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An epidemiological study on prevalence of Goat Warble Fly Infestation (GWFI) in Punjab Province, Pakistan.



An epidemiological study on prevalence of Goat Warble Fly Infestation (GWFI) in Punjab Province, Pakistan.
The purpose of the present study was to determine the prevalence of Warble Fly Infestation (WFI) in goats of Punjab Province, Pakistan.
Goat warble y infestation is caused by Przhevalskiana silenus (Diptera: Oestridae). There were a total of five hundred animals examined from
July 2012 to January 2013 from Khoshab and Chakwal districts of Punjab province for the prevalence of warble. The larvae were collected
from the infested goats and identified as P. silenus. The results showed that the prevalence of GWFI was 17.8% (89/500). The number of
nodules in the infested animals ranged from 1-14 (6.61±2.4). The breed wise prevalence was in beetle breed (13.2%), local breed (18%) and
desi breed (22.9%), respectively. The sex wise prevalence was in male (15.3%) and in female (19.4%). The prevalence based on age showed
that the rate of infestation in animals having age group (1-3 year) was 20.9%, (4-6 year) was 14.6% and (>6 year) was18.1%, respectively. The
present study showed that these epidemiological factors have a significant eect on the prevalence of WFI in goats of Punjab Province. The
results showed the eect of dierent treatments given to animals on the basis of sex, age groups, infested and non-infested animals. The
results of this survey showed that the y is active from March to June. It was first study on GWFI in Punjab Province; northern part of Pakistan.
It would be very helpful in devising the future strategies towards the eradication and control of warble y in other endemic areas of Pakistan.
Keywords: Goat Warble Fly Infestation, GWFI, Prevalence, Przhevalskiana silenus, Khoshab, Chakwal districts, Pakistan
Pakistan Punjab Eyaletindede Keçi Nokra Enfestasyonunun
Prevalansı Üzerine Epidemiyolojik Bir Çalışma
Bu çalışmanın amacı Pakistan’ın Punjab Eyaletinde Keçi Nokrasının prevalansını tespit etmektir. Keçi Nokrası Przhevalskiana silenus
(Diptera: Oestridae) tarafından meydana getirilir. Prevalansın tespiti amacıyla Punjab’ın Khoshab ve Chakwal bölgelerinde Temmuz 2012
ile Ocak 2013 tarihleri arasında toplam 500 adet hayvan incelendi. Larvalar enfekte keçilerden toplandı ve P. silenus olarak identifiye edildi.
Keçi Nokrasının prevalansı %17.8 (89/500) olarak tespit edildi. Hayvanlardaki nodüllerin sayısı 1-14 (6.61±2.4) olarak belirlendi. Türlere göre
prevalans beetle ırkında %13.2, lokal ırklarda %18 ve desi ırklarda %22.9 olarak tespit edildi. Tekelerde prevalans %15.3 iken dişilerde %19.4
idi. Enfestasyon; 1-3 yaş arası keçilerde %20.9, 4-6 yaş arası olanlarda %14.6 ve 6 yaş üzerilerde %18.1 oranlarında mevcuttu. Araştırılan
epidemiyolojik faktörlerin Punjab Eyaletinde Keçi Nokrasının prevalansı üzerinde önemli etkisi olduğu tespit edildi. Çalışmanın sonuçlarına
göre nokranın Mart ayından Temmuz ayına kadar aktif olduğu belirlendi. Bu çalışma Keçi Nokrası üzerine Punjab Eyaletinde yapılan ilk
çalışmadır. Çalışmanın Pakistan’ın diğer endemik bölgelerinde nokranın eradikasyonu ve kontrol edilmesine yönelik stratejileri belirlemede
yararlı olacağı görüşündeyiz.
Anahtar sözcükler: Keçi Nokra Enfestasyonu, GWFI, Prevalans, Przhevalskiana silenus, Khoshab, Chakwal bölgeleri, Pakistan
An Epidemiological Study on Prevalence of Goat Warble Fly
Infestation (GWFI) from Punjab Province, Pakistan
Mohammad ARSHAD 1 Farzana SIDDIQUE 3 Shahtaj AHMAD 1 Irfan MUSTAFA1
Muhammad Farooq NASIR 3 Pervez ANWAR 3 Saira ASIF 3 Mobushir Riaz KHAN 4
Muneeb HUSSAIN 5 Haroon AHMED 2
Department of Biological Sciences, University of Sargodha, Sargodha - PAKISTAN
Department of Biosciences, COMSATS Institute of Information Technology, Park Road, 46300, Islamabad - PAKISTAN
Pir Mehr Ali Shah, Arid Agriculture University, Shamsabad, Muree Road Rawalpindi - PAKISTAN
Institute of Space Technology, Near Rawat Toll Plaza, Islamabad Express Way, Islamabad - PAKISTAN
Animal Health Institute, Animal Health Program, NARC, 46300 Islamabad - PAKISTAN
Makale Kodu (Article Code): KVFD-2013-9402
Pakistan is an agricultural country and livestock acts as
the backbone of agriculture. Milk, meat, hides and wool
obtained from the livestock help to increase the export of
Pakistan as well as prosperity of the farmer.
İleşim (Correspondence)
+09251 9290267
Journal Home-Page:
Kafkas Univ Vet Fak Derg
20 (1): 35-40, 2014
DOI: 10.9775/kvfd.2013.9402
An epidemiological Study on ...
Parasitism is one of the major problems of low
productivity in livestock sector of the world [1]. One of these
is WFI, which cause infection in cattle, bualoes, sheep and
goats [2-4]. Hypodermosis prevalence is common in semi-
hilly, mountainous and riverine areas of Pakistan [3]. Due to
its high prevalence, it exists in many parts of the world. It
was found that the prevalence of warble y infestation was
almost 80% in Czech Republics, 49.2% in Greece, 85% in
Italy, 52.3% in Spain, 40% in United Kingdom and 32-43%
in Romania [5]. The prevalence of Warble Fly Infestation
(WFI) was 3.2%, 18.4% in bualo and cattle of Pakistan [6,7].
Previous studies showed that hypodermosis is one of
the major parasitic infection in many countries of the
northern hemisphere. This menace not only causes the
physical damage to the animal, but also aects the internal
organs and damages the host immune system. In many
European and North American countries, chemotherapy
treatments used against adult y and first larval stage,
have significantly reduced the infestation of this disease [8].
The infestation rate was in cattle (14.1%), sheep (2.1%) and
goats (24.9%) respectively in Green mountains, Libya. The
goats were infested by P. silenus [9]. The adult y is active
from April to June in dierent areas of world. The adult y
lacks mouthparts and survives on resources accumulated
during the larval period. During the periods that the
y is active, the first instar larvae emerge from eggs laid
directly on the hairs of the hind legs (mainly tarsal and
femoral regions) of the goat. The larvae then penetrate
the epidermis and dermis to enter into the subcutaneous
tissue to migrate for a short distance to reach the anks and
sacrum. The migration pattern inside the body of animals
seems to be exclusively subcutaneous [10,11]. Leather industry
is one of the major industrial units working in Pakistan and
producing large export products but, due to this parasite,
this industry is suering from economic losses. The losses
due to this menace cannot be calculated due to a number
of factors, while hide damage was the most important
consequence of the infestation resulting in low price
on account of holes formed by the warble y. Pakistan
produces 7.5 million hides and 36.3 million skins, annually.
The estimated losses in D. G. Khan and Rajanpur districts
were Rs: 12.9, 9.9 million, respectively. The total losses were
Rs 22.8 million from cattle and Rs 2.2 million from
buffaloes [12]. Although Pakistan is an agricultural
land having a large number of livestock; warble fly is
continuously attacking the livestock products but no
important work has been done in this regard to calculate
damage caused by this notorious parasite.
The purpose of present study is to determine
the prevalence of Warble Fly Infestation (WFI) in district
Khoshab and Chakwal of Punjab province, Pakistan. The
objectives of the present were (1) Treatments given to
dierent animals in dierent herds and their eectiveness.
(2) Sex & breed wise prevalence of Warble Fly Infestation
(WFI) in goats of different areas of Punjab Province
(Khoshab and Chakwal).
Punjab is the Pakistan’s second largest province at
205.344 km2 (79.284 sq2 miles) after Balochistan and is
located at the northwestern edge of the geologic Indian
plate in South Asia. The geographical location of the
Chakwal is 32° 56’ 0” North, 72° 52’ 0” East and of Khoshab
is 32° 17’ 48” North, 72° 21’ 9” East in Punjab Province,
The Punjab province is bordered byKashmir(Azad
Kashmir, Pakistan and Jammu and Kashmir, India) to the
north-east, the Indian states of Punjab and Rajasthan to
the east, the Pakistani province of Sindh to the south,
the province of Baluchistan to the southwest, the province
of Khyber Pakhtunkhwa to the west, and the Islamabad
Capital Territory to the north. Undivided Punjab is home
to six rivers, of which five ows through Pakistani Punjab.
From west to east, these are: theIndus, Jhelum, Beas,
Chenab,RaviandSutlej. Nearly 60% of Pakistan’s population
lives in the Punjab. It is the nation’s only province that
touches every other province; it also surrounds the federal
enclave of the national capital city atIslamabad. This
geographical position and a large multi-ethnic population
strongly inuence Punjab’s outlook on National aairsand
induces in Punjab a keen awareness of the problems of
the Pakistans other important provinces and territories.
The landscape is amongst the most heavily irrigated on
earth andcanalscan be found throughout the province.
Weather extremes are notable from the hot and barren
south to the cool hills of the north. The foothills of
theHimalayasare found in the extreme north as well.
The habitat of the warble fly is hilly and semi-hilly
areas. According to it those areas are selected that have
hilly or semi hilly conditions like Chakwal and Khoshab.
These areas have suitable temperature conditions and
other ecological factors like high altitudes that are ideal for
the growth and development of the warble y. Moreover;
these areas also have large number of livestock that help
to further increase the living conditions and host of the
warble y.
Experimental Design
This epidemiological survey was conducted from
September, 2012 to March, 2013. These months are
selected because warbles present on the back of the
animals start developing from September and last till
February. The larvae were collected from infested animals.
Palpation Method
The animals of these areas were examined on monthly
basis by palpation method. The nodules were counted by
using visual and hand palpation method. The counting of
nodules on animal started from anterior portion leading
to the posterior portion. The animals were examined
on monthly basis to count the numbers of nodules and
all this was recorded on a separate data sheet. Initially
some of the larvae were directly collected from the upper
dorsal part of the animal near the vertebral column. These
were collected with the help of hands. The larvae were
collected by picking them from the ground, when they
dropped. The larvae from animal skin dropped on the
ground during the months of January to onward to form
mature y which starts the life cycle again. So during
these months (February, March) larvae are collected from
the ground instead of animal skin directly. The larvae
were collecting in bottle containing 70% ethanol and
kept in freezer at -20°C.
Statistical Analysis
The Statistical analysis (Chisquare) was done by using
the statistical package SPSS for Windows 20.0.
Out of
five hundred goats
were found to be
infested by Przhevalskiana silenus.
of nodules
in the infested animals ranged from 1-14
(6.61±2.4). The
nodules were observed on the back of infested goats.
warble started to appear by the start of September
skin perforation started from end of October to
larvae collected from infested goats were
as P. silenus according to Zumpt [
silenus in goats of Khoshab and Chakwal district,
Pakistan (Fig. 1).
The present study was conducted in 10 villages, 40
herds of Khoshab and Chakwal district to determine
the prevalence of warble y infestation in the goats from
July 2012 to January 2013. The results of present study
revealed that the rate of infestation was 17.8% (89/500).
The village wise prevalence was determined from the
ten villages. The prevalence in villages of Khoshab district
as in Dhokri (12.7%), Ghatti (13.2%), Jabbi sharif (9.1%),
Warcha (0%) and Chohasharif (6.7%). In district Chakwal
it was in village Manara, (25.5%), Runsial, (34.9%), Bhone,
(30%), Tala gang, (14.3%) and Choa Saidan shah, (9.1%). The
statistical analysis has showed the significant dierences
(P<0.05) in the prevalence of GWFI in dierent villages of
Punjab Province, Pakistan.
The goats of three breeds (Beatle, Desi breed and local
breed) were examined in the present study on monthly
basis. The statistical analysis shows that prevalence in
beetle breed was (13.2%), local breed (18%) and desi breed
(22.9%), respectively. Among all three breeds the highest
infestation was observed in desi breed (22.9%) (Fig. 2).
The results showed that majority of the non-infested
animals were medicated {local treatment (29.4%), Anti-
parasitic drugs (43.1%)} as compared to non medicated
goats (27.5%) The medication schedule of all the examined
Mean No of Nodules
August September October November December January February March
Number of Animals
Fig 2. Breed wise prevalence of WFI in goats of Punjab
Province, Pakistan
Şekil 2. Pakistan’ın Pencap Eyaletinde Keçi nokra enfestas-
yonunun ırklara göre dağılımı
Fig 1. Month wise intensity of Infestation of WFI in goats
Şekil 1. Keçi nokra enfestasyonunun aylara göre dağılımı
An epidemiological Study on ...
goats was recorded consisting of non-medicated,
local treatment and anti-parasitic drugs. In beatle
breed the non-medicated was 13/197 (6.6%), local
treatments 96/197 (48.7%) and anti-parasitic drugs
88/197 (44.7%). In desi breed, non-medicated was
29/133 (21.80%), local treatments 21/133 (15.78%) and
anti-parasitic drugs 83/133 (62.4%). In local breed non-
medicated was 93/170 (54.7%), local treatments 58/197
(34.1%) and anti-parasitic drugs 19/170 (11.2%). There
are 27% (135/500) goats were non medicated, 35% (175)
were given local treatment and 190 (38%) were given anti-
parasitic drugs (Fig. 3).
The results showed that female 60/310(19.4%) and
male 29/190 (15.3%) goats were infested (Fig. 4). The
medication schedule was also recorded in both the sexes
(Fig. 5). The prevalence in goats having age group (1-3 year)
was 33/158 (20.9%), in age group (4-6 year) was 25/171
(14.6%) and in age group (> 6 year) 31/171 (18.1%) were
infested. The results showed that younger animals were
Number of Animals
Fig 3. Eect of treatments given to dierent breeds of goats
of Punjab Province, Pakistan
Şekil 3. Pakistan’ın Pencap Eyaletindeki farklı ırk keçilerde
tedavinin etkisi
Fig 4. Sex wise prevalence of WFI in goats of Punjab Province,
Şekil 4. Pakistan’ın Pencap Eyaletindeki keçilerde Keçi
nokrasının cinsiyet üzerindeki yaygınlığı
Fig 5. Use of Medication in dierent sexes examined for WFI
in goats of Punjab Province, Pakistan
Şekil 5. Pakistan’ın Pencap Eyaletinde Keçi nokrası için
muayene edilen farklı cinsiyetteki keçilerde ilaç kullanımı
Fig 6. Age wise prevalence of WFI in goats of Punjab Province,
Şekil 6. Pakistan’ın Pencap Eyaletinde nokralı keçilerin yaş
more infested as compared to older animals (Fig. 6).
The statistical analysis showed that there is significant
dierence between infested and non-infested animals in
all age groups (Table 1).
The prevalence in goats of Khoshab and Chakwal
districts was 17.8%. Our results were correlates as 25% goats
were infested with WFI in Pakistan [2]. In Rakhi Manu and
Rakhi Guage area the rate of infestation was 41% and 40%
in goats [4]. Similarly, Otify and Mansour reported 24.9% [9],
in northern Jordan 10% goats were infested from WFI [11] and
in Iran 7% to 18.9% [14]. These results contradictions with
present research results might be due to the use of anti-
parasitic drugs in the study area. As far as the prevalence
of warble y infestation in district Khoshab and Chakwal
is concerned, this is the first report related to goat warble
y infestation.
The female (19.4%) were more infested as compared
to male (15.3%). The statistical analysis showed no
significance dierences (P<0.05) between two sexes. Our
results were similar to as prevalence rate was same in male
and female [11], there was no significant dierence between
male and female (P<0.05) [15]. Similarly, no significant
dierence among male (47.81%) and female (46.82%) in
Jammu province of India [16]. Likewise, Mohammad Hossein
Radfar investigated that the dierence in the prevalence
of the infection between males and females was not
significant (P>0.05) [17].
The present study shows that highest infestation was
observed in desi (Taedi) (22.9%) breed as compare to local
(18%) and beatel breed (13.2%) due to the poor immune
response. Our results were in accordance with Yadav et
al.[16] reported the significantly higher infestation rate
among Bakerwali (51.51%) breed as compare to the Beetle
The prevalence in goats having age group (1-3 year)
was 33/158 (20.9%), in age group (4-6 year) was 25/171
(14.6%) and in age group (>6 year) 31/171 (18.1%)
were infested. The results showed that younger animals
were more infested as compared to older animals.
Similarly, the statistical analysis in relation to age showed
significant (P<0.01) dierence among dierent age
groups <1 year (2.81%), 1-3 years (51.17%), and >3 years
(43.16%) [16].
Table 1. Showing the statistical analysis of dierent epidemiological factors on the prevalence of WFI in goats of Punjab Province, Pakistan
Tablo 1. Pakistan’ın Punjab Eyaletinde Keçi nokrasının prevalansı üzerine değişik epidemiyolojik faktörlerin istatistiksel analizi
S. No Factors Groups
Prevalence Statistical Analysis
Infested Non-Infested
1-3 33 (20.9%) 125 (79.1%)
df=2 p=0.329
4-6 25 (14.6%) 146 (85.4%)
>6 31 (18.1%) 140 (81.9%)
2Sex Male 29 (15.3%) 161 (84.7%) χ² = 1.348
df = 1 p = 0.246
Female 60 (19.4%) 250 (80.6%)
3 Breed
Beatle 26 (13.2%) 171 (86.6%)
df=2 p=0.05
Desi breed (Taedi) 39 (22.9%) 131 (77.1%)
Local breed 24 (18%) 109 (82%)
Dhokri, (Khoshab) 7 (12.7%) 48 (87.3%)
df=9 P=0.00
Ghatti, (Khoshab) 7 (13.2%) 46 (86.8%)
Jabbi sharif, (Khoshab) 5 (9.1%) 50 (90.9%)
Warcha, (Khoshab) 0 (0%) 48 (100.0%)
Chohasharif, (Khoshab) 3 (6.7%) 42 (93.3%)
Manara, (Chakwal) 14 (25.5%) 41 (74.5%)
Runsial, (Chakwal) 38 (34.9%) 71 (65.1%)
Bhone, (Chakwal) 9 (30.0%) 21 (70.0%)
Tala gang, (Chakwal) 4 (14.3%) 24 (85.7%)
ChoaSaidan shah, (Chakwal) 2 (9.1%) 20 (90.9%)
5 Medication
Non Medicated 22 (24.7%) 113 (27.5%)
df=2 P=0.396
Local treatment 54 (60.7%) 121 (29.4%)
Anti-parasitic drugs 13 (14.6%) 177 (43.1%)
An epidemiological Study on ...
It is concluded from the present study that WFI is serious
threat in goats of Pakistan. So it is strongly recommended
that due to the economic significance of this parasitic
disease, it should be explored in dierent areas of Pakistan
and its eects and damages must be studied for its control.
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... In Pakistan, different authors have reported variable percentages of larval infestation ranging from 5 to 75% (Khan et al., 1991Arshad et al., 2014). Recently, Jan et al. (2014) observed that 64.16% of goats tested positive for P. silenus antibodies using an ELISA kit. ...
Myiasis caused by Hypodermatinae flies is an economically important disease affecting domesticated and wild ruminants in countries of the Mediterranean and Indian subcontinent. The adult flies have a short life span of 1 week, and they spread disease by laying their eggs on the coat of animals. Hypoderma spp. primarily lay their eggs on cattle, buffalo, roe deer, red deer and reindeer, while Przhevalskiana spp. lay eggs on the coat of goats. The larvae live as tissue parasites, inducing myiasis in the host, and have a major impact on the productivity and welfare of infested animals. Diagnosis of myiasis is mainly based on clinical examination of the animal and immunodiagnosis using serum and milk samples. Chemical control of this pest is considered the best treatment option. Treatment with microdoses of ivermectin (2 μg/kg body weight) combined with immunosurveillance strategies has led to the eradication of bovine hypodermosis in a few countries; however, these flies are still prevalent throughout the northern hemisphere. This paper reviews the current status, diagnosis and control measures for Hypodermatinae myiasis of domestic and wild ruminants in the Indian subcontinent and Mediterranean region.
... It results in severe decrease in meat and milk production and reducing the hide quality, causes a great deal of economic loss in developing countries [2]. The present report shows the systemic pattern of hypodermosis in Pakistan [2][3][4][5][6][7][8], Iran [9][10][11][12][13][14] and Turkey [15][16][17][18][19] from 2000-2015. The data analysis showed that hypodermosis is highly prevalent in Pakistan followed by Iran and Turkey (Table 1). ...
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The purpose of the present study to determine the geographical distribution of Hypoderma in the Northern Punjab, Pakistan. One thousand cows were examined by palpation method for the presence of warbles in different areas from northern Punjab from August 2010 to February 2011. The overall prevalence was 18.40% with significant differences in the geographical distribution of Hypoderma, when the grazing pattern, Topography, Water Bodies and Village were considered in different geographic areas. The prevalence was higher in hilly and semi-hilly areas as compared to the plane areas.
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Hypodermosis is an endemic disease in semi-hilly and mountainous areas of Pakistan. Keeping in view the importance of buffaloes an epidemiological survey was conducted to find the prevalence of hypodermosis in district Jhelum Punjab, Pakistan, during the year 2010-2011. Out of 1000 buffaloes examined clinically, for warble fly infestation in the study area 32 (3.2%) found to be positive for the warble fly infestation. The number of nodules in the infested animals ranged from 1-5 (2.7±1.1). There were significant differences in the prevalence of Hypoderma when the sex, age and different geographic areas were considered. The Prevalence was higher in males and young animals and also in those animals grazing in hilly and semi-hilly areas. The climatic conditions (Temperature, humidity, sunshine, wind speed) favour the warble fly activity and contribute in the onset of disease.
Goat warble fly infestation (GWFI) by the larvae of Przhevalskiana silenus is endemic in goats of semi-hilly and mountainous regions of Iran. This myiasis has severe economic impact on tanning industries, and it is responsible for impaired milk and meat production, growth retardation and carcass depreciation. To estimate the prevalence of GWFI in the southern areas of Iran, from October 2006 to December 2008, the carcasses of 8000 goats at a Shiraz slaughterhouse and 1000 each at Marvdasht and Darab cities were examined weekly for the presence of P. silenus larvae. In addition, appropriate sections from the skin and subcutaneous tissues were processed for histopathological investigation. The prevalence rate of infestation in different cities varied from 7.0% to 18.9% and the minimum and maximum infestation rate was 3 and 78, with an average rate of infestation of 26.2 warbles per animal. Significant differences were observed in the prevalence among different age groups with no significant difference between male and female animals. First instar larvae (L(1)) were found on infected animals from early August to end of September, second larval stage (L(2)) from early October to end of November and third-stage larvae (L(3)) from early December to mid-March. No larvae were found on skin or subcutaneous tissues from end of March to late July. Live L(1) initiated mild lymphocyte, macrophage and eosinophil infiltration while dead L(1) initiated granulomatous or pyogranulomatous reactions. Live L(2) induced severe inflammatory reaction and massive tissue necrosis, which continued for L(3) and until the end of infestation phase. The subcutaneous tissues, dermis and epidermis became necrotic and fragmented, and L(3) penetrated the necrotic area to start its aerobic life cycle.
Infestation by the warble-fly Przhevalskiana silenus in goats was characterized by formation of thick walls of chronic non-suppurative granulomatous reaction around second and third instar larvae in the back. Significant host reaction began shortly before the larval penetration of dermal tissues and intensified with the shedding of cuticle at the times of moulting. In the early stages there were many granulocytic leukocytes which were later replaced by lymphocytes, plasma cells, macrophages and giant cells. Large mononuclear cells with coarse, pink cytoplasmic granules were seen near the larvae. The wall was partly lined by squamous epithelium growing down from the margins of opening in the skin. Masses of neutrophil leukocytes were present in the midgut of third instar larvae as well as in the warble cavity. The holes in skin were closed three weeks after the removal of third instar larvae. The larvae dying in the animal body were enclosed in a suppurative or non-suppurative granuloma, probably depending upon secondary bacterial infection. The tissue changes were similar to those reported for warble infestation in cattle caused by the larvae of Hypoderma lineatum and H. bovis except that larvae or lesions were not observed in the eosophagi and spinal canals of goats.