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Abstract

Oestrus ovis, the sheep 'nasal bot fly', somewhat looks like a honey bee, has a rudimentary mouth parts and do not feed. The larva of the sheep nasal fly is responsible for causing a condition in sheep and goat called nasal myiasis, oestriosis or 'false gid'. The disease occurs when adult fly deposit first larvae (L1) into the nostrils of its host. The larvae develop into L2 and L3 in the nasal cavities and sinuses in due course. Sneezing and nasal discharges are the major clinical signs seen in infected animals. The pathogenic reaction occurs when the larvae irritate the mucosa with their spines and hooks during their development and also due to an allergic reaction induced by molecules excreted/secreted by the larvae. Sometimes damage of the skulls of the bones and injury to the brain occur to such an extent that signs of high-stepping gait and in-coordination suggesting the animal suffers from Coenurus cerebralis infection and hence the infection is also called false gid. Keeping in view the importance of the fly, the morphology, biology, pathogenesis, immunological reaction and various control measures of Oestrus ovis are discussed in this review.
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Nasal Myiasis in animals due to Oestridae - A
Mini Review
Gautam Patra1*, Papia Biswas2, Ana Sahara3, Parthasarathi Behera4,
Subhamoy Ghosh1, Ajit kumar4, S.K. Borthakur1, Seikh Sahanawaz Alam5,
and Apurba Debbarma6
1Department of Veterinary Parasitology; 2Department of Veterinary Public Health and Epidemiology; 3Department of
Veterinary Parasitology, Gadjah Mada University, Yogyakarta, Indonesia.
4Department of Veterinary Parasitology; WBUAFS, Kolkata-37, West Bengal, India.
5District Microbiologist, Malda Medical College & Hospital, Malda, West Bengal, India.
6Department of Veterinary Parasitology, College of Veterinary Sciences & Animal Husbandry, R.K. Nagar, Agartala,
Tripura, India.
*Corresponding author: Gautam Patra, Department of Veterinary Parsitology, College of Veterinary Sciences and Animal
Husbandry, Selesih, Aizawl, India. Tel: +91 8582859415; E-mail: dr.gautampatra@yahoo.co.in
Abstract Oestrus ovis, the sheep ‘nasal bot fly’,
somewhat looks like a honey bee, has a rudimentary
mouth parts and do not feed. The larva of the sheep nasal
fly is responsible for causing a condition in sheep and
goat called nasal myiasis, oestriosis or ‘false gid’. The
disease occurs when adult fly deposit first larvae (L1) into
the nostrils of its host. The larvae develop into L2 and L3
in the nasal cavities and sinuses in due course. Sneezing
and nasal discharges are the major clinical signs seen in
infected animals. The pathogenic reaction occurs when
the larvae irritate the mucosa with their spines and hooks
during their development and also due to an allergic
reaction induced by molecules excreted/secreted by the
larvae. Sometimes damage of the skulls of the bones and
injury to the brain occur to such an extent that signs of
high-stepping gait and in-coordination suggesting the
animal suffers from Coenurus cerebralis infection and
hence the infection is also called false gid. Keeping in
view the importance of the fly, the morphology, biology,
pathogenesis, immunological reaction and various
control measures of Oestrus ovis are discussed in this
review.
Keywords Oestrus ovis; morphology; biology;
immunopathology; control measures.
I. INTRODUCTION
Oestrus ovis which is commonly called ‘sheep nasal fly’
or ‘nas al bot fly’, is res pons ible for s evere economic
losses in livestock across the globe (El-Tahawy et al.
2010). The larval phases (parasitic) of the fly irritate the
nasal mucosa with their spines and hooks while feeding to
support their growth and development (Cepeda-Palacios
et al. 1999; Tabouret et al. 2003). The migratory larvae
even penetrates and erode the dorsal turbinate bones,
frontal sinuses and occasionally the skull bones while
entering into the cerebral cavity causing ‘false gid’
(Taylor et al. 2016).
Human in close contact with livestock, sheep
particularly are at greater chance to become accidental
hosts for the O. ovis larvae. So the disease is also have
public health importance (Cepeda-Palacois 2001; Einer
and Ellegard 2011; Hummelen et al. 2011; Hoyer et al.
2016). Clinical signs are manifested by mucopurulent
nasal discharge, frequent sneezing and difficulty in
grazing, restlessness, incoordination and dyspnoea
(Dorchies et al. 1992; Dorchies and Alzieu 1997;
Dorchies et al. 2000). The pathogenic effects of oestriosis
are due to the damages in the nasal mucosa caused by the
cuticular spines and oral hooks but also by immunological
reactions of larval antigens (Jacquiet et al. 2005).
Important losses sue to O. ovis include upto 22% loss
body weight, 16% in wool production and 10% in milk
production (Shcherban 1973). The fly has cosmopolitan
in distribution where sheep and goats rear. They also
attack deer and occasionally horses, cattle, dogs and
human. The current method of oestriosis is based on
chemotherapy in sheep because no bait or traps are
available to control the free living adult fly (Cepeda-
Palocios and Scholl 2000b). Endectocides and fasciolicide
drugs such as closantel and nitroxynil are often used to
treat nasal myiasis in sheep and goats (Dorchies et al.
1997).
The purpose of this review is to discuss the
morphology, biology of Oestrus ovis together with
immunopathology caused by the larvae of this fly vis-à-
vis some of the controlling measures based on available
literature.
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II. MORPHOLOGY
The genus Oestrus contains four species O.
aureogentatus, O caucacicus, O ovis and O. variolasus.
O. aureogentatus and O. variolosus are found throughout
Africa, south of the Sahara and O. caucacicus is present
in domestic and wild animals of the Caucasus regions and
central Asia. However, O. ovis is found in all sheep
farming areas of the world. The adult fly is about 13-15
mm in length and grey in colour with black spots on the
thorax and abdomen and somewhat resembles a bee (Fig.
1). The whole body is covered with light brown hair. The
mouthparts are vestigial. The head is broad with small
eyes. The segments of the antennae are small and the
arista bare. They have a yellow-brown head, with small
tubercles of equal size on the thorax and the yellow legs.
They possess yellow-veined wings which have a strongly
bent M vein joining the R4+5 veins before the wing
margin. It is an obligate parasite in sheep and goats in
many parts of the world.
The tiny first-stage larvae are white or slightly
yellow in colour and spindle in shape, 1-3 mm long with
relatively large cephaloskeleton which may be seen
during post-mortem by sawing the skull in half-
longitudinally (Fig. 2). They are provided with strongly
bent sclerites (gently curved mouth-hooks) and 22-25
terminal spines arranged in two groups. The third
segment contains a row of denticles on the dorsal side.
Ventrally the segments at their anterior margins show two
to three rows of spine and hair like structures. Laterally,
they have 22-25 hooks (Zumpt 1965).
The second instar larva is white in colour and
3.5-12 mm long with few weak denticles on the dorsal
side of the second segment, the median part of the post
anal bulge is spinulose, ventrally the segments are
provided with spines, the posterior peritremes are more or
less circular, the channels are indicated by distinct suture
(Zumpt 1965).
The mature larvae are about 2-3 cm long and
brown with transverse, dorsal blackish bands. The
anterior end is somewhat tapering but the posterior
surface has a flat surface. The larvae bear large, black oral
hooks, connected to an internal cephalopharyngeal
skeleton (Fig. 3) The dorsal surface is devoid of spines
while the ventral surface bears rows of small spines and
the black stigmatic plates are circular, with a central
ecdysial scar, and without a distinct suture (Zumpt 1965).
III. PREVALENCE AND DISTRIBUTION
The prevalence and incidence are greatly varied
depending on climate and ecological factors. In temperate
countries the flies occur in late spring and summer
whereas in warm climate it can infest the sheep
throughout the year. The prevalence and distribution of
the fly is shown in Table no. 1.
Table.1: Prevalence rates of Oestrus ovis infestation in
different countries
Country
Prevalence
Rate (% )
Reference(s)
Saudi Arabia
5.5
Alahmed et al.,
2002
India
8.1
Pathak, 1992;
Godara et al., 2010
Zimbabwe
6 52
Pandey, 1989
Morocco
10 100
Paney and Ouhelli,
1984
Ethiopia
21.0
Gebremedhin, 2011;
Bekele and Mukasa-
Mugerova, 1994
Libya
22.6
Gabaj et al., 1993
France
33.2 65
Dorchies et al., 2000
Jordan
58.0
Abo-Shehada et al.,
2000
Algeria
67.4
Benakhla et al.,
2004
Spain
71.1
Alcaide et al., 2003
Italy
91.0
Caracappa et al.,
2000
Spain
27.3
Barroso et al., 2017
IV. BIOLOGY AND HABITS
The life cycle of the sheep nasal fly is shown in figure 4.
The life cycle begins when the young larvae are deposited
by the adult flies. Each female can produce up to 500
larvae. Bart and Minar (1992) reported that many L1 are
destroyed in the nasal cavities during the hypobiotic
period. After being deposited the larvae crawl onto the
mucous membrane of the nasal passage where they spend
at least two weeks and are found attached to the mucous
membrane by means of oral hooks. First stage larvae are
deposited in packages directly into the nostrils with
accurate precision. Thermo sensible cuticular sensilia and
a quick mobility of the larvae allow them to overcome the
first defence reactions such as sneezing and rubbing
against close objects (Colwell and Scholl, 1995). It has
been reported that the rate of larval establishment is 0-
48% in sheep (Frugere et al. 2000) and 29-40% in goats
(Angulo-Valadez et al. 2009). It is known that better
water economy in goats leads to len humid noses than in
sheep. This higher humidity is more conducive for larval
survival in sheep than goats (Papodopoulos et al. 2010).
Inside the host’s nos e, the larvae either continue to grow
or hibernate in response to a combination of intrinsic
rhythms and external environmental stimuli. Temperate
countries, the first stage larvae hibernate but very high
temperature slows the growth rate (Yilma and Dorchies
1991). Limited information is available about second
stage larvae. They quickly develop into the sinuses of the
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host and trigger a strong cellular reaction with infiltration
of mast cells and eosinophils. This stage relies on a high
protein diet which mainly they derive from mucus and
seroproteins by way of trypsin like enzymes (Tabouret et
al. 2003b). Finally the full grown larvae crawl out and
expelled by the sneezing of the host onto the ground
where they pupate. Under favourable environmental
conditions, the duration of the first, second and third
stages vary from 10-25 days, 7-15 days and 13-18 days,
respectively (Cepheda-Palacios 2002). Intrapuparial
metamorphosis occurs over 19-27 days before adult flies
emerge.
Adults do not bear functional mouth parts and
therefore minimize the energy loss by localizing their
potential hosts and suitable mates with their large eyes.
They are swift fliers and since they do not feed, the
lifetime of adult is short and females emerge from the
puparium bear fully developed eggs which are ready to
fertilize (Taylor et al. 2016).
V. IMMUNOPATHOLOGICAL REACTIONS
The intensity of local changes inoculated by O. ovis
larvae in the mucosa of the upper respiratory tract of the
host is not related to larvae density but Biggs et al. (1998)
suggested that any larval number above 10 is potentially
dangerous. The most significant lesions are seen in the
sinus and ethmoidal mucosa. In natural or artificial
infection, there is hyperplasia and abrasion of muco-
ciliary film (Dorchies et al. 2006). A strong cellular
response is elicited as many cells are positively marked as
Ki67 epitopes (Nguyen Van Khanh et al. 1998). Many
ultra-structural changes in the nasal sinus are due to a
combination of mechanical damage associated with
effects of secreted proteases from the larvae. These
changes increase the permeability of the mucosa allowing
the diffusion of antigenic/ excretory products through the
mucosa to come in close contact with the locally recruited
immune cells (Dorchies et al. 2006). Histopathological
data indicates pathogenesis of ovine oestrosis is due to
Type-I immediate hypersensitivity phenomenon. Many B
and T lymphocytes, phagocytic mononuclear cells
(PMC), eosinophils, mast cells and globule leucocytes
have been observed where larval moult occurs (Tabouret
et al. 2003b). Nasal myiasis also induces IgM and IgG
production in both sheep and goats (Suarez et al. 2005;
Angulo-Valadiz et al. 2008, 2009).
Clinical signs can be described into three
categories: fly strike, sinusitis and other consequences.
5.1. Fly strike
Fly activity causes great annoyance when attack sheep to
deposit larvae into the nostrils. The animals get nervous
and congregate together, keeping their noses deep inside
the fleece of the other sheep or close to the ground (Fig.
5, 6). Animals become restless and stop feeding. Goats
are less reactive because of their browsing habits (Hoste
et al. 2001).
5.2. Sinusitis
The irritation of the nasal mucosa caused by the oral
hooks and spines of the fly larvae manifests by nasal
discharge and sneezing. Sheep are agitated and the nasal
discharge occasionally become purulent tinged with blood
(snotty nose, Fig. 7). Sometimes erosion of the bone and
eventual injury to the brain with neurological signs
including ataxia, nystagmus, high stepping gaits and in-
coordination of movements may be misdiagnosed as C.
cerebralis infection. For this reason, the infection is also
called false gid.
5.3. Other consequences
In some breeds of sheep, neoplastic growth might be
found (Bergeaud et al. 1994). In some cases, interstitial
pneumonia with interstitial emphysema and pleural
adhesion has also been observed (Dorchies et al. 1993).
VI. TREATMENT AND CONTROL
The objective of the treatment is to eliminate or at least
suppression of clinical signs and to limit the extension of
the endemic zone of the parasite. Sheep already infected
with nasal bot flies can be successfully treated with
several parasiticides. Ivermectin either as injectable form
or oral drenches have excellent curative effect and gives
protection against re-infestation after several weeks of
treatment (Bowman 2014). Roncalli (1984) reported that
larvae of O. ovis are highly susceptible to ivermectin at a
dose rate of 0.2 mg/Kg body weight. The efficacy of
eprinomectin at with 0.5 mg/Kg and 1 mg/Kg body
weight ranges from 83.5 100% (Hoste et al. 2004;
Habela et al. 2006).
Anthelmintics which are commonly used against
nasal bots include closantel nitroxynil and rafoxanide.
Closantel have a persistent effect on larvae and can give
protection to animals from reinfestation during fly season
(Dorchies et al. 1997).
Enhanced immune responses may have a
detrimental effect on O. ovis larvae led to immunological
trials against O. ovis in sheep using excreted/secreted
products and digestive tract protein extracts of third
instars by previous works (Frugere et al. 2000; Angulo-
Valadez et al. 2007). It was predicted that immunized
animals would develop humoral responses against such
antigens. The authors concluded that a reduction of 40%
mature larvae weight would reduce 38% adult population.
Further experiment is required to ascertain whether such
immunization can affect the adult population
significantly.
The more general control measure includes
feeding in narrow troughs, the edges of which are
smeared with tar. This automatically tars the animals and
thus acts as a repellent (Bowmann 2014).
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ACKNOWLEDGEMENT
The authors are thankful to the Dean, College of
Veterinary Sciences and Animal Husbandry, Central
Agricultural University, Selesih, Aizawl, India for
providing necessary support.
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Figures:
Fig.1: Adult O. ovis fly (Anon, 2018)
Fig.2: Third stage larvae of bot fly in nasal sinus
(Anon, 2018)
.
Fig.3: Cephalopharyngeal skeleton of O. ovis
larvae (Anon, 2018)
Fig.4: Schematic diagram of O. ovis life cycle (Anon,
2018)
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Fig.5: O. ovis infested sheep (Anon, 2018)
Fig.6: Depression in a sheep due to false gid (Mozaffari
et al., 2013)
Fig.7: snotty nose (Anon, 2018)
... Larvae pass through three stages or instars. 6 The female O. ovis fly is viviparous and deposits L1 in or around the nostrils. Inside the nasal cavities, the first instar larvae attach to the mucous membrane, change to second instars, move up to the sinuses and molt to L3. ...
... 2,5 Oestrus ovis is a problem for sheep and goats worldwide. 6 Both adult and larval stages have an effect on the host. The activities of adult flies during the deposition of larvae cause annoyance, which results in loss of body condition. ...
... Larvae sometimes migrate into the brain of sheep and cause in coordination called "false gid". 4,6 Oestrosis in small ruminants causes substantial economic losses to sheep and goat producers. 6,7 The pathogenic effects cause a reduction in production and serious economic losses, which have been estimated at 1.1-4.6 kg of meat, 200-500 g of wool, and up to 10% of milk per animal. ...
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Background: Ovine oestrosis is an economically important and widely distributed parasitic disease of sheep that is caused by Oestrus ovis larvae across the world. Despite the fact that Oestrus ovis is a common parasite in Ethiopia and that there are many sheep in the study area, there is no information on the prevalence, larval burden, predilection sites, and risk factors associated with Oestrus ovis infestation in sheep in the Dendi district of West Shewa Zone, Ethiopia. Methods: A cross-sectional study was conducted from November 2017 to April 2018, to estimate the prevalence, risk factors, and larval burden, and identify common predilection sites for Oestrus ovis larvae. A total of 180 sheep heads were randomly selected from five purposely selected restaurants in Ginchi town, Dendi district, transported to the laboratory, opened with a hand saw, and visually examined for infestations. The larvae were collected from positive sheep heads and counted. The sites where the larvae were obtained were recorded. The data were analyzed using SPSS version 20 software. Results: Of the total of 180 examined sheep heads, 104 (57.8%) were infested with larvae of Oestrus ovis. In the study, a statistically significant difference (p > 0.05) was not observed in the prevalence of Oestrus ovis in relation to all considered risk factors such as sex, age, and origin of sheep. From 104 infested sheep, a total of 664 larvae were detected in different parts of sheep heads. The mean larval intensity per infected animal with Oestrus ovis was 6.38. In this study, the minimum and maximum numbers of larvae recovered were 1 and 26, respectively. The nasal cavity, nasal sinus and frontal sinus were the predilection sites of Oestrus ovis larvae identified in this study. Conclusion: Oestrosis is an important and common parasitic disease of sheep in the study area.
... Afterward, Myiasis abscess in the lungs leads to starvation that might cause death (Kamal et al., 2021a,b). Occasionally, larvae move from frontal sinuses and nasal cavity to the brain leading to false gid (Patra et al., 2018). Ultimately the pathogenic effects lead to considerably less animal production and significant economic losses to the agricultural industry as estimated roughly as 200-500 gm of wool, 1.1-4.6 kg of meat, and up to 10 % milk per animal (El-Tahawy et al., 2010;Ipek, 2018). ...
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The study was planned to evaluate the inter, and intra population genetic variation in general protein banding pattern in Oestrus ovis larvae, by using 10% sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS PAGE). The larvae were collected from slaughtered goats head from five different locations (AAS, PN, LA, GM, and BC) of Karachi, Pakistan. The data obtained was subjected to POPGENE (Population Genetic Analysis) software for analysis. The polymorphic loci within populations ranged from 45.45% to 90.91%. Polymorphic loci observed in all populations were 90.91%. The expected heterozygosity observed was 0.181±0.096 in all populations. The chi-square test showed 5 out of 11 loci at H-W equilibrium. The overall fixation index (FST) value was 0.108, showing that the likelihood of subpopulations being differentiated from one another is about 11 percent. The gene flow value (Nm=2.065) was higher, showing that genes flow occurs between populations. The values of genetic identity were greater, and genetic distance was smaller among all the populations. It means that all the populations were more alike and closer to each other. It was concluded that there was no sympatric and parapatric population differentiation observed among all the population of O. ovis. The populations of the five different locations were not genetically and reproductively isolated from each other.
... Furthermore, this disease can be complicated by sensual tumors and lung abscesses, and sometimes this infection leads to starvation, which might cause death (Dorchies et al., 1993;Özdal et al., 2016). Occasionally, the larvae from frontal sinuses and nasal cavity may move into the brain leading to false gids (Patra et al., 2018). ...
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