Research Article Prevalence and Morphological ...downloads.hindawi.com/journals/jpr/2015/569340.pdf · Journal of Parasitology Research [ ] S.Rouhani,M.Ebrahimi,A.Rostami,andS.H.Fallahi,

Research ArticlePrevalence and Morphological Characterizationof Cheilospirura hamulosa Diesing 1861(Nematoda Acuarioidea) from Partridges in Iran

Maryam Ebrahimi1 Soheila Rouhani1 Iraj Mobedi23 Ali Rostami1

Hoshang Khazan1 and Mohammad Bagher Ahoo3

1Department of Parasitology and Mycology School of Medicine Shahid Beheshti University of Medical Sciences Tehran Iran2Department of Medical Parasitology and Mycology School of Public Health Tehran University of Medical Sciences Tehran Iran3Department of Parasitology Faculty of Veterinary Medicine University of Tehran Tehran Iran

Correspondence should be addressed to Soheila Rouhani srouhani11sbmuacir

Received 17 July 2015 Revised 18 October 2015 Accepted 22 October 2015

Academic Editor Bernard Marchand

Copyright copy 2015 Maryam Ebrahimi et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

This study reports data on the prevalence morphology and morphometry of the nematode Cheilospirura hamulosa on the basis oflight and stereoscopic microscopy and also camera lucida Specimens were recovered after necropsies of 100 partridges (Alectorischukar) from Taleqan County in Alborz Province Iran The prevalence of C hamulosa in partridges was of 30 with a meanintensity of 39 and range of infection of 1ndash12 The mean length and width of females were 175 plusmn 214 and 039 plusmn 004mm whilethose of males were 122 plusmn 067 and 03 plusmn 006mm respectively The characteristic digitiform tail was observed in females and theunequal spicules caudal alae and ten pairs of caudal papillae were seen inmalesThe taxonomic characteristic longitudinal cordonsandmuscular and glandular oesophagus were observed in both sexes Ratio between cordons and body length inmales and femaleswas 1 133 and 1 168 respectively Ratio between long and short spicules in males was 1 23The average size of embryonated eggswas 5125 times 295 120583m In the present study C hamulosa (Nematoda Acuarioidea) is recorded for the first time from partridges inIran Therefore the morphological characters described in this study will be useful in the future diagnostic and taxonomic studiesof Acuarioidea family

1 Introduction

The parasitic nematode Cheilospirura hamulosa ldquoDiesing1861rdquo (syn Acuaria hamulosa) is a species of Acuariidaefamily and etiological agent of cheilospirurosis in birdssuch as chickens turkeys pigeons and guinea fowls [1 2]Cheilospirura hamulosa has cylindrical body with two trian-gular lips and 4 cuticular cordons that extend near posteriorextremity Male worms have two distinctly unequal anddissimilar spicules Female worm tails are curved ventrallyand digitiform [3 4]

The C hamulosa is located under gizzard cuticle mainlyin koilin or muscular wall of the host [1 2] This nema-tode has indirect life cycle The grasshoppers (Melanoplus

Oxyanitidula and Spathosternum parasinifrum) beetles andweevils are intermediate hosts for C hamulosa and birdsacquire their infections by eating contaminated arthropodscontaining infective third-stage larvae [1] Due to its highpathogenicity in poultry the C hamulosa has veterinary andpublic health importance Cheilospirura hamulosa can causeseveral complications such as granulomas and nodules thatlead to anemia impotence and mortality in chickens [2]Cheilospirura hamulosa may cause zoonosis and has beenrecovered from a nodule on the conjunctiva of a Filipinofarmer [5] The previous studies in rural areas of Iranindicated that the infection of this worm is common amongfree-range chickens [6] whereas there is no published dataon partridges in Iran The main goal of the present study

Hindawi Publishing CorporationJournal of Parasitology ResearchVolume 2015 Article ID 569340 6 pageshttpdxdoiorg1011552015569340

2 Journal of Parasitology Research

was to survey prevalence of Cheilospirura hamulosa infectionin partridges (Alectoris chukar) using morphological-basedmethods in Taleqan County of Iran

2 Materials and Methods

The study was conducted in Taleqan County This area islocated in Alborz Province and its height is 1900m above thesea level Latitude and longitude of Taleqan are 36 degrees151015840N and 50 degrees 461015840E respectively

One hundred partridges were collected from Taleqanmountainous region between 2011 and 2013 Every year fromthe end of September to the beginning of February a licenseis issued by the Environment Protection Agency (EPA) ofIran for hunting partridges Every hunter has permissionto hunt the maximum of three partridges weekly For thisresearch the gizzard of each partridge was removed fromthe alimentary tract and delivered to the helminthologylaboratory of Shahid Beheshti University ofMedical SciencesThe gizzards were examined macroscopically and then dis-sected in a 085 NaCl solution (normal saline) to removecuticleWormswere visible to the naked eyeThewormswererinsed in normal saline and fixed in Alcohol-Glycerin (70Alcohol 50mL Glycerin 50mL) solution Nematodes wereelucidated with acetic acid and phenol mounted in Canadabalsam Helminthes were counted and identified under lightmicroscopy (Zeiss Germany) and stereoscopic microscope(Zeiss Germany) and traced by camera lucida (Zeiss Ger-many)Themorphological identification of the nematodes tothe species level was done according tomethods described bySkrjabin et al [9]

3 Results

31 Prevalence of C hamulosa Out of a total of 100 partridgesexamined the prevalence of C hamulosa was 30 with amean intensity of 39 and range of infection of 1ndash12 Atotal of 116 worms were recovered from partridges Amongthe recovered helminthes 603 were female and 397male The specimens of C hamulosa were found free underthe gizzard cuticle partially or fully burrowed in the walls(Figure 1) Microscopic description was based on 10 adultworms five males and five females (Table 1)

32 Male (119899 = 5 Except When Otherwise Indicated) Theaverage length of adult males was 122 plusmn 067mm and theiraverage width was 03 plusmn 006 Buccal cavity was 021 long0019 wide (119899 = 1) Muscular oesophagus was 037ndash038(0375 119899 = 2) long Glandular oesophagus was 16ndash24 (2119899 = 2) long Length of total oesophagus was 197ndash278 (237119899 = 2) The mean of cordons length was 92 plusmn 028 ratiobetween cordons and body length was 1 133 (Figure 2 (A1)ndash(A3)) long spicule slender was 144 plusmn 008mm in lengthshort spicule shaped like a chopping knife was 062plusmn011mmlong and ratio between long and short spicules was 1 23The ratio between mean of long and short spicules lengthand body lengthwere 011mm and 004mm respectivelyThemean length of caudal alae was 042 plusmn 002 and its width

Figure 1 Cheilospirura hamulosa under the gizzard cuticle

was 032 plusmn 002 with tail 043mm long (119899 = 1) In eachworm there were ten pairs of caudal papillae three coupleswere observed in precloacal two pairs in adcloacal and fivecouples in postcloacal (Figure 2 (B1)ndash(B3))

33 Female (119899 = 5 Except When Otherwise Indicated) Themean length and width of females were 175 plusmn 214 and039 plusmn 004mm respectively Buccal cavity was 022 longand 0028 wide (119899 = 1) Muscular oesophagus was 029ndash075 (045 119899 = 3) long Glandular oesophagus was 21ndash27(23 119899 = 3) long Length of total oesophagus was 239ndash305(282 119899 = 3) The mean of cordon length was 1296 plusmn 072and ratio between cordons and body length was 1 168 Thefemales were amphidelphic and their vulva is located slightlyposterior to the middle of the body at 229 plusmn 092 from theposterior end circular sphincter 0064 times 0065 tail 044 (119899 =1) long (Figure 3 (A1)-(A2) and (B1)-(B2)) Embryonatedeggs were 0045ndash0055 (0051) long and 0028ndash003 (0029)wide (Figure 4)

4 Discussion

ThenematodeC hamulosa reported herein is reported for thefirst time from partridges in Iran Studies on this nematodein Iran only was carried out in native fowls The partridge(Alectoris chukar) is the most important bird hunted inIran In the present study prevalence of C hamulosa in thepartridge was 30 with a mean intensity of 39 and rangeof infection of 1ndash12

The reported prevalence of this nematode by Menezeset al [2] in Brazil was 143 in ring-necked pheasants(Phasianus colchicus) with a mean intensity and range ofinfection of 15 1-2 respectively In domestic chickens (Gallusg domesticus) the prevalence mean intensity and range ofinfection were 267 4 and 1ndash12 respectively [2] A 2-yearstudy inKashmir India on the prevalence of the nematodeChamulosa in indigenous fowl has shown an overall prevalenceof 35 (17478) [10] The prevalence of C hamulosa inguinea fowls (Numida meleagris galeata Pallas) from Ghanaand chickens in Zimbabwe and Cuba was 378 466 and846 respectively [11ndash13] These results are higher thanour finding The reported prevalence of C hamulosa on

Journal of Parasitology Research 3

(A2)(A1)mo

bc mo

bc

5 0mm

(A3)

moc

go

100120583m

times10

times40

(a)

(B3)

(B2)(B1)

capa

ssplsp ca pa

pa

ssp

lsp

ca

passp

lsp

500120583m

(b)

Figure 2 Male of Cheilospirura hamulosa light micrographs and camera lucida (A1) Enlarged view of the anterior region buccal cavity (bc)muscular oesophagus (mo) (A2) anterior end lateral view buccal cavity (bc) muscular oesophagus (mo) (A3) anterior end sublateral viewmuscular oesophagus (mo) glandular oesophagus (go) and cordon (c) (B1) and (B2) male posterior end showing small (ssp) and large (lsp)spicules caudal alae (ca) and caudal papillae (pa) (B3) posterior end of male lateral view papillae (pa) long spicule (lsp) short spicule (ssp)and caudal alae (ca)

native fowls from Golestan Province in north of Iran was 4which is significantly lower than our result because the studypopulation is completely different from our study [6]

The nematodes of the genus Acuaria (Cheilospirura) areparasitic among different families of birds and they arelocated under the koilin layer usually in the cardiac orpyloric regions [2] Also in our study the specimens of Chamulosa were found under the gizzard cuticle partially orfully burrowed in the walls of the organ (Figure 1)

Most of the reported lengths for male and female Chamulosa are within the range of 9ndash14 and 15ndash25 respec-tively ([3 14] and [1 7 8]) (Table 1) In this study maleworms were smaller than the female worms in average bodylength overall cordon glandular oesophagus and muscularoesophagus length (Table 1) Moreover in our study the longspicules were smaller and the length of short spicules waslonger compared with previous studies reported by Cram[1 3] Yamaguti [7] and Gomes et al [8] (see Table 1 for


(A2)(A1)

vu

e

vu

t

(a)

(B2)(B1)

vu

t

vu

e

u

times1005mm times40

100120583m

(b)

Figure 3 Female of Cheilospirura hamulosa light micrographs and camera lucida (A1) Female posterior end showing vulva (vu) tail (t)(A2) enlarged view of the female posterior region showing vulva (vu) embryonated eggs (e) (B1) and (B2) posterior end of female vulva(vu) utri (u) egg (e) and tail (t)

comparison) In our study average length of male worms washigher than those reported by Gomes et al [8] In our studythe female worms were smaller in maximum body lengththan those described by Cram and Yamaguti [3 7] but stillwere bigger than those described by Gomes et al [8] Thefemale of C hamulosa in our study had smaller muscularand glandular oesophagus than those reported by Gomesand Yamaguti [7 8] whereas values obtained for the lengthof tail and egg size were bigger compared to two studiesmentioned above (Table 1) We observed 10 pairs of papillaein C hamulosa as reported by Cram [3] and Gomes et al[8] however in the precloacal region 2 pairs of papillae wereunclear (Figure 2 (B1)ndash(B3))

Due to the significant pathogenic effects of these nema-todes (Cheilospirura spp) in poultry andwild bird populationand very limited prevalence data of these helminthes in Iranfurther study will be needed on different aspects of Acuari-oidea family including pathogenesis and their prevalence inother avian species

5 Conclusions

In the present study we report for the first time the isolationand morphological characterization of Cheilospirura hamu-losa from partridges in Iran The morphological characters


Table 1 Comparison of Cheilospirura hamulosa body parts from partridges of Iran with those of previous reports (mm)

Cram 1931 [1] Yamaguti 1954 [7] Gomes et al 2004 [8] This study 2014

Male mdash 119899 = 1 119899 = 4 119899 = 5

Body length (mm) 9ndash13 136 954 1118ndash13 (1222)

Body width (mm) 03ndash032 032 028 025ndash04 (03)

Cordons length 72ndash88 mdash mdash 9ndash96 (92)

Buccal cavity mdash 024 times 003 mdash 021 times 0019lowast

Muscular oesophagus length mdash 091 times 0098 067 037ndash038 (0375)lowastlowast

Glandular oesophagus length mdash 255 times 0154 221 16ndash24 (2)lowastlowast

Tail length 0416ndash0488 056 mdash 043lowast

Long spicule (lsp) 16ndash18 24 148ndash174 (160) 14ndash16 (144)The ratio between lsp length andbody length

mdash 017 016 011

short spicule (ssp) 02ndash022 018 022ndash026 (022) 05ndash08 (062)The ratio between ssp length andbody length

mdash 001 002 004

Pairs of postcloacalPapillae

6 3 5 5

Female mdash 119899 = 2 119899 = 5 119899 = 5

Body length (mm) 15ndash22 24-25 97ndash2309 (1536) 16ndash20 (175)

Body width (mm) 04ndash065 046ndash05 040 035ndash045 (039)


Buccal cavity length mdash 033 times 0047ndash0057 mdash 023 times 0028lowast

Muscular oesophagus length mdash 126ndash13 082 029ndash075 (045)lowastlowastlowast

Glandular oesophagus length mdash 42ndash45 283 21ndash27 (23)lowastlowastlowast

Tail length 042ndash059 028 033 044lowast

Egg (120583m) 40 times 27 39ndash45 times 24ndash26 36 times 22 5125 times 295lowastMeasurements from one male and female onlylowastlowastMeasurements from two males onlylowastlowastlowastMeasurements from three females only

F

100120583

Figure 4 Camera lucida of embryonated egg

described in this study will be useful in the future diagnosticand taxonomic studies of Acuarioidea family

Conflict of Interests

None of the above authors have any conflict of interests

Acknowledgments

The authors thank Dr Shoreh Miller for English editing ofthis paper and Mr Naser Bagheri for sending the alimentarytract of partridges

References

[1] E B Cram ldquoDevelopmental stages of some nematodes of theSpiruroidea parasitic in poultry and game birdsrdquo TechnicalBulletin 227 United State Deprtment of Agriculture 1931

[2] R C Menezes R Tortelly D C Gomes and R M PintoldquoPathology and frequency of Cheilospirura hamulosa (Nema-toda Acuarioidea) in Galliformes hosts from backyard flocksrdquoAvian Pathology vol 32 no 2 pp 151ndash156 2003

[3] E B Cram ldquoBird parasites of the nematode suborders strongy-lata ascaridata and spiruratardquo Bulletin of the United StatesNational Museum vol 140 pp 1ndash465 1927


[4] S Rouhani M Ebrahimi A Rostami and S H Fallahi ldquoEffec-tive appropriate and simple culture egg hatching and cry-opreserving of the nematode Cheilospirura hamulosardquo BritishPoultry Science vol 55 no 6 pp 846ndash849 2014

[5] R Muller Worms and Human Disease CABI Publishing 2ndedition 2002

[6] A Eslami P Ghaemi and S Rahbari ldquoParasitic infectionsof free-range chickens from Golestan province Iranrdquo IranianJournal of Parasitology vol 4 no 3 pp 10ndash14 2009

[7] S Yamaguti ldquoParasitic worms mainly from Celebes Part 10Nematodes of birds andmammalsrdquo ActaMedica Okayama vol9 pp 134ndash135 1954

[8] D C Gomes R CMenezes J J Vicente RM Lanfredi and RM Pinto ldquoNew morphological data on Cheilospirura hamulosa(NematodaAcuarioidea) bymeans of bright-field and scanningelectron microscopyrdquo Parasitology Research vol 92 no 3 pp225ndash231 2004

[9] K I Skrjabin A A Sobolev and V M Ivashkin Essentialsof Nematodology XIV Spirurata of Animals and Man and theDiseasesThey Cause Acuarioidea part 3 Akademii Nauk SSSRMoscow Russia 1965

[10] S T Salam M S Mir S Shahnaz and R A Khan ldquoPrevalenceand the associated lesions of Cheilospirura (Acuaria) hamulosain the indigenous chicken of Kashmir Valley Indiardquo Journal ofParasitology vol 95 no 6 pp 1436ndash1439 2009

[11] J Hodasi ldquoThe helminth parasites of the helmet guinea fowl(Numida meleagris galeata pallas) in Ghanardquo Bulletin of AnimalHealth and Production in Africa vol 24 pp 81ndash87 1976

[12] E Cruz ldquoComunicacion sobre una considerable extension deinvasion porCheilospirura hamulosa en aves ponedoras (1966)rdquoCiencia y Tecnica en laAgricultura Veterinaria vol 3 pp 67ndash691966

[13] J Jansen and V Pandey ldquoObservations on helminth parasitesof domestic fowls in Zimbabwerdquo Zimbabwe Veterinary Journalvol 20 no 1 pp 15ndash17 1989

[14] H D Srivastava ldquoStudies on the helminth parasites of Indianpoultry Part IIITheoccurrence of two spirurid stomachwormsin fowlsrdquo Journal of Veterinary Science and Animal Husbandryvol 9 no 2 pp 225ndash227 1939

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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International Journal of

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Zoology


Molecular Biology International

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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014


BioinformaticsAdvances in

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Signal TransductionJournal of


BioMed Research International

Evolutionary BiologyInternational Journal of



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Genetics Research International


Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational



Enzyme Research



Microbiology


was to survey prevalence of Cheilospirura hamulosa infectionin partridges (Alectoris chukar) using morphological-basedmethods in Taleqan County of Iran

2 Materials and Methods

The study was conducted in Taleqan County This area islocated in Alborz Province and its height is 1900m above thesea level Latitude and longitude of Taleqan are 36 degrees151015840N and 50 degrees 461015840E respectively

One hundred partridges were collected from Taleqanmountainous region between 2011 and 2013 Every year fromthe end of September to the beginning of February a licenseis issued by the Environment Protection Agency (EPA) ofIran for hunting partridges Every hunter has permissionto hunt the maximum of three partridges weekly For thisresearch the gizzard of each partridge was removed fromthe alimentary tract and delivered to the helminthologylaboratory of Shahid Beheshti University ofMedical SciencesThe gizzards were examined macroscopically and then dis-sected in a 085 NaCl solution (normal saline) to removecuticleWormswere visible to the naked eyeThewormswererinsed in normal saline and fixed in Alcohol-Glycerin (70Alcohol 50mL Glycerin 50mL) solution Nematodes wereelucidated with acetic acid and phenol mounted in Canadabalsam Helminthes were counted and identified under lightmicroscopy (Zeiss Germany) and stereoscopic microscope(Zeiss Germany) and traced by camera lucida (Zeiss Ger-many)Themorphological identification of the nematodes tothe species level was done according tomethods described bySkrjabin et al [9]

3 Results

31 Prevalence of C hamulosa Out of a total of 100 partridgesexamined the prevalence of C hamulosa was 30 with amean intensity of 39 and range of infection of 1ndash12 Atotal of 116 worms were recovered from partridges Amongthe recovered helminthes 603 were female and 397male The specimens of C hamulosa were found free underthe gizzard cuticle partially or fully burrowed in the walls(Figure 1) Microscopic description was based on 10 adultworms five males and five females (Table 1)

32 Male (119899 = 5 Except When Otherwise Indicated) Theaverage length of adult males was 122 plusmn 067mm and theiraverage width was 03 plusmn 006 Buccal cavity was 021 long0019 wide (119899 = 1) Muscular oesophagus was 037ndash038(0375 119899 = 2) long Glandular oesophagus was 16ndash24 (2119899 = 2) long Length of total oesophagus was 197ndash278 (237119899 = 2) The mean of cordons length was 92 plusmn 028 ratiobetween cordons and body length was 1 133 (Figure 2 (A1)ndash(A3)) long spicule slender was 144 plusmn 008mm in lengthshort spicule shaped like a chopping knife was 062plusmn011mmlong and ratio between long and short spicules was 1 23The ratio between mean of long and short spicules lengthand body lengthwere 011mm and 004mm respectivelyThemean length of caudal alae was 042 plusmn 002 and its width

Figure 1 Cheilospirura hamulosa under the gizzard cuticle

was 032 plusmn 002 with tail 043mm long (119899 = 1) In eachworm there were ten pairs of caudal papillae three coupleswere observed in precloacal two pairs in adcloacal and fivecouples in postcloacal (Figure 2 (B1)ndash(B3))

33 Female (119899 = 5 Except When Otherwise Indicated) Themean length and width of females were 175 plusmn 214 and039 plusmn 004mm respectively Buccal cavity was 022 longand 0028 wide (119899 = 1) Muscular oesophagus was 029ndash075 (045 119899 = 3) long Glandular oesophagus was 21ndash27(23 119899 = 3) long Length of total oesophagus was 239ndash305(282 119899 = 3) The mean of cordon length was 1296 plusmn 072and ratio between cordons and body length was 1 168 Thefemales were amphidelphic and their vulva is located slightlyposterior to the middle of the body at 229 plusmn 092 from theposterior end circular sphincter 0064 times 0065 tail 044 (119899 =1) long (Figure 3 (A1)-(A2) and (B1)-(B2)) Embryonatedeggs were 0045ndash0055 (0051) long and 0028ndash003 (0029)wide (Figure 4)

4 Discussion

ThenematodeC hamulosa reported herein is reported for thefirst time from partridges in Iran Studies on this nematodein Iran only was carried out in native fowls The partridge(Alectoris chukar) is the most important bird hunted inIran In the present study prevalence of C hamulosa in thepartridge was 30 with a mean intensity of 39 and rangeof infection of 1ndash12

The reported prevalence of this nematode by Menezeset al [2] in Brazil was 143 in ring-necked pheasants(Phasianus colchicus) with a mean intensity and range ofinfection of 15 1-2 respectively In domestic chickens (Gallusg domesticus) the prevalence mean intensity and range ofinfection were 267 4 and 1ndash12 respectively [2] A 2-yearstudy inKashmir India on the prevalence of the nematodeChamulosa in indigenous fowl has shown an overall prevalenceof 35 (17478) [10] The prevalence of C hamulosa inguinea fowls (Numida meleagris galeata Pallas) from Ghanaand chickens in Zimbabwe and Cuba was 378 466 and846 respectively [11ndash13] These results are higher thanour finding The reported prevalence of C hamulosa on


(A2)(A1)mo

bc mo

bc

5 0mm

(A3)

moc

go

100120583m

times10

times40

(a)

(B3)

(B2)(B1)

capa

ssplsp ca pa

pa

ssp

lsp

ca

passp

lsp

500120583m

(b)






(A2)(A1)

vu

e

vu

t

(a)

(B2)(B1)

vu

t

vu

e

u

times1005mm times40

100120583m

(b)




5 Conclusions





Male mdash 119899 = 1 119899 = 4 119899 = 5









mdash 017 016 011


mdash 001 002 004


6 3 5 5

Female mdash 119899 = 2 119899 = 5 119899 = 5









F

100120583





Acknowledgments


References























Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


(A2)(A1)mo

bc mo

bc

5 0mm

(A3)

moc

go

100120583m

times10

times40

(a)

(B3)

(B2)(B1)

capa

ssplsp ca pa

pa

ssp

lsp

ca

passp

lsp

500120583m

(b)






(A2)(A1)

vu

e

vu

t

(a)

(B2)(B1)

vu

t

vu

e

u

times1005mm times40

100120583m

(b)




5 Conclusions





Male mdash 119899 = 1 119899 = 4 119899 = 5









mdash 017 016 011


mdash 001 002 004


6 3 5 5

Female mdash 119899 = 2 119899 = 5 119899 = 5









F

100120583





Acknowledgments


References























Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


(A2)(A1)

vu

e

vu

t

(a)

(B2)(B1)

vu

t

vu

e

u

times1005mm times40

100120583m

(b)




5 Conclusions





Male mdash 119899 = 1 119899 = 4 119899 = 5









mdash 017 016 011


mdash 001 002 004


6 3 5 5

Female mdash 119899 = 2 119899 = 5 119899 = 5









F

100120583





Acknowledgments


References























Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology




Male mdash 119899 = 1 119899 = 4 119899 = 5









mdash 017 016 011


mdash 001 002 004


6 3 5 5

Female mdash 119899 = 2 119899 = 5 119899 = 5









F

100120583





Acknowledgments


References























Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology




















Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology








Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

Documents

Research Article Prevalence and Morphological ...downloads.hindawi.com/journals/jpr/2015/569340.pdf · Journal of Parasitology Research [ ] S.Rouhani,M.Ebrahimi,A.Rostami,andS.H.Fallahi,