Camelus dromedarius) during prenatal life: A light and ...In this stage, the tongue was well developed and attained the form of adult tongue with prominent Torus linguaeAll .lingual

Anat Histol Embryol. 2017;1–8. wileyonlinelibrary.com/journal/ahe  | 1© 2017 Blackwell Verlag GmbH

Received:18November2016  |  Accepted:10October2017DOI:10.1111/ahe.12321

O R I G I N A L A R T I C L E

Morphogenesis of lingual papillae of one- humped camel (Camelus dromedarius) during prenatal life: A light and scanning electron microscopic study

A. S. Abou-Elhamd1,2 | M. Abd-Elkareem1 | A. El-Zuhry Zayed1,2

1DepartmentofAnatomy,HistologyandEmbryology,FacultyofVeterinaryMedicine,UniversityofAssiut,Assiut,Egypt2DepartmentofMedicalBiology,JazanUniversity,Jazan,SaudiArabia

CorrespondenceAlaaSayedAbou-Elhamd,DepartmentofAnatomyandHistology,FacultyofVeterinaryMedicine,AssiutUniversity,Assiut,Egypt.Email: [email protected]

SummaryThis studywasmade on 24 camel fetuses of crown-rump vertebral length (CVRL)rangingfrom10.5cmto105cmCVRL(94–352daysold).Thesecamelfetuseswereclassifiedintothreegroupsrepresentingthethreetrimestersofprenatallife.Duringthefirsttrimester(94–142days),lingualpapillae(circumvallateandlentiformpapillae)weredemonstratedonthelingualroot,butlingualbodyandtheapexwerealmostfreeofpapillaeexceptforsomescatteredepithelialprojectionsespeciallynearthelateralbordersofthebody. Inthesecondtrimester (152–229days), the lentiformpapillaecoveredtheentirerootofthetongueexceptforareasoccupiedbythecircumvallatepapillae.Tastebudswithclearporeswereobservedforthefirsttimeinareasbetweenthecircumvallategustatoryfurrowandsurfaceepitheliumofthetongue.Inaddition,shortnumerousfiliformpapillaewereobservedontherostralpartofthelingualbodyand the lateralpartsof theapex.Fungiformpapillae,however,weredemonstratedamidstthefiliformpapillae.Inthistrimester,tastebudswerealsoseenonthetopofthefungiformpapillae.Inthethirdtrimester(256–352days),alllingualpapillaewereclearlydemonstratedonthedorsumoftheroot,bodyandapexofthetongue.Bothtypes of gustatory papillae (circumvallate and fungiform) hadwell-developed tastebuds.Mechanicalpapillae(filiformandlentiform)werewelldeveloped.Lentiformpa-pillaeoccupiedmostofthedorsalaspectoftheTorus linguae;theywerelargerinsizewithsemicircularapices.Filiformpapillae,however,werenumerousanddemonstratedheavilyonthelateralandrostralpartsofthebodyaswellasontheapexofthetongue.

1  | INTRODUCTION

Camelus dromedarius(one-humpedcamel)isamongthelargestmam-malianspecies,livesinregionswithhightemperatureanddryclimateand fed on thorny plants with rough and hard stems (Bello etal.,2012,2015).Thecamel’smouth isverysturdyandhasdevelopedaspecialfeaturetomaintainefficientfeedingontheseplants(Sui,Su,&Chen,1983).The tongue isamuscularorgancoveredbymucousmembranewithanumberofsalivaryglandsandnervesembeddedinbetweenthemuscletissues.Onthedorsalsurfaceofthetongue,thelingualmucosawas thrown intoprojections called the lingualpapil-lae (Dyce, Sack, &Wensing, 1996; Sisson &Grossman, 1975). Thelingual papillae fulfil diverse functions during food intake, transport

andswallowing(Abbateetal.,2008;Skieresz-Szewczyk&Jackowiak,2017).The lingualpapillae in camels, likeothermammalian species,were classified into mechanical and gustatory papillae. Mechanicalpapillae, as previously described, include filiform, lentiform, conicalandwart-likepapillae (Qayyum,Fatani,&Mohajir, 1988).Gustatorypapillaewithtastebudsarefungiformandcircumvallate(Erdunchaoluetal., 2001;Qayyumetal., 1988;Salehietal., 2010).Foliategusta-torypapillaedemonstratedinothervertebrates(Abbateetal.,2009,2010;Abd-Elnaeim,Zayed,&Leiser,2002)havenotbeendescribedin theone-humped camel (Dyceetal., 1996).Themorphogenesisofthetongueanditspapillaewasinvestigatedinvariousmammalssuchasmouse(Iwasaki,Okumura,&Kumakura,1999;Iwasaki,Yoshizawa,&Kawahara,1996),goats (Shawulu,Kwari,&Abgyal,2012),human

2  |     ABOU- ELHAMD Et AL.

(Bradley&Stern,1967),rabbit (Elnasharty,Sharaby,&El-Din,2013)and sheep (Hejazi&Baroughi,2013).Mostprevious studieson theprenatal development of the camel’s lingual papillae (Abd-Elnaeim,Kelany,Dorreia,&Abdel-Moneim,2008;Bello,Alimi,Umaru,&Onu,2015;Belloetal.,2014;Bello,Alimi,Sonfada,etal.,2015;Dougbag,1987a,b;Salehietal.,2010)describedindividual lingualpapillaeandhavenotgivenageneraloutlineoftheirmorphogenesisandtimingoftheirdifferentiation.Inourpreviousreport(Gad-Allah,Abou-Elhamd,Abdelmonem,&Zayed,2015),wediscussedtheveryearlystagesofdevelopment of the tongue of one-humped camel. The aim of thisstudywastocompleteourinvestigationaboutthemorphogenesisofthecamel’stongueanditspapillaeduringprenatallifeusinglightandscanningelectronmicroscopethatmayhelpinbetterunderstandingthe relationships between the lingual morphology and the feedinghabitsinthisuniquespecies.

2  | MATERIAL AND METHODS

This study was made on 24 camel fetuses of CVRL ranging from10.5cmCVRLto105cmCVRL.Theageof the fetuseswascalcu-latedusing theequation:Age=(CVRL+23.99)/0.366according toElwishy,Hemeida,Omar,Mobarak,andElSayed (1981).Camel fe-tuseswere collected fromCairo Slaughter house; then, theywereclassifiedintothreegroupsrepresentingthethreetrimestersofpre-natal life; ten in the first, nine in the second and five in the thirdtrimester.Fetuses in the first trimester rangedfrom10.5 to28cmCVRL(94–142days),inthesecondtrimesterfrom32to60cmCVRL(152–229days)whileinthethirdtrimestertheyrangedfrom70to105cmCVRL(256–352days).Afterinvestigationofthegrossmor-phologyofthewholetongue,smallpiecesofthelingualmucosaandunderlying lingual tissue in the root, body and apexof the tongueweretakenandprocessedforlightandscanningelectronmicroscopy.Forlightmicroscopy,smalltissueblockswerefixedinneutralbufferformalin, washed under tap water, dehydrated in graded ethanol,clearedinmethylbenzoateandembeddedinparaffinwax.Three-to

five-micrometre-thickparaffinsectionsweremadeandstainedwithhaematoxylinandeosin,trichrome,PASandalcianbluestains,thenexaminedandphotographedmicroscopically.Forscanningelectronmicroscopy, small tissue blocks with the covering lingual mucosawerefixedinmixtureofparaformaldehydesolution(2.5%)andglu-taraldehydesolution (2.5%) inphosphatebuffer (pH7.3) for24hr.Sampleswerethenwashed in0.1Mphosphatebuffer,dehydratedin ascendinggradesof ethanol, critical point-dried in liquid carbondioxideandthencoatedwithgoldpalladiusinsputteringdevice.ThesampleswerethenexaminedandphotographedusingJSM-5400LVScanningelectronmicroscopeoperatedat20KVintheEMCenterofAssiutUniversity.

Thestudywasconductedinaccordancewiththeapprovalandguide-linessetoutbytheEthicsCommissionatAssiutUniversityinEgypt.

3  | RESULTS

Thedromedarylingualpapillaepresentspecificgrossanatomicaldur-ingprenataldevelopment.

3.1 | First trimester (94–142 days)

The tongue appeared elongatedwith a flat surface and almost uni-forminthicknessandwidththroughoutitslength(Figures1aand2b).Lingualpapillaeweredemonstratedon the lingual root (2b). Lingualbodyandtheapexwerealmostfreeofpapillaeexceptforsomescat-teredepithelialprojectionsespeciallyonthelateralpartsofthedorsumof thebody.Theearly formed lingualgrooveappearedon themid-sagittallineoftheDorsum linguae(Figure2a,b).Thesurfaceepitheliumisformedofstratifiedcuboidalepithelium(Figure3a).Theprimordiaof circumvallate and lentiform papillae were clearly demonstratedonthelingualroot(Figure3a).Thecircumvallatepapillaappearedassmallprominencessurroundedbycirculargroovesandanannularpad(Figure3b). The circular groove of circumvallate papillawas formedasaresultofsequesteringepithelialcells(3c).Someepithelialplaco-desappearedonthelingualbodyresultingfromdifferentialepithelialgrowthrepresentingtheprimordiaoffungiformpapillae(Figure3d–f).

3.2 | Second trimester (152–229 days)

The tongue attained a more elongated form with tapering end(Figure1b). The covering lingual epithelium displayed the featuresof keratinized stratified squamous epitheliumonbothpapillary andinterpapillarydorsal lingualsurface.Thecircumvallateand lentiformpapillaeweredemonstratedonlyontherootofthetongue.Thelenti-formpapillaeappearedcoveringalltherootofthetongueexcepttheareaoccupiedbythecircumvallatepapillae,andtheywerearrangedlaterallyintworows(4–5each)oneithersideofthelingualroot.Theyappearedassmallprominencesurroundedbycirculargroovesandan-nularpadsofthesurroundinglingualmucosa(Figure4a,c).Tasteporeswereobservedintheareabetweenthecircumvallategustatoryfur-rowandthesurroundingsurfaceepitheliumofthetongue(Figure4b).

F IGURE  1 AGrossphotographshowingfetalcameltonguesatdifferentstagesofdevelopment:(a)(firsttrimester),(b)(secondtrimester)and(c)(thirdtrimester).Abbreviations:A;apex,B;body,R;root.NotetheprominentTorus linguaeintherootregioninthethirdtrimester

(a)

(b)

(c)

     |  3ABOU- ELHAMD Et AL.

Inthisstage,shortnumerousfiliformpapillae,whichappearedasdome-like elevations,were observed laterally on the rostral part ofthebodyandtheapexandofthetongue.Manythread-likeepithelialprojectionswereseenamongthem(Figure4f,g).Thefungiformpapil-laeweredemonstratedamidstthefiliformpapillae.Inthisstage,tastebudswerefirstseenonthetopofthesepapillaewithwell-demarcatedtastepores(Figure4e,h).

3.3 | Third trimester (256–352 days)

Inthisstage,thetonguewaswelldevelopedandattainedtheformof adult tongue with prominent Torus linguae. All lingual papil-lae were clearly demonstrated on the dorsum of the root, bodyand apex of the tongue (Figure1c). The gustatory papillae (cir-cumvallate and fungiform) hadwell-developed taste buds,whichshowed basal, supporting and neuroepithelial cells. The tasteporesweredemonstratedon the freeand lateral surfacesof thepapillae (Figure5a,c,e). Axons of neuroepithelial cells were seenpenetrating thesubepithelial connective tissue (Figure5c). Inad-dition, Ebner’s glandswerewell developed and their ductswereseenpenetratingthegustatoryfurrow(DataS1).TheseglandswerenegativetoPASandalcianbluereactions(DataS2).Thefungiformpapillaewereroundedandeachonewassurroundedbyapromi-nentgroove;tasteporesweredemonstratedontheirfreesurfaces.Lentiform papillae were numerous and larger in size with semi-circularapices (Figure5g), and theycoveralmostallof theTorus linguae except areas occupied by circumvallate papillae. Filiformpapillae, however, were more numerous and larger in size; theyweredemonstratedheavilyonthe lateralandrostralpartsofthebodyaswellasontheapex(Figure5f).

4  | DISCUSSION

Thepresentstudywascarriedouton24camelfetuses(94–352days)toinvestigatethedevelopmentalchangesinthetongueanditspapil-laeduringthethreetrimestersoftheprenatallife.

In agreementwith Saidu etal. (2015) and Bello,Alimi, Sonfada,etal.(2015),thetongueappearedelongatedwithflatsurfaceandal-mostuniformthicknessandwidththroughoutitslengthinallstagesofdevelopment.

Thecamellingualepithelium,asdemonstratedinthecurrentstudy,experiencedthefirstappearanceofpapillaewhenthisepitheliumat-tainedastratifiedform.SimilarconclusionhasbeenreportedbyHejaziandBaroughi(2013),whomentionedthatthetimeofemergenceandgrowthof the lingualpapillaeaccompanytheformationofstratifiedsquamousepithelium. InastudyontheGeomyid&Heteromyidro-dents(Frederick,Stangl,&Russell,1994)statedthatmechanicalpapil-laeare the firstdifferentiated lingualpapillaeandgustatorypapillaewithtastebudcellsarethelasttoappearandtheyemergenearthedelivery.Thelaststatementdisagreeswithourcurrentfindingswherethetimingofemergenceof lingualpapillae isaregional issuewherebothmechanicalandgustatorypapillaeappearedfirstonthelingualrootwhilethoseonthebodyandapexappearedlateron.Moreover,the fungiformpapillae (gustatorypapillae)preceded theappearanceoffiliformpapillae(mechanicalpapillae)onthebodyandapexofthecameltonguefetuses.

In agreement with previous studies (Erdunchaolu etal., 2001;Qayyum,Fatani,Mehta,Shaad,&Mustafa,1991;Saiduetal.,2015;Salehietal.,2010),thelingualpapillaeinadultcamelsincludefiliform,lentiform as mechanical papillae and fungiform and circumvallateasgustatorypapillae.Qayyumetal. (1991)describeda special type(wart-like)papillaeincloserelationshipwithcircumvallatepapillae.Inaddition,Ramayyaetal.(Ramayya,Babu,Rao,Lakshmi,&Patki,2012)reportedconicalpapillaeontheperipheryofthedorsalsurfaceofthetongue especially on the Torus linguae. According to Qayyum etal.(1988),thewart-likepapillaeseenontherootofthetonguecanbeclassifiedintotwomajortypes:withpointedandbluntends,respec-tively.Itisclearthatthereisacontroversyinthetypesofmechanicalpapillaedemonstratedonthelingualrootofthecamel.Inouropinionandaccordingtothecurrentfindings,thecamelhasonlytwotypesofmechanicalpapillae:oneonthebodyandapex (filiform)andoneontheroot(lentiformtype)whichsometimeshasapointedendanddescribedaswart-likeorbluntendanddescribedasconicalpapillabysomeauthors.Itseemsthatthesearesubtypesoflentiformpapillaewhichmaydeveloppostnatallyastheyhavenotbeendemonstratedinthecurrentprenatalstudy.

Thepresentstudyshowedthatthecircumvallatepapillaeappearedearlyinthefirsttrimesterassmallprominencessurroundedbycirculargrooves.Theywerearrangedintworows(4–5ineachraw)oneithersideoftheTorus linguaeinbetweenthedevelopinglentiformpapillae.Thenumberofthiskindofgustatorypapillaediffersgreatlyamongspe-cies(Agungpriyonoetal.,1995;Ateş,Bozkurt,Kozlu,Alan,&DÜzler,2013; Chamorro, De Paz, Sandoval, & Fernandez, 1986; Chamorro,Fernandez, De Paz, Pelaez, &Anel, 1994; Erdunchaolu etal., 2001;

F IGURE  2 Lightmicrograph(a)andscanningelectronmicrograph(b)offetalcameltonguesinthefirsttrimestershowinglingualpapillae(arrows)onthelingualroot(R).Lingualbody(B)andapex(A)arealmostfreeofpapillaeexceptforsomescatteredepithelialprojectionsespeciallyonthelateralaspectsofthebody.Theearlyformedlingualgrooveappearsonthemid-sagittallinein(b)(asterisks).Noticetheintrinsiclingualmuscle(ILM)andextrinsiclingualmuscle(ELM)in(a).(a)Isstainedwithhaematoxylinandeosin

(a)

(b)

4  |     ABOU- ELHAMD Et AL.

Fredericketal.,1994).Itcanbepostulatedthatanimalswithoutfoliategustatorypapillaelikecamelhavenumerouscircumvallatepapillaeincomparisonwiththosewhichhavefoliatepapillaelikeequines.

In the second trimester, tastebudswere firstobservedopeninginthelateralwallofthecircumvallatepapillae.Bythethirdtrimester,tastebudswereseenopeningonbothdorsalandlateralsurfacesofthepapillae.Inthesamecontext,Erdunchaoluetal.(2001)andBello,Alimi,Sonfada,etal.(2015)foundtastebudsonthelateralpapillarysurfacewhile (Doughbag, 1988; Salehi etal., 2010) observed tastebudsonthedorsalsurfaceofthecircumvallatepapillaeofdevelopingcameltongue.Inadultcamel,ElSharapy(ElSharaby,2006;ElSharaby,Alsafy,El-Gendy,&Wakisaka,2012)mentionedthatthefreesurfaceof thecircumvallatepapillae is freeof tasteporeandmostof themwerelocatedalongthemedialwallepitheliumandoccasionallyinthelateralwall.Thelastresultsinadultcamelsmaybeduetoapostnatal

modulationofthepapillaryepitheliumasaresultofcellularinvolutionthatmayaccompanyincreasingdepthsofthepapillarycirculargroovesduringpostnataldevelopment.

PrematureEbner’sglandswereobservedinthethirdtrimesterinthedeeperpartsofthecircumvallatepapillaeandtheywereopeningintothegustatoryfurrow.TheyshowednegativereactivitytoPASandalcianbluereactionindicatingthattheirsecretionsaremainlyserousand free frommucus contents. Sbarbati,Crescimanno, andOsculati(1999)statedthattheseglandsaremainlyinvolvedinthewashingofthevallumaroundthecircumvallatepapillae.Thelastauthorsaddedthat both circumvallate papillae and Ebner’s glands form a singlefunctionalunitywhichseemstorepresentanimportantenzyme-andpheromone-producing system composed of a sensitive (taste buds)and an effectory (Ebner’s gland) branch linked by feedbackmecha-nismsofcontrol.Theyhypothesizedthatthetastebudslocatedinthe

F IGURE  3 Lightandscanningelectronmicrographsoffetalcameltonguesatthefirsttrimestershowingthedevelopingcircumvallate(a,b,c)andfungiformpapillae(e,d,f,longarrows).Thesurfaceepitheliumisformedofstratifiedcuboidalepithelium.Theprimordiumofcircumvallatepapilla(bluearrow)andlentiformpapillae(bluearrowhead)isclearlydemonstratedontheroot(a)whiletheprimordiaoffungiformpapillaeappearonthebody(d)intheformofepithelialplacodes(blackarrows).Noticethatthecircumvallatepapillaappearsassmallprominencesurroundedbycirculargroove(arrowheads)andanannularpad(asterisks).(c)Demonstratesahighermagnificationoftheformingcirculargrooveofcircumvallatepapillabysequesteringepithelialcells(redarrows).(f)Demonstratesahighermagnificationofthedevelopingfungiformpapillaintheformofepithelialplacodethatresultsfromdifferentialepithelialgrowth.(a,d)Arestainedwithhaematoxylinandeosin

(a) (d)

(b) (e)

(c) (f)

     |  5ABOU- ELHAMD Et AL.

distalportionoftheEbner’sglandsductalsystemcanbeconsideredsimilartothechemoreceptorcellslocatedinotherportionsofthedi-gestiveapparatussuchaspancreaticandbileducts.

In agreementwith that reportedbyGad-Allah etal. (2015), at94days of pregnancy, the primordia of the fungi papillae firstlyappeared on the apex of the camel tongue and the circumvallateand lentiform papillae on the root, however, filiform papillae ap-pearedlater.Thepresentfindingsrevealedthatfungiformpapillaeappeared as epithelial placodes in the first trimester and became

differentiatedgraduallyinthesecondtothethirdtrimester.Similartothatobservedincattle(Chamorroetal.,1986),thebactriancamel(Erdunchaolu etal., 2001), Akkaraman sheep (Ünsal, Aktumsek,Celik,&Sur,2003)andreeves’muntjacdeer (Zheng&Kobayashi,2006), dromedary camel (Sharifabad and Salehi, 2014), the tastebudswith taste poreswere demonstrated on the free surface ofthefungiformpapillae.Unlikely,fungiformpapillaeofgoat(Kumar,Kumar,& Singh, 1998;Kurtula&Atalgınb, 2008;Qayyum&Beg,1975),Japaneseweasels(Furubayashi,Sato,&Ishibashi,1989)and

F IGURE  4 Lightandscanningelectronmicrographsoffetalcameltonguesatthesecondtrimestershowingthepapillaeontheroot(circumvallate;a,c,dandlentiformpapillae;b)andpapillaeonthebody(Fungiform;e,handfiliformpapillaef,g).(d)Demonstratesahighermagnificationoftheareabetweenthecircumvallategustatoryfurrowandsurfaceepitheliumofthetongue.Abbreviations:AP(Annularpad),F(filiformpapillae),arrowheads(tastepores),asterisks(gustatoryfurrow).Notethekeratinizedcoveringepitheliumofthelingualpapillae.(a,b,e,f)Arestainedwithhaematoxylinandeosin

(a) (e)

(b) (f)

(c) (g)

(d) (h)

6  |     ABOU- ELHAMD Et AL.

Egyptian camel (Korans&Bachir, 2004)werewithout taste buds.The last finding that fungiform papillae in Egyptian camel lacktaste budsmaybe attributed to amisleading findingdue to non-representingtissuematerials.

Thepresent study revealed that the lentiformpapillaewere thefirstmechanicalpapillaeseenonthe lingualsurfaceofcamel in thefirsttrimester.InaccordancewithErdunchaoluetal.(2001),onlysim-pletypeof lentiformpapillaewasobservedonthedorsalsurfaceofthetongueofcamel.However,simpleandcompoundtypeof thesepapillaewasreportedincaprine(Kumaretal.,1998).

In thepresent study, the filiformpapillaebecameclearlyvisiblein the second trimester of prenatal life then they became heavilydemonstratedonthelateralandrostralpartsofthebodyaswellasontheapex.InaccordancewithQayyumetal.(1988),therewerenosecondarypapillaryprojections in the filiformpapillaeof the cameltongue.

In agreementwithHejazi andBaroughi (2013), keratinizationofpapillaryepitheliumwasdemonstratedduringembryoniclifeandthatthereisnorelationshipbetweentheirkeratinizationandthedietoftheanimalafterthebirth.

F IGURE  5 Lightandscanningelectronmicrographsoffetalcameltonguesatthethirdtrimestershowingthegustatory(circumvallatepapillaea-dandfungiforme,f)andmechanicalpapillae(filiformpapillae;e,fandlentiform;g).(d)Demonstratestastepores(asterisks)inthegustatoryfurrow(blackarrows)ofthecircumvallatepapillae.Insetin(a)showsahighermagnificationofthemarkedareawiththetastebudsofthecircumvallatepapilla.Noticethetastebudswiththeaxonsofneuroepithelialcellspenetratinginthesubepithelialconnectivetissuein(c)(blackarrowheads).Abbreviationsandshapes:annularpad(AP),Ebner’sgland(Eg),fungiformpapilla(redarrow),filiformpapillae(F),lentiformpapillae(L),tastebuds(bluearrowheads).(a,e)Arestainedwithhaematoxylinandeosin,while(c)isstainedwithtrichromestain

(a) (e)

(b) (f)

(c)

(d)

(g)

     |  7ABOU- ELHAMD Et AL.

ACKNOWLEDGEMENTS

We are grateful to the technician staffs of the Department ofAnatomy,HistologyandEmbryology,FacultyofveterinaryMedicine,AssiutUniversity,fortheirhelpandvaluabletechnicalassistance.TheprojectisfundedbyAssiutUniversity,Egypt.

CONFLICT OF INTEREST

Theauthorsdeclarenoconflictofinterest.

REFERENCES

Abbate, F., Guerrera,M. C.,Montalbano, G., Zichichi, R., Germana,A., &Ciriaco,E.(2010).MorphologyofthelingualdorsalsurfaceandoraltastebudsinItalianlizard(Podarcis sicula).Anatomia Histologia and Embryologia,39,167–171.https://doi.org/10.1111/ahe.2010.39.issue-2

Abbate, F., Latella, G.,Montalbano,G., Guerrera,M. C., Germana,G. P.,&Levanti,M.B.(2009).Thelingualdorsalsurfaceoftheblue-tongueskink(Tiliqua scincoides).Anatomia Histologia and Embryologia,38,348–350.https://doi.org/10.1111/ahe.2009.38.issue-5

Abbate,F.,Latella,G.,Montalbano,G.,Guerrera,M.C.,Levanti,M.B.,&Ciriaco, E. (2008). Scanning electronmicroscopical study of the lin-gual epithelium of green iguana (Iguana iguana).Anatomia Histologia and Embryologia,37, 314–316.https://doi.org/10.1111/ahe.2008.37.issue-4

Abd-Elnaeim,M.M.M.,Kelany,A.,Dorreia,A.M.,&Abdel-Moneim,M.E.(2008).PrenatalDevelopmentoftheTongueanditsPapillaeintheOne-humpedCamel (Camelusdromedarius). InA.S. Saber (Ed.)First Scientific Congress of the African Association of Veterinary Anatomists (pp.81–95).Cairo,Egypt:JournalVeterinaryAnatomy.

Abd-Elnaeim,M.M.,Zayed,A.E.,&Leiser,R.(2002).Morphologicalchar-acteristicsofthetongueanditspapillaeinthedonkey(Equus asinus):Alightandscanningelectronmicroscopicalstudy.Annals of Anatomy- Anatomischer Anzeiger, 184, 473–480. https://doi.org/10.1016/S0940-9602(02)80081-4

Agungpriyono,S.,Yamada,J.,Kitamura,N.,Nisa,C.,Sigit,K.,&Yamamoto,Y.(1995).Morphologyofthedorsallingualpapillaeinthelessermousedeer. Tragulus javanicus. J Anat,187(Pt3),635–640.PMC1167466.

Ateş,S.,Bozkurt,Y.A.,Kozlu,T.,Alan,A.,&DÜzler,A.(2013).Lightandscan-ningelectronmicroscopicstudiesonthelingualpapillaeof80-day-oldwildpigfetalsiblings.Turkish Journal of Veterinary and Animal Sciences,37,664–671.

Bello,A.,Alimi,A.O.,Sonfada,M.L.,Umaru,M.A.,Onu,J.E.,Onyeanusi,B.I.,&Shehu,S.A.(2014).Prenataldevelopmentofthefiliformpapil-laeofone-humpedcamel(Camelus dromedarius):Histomorphologicalstudy. International Journal of Agricultural Research and Review, 2,129–135.

Bello,A.,Alimi,O.O.,Sonfada,M.L.,Umaru,M.A.,Onu,J.E.,Onyeanusi,B. I., & Shehu, S.A. (2015).Histomorphometric study of the prena-talDevelopmentof theCircumvallatePapillaeofone-humpedcamel(Camelus dromedarius). Anatomy & Physiology, 5, 168. https://doi.org/10.4172/2161-0940.1000168

Bello,A.,Alimi,O.A.,Umaru,M.A.,&Onu,J.E. (2015).Prenataldevel-opment of the fungi form papillae of one-humped camel (Camelus dromedarius):Ahistomorphologicalstudy.African Journal of Agricultural Science and Technology (AJAST),3,500–504.

Bello, A., Onyeanusi, B. I., Sonfada, M. L., Adeyanju, J. B., Umar, A. A.,Umaru,M.A.,…Hena,S.A.(2012).Histomorphologicalstudiesoftheprenataldevelopmentofoesophagusofonehumpedcamel(Camelus dromedarius).Scientific Journal of Agriculture,1,100–104.

Bradley,R.M.,&Stern,I.B.(1967).Thedevelopmentofthehumantastebudduringthefoetalperiod.Journal of Anatomy,101,743–752.

Chamorro, C. A., De Paz, P., Sandoval, J., & Fernandez, J. G. (1986).Comparativescanningelectron-microscopicstudyofthelingualpapil-laeintwospeciesofdomesticmammals(Equus caballus and Bos tau-rus). 1. Gustatory Papillae. Acta Anatomica, 125, 83–87. https://doi.org/10.1159/000146141

Chamorro,C.A.,Fernandez,J.G.,DePaz,P.,Pelaez,B.,&Anel,L.(1994).Scanningelectronmicroscopyofthewildboarandpiglingualpapillae.Histology and Histopathology,9,657–667.

Dougbag, A. E. I.-S. (1987a). Scanning electron microscopic studies ofthemorphogenesisof the lingual gustatorypapillaeof camel (Cameldromedarius)I.Morphogenesisofthefungiformpapillae.Zeitschrift fur mikroskopisch- anatomische Forschung,101,881–892.

Dougbag, A. E. I.-S. (1987b). Scanning electron microscopic studies ofthemorphogenesis of the lingual lentiform and coniform papillae incamel (Camel dromedarius). Zeitschrift fur mikroskopisch- anatomische Forschung,101,893–903.

Doughbag,A.E.(1988).Electronmicroscopicstudiesonthemorphogen-esisof the lingual gustatorypapillaeof camel (Camelus dromedarius).II.Morphogenesisofthevallatepapillae.Zeitschrift fur mikroskopisch- anatomische Forschung,102,259–271.

Dyce,K.M.,Sack,W.O.,&Wensing,C.J.G.(1996).Text book of veterinary anatomy,2nded.Philadelphia,PA:W.B.SaundersCo.

ElSharaby,A.A.(2006).Comparative morphological studies of the circumval-late papillae in three mammalian species: rat, dog and sheep. 12thscien-tific congress. (pp.661–680).Assiut:FacultyofVeterinaryMedicine.AssiutUniversity.

El Sharaby,A.A., Alsafy,M.A., El-Gendy, S. A., &Wakisaka, S. (2012).Morphologicalcharacteristicsofthevallatepapillaeoftheone-humpedcamel(Camelus dromedarius).Anatomia Histologia and Embryologia,41,402–409.https://doi.org/10.1111/ahe.2012.41.issue-6

Elnasharty,M.,Sharaby,A.E.,&El-Din,A.N.(2013).Histogenesisofrabbitvallatepapillae.World Academy of Science, Engineering and Technology,76,509–516.

Elwishy,A.B.,Hemeida,N.A.,Omar,M.A.,Mobarak,A.M.,&ElSayed,M.A.(1981).Functionalchangesinthepregnantcamelwithspecialrefer-encetofoetalgrowth.British Veterinary Journal,137,527–537.

Erdunchaolu,E.,Takehena,K.,Yamamoto,E.,Kobayashi,A.,Cao,G.,Aiyin,B.,…Tangkawattana,P.(2001).Characteristicsofdorsallingualpapil-lae of the Bactrian camel (Camelus bactrianus). Anatomia Histologia and Embryologia,30, 147–151.https://doi.org/10.1111/ahe.2001.30.issue-3

Frederick, B., Stangl, J., & Russell, S. P. (1994). Gross Morphology &DistributionpatternoflingualpapillaeinSomeGeomyid&HeteromyidRodents.Proc. Okla. Acad. Sci,74,25–29.

Furubayashi,R.,Sato,E.,&Ishibashi,T.(1989).HistologicalpatternofthetongueintheJapaneseweasels,Mustela itatsi,withspecialreferencetothemorphologyanddistributionofpapillae,tastebudsandlingualglands.Kaibogaku Zasshi,64,210–214.

Gad-Allah,A.,Abou-Elhamd,A. S.,Abdelmonem,M. E., & Zayed,A. E.-Z. (2015).Earlyprenataldevelopmentof the tongue inone-humpedcamel(Camelus dromedarius):Alightandscanningelectronmicroscopicstudy.Journal of International Academic Research for Multidisciplinary,3,309–319.

Hejazi,S.,&Baroughi,R. (2013).Histogenesisstudyof lingualpapillaeinsheepfetus.European Journal of Zoological Research,2,26–31.

Iwasaki,S.,Okumura,Y.,&Kumakura,M.(1999).Ultrastructuralstudyofthe relationship between themorphogenesis of filiformpapillae andthekeratinizationofthelingualepitheliuminthemouse.Cells Tissues Organs,165,91–103.https://doi.org/10.1159/000016679

Iwasaki, S., Yoshizawa, H., & Kawahara, I. (1996). Study by scanningelectron microscopy of the morphogenesis of three types of lin-gual papilla in the mouse. Acta Anatomica, 157, 41–52. https://doi.org/10.1159/000147865

Korans, S., & Bachir,M. H. (2004).Morphofunctional study of differ-enttonguepapillaeinruminantsandrodentia(Ascanningelectron

8  |     ABOU- ELHAMD Et AL.

microscopic and histological studies). Cairo Dental Journal, 20,215–220.

Kumar,P.,Kumar,S.,&Singh,Y.(1998).Tonguepapillaeingoat:Ascanningelectron-microscopic study.Anatomia Histologia and Embryologia,27,355–357.https://doi.org/10.1111/ahe.1998.27.issue-6

Kurtula, I., & Atalgınb, S. H. (2008). Scanning electron microscopicstudy on the structure of the lingual papillae of the Saanen goat.Small Ruminant Sesearch, 80, 52–56. https://doi.org/10.1016/j.smallrumres.2008.09.003

Qayyum,M. A., & Beg, M. A. (1975). Anatomical and neurohistologicalobservations on the tongue of the India goat, Capra aegagrus. Acta Anatomica,93,554–567.https://doi.org/10.1159/000144533

Qayyum,M.A.,Fatani,J.A.,Mehta,L.,Shaad,F.U.,&Mustafa,F.(1991).Anatomical and histological observations on the tongue of one-humped camel, Camelus dromedarius. Functional and Developmental Morphology,1,23–26.

Qayyum,M.A., Fatani,J.A.,&Mohajir,A.M. (1988). Scanningelectronmicroscopic study of the lingual papillae of the one humped camel,Camelus dromedarius. Journal of Anatomy,160,21–26.

Ramayya,P.J.,Babu,A.P.,Rao,S.D.,Lakshmi,J.B.,&Patki,H.S.(2012).Grossanatomyofthetongueofcamel.Indian Veterinary Journal,89,50–51.

Saidu, A., Jaji, A., Yawulda, P., Da’u, F., Ahmad, Y., & Elelu, N. (2015).Grossmorphology andmorphometry of foetal and adult dromedarytongues.Sokoto Journal of Veterinary Sciences,13, 49–53.https://doi.org/10.4314/sokjvs.v13i2.8

Salehi,E.,Pousti,I.,Gilanpoor,H.,&Adibmoradi,M.(2010).Themorpho-logicalobservationsof some lingualpapillae in camelusdromedariesembryoes. Journal of Animal and Veterinary Advances, 9, 514–518.https://doi.org/10.3923/javaa.2010.514.518

Sbarbati,A.,Crescimanno,C.,&Osculati,F.(1999).Theanatomyandfunc-tionalroleofthecircumvallatepapilla/vonEbnerglandcomplex.Medical Hypotheses,53,40–44.https://doi.org/10.1054/mehy.1997.0708

Sharifabad,M.M.,&Salehi,E.(2014).Thehistogenesisoffungiformpapil-lae in Camelus dromedaries. International Journal of Biosciences, 5,101–106.

Shawulu,J.C.,Kwari,H.D.,&Abgyal,A.Y.(2012).Pre-natalgrowthofthetongueanddevelopmentofthe lingualpapillae insahelgoats (Capra hircus).Agricultural Journal,7,5–9.

Sisson,S.,&Grossman,J.D.(1975).The anatomy of the domestic mammals,4thed.Philadelphia,WB:Saunders.

Skieresz-Szewczyk,K.,&Jackowiak,H.(2017).Developmentofmechanicalpapillaeofthetongueinthedomesticgoose(Anseranserf.domestica)duringtheembryonicperiod.Protoplasma,254,147–160.https://doi.org/10.1007/s00709-015-0927-x

Sui,S.R.,Su,X.X.,&Chen,B.H. (1983).Foodofcamel (inChinese). InY. Nong (Ed.), Camel Industry (pp. 128–135). Beijing: AgriculturalPublishingCompany.

Ünsal,S.,Aktumsek,A.,Celik,I.,&Sur,E.(2003).Thenumberanddistribu-tionoffungiformpapillaeandtastebudsinthetongueofyoungandadultAkkaramansheep.Revue de médecine vétérinaire,154,709–714.

Zheng,J.,&Kobayashi,K.(2006).Comparativemorphologicalstudyonthelingualpapillaeandtheirconnectivetissuecores(CTC)inreeves’munt-jacdeer(Muntiacus reevesi).Annals of Anatomy- Anatomischer Anzeiger,188,555–564.https://doi.org/10.1016/j.aanat.2006.05.014

SUPPORTING INFORMATION

Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle.

How to cite this article:Abou-ElhamdAS,Abd-ElkareemM,El-ZuhryZayedA.Morphogenesisoflingualpapillaeofone-humpedcamel(Camelus dromedarius)duringprenatallife:Alightandscanningelectronmicroscopicstudy.Anat Histol Embryol. 2017;00:1–8. https://doi.org/10.1111/ahe.12321