Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 October 2023 | 15(10): 24079–24085
ISSN 0974-7907
(Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.8236.15.10.24079-24085
#8236 | Received 24
October 2022 | Final received 07 June 2023 | Finally accepted 27 August 2023
Efficacy of levamisole and
oxyclozanide treatment on gastrointestinal nematodes of ungulates at the
Central Zoo, Nepal
Pratik Kiju
1, Amir Sadaula 2, Parbat Jung Thapa
3 & Chiranjibi
Prasad Pokheral 4
1 B.V.Sc. and A.H, Institute of
Agriculture and Animal Science, Tribhuvan University, Paklihawa
Campus, Siddharthanagar, 32900, Nepal.
2,3,4 National Trust for Nature
Conservation, P.O. Box 3712, Khumaltar, Lalitpur,
44600, Nepal.
1 pratikkiju2@gmail.com
(corresponding author), 2 naturalamir@gmail.com, 3 parbatjungthapa26@gmail.com,
4 cppokharel@ntnc.org.np
Editor: B.R. Latha, Madras
Veterinary College Chennai, India. Date of publication: 26 October
2023 (online & print)
Citation: Kiju, P., A. Sadaula,
P.J. Thapa & C.P. Pokheral (2023). Efficacy of
levamisole and oxyclozanide treatment on gastrointestinal nematodes of
ungulates at the Central Zoo, Nepal. Journal of Threatened Taxa 15(10): 24079–24085. https://doi.org/10.11609/jott.8236.15.10.24079-24085
Copyright: © Kiju et al. 2023. Creative Commons Attribution 4.0
International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by providing adequate credit to the
author(s) and the source of publication.
Funding: None.
Competing interests: The authors declare no competing interests.
Author details: Pratik Kiju is a veterinarian and currently pursuing an Erasmus Mundus Joint master’s degree in Infectious Disease and One Health program. He is also working as a research assistant in the Center for One Health Research and Promotion. Amir Sadaula is a wildlife veterinarian at the National Trust for Nature Conservation (NTNC) - Biodiversity Conservation Center and has more than a decade of experience in treating wild animals all over Nepal. Parbat Jung
Thapa is a zoo and wildlife veterinarian at the National Trust for Nature Conservation (NTNC) - Central Zoo Jwalakhel Nepal. Chiranjibi Prasad Pokheral is the Project Manager at National Trust for Nature Conservation – Central Zoo, Nepal.
Author contributions: PK-—conceptualization, lab works, manuscript writing, editing, data compilation and analysis. AS, PJT & CPP—conceptualization, field methodology, review and editing.
Acknowledgements: My utmost gratitude towards
Shambhu Shah, PhD, member secretary of the Internship Advisory Committee 2021
and prof. Hari Bahadur Rana for his commendable suggestions and guidance. My
humble thanks to Dr. Subash Rimal,
Dr. Persia Carrol Thapa, Dr.
Swochhal Prakash Shrestha, Prof.
Hari Bahadur Rana and Ms. Shristy Buddha Magar for
their continuous guidance and support. Similarly, I would also like to express
my appreciation towards zoo keepers; Mr. Ram Bahadur Shrestha and Mr. Kishor Bista who assisted me in the sample collection.
Abstract: The efficacy evaluation of
levamisole and oxyclozanide treatment on the gastrointestinal nematodes of
ungulates at the central zoo, Nepal was carried out from June—August 2021. A
total of 40 fecal samples were collected from 10 species of ungulates from the
central zoo for determining the efficacy of the anthelmintic given at day 0 of
pretreatment and post-treatment analysis on day 07 and day 14. The
concentration method (floatation concentration) was used for the microscopic
examination of eggs, and quantitative examination (EPG) of nematode eggs was
carried out with the help of modified McMaster slides. The identification was
done using an optic micrometer and fecal egg culture. Anthelmintic resistance
status was evaluated by the Fecal Egg Count Reduction Technique (FECRT) based
on the method described by the World Association for the Advancement of
Veterinary Parasitology (WAAVP) guidelines and with the Bayesian hierarchical
model. Out of 40 samples, nematode prevalence was found to be 68%, in which
single infection was detected in 48% and double infection in 52%. The efficacy
of Zanide L forte (levamisole-0.75 g and
oxyclozanide-1.00 g) was found to be 85% (UI 80-89) at day 07 and 89% (UI
85-92) at day 14 by using Hierarchical Modelling of Fecal Egg count based on
‘eggCounts-2.3 on R version 3.6.1 and 86% (CI 61.51–95%) at day 07 and 90% (CI
74.18–95%) at day 14 by WAAVP guidelines. This study represents the first
documented case of ineffectiveness of anthelmintic treatment resulting in
anthelmintic resistance in the central zoo. Thus, there is a requirement for a
suitable and efficacious anthelmintic program.
Keywords: Anthelminthic, captive wild
ungulates, efficacy, FECRT %, nematodes.
INTRODUCTION
Zoos are centers in which wild animals are kept for aesthetic,
educational and conservation purposes (Thawait et al. 2014). The Central Zoo of Nepal was established in 1932. Ungulates
cover the major population
of the zoo animals in the Central Zoo, which includes Spotted Deer, Sambar
Deer, Four-horned Antelopes,
Himalayan Goral, Blue Bull,
Barking Deer, One-horned Rhinoceros, Wild Boar, and Wild Water Buffalo.
Parasitic infection
is one of the causes of morbidity and mortality in captivity, along with improper diet
and poor husbandry practice (Singh et al. 2006; Mir et al.
2016; Kolapo & Jegede
2017). In the wild, animals
generally have a natural resistance to parasites due to their
diverse habitat and food, but due
to the confinement
and change in living conditions,
captive wild animals might be more susceptible
to many diseases
caused by viruses, bacteria, rickettsia and parasites
(Goossens et al. 2005; Thawait et al. 2014).
Nematodes are generalist parasites of a
wide range of hosts (Walker
& Morgan 2014). Generally, ungulates are infected by nematodes
by ingesting infective larvae from the pasture,
and in some species, larvae also penetrate
through the skin (Walker
& Morgan 2014). Zoo ruminants are particularly vulnerable to gastrointestinal nematodes due to
high stocking density
without the possibility of pasture rotation, leading the pasture
to heavy exposure to infective nematode larvae or eggs (Goossens et al. 2006).
The epidemiology
of nematodosis in domestic ruminants is well studied, but there are limited studies and reports that
directly address parasite
control programs in captive wild ruminants
(Isaza et al. 1990; Goossens et al. 2006). Regular parasite load examination, anthelmintic
efficacy, and resistance evaluation are not frequently done in many zoological
gardens and parks. Furthermore, there is no published data on the efficacy of anthelmintics in captive wild ungulates in Nepal. Fecal egg count reduction
(FECR) is the simplest,
most effective, and most widely used method
to evaluate the efficacy of anthelmintics (Coles et al. 1992; Cabaret & Berrag 2004) and has been used in captive wild animals (Nalubamba & Mudenda 2012; Pawar et al. 2020).
Anthelmintic resistance is becoming a threatening issue in every livestock class and in every anthelmintic class globally (Kaplan 2004). Idiosyncrasies
are also one of the major factors that contribute to the
efficacy of anthelmintics
on different wild animals on certain
occasions (Ortiz et al. 2001). Thus,
this present study will aim to
contribute to establishing the prevalence of gastrointestinal
nematode parasites and the anthelminthic efficacy of oxyclozanide and levamisole administration in the ungulates in Central Zoo,
Nepal.
MATERIALS AND METHODS
Time and place of research
The research was carried
out at the Central Zoo from
19 June 2021 and ended on 19 August 2021.
Sample collection
Pooled fecal samples were
collected from the fresh feces of the ungulates early
in the morning from different spots of the enclosure with the help of zoo
keepers. The fresh sample was randomly taken on the basis of the number of
ungulates in each enclosure. The sample was labelled accordingly and the method
was followed as per Soulsby (2005). The sample of
around 15 gm was kept in an airtight plastic zipper bag and transported in a
cool box to the laboratory at the Department of Animal Science, Institute of
Agriculture and Animal Science (IAAS), Tribhuvan University. Macroscopic
examination of the helminths, if present, was done from the feces.
The concentration method (floatation concentration) was used for the
microscopic examination of eggs, and quantitative examination of eggs was
carried out with the help of modified McMaster slides. The size of the eggs was
measured using an optic micrometer. The sample
containing more than one species of nematodes were kept as mixed infection
sample and while samples with only one species were labelled as single
infection.
For further confirmation, the fecal
culture method using the ‘Falcon tube method of fecal
culture’ for nematode larva was also carried out in accordance with the method
provided by Soulsby (2005) and Zajac & Conboy
(2012). One gram of feces was wrapped up in a
blotting paper making a pouch. In a falcon tube, water was placed up to the
circular rim at the distal end of the tube. The pouch was attached to the
distal interior end of the Falcon tube using a long piece of the same blotting
paper. The tube was now made airtight and left in a dark place for up to 7–8
days for incubation of nematodes larvae. After about 7–8 days, the blotting
paper and the sample were removed.
Twenty microliters of water was transferred to a glass slide with the
help of a micropipette, which was then examined for the larvae of nematode
under a microscope.
Assessment of
drug efficacy and anthelmintic resistance
Anthelmintic resistance status was evaluated by FECRT
based on the method described by the World Association for the Advancement of
Veterinary Parasitology (WAAVP) guidelines (Coles et al. 1992; McKenna 1994;
Storey 2015). The FECRT has been the most recommended method so far being
broadly utilized for field or research studies (Coles et al. 1992). FECRT
assesses the anthelmintic resistance of a given compound by comparing worm egg
counts from animals before and after treatment.
All the individuals who were positive for nematode eggs
were subjected to EPG on day 0 before treatment, day 07 and day 14 after
treatment.
FECR (%) = 100 %*(1-[T2/T1])
Here, T1 is the pre-treatment EPG
T2 is post-treatment EPG.
(Coles et
al. 1992; McKenna 1994;
Cabaret & Berrag 2004; Pawar
et al. 2020)
Resistance is
present when two criteria are met:
I. The
percentage reduction in egg count is less than 95%.
II. The lower
limit of its 95% confidence interval is equal or below 90%.
Treatment
At 10 mg per kg, ZANIDE- L Forte Bolus (Levamisole
Hydrochloride BP 0.75 g and Oxyclozanide BP (Vet) 1 g) was given to the
ungulates. There was a specific deworming practice at the zoo of changing the
anthelminthic drug types regularly at the interval of 4-months. Ivermectin was
used 4-months prior to this research and four months before Ivermectin,
albendazole was used. So, this time it was the turn of ZANIDE- L Forte Bolus
(Levamisole Hydrochloride BP 0.75 g and Oxyclozanide BP (Vet) 1 g). So, in
accordance with that schedule, ZANIDE-L Forte was used. This research showed
the deworming status of levamisole and oxyclozanide in the nematodes. After the
determination of pre-anthelmintic EPG at Day 0, the post-anthelmintic EPG at
Day 07 and Day 14 were also determined using the same procedure as mentioned
earlier. The mean EPG of Day 7 and Day 14 is used to determine the efficacy of
the respective days.
Data analysis
Fecal egg count in
EPG is determined from a sample taken on day 0 prior to treatment with an
anthelmintic drug, as well as on days 07 and 14 following treatment. The data
were entered into a spreadsheet and imported into IBM SPSS version 25 to test
for statistical significance.
Egg count data on FECRT was analyzed
for fecal egg count reduction (%FECR) using
‘eggCounts-2.3’ on R version 3.6.1. (Young et al. 2000; Torgerson et al. 2014;
Wang et al. 2018)
For analysis of drug efficacies, a ‘z’-test (Sample size
> 30) was done to analyze the significance of the pretest and the posttest group on
different days. Similarly, to determine the association within different
groups, a chi-square test was done.
A p-value of less than 0.05 at 95% CI was considered
statistically significant. Finally, tables and charts were used to present the
results generated from SPSS and the graphical presentation was completed in MS
Excel 2016.
RESULTS
During the study, out of 40 samples examined by the
floatation concentration method, 27 samples were positive for the presence of
nematode eggs as given in Table 1. Thus, the prevalence was found to be 67.5%.
Single parasitic infection was detected in 13 (48.15%) and mixed parasitic
infection in 14 (51.85%) samples. The intensity of eggs belonging to eight
different types of nematodes, i.e., Bunostomum spp., Strongyloides
spp., Trichuris
spp., Ostertagia spp., Haemonchus
spp., Capillaria spp., Ascaris
spp., and Oesophagostomum spp., varied from + to +++ in the study. The eggs were
identified on the basis of their sizes using the calibrated optic micrometer (Soulsby 2005).
Further confirmation was done by the fecal culture
method with reference to Soulsby (2005) and Zajac
& Conboy (2012).
The Strongyloides spp.
were major nematode eggs seen during the study with 44.44% prevalence, followed
by Bunostomum spp. 22.22% and Trichuris spp., Ostertagia spp., Haemonchus spp., Capillaria spp., Ascaris
spp., Oesophagostomum
spp., with 5.56%
each as shown in Figure 2.
The efficacy of Zanide L forte
(levamisole-0.75 g and oxyclozanide-1.00 g) was found to be 85.3% (CI 80.4–89)
at day 07 and 89.2% (CI 85–92.3) at day 14 by using hierarchical modelling of fecal egg count based on ‘eggcounts-2.3 on R version 3.6.1
and 85.47% (CI 61.51–94.48%) at day 07 and 89.67% (CI 74.18–95.61%) at day 14
by WAAVP guidelines.
Since, the
P value is less than 0.05 in both the days, the
pretest at day 0 and post test data at day 07 and day 14 are statistically significant respectively.
So, we reject the null hypothesis, i.e., there is a statistical difference between the mean of the
two data sets. The anthelminthic
treatment at day 0 has a significant effect on the EPG count of day 7 and day
14.
DISCUSSION
This study
shows the overall prevalence
of 67.5% of nematode infection in the
total of 40 samples taken, in which
single infection was detected
in 48.15% and double in 51.85%. The findings of Pun (2014) were similar to
the research conducted,
i.e., prevalence of 59% of parasite infection in the central zoo, Kathmandu. The present findings
in respect to overall prevalence
in captive herbivores agreed with Bir
Moti Bagh Mini Zoo, India
(68%) (Mir et al. 2016), Dehiwala
National Zoological Gardens,
Sri Lanka (62.9%) (Aviruppola et al. 2016), Ljubljana Zoo,
Slovenia (61%) (Kvapil et al. 2017), Rangpur Recreational Garden and Zoo, Bangladesh
(60%) (Khatun et al. 2014) but disagreed
with research at the Zoological gardens of Malaysia
(45.7% of ungulates) (Lim et al. 2008), Maharajbag Zoo, Nagpur (50%) (Borghare
et al. 2009), the Antwerp
Zoo and the Animal Park Planckendael, Belgium
(36.5%) (Goossens et al. 2005), and Mahendra Choudhury Zoological Park, Chhatbir, Punjab
(25.17%) (Singh et al. 2006).
Strongyloides spp.
(44.44%) were the major nematodes detected in the study, followed
by Bunostomum spp. (22.22%) and Capillaria spp., Haemonchus spp., Trichuris spp., Oesophagostomum spp., Ascaris spp., and Oestertagia spp., were found at 5.65% each.
Nematodes were the group of concern in this research because the majority of studies reported a null prevalence of parasitic infection with trematode and cestode
(Atanaskova et al. 2011; Pun
2014; Mir et al. 2016; Pawar
et al. 2020;). Cestodes and
trematodes need intermediate hosts and are less likely
to accumulate in captive and enclosed
ecosystems (Atanaskova et
al. 2011). On the contrary,
nematodes are one of the most important veterinary helminths that have a negative impact on wildlife
health as well as conservation ecology
(Goossens et al. 2006; Singh et al. 2006).
Many nematode parasites of veterinary importance have a huge genetic diversity
and features that favor the development of anthelmintic resistance (Kaplan
2004). Similarly, the author has also stated that anthelmintic
resistance has been reported
in every anthelmintic
class.
The present study
reports the baseline study of the effectiveness
of the levamisole and oxyclozanide treatment on the nematodes of the captive ungulates
of the Central Zoo. The present study
agrees with WAAVP guidelines (Coles et al. 1992) for
the diagnosis of anthelmintic
resistance without using a
control group (pretreatment mean
was used for comparison) and similar studies were also conducted by Young et al. (2000), Goossens et al. (2006), and Pawar et al. (2020).
The result
(<90% FECR and lower CI
<95%) indicated presence
of anthelmintic resistance
(Coles et al. 1992; McKenna 1994). Similar results were obtained from
captive wild impala in Zambia, in which
the efficacy using FECR % was around 90% showing low efficacy and suggesting anthelmintic failure (Nalubamba
& Mudenda 2012).
The failure of an anthelmintic could be the
result of resistance, either from the
survival of existing nematodes
or the establishment of a new infection.
The unavailability of the
correct dose for the specific wild captive animals with an improper
route of anthelmintic (causing
more wastage and low dosage) (Nalubamba & Mudenda 2012) and idiosyncrasies (Ortiz et al.
2001) may have contributed to the development of the anthelmintic resistance in the current study. Additionally, ZANIDE-L Forte Bolus (Levamisole
Hydrochloride BP 0.75 gm and
Oxyclozanide BP (Vet) 1 gm
is not a specific drug for nematodes, especially the oxyclozanide may not be effective
to the extent
required. So, the necessity in this case is to change the drugs used for the rotation,
based on the infection that is prevalent.
CONCLUSION
Infection with
nematodes is of major veterinary
importance. Frequent, unnecessary,
and under-dosing of anthelmintics has given rise to a major problem of anthelmintic resistance in animals. The serious problem of anthelmintic resistance is based on the fact
that levels of resistance can increase rapidly
and the development of new
classes of drugs is less. The efficacy
of levamisole and oxyclozanide is found to be less than
90% with a lower confidence limit of 95% confidence
level less than 90% suggesting the presence of resistance of gastrointestinal nematodes against the anthelmintic
at the Central Zoo. This study is the first documentation of the efficacy of the anthelmintic used in the captive wild animal setting, in the Central
Zoo, Kathmandu. The low efficacy of the anthelmintic is a concerning factor that requires proper nutrition, sanitation, and periodic deworming strictly based on advanced scientific strategies with periodic checks on anthelmintic resistance, which will aid in combating
the serious issue of anthelmintic resistance.
Table 1. Prevalence of gastro intestinal
nematode infection in captive ungulates of the Central Zoo.
|
|
Ungulate species |
No. of sample collected |
No of sample positive for
nematodes |
Sample demonstrating single
infection |
Sample demonstrating mixed
infection |
Types of infection |
|
1 |
Spotted Deer Axis axis |
12 |
6(50%) |
3 |
3 |
Bunostomum spp., Strongyloides spp., Trichuris spp. |
|
2 |
Blue Bull Boselaphus
tragacamelus |
4 |
2(50%) |
0 |
2 |
Ostertagia spp., Strongyoides spp. |
|
3 |
Black Buck Antelope cervicapra |
2 |
2(100%) |
0 |
2 |
Bunostomum spp., Haemonchus spp., Strongyloides
spp. |
|
4 |
Barking Deer Muntiacus muntjak |
9 |
7(77.78%) |
4 |
3 |
Bunostomum spp., Trichuris
spp., Strongyloides spp. |
|
5 |
Sambar Deer Rusa
unicolor |
1 |
0 |
0 |
0 |
- |
|
6 |
Himalayan Goral Naemorhedus goral |
2 |
2(100%) |
1 |
1 |
Trichuris spp., Strongyloides spp. |
|
7 |
Four-horned Antelop
Tetracerus quadricornis |
1 |
1(100%) |
1 |
0 |
Strongyloides spp. |
|
8 |
Wild Boar Sus
scrofa |
2 |
2(100%) |
0 |
2 |
Ascaris spp., Oesophagostomum spp. |
|
9 |
Wild Water Buffalo Bubalus arnee |
4 |
3(75%) |
2 |
1 |
Bunostomum spp., Strongyloides spp., Capillaria
spp. |
|
10 |
One-horned Rhino Rhinocerous unicornis |
3 |
2(66.67%) |
3 |
0 |
Strongyloides spp. |
|
|
Total |
40 |
27(67.50%) |
13(48.15%) |
14(51.85%) |
|
Table 2. Nematode species identified from the
size of their eggs.
|
|
Nematode Species |
Size of Egg |
Reference value Soulsby (2005). |
|
1 |
Strongyloides spp. |
47 by 20 μm |
40–60 by 20–25 μm |
|
2 |
Bunostomum spp. |
84 by 49 μm |
79–97 by 47–50 μm |
|
3 |
Trichuris spp. |
67 by 34 μm |
68–75 by 36–40 μm |
|
4 |
Haemonchus spp. |
78 by 36 μm |
70–85 by 41–48 μm |
|
5 |
Ascaris spp. |
59 by 41 μm |
50–75 by 40–50 μm |
|
6 |
Oestartagia spp. |
65 by 35 μm |
60–85 by 40–45 μm |
|
7 |
Capillaria.spp. |
42 by 25 μm |
45–50 by 22–25 μm |
|
8 |
Oesophagostomum spp. |
35 by 63 μm |
35-45 by 60–80 μm |
Table 3. Egg per gram (EPG) counts and FECR%
(Bayesian hierarchical model) of captive wild ungulates from Nepal's central
zoo treated with Zanide-L forte* at 10mg/kg body
weight.
|
|
Ungulate species |
No. of sample taken |
EPG Day 0 |
EPG Day 7 |
EPG Day 14 |
FECR Day 7 UI |
FECR Day 14 UI |
|
1 |
Spotted Deer Axis axis |
12 |
1050 |
150 |
150 |
82.1% (51%.9–95%) |
82.1% (51%.9–95%) |
|
2 |
Blue Bull Boselaphus
tragacamelus |
4 |
7950 |
1250 |
650 |
83.4% (75.2–89.3) |
91.2% (85.3–95.1) |
|
3 |
Black Buck Antilope
cervicapra |
2 |
4150 |
350 |
250 |
90.5% (81.5–95.7) |
93% (85.3–97.3) |
|
4 |
Barking Deer Muntiacus muntjak |
9 |
1500 |
200 |
300 |
84.3% (62.1–94.9) |
77.5 (51.4–91.1) |
|
5 |
Sambar Deer Rusa
unicolor |
1 |
- |
- |
- |
- |
- |
|
6 |
Himalayan Ghoral
Naemorhedus goral |
2 |
1400 |
250 |
200 |
78.9% (52.1–92.1) |
82.6 (57.5–94.2) |
|
7 |
Four-horned Antelop
Tetracerus quadricornis |
1 |
500 |
50 |
0 |
81.6% (24.7–97.77) |
92.1% (48.6–99.7) |
|
8 |
Wild Boar Sus
scrofa |
2 |
700 |
200 |
200 |
64.9% (16.3–88.7) |
65% (16.6%–89.2%) |
|
9 |
Wild Water Buffalo Bubalus arnee |
4 |
450 |
100 |
50 |
69.7% (11.1–93.8) |
80.07% (26.9–97.5) |
|
10 |
One-horned Rhino Rhinocerous unicornis |
3 |
200 |
50 |
50 |
56.3% (41.6–94.3) |
56.3% (41.6–94.3) |
|
|
Total |
40 |
17900 ± 2527.81 |
2600 ± 373.14 |
1850 ± 181.04 |
85.3% (80.4–89) |
89.2% (85–92.3) |
Table 4. ‘Z’ test two sample means for day 0
and day 7.
|
|
Sample size |
Treatment |
Pre-treatment Day 0 (Mean EPG ±
S.E) |
Post- treatment Day 07 (Mean
EPG ± S.E) |
‘z’ value |
p value |
|
1 |
40 |
Levamisole and Oxyclozanide |
17900± 2527.81 |
2600 ± 373.14 |
2.520991 |
0.012 |
Table 5. ‘Z’ test two sample for means of Day
0 and Day 14.
|
|
Sample size |
Treatment |
Pre-treatment Day 0 (Mean EPG ±
S.E) |
Post- treatment Day 14 (Mean
EPG ± S.E) |
‘z’ value |
p value |
|
1 |
40 |
Levamisole and Oxyclozanide |
17900± 2527.81 |
1850 ± 194.36 |
2.654587 |
0.007 |
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