecal samples collected from different animals like
cattle, sheep, goat, pig and poultry contain L. monocytogenesbut don’t exhibit any clinical symptoms of listeriosis(Meng & Doyle 1997; Wesley 1999). Listeria species have previously
been reported in Odisha from milk samples of cows and
from faecal samples of various domestic animals (Sarangi et al. 2009; Sarangi& Panda 2012). In the present
study Listeria species were isolated from 24 (23.07%) out of 104 faecal samples of healthy zoo animals. Listeria infection is mostly food
borne (Ryser 1999) and raw meat,vegetable and fruits used as animal feeds in zoological parks might be the
major source of Listeria infections.
Listeria species have been reported from a number of wild animals in the
past. L. monocytogenes have been isolated from
the faecal sample of foxes, Roe Deer, badgers, hares
and Pine Marten (Weis 1975), African Lion (Haigh et
al. 1978), Grey Fox (Black et al. 1996), primates, hippopotamus, fox and bear (Arumugaswamy & Gibson 1999), farm chinchilla (Sabocanec et al. 2000), captive antelopes (Bauwens et al. 2001), wild boars (Hayashidaniet al. 2002), Colobus Monkey (Kocket al. 2003), jackal, Indian Fox, Sambar, wolf and
Spotted Deer (Kalorey et al. 2006) and from other
deer, raccoon and moose (Lyautey et al. 2007). Similarly, L. ivanovii has been isolated from Grauer’s Gorilla and Red
Ruffed Lemur (Bauwens et al. 2003) and from a septicaemic chinchilla (Kimpe et
al. 2004). However, we isolated Listeriaspecies from tiger, hyena, leopard, zebra, elephant, blue bull, barking deer
and porcupine which all have to date not been reported to carry Listeria.
Our
overall infection rate of 23.07% is comparable to infection rates found by
other researchers. Bernagozzi et al. (1999) reported
24.1% of Listeria spp. in faeces of wild
animals in National Park of Casentineforest (112 samples). Bauwens et al. (2001) isolated Listeria spp. from
22.8% of the faecal samples of Wild Animal Park, Planckendael (70 samples). Bauwens et al.
(2003) also reported a Listeria occurrence of 21% in faecalsamples of wild animals in Antwerp Zoo (200 samples). In India, Kaloreyet al. (2006) isolated L. monocytogenes in 16%
of faeces of wild animals (50 samples). A much lower infection
rate was reported by Yoshida et al. (2000), who only found an infection rate of
6.1% (623 samples) in all animals tested. However in Japanese macaques
the infection rate was also 20%. Recently, Yadav et al. (2011) isolated two Listeriaspecies (L. monocytogenes and L. innocua) out of three positive isolates from 56 faecal samples collected from mammals and birds at Baroda
Zoo, Vadodara, Gujarat State, India, which equals to a prevalence of only
5.3%. However as the range of
species and animals examined in these studies are entirely different it is not
possible to conclusively compare the infection rates found.
In
the present study 11 (10.57%) L. monocytogeneswere isolated which differ from the observation of Arumugaswamy& Gibson (1999) who after examination of 86 animals of Taronga Zological Garden, New South Wales, Australia,
revealed 25.6% were carrier of Listeria species and 18.6% were excretingL. monocytogenes. This difference may be due to varying
environmental condition between different locations, previous occurrence of the
disease and hygienic measures adopted in the zoo.
Listeria spp. have in the past been reported to
be sensitive to antibiotics active against gram positive bacteria (Hawkins et
al. 1984), but some time later reports of resistance in Listeria spp.
appeared (Abrahim et al. 1998; Walsh et al.
2001). An increase in antibiotic
resistance in Listeria spp. is in line with a global pattern of an
increasing antibiotic resistance, including resistances against multiple
antibiotics in many groups of bacteria. The occurrence of antibiotic resistance in non-pathogen forms poses a
major risk as there is possibility to transfer the resistance
factor from non-pathogens to pathogenic organisms (Walsh et al. 2001).
In
our study we found high to moderate sensitivity towards ciprofloxacin,
levofloxacin, amoxicilin, azithromycin, enrofloxacin, chloramphenicol and amikacinand resistance towards oxytetracyclin, gentamycin, cephadroxil, penicillin-G, tobramycin, cephotaxim,
cephalexin, ceftriaxone and nalidixic acid. Similar results have
been reported by Lyautey et al. (2007) who found
resistance against kanamycin, gentamycin, streptomycin and rifampicin. This differs from findings of Butko et al. (1972), who reported the sensitivity of Listeriaspp. to erythromycin, chlortetracycline, streptomycin, levomycin,
neomycin and monomycin and resistance to
penicillin. This variation in
antibiotic sensitivity might be due the above mentionedglobal increase in antibiotic resistance in the bacteria over decades.
The
present study shows the occurrence of Listeria species in captive wild
animals of Nandankanan Zoo, Baranga,Odisha, which may act as nidusof infection for other susceptible animals and cause death of animals. A further study investigating the role
of Listeria in sick wild animals is necessary and emphasis should be
given to control the food borne transmission of the diseases.
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