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Global Journal of Medical Research: G
Veterinary Science and Veterinary Medicine
Volume 17 Issue 2 Version 1.0 Year 2017
Type: Double Blind Peer Reviewed International Research Journal
Publisher: Global Journals Inc. (USA)
Online ISSN: 2249-4618 & Print ISSN: 0975-5888
Equine Lung Worm: A Systematic Review
By Nuraddis Ibrahim
Jimma University
Abstract-
Lungworms are parasitic nematode worms of the order Strongylidae that infest the lungs of vertebrates.
Dictyocaulus arnfieldi is the true lungworm affecting donkeys, horses, mules and zebras and is found throughout the
world. Dictyocaulus arnfeildi can cause severe coughing in horses and because patency is unusual in horse (but not
in donkeys) differential diagnosis in disease due to other respiratory disease can be difficult. Adult Dictyocaulus
worms are slender, medium sized roundworms, up to 8 centimeter long. Females are about one third longer than
males. They have a whitish to grayish color. Dictyocaulus worms have a direct lifecycle, i.e. there are no intermediate
hosts involved. The pathogenic effects of lungworm depends on their location within the respiratory tract, the
number of infective larvae ingested, the animal immune status, on the nutritional status and age of the host. Despite
the prevalence of patent D. arnifieldi infection in donkeys, overt clinical signs are rarely seen; however, on close
examination slight hyperpnoea and harsh lung sounds may be detected. Diagnosis is based on clinical signs,
epidemiology, presence of first-stage larvae in feces, and necropsy of animals in the same herd or flock.
Bronchoscopy and radiography may be helpful. Larvae are not found in the faeces of animals in the prepatent or
postpatent phases and usually not in the reinfection phenomenon. ELISA tests are available in some laboratories.
Bronchial lavage can reveal Dictyocaulus arnifieldi infections in horses. The concern of lungworm in Ethiopia is
increasing and is now to be a major problem of equines. Routine deworming of horses and donkeys may help
prevent cross infection when kept together. Reducing pasture contamination with infective larvae is a key
preventative measure that can be achieved to a large extent with adequate management measures. Rotational
grazing with a change interval of 4 days and keeping the paddocks empty for at least 40 days significantly reduces
pasture contamination.
Keywords: coughing, dictyocaulus arnfeildi, lifecycle, lung, pathogenic effect.
GJMR-G Classification: NLMC Code: WA 360
EquineLungWormASystematicReview
Strictly as per the compliance and regulations of:
Equine Lung Worm: A Systematic Review
Nuraddis Ibrahim
Summary-
Lungworms are parasitic nematode worms of the
order
Strongylidae
that infest the lungs of vertebrates.
Dictyocaulus arnfieldi
is the true lungworm affecting donkeys,
horses, mules and zebras and is found throughout the world.
Dictyocaulus arnfeildi
can cause severe coughing in horses
and because patency is unusual in horse (but not in donkeys)
differential diagnosis in disease due to other respiratory
disease can be difficult. Adult
Dictyocaulus
worms are slender,
medium sized roundworms, up to 8 centimeter long. Females
are about one third longer than males. They have a whitish to
grayish color.
Dictyocaulus
worms have a direct lifecycle, i.e.
there are no intermediate hosts involved. The pathogenic
effects of lungworm depends on their location within the
respiratory tract, the number of infective larvae ingested, the
animal immune status, on the nutritional status and age of the
host. Despite the prevalence of patent
D. arnifieldi
infection in
donkeys, overt clinical signs are rarely seen; however, on
close examination slight hyperpnoea and harsh lung sounds
may be detected. Diagnosis is based on clinical signs,
epidemiology, presence of first-stage larvae in feces, and
necropsy of animals in the same herd or flock. Bronchoscopy
and radiography may be helpful. Larvae are not found in the
faeces of animals in the prepatent or postpatent phases and
usually not in the reinfection phenomenon. ELISA tests are
available in some laboratories. Bronchial lavage can reveal
Dictyocaulus arnifieldi
infections in horses. The concern of
lungworm in Ethiopia is increasing and is now to be a major
problem of equines. Routine deworming of horses and
donkeys may help prevent cross infection when kept together.
Reducing pasture contamination with infective larvae is a key
preventative measure that can be achieved to a large extent
with adequate management measures. Rotational grazing with
a change interval of 4 days and keeping the paddocks empty
for at least 40 days significantly reduces pasture
contamination.
Keywords: coughing, dictyocaulus arnfeildi, lifecycle,
lung, pathogenic effect.
I. Introduction
quines are one of the most important and mostly
intimately associated with man. They have
enormous contribution through their involvement
in different social and economic sectors. Equines play
an important role as working animals in many parts of
the world, for packing, riding, carting and ploughing.
Equine power is very crucial in both rural and urban
transport system. This is because of its cheapness and
availability and so provides the best alternative transport
means in places where the road network is insufficiently
developed and the landscape is rugged and
Author: Jimma University, School of Veterinary Medicine, Jimma,
Ethiopia. e-mail: inuraddis@yahoo.com
mountainous and in the cities where narrow streets
prevent easy delivery of merchandise (Feseha
et al.
,
1991). In Ethiopia equines have been as animals of
burden for long period of time and still render valuable
services mostly as pack animals throughout the country
particularly in areas where modern means of
transportation are absent, unaffordable or inaccessible
(Abayneh
et al.
, 2002).
In some areas of North West Kenya and
Southern Ethiopia, donkey meat is a delicacy and the
milk believed to treat whooping cough (Fred and Pascal,
2006). Even though mules and donkeys have often
been described as sturdy animals; they succumb to a
variety of diseases and a number of other unhealthy
circumstances. Among these, parasitic infection is a
major cause of illness (Sapakota, 2009). Lungworms are
widely distributed throughout the world providing nearly
perfect conditions for their survival and development but
are particularly common in countries with temperate
climates, and in the highlands of tropical and
subtropical countries
. Dictyocaulidae
are known to exist
in East Africa and South Africa (Hansen and Perry,
1996).
Dictyocaulus arnfieldi
is the true lungworm
affecting donkeys, horses, ponies and zebras and is
found throughout the world (Smith, 2009). Donkeys and
their crosses (Mules) are the natural hosts for lungworm
and the condition in horses is usually found in those that
have been in the company of donkeys and mules (Rose
and Hodgson, 2000). This review article supports
researchers to more understand the equine lung worm
disease and factors influencing the disease occurrence
under Ethiopian condition. It also helps policy makers to
draw sound decisions in order to improve the control
policy. The review paper gives information to farmers
and cattle rearing people regarding equine lung worm
disease.
And therefore, the objectives of this paper are to
give background information on the disease and
recommend modern control measures.
II. Definition and Etiology of
Lungworm
Lungworms are parasitic nematode worms of
the order
Strongylidae
that infest the lungs of
vertebrates. The taxonomy of this parasite is belonging
to kingdom
Animalia
, phylum
Nematode
, class
Secernentea
, family
Dictyocaulidae
, genus
Dictyocaulus
E
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and species of
Dictyocaulus arnfieldi
(Johnson
et al.,
2003). An infection of lower respiratory tract, usually
resulting in bronchitis or pneumonia can be caused by
several parasitic nematodes, including
D. viviparous
in
cattle and deer;
D. arnfeildi
in horses and donkeys;
D.
filaria
,
Protostrongylus rufescens,
and
Mullarius
capillaries
in sheep and goats;
Metastrongylus apri
in
pigs;
Filaroides (Oslerus) osleri
in dogs; and
Aelurostrongylus absrtusus
and
Capillaria aerophila
in
cats, other lungworm infection occur but less common
(Fraser, 2000).
Dictyocaulus arnfieldi
is the true lungworm
affecting donkeys, horses, mules and zebras and is
found throughout the world (Smith, 2009). It is a
relatively well adopted parasite of donkeys but tend to
be quite pathogenic in horses, where this parasite is
endemic (Bowman, 2003).
The first three lungworm listed above belong to
superfamily
Trichostrongylidea
and have direct life cycle;
others belong to
Metastrongylidea
and, except F
.osleri
and
C.aerophila
have indirect life cycle. Diseases
caused by the three
Dictyocaulus
species are of most
economic importance. The cattle lungworm
Dictyocaulus viviparous
is common in Northwest Europe
and is the cause of severe outbreaks of “husk” or
“hoose” in young grazing cattle. The lungworm of sheep
and goat,
Dictyocaulus filarial
is less pathogenic but
does cause losses especially in Mediterranean
countries, although it also recognized as a pathogen in
Australia, Europe and North America.
Dictyocaulus
arnfeildi
can cause severe coughing in horses and
because patency is unusual in horse (but not in
donkeys) differential diagnosis in disease due to other
respiratory disease can be difficult.
Mullarius capillaries
present worldwide and, while usually nonpathogenic in
sheep, can cause severe signs in goats. Other
lungworm infections generally cause occasional
sporadic infection on many species in many countries
(Fraser, 2000)
III. Morphology of
Dictyocaulus
Arnfieldi
Adult
Dictyocaulus
worms are slender, medium
sized roundworms, up to 8 centimeter long. Females are
about one third longer than males. They have a whitish
to grayish color. As in other roundworms, the body of
these worms is covered with a cuticle, which is flexible
but rather tough. The worms have a tubular digestive
system with two openings, the mouth and the anus.
They also have a nervous system but no excretory
organs and no circulatory system, i.e. neither a heart nor
blood vessels. The female ovaries are large and the uteri
end in an opening called the vulva. Males have a
copulatory bursa with two short and thick spicules for
attaching to the female during copulation. The eggs of
Dictyocaulus arnfieldi
are approximately 60x90
micrometers. They have an ovoid shape and contain a
fully developed L1 larva (Junquera, 2014).
Figure 1:
Egg of
Dictyocaulus arnfieldi
Source: (http://www.studyblue.com)
Lungworm larvea are slender and 25 to 70
millimeters long. The
D. arnfeildi
larvae resemble those
of
D
.
viviparous
but the tail ends in a small spine (Fraser,
2000).
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Figure 2:
Larva of
Dictyocaulus arnfeildi
Source: (http://www.studyblue.com)
a)
Epidemiology
The epidemiology of lungworm disease is
largely concerned with factors determining the number
of intensive larvae on the pasture and the rate at which
they accumulate. The third stage larvae are long living in
damp and cool surroundings. Warm and wet summers
give rise to heavier burdens in the follow autumn and
spring. Horses are not the favorite host of this parasite
and do not usually transmit the disease to other horses.
In most instances, horses acquire this disease when
pastured with donkeys (Blood
et al.
, 1999).
Under optimal condition the larvae may survive
in the pasture for a year. They are quite resistant to cold
although it generally delays their maturations. They can
withstand temperature of 4-5 degree Celsius; Larvae
can over winter in cold climates (Blood
et al.,
2000).
Most outbreak of verminous pneumonia occur during
cool season specially autumn and early winter because
the larvae stages of the causative worms tolerate and
prefer low temperatures (Hansen and Perry, 1996).
The natural host of the parasite is donkey, and
comparably, large numbers of parasites can accumulate
in the lungs of this host without clinical signs. Donkeys
and mules can act as a reservoir for horses (Beelitz
et
al.,
1996).
Pilobolus
fungi may play a role in the
dissemination of
D. arnifieldi
larvae from faeces, as
D.
viviparus. D. arnfieldi
is found worldwide, particularly in
areas with heavy rainfall (Urquhart
et al
., 1999).
b)
Life Cycle
The detailed life cycle is not fully known, but is
considered to be similar to that of bovine lungworm
,
Dictyocaulus viviparus
except in the following respect.
The adult worms are most often found in the small
bronchi and their eggs, containing the first stage larvae,
hatch soon after being passed in the faeces (Urquhart
et
al
., 1999).
Dictyocaulus
worms have a direct lifecycle, i.e.
there are no intermediate hosts involved. Adult females
lay eggs in the airways of infected hosts. These eggs
are transported to the pharynx within respiratory
secretions. From the pharynx these eggs are coughed
out, into the mouth to be swallowed or directly to the
outside. Those that are swallowed release the L1 larvae
in the gut, which are shed in the faeces. Once in the
environment, L1-larvae develop to infective L3 larvae in
about 1 week. These larvae show a low motility and
remain close to the droppings. Animals become
infected mainly while grazing, but infection can also
happen indoors through contaminated hay or bedding.
Once ingested and in the host's gut infective larvae
penetrate into the gut's wall and reach the lymphatic
nodules where the molt to L4 larvae. Through the
thoracic duct and the jugular vein they reach the heart
and are pumped to the lungs. Once in the lungs they are
stopped in the lung capillaries, cross their wall and
reach the bronchioles, bronchi or the trachea where they
complete development to adult worms. The prepatent
period (time between infection and first larvae shed with
the faeces) lasts about 4 weeks. However, larvae in the
lungs may become arrested (dormant, hypobiotic,
inhibited) for up to 5 months. These larvae resume
development at early spring and re-infect the pastures
during the next season (Junquera, 2014).
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Figure 3:
The lifecycle of
Dictyocaulus arnfieldi
Source: http://www.merial.ph/SiteCollectionDocuments/equine
c)
Pathogenesis
The pathogenic effects of lungworm depends
on their location within the respiratory tract, the number
of infective larvae ingested, the animal immune status,
on the nutritional status and age of the host (Blood
et
al.,
1989; Fraser, 2000). Larvae migrating through the
alveoli and bronchioles produce an inflammatory
response, which may block small bronchi and
bronchioles with inflammatory exudates. The bronchi
contain fluid and immature, latter adult worms and the
exudates they produce also block the bronchi.
Secondary bacterial pneumonia and concurrent viral
infections are of the complication of Dictyocaulosis
(Howard, 1993). The major pathologic changes which
results from primary infection may be divided into three
stages. These are the prepatent stages, where blockage
of small bronchi and bronchioles by eosinophilic
exudates produced in response to the developing and
migrating larvae. The patent stage, when adult worms
cause bronchitis and primary pneumonia development
occurs. The post patent phase is when adult worms are
expelled and majority of animals gradually recover. The
pathological changes seen in the lungs during necropsy
are atelectasis, emphysema, petechial hemorrhage and
lung consolidation (Aiello and Mays, 1998).
d)
Clinical Signs
Despite the prevalence of patent
D. arnifieldi
infection in donkeys, overt clinical signs are rarely seen;
however, on close examination slight hyperpnoea and
harsh lung sounds may be detected. This absence of
significant clinical abnormality may be partly a reflection
of the fact that donkeys are rarely required to perform
sustained exercise. Infection is much less prevalent in
horses. However, patent infections may develop in foals
and these are not usually associated with clinical signs.
In older horses infections rarely become patent but are
often associated with persistent coughing and an
increased respiratory rate (Urquhart
et al
., 1999).
Donkeys usually show no disease signs and can be
silent carriers and shedders of this parasite, which
causes clinical signs in horses (Johnson
et al.,
2003).
e)
Diagnosis
Diagnosis is based on clinical signs,
epidemiology, presence of first-stage larvae in feces,
and necropsy of animals in the same herd or flock.
Bronchoscopy and radiography may be helpful. Larvae
are not found in the faeces of animals in the prepatent
or postpatent phases and usually not in the reinfection
phenomenon. ELISA tests are available in some
laboratories. Bronchial lavage can reveal
Dictyocaulus
arnifieldi
infections in horses (Stuart, 2012).
Verminous pneumonia is easily confused
clinically with bacterial bronchopneumonia, with acute
and chronic interstitial pneumonia, and with viral
pneumonia. The disease usually occurs in outbreak
form in summer and autumn (Blood
et al.,
1999). The
diagnostic methods of lungworms are described as the
following ways in details.
f)
Clinical Diagnosis
Typical signs and symptoms are heavy
coughing (often paroxysmal), accelerated and/or difficult
breathing and nasal discharge. Affected animals lose
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appetite and weight. Severe infections can also cause
pneumonia (lung inflammation), emphysema (over
inflation of the alveoli), and pulmonary edema (liquid
accumulation in the airways). Adult livestock usually
develops resistance and if re-infected may not show
clinical signs but continue shedding larvae that
contaminate their environment (Junquera, 2014).
g)
Faecal Examination
A convenient method for recovering larvae is a
modification of the Baermann technique in which large
faecal samples (5-10 grams) are wrapped in tissue
paper or cheese cloth and suspended or placed in
water contained in a beaker. The water at the bottom of
the beaker is examined for larvae after 4 hours; in heavy
infections, larvae may be present within 30 minutes.
Bronchial lavage can reveal
Dictyocaulus arnfieldi
infections in horses (Stuart, 2012).
h)
Serological Diagnosis
Enzyme Linked Immuno Sorbent Assay (ELISA)
test can demonstrate antibodies from five weeks after
the animals have been exposed and it may be useful in
identifying infected animals when heavy burdens of
worms do not generate and larvae in the feces. This
time need to perform an ELISA depends on the
availability of antigen-coated microstate-plates. If such
plates can be provided; the result can be obtained
within four hours after the serum has been prepared. If
not, plates have to be coated with antigen for up to 16
hours (Boon
et al.,
1984).
IV. Necropsy Findings
The morphological change in the lungs include
wide spread areas of collapsed tissue of dark pink color,
hemorrhagic bronchitis with much fluid filling all the air
passed and enlargement of the regional lymph nodes.
Histologically, the characteristic lesions are edema,
eosinophilic infiltration, debris and larvae in the
bronchioles and alveoli. The most obvious lesions at
necropsy are discrete patches of over inflation. The
bronchial epithelium is hyperplasic and heavily infiltrated
by inflammatory cells, particularly eosinophils (Reinecke,
1989).
Figure 4:
Necropsy finding of
Dictyocaulus arnifieldi
in lung of horse
Source: Staurt (2012)
a)
Differential Diagnosis
On a clinical basis, bacterial pneumonia is
considered as the first tentative diagnosis. Other
probable tentative diagnoses are considered such as
chronic hypersensitivity pneumonitis, chronic obstructive
pulmonary disease, fungal pneumonia, immune
mediated interstitial or vascular disease and unusual
drug reactions as well as foreign body in the trachea
(Burks, 1998).
b)
Control and Preventions
Routine deworming of horses and donkeys may
help prevent cross infection when kept together.
Pastures that housed donkeys may be infected with
lungworm larvae. As a result, horses and donkeys
should not be grazed together (Johnson
et al.,
2003).
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Reducing pasture contamination with infective
larvae is a key preventative measure that can be
achieved to a large extent with adequate management
measures. Rotational grazing with a change interval of 4
days and keeping the paddocks empty for at least 40
days significantly reduces pasture contamination. This is
due to the fact that larvae are susceptible to dryness
and won't survive more than 4 or 5 weeks on pasture if
they do not find an adequate host. Obviously, by very
moist weather or where pastures are almost
permanently moist survival may be longer. Alternate
grazing with sheep and/or horses may be considered,
since
Dictyocaulus
species are quite host-specific (for
cattle, sheep & goats, horses). The longer the absence
of the specific host, the higher
will be the reduction of its
specific lungworm. However, this may not be advisable
in places infected with gastrointestinal roundworms that
are simultaneously parasitic of cattle and sheep or
horses. For their first grazing season it is highly
advisable that young stock does not share the pastures
with older stock that has been exposed earlier to
infected grounds and can therefore shed larvae. It must
also be avoided that young stock uses pastures already
used by older stock during the same season. It must
also be considered that heavy rains and flooding can
disseminate infective larvae inside a property or from
one property to neighboring ones. Keeping the pastures
as dry as possible and keeping livestock away from
places excessively humid are additional key measures
to reduce the exposure of livestock to infective larvae. In
endemic regions preventative strategic treatment of
young stock is often recommended just prior to their first
grazing season, followed by additional treatments
depending on the infestation level of the pastures and
the residual effect of the administered anthelmintic
(Junquera, 2014).
Table 1:
Different modern broad-spectrum anthelminthic drugs currently used against Lungworm
Drug groups Anthelminthic drugs Dose (mg/kg) Routs of administration
Macrolides Ivermectin 0.05 PO and SC
Benzimidazole Oxfendazole 2.5 PO
Fenbendazole 5.0 PO
Albendazole 7.5 PO
Febantele 10 PO
Imidathiazole Levamisole 8.0 PO
Source: Blood et al. (2000)
c)
Economic Impact of the Disease
The vitality and wellbeing of horses of all age
are thread by a variety of internal parasites and the use
of control ensures and the best performance (Power,
1992). Internal parasites are one of the greatest limiting
factors to successful horse rising throughout the world.
All horses at pasture become infected and suffer a wide
range of harmful effects ranging from impaired
development and performance to death despite the
availability of large array of modern anthelmintic,
parasite controls often fail to safeguard horse health.
The main reason for these break downs are errors the
choice of anthelmintic and in the time of treatment
(Herd, 1987).
d)
Prevalence of lungworm infection in different parts
of Ethiopia
The concern of lungworm in Ethiopia is
increasing and is now to be a major problem of equine
in the central highlands of Ethiopia. However there were
little preliminary findings of lungworm infection which
were done by few researchers of the country (Table 2).
Table 2:
Prevalence of lungworm infection in different parts of Ethiopia
S. No- Site of study Prevalence in % Researcher name
2 North Wollo 17.5 Belay, 2005
4 Jimma 13.8 Tihitna et al., 2012
5 South eastern Ethiopia 42.7 Kamil et al. (2017)
V. Conclusion
Dictyocaulus arnfieldi
is the true lungworm
affecting donkeys, horses, ponies and zebras and is
found throughout the world. The natural host of the
parasite is donkey, and comparably, large numbers of
parasites can accumulate in the lungs of this host
without clinical signs. Donkeys and mules can act as a
reservoir for horses. The epidemiology of lungworm
disease is largely concerned with factors determining
the number of intensive larvae on the pasture and the
rate at which they accumulate. The third stage larvae are
long living in damp and cool surroundings. Warm and
wet summers give rise to heavier burdens in the follow
autumn and spring. Pastures that housed donkeys may
be infected with lungworm larvae. As a result, horses
and donkeys should not be grazed together. In endemic
regions preventative
strategic
treatment
of
young
stock
is often recommended just prior to their first grazing
season, followed by additional treatments depending on
the infestation level of the pastures and the residual
effect of the administered anthelmintic.
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Global Journal of Medical Research Volume XVII Issue II Version I
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Equine Lung Worm: A Systematic Review
