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First report of Ophidascaris spp. (Class: Nematode) Infection in Wild-Caught Javanese Keelback Water Snake (Fowlea melanzostus) in Banyuwangi District

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Abstract

The javanese keelback water snake (Fowlea melanzostus) is a semi-aquatic reptile that often found in Indonesia and endemic to Java island. Water tiger snakes are usually kept as exotic pets. Wild caught javanese keelback water snakes have risks of spreading several disease agents that can be zoonotic, which is nematodiasis caused by Ophidascaris spp. This study aims to determine the prevalence level of Ophidascaris spp. infections in javanese keelback water snakes from Banyuwangi district. This study used a descriptive method with accidental sampling. The total sample in this study was 33 wild-caught javanese keelback water snakes. The identification method used is snake samples that have been collected are then euthanized and necropsied to check for nematode infections in the subcutan, muscular, and visceral part. The result showed that 28 samples were positive for nematode infection and 5 samples were negative with a prevalence rate of 84.84%. The nematodes that have been identified come from the genus Ophidascaris spp. Therefore, further research is needed to determine the incidence of nematode transmission in other wild caught snakes in Indonesia.
Journal of Parasite Science
Vol. 8 No. 1 March 2024 | Page 27 30
Journal of Parasite Science (JoPS) | p2599-0993 ; e2656-5331
doi.org/10.20473/jops.v8i1.54578 27
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JOURNAL OF PARASITE SCIENCE
https:/e-journal.unair.ac.id/JoPS
2599-0993 (print) | 2656-5331 (online)
Original Research
First Report of Ophidascaris spp. (Class: Nematode) Infection on Wild Javanese
Keelback Water Snake (Fowlea melanzostus) in Banyuwangi
1)Elma Salsabila Putri , 2)Aditya Yudhana , 3)Ragil Angga Prastiya , 4)Maya Nurwartanti
Yunita , 5)Bodhi Agustono , 6)Prima Ayu Wibawati
1)Student, Faculty of Health, Medicine, and Life Sciences (FIKKIA), Universitas Airlangga
2)Division of Parasitology, Faculty of Health, Medicine, and Life Sciences (FIKKIA), Universitas Airlangga
3)Division of Veterinary Reproduction, Faculty of Health, Medicine, and Life Sciences (FIKKIA), Universitas Airlangga
4)Division of Veterinary Pathology, Faculty of Health, Medicine, and Life Sciences (FIKKIA), Universitas Airlangga
5)Division of Animal Husbandry, Faculty of Health, Medicine, and Life Sciences (FIKKIA), Universitas Airlangga
6)Division of Veterinary Public Health, Faculty of Health, Medicine, and Life Sciences (FIKKIA), Universitas Airlangga
*Corresponding author: adityayudhana@fkh.unair.ac.id
ABSTRACT
ARTICLE INFO
The javanese keelback water snake (Fowlea melanzostus) is a semi-
aquatic reptile that often found in Indonesia and endemic to Java
island. Water tiger snakes are usually kept as exotic pets. Wild caught
javanese keelback water snakes have risks of spreading several disease
agents that can be zoonotic, which is nematodiasis caused by
Ophidascaris spp. This study aims to determine the prevalence level
of Ophidascaris spp. infections in javanese keelback water snakes
from Banyuwangi district. This study used a descriptive method with
accidental sampling. The total sample in this study was 33 wild-caught
javanese keelback water snakes. The identification method used is
snake samples that have been collected are then euthanized and
necropsied to check for nematode infections in the subcutan, muscular,
and visceral part. The result showed that 28 samples were positive for
nematode infection and 5 samples were negative with a prevalence rate
of 84.84%. The nematodes that have been identified come from the
genus Ophidascaris spp. Therefore, further research is needed to
determine the incidence of nematode transmission in other wild caught
snakes in Indonesia.
Article history
Received: January, 29th 2024
Revised: February, 23rd 2024
Accepted: February, 23rd 2024
Published: March, 15th 2024
Keywords
Fowlea melanzostus,
Infectious disease,
Neglected disease,
Ophidascaris spp.
INTRODUCTION
One type of snake that is commonly found in
Indonesia and endemic to Java Island is the Fowlea
melanzostus (Vogel & David, 2012). Also known as
the Javanese Keelback Water Snake, this water
snake species belong to the genus Fowlea is semi-
aquatic, with its habitat located in both terrestrial and
aquatic environments such as rivers, ponds, or
reservoirs. The common prey of the water snake
includes frogs, fish, and small birds (Bharati, 2018).
Wang et al (2014) reported that the water snake is
often kept as an exotic pet and traded as a food
product for consumption in China. The maintenance
of wild-caught water snakes poses risks in the spread
of several disease agents that can be zoonotic
(Nardoni et al., 2008). One of the diseases that can
infect snakes is parasitic disease caused by worms,
with two modes of infection transmission: through
infective larvae and infective eggs. One type of
worm that commonly infects snakes is the nematode
worm (Halan & Kottferova, 2021).
Nematode infections can cause harm to
keepers and the health of the snake itself, because
nematode infections can damage the snake's
digestive tract and even result in death (Hanafiah et
al., 2018). Nematode infections in snakes have
zoonotic potential which can be transmitted between
vertebrate animals and humans through direct or
indirect contact. One factor in the occurrence of
nematode infections can increase due to improper
Journal of Parasite Science
Vol. 8, No.1, March 2024, pp 27-30
28 Putri et.al (First Report of Ophidascaris spp. Infection on Fowlea melanzostus in Banyuwangi)
maintenance of snakes, such as not giving worm
medicine to the snakes being kept. In addition, snake
cages that are not properly kept clean can be a source
of nematode transmission, because infected snake
feces contain eggs which can develop into infective
larvae which can be contaminated through food or
drink and infect other snakes (Telnoni et al., 2016).
Cases of nematode infections that often infect
snakes come from the nematode class
Nemathelminthes, genus: Rhabdias spp., Oxyuris
spp., Ophidascaris spp., Kalicephalus spp.,
Strongyloides spp., Capillaria spp. (Klingenberg,
2007). Nematode infections can be detrimental to
snakes because they can cause loss of nutrition,
tissue and organ obstruction and increase the
possibility of secondary infections caused by
bacteria (Rahmayani, 2014). Ophidascaris spp. can
cause infections affected with regurgitation, diarrhea
and pneumonia caused by nematodes that block the
snake's stomach (Akhila et al., 2018).
From the research report, javanese keelback
water snake has previously been reported to be
infected by tapeworms (Genus: Sparganosis) with
prevalence of 92.72% (Yudhana, 2021). However
nematode infections in javanese keelback water
snakes have never been reported from the
Banyuwangi Regency area, so further research needs
to be conducted regarding the incidence of nematode
infections in javanese keelback water snakes
(Fowlea melanzostus) in the Banyuwangi district.
METHODS
The materials used for the process of storing
samples are solution of NaCl and glycerin alcohol
concentration of 5%. The materials used for staining
samples are carmine solution, distilled water, 70%
alcohol, 85% alcohol, 95% alcohol, acidic alcohol,
base alcohol and entellan. The tools used to identify
nematode worms in javanese keelback water snake
samples are ruler, scalpel, surgical scissors, scissors,
anatomical tweezers, sample pot, petri dish, tray,
staining jar, object glass, and binocular microscope.
This research is a type of descriptive research
using wild caught javanese keelback water snakes in
the Banyuwangi Regency area as samples. The
sampling method uses accidental sampling and
sample calculation uses the Slovin formula. The
research conducted in September-December 2023 at
the Parasitology Laboratory, Faculty of Health,
Medicine and Life Sciences (FIKKIA) Airlangga
University in Banyuwangi.
The javanese keelback water snake was
euthanized in accordance with operational standards
for ethical testing, then a necropsy was carried out,
starting with an incision from one side of the mouth
to the tail, then separating the subcutaneous part,
muscles and internal organs. The nematodes
obtained were then stored in 70% alcohol and
stained using the carmine semichen-acetic method.
The results of the identification and prevalence of
nematode infections in javanese keelback water
snakes in the Banyuwangi district were calculated
using the prevalence calculation formula and
presented in table form.
RESULTS AND DISCUSSION
The results showed that of the 33 samples of
javanese keelback water snakes (Fowlea
melanzostus), 28 samples were positively infected
with nematodes. The prevalence of nematode
infection in javanese keelback water snakes was
84.84%. The total number of nematodes collected
was 655 nematodes with infection degrees of 98
nematodes that had a predilection for the stomach
and 557 nematodes that had a predilection for the
small intestine. The nematodes that were identified
were the genus Ophidascaris spp. and no other
nematodes were found in any predilection that was
examined. Ophidascaris spp. has average body
length of 11 cm, an elongated cylindrical body that
is light brown in color, a mouth with 2 papillae, the
distance between the mouth and the end of the
esophagus is relatively long, and the spicules tend to
be short. Macroscopic morphology and predilection
that can be seen in Figure 1.
Figure 1. A) Predilection of Ophidascaris spp. on
small intestine of javanese keelback water snake are
shown on the blue box. B) Macroscopic
morphology of Ophidascaris spp. with a size of
11.5 cm.
Microscopic morphology of Ophidascaris
spp. has three lip formations, the dorsal lip has two
papillae and the other side lips each have one
papilla, there are interlabials around the mouth
which are characteristic of the Ascarididae family,
and the cervical alae are narrow. Identification of
Ophidascaris spp. microscopically using the
Carmine Semichen-Acetic staining method
(Kuhlman, 2006) and observations were made
using a microscope with 400x magnification.
Microscopic morphology of Ophidascaris spp. can
be seen in Figure 2.
A
B
Journal of Parasite Science
Vol. 8 No. 1 March 2024 | Page 27 30
Putri et.al (First Report of Ophidascaris spp. Infection on Fowlea melanzostus in Banyuwangi) 29
Figure 2. Microscopic morphology of Ophidascaris spp. identified using the carmine semichen-acetic
staining method. A) Anterior part of Ophidascaris spp. B) Posterior part of Ophidascaris spp. 1) Cervical
alae. 2) Mouth. 3) Spicule.
The prevalence rate of Ophidascaris spp. is
included in the usually category in the sense that the
nematode usually infects wild-caught javanese
keelback water snakes (Williams & Bunkley-
Williams, 1996). The prevalence data of
Ophidascaris spp. infection can be seen in Table 1.
Table 1. The Prevalence of Ophidascaris spp. infection in javanese keelback water snakes (Fowlea
melanzostus) in Banyuwangi Regency area based on age
The prevalence rate of Ophidascaris spp.
can be caused by age, habitat and diet factors
(Kondzior et al., 2018). The prevalence rate of
Ophidascaris spp. In this study there are differences
in categorization of the age of the snake, javanese
keelback water snakes are categorized into 3 ages
based on the length of the snake's body, namely
hatchlings with an age of 0-2 weeks (length <59
cm), juveniles with an age of 2 weeks - 1 year
(length 60-79 cm), and adults aged more than 1 year
(length > 79 cm) (Yudhana, 2021). For snakes in
the juvenile age category, the prevalence rate is
95.2%, which is higher than the prevalence rate for
hatchlings, 66.6% and adults, 66.6%. This
difference in prevalence rates is due to the different
availability of prey in the wild. This research used
wild caught javanese keelback water snakes
obtained from four different locations located in the
Sempu district area, Banyuwangi which is flowed
by the Setail river. Banyuwangi district is
climatically and geographically suitable for the
habitat of javanese keelback water snakes because
it is included in the wet and dry tropical climate
category.
Life cycle of Ophidascaris spp. is an indirect
life cycle. Eggs are excreted in the environment
through the host's feces, then intermediate hosts
(rodents and amphibians) ate the eggs containing
L2 larvae. The snake then eats an intermediate host
that has L2 larvae in muscle or visceral tissue. The
eggs then hatch and perforate the intestines of the
definitive host and migrate to the lungs where L3
larvae occur. These larvae migrate to the pharynx
and are swallowed along with bronchial secretions.
L3 larvae molt in the abdomen to become L4 and
L5 larvae or adult worms, which will then penetrate
strongly into the stomach wall and release eggs
back into the environment (Mello et al., 2017).
Cases of infection with Ophidascaris spp.
has been reported by Bimi et al (2021) in Ghana,
Africa in African rock python snakes (Phyton
sebae), adult stage worms were found and the
predilection was in the digestive tract, especially in
the anterior part of the small intestine just below the
pyloric sphincter of the stomach. Pathogenesis due
to infection with nematodes from the Ascarididae
family, especially Ophidascaris spp. often causes
gastrointestinal disease, liver and lung lesions.
Ascarididae nematodes live in the digestive tract of
snakes, in inflammatory nodules near the pylorus of
the stomach, distal esophagus, stomach and small
intestine. Reports of similar cases also occurred in
tropical rattlesnakes (Crotalus dorissus) in Minas
Gerais, Brazil. Results from a total sample of 35
rattlesnakes, 19 of which were positively infected
with Ophidascaris spp. which has a predilection for
the gastric mucosa, ulcerated lesions with a
diameter of 1-2 mm were also found on the surface
mucosa of the stomach (Mello et al., 2017). The
results of the snake necropsy in the case of the death
of the Indian rock python (Python molurus) in
Sistan, Iran found 2 nematodes identified as
Ophidascaris spp. which causes gastrointestinal,
liver and lung damage. Ophidascaris spp. is an
important pathogen that needs attention, if the
Snake Age
Category
Number
Of
Samples
(N)
Number Of
Positive
Samples (N)
Prevalence
(%)
Degree of
Infection
(N)
Infection Predilection
Ophidascaris spp. (N)
Stomach
Small
Intestine
Hatchling (<2
weeks)
3
2
66,6
10
1
9
Juvenile (2
weeks1 year)
21
20
95,2
414
69
345
Adult (>1 year)
9
6
66,6
231
28
203
Total
33
28
84,84
655
98
557
B
3
A
1
2
Journal of Parasite Science
Vol. 8, No.1, March 2024, pp 27-30
30 Putri et.al (First Report of Ophidascaris spp. Infection on Fowlea melanzostus in Banyuwangi)
infestation is in large numbers it can have fatal
consequences (Ganjali et al., 2015).
Based on research that has been carried out,
33 samples of javanese keelback water snakes, 28
positive and 5 negative, were found, totaling 655
Ophidascaris spp. which shows that the potential
for transmission is very high. Several measures for
treating nematodiasis in snakes, especially
Ophidascaris spp. infections, such as administering
Fenbedazole (25-50 mg/kg) orally once a day for 5
days and repeated in 10 days or (50-100 mg/kg
orally) repeated in 14 day. Administration of
Ivermectin (0.2 mg/kg) intramuscularly or
subcutaneously for 2 weeks, and Albendazole (50
mg/kg) orally once (Mitchell & Diaz-Figueroa,
2005). Prevention of infection with Ophidascaris
spp. for snakes that are used as exotic pets, can be
done by paying attention to maintenance
management such as habitat, drinking water and
food for snakes which have the potential to transmit
Ophidascaris spp. infections. The snake's health
also needs to be checked regularly for parasites and
other pathogens. Prevention of infection with
Ophidascaris spp. in humans, this is done by paying
attention to surrounding sanitation, such as
separating pet snakes from areas where food is
prepared, maintaining the cleanliness of food
ingredients, clean hands and eating utensils which
can potentially cause transmission of Ophidascaris
spp. infections (Mendoza-Roldan et al., 2020).
CONCLUSION
The prevalence of nematode infection in
javanese keelback water snakes in the Banyuwangi
Regency area is 84.84%. Based on the
identification and calculation results of the
prevalence of nematode infection in javanese
keelback water snakes (Fowlea melanzostus) in the
Banyuwangi district, from a total of 33 samples
there were 28 positive samples infected with
nematodes and 5 negative samples infected with
nematodes. The total number of nematodes
collected was 655 nematodes with a predilection for
the stomach and small intestine. The nematodes that
were identified were Ophidascaris spp. and no
other nematodes were found in any predilection that
had been examined.
ACKNOWLEDGMENT
The author would like to thank Faculty of
Health, Medicine and Life Sciences (FIKKIA)
Universitas Airlangga for the support in the form of
facilities and assistance from various parties who
supported the research process until the completion
of this study.
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